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Food Control 18 (2007) 707712

www.elsevier.com/locate/foodcont

Food handling: Comparative analysis of general knowledge and practice


in three relevant groups in Portugal
Eduarda Gomes-Neves

a,b,

, Ana Cristina Arajo a, Elisabete Ramos c, Carla SoWa Cardoso

Molecular Pathology and Immunology, Instituto de Cincias Biomdicas Abel Salazar (ICBAS), University of Porto,
Largo Prof. Abel Salazar 2, 4050-011 Porto, Portugal
b
Direco Regional de Agricultura de Entre Douro e Minho (DRADEM), Ministrio de Agricultura, Rua Dr. Francisco Duarte,
355 1 4710-093 Braga, Portugal
c
Department of Hygiene and Epidemiology, Porto Medical School, University of Porto, Alameda Professor Hernni Monteiro,
4200-319 Porto, Portugal
d
Iron genes and Immune System group (IRIS), Institute for Molecular and Cell Biology (IBMC), University of Porto, Rua do Campo Alegre,
823 4150-180 Porto, Portugal
Received 25 January 2006; received in revised form 15 March 2006; accepted 20 March 2006

Abstract
A self-administered questionnaire designed to assess Knowledge and Practice of public hygiene measures was tested in a group of
food handlers (n D 79) and two groups of undergraduate students (n D 152). Students were poorly acquainted with practical aspects, relating speciWcally to temperature control and food storage requirements. A signiWcant proportion of food handlers lacked basic knowledge
and understanding of microbiological hazards, hygiene and safety rules. The mean food safety Knowledge score among food handlers
was 55.0 18 and the mean Practice score was 69.0 17. The results point to the need to improve training and increasing awareness of
the measures imposed by food safety laws in Europe.
2006 Elsevier Ltd. All rights reserved.
Keywords: Hygiene; Food handlers; Undergraduate students; Knowledge; Practice; Portugal

1. Introduction
A high level of public health protection is one of the fundamental objectives of EC food law. The demand of application of HACCP (hazard analysis and critical control
points) principles introduced by the Codex Alimentarius 30
years ago became law in Portugal in 1998 (Dirio da Repblica, 1998). Regulation (EC) No 852/04 underlining the
need of all the food businesses to identify the steps of the
production process in order to secure food safety has been
implemented in 2006. Regulation No 178/2002 created the
*
Corresponding author. Address: Molecular Pathology and Immunology, Instituto de Cincias Biomdicas Abel Salazar (ICBAS), University
of Porto, Largo Prof. Abel Salazar 2, 4050-011 Porto, Portugal. Tel.: +351
22 2062200; fax: +351 22 2062232.
E-mail address: egomesneves@mail.icav.up.pt (E. Gomes-Neves).

0956-7135/$ - see front matter 2006 Elsevier Ltd. All rights reserved.
doi:10.1016/j.foodcont.2006.03.005

European Food Safety Authority and deWned the general


principles and requirements of food law laying down procedures in matters of food safety. According to the latter,
food must not enter the market if it does not meet the
established safety standards. FoodstuV safety, however, is
ensured mainly by preventive measures, such as implementation of good hygiene practice and application of procedures based on HACCP principles and other hygiene
control measures (Sun & Ockerman, 2005). Moreover, the
impending EC legislation will require documented HACCP
in all food businesses from 2006 (Taylor & Kane, 2005).
The measures to be taken by the food business operators in
order to ensure compliance with the established criteria
include, among other things, control of raw materials,
hygiene, temperature and shelf-life of the products.
A successful implementation of the law recognizes education of food handlers as a crucial line of defence in the

