Food Control 34 (2013) 613e618

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Food Control
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Evaluation of food safety training on hygienic conditions in food establishments

K. Soares a, J. Garca-Dez b, A. Esteves a, I. Oliveira c, C. Saraiva a, *
a

School of Agrarian and Veterinary Sciences, DCV, CECAV, University of Trs-os-Montes and Alto Douro, Apart. 1013, P 2, 5001-801 Vila Real, Portugal Cooperativa Agrcola de Chaves, ADS Vila Pouca de Aguiar, Bairro da Brangada, 5450-005 Vila Pouca de Aguiar, Portugal c School of Science and Technology, DM, CM-UTAD, University of Trs-os-Montes and Alto Douro, Apart.1013, 5001-801 Vila Real, Portugal
b

a r t i c l e i n f o
Article history: Received 11 April 2013 Received in revised form 30 May 2013 Accepted 4 June 2013 Keywords: Training Food safety Food handlers Hygiene

a b s t r a c t
Food handlers training is fundamental in order to ensure the safety of the foodstuff. However, the success of training programs that provide only information is unclear and changes in improper food practices are not usually achieved. Food training programs based on theoretical as well as practical activities have been revealed as an important tool in which food handlers can put information into practice. Thus, the objective of this study was to assess the inuence of food safety training, based on both theoretical and practical approaches, on the microbiological counts of food contact surfaces, food tools, food equipment surfaces and hand washing in canteens and cafes of one university campus. After food safety training, total plate counts decreased about 60% in the case of canteens and almost 45% in cafes while moulds and yeasts decreased approximately 65% in canteens and 55% in cafes. In terms of location, the microbiological reductions observed were higher for food equipment in canteens and for food tools in cafes. The microbiological counts of food handlers hands decreased after both food safety training and disinfection. Food safety training inuenced the reduction of overall microbiological parameters. Parametric t-tests (after vs before training) indicated that reductions were statistically signicant before and after disinfection for total plate counts. The decrease observed for total coliforms and Enterobacteriaceae, were statistically signicant only before disinfection. The food safety programs cannot be based entirely on a theoretical approach but also on adequate training which includes a practical approach. The success of the microbiological reductions in the study was associated to the practical lessons which let the handler put into practice the knowledge acquired in the theoretical part. 2013 Elsevier Ltd. All rights reserved.

1. Introduction Food-related infections constitute an important health problem in both developed and developing countries. Nowadays, food establishments in Europe must comply with strict food legislation which requires them to have food safety systems in place based on HACCP principles (Reg. N 852/2004). Various studies demonstrated that implementation of HACCP plans and pre-requisite programs improved the safety of meals served (Cenci-Goga et al., 2005; Soriano, Rico, Molt, & Maes, 2002), however, foodborne outbreaks still occurred. In addition, the successful implementation of the procedures based on the HACCP principles requires the full cooperation and commitment of food business employees. Food handlers training is fundamental in order to ensure the safety of

* Corresponding author. Tel.: 351 259350000; fax: 351 259350480. E-mail address: crisarai@utad.pt (C. Saraiva). 0956-7135/$ e see front matter 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.foodcont.2013.06.006

the products (Jevsnik, Hlebec, & Raspor, 2008). However, current evidence suggests that food handlers are one of the main vehicles for contamination of foodstuffs and may also be asymptomatic carriers of food-borne microorganisms (Greig, Todd, Bartleson, & Michaels, 2007). Moreover, factors including but not limited to contaminated raw materials, poor hygiene of equipment, food tools, facilities, as well as improper practices also contribute to the occurrence of food-borne outbreaks (Jianu & Chis, 2012). The increase of the food safety standards implies food safety education, which is essential to any food safety system where the presence of food handlers with poor hygienic practices and/or food safety training could be a real threat to the safety of food (Kaferstein, Motarjemi, & Bettcher, 1997). Several authors stated that the success of training programs providing only information is unclear and changes in improper food practices are not usually achieved (Clayton, Grifth, Price, & Peters, 2002; Seaman & Eves, 2008). To avoid this problem, food training programs based on theoretical and practical activities have revealed to be important tools in which

