Food Control 63 (2016) 187e194

Contents lists available at ScienceDirect

Food Control
journal homepage: www.elsevier.com/locate/foodcont

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

a r t i c l e i n f o a b s t r a c t

Article history: This study was performed with the aim to investigate and compare the level of food safety knowledge
Received 1 July 2015 among food handlers in three different countries, Serbia, Greece and Portugal, in different food estab-
Received in revised form lishments, namely restaurants, take-away places and catering companies. Total of 377 food handlers
9 November 2015
were involved in this study with 115 food handlers from Serbia (30.5%), 180 food handlers from Greece
Accepted 12 November 2015
(47.7%) and 82 food handlers from Portugal (21.8%). For each participant, the knowledge score (KS) was
Available online 18 November 2015
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%),
Keywords:
Food safety knowledge
followed by Serbian (71.3%), whereas Greek food handlers showed lower scores (69.1%, p < 0.05). The
Food handlers biggest knowledge gaps that have been identified in relation to temperature control, source of
Restaurants contamination of foods and food-stuffs and high-risk foods can be used as a foundation for further
Take-away improvements in food safety trainings.
Catering © 2015 Elsevier Ltd. All rights reserved.

1. Introduction connected with the consumption of food in take-away places or

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 mea-
sures that were recommended and implemented in the food in-
dustry, 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 food-
borne 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 res-
taurants, cafes, pubs, bars and hotels (EFSA & ECDC, 2015). Ac-
cording 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: nadasmigic@agrif.bg.ac.rs (N. Smigic).
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 inade-
quate 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 path-
ogens 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 cross-
contaminate 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,

http://dx.doi.org/10.1016/j.foodcont.2015.11.017
0956-7135/© 2015 Elsevier Ltd. All rights reserved.
188 N. Smigic et al. / Food Control 63 (2016) 187e194
Bartleson, & Michaels, 2008). The most often reported food han-
dlers' 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 Au-
thority 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 em-
ployees 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 per-
sonal 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, restau-
rants 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 dis-
tribution of food to the final consumer, as it is in restaurants, take-
away 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 (Baş, Şafak 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 establish-
ments. 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. Take-
away 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 ques-
tionnaires to workers/food handlers. In order to answer the ques-
tions, 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. Question-
naires 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 estab-
lishments (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) Serbia (n ¼ 115) Greece (n ¼ 180) Portugal (n ¼ 82) Between

p-value
N (%) KSx Withiny N (%) KS Within N (%) KS Within p- N (%) KS Withinz
p-value p- value p-value
value

377 70.5 115 71.3A 180 69.1B 82 72.6A 0.000*

(100%) (30.5%) (47.7%) (21.8%)