708

E. Gomes-Neves et al. / Food Control 18 (2007) 707712

prevention of food borne illnesses (Legnani, Leoni, Berveglieri, Mirolo, & Alvaro, 2004; Martnez-Tom, Vera, &
Murcia, 2000; Sun & Ockerman, 2005; Worsfold, 2001).
Recent survey studies conducted in Turkey, South Africa
and the United Kingdom pinpointing the need for training
and education of food handlers in public hygiene measures
and revealed a general lack of knowledge of microbiologic
food hazards, refrigerator temperature ranges, cross contamination and personal hygiene (Bao, Ersun, & Kvan,
2006; Nel, Lues, Buys, & Venter, 2004; Walker, Pritchard, &
Forsythe, 2003). The available information about knowledge and practice of food handlers from small food businesses in Portugal is limited in spite of increasing consumer
demands (Santos, 2004). Consumers are worried about the
safety of food products. These increasing concerns relate to
food safety incidents reported in the last decade (Beulens,
Broens, Folstar, & Hofstede, 2004; Blaha, 1999; Bruhn,
2005; Nel et al., 2004; Sun & Ockerman, 2005). Nevertheless, to our knowledge, there are no studies assessing general knowledge and/or practice of hygiene measures by
food handler groups and/or other relevant groups in Portugal.
The aim of this study was to evaluate and compare the
level of general knowledge and practice in food handling
and food storage in three groups: food handlers from small
food businesses, 1st year undergraduate students and 3rd
and 4th year undergraduate students from the University of
Porto (Portugal). To our knowledge, this is the Wrst comparative survey of food handling knowledge and practice in
Portugal between three relevant groups. Valuable studies
focusing on food handlers have been reported recently in
other countries (Bao et al., 2006; Nel et al., 2004; Walker
et al., 2003).
2. Material and methods
2.1. Questionnaire design
A self-administered questionnaire was developed for this
study with 23 multiple choice questions with three, four or
Wve possible answers, including do not know, to minimize the possibility of selecting the correct answer by
chance.
The questions were designed and structured in two
groups (Table 1). A group designated Knowledge (10
questions) designed to assess knowledge about microbiologic food hazards, food poisoning and food borne illness,
high-risk food groups and water treatment, as water supply
and quality and food security and safety are intertwined
(Kirby, Bartram, & Carr, 2003). A second group of questions designated Practice (13 questions) was designed to
assess practice habits focused on personal hygiene, safety
and health requirements, temperature control, food storage
and cross-contamination and working surface and instrument cleaning.
The participants answering the questionnaire remained
anonymous and were identiWed by job description, age and

Table 1
Summary of the focus of the questionnaire contents
Questions Knowledge
Visual, olfactory or taste checks identify bacteria contaminated food?
Food borne illness agents transmission
Origin of Staphylococcus aureus food contamination
Food borne illness most frequent symptoms
Identify high-risk food groups
Food groups related with Botulism
Identify sterile food
Nitrate contaminated wateris it proper if boiled?
Insect control and food hazard
Food borne illness and food production animals
Questions Practice
DiVerent situations that imply hand washing before food handling
DiVerent steps to correct hand wash
Health conditions that are not acceptable in food handling
Refrigerator temperatures and bacteria development
Temperature ranges and food poisoning agents development
Freezing temperatures
Storing temperatures for chopped meat
Refrigerator raw food and cooked food packing
Refrigerator raw food and cooked food storage requirements
Cross contamination and change of working instruments
Working surfaces and instruments washing products
Working surfaces and instruments washing requirements
Potable water use/Water supply
Freeze food and date of validity

number of years of formal education. Each participant was


informed of the purpose of the survey with the understanding that conWdentiality would be assured.
2.2. Questionnaire delivery
2.2.1. Food handlers (FH)
The questionnaire was delivered in person in 99 small
independent food businesses, during a routine inspection of
the Veterinary OYcial Services between January and April
of 2005, in two diVerent regions of the north of Portugal,
Porto and Viana do Castelo. In each small food business
the questionnaire was delivered to the Wrst handler contacted who accepted to participate. The answers were collected in person one week later.
2.2.2. Undergraduate students (S1 and S34)
The same questionnaire was distributed among two
groups of undergraduate university students, 89 from the
1st and 63 from the 3rd and 4th years of four courses of
the University of Porto (Table 2). The selected University
courses were Medicine, Veterinary Medicine, Aquatic Environment Sciences and Agriculture Engineering. The aim of
the student participation in this study was to evaluate their
knowledge in food hygiene and safety when they arrive to
the university (1st year students) and what knowledge was
acquired during their courses, without speciWc training in
the areas of the questionnaire. All the students have undergone basic education in Microbiology during their courses.
Medicine and Vet students have speciWc training in Public

