Food safety knowledge, self-reported practices and

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ARTICLE NO: 610144 ARTICLE TITLE: Food safety knowledge, self-reported practices and attitude of poultry meat handling among Slovenian consumers AUTHORS:

Meta Sterniša, Sonja Smole-Možina, Sonja Levstek, Andreja Kukec, Peter Raspor and Mojca Jevšnik

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Received 30 June 2017 Revised 15 December 2017 Accepted 18 December 2017

Food safety knowledge, self-reported practices and attitude of poultry meat handling among Slovenian consumers Meta Sterniša Department of Food Science and Technology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia

Sonja Smole-Možina Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia

Sonja Levstek Department of Food Science and Technology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia

Andreja Kukec Department of Public Health, Medical Faculty, University of Ljubljana, Ljubljana, Slovenia

Peter Raspor Faculty of Health Sciences, University of Ljubljana, Ljubljana, Slovenia, and

Mojca Jevšnik University of Ljubljana, Ljubljana, Slovenia Abstract Purpose – The purpose of this paper is to investigate Slovenian consumers’ knowledge and self-reported practices in poultry meat handling during purchase, transport, and preparation in home kitchens and to assess the awareness of the microbiological risk associated with poultry meat, with an emphasis on Campylobacter. Design/methodology/approach – A cross-sectional study of consumers’ food safety knowledge, self-reported practices, and awareness of the microbiological risk was conducted from March to April 2015 at supermarkets in different parts of Slovenia. A convenience sample of 560 consumers was obtained. Gender and age distribution were controlled by 28 interviewers, each of whom distributed 20 questionnaires. The questionnaire included 33 questions divided into four parts. Findings – The results revealed consumers awareness of food safety issues. Respondents have some basic knowledge about proper food handling. However, a substantial number of consumers still lacks knowledge of the microbiological risk and has bad habits in domestic poultry meat preparation. Research limitations/implications – The research did not reflect a representative sample of Slovenian consumers. Practical implications – The results indicate some gaps in consumers’ food safety knowledge and self-reported practices. Current Campylobacter preventive strategies regarding retail poultry meat contamination are not yet sufficiently successful. Originality/value – The study provides valuable insight into consumers’ food safety knowledge and self-reported practices in poultry meat handling from shopping to eating. Opportunities for improvement in consumers’ formal and informal education and training should be offered. Keywords Consumer, Food safety, Knowledge, Campylobacteriosis, Poultry meat, Self-reported practice Paper type Research paper

British Food Journal © Emerald Publishing Limited 0007-070X DOI 10.1108/BFJ-06-2017-0360

Introduction Since 2005, the most commonly reported zoonotic disease in the European Union has been campylobacteriosis, with a statistically significant increasing trend over the eight-year period of 2008-2015, reaching the prevalence of 65.5 per 100,000 people (European Food Safety Authority

(EFSA) and European Centre for Disease Prevention and Control (ECDC), 2016). The Slovene campylobacteriosis prevalence in 2015 was 64.4 per 100,000 people (EFSA and ECDC, 2016). Despite the efforts of the industry to ensure that poultry meat is free of Campylobacter (Lin, 2009), the prevalence of these bacteria is high (Kurinčič et al., 2005; Gruntar et al., 2015). Broiler meat is considered to be the largest single source of human campylobacteriosis. According to EFSA and ECDC (2016), over 90 per cent of reported campylobacteriosis cases originate from domestic environments, and they occur sporadically. Home preparation of poultry meat and microbiological risks related to it have been the subject of research since the 1970s (De Wit et al., 1979), when also consumers’ behaviour in relation to risks and possible intervention appears in the professional literature (Roselinus, 1971). Despite the longstanding awareness of the professional public about the problem of campylobacteriosis and the connection with improper behaviour of consumers, there were only few studies (Sampers et al., 2012; Bearth et al., 2014; Millman et al., 2014) devoted to studying this topic. Otherwise, an assessment of consumers’ general food safety knowledge, attitudes, and behaviour is the subject of numerous large-scale research (Milton and Mullan, 2010; Young and Waddell, 2016), and yet, the same conclusions have been made for years. Cross-contamination and noncompliance with good hygiene practice during home meal preparation are key factors influencing the occurrence of foodborne disease at home (Millman et al., 2014). Therefore, it is crucial that poultry meat consumers know the measures that eliminate the risk of Campylobacter infection. These are the preservation of the cold chain from retail to home, good hygiene practice, thorough cooking, and (probably the most important) avoiding cross-contamination ( Jevšnik et al., 2008; Bell and Kyriakides, 2009; Bearth et al., 2014). Therefore, consumers’ behaviour is a major factor in the transmission of foodborne disease, but consumers are still not aware of their role in the food supply chain, and their food-related behaviour creates many possibilities for the microbiological contamination of foods ( Jevšnik et al., 2008). Consumers have a feeling of invulnerability because the microbiological quality of foods is at a high level and because they believe that food risk management is the responsibility of the relevant state authorities, industry, and retailers (Brewer and Rojas, 2008; Jevšnik et al., 2008; Nesbitt et al., 2014). Consumers also believe that food prepared by themselves is safer than food prepared by others (Bergsma et al., 2007; Bearth et al., 2014). Because home food safety cannot be controlled in a manner similar to that in industrial processing, it is crucial that the demands of good hygiene practices during purchase, transport, storage, and preparation are met to prevent contamination at home. Recent food-related incidents have increased public interest in food safety. However, microbiological risks are not among those recognised by consumers as the most important (Bearth et al., 2014). Only by evaluating consumers’ current knowledge of safety risks associated with handling poultry meat and by knowing the practices of handling and preparing poultry meat can changes be made in the direction of education. The aim of this study was to investigate Slovenian consumers’ knowledge and self-reported practices of handling poultry meat from purchase to meal preparation and to assess the awareness of the microbiological risk associated with poultry meat, with an emphasis on Campylobacter. The specific goal was to compare our results with another Slovene survey conducted a decade earlier in the same research field.

