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Systematic Literature Review of Oral Hygiene Practices for Intensive Care Patients Receiving Mechanical Ventilation
Background: Oropharyngeal colonization with pathogenic organisms contributes to the development of ventilator-associated pneumonia in intensive care units. Although considered basic and potentially nonessential nursing care, oral hygiene has been proposed as a key intervention for reducing ventilator-associated pneumonia. Nevertheless, evidence from randomized controlled trials that could inform best practice is limited.
Objective :To appraise the peer-reviewed literature to determine the best available evidence for providing oral care to intensive care patients receiving mechanical ventilation and to document a research agenda for this important activity in optimizing patients’ outcomes.
Methods: Articles published from 1985 to 2006 in English and indexed in the CINAHL, MEDLINE, Joanna Briggs Institute, Cochrane Library, EMBASE, and DARE databases were searched by using the key terms oral hygiene, oral hygiene practices, oral care, mouth care, mouth hygiene, intubated, mechanically ventilated, intensive care, and critical care. Reference lists of retrieved journal articles were searched for publications missed during the primary search. Finally, the Google search engine was used to do a comprehensive search of the World Wide Web to ensure completeness of the search. The search strategy was verified by a health librarian.
Results: The search yielded 55 articles: 11 prospective controlled trials, 20 observational studies, and 24 descriptive reports. Methodological issues and the heterogeneity of samples precluded meta-analysis.
Conclusions: Despite the importance of providing oral hygiene to intensive care patients receiving mechanical ventilation, high-level evidence from rigorous randomized controlled trials or high-quality systematic reviews that could inform clinical practice is scarce.
Objectives
The goals of this review were to evaluate peer-reviewed publications to determine the best available evidence for providing oral care to ICU patients receiving mechanical ventilation and to document a research agenda to improve patients’ outcomes.
Method
Approaches used to review the scientific literature range from a purposeful, systematic evaluation of rigorous studies to subjective overviews of descriptive articles.18(p53) Well-conducted systematic reviews can result in 3 major outcomes. First, increased power can be obtained by combining the effects of a number of smaller studies on the same topic when homogeneity allows meta-analysis. Second, systematic reviews to some extent enable the comparison of effects of studies with different designs.18(p53) Finally, a prospective and systematic review allows synthesis of the data and should assist in providing quality current evidence to guide clinical practice.19
Development of evidence-based guidelines is limited by the small number of randomized controlled trials and the variability of interventions studied.
Formulation of the review question requires extensive background research to enable an informed outcome. The question must accurately reflect the extent of the issue to be reviewed. Therefore, a comprehensive approach, including a wide-ranging search of the literature together with consultation with experts, including nurses, in the field of dental health and critical care resulted in the following review question: With respect to intensive care patients receiving mechanical ventilation, what is the best method for providing oral hygiene that will result in a reduction of colonization of dental plaque with respiratory pathogens?
Both experimental and nonexperimental study designs were included in the review. Because of the scarceness of review material on ICU patients receiving mechanical ventilation, articles that focused on specific oral care tools or solutions for the seriously ill also were included in the review.
This review considered studies that included patients in ICUs who were intubated and receiving mechanical ventilation. Also included were studies that proposed a link between oral hygiene and systemic diseases. The interventions of interest were those designed to affect dental plaque specifically and oral hygiene in general. The types of outcome measures considered were general and specific indicators of oral health:
Microbial counts
Plaque indices
Oral assessment scores
Validation of tools used in the provision of oral care
Articles were excluded if the study sample consisted of healthy participants or the study was done in a setting other than a critical care environment (eg, oncology).
Articles published from 1985 to 2006 in English and indexed in the following databases were searched: CINAHL, MEDLINE, Joanna Briggs Institute, Cochrane Library, EMBASE, DARE, and the World Wide Web search engine, Google. Key search terms used in the review were oral hygiene, oral hygiene practices, oral care, mouth care, mouth hygiene, intubated, mechanically ventilated, intensive care, and critical care. This search strategy was verified by a health librarian.
Full copies of articles considered to meet the inclusion criteria (on the basis of their title, abstract, and subject descriptors) were obtained for data synthesis. Articles identified through reference lists and bibliographic searches were considered for data collection depending on the titles. Articles were independently selected according to prespecified inclusion criteria by 3 reviewers, each with a minimum of a master’s degree and certification in critical care. Discrepancies in the reviewers’ selections were resolved at meetings between the reviewers before the selected articles were included.
Until recently, one system used to grade levels of evidence was based on work by the US Agency for Healthcare Research and Quality. Because of the increasing awareness of the limitations of that system, however, the classification structure was revised by the Scottish Intercollegiate Guidelines Network. Therefore, the rating method used for categorization of levels of evidence found in this review was based on the revised system (Tables 1⇓ and 2⇓).20
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Table 1
Guide to the levels of evidence
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Table 2
Grades of recommendations
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Results
Although we found a number of references for the provision of oral hygiene in the management of oncology and other medical patients, most articles related to critical care were review articles. For the prospective randomized control trials we found, meta-analysis could not be used to synthesize the results because of variations in the methods of these studies. For example, in some studies, the populations assessed differed, and for those studies in which the populations were the same, the interventions were often dissimilar. These limitations were recognized in a recent meta-analysis on the use of chlorhexidine and the incidence of nosocomial pneumonia.21
Using the classification system developed by the Scottish Intercollegiate Guidelines Network, we reviewed 11 prospective controlled trials,3,4,13,14,22–28 20 observational studies,15,29–47 and 24 descriptive studies.21,48–70 The 11 articles on prospective controlled trials are presented in Table 3⇓. Summary tables of the observational studies (Table 4) ⇓ and descriptive papers (Table 5) ⇓are available only on the American Journal of Critical Care Web site (http://www.ajcconline.org) in the full-text view of this article.