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food handlers can put acquired knowledge into practice. The effects of food safety training on food handlers knowledge have been previously described (Martins, Hogg, & Otero, 2012; Soares, Almeida, Cerqueira, Carvalho, & Nunes, 2012), however, the information about the real impact on food safety by practical food safety training is scarce. The aim of this study was to assess the inuence of theoreticalpractical food safety training based on the microbiological counts on food contact surfaces, food tools, food equipment surfaces and hand washing by handlers in canteens and cafes of a university campus. 2. Material and methods 2.1. Food establishment characterization The inuence of food training on the microbiological counts on equipment, food tools and surfaces was studied at 5 canteens and 6 cafes on the campus of a university in northern Portugal. Canteens presented different areas to prepare each group of products (meat, sh and vegetables), the kitchen, pastry area, serving area and washing area. The canteens main activity is to serve lunch and dinner, approximately 200 thousand meals per year (meat, sh and vegetarian). On the other hand, the cafes were smaller than the canteens and held no specic areas as presented as described above. Their main activity is to serve fast food, pastry, sugar drinks and/or juices and coffees. At the moment of study, all food establishments had already implemented a food safety system based on the HACCP methodology, according to the national food law. As a part of the study, all of the food establishments handlers were individually interviewed to obtain systematic information on gender, age, education, professional experience and any previous food safety training. 2.2. Food handlers training A food safety training program was specially developed for all of the food establishments handlers on the campus. Training was given by only one trainer. Food safety training consisting of 9 h (3 sessions of 3 h each) per group and was divided into three parts per session: (1) General concepts of hygiene and food safety, (2) practice and (3) in-situ application of the knowledge acquired. The rst part consisted of a theoretical approach of concepts such as personal hygiene, temperature control, pest-control, cleaning and disinfection, food hygiene, food microbiology, traceability and HACCP, all according to the specications of the Training Manual on Food Hygiene and the Hazard Analysis and Critical Control Point (HACCP) System (FAO, 2002). Training sessions were given to small groups of 4 food handlers belonging to canteens and groups of 2 food handlers belonging to cafes to better achieve a strict interaction between trainer and handler. During the theoretical part, several slides, pictures and videos were presented to the participants and were used for in-depth explanation of several food safety practices. The second part consisted of practical training in order to consolidate the knowledge acquired in the rst part. In this section, the instructor demonstrated the practical aspect of each HACCP pre-requisite. For example, how cross contamination occurs, the effectiveness of hand washing, temperature checking, correct record of temperatures, cleaning, disinfection and traceability, identication in-situ of critical control points, deviation procedures as well as others, were shown to participants. This step reinforced the food safety concepts previously discussed in the theoretical portion. Finally, in-situ application of the previously acquired knowledge consisted of an audit done by the food safety trainer in order to