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Materials and methods Sampling plan A cross-sectional study of consumers’ food safety knowledge, self-reported practices, and awareness of the microbiological risk was conducted from March to April 2015. Based on the data of population in the level of 12 statistical regions of Slovenia (Statistical Office, 2017) and permanent residence address of the interviewers we included in the study two

Food safety knowledge

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supermarkets from each of ten smaller statistical regions and four from the two statistical regions, with the two biggest cities in Slovenia. In 28 selected supermarkets, volunteered but trained interviewers distributed 20 questionnaires. Due to feasibility of the study and generation of hypothesis, a convenience sample of 560 consumers was obtained from all observed supermarkets in Slovenia. For the control of the variables (gender, age, education attainment, and living area), multiple logistic regression was used (Dos Santos Silva, 1999). According to the aim of this study, we did not assess consumers who do not eat and/or prepare poultry meat in the study. Interviewers briefly explained the purpose and nature of the study to the potential adult respondents (over 18 years of age) and sought permission for inclusion in the survey. To guarantee the anonymity of respondents and enable easier identification of questionnaires, identity numbers were assigned to each questionnaire. The questionnaire included 33 questions divided into four parts: entry questions on poultry meat purchasing and the preparation for acceptance of the questionnaire in the study, demographic characteristics (gender, age, education attainment, and living area), knowledge, self-reported practices, and awareness of poultry meat handling during purchase, transport, and preparation in the home kitchen, and knowledge of microorganisms with emphasis on Campylobacter in poultry meat. Pilot survey The questionnaire was pilot tested by 12 participants during January and February 2015 to confirm question clarity, identify response options and gauge likely interview duration. The questionnaire was revised based on the pre-test results and other recommendations. Data analysis Descriptive statistical methods were performed for all the questions. For the assessment of the association between consumers’ characteristics and their knowledge, self-reported practices, and attitudes towards microorganisms with emphasis on Campylobacter in poultry meat in the first phase of statistical analysis the χ2 test and in the second phase multiple logistic regression analysis was done. In the regression models, we assessed the association between observed questions (respondents’ food microbiology knowledge with emphasis on Campylobacter in poultry meat) and demographic variables. Based on frequency analysis of demographic data and previous similar studies, we divided observed demographical variables in categories as shown in Table III. In statistical tests, a p-value of 0.05 or less was considered significant. Only significant results are presented. Data were analysed using the software Statistical Package for the Social Sciences (SPSS) 21.0.0. For 14 questions, content analysis of answers was done when the explanation of the answer was possible. For analysing the open questions, we used the description method based on the qualitative content analysis (Denzin and Lincoln, 1994), which is based upon the grounded theory (Strauss, 1996). We divided answers into three groups: “sufficient knowledge/awareness”, “neutral knowledge/awareness”, and “insufficient knowledge/awareness”. In the first group, the answers indicated that respondents have knowledge/are aware. In the second group, the respondents have partial knowledge/are partially aware of the question topic. In the third group, the answers indicated that respondents do not have knowledge/are not aware of the question topic. Results and discussion Respondents’ characteristics The response rate was 79.6 per cent; 446 of the 560 interviewed respondents completed the interview (Table I) and answered affirmatively to the first two questions regarding buying

Respondents characteristic

n

%

Gender (n ¼ 442) Women Men

292 150

66.1 33.9

Age group (n ¼ 446) Young adults (⩽ 25 years) Adults (26-59 years) Seniors (⩾ 60 years)