A review of food safety and food hygiene training studies
in the commercial sector
M.B. Egan
a
, M.M. Raats
a,¤
, S.M. Grubb
a
, A. Eves
b
,
M.L. Lumbers
b
, M.S. Dean
a
, M.R. Adams
c
a
Food, Consumer Behaviour and Health Research Centre, University of Surrey, Guildford, Surrey GU2 7XH, UK
b
School of Management, University of Surrey, Guildford, Surrey GU2 7XH, UK
c
School of Biomedical and Molecular Sciences, University of Surrey, Guildford, Surrey GU2 7XH, UK
Received 2 May 2005; received in revised form 2 August 2006; accepted 5 August 2006
Abstract
This review summarises the methods and results of studies conducted worldwide on the eVectiveness of food safety and food hygiene
training in the commercial sector of the food industry. In particular it focuses on those studies that have tried to evaluate the eVectiveness
of such training. Forty-six studies of food hygiene training are included which used some outcome measure to assess the eVectiveness of
training. The short-term nature and variety of measures used limited the majority of studies. The need for the development of evaluation
criteria of eVectiveness of food hygiene training is discussed.
© 2006 Elsevier Ltd. All rights reserved.
Keywords: Food safety; Training; Evaluation; HACCP
1. Introduction
Food safety remains a critical issue with outbreaks of
foodborne illness resulting in substantial costs to individuals, the food industry and the economy (Kaferstein,
Motarjemi, & Bettcher, 1997). Within England and Wales
the number of food poisoning notiWcations rose steadily
from approximately 15,000 cases in the early 1980s to a
peak of over 60,000 cases in 1996 (Wheeler et al., 1999).
This may be partly attributed to improved surveillance
(GriYth, Mullan, & Price, 1995; Kaferstein & Abdussalam,
1999) but may equally reXect increased global trade and
travel, changes in modern food production, the impact of
modern lifestyles, changes in food consumption and the
emergence of new pathogens (Collins, 1997; Tauxe, 1997).
Recent years have seen a reversal in this trend but food poisoning remains a high priority for the public and government (Parliamentary OYce of Science & Technology, 2003).
Mishandling of food plays a signiWcant role in the occurrence of foodborne illness. Improper food handling may be
implicated in 97% of all foodborne illness associated with
catering outlets (Howes, McEwan, GriYths, & Harris,
1996). In two studies of general outbreaks of infectious
intestinal disease (IID) in England and Wales the primary
causes were related to poor food-handling practices
(Djuretic, Ryan, & Wall, 1996; Evans et al., 1998). Improper
practices responsible for microbial foodborne illnesses have
been well documented (Bryan, 1988) and typically involve
cross-contamination of raw and cooked foodstuVs, inadequate cooking and storage at inappropriate temperatures.
Food handlers may also be asymptomatic carriers of food
poisoning organisms (Cruickshank, 1990).
Food handler training is seen as one strategy whereby
food safety can be increased, oVering long-term beneWts to
the food industry (Smith, 1994). A postal survey of manufacturing, retail and catering food businesses by Mortlock,
Peters, and GriYth (2000) revealed that less than 10% had
failed to provide some food hygiene training for staV. Less
encouraging was the fact that less than 20% of managers
*
Corresponding author. Fax: +44 1483 689553.
E-mail address: [email protected] (M.M. Raats).M.B. Egan et al. / Food Control 18 (2007) 1180–1190 1181
were trained to supervisory level. This lack of training for
food managers may restrict their ability to assess risks in
their business and to assign appropriate hygiene training
for their staV.
The aim of this review is to analyse studies of food
hygiene training; in particular studies that have attempted
to evaluate the eVectiveness of training. The studies will be
evaluated principally on the outcome measures used in each
study and their limitations for evaluating training eVectiveness discussed.
2. Background
2.1. Food hygiene legislation in the United Kingdom
New food hygiene legislation has applied throughout the
UK from 1st January 2006. Regulation 852/2004 (EC) of
the European Parliament and Council on the Hygiene of
Food StuVs now applies to all food businesses. The Food
Hygiene (England) Regulations (2006); also come into
force and separate but similar legislation will apply in Scotland, Wales and Northern Ireland. Article 5 states that:
Food businesses operators shall put into place, implement
and maintain a permanent procedure based on the principles of hazard analysis critical control points (HACCP).
With regard to training Chapter XII states that food business operators are to ensure that: “food handlers are supervised and instructed and/or trained in food hygiene matters
commensurate with their work activity; that those responsible for the development and maintenance of the procedure
referred to in Article 5 (1) of the Regulation or for the operation of the relevant guides have received adequate training
in the application of HACCP principles, and compliance
with any requirement of national law concerning training
programmes for persons working in certain food sectors”.
Managers responsible for maintaining a food safety management system will require adequate training to enable
them to carry out the statutory requirement. Accordingly a
new set of food safety qualiWcations will be launched in
2006 to help train managers and other staV in the essentials
of food safety management systems. Furthermore Article 7
of Regulation (EC) 852/2004 on the hygiene of foodstuVs
provides for the development of national Guides to Good
Hygiene Practice and the Application of HACCP principles
(known as Good Practice Guides). These guides are being
developed by individual food sectors, in consultation with
interested parties. Butchers’ shop licensing has been withdrawn across the UK from the end of 2005. Since 1st
January 2006, all retail butchers are subject to the new EC
hygiene regulations that apply to all other retail and catering businesses.