E. Gomes-Neves et al. / Food Control 18 (2007) 707712


Table 2
Origin and number of participants that responded to the questionnaires
Origin

Number

Small food businesses


Butcher shops
Restaurants
Deboning rooms and small industry of meat products
Canteens
Cafs
Bakeries and pastry shops
Fishmongers

Food handlers
27
22
13
9
4
2
2

Total

79

Undergraduate students

1st year

3rd and 4th years

Medicine (Med)
Veterinary Medicine (Vet M)
Aquatic Environment Sciences
Agriculture Engineering

37
22
22
8

19a
33
3
8

Total

89

63

The Med students belonged to the Wnal year (3rd year) of the basic sciences cycle. Vet M students were tested in the year before the Wnal year
when they are tutored on Public Health and Sanitary Inspection practice.
a

Health. The questionnaire was delivered during a class of


each course and all the present students were invited to
return the fulWlled questionnaire at the end of the class.
The details of the origin and number of participants in
the diVerent groups tested are summarised in Table 2.

709

Table 3
Percentage of correct answers to the Knowledge and Practice questions within each group studied
Participant group

Question group
Knowledge

Practice

FH
S1
S34

55.0 18a
66.0 13
77.0 15

69.0 17
63.0 14
68.0 13

p-value (one-way ANOVA)

60.0001

0.041

Mean 1SD.

lowed by 1st year students (S1) with 66.0% of correct


answers and the 3rd4th year students (S34) with 77.0%
(Table 3).
In the Practice group of questions, FH had the highest
proportion of correct answers (69.0%) and the students
presented a positive evolution from 63.0% (S1) to 68.0%
(S34). The diVerence between the proportions of correct
answers to the questions Knowledge and Practice are
statistically signiWcant between the FH and the S34 groups
(Table 3).
3.2. Qualitative results
It was considered important to detect Wner diVerences
between answers to questions that tested the quality of the
information sought (Tables 4A and 4B).

2.3. Statistical analysis


The analysis of the questionnaires was performed using
the computer software SPSS (SPSS Inc., Chicago, IL; version 13.0). The signiWcance of the statistical diVerences of
the proportion of correct and incorrect answers in each
group of participants was identiWed using the chi-Square
test for signiWcance. DiVerences in the mean of participants
within each group studied were done using one-way
ANOVA. In all tests, the statistical signiWcance was twosided and considered signiWcant at p < 0.05. Mid-p 95% conWdence intervals (95% CI) of the proportion of correct
answers were computed using EpiInfo version 6.04d (http://
www.cdc.gov/epiinfo/Epi6/ei6.htm).

3.2.1. Questions Knowledge (Table 4A)


3.2.1.1. Food poisoning and food born illness. Fifty-six (55.7)
percent of FH believed that one could tell if food was contaminated with food poisoning bacteria by visual, olfactory
or taste checks, but only 5.6% of S1 and 3.2% of S34
thought the same. The majority of the FH (72.2%) and of
the students (87.6% S1 and 95.2% S34) were aware that
insects, other food handlers and raw food were sources of
bacteria, but 86.1% of the FH, 71.9% of the S1 and 42.9% of
the S34 did not identiWed food handlers as a source of
food contamination with Staphylococcus aureus. A signiWcant majority within the three groups knew that diarrhoea
is the symptom most associated with food born illness
(89.9% FH, 96.6% S1 and 96.8% S34).