159 226 61

35.7 50.7 13.7

Educational attainment (n ¼ 445) Group 1 (less than basic (ISCED 1), basic (ISCED 2), short-term vocational (ISCED 3)) Group 2 (upper secondary vocational (ISCED 4), vocational-technical/technical/general upper secondary (ISCED 4), short-cycle higher vocational (ISCED 5)) Group 3 (1st cycle higher (ISCED 6), 2nd cycle higher (ISCED 7), 3rd cycle higher (ISCED 8))

52

11.7

329 64

73.9 14.4

Living area (n ¼ 445) Rural Urban and suburban

246 199

55.3 44.7

Living conditions (n ¼ 444) Family Single

412 32

92.8 7.2

I learned about safe food preparation…a (n ¼ 445) …from family 304 68.3 …at school 150 33.7 …from books, magazines 144 32.4 …from the internet 135 30.3 …at work 102 22.9 Notes: ISCED, International Standard Classification of Education; n, number of respondents answering the question. aMore than one answer possible

and preparing poultry meat. Two-thirds of the respondents were women, which can indicate that women still do more food shopping and home food preparation than men do in Slovenia. Three age groups were formed, identifying them as young adults (⩽ 25 years), adults (26-59 years), and seniors (⩾ 60 years) with 35.7, 50.7, and 13.7 per cent, respectively, showing that young adults are becoming involved in food preparation. Furthermore, three educational groups were formed, as shown in Table I, and over 70 per cent of respondents were in Group 2. The predominating living area was rural (55.3 per cent); the majority of respondents lived in a family household (92.8 per cent); most commonly, respondents had gained their safe food preparation knowledge from other family members (68.3 per cent). Respondents’ knowledge, self-reported practices, and awareness of poultry meat handling during purchase, transport, and preparation in the home kitchen Respondents’ knowledge, self-reported practices, and awareness of poultry meat handling during purchase, transport, and preparation in the home kitchen were evaluated, and detailed results are shown in Table II. Results of multivariate analysis of association between observed respondents’ food microbiology knowledge with emphasis on Campylobacter in poultry meat and demographic variables are shown in Table III. Additional explanations of answers were evaluated to determine the level of knowledge and awareness (Table IV ). The preferred places where respondents most frequently buy poultry meat were supermarkets (67.3 per cent), followed by butchers (29.6 per cent) and primary producers (16 per cent). Four respondents reported raising their own poultry and two


Table I. Demographic characteristics of respondents

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Table II. Respondents’ knowledge, selfreported practice, and awareness of poultry meat handling during purchase, transport, and preparation in the home kitchen, and respondents’ food microbiology knowledge with emphasis on Campylobacter in poultry meat

Statement

Response

n

%

Respondents’ knowledge, self-reported practice, and awareness of poultry meat handling during purchase, transport, and preparation in the home kitchen …in a supermarket 298 67.3 I buy poultry meat…a (n ¼ 443) …at butchers 131 29.6 …at primary producer 71 16.0 …other – own production, 6 o 0.1 buying live animals …fresh, unpacked… 235 52.9 I buy… poultry meata (n ¼ 444) …fresh, packed… 227 51.1 …frozen… 23 5.2 …ready-to-prepare… 19 4.3 Before poultry meat purchase, I check for freshness (n ¼ 420) Yes 395 94.0 No 25 6.0 Before poultry meat purchase, I check the date of minimum shelf life Yes 388 90.9 (n ¼ 427) No 39 9.1 Before poultry meat purchase, I check the origin of poultry meat Yes 224 56.0 (n ¼ 400) No 176 44.0 I use an insulated bag when buying raw poultry meat (n ¼ 442) Yes 176 39.8 No 266 60.2 I follow instructions for poultry meat preparation if they are Yes 229 51.9 included on the packaging label (n ¼ 441) No 212 48.1 a …roasting/baking 379 86.1 I prepare poultry meat by… (n ¼ 440) …barbecue 109 24.8 …cooking 50 11.4 b Yes 81 18.2 I always store poultry meat in the same place in a refrigerator (n ¼ 446) No 363 81.8 …on kitchen surfaces at 262 59.7 I defrost poultry meat…a (n ¼ 439) room temperature …in a refrigerator 110 25.1 …under tap water 103 23.5 …in a microwave 56 12.8 I sometimes freeze previously defrosted poultry meat (n ¼ 440) Yes 39 8.9 No 401 91.9 a 257 58.7 I use… for hand drying during poultry meat preparation (n ¼ 438) …paper towels… …dishcloth… 201 45.9 I always use the same cutting board for poultry meat preparation Yes 212 48.2 (n ¼ 440) No 228 51.8 I use different cutting boards for different foods (n ¼ 441) Yes 291 66.0 No 150 34.0 Yes 367 83.6 I pay attention to sufficient heat treatment of poultry meatb (n ¼ 439) No 72 16.4 Yes 330 74.7 Improper home raw poultry meat preparation presents a health b No 112 25.3 risk (n ¼ 442) Respondents’ food microbiology knowledge with emphasis on Campylobacter in poultry meat Yes Poultry meat in retail can be contaminated with harmful No microorganismsb (n ¼ 443) Yes Microorganism can multiply in a fridgeb (n ¼ 430) No Microorganism can multiply in prepared, heat-treated foods left on Yes No a kitchen counterb (n ¼ 437) Yes I know what is Campylobacterb (n ¼ 442) No I know how Campylobacter can contaminate poultry meatb (n ¼ 441) Yes