Gender Male 173 70.0 0.535 40 70.0A 0.088 106 68.7A 0.416 27 72.6B 0.972 0.050*
(45.9%) (34.8%) (58.9%) (32.9%)
Female 204 70.6 75 72.1A 74 69.6B 55 72.7A 0.016*
(54.1%) (65.2%) (41.1%) (67.1%)
ab a
Age <24 55 70.0 0.023* 16 68.6 0.048* 35 69.6 0.840 11 69.7 0.094 0.855
(16.4%) (13.9%) (19.4%) (13.4%)
ab abA A B
25e34 88 71.1 31 70.0 58 69.0 16 74.5 0.010*
(26.2%) (27.0%) (32.2%) (19.5%)
35e44 83 70.6ab 32 73.6bA 34 68.2B 27 73.6A 0.002*
(24.7%) (27.8%) (18.9%) (32.9%)
45e54 55 71.9b 22 70.4ab 20 69.1 16 72.2 0.468
(16.4%) (19.1%) (11.1%) (19.5%)
a b
>55 55 67.6 14 73.3 33 70.1 12 72.2 0.38
(16.4%) (12.2%) (18.3%) (14.6%)
Education Elementary 54 69.7 0.287 4 70.1 0.319 5 (2.8%) 67.2 0.047 45 71.4 0.134 0.302
school (16.1%) (3.5%) (54.9%)
High school 156 71.2 88 71.7A 43 69.5A 32 74.0B 0.039*
(46.4%) (76.5%) (23.9%) (39.0%)
College 68 69.4 17 68.6 61 67.1 3 74.2 0.189
(20.2%) (14.8%) (33.9%) (3.7%)
University 58 69.8 6 73.3 71 70.7 2 78.4 0.218
degree (17.3%) (5.2%) (39.4%) (2.4%)
Total work experience in food <2 years 86 69.8 0.786 45 71.0 0.314 38 70.9 0.359 14 69.5a 0.007* 0.763
sector (25.6%) (39.1%) (21.1%) (17.1%)
2-8 years 127 70.5 30 72.4A 84 68.8B 30 72.6abA 0.010*
(37.8%) (26.1%) (46.7%) (36.6%)
AB A bB
8-16 years 61 70.9 20 72.5 31 68.6 19 76.1 0.008*
(18.2%) (17.4%) (17.2%) (23.2%)
>16 years 62 70.1 20 69.0 27 67.8 19 71.6ab 0.099
(18.5%) (17.4%) (15.0%) (23.2%)
Work experience at the current <2 years 173 69.8 0.353 79 71.6 0.163 97 69.5 0.814 22 71.5 0.123 0.086
placae (51.5%) (68.7%) (53.9%) (26.8%)
AB A B
2-8 years 104 71.1 16 72.6 60 69.0 41 73.0 0.018*
(31.0%) (13.9%) (33.3%) (50.0%)
AB A B
8-16 years 31 71.5 11 70.9 9 (5.0%) 67.5 11 75.6 0.018*
(9.2%) (9.6%) (13.4%)
>16 years 28 69.3 9 66.0 14 68.0 8 70.0 0.704
(8.3%) (7.8%) (7.8%) (9.8%)
Food safety training courses Yes, organised by 80 71.2 0.286 18 68.7A 0.170 62 68.0A 0.163 15 73.5B 0.514 0.048*
Ministry (23.8%) (15.7%) (34.4%) (18.3%)
AB
Yes, organised by 173 69.7 56 72.2 118 69.0A 25 73.3 B
0.008*
others (51.5%) (48.7%) (65.6%) (30.5%)
No 83 70.8 41 71.1 0 (0.0%) 0.0 42 71.9 0.603
(24.7%) (35.7%) (51.2%)
Current food establishment Restaurant 122 70.8 0.389 30 69.0a 0.001* 60 68.7 0.193 32 71.7 0.345 0.135
(36.3%) (26.1%) (33.3%) (39.0%)
aA A B
Fast food 107 70.0 31 69.0 60 68.1 16 74.3 0.007*
(31.8%) (27.0%) (33.3%) (19.5%)
bA B AB
Catering 107 70.6 54 73.3 60 70.5 34 72.8 0.033*
(31.8%) (47.0%) (33.3%) (41.5%)
Number of employees at current 10 employees 145 70.6 0.787 56 68.9aA 0.000* 67 68.3A 0.092 38 73.3B 0.783 0.016*
food establishment (43.2%) (48.7%) (37.2%) (46.3%)
10- 25 100 69.9 11 68.8a 83 70.4 22 72.5 0.278
employees (29.8%) (9.6%) (46.1%) (26.8%)
bA B A
25 employees 91 70.5 48 74.6 30 67.3 22 73.4 0.000*
(27.1%) (41.7%) (16.7%) (26.8%)