2.2. Hazard analysis and critical control points (HACCP)
HACCP is an internationally recognised food safety
assurance system that concentrates prevention strategies on
known hazards; it focuses on process control, and the steps
within that, rather than structure and layout of premises
(Kirby, 1994; Worsfold & GriYth, 1995). HACCP establishes procedures whereby these hazards can be reduced or
eliminated and requires documentation and veriWcation of
these control procedures (Codex, 1997). Whilst HACCP
has been widely adopted by the food manufacturing industry and the larger companies in the hospitality and catering
sector, there have been concerns about implementation by
smaller businesses. Barriers to the implementation of
HACCP in small businesses have been identiWed which
include lack of expertise, absence of legal requirements,
Wnancial constraints and attitudes (Ehiri, Morris, &
McEwen, 1995; Taylor, 2001; Walker, Pritchard, & Forsythe, 2003; WHO, 1999).
2.3. Training and evaluation of training eVectiveness
The Manpower Services Commission (1981) deWned
training as ‘a planned process to modify attitude or skill
behaviour through learning experience to achieve eVective
performance in an activity or range of activities’. Evaluation is integral to the cycle of training, providing feedback
on the eVectiveness of the methods used, checking the
achievement of the objectives set by both the trainer and
trainee and in assessing whether the needs originally identiWed have been met (Bramley, 1996). Criteria that may
be used for evaluating the eVectiveness of a training
programme include reaction to training, knowledge acquisition, changes in job-related behaviour and performance
and improvements in organisational-level results (Kirkpatrick, 1967). Research on training eVectiveness has focused
primarily on factors that are directly related to training
content, design and implementation (Tannenbaum & Yuki,
1992). However other factors outside the training environment may inXuence the eVectiveness of any programme
(Tracey, Tannenbaum, & Kavanagh, 1995).
Despite general acceptance that training eVorts must be
systematically evaluated, few studies have tried to identify
the beneWts food hygiene training brings to the industry.
This is illustrated by a survey of the US lodging industry
where fewer than 10% of the hospitality companies conducted formal evaluations of their training programmes
(Conrade, Woods, & Ninemeir, 1994).
2.4. Transfer of knowledge into practice
To be eVective food hygiene training needs to target
changing those behaviours most likely to result in foodborne illness. Most food hygiene training courses rely
heavily on the provision of information. There is an
implied assumption that such training leads to changes in
behaviour, based on the Knowledge, Attitudes and Practices (KAP) model. This model has been criticised for its
limitations (Ehiri, Morris, & McEwen, 1997b; GriYth,
2000). It is accepted that knowledge alone is insuYcient to
trigger preventive practices and that some mechanism is
needed to motivate action and generate positive attitudes1182 M.B. Egan et al. / Food Control 18 (2007) 1180–1190
(Tones & Tilford, 1994). In an evaluation of food hygiene
education Rennie (1994) concluded that knowledge alone
does not result in changes in food handling practices. Various studies have shown that the eYcacy of training in
terms of changing behaviour and attitudes to food safety is
questionable (Mortlock, Peters, & GriYth, 1999).
3. Overview of studies
3.1. Mapping exercise
The aim of the review was to identify criteria used by
previous studies to evaluate the eVectiveness of food safety
and hygiene training. Reports referring to training in the
context of food safety training or food hygiene training in
the commercial sector were considered relevant. Only those
studies written in the English language were included.
DiVerent sources of published and unpublished
research literature were searched to locate relevant papers.
Searches were conducted on commercially available electronic databases including PsycINFO, Medline, ERIC,
CINAHL, Social Science Citation Index, Science Direct,
etc. These searches covered the full range of publication
years available in each database at the time of searching.
For all the databases the following search strategy was
used: [{Food safety} or {Food hygiene}] and [{train*} or
{teach*} or {course*} or {educat*}]. All citations identiWed by these searches were downloaded and when possible
captured and compiled as a Reference Manager database.
Further studies were identiWed through hand searching
journals and references to publications in retrieved
papers.
3.2. General characteristics of relevant studies included in
review
Studies were included in the review if they met two
criteria:
• The study used some outcome measures to assess the
eVectiveness of food hygiene training.
• The study was based in a commercial setting.
A total of forty-six studies of food hygiene training were
retained and included in this review. Full details of the
included studies are given in Tables 1–5. The earliest study
in this review was undertaken in 1969 and the most recent
in 2003. Fifteen studies (32%) were from the UK, twenty
(43%) from the USA, two (4%) each from Canada, Italy
and Malaysia and one (2%) each from Australia, Bahrain,
New Zealand, Nigeria and Saudi Arabia.
Thirty studies (65%) involved food handlers, 11 (24%)
focused on food managers and one study involved both
(Burch & Sawyer, 1991). The level of training was not speciWed in the majority of the studies, the UK studies generally
used standard basic food hygiene courses. Twenty-two
studies (48%) included a training intervention (Tables 1 and
3–5). Twenty-nine studies (63%) measured knowledge
(Tables 1 and 3–5). Most studies addressed attitude, behaviour and work practices concerning food safety and food
hygiene in some form, however the methods varied greatly.
Only four of the studies (Ehiri et al., 1997b; Laverack,
1989; Reicks, Bosch, Herman, & Krinke, 1994; Tracey &
Cardenas, 1996) make reference to a social cognition theoretical model as a basis for their study.
3.3. Training interventions
Of the 22 studies involving a training intervention, 15
were from North America, Wve from the UK and one from
Bahrain. North American training included courses for
food handlers and food service managers. It also encompassed diVerent types of training such as home study, workshops and more formal courses. A number of those studies
also compared the results of using diVerent methods of
delivering training. Seventeen of the 22 studies used a
knowledge measure to evaluate the eVectiveness of the
intervention, most commonly a pre- and post-test.