3. Results

3.1.1. Participants response


Answers were obtained from 79 out of 99 food businesses contacted. All the 152 students contacted returned
their answers.

3.2.1.2. High-risk food groups. Fifty-eight (58.2) percent of


the FH, 67.4% of the S1 and 73.0% of the S34 recognised
chopped meat as a potential source of food poisoning, however few (32.9% FH, 19.1% S1 and 52.4% S34) established
a connection between canned food and Botulism. Sixty-Wve
(64.6) percent of the FH, 60.7% of the S1 and 58.7% of the
S34 thought pasteurised milk was sterile.

3.1.2. Comparative analysis of response to Knowledge


and Practice questions (Table 3)
Food handlers (FH) had the lowest proportion of
correct answers in the group Knowledge (55.0%), fol-

3.2.1.3. Water treatment. Sixty-Wve (64.6) percent of FH,


68.5% of the S1 and 41.3% of the S34 thought that boiling
is suYcient to make nitrate contaminated water adequate
to public consumption.

3.1. Quantitative results

710

E. Gomes-Neves et al. / Food Control 18 (2007) 707712

Table 4A
Percentages of correct answers and 95% conWdence intervals (CI) of the questions Knowledge
Questions Knowledge

% Correct answers (95% CI)


FH

S1

S34

Visual, olfactory or taste checks identify bacteria contaminated food?

44.3
(33.755.4)

94.4
(88.097.9)

96.8
(89.999.5)

Food borne illness agents transmission

72.2
(61.581.2)

87.6
(79.593.3)

95.2
(87.698.8)

13.9
(7.522.9)

28.1
(19.538.1)

57.1
(44.768.9)

Food borne illness most frequent symptoms

89.9
(81.795.2)

96.6
(91.199.1)

96.8
(89.999.5)

Identify high-risk food groups

58.2
(47.168.7)

67.4
(57.276.5)

73.0
(61.182.9)

Food groups related with Botulism

32.9
(23.243.8)

19.1
(11.928.3)

52.4
(40.164.5)

Identify sterile food

35.4
(25.546.4)

39.3
(29.649.7)

41.3
(29.653.7)

Nitrate contaminated water- is it proper if boiled?

35.4
(25.546.4)

31.5
(22.541.6)

58.7
(46.370.4)

Origin of Staphylococcus aureus food contamination

Table 4B
Percentages of correct answers and 95% conWdence intervals (CI) of the questions Practice
Questions Practice

% Correct answers (95% CI)


FH

S1

S34

Health conditions that are not acceptable in food handling

40.5
(30.151.6)

71.9
(61.980.5)

71.4
(59.481.5)

Refrigerator temperatures and bacteria development

79.7
(69.887.5)

80.9
(71.788.1)

87.3
(77.393.9)

Temperature ranges and food poisoning agents development

35.4
(25.546.4)

53.9
(43.564.1)

71.4
(59.481.5)

Freezing temperatures

59.5
(48.469.9)

16.9
(10.125.2)

22.2
(13.233.7)

Storing temperatures for chopped meat

53.2
(42.164.0)

31.5
(22.541.6)

28.6
(18.440.6)

Refrigerator raw food and cooked food packing

96.2
(90.099.0)

94.4
(88.097.9)

100.0
(95.4100.0)

Refrigerator raw food and cooked food storage requirements

36.7
(26.647.7)

33.7
(24.544.0)

41.3
(29.653.7)

Cross contamination and change of working instruments

73.4
(62.982.3)

62.9
(52.572.5)

76.2
(64.585.5)

Working surfaces and instruments washing products

93.7
(86.597.6)

85.4
(76.991.6)

98.4
(92.499.9)

Working surfaces and instruments washing requirements

75.9
(65.684.4)

65.2
(54.874.5)

57.1
(44.768.9)

Potable water use/water supply

83.5
(74.190.5)

77.5
(68.085.3)

81.0
(69.989.2)