*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 Additionally, data were analysed to identify knowledge gaps
than two groups, such as age, level of education, experience in food among food handlers and for that purposes chi-square test was
sector or participation in food safety training. 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 statis-
tical 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 han-
dlers 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 restau-
rants (32.4%), take-away (28.4%) and catering companies (39.3%).
Finally, 42.7% of all participants were employed in food establish-
ments 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 partici-
pants, education, type of food establishments and number of em-
ployees (p < 0.05) (Table 1). The youngest participants aged <24
years had the lowest KS, although no statistical significant differ-
ence among different age groups was found. Our results indicated
that food handlers holding college degree had the lowest knowl-
edge scores (69.4%) which was different from those with elemen-
tary, 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 pro-
viders) (p > 0.05). Food handlers from the enterprises with >25
employees had average scores of 70.5%, medium (10e25 em-
ployees) 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 em-
ployees) 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 in-
gredients, 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 por-
tions, 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 equip-
ment. 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 partici-
pants were asked about the importance to measure internal tem-
perature 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 bac-
terial 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 trans-
ferring 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 contamina-
tion, 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 per-
centage 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 patho-
gens, such as Campylobacter and Salmonella in domestic and
catering kitchens (Boer & Hahne , 1990; Elizabeth, Christopher,
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%) diar-
rhoea (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 con-
nected 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, Por-
tuguese 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 food-
borne 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 signifi-
cantly 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 Portu-
guese 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 re-
sults 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.
192 N. Smigic et al. / Food Control 63 (2016) 187e194

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

Question Correct answers (%)