3.4. Study design and theoretical models
Few of the reports speciWed their study design. For clarity we have attributed each to one of the Wve evaluation
designs detailed by Ovretveit (1998). A brief description of
each of the designs is given here:
(i) Descriptive: Evaluator observes and selects features of
the intervention, which he or she describes. Twentysix of the 46 studies reviewed fell into this category
(Table 1).
(ii) Audit: Evaluator compares what the service does with
what it should or was intended to do, according to
written standards or procedures. Three (Audit Commission, 1990; Holt & Henson, 2000; Morrison,
CaYn, & Wallace, 1998) of the 46 reviewed fell into
this category (Table 2).
(iii) Before–after: Evaluator compares a group of participants before and after an intervention. Seven of the
46 studies reviewed fell into this category (Table 3).
(iv) Comparative-experimentalist: Evaluator compares the
outcomes of two groups undergoing diVerent interventions. Five (Costello, Gaddis, Tamplin, & Morris,
1997; Howes et al., 1996; Kirby & Gardiner, 1997;
Nabali, Bryan, Ibrahim, & Atrash, 1986; Rinke,
Brown, & McKinley, 1975) of the 46 studies reviewed
fell into this category (Table 4).
(v) Randomised controlled experimental: Evaluator compares one group that receives an intervention with
another group that does not, but that is in all other
possible respects the same. Five (Ehiri et al., 1997b;
Reicks et al., 1994; SoneV, McGeachy, Davison,
McCargar, & Therien, 1994; Waddell & Rinke, 1985;
Wright & Feun, 1986) studies fell into this category
(Table 5).M.B. Egan et al. / Food Control 18 (2007) 1180–1190 1183
Table 1
Food hygiene training evaluation studies using a descriptive design
Study and year Country Participants (number) Training intervention Knowledge Attitude, behaviour
and working practices
Al-Dagal (2003) Saudi Arabia Sanitarians (n D 82) None Questionnaire Self-reported practices
Burch and Sawyer (1991) USA Managers (n D 13) and
employees (n D 27) of 13
convenience stores
None Sanitation quiz
(8 questions)
Researcher survey
Angellilo et al. (2000) Italy Food handlers (n D 411) None Face-to-face
interviews
using structured
questionnaire
Self-reported hygiene
practices
Angellilo et al. (2001) Italy Food handlers (n D 290) in
hospitals (n D 36)
None Questionnaire Questionnaire
Clayton et al. (2002) UK Food handlers (n D 137)
from 52 food SMEs
None Not assessed Questionnaire,
self-reported practices
Cook and Casey (1979) USA Food service managers NIFI course, over a
5-week period
Written examination Comparison of post-course
sanitation inspection scores
Hart et al. (1996) USA Beef demonstrators (n D 93) National Restaurant
Association
SERVSAVE
programme
Pre and post-training
questionnaires
Pre- and post-training
questionnaires
Hennum et al. (1983) USA Restaurants (n D 16) None Interview Interview and observation
Hine et al. (2003) USA Restaurant managers
(n D 500)
None Not assessed Survey
Johnston et al. (1992) New Zealand Managers of food
service outlets (n D 300)
None Not assessed Questionnaire
Little et al. (2002) UK Take-away restaurants
and sandwich bars
None Not assessed Microbiological study
Manning and Snider (1993) USA Food handlers (n D 64) None Questionnaire Questionnaire,
observation checklist
McElroy and Cutter (2004) USA Participants (n D 1,448)
in Statewide Food safety
CertiWcation program (SFSCP)
Food safety
workshop
(16hrs)
Not assessed Self-reported changes in
food safety behaviours
assessed by questionnaire
Oteri and Ekanem (1989) Nigeria Hospital food handlers
(n D 161)
None Not assessed Structured interview,
observation of some
practices
Powell et al. (1997) UK StaV in 30 food premises CIEH basic certiWcate
in food hygiene
Basic food hygiene
certiWcate examination
Frequency inspection
ratings
Sumbingco et al. (1969) USA Food service employees
(n D 11) of university
residence halls
Programmed texts for
two food service tasks
Oral test Quality of work assessed,
time for doing tasks
measured
Tebbutt (1986) UK Premises selling sliced
cooked meats (n D 160)
None Not assessed Microbiological sampling,
questionnaire on cleaning
and disinfection
Tebbutt (1991) UK StaV in 89 restaurants None Multiple choice
questions
Premises assessed
Tebbutt (1992) UK StaV in 75 premises producing
high-risk foods
None Multiple-choice
questions
Numerical scores for
premises based on 20
variables
Toh and Birchenough (2000) Malaysia Food hawkers (n D 100)
from 15 sites
None Structured on-site
interview
Thirteen attitude items
using a Likert scale
Wade (1998) UK Hospitality managers (n D 27) None Not assessed Survey of hygiene
management
Walker et al. (2003) UK Food handlers (n D 444),
from 104 small food businesses
None Multiple-choice
questions
Not assessed
Worsfold (1993) UK Members of the Women’s
Royal Voluntary
Service (n D 93)
Royal Society of
Health Basic Food
hygiene course
Pre-course
questionnaire
End-of-course evaluation
Worsfold and GriYth (2003) UK Small or medium sized
businesses handling high-risk
foods (n D 66)
None Not assessed Semi-structured interview
with manager; observation
of hygiene practices
Wyatt (1979) USA Managers or owners of food
markets (n D 219)
None Questionnaire Questionnaire on attitudes,
opinions, experiences and
practices
Zain and Naing (2002) Malaysia Food handlers (n D 430) None Questionnaire Questionnaire evaluating
attitude and practice1184 M.B. Egan et al. / Food Control 18 (2007) 1180–1190
3.5. Outcome measures
One of the aims of the review was to identify criteria for
evaluating the eVectiveness of food safety and hygiene
training. Evaluation of training is complex given the number of variables that may inXuence the outcome, including