verify the procedures performed by the food handlers during the workday. Throughout this procedure, corrective measures were applied in cases of inappropriate hygiene and/or food safety procedures detected. The objective was to enhance the theoretical knowledge learnt during the rst part of the training program and then also apply it daily. 2.3. Microbiological sampling of surfaces, food equipment, food tools and food handlers hands A total of 504 microbiological samples of surfaces, food tools and food equipment were taken in the establishment of the study after cleaning and disinfection. Half were taken before the food handlers food safety training and the other half fteen days after food safety training. Food contact surface samples included walls, shelves and food tables. Food equipment included all kinds of appliances, such as coffee machines, washing machines, ovens, microwave ovens, roasters, fridges, freezers, slicers, gas and electrical hot points, squeezers. Food tools included all kinds of utensils used for food handling and/or food serving, such as cutting boards, cutlery, dishes, glasses, wine glasses, bowls, coffee cups, tea spoons, knives, clamps, ladles, casseroles, frying pans, slotted spoons, saucers, and lunch boxes. Food handlers hygiene was evaluated by 480 microbiological samples of bare hands. 120 microbiological samples (60 of each hand) were taken before and after the food safety training as well as before and after the cleaning and disinfection of hands. The objective of the microbiological analysis of separate hands was to investigate the relationship between microbial load and the food handlers dominant and non-dominant hand. Total plate counts, moulds and yeasts were evaluated on surfaces, food tools and food equipment. Initially, Enterobacteriaceae was randomly evaluated on 100 food contact surfaces, food tools and food equipment and, in all of them, counts were below the detection limit. In consequence, Enterobacteriaceae was not evaluated during all the studied period. The hygiene of food handlers was assessed by the microbiological analysis of total plate counts, moulds and yeasts, Enterobacteriaceae, Escherichia coli and coagulase-positive Staphylococcus aureus. The food contact surfaces, food equipment, food tools, and food handlers bare hands samples were collected using the swab-rinse technique in duplicate. A sterile swab, moistened with tryptone salt solution, was rubbed for 20 s over the surface to be sampled. Sampling of food-contact surfaces, food equipment and food tools was carried out by using a sterile paper template of 10 cm2, 25 cm2 and 100 cm2 that was used to outline a known area, inside which the swabbing was done. The swab was then placed in a tube containing 10 ml of tryptone salt, shaken and stored at 2  C in an ice container and then analyzed within 2 h of arrival at the laboratory. Then, 1 ml (for coliforms, Enterobacteriaceae and E. coli) or 0.2 ml (for moulds, yeasts, and S. aureus) of the rinse uid was poured in appropriate culture media onto 90 mm Petri dishes. The total coliform counts were obtained after incubation on Violet Red Bile lactose agar (Oxoid, England) at 30  C for 24 h, the Enterobacteriaceae counts were obtained after incubation on Violet Red Bile glucose (Oxoid, England) at 34  C for 24 h. The total plate counts were obtained after incubation on plate count agar (Oxoid, England) at 30  C for 24 h, the mould and yeast counts were obtained after incubation on Chloramphenicol glucose agar (Biokar diagnostics) at 25  C for 3e5 days. The S. aureus counts were obtained after incubation on Baird-Parker agar (Biokar diagnostics) at 37  C for 24 h, and the E. coli counts were obtained after incubation on Tryptone bile glucuronic agar (Biokard diagnostics) at 41.5  C for 24 h. The enumeration of characteristic cell forming units for total coliforms (NP 788:1990), total plate count (ISO 4833:2003), mould and yeast (ISO 13681:1995) and E. coli (ISO 16649-2/2001) was

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based on the identication procedures. The enumeration of Enterobacteriaceae (ISO 21528-2:2004) and coagulase-positive S. aureus (ISO 6888-1:1999, ISO 6888-2:1999) was performed by biochemical tests and a coagulase test respectively. In case the microorganism counts were below the detection limit, the result was considered to be zero for statistical purposes. For cleaned and disinfected food-contact surfaces, food tools and food-contact equipment, the standards considered were previously described by Sneed, Strohbehn, Gilmore and Mendonca (2004). Briey, the standard for total plate count was less than 1.3 Log cfu/cm2. For total coliforms and Enterobacteriaceae, the standard considered was less than 1.0 Log cfu/cm2. For study considerations, authors considered the standard for moulds and yeasts less than 1.0 Log cfu/cm2. The results were expressed in Log cfu/ cm2. For bare hand analysis, a standard of less than 2 Log cfu/cm2 for total plate counts was adopted (Republic of South Africa, 1999). Due to the absence of microbiological criteria for Enterobacteriaceae, coliforms, moulds and yeasts, a target value less than 0.4 Log cfu/ cm2 as described by Moore and Grifth (2002) was adopted. 2.4. Data analysis The effect of food safety training on microbiological counts of surfaces, food tools and Equipment, carried out in canteens and cafes, was assessed using t-tests. Descriptive results were evaluated within each establishment .The comparison of the microbiological counts means between the left hand and right hand was assessed by paired samples within each treatment (before and after disinfection) in each moment of training (before and after) (Pestana, & Gageiro, 2008). The mean microbiological counts of both hands were also evaluated using t-test for independent samples (before and after training) in each treatment (before and after disinfection). Values of p < 0.05 were considered as statistically signicant. 3. Results 3.1. Food handlers socio-demographic composition A total of 60 food handlers were individually interviewed. The socio-demographic characteristics, such as sex, age, educational level, seniority, job responsibility and previous food safety training are described in Table 1.
Table 1 Demographics of food handlers of canteens and cafes. Demographics items Sex Age Male Female 35 35e45 46e55 !55 6th degree 9th degree 12th degree 2e5 years 6e10 years 11e20 years >20 years Food handling/cooking Food handling/public attendant Payment Warehouse Yes No N 14 46 8 18 16 18 13 28 19 7 13 27 13 29 20 7 4 51 9 % 23.33 76.67 13.33 30.00 26.67 30.00 21.67 46.67 31.67 11.67 21.57 45.00 21.67 48.33 33.33 11.67 6.67 85.00 15.00