256 187 323 107 335 102 74 368 45

57.4 42.2 75.1 24.9 76.7 23.3 16.7 83.3 10.2

(continued )

Statement

Response

n

%

No 396 89.8 18 4.1 I know how often Campylobacter is present on retail poutry meatb Yes (n ¼ 443) No 425 95.9 37 8.4 I know at which temperature Campylobacter can multiplyb (n ¼ 442) Yes No 405 91.6 Yes 48 10.9 I know which temperatures destroy Campylobacter during meat No 394 89.1 preparationb (n ¼ 442) b 55 12.4 I know what disease can be caused by Campylobacter (n ¼ 442) Yes No 387 87.6 18 4.1 I know how many Campylobacter cells are needed to cause diseaseb Yes (n ¼ 442) No 424 95.9 b Yes 19 4.3 I know something else about Campylobacter (n ¼ 441) No 422 95.7 Notes: n, number of respondents answering the question. aMore than answer one; banswers with explanation

Microbiology knowledge/demographic variables Category

OR

Poultry meat in retail can be contaminated with harmful microorganisms (n ¼ 437) Gender Women 1.000 Men 1.994 Microorganism can multiply in a fridge (n ¼ 424) Age group Adults (26-59 years) Young adults (⩽ 25 years) Seniors (⩾ 60 years) Educational attainment Group 3 (higher) Group 2 (moderate) Group 1 (low) I know what is Campylobacter (n ¼ 436) Age group

95% CI limits for OR Lower Upper

1.329

2.991

0.001

0.621 1.078

1.057 2.079

0.120 0.016

0.818 1.068

1.291 1.934

0.817 0.017

Adults (26-59 years) 1.000 Young adults (⩽ 25 years) 0.740 Seniors (⩾ 60 years) 1.297

0.565 0.742

0.971 2.264

0.030 0.361

1.076

5.337

0.033

0.838 1.014

1.481 4.338

0.457 0.046

4.285

0.035

1.000 2.396 1.000 1.114 2.097

I know what disease can be caused by Campylobacter (n ¼ 436) Gender Women 1.000 Men 2.124 1.052 Educational attainment Group 3 (higher) 1.000 Group 2 (moderate) 1.104 0.852 Group 1 (low) 2.151 1.054 Notes: OR, odds ratio; CI, confidence interval; n, number of respondents answering p-value ¼ 0.05 or less was considered significant; *only significant results are presented

Table II.

p*

1.000 0.810 1.497 1.000 1.027 1.437

I know how Campylobacter can contaminate poultry meat (n ¼ 435) Gender Women Men Educational attainment Group 3 (higher) Group 2 (moderate) Group 1 (low)


1.430 0.453 4.390 0.035 the question.

Table III. Results of multivariate analysis of association between observed respondents food microbiology knowledge with emphasis on Campylobacter in poultry meat and demographic variables

BFJ Question Do you always store poultry meat in the same place in the refrigerator? Does improper home raw poultry meat preparation present a health risk? Do you pay attention to sufficient heat treatment of poultry meat? Do you know that poultry meat in retail outlets can be contaminated with harmful microorganisms? Can microorganisms multiply in the fridge? Can microorganisms multiply in prepared, heat-treated foods left on the kitchen counter? Do you know what Campylobacter is? Do you know how Campylobacter can contaminate poultry meat? Do you know how often Campylobacter is present in retail poultry meat? Table IV. Do you know at which temperature Campylobacter multiplies? Content analysis of Do you know which temperatures destroy Campylobacter during meat answers to assess preparation? knowledge and Do you know what disease can be caused by Campylobacter? awareness regarding Do you know how many Campylobacter are needed to cause disease? food hygiene and poultry meat handling Do you know anything else about Campylobacter? in the home kitchen Note: n, number of respondents answering the question

n

Sufficient Neutral Insufficient n % n % n %

46 13 28.3 28 60.8 231 213 92.2 17 7.4 241 203 84.2 35 14.5

5 1 3

10.8 0.4 1.2

139 120 86.3 18 12.9 1 229 153 66.8 57 24.9 19

0.7 8.3

189 169 89.4 20 10.5 67 61 91.0 3 4.5 45 28 62.2 11 24.4 17 10 58.8 5 29.4 41 15 34.1 22 53.7 59 62 18 16