who is being trained, the level of training, motivation and
cultural dimensions. Unfortunately few of the studies were
Table 2
Food hygiene training evaluation studies using an audit design
Study and year Country Participants (number) Training
intervention
Knowledge Attitude, behaviour
and working practices
Audit Commission (1990) UK Food premises
(n D 5,000)
None Not assessed Survey of premises and
working practices
Holt and Henson (2000) UK Manufacturers of
ready to eat meat
products (n D 24)
None Not assessed Hygiene audit using
EFSIS protocol
Morrison et al. (1998) Australia Food service
operations (n D 19)
None Not assessed Survey checklist us for
practices observed and
standards measured
Table 3
Food hygiene training evaluation studies using a before-after design
Study and year Country Participants (number) Training intervention Knowledge Attitude, behaviour and working
practices
Cotterchio
et al. (1998)
USA 3 groups of trainee
restaurant managers
(n D 96)
Food manager training
and certiWcation programme
Not assessed Routine sanitary inspection scores
compared pre- and post-training
Kneller and
Bierma (1990)
USA Food service facilities
(n > 400)
None Not assessed Review of pre- and postcertiWcation inspection scores
Laverack (1989) UK Food handlers IEHO Basic Food Hygiene
Course
Pre- and post-training
tests
Questionnaire pre and posttraining
Medeiros
et al. (1996)
USA Food safety educators
(n D 45) and voluntary
cooks (n D 136)
Safe food handling for
occasional cooks training
programme
Pre- and post-course
test of 55 questions
Self-declared behaviour checklist
used at time of initial training
Palmer
et al. (1975)
USA Food service managers
in 31 takeout restaurants
Manager training
programme (2 £ 2 h sessions)
Not assessed Before and after survey of premises,
total demerit score awarded
Sparkman
et al. (1984)
USA Food service workers
(n D 23)
Food service training
manual, 3 h training session
Pre- and post-test with
21 multiple-choice
questions post-training
On-the job performance evaluation
with 30 observations
Tracey and
Cardenas (1996)
USA Dining services division
of two private colleges
(n D 76)
Two food-service safety
training programmes
Pre- and post-training
tests based on course
training materials
Pre-training motivation assessed
by survey, reactions to training
surveyed immediately
post-training
Table 4
Food hygiene training evaluation studies using a comparative-experimentalist design
Study and year Country Participants (number) Training intervention Knowledge Attitude, behaviour
and working practices
Costello
et al. (1997)
USA Employees of 6 quick
service restaurants (n D 43)
Two teaching methods—lecture
format or computer
interactive method
Questionnaire—25
multiple-choice
questions; pre- and
post-training tests
Not assessed
Howes
et al. (1996)
Canada Food handlers (n D 69) Home study food-handler
certiWcation course
Pre- and post-instruction
tests using 50
multiple-choice
questions
Pre-observation of 16 food
safety practices; postobservation of two hand
washing practices
Kirby and
Gardiner (1997)
UK StaV in 30 food premises CIEH basic certiWcate in
food hygiene
Not assessed Pre- and post-training
hygiene
audit for each premise
Nabali
et al. (1986)
Bahrain Food service managers
in 24 premises
Manager training programme
(2 £ 2.5 days sessions)
Pre- and post-course
test of 50 questions
Pre- and post-course
inspection surveys
of premises
Rinke
et al. (1975)
USA Food production
personnel in university
residence halls (n D 60)
Training program, presented
as live instruction or taped
instruction
Pre- and post-training
testing
Not assessedM.B. Egan et al. / Food Control 18 (2007) 1180–1190 1185
similar enough to allow any direct comparisons. Data were
collected using a variety of research methods. These
included self-completed questionnaires, face-to-face interviews, premises inspections, observation and microbiological sampling. We identiWed four outcome measures that
could be used to compare the studies: knowledge; attitudes,
behaviour and work practices; retraining and duration of
eVects. Our evaluation is based on these measures.
4. Results
4.1. Knowledge
Assessment of knowledge featured in 29 (63%) of the
studies reviewed here (Tables 1 and 3–5). Questionnaires
were used as the principal measure of knowledge. Generally
these were of multiple-choice format with the number of
questions varying from 8 (Tracey & Cardenas, 1996) to 55
(Medeiros et al., 1996), but some (e.g. Wright & Feun, 1986)
providing no detail. Few of the studies detailed the questions used, referring only to the general topics covered.
These included high-risk foods, foodborne pathogens,
cross-contamination, personal hygiene, temperature control and cleaning. A number of the studies (Costello et al.,
1997; Hart, Kendall, Smith, & Taylor, 1996; Laverack,
1989; Medeiros et al., 1996; Nabali et al., 1986; Reicks et al.,
1994; Taylor, 1996; Tracey & Cardenas, 1996; Wright &
Feun, 1986) involved interventions using pre- and posttraining tests of knowledge. Nine studies (Costello et al.,
1997; Hart et al., 1996; Howes et al., 1996; Medeiros et al.,
1996; Nabali et al., 1986; Reicks et al., 1994; Sparkman,
Briley, & Gillham, 1984; Tracey & Cardenas, 1996; Waddell
& Rinke, 1985) found statistically signiWcant improvements
in the test scores of the intervention groups, whilst a further
two (Laverack, 1989; Wright & Feun, 1986) measured some
improvement. Two studies (Ehiri et al., 1997b; Reicks et al.,
1994) found a signiWcant diVerence between the intervention and control group. Only one intervention (Powell,
Attwell, & Massey, 1997) measured no signiWcant diVerence
in post-training scores.