3.2. Food working surfaces, food tools and food equipment microbiological results After food safety training, total plate counts decreased approximately 60% in canteens and almost 45% in cafes while the mould and yeast counts decreased 65% in canteens and 55% in cafes. The reductions of the microbiological counts in canteens ranged from 22% to 87%. In addition, the canteen with the highest microbiological counts before food handlers training showed the largest decrease after the training program. The reductions of the microbiological counts observed in 5 cafes ranged from 47% to 75% and in one cafe it was observed for total plate counts an increase of 22% after the food safety training program. In terms of location, the reductions of total plate counts were larger for food equipment and food tools in canteens and cafes respectively (Table 2). The microbiological counts of results observed for moulds, yeasts and total plate counts decreased after food handlers training and they were higher in canteens than cafes, however, higher mould and yeast counts were observed in two cafes after food training program. In contrast, a total decrease for below limit detection was achieved in two cafes. In terms of location the largest reductions of moulds and yeasts (Table 2) were achieved in food equipment and food contact surfaces for canteens and in food tools for cafes. With regard to the standard criteria, before food safety training, in general all canteens and three cafes presented acceptable total plate counts, while after food safety training, all establishments presented acceptable levels of total plate counts. On the other hand, mould and yeast counts were acceptable for both canteens and cafes after and before food training. The paired t-test showed that food safety training was statistically signicant for the microbiological reductions of total plate counts, moulds and yeasts in canteens food equipment. In addition, the reductions of total plate counts observed for cafes food tools were statistically signicant. 3.3. Food handlers bare hands microbiological results Data on microbiological parameters are presented in Table 3. Neither E. coli nor coagulase-positive S. aureus were detected in any of the sampling periods. According to the standard described before, the overall results for total plate count were acceptable, however, the absence of proper food safety training resulted in nonacceptable microbiological counts for Enterobacteriaceae and total coliforms for both the left and right hand before disinfection. The microbiological counts were 20% higher in the right hand for moulds, yeasts and coliforms before food safety training and before disinfection. In contrast, the counts of Enterobacteriaceae were 20% lower in the right hand. After hand washing, the counts of

Education level

Table 2 Paired students t-test for mean difference of microbiological values (Log ufc/cm2) after vs before training for food establishments. Food establishment Sample location Total plate counts P value After vs before training 0.3249 0.0227 0.0748 0.0012 0.5477 0.2081 Moulds and yeasts P value After vs before training 0.2440 0.1161 0.2883 0.1731 0.0477 0.0079

Seniority

Canteens

Job responsibilities

Cafes

Previously food safety training

Food equipment Food tools Food-contact surfaces Food equipment Food tools Food-contact surfaces

0.023 0.931 0.720 0.996 0.365 0.016

0.023 0.479 0.050 0.136 0.323 0.971

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Table 3 Microbiological counts for food handlers and independent student t-test for mean difference of microbiological values (Log ufc/cm2) after vs before training for both hands before and after disinfection.