33 47 9 11

0 3 6 2 5

0 4.5 13.3 11.8 12.2

55.9 24 40.7 2 75.8 3 4.8 12 50.0 7 38.9 2 68.8 2 11.1 3

3.4 19.4 11.1 18.8

respondents reported buying live animals. An earlier Slovene survey of Jevšnik et al. (2008) estimated that more consumers preferred to purchase poultry meat in supermarkets (81.8 per cent) and fewer bought it from primary producers (6.7 per cent). The popularity of locally produced food could influence buying habits. Retail food has high safety standards with increasing numbers of consumers believing that locally produced poultry meat and other foods are the safest ( Jevšnik et al., 2008; Bearth et al., 2014). The majority of respondents always check poultry meat for freshness (94 per cent) and the date of minimum shelf life (use by date) (90.9 per cent), but 44 per cent do not pay attention to the origin of poultry meat (Table II). These percentages are better than those reported in the previous Slovene survey ( Jevšnik et al., 2008) in which 54.2 per cent of consumers stated that they always check the date of minimum shelf life. The labelling provides food quality or attributes information to the consumer (Bernués et al., 2003). Despite transparent labels, the product may be subjected to rough handling or discontinued cold chain, which may damage the packaging or facilitate the growth of microorganisms. So, visual inspection of poultry meat, packaging, and labels during purchase should be done by consumers. In that way, consumers can avoid sensory unacceptable products or products past the use by date. Respondents were questioned about the state of the poultry meat they buy. Half of them reported buying fresh packed or unpacked poultry meat as the preferred form (Table II); the same was reported from the Netherlands (Bergsma et al., 2007), Belgium (Sampers et al., 2012), and the USA (Mazengia et al., 2015). In contrast, only 5.2 per cent of respondents reported buying frozen poultry meat. Providing a cold chain for refrigerated and frozen food products from the place of purchase to home is one of the important factors in assuring poultry meat safety ( Jevšnik et al., 2008; Taché and Carpentier, 2014). To minimise the temperature effect, the use of insulated bags is necessary, and 39.8 per cent of respondents stated using them when buying poultry meat (Table II), which is a larger share in comparison to the 15.3 per cent from the survey of Jevšnik et al. (2008) or the 18.6 per cent reported from New Zealand (Gilbert et al., 2007). The use of insulating bags in Slovenia is markedly more promoted in the supermarkets. This suggests that the supermarkets are getting involved in the safe chilled foods transport of consumers, which is often the point of breaking the cold chain of the product (Derens-Bertheau et al., 2015).