The results from those studies not involving any intervention also varied. These were frequently based on questionnaires and results ranged from good knowledge
through to poor knowledge in critical aspects of food
safety. Generally there was good awareness of common
food pathogens (Al-Dagal, 2003; Angellilo, Viggiani,
Greco, Rito, & the Collaborative group, 2001), but poor
knowledge of temperature control, especially regarding
reheating and cooling (Manning & Snider, 1993; Zain &
Naing, 2002).
In summary it is very diYcult to make any direct comparisons as the studies were all conducted in diVerent ways,
involving diVerent tests. Of the 21 studies where a training
intervention was included, four (Cotterchio, Gunn, CoYll,
Tormey, & Barry, 1998; Kirby & Gardiner, 1997; Palmer,
Hatlen, & Jackson, 1975; SoneV et al., 1994) did not use any
knowledge tests to evaluate the training.
4.2. Attitudes, behaviour and work practices
Very few of the studies reviewed included any detailed
investigation of attitude, a cognitive element that may inXuence food safety behaviour and practice. Again any direct
comparison of results is diYcult because of the disparity of
the measures used in the reported studies. The means of
evaluating attitudes, behaviour and work practices fall into
two broad categories, namely surveys or inspections of premises and structured questionnaires. Seventeen of the studies included a premises survey or observation of behaviour,
and Wve studies (Cook & Casey, 1979; Cotterchio et al.,
1998; Kneller & Bierma, 1990; Powell et al., 1997; Wright &
Feun, 1986) used routine inspection scores. In some
instances this was the sole measure of behaviour and
hygiene practices. The exact range of the surveys varied but
usually included inspection of physical facilities and assessments of cleaning procedures, personal hygiene and
Table 5
Food hygiene training evaluation studies using a randomised controlled experimental design
Study and year Country Participants (number) Training intervention Knowledge Attitude, behaviour and
working practices
Ehiri et al. (1997b) Scotland Intervention group (n D 188)
and comparison group (n D 204)
who receive no training
REHIS elementary food
hygiene course
Self-administered test
of 20 questions
Not assessed
Reicks et al. (1994) USA Leaders of home study
groups (n D 97)
Food safety instruction
(2 h lesson)
Thirteen multiple choice
questions, pre- and
post-instruction
Pre- and post-instruction
evaluation of attitudes to
food safety, using 5-point
Likert scale
SoneV et al. (1994) Canada StaV at 46 community
based adult care facilities
Training workshop plus
manual, manual only or
no intervention
Not assessed Pre- and post-training
assessment of staV practices
Waddell and
Rinke (1985)
USA Food service employees
(n D 230) at large military hospital
Computer assisted training
(CAI) and lecture method
of instruction (LMI)
Pre- and post-test
questionnaire,
33 questions
Questionnaire to assess
attitude to training using
Likert scale
Wright and
Feun (1986)
USA Food service managers (n D 54);
study group (n D 27) and control
group (n l D 27)
NIFI training programme Pre- and post-tests used Pre-inspection of premises;
two post-inspections soon
after course1186 M.B. Egan et al. / Food Control 18 (2007) 1180–1190
temperature control. Quite often premises were assigned an
inspection score, most usually when the study involve a preand post-training inspection.
Questionnaires or interviews were used to document
self-reported food hygiene practices and attitudes to food
hygiene and training. Attitudes were measured most commonly using a 5-point Likert scale. Less frequently studies
incorporated researcher observation of food safety practices on site. In one study (Howes et al., 1996) 16 practices
were observed prior to training but this was reduced to two
practices post-training because of inherent diYculties with
completing these observations. In three studies (Little, Barnes, & Mitchell, 2002; Tebbutt, 1986; Tebbutt, 1991) microbiological sampling was used as a measure of eVectiveness.
A number of interesting results do emerge. The majority
of food handlers and managers expressed a positive
attitude to food safety but this was not supported by selfreported practices (e.g. Angellilo, Viggiani, Rizzio, &
Bianco, 2000). Furthermore some studies have demonstrated the discrepancy between self-reported behaviour
and observed or actual behaviour (Clayton, GriYth, Price,
& Peters, 2002; Oteri & Ekanem, 1989).
In studies using inspections/surveys of premises four of
the Wve studies using routine inspection scores (Cook &
Casey, 1979; Cotterchio et al., 1998; Kneller & Bierma,
1990; Wright & Feun, 1986) found a signiWcant improvement in post-training inspection scores. In the Cook &
Casey study however the improved inspection score was
not signiWcantly higher than that of control establishments.
Other studies using inspections (e.g. Kirby & Gardiner,
1997) reported no signiWcant improvements. Furthermore
there seemed to be no correlation between knowledge test
scores and hygiene inspection scores (e.g. Cook & Casey,
1979; Powell et al., 1997).
In one UK study (Little et al., 2002) the presence of a
trained manager improved food safety procedures and in
one US study (Cotterchio et al., 1998) the mandatory attendance of managers resulted in improved inspection scores. A
poor correlation emerged between microbiological examinations and visual inspections (Tebbutt, 1986, 1991).
4.3. Retraining and duration of eVects
Retraining or refresher training featured in only four
studies (Holt & Henson, 2000; Tebbutt, 1991, 1992; Worsfold & GriYth, 2003). Three studies (Holt & Henson, 2000;
Tebbutt, 1992; Worsfold & GriYth, 2003) checked on the
frequency of refresher training whilst the fourth study
(Tebbutt, 1991) assessed the management attitude to
retraining as part of an interview. In one UK study (Tebbutt, 1992), 41% of the businesses involved oVered very limited or no retraining whilst a more recent UK study
(Worsfold & GriYth, 2003) reported very little refresher
training being carried out.