After training

1.23 0.35 0.28 0.09 ND

1.60 0.00 0.00 0.00

Enterobacteriaceae and total coliforms were double in the right hand than in the left one, however, no signicant differences between hands were observed (p > 0.05). The observed decrease for Enterobacteriaceae after disinfection was statistically signicant (p < 0.01). After food safety training, the right hand presented higher microbiological counts for total plate counts, moulds and yeasts before hand washing and for total plate counts, Enterobacteriaceae and coliforms after hand washing. In contrast, the microbiological analysis of bare hands did not present differences between them (p > 0.05). The decrease of total coliforms and Enterobacteriaceae observed after hand washing was statistically signicant (p < 0.01). The previous positive knowledge of hand washing presented by food handlers before food safety training may be associated to the previous food safety training declared by 85% of respondents (data not shown) and in accordance of the HACCP plan. In addition, the reductions observed in the overall microbiological parameters before and after disinfection were statistically signicant (p < 0.001). After food safety training, the overall microbiological counts decreased after hand washing, however, only the decrease which occurred for total plate counts (p < 0.001) and Enterobacteriaceae (p < 0.01) were statistically signicant. The food safety training inuenced the reduction of overall microbiological parameters studied, ranging from 24% for moulds and yeasts up to 64% for total coliforms. Indeed, the comparison between before and after food safety training (Table 3) showed a statistically signicant decrease for total plate counts before (p < 0.001) and after (p < 0.01) disinfection respectively. With regards to total coliforms (p < 0.01) and Enterobacteriaceae (p < 0.01), reductions were statistically signicant only before disinfection.
Results were expressed as mean Log cfu/cm standard deviation. ND: not detected. L: left hand, R: right hand.

After training

0.21 0.00 ND 0.33 0.00 0.14 0.00 ND 0.57 0.00 ND 0.44 0.00 0.12 0.00 ND 0.17 0.00 ND 0.05 0.00 0.00 0.00 ND 0.59 0.00 ND 0.20 0.00 0.05 0.00 ND 0.3886 0.000 0.1329 0.0146 e 0.002 e 0.198 0.752 e

Right hand

Before training

After training

Left hand

Before training

After hands disinfection

Bare hands (L and R)

After vs before training

P value

ND

ND

ND

ND

ND

4. Discussion Food safety training of the food handlers in restaurants and cafes is fundamental to guarantee the safety of the foodstuff. In other countries, all the employees in the food retail sector must participate in a food protection certication program like Servsafe, the food handler program of the National Restaurant Association, USA. In Portugal, unspecic training of 35 h per year is mandatory (Portugal, 2009). However, a previous certicate on food safety is not compulsory in order to work in the catering/ restaurant sector. Although there are several studies on food handlers education, the novelty of this study is based on the evaluation of the training programs real efciency throughout the microbiological analysis of the hygienic conditions of canteens, cafes and food handlers. The improvement (enhancement) of the establishments hygiene because of the food handlers food safety training was clearly identiable. The overall microbiological counts decreased after training according to Capunzo et al. (2005). Reductions were larger for canteens than cafes. In addition, the largest higher microbiological reductions were achieved in food-contact surfaces in canteens while the lowest counts were observed for food tools in cafes. The fact that the largest reductions of the overall microbiological counts occurred in canteens rather than in cafes may be due to the higher number of employees in canteens than in cafes. The differences in work routine between canteens and cafes may have also inuenced the largest microbiological reductions observed in the rst establishments. Since the main activity of canteens is serving lunch and dinner, it was observed that employees had a greater willingness in cleaning and disinfection operations. This fact may explain the statistical signicance of reductions for total plate counts, moulds and yeasts after food safety training for food equipment (Table 2). In contrast, the

Right hand

Before training

1.90 0.47 0.65 0.60 ND 1.14 0.30 0.40 0.22 ND 1.88 0.39 0.80 0.49 ND 0.7112 0.0996 0.3898 0.3904 e 2.10 0.00 0.00 0.00 1.32 0.00 0.00 0.00

2.17 0.00 0.00 0.00

After training

Left hand

Before training

Before hands disinfection

Bare hands (L and R)

After vs Before training

ND e e

ND

ND

P value

Total plate counts Moulds and yeasts Enterobacteriaceae Total coliforms S. aureus coagulase positive E. coli