Overall Serbia Greece Portugal p-

(n ¼ 377) (n ¼ 115) (n ¼ 180) (n ¼ 82) value

Cross-contamination
The reason for storing raw and cooked food separately. 92.2 88.8 92.2 96.3 0.181
Good practice of storing raw meat and bean salad in the same refrigerator. 73 60.4 71.2 94.9 0.000*
The possibility of storing raw meat anywhere in the refrigerator when tightly sealed in plastic film. 50.7 59.1 48.3 44.2 0.090
Possible route of transferring food-borne pathogens:
Food handlers, 91 100 83.9 95.1 0.000*
Raw food (raw meat, raw eggs, raw vegetables, etc.), 85.1 88.3 81.7 88.9 0.188
Bread and bakery products, 64.9 45.2 80.6 47.5 0.000*
Insects. 82.8 90.5 74.4 92.5 0.000*
Vegetables for a salad splashed with a few drops of raw chicken juice can be rinsed with water and further 82.6 75.5 85 86.3 0.08
used for food preparation.
Good practice after using the cutting board for cutting raw foods. 90.2 90.4 89.4 91.5 0.091
Good practice after using the knife for cutting raw meat. 68.3 85.1 72.8 34.6 0.000*
Good practice of putting ice cubes in glass:
Using tongs, 91.7 99.1 87.2 91.5 0.002*
Using an ice scoop, 81.8 95.6 71.7 88.9 0.000*
Scooping ice into the ice cubes, 89.5 55.6 96.1 82.1 0.000*
Picking ice cubes with bare hands. 96.8 91.1 97.8 100 0.004*
Good practice of thawing food. 18.2 13.9 20.0 19.8 0.000*
Temperature regime
Food handlers' reaction when food is delivered at inadequate (too high) temperature. 52 32.2 56.1 71.3 0.000*
Optimal temperature for bacterial multiplication. 66.4 67.3 66.5 64.9 0.000*
Bacterial behaviour at chilled temperatures. 53.7 47.7 52.8 63.8 0.000*
Required temperature inside refrigerator. 81.9 79.5 80 89.7 0.000*
Given temperature of 13 C is allowed for chilled storage of cold food. 40.5 32.3 49.4 29.9 0.002*
Good practice of portioning hot food in smaller portions when chilling. 60 69.4 50.6 69.5 0.001*
Maximum period for keeping cooked food at chilled 4  C. 90.5 93.5 85 98.8 0.000*
Minimal allowed temperature for keeping thermally processed warm food. 43.9 49 41.5 41.2 0.000*
Why it is important to measure internal temperature during thermal food preparation? 20.5 6.7 9.4 68.1 0.000*
Maximal tolerable temperature during oil or fats heating. 51.9 55.6 36.1 85.3 0.000*
Good practice and frequencies of changing oil or fats used for heating. 49.9 47.4 60.6 29.1 0.000*
If fish has been stored at temperature that is too warm, but then it is properly cooked to the correct internal 66.7 71 65 65 0.557
temperature, it becomes safe to eat.
Food handling and health problems
May handle food when:
…having a diarrhoea 80.9 81.8 87.8 64.2 0.000*
…having hypertension 69.5 60.4 63.3 95 0.000*
…having a cold 88.6 91.7 92.2 76.3 0.000*
…having a toothache 73.9 63.1 71.7 92.6 0.000*
…coughing and wearing protective mask 53 41.9 48.9 76.5 0.000*
…having raised temperature 71.3 73.6 74.4 61.3 0.078
…vomiting 93.7 92.2 93.9 95.1 0.716
…I had cut myself 89.8 85.6 93.3 87.5 0.084
…wearing nail polish 91.3 88.8 90.6 96.3 0.172
…I am upset 69.6 65.7 59.4 97.5 0.000*
…having wounds on my hands 93.4 92.5 97.2 86.3 0.004*
Good practice when handler had an open cut on his finger and working on ready to eat food preparation. 87.9 91.6 85 90.1 0.222
Hand hygiene
Washing hands is mandatory after…
…handling raw foods 97.6 99.1 95.6 100 0.041*
…using the toilet 97.9 100 95.6 100 0.011*
…touching money 95.2 99.1 91.7 97.6 0.008*
…handling garbage 98.4 100 96.7 100 0.036*
…blowing nose 97.3 99.1 95 100 0.024*
…eating or drinking 90.4 97.4 83.3 96.3 0.000*
Food and food-borne diseases
Identification of food contaminated with food-borne pathogens. 36.3 20.9 48.9 28.9 0.000*
Identification of cooked food that might cause food-borne disease. 27.2 25.5 35.9 10.3 0.000*
Identification of food that might cause food-borne disease if not properly cooked.
Beef 70.5 93.5 55.6 73.2 0.000*
Eggs 82.3 93.4 72.2 90.1 0.000*
Carrots 91.7 77.3 95.6 98.8 0.000*
Poultry 95.6 98.1 96.1 91.5 0.079
Identification of sterilized food. 45.8 48.5 43.3 48.6 0.000*
Foodstuffs frequently implicated in Salmonella food poisoning:
Eggs 85.8 97.1 75.6 93.9 0.000*
Dairy 47.4 70.6 31.7 58.4 0.000*
Fish 57.6 45.8 68.3 43.6 0.000*
Chicken meat 85.7 93.6 90 67.1 0.000*
Potato puree 82.4 72.7 96.1 59.5 0.000*
Common symptoms of food-borne diseases. 90.8 89.2 90 94.8 0.017*

*Statistical significance p < 0.05.

 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 tempera-
ture 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. Addi-
tionally, 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 wa-
ter, 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 food-
borne 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 mi-
crobial 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 ani-
mals' 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 ob-
tained 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 non-
trained 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 imple-
mented. 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 com-
bined 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 Eu-
ropean countries involved in this study have one cultural dimen-
sion 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 re-
sponsibility, 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 un-
derstanding 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 simpli-
fied explanation of specific issues, such as time and temperature
and cross contamination. Additionally, the in-depth comprehen-
sion 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 method-
ologies. 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 tem-
perature 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
194 N. Smigic et al. / Food Control 63 (2016) 187e194
of training formats. This might help improving and targeting ma-
terial for legally obliged trainings, and subsequently improve food
safety practices among food handlers.
Appendix A. Supplementary data
Supplementary data related to this article can be found at http://
dx.doi.org/10.1016/j.foodcont.2015.11.017.
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