Thirteen studies included some measure of the impact of
training over time. The time period used for those studies
(Costello et al., 1997; Hart et al., 1996; Laverack, 1989;
Medeiros et al., 1996; SoneV et al., 1994; Sparkman et al.,
1984; Sumbingco, Middleton, & Konz, 1969; Worsfold,
1993; Wright & Feun, 1986) ranged from one week to six
months. When an inspection was the measure, the time
period increased up to Wve years (Cotterchio et al., 1998;
Kneller & Bierma, 1990; Wright & Feun, 1986). Two US
studies (Cotterchio et al., 1998; Kneller & Bierma, 1990)
reported that improvements in inspection scores were sustained for 18–24 months and only began to decline after
three years. However another study from the US reported a
reduction in post-training performance after only eight
weeks (Sparkman et al., 1984) whilst another found
reduced inspection scores after six months (Wright & Feun,
1986).
4.4. HACCP training studies
A search of the food safety literature identiWed only Wve
studies that involved some evaluation of HACCP training,
these included a HACCP training programme in the
Lithuanian dairy industry (Boccas et al., 2001), a survey of
HACCP implementation in Glasgow (Ehiri, Morris, &
McEwen, 1997a) and an evaluation of a short HACCP
course involving representatives from residential care
homes (Worsfold, 1998). A lack of food hygiene knowledge
by staV was identiWed as the greatest problem in a study of
the application of HACCP in a Xight catering establishment (Lambiri, Mavridou, & Papadakis, 1995). Training
was seen as critical in order to assess hazards and control
food safety in the long-term. In a study of cleaning standards and practices in 1502 food premises in the UK
(Sagoo, Little, GriYth, & Mitchell, 2003a), deWciencies were
associated with premises that did not have management
food hygiene training or hazard analysis. Education and
training is crucial in implementing any HACCP system.
This has been recognised previously by both the Codex
(1997) and NACMCF (1998) and is now more relevant in
the UK with the introduction of new hygiene legislation.
5. Discussion and conclusions
This review particularly focused on studies that
attempted to evaluate the eVectiveness of food safety and
hygiene training. Other reviews of eVective food safety
training support many of the Wndings from the studies
examined here.
A number of reviews (Riben, Mathias, Campbell, &
Wiens, 1994; Riben, Mathias, Wiens, et al., 1994; Mathias
et al., 1994) undertook critical appraisals of the literature
relating to food safety education in Canada, focusing on
routine restaurant inspections and education of food handlers. They identiWed thirteen studies but many were weak,
lacking in methodological detail and with poorly deWned
outcomes. They concluded that training had an impact on
examination scores and restaurant inspection scores in the
short-term. It was impossible to deWne a particular educational intervention as most eVective due to diVerences inM.B. Egan et al. / Food Control 18 (2007) 1180–1190 1187
those used and lack of controls. In a follow up study, Mathias, Sizto, Hazelwood, and Cocksedge (1995) examined the
eVects of inspection frequency and food handler education
on restaurant inspection violations. Those restaurants with
any staV having food handler education did signiWcantly
better on the overall inspection score than those with staV
who had no such education.
In a further review of the eVectiveness of Canadian public health interventions in food safety 15 studies were examined and three categories of interventions identiWed
(Campbell et al., 1998). These were inspections, food handler training and community-based education. Once again
there was some evidence that interventions can result in
improved food safety, but the authors emphasize that
because of diVerences in protocols many studies are not
useful in establishing guidelines.
This work was recently extended (Mann et al., 2001) and
now includes 55 papers of which seven were rated as moderate and 48 rated as weak. The authors concluded that
four of the seven studies provided good evidence to support
the eVectiveness of the food safety interventions with positive results for the main outcome measured. Five of the
seven studies included in the review focused on food handler training and or certiWcation, three of which (Cotterchio
et al., 1998; Rinke et al., 1975; Waddell & Rinke, 1985) provided evidence for the eVectiveness of the intervention.
Several other reviews have attempted to identify the key
features of an eVective training programme (Sprenger,
1991; Rennie, 1994; Taylor, 1996). Training in the workplace is one such feature. Current training is often conducted away from the workplace and there may be
diYculties in translating theory into improved food handling. Rennie (1994) concluded that the need for improvements in food handling practices might be better served by
training in the workplace, allowing for practical reinforcement of the hygiene message. Taylor (1996) reiterated this,
arguing that the impact of food handler training is minimal
and would be more eVective if conducted in the workplace,
where it can be job speciWc. She cites the minimal eVect of
training courses on knowledge, attitudes and behaviour of
food handlers as well as their inability to inXuence operational practices.
Another critical issue is that of eVective management
training. In an evaluation of a fast food management training programme Jackson, Hatlen, and Palmer (1977), concluded that management training can be eVective if it is
administered on a continuous basis, supported by the owners and includes frequent follow-up. Nabali et al. (1986),
concluded from their study that training of managers was
eVective in improving hygiene standards. A microbiological
study of open, ready-to-eat, prepared salad vegetables from
retail or catering premises by Sagoo, Little, and Mitchell
(2003b), identiWed a direct relationship between food
hygiene training of management, increased conWdence in
the food business management and the presence of food
safety procedures. In a study of ready-to-eat stuYng from
retail premises in the northeast of England, Richardson and
Stevens (2003) suggested that poor microbiological quality
of product might be related to management food hygiene
training and conWdence in management scores. Sprenger
(1991) argues that prioritising the training of managers may
be more important than that of basic food handlers. The
numerous beneWts of management training include the ability of managers to inXuence premises hygiene, less turnover
of managers and their impact on the training of staV.