0.000 0.458 0.005 0.001 e

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highest number of activities and its variety (and also associated to the lower number of employees) carried out in cafes, cleaning and disinfection operations were conducted on-demand, mainly on food tools. The differences observed in food facilities and equipment between canteens and cafes may also explain the differences between the microbiological counts. In canteens, the hygienic design of food contact surfaces or presence of stainless steel equipments may facilitate the cleaning and disinfection operations (Dr, 2007), where as cafes presented a high number of difcult equipment to clean, such as coffee machines, toasters, microwave ovens, glass shelves, among others. Both canteens and cafes presented, in general, acceptable microbiological counts with regard to the standard criteria described above (Sneed et al., 2004) after training food handlers, however, the presence of three cafes with non-acceptable levels of total plate counts before training, may be associated to the employees lower level of knowledge due to their lack of experience and/or absence of previous food safety education. The microbiological analysis of bare hands showed that correct hand washing and disinfection was achieved throughout the food safety training, which is in agreement with other authors (Egan et al., 2007; McIntyre, Vallaster, Wilcott, Henderson, & Kosatsky, 2013). As expected, the hand washing decreased the microbiological counts; however, further reductions were achieved after food safety training (Acikel et al., 2008). This may be explained by lower microbiological counts before and after disinfection after food safety training compared to before training. It suggests that food handlers started to follow the rules of hand disinfection more rigorously after food safety training. The occurrence of high microbiological counts on the right hand compared to the other one, before and after food safety training, can be related to the fact that most handlers of the study were right-handed, as reported by an, Kuckkaraaslan, Baysallar and Bas lu Ayiek, Aydog ustaog (2004), however, no statistical differences were found between the left and right hand. Results observed for total plate counts, coliforms and Enterobacteriaceae were according to Lues and Van Tonder (2007). In addition, E. coli was not detected in all of the food handlers hand samples. Lues and Van Tonder (2007), also reported the presence of E. coli in only 1 of 50 food handlers hand samples. E. coli has been reported as an acknowledged indicator for faecal contamination, however, it is normally absent from hands (Lues and Van Tonder, 2007). Presence of S. aureus has been largely found on food handlers hands (Acikel et al., 2008; Ayiek et al., 2004; Sospedra, Mas, & Soriano, 2012; Todd, Michaels, Smith, Greig, & Bartleson, 2010) because this bacteria is the only pathogenic microorganism in the permanent group of bacteria associated with human skin (Ayiek et al., 2004), however, no food handlers hand sample of our study was positive, due to the negative results of the coagulase biochemical tests (Ramalhosa, Magalhes, & Pereira, 2012). The main limitation of this study was associated to the rst part of the food handlers food safety training due to their work schedule. To avoid this problem, the rst part of the food safety training as described above was given during the pause periods due to the interest shown by all food handlers involved in this study. 5. Conclusion The results of this study showed that the effect of food handlers training was essential to increase the hygienic conditions of the food establishments in the study. Although the overall microbiological counts decreased after the food safety training program, several differences related to the specic characteristics of the two categories of establishments in our study were found. Thus, the differences in layout, equipment, hygienic design, food services and

food handlers in these establishments imply that the food safety training programs have been specially developed for each food sector and/or establishment size. In addition, the success in the microbiological reductions was achieved due to the practical approach of the food safety program which let the employee put the acquired knowledge in play. With regard to the microbiological counts of hand washing, an increase in the knowledge of food safety resulted in the lower level of hand contamination. Moreover, this study demonstrates that food safety training is also important to guarantee the safety of foodstuff, thus avoiding the implication of food handlers in food-borne outbreaks. Further research about the inuence of theoretical and practical food safety training on the microbiological counts of ready-to-eat foodstuff has to be carried out. Acknowledgements The authors would like to thank SASUTAD for their facilities, Mrs. Ana Leite and Mr. Felisberto Borges for their laboratorial support, CECAV-UTAD, CM UTAD and the research funded by the Portuguese Government through FCT under the project and PEstOE/MAT/UI4080/2011. References
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