Three-quarters of respondents affirmed that “improper home raw poultry meat preparation presents a health risk” (Table II). Consumers generally have some knowledge of proper food handling, cross-contamination, and the importance of cooking to prevent foodborne disease, but their behaviour does not always correspond to their knowledge (Unusan, 2007; Jevšnik et al., 2008; Sampers et al., 2012; Mazengia et al., 2015). Only 18.2 per cent of respondents reported always storing poultry meat in the same place, which was a much lower percentage in comparison to other reported research: Canada 40 per cent (EKOS Research Associates Inc., 2010), USA 61 per cent (Mazengia et al., 2015), New Zealand 62.5 per cent (Gilbert et al., 2007). Explanations of respondents, shown in Table IV, showed that only 28.3 per cent of respondents who always store poultry meat in the same place had sufficient knowledge of the topic. The answers given were: “to prevent contact with other foods” and “to prevent dripping on to other foods”; 10.8 per cent of respondents showed a total lack of knowledge of proper poultry meat storage in the refrigerator. According to Sampers et al. (2012), proper storage of poultry meat in the refrigerator is necessary to prevent growth of spoilage and pathogenic microorganisms, and cross-contamination during storage at home. It should be stored below 5°C, on the lowest shelf in the refrigerator to prevent possible dripping over other foods and preferably always in the same spot. The most preferred way of defrosting poultry meat reported by respondents is on kitchen surfaces at room temperature (59.7 per cent), followed by defrosting in a refrigerator (25.1 per cent), under tap water (23.5 per cent) and in a microwave (12.8 per cent). Jevšnik et al. (2008) obtained similar results, with 50.4 per cent reported thawing meat on kitchen surfaces, 16.6 per cent in a refrigerator, 12.8 per cent in hot water, and 11.4 per cent in a microwave. Results regarding particular ways of defrosting were determined in different studies, but the majority of defrosting is done at room temperature (Badrie et al., 2006; Gilbert et al., 2007) or in the refrigerator (Nesbitt et al., 2009; Sampers et al., 2012; Ergönül, 2013; Mazengia et al., 2015). This way of defrosting poultry meat can present a risk of bacteria multiplying or contaminating surroundings by dripping onto other surfaces. Although freezing poultry meat is regarded as safe, re-freezing of already defrosted poultry meat can be risky, and 8.9 per cent of respondents claimed to do so, which is better than the 21 per cent revealed in a Canadian survey (EKOS Research Associates Inc., 2010). In our survey, 66 per cent of respondents reported using different cutting boards for different foods, and 48.2 per cent of respondents reported always using the same cutting board for poultry meat preparation. In the survey of Jevšnik et al. (2008), one-third of consumers reported using the same cutting board for poultry meat and other foods. Use of the same cutting board for poultry meat and other foods was also reported in other surveys: New Zealand 28 per cent (Gilbert et al., 2007), USA 45 per cent (Mazengia et al., 2015), and Turkey 59 per cent (Ergönül, 2013). To reduce the risk during food preparation, different cutting boards should be used for different foods. More of the respondents reported using paper towels (58.7 per cent) during poultry meat preparation than dishcloths (45.9 per cent), but some reported using both. Improvement is shown in the use of disposable paper towels in comparison to the 27.5 per cent from the survey of Jevšnik et al. (2008). A Turkish survey shows that 34.9 per cent of young consumers and 24.7 per cent of adult consumers always use paper towels (Sanlier, 2009). Moist hands promote bacterial transfer, so hands should be dried. To dry hands during meal preparation, paper towels should be used instead of dishcloths, as they are disposable. Proper heat treatment of poultry meat is crucial for killing pathogenic bacteria and making it safe for consumption. The majority of our respondents agreed with the statement “I pay attention to sufficient heat treatment of poultry meat” (Table II), and 84.2 per cent showed sufficient knowledge about it. However, most of the respondents explained that they check proper temperature treatment by cutting the meat or by assessing colour, only a few


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did so by measuring the internal temperature. The same was observed in the USA (Mazengia et al., 2015), the Netherlands (Bergsma et al., 2007), Belgium (Sampers et al., 2012), and Switzerland (Bearth et al., 2014). However, visual inspection is not necessarily a good indicator of the absence of bacteria (Bergsma et al., 2007). The only way to be certain about internal meat temperature during cooking is by using a thermometer. Almost half of respondents agreed with the statement “I follow instructions for poultry meat preparation if they are included on the packaging label” (Table II). Roasting or baking was reported as the preferred way of poultry meat preparation (Table II). The same was reported in two other studies (Bergsma et al., 2007; Gilbert et al., 2007). Another reported regularly used way of poultry meat preparation is barbecue, especially during Spring and Summer. This could be one of the reasons that the campylobacteriosis rate rises during these months in Slovenia (Nacionalni inštitut za javno zdravje/National Institute of Public Health, 2016). Respondents’ knowledge of microorganisms with emphasis on Campylobacter in poultry meat Respondents were asked some basic microbiology-related questions associated with foods, followed by questions regarding Campylobacter. Some of the results, shown in Tables II and III, in our study are worrying as only 57.8 per cent of respondents stated, “poultry meat in retail can be contaminated with harmful microorganisms”. Out of the 139 respondents who added explanations, 86.3 per cent showed sufficient knowledge of the topic (Table IV ). A Swiss survey showed that 17 per cent of consumers believed that poultry meat does not contain pathogenic microorganisms (Bearth et al., 2014). Although 42.2 per cent of respondents in our study were not aware of the presence of harmful microorganisms on foods in retail, only 24.9 per cent of respondents did not know that microorganisms can multiply in a refrigerator and in foods at room temperature (Table II). Sanlier (2009) reported that over 90 per cent of Turkish consumers are aware of bacterial growth on food. Additional questions regarding Campylobacter knowledge had a low response rate, indicating insufficient knowledge of Campylobacter in the field of food safety in home kitchens (Table II). Only 16.7 per cent of respondents reported knowing about the bacteria Campylobacter and 91 per cent out of 67 respondents who added explanations showed sufficient knowledge (Tables II and IV ). The most comparable results were obtained in Trinidad with around 15 per cent of consumers aware of Campylobacter (Badrie et al., 2006). Dutch consumers were more aware of bacteria on poultry meat, but their precise knowledge was limited. Only 4.3 per cent mentioned Campylobacter as bacteria connected to poultry meat, and the most frequently named bacteria was Salmonella (Bergsma et al., 2007). The best results were reported from New Zealand, where over 70 per cent of consumers connected Campylobacter and other bacteria to poultry meat (Gilbert et al., 2007), which was probably because of the campaign aimed at the education on campylobacteriosis in New Zealand. Responses to further questions about Campylobacter were not so good, as the majority of the respondents did not know the correct answers. It is quite worrying that respondents did not know about poultry meat contamination with Campylobacter (95.9 per cent) and that they did not know about proper heat treatment to eliminate it (89.1 per cent). This is one of the measures to assure safe poultry meat for consumption because Campylobacter is sensitive to temperatures above 70°C, and thorough cooking kills it (Bell and Kyriakides, 2009). Knowledge of proper heat treatment was better in Switzerland and the USA, where 30 per cent (Bearth et al., 2014) and 37 per cent (Mazengia et al., 2015) of consumers, respectively, did not know the proper internal temperature for poultry meat. Furthermore, other answers to detailed questions about Campylobacter showed a lack of knowledge of the contamination route of Campylobacter, the temperature that enables growth of Campylobacter, and the infective dose required to cause campylobacteriosis