3.2.2. Questions Practice (Table 4B)


3.2.2.1. Personal hygiene. To the question identify diVerent situations that imply hand washing before food handling, 16.6% of FH, 10.0% of S1 and 18.9% of S34 did not
answer. The answers between handling diVerent raw

food, after garbage handling and after using WC are


the most frequent to FH and only they refer after touching
the body. To the question diVerent steps to correct hand
wash, 16.5% of FH, 11.7% of S1 and 3.4% of S34 did not
answer. The use of nail brush was only referred by a small

E. Gomes-Neves et al. / Food Control 18 (2007) 707712

proportion of FH (3.8%). The Wnal step in hand-washing is


drying but the use of disposable paper towels for this purpose was referred by only 15.2% of the FH, 1.1% (n D 1) of
S1 and 1.6% (n D 1) of S34.
3.2.2.2. Safety and health requirements. Many FH did not
seem aware of basic safety and health requirements to work
with food. Only 40.5% of FH identiWed skin disease, gastrointestinal disturbances, and eye/ear and throat disease, as
conditions that are not acceptable in food handling. Seventy-two (71.9) percent of S1 and 71.4% of S34 identiWed
correctly these conditions. Only one FH and one S1 were
aware of the need of skin injury protection in food handling.
3.2.2.3. Temperature control. Eighty (79.7) percent of the
FH, 80.9% of S1 and 87.3% of S34 knew that refrigerator
temperatures does not kill food poisoning bacteria. From
three ranges of temperatures presented, 04 C/565 C/70
80 C, only 35.4% of the FH identiWed the range 565 C as
high-risk food storing temperature. Fifty-four (53.9) percent
of the S1 and 71.4% of the S34 answered correctly. Sixty
(59.5) percent of FH knew the correct freezing temperature,
but only 16.9% of the S1 and 22.2% of the S34 answered
correctly. Fifty-three percent (53.2) of the FH knew the correct store temperature for chopped meat, but only 31.5% of
the S1 and 28.6% of the S34 answered correctly.
3.2.2.4. Food storage and cross-contamination. Ninety-six
(96.2) percent of the FH, 94.4% of the S1 and 100% of the
S34 recognise the need to pack and separate cooked from
raw food, before refrigerator storage. Only 36.7% of the
FH, 33.7% of S1 and 41.3% of the S34 knew how to store
cooked and raw food correctly in the diVerent shelves of a
refrigerator. Seventy-three (73.4) percent of the FH, 62.9%
of the S1 and 76.2% of the S34 recognise the need of washing or changing knives when manipulating raw food from
diVerent origins, exempliWed as meat from diVerent animals.
3.2.2.5. Instruments and working surface cleaning. Eightyfour (83.5) percent of FH, 77.5% of S1 and 81.0% of the S34
knew that non-potable water cannot be used for the cleaning of working surfaces and instruments. Ninety-four (93.7)
percent of the FH, 85.4% of the S1 and 98.4% of the S34
identiWed disinfectants as the best process of killing bacteria.
However, 24.1% of the FH, 34.8% of S1 and 42.9% of S34
did not know that after the use of disinfectant on instruments and surfaces both must be cleaned with potable water.
4. Discussion
The present results were reached from self-reported
behaviour and practice. In spite of this option or perhaps as
a result of it, the questionnaire designed for the present
study permitted to detect quantitative diVerences in theoretical knowledge and practice between the participants