Whereas training food handlers has had minimal impact,
training managers may be more cost eVective, premises
hygiene is more within their remit and managers can
self-inspect and train employees (Taylor, 1996). However a
previous study of 300 professionally qualiWed catering
managers does not support many of these assertions
(Taylor, 1994). The results suggested that trained managers
did not put their theoretical knowledge into practice or
alternatively did not possess the knowledge that their qualiWcation should have delivered. Ultimately the training did
not result in the implementation of critical food safety
practices in the workplace.
A further issue to arise from US studies is that of mandatory training. Penninger and Rodman (1984) addressed
this issue by determining the eVectiveness of both voluntary
and mandatory food service managerial certiWcation training programs in a limited random study. Mandatory programmes were more successful in certifying managers than
voluntary programs with 91% of mandatory agencies
claiming improvement in inspection scores, compared to
33.3% of voluntary agencies. However these Wndings were
based on a response rate of less than 35% of the agencies
surveyed. In an evaluation of the Ohio Food service manager certiWcation course (Clingman, 1976), there was a 5.5%
improvement in overall sanitation level for those restaurants whose managers had been certiWed. This compared to
a 3.3% improvement for restaurants whose mangers were
not certiWed. This study also noted that management turnover in non-certiWed manager establishments was 29.7%,
whereas that in certiWed manager establishments was 19.5%
over the study period. Similarly, the voluntary nature of the
Minnesota Quality Assurance Programme for the Prevention of Foodborne Illness reduced its eVectiveness (Heenan
& Synder, 1978). Burch and Sawyer (1991), also recommended mandatory training based on their Wnding that the
sanitary condition of stores was closely associated with the
food safety knowledge of management.
The importance of training food handlers is acknowledged by many as critical to eVective food hygiene yet there
have been limited studies on the eVectiveness of such training. Many of the authors recommend approaches that may
result in improved food handling practices. Rennie (1995)
suggests that behavioural change would be more likely if
the settings approach to health promotion were adopted in
food premises.
Studies involving an assessment of food hygiene training
were included in this review. It is very diYcult to make any
direct comparisons between studies because of the varied
designs and outcome measures used. Within the various1188 M.B. Egan et al. / Food Control 18 (2007) 1180–1190
measures there was much variation and incomplete reporting of the details of the intervention methods and outcome
measures. For example, few studies reported details of the
questionnaires used. The majority of the studies were only
short-term and while these can provide useful information,
longer-term interventions and evaluations are needed to
assess behavioural change. Another limitation of the studies involving interventions was the lack of information on
costs or cost-eVectiveness, an issue often cited as a barrier
to training.
The limitations of measures used to assess training interventions are further discussed by Ehiri and Morris (1996).
They found the use of pre- and post-training test scores limited for evaluation purposes as they often measure knowledge of items not reXected in behaviour change. They also
highlighted the lack of correlation between examination
scores and improvements in food safety by reference to the
studies of Luby, Jones, and Horan (1993) and Laverack
(1989). The use of food hygiene inspection scores as a
means of evaluation is limited by the lack of correlation
between training and inspection scores. It is worth noting
also that these studies were based solely in the commercial
sector. Commercial food safety is very dependant on organisational structures and cannot easily be related to individual behaviour.
EVorts to reduce the incidence of foodborne illness
through interventions have had mixed results. The focus of
interventions, in the commercial sector, has been on
improving food handling practices. A primary aim and
therefore a primary criterion for evaluation of any training
is a change in behaviour towards less risky food handling
practices. A related goal is to improve knowledge about food
safety practices such as cross-contamination, temperature
control and personal hygiene. Related to these is the issue
of measuring outcomes. The principal conclusions of this
review of the literature are:
Current evidence for the eVectiveness of food hygiene
training is limited. This review has shown that many of the
studies on food hygiene training are limited both by a lack
of methodological detail and of well deWned outcomes,
Comparisons between studies are restricted and it becomes
impossible to deWne eVective interventions due to these
diVerences. There is a need to identify meaningful performance indicators at an individual level that can be used to
measure the eVectiveness of food hygiene training.
Questionnaires are a convenient measure of knowledge
and attitudes but direct observation has limited value. Reliable data from the workplace is essential to develop, implement and evaluate eVective food hygiene training, however
information on food hygiene behaviours obtained by direct
observation has limited value. Such observations are usually restricted to a small number of practices because of the
variety and complexity of roles involved in food handling.
StaV may also exhibit altered behaviours in the presence of
the observer to present what is perceived to be a more desirable image. There are also practical considerations in relation to time and cost involved in such observations.
Evaluation of training is essential and factors other than
training content and design are important. It is necessary to
look beyond the training context to understand how and
why training does or does not work. Issues such as managerial support, the availability of equipment and tools, training and pre-training motivation can all inXuence the extent
to which individuals react to the training experience. Training outcomes will also be inXuenced by a host of other factors, both organisational and individual. These may include
cultural dimensions, legislation, environmental.
Training of managers can be eVective in reducing food
safety problems. The training of managers is seen by many
as a necessary precursor to the implementation of realistic
food safety practices within the workplace. If managers
were trained to advanced levels they would then provide
basic training for food handlers in-house and make training
more sector speciWc. The eVectiveness of training is very
dependent on both management attitude and their willingness to provide the resources and systems for food handlers
to implement good practice.
Evidence from the literature suggests that food hygiene
training as a means of improving food safety standards is
limited by a lack of understanding of those factors contributing to successful outcomes. There is a need to develop
training methods that are proven to change behaviour as
well as imparting knowledge. Further research is needed on
issues including course content, the site of training, duration of courses and refresher training. Such research needs
to be clearly thought out, well designed with good baseline
data to achieve worthwhile results.
Acknowledgement
This study has been carried out with Wnancial support
from the Food Standards Agency. It does not necessarily
reXect its views and in no way anticipates the Agency’s
future policy in this area.
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