(Table IV ). Explanations in the microbiological part were answered only by a small share of all respondents, only by the consumer cluster that declared that they have knowledge on the topic. By not answering, consumers avoid revealing their ignorance about food safety while simultaneously not learning anything about the issue. Knowledge of basic characteristics of Campylobacter could improve awareness of microbiological risks associated with poultry meat. Association between respondents’ characteristics and their knowledge and attitude Statistically significant differences between gender, age group, educational attainment, and living area where respondents gained their knowledge of safe food preparation were determined. There was no statistically significant difference according to the living area of respondents. Our results indicate a gender impact as men were less aware of the health risks associated with improper poultry meat preparation (37.8 per cent, po0.001), were less aware of retail poultry meat contamination with harmful microorganisms (53.4 per cent, p ¼ 0.001) and were less aware of the fact that bacteria can multiply in prepared, heat-treated foods left on the kitchen counter (32.4 per cent, p ¼ 0.002). Respondents with lower educational attainment were less aware of the health risks associated with improper poultry meat preparation (14.1 per cent, po0.001) and were less aware of the fact that microorganisms can multiply in the refrigerator (20.6, po0.001). Senior respondents were less aware of the fact that bacteria can multiply in prepared, heat-treated foods left on the kitchen counter (36.2 per cent, p ¼ 0.003) and were less aware of the fact that microorganisms can multiply in the refrigerator (46.6 per cent, po0.001). More respondents of ⩽ 25 years of age reported using dishcloths for hand drying during poultry meat handling than the other two age groups (84.4 per cent, p ¼ 0.020). Furthermore, in comparing sources of knowledge about safe food preparation gained, some statistically significant differences were observed. In the group of respondents who gained knowledge at work, these differences were present with the statement that improper home raw poultry meat preparation does not present a health risk (17.6 per cent, p ¼ 0.040) with not using a dishcloth (66.7 per cent, p ¼ 0.005) and with not using the same cutting board for different foods (23.5 per cent, p ¼ 0.012). In the group of respondents who gained knowledge in school, differences were present with the statement that improper home raw poultry meat preparation does not present a health risk (14.2 per cent, p o0.001) and with not knowing that retail poultry meat can be contaminated with harmful microorganisms (31.3 per cent, p ¼ 0.001). There were no statistically significant differences in other groups of respondents according to the source of knowledge of safe food preparation. Results of multivariate analysis of our study (Table III) have shown that men, respondents with lower educational attainment, and seniors were identified as groups of consumers with less awareness of the health risks associated with improper poultry meat preparation and with less knowledge about microorganisms, with emphasis on Campylobacter in poultry meat. Similar results were obtained from many other studies (Unusan, 2007; Sanlier, 2009; Ergönül, 2013) indicating gender, age and formal education as important factors in food safety knowledge and awareness. Possible strategies to improve consumers’ knowledge In countries where severe campylobacteriosis problems appeared, different measures were taken and many of them were consumer-oriented. Iceland implemented measures against campylobacteriosis in 1995, but an epidemic of campylobacteriosis was reported in 1999 (Tustin et al., 2011). In New Zealand, reported campylobacteriosis cases were much higher in comparison to other developed countries and poor hygiene was noted as the main reason for this (Al-Sakkaf, 2013). A targeted approach to fight campylobacteriosis was introduced in