711

of the three relevant groups analysed. The satisfactory participation and response of all groups permitted to highlight
the existence of diVerences between students and food handlers in general knowledge. The proportion of correct
answers in the students group is statistically signiWcantly
higher than the food handlers in the Knowledge group of
questions. The results also indicate that the correct score
of students increased with progression in the courses. This is
interesting and somewhat reassuring. Nevertheless further
Wner analysis of the content of the questions themselves
(qualitative results) does not lead to the same sense of reassurance. The food handlers tested have a poor knowledge of
microbiological hazards. Although they may be aware of
personal hygiene there are other critical aspects of the
hygiene of food handling that seemed to escape them, such
as cleaning the instruments and the work-surfaces. Foods,
especially raw materials that are stored in refrigerators, frequently contain pathogenic organisms, including Listeria
monocytogenes (Azevedo et al., 2005; Cox et al., 1989; Mena
et al., 2004; Sergelidis et al., 1997). In addition, they did not
seem to value the role of temperature in cooking and low
temperature storage for the control of microbiologic hazards. Since temperature treatment is frequently the critical
control point of a production process, the issue of poor temperature understanding could be a major hindrance to eVective HACCP implementation (Walker et al., 2003).
Food handlers have better results in the group of questions Practice and, in general, students in the S34 group
have better results than S1 in both groups of questions,
Knowledge and Practice.
The S1 and S34 answers to the Practice questions
show that less than 30.0% knew the correct freezing temperature and chopped meat store temperature, although more
than 90.0% of the two groups were aware of the need of
packing and separating raw food in the refrigerator. Participants in S34 have better results than S1 in both groups of
questions but they lacked knowledge related to temperature control and personal hygiene. More than 50.0% of S1
and S34 were confused between personal hygiene and
instruments/working surfaces hygiene and were not aware
of the need of the use of protection clothes to handle food.
Only few S34 referred the use of disinfectants in hand
washing. Desmarchelier, Higgs, Mills, Sullivan, and Vanderlinde (1999) recommends that hand-washing alone has
no eVect on S. aureus counts on hands and that the reduction of bacteria in hands depends on the mechanical action,
the duration and the type of soap and the sanitizers used.
The study demonstrates that less than 60.0% of the FH
knew the correct answers to the Knowledge questions
and although the proportion of correct answers of FH to
Practice questions was higher than the S1 and S34 questions they lack knowledge of considerable signiWcance in
Public Health protection. A possible explanation for these
results may relate to the low educational level of the FH,
the average formal education years of FH was 7 years (in
Portugal the mandatory formal education is 9 years) in a
group with a mean age of 42 years.

712

E. Gomes-Neves et al. / Food Control 18 (2007) 707712

The signiWcance of the present results is limited in part by


the sample size available in the study. It is possible to conclude however that there is a need for eVective professional
training and evaluation in Hygiene and Food Safety of FH
in order to prevent mistakes and failure of the HACCP
application, veriWcation and validation (Blaha, 1999; Fairman & Yapp, 2004; Taylor, 2001; Taylor & Kane, 2005;
Sperber, 2005).
The main problem identiWed with food handlers relate to
the fact that they receive no speciWc training and need no
qualiWcation certiWcate to work with food. In addition,
their health is not periodically evaluated by an independent
health authority (Santos, 2004). Food hygiene training is a
legal requirement within food industry and should be only
one part of an eVective food safety management strategy.
Attitudes, an important factor besides knowledge and
enforcement, ensure a downward trend of food borne illnesses. The link of positive behaviour, attitudes and continued education of food handlers towards the sustainability
of safe food handling practices has been reported (Howes,
McEwen, GriYths, & Harris, 1996; Seaman & Eves, in
press). As Seaman and Eves (in press) pointed out training
will only lead to an improvement in food safety if the
knowledge imparted leads to desired changes in behaviour
in the workplace.
The present results indicate also that there is a need to
improve student knowledge and training in courses that
prepare professionals with responsibility in food safety and
hygiene related Public Health measures. Such professionals,
particularly those in veterinary and human medicine, may
in the future be encouraged to contribute to the work in
training and professional evaluation of food handlers.
Acknowledgements
We gratefully acknowledge Prof. Maria de Sousa for the
comments and help in the preparation of the manuscript.
Dr. C.S. Cardoso is the recipient of a post-doc Fellowship
(SFRH/BPD/18133/2004) and E. Ramos, is a recipient of a
Ph.D. Fellowship from the National Foundation for Science
and Technology (FCT), Portugal (SFRH/BD/11114/2002).
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