Systematic Literature Review of Oral Hygiene

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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