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the UK to lower the burden of foodborne diseases with the public campaign “Acting on Campylobacter together” (Food Standards Agency (FSA), 2013). Interventions against campylobacteriosis included multidisciplinary co-operation to control Campylobacter in poultry, education of primary producers and processors, changes in poultry processing, packaging without leakage, freezing policy, and improvement of legislation and education of consumers (Tustin et al., 2011; Al-Sakkaf, 2013; FSA, 2013). For consumers’ education different campaigns were carried out. Information was spread with pamphlets distributed by post, available on line and in supermarkets, advertisements in the newspapers, public services announcements on television and radio (Tustin et al., 2011; FSA, 2013). Food safety knowledge and awareness among Slovenian consumers has increased over the past nine years, especially about checking poultry meat for the date of minimum shelf life (use by date), using of insulated bags when buying poultry meat and using paper towels during poultry meat preparation rather than dishcloths. The general picture is improved, however, most people still thaw frozen meat at room temperature, thus increasing the chances of bacterial growth and putting themselves at a risky position. Interestingly, there was an increase in reporting on the purchase of meat in butcher shops or at local producers. Despite these changes, the domestic environment remains the main source of food information. We anticipate that these changes have occurred due to the influence of the media and the promotion of the shop themselves – that is, improving product checking and transporting refrigerated foods. It also influenced purchasing habits due to the popularisation of so-called home-produced and bio-products. According to the data obtained, there remains room for improvement, especially with the focus on home food preparation, its preservation and improving awareness of possible risks in case of improper handling of food in the domestic environment. The mere awareness of consumers about the presence of Campylobacter on poultry meat and the importance of heat treatment to prevent the potential introduction of the pathogen into the body could most likely improve the knowledge and behaviour of consumers in Slovenia. Still, certain groups should know more detailed information, such as public kitchen facilities employees, which are often responsible for cooking for risk groups. In such a way they would be better aware of the risks of campylobacteriosis. Should opportunities be sought for improvement in consumers’ education via mass media campaigns? Such campaigns have been used to promote different health issues and, as such, they can prevent negative changes or produce positive changes in behaviour over general populations (Wakefield et al., 2010). As shown in Figure 1, gaps in consumers’ knowledge of poultry meat handling and food microbiology remain. Therefore, all possible routes to promote consumers formal and informal education and training should be activated and encouraged by state authorities. Conclusion Consumers mistakes regarding food safety knowledge or self-reported practice happen somewhere along the line between buying and eating because of carelessness, distraction, ignorance, but some are made by chance. In our study, we obtained information about the knowledge and habits regarding the microbiological risk of poultry meat preparation at home. The results revealed that consumers are aware of food safety issues and have some basic knowledge on proper food handling. However, it was found that a substantial part of consumers still lacks knowledge of the microbiological risk (e.g. only 57.4 per cent knew that retail poultry meat can be contaminated with potentially pathogenic bacteria, and over 80 per cent did not know about Campylobacter and its importance) and have poor habits in domestic poultry meat preparation (e.g. use of the same cutting board for the poultry meat and other foods, not assuring cold chain during transport, inconsistent storage of poultry meat, thawing of poultry meat at room temperature). Men, people with lower educational attainment, young adults, and seniors showed less knowledge and awareness than others did.


Current Weaknesses

Awareness during poultry meat purchasing and transport Awareness of the risk related to improper home raw poultry meat preparation

Sufficient Knowledge/ Awareness

Gaps in habits and knowledge of handling and preparation of poultry meat in the home kitchen

Total lack of knowledge of food microbiology and awareness of Campylobacter in poultry meat

Neutral Knowledge/ Awareness

Insufficient Knowledge/Awareness

Current Strengths

Sufficient food safety awareness can stimulate the demand for knowledge and self-reported practices that comprise the foundation of good housekeeping in domestic kitchens. Current Campylobacter preventive strategies regarding retail poultry meat contamination are not yet sufficiently successful. As we have illustrated, food safety knowledge, self-reported practices, and awareness of poultry meat handling among Slovenian consumers have improved, but a place for more improvement remains, especially through formal and informal education if we mobilise all relevant players in the food supply chain who represent partners of trust for consumers. Research limitation According to convenience sample technique, these results are limited in generalisation and inference making about the entire Slovenian population. In the future, we would like to obtain information for hypothesis generation and implement the research on representative national samples, which would improve the quality of the final results. However, for control the age and gender distribution in the study the multiple logistic regressions were used (Dos Santos Silva, 1999). The authors clearly advised all the Slovenian regions and relevant supermarket chains what gives indications about state of the art in knowledge and practice during buying and food preparation specially oriented on Campylobacter and poultry meat. Nevertheless, at the same time the publication gives clear view on development within consumer cluster as expected by the time frame. References Q2

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Figure 1. Opportunities for improvement in consumers’ formal and informal education and training

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Q5

Further reading XXXX (2015), “Statistical Office of Slovenia: population by age and sex, statistical regions”, Slovenia, available at: http://pxweb.stat.si/pxweb/Dialog/varval.asp?ma=05C2001E&ti=&path=../ Database/Demographics/05_population/10_Number_Population/10_05C20_Population_stat_ regije/&lang=1 (accessed 2 December 2017).

Corresponding author Mojca Jevšnik can be contacted at: [email protected]

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