MICROBIOLOGICAL RISK ASSESSMENT SERIES

19

Salmonella and Campylobacter in

chicken meat
MEETING REPORT
 — ii —

The designations employed and the presentation of material in this information product
do not imply the expression of any opinion whatsoever on the part of the Food and
Agriculture Organization of the United Nations or of the World Health Organization
concerning the legal or development status of any country, territory, city or area or of
its authorities, or concerning the delimitation of its frontiers or boundaries. The mention
of specific companies or products of manufacturers, whether or not these have been
patented, does not imply that these have been endorsed or recommended by FAO or
WHO in preference to others of a similar nature that are not mentioned. All reasonable
precautions have been taken by the World Health Organization and the Food and
Agriculture Organization of the United Nations to verify the information contained in
this publication. However, the published material is being distributed without warranty
of any kind, either expressed or implied. The responsibility for the interpretation and
use of the material lies with the reader. In no event shall the World Health Organization
or the Food and Agriculture Organization of the United Nations be liable for damages
arising from its use. This report contains the collective views of an international group
of experts and does not necessarily represent the decisions or the stated policy of FAO
or of WHO.

Responsible technical units

Department of Food Safety and Nutrition and Consumer Protection

Zoonoses Division
Food and Agriculture Organization
World Health Organization of the United Nations

©FAO and WHO 2009

 — iii —

Contents
Acknowledgements vii
Contributors (Meeting Participants) ix
Abbreviations xi
Foreword xiii
Executive summary xv
1. Introduction 1
1.1 Background 1
1.2 Scope 1
1.3 Data sources and objectives 2
2. Differences in the nature of chicken meat production and
the implications for Salmonella and Campylobacter 3
2.1 General characteristics of chicken meat production and
processing systems 3
2.2 Regional perspectives: identification and consideration of critical
differences 4
2.2.1 Primary production 4
2.2.2 Slaughterhouse 5
2.2.3 Data for risk assessment 5
3. Review of available scientific information on control of
Salmonella and Campylobacter: occurrence and challenges,
and state of the science 7
3.1 Primary production 7
3.1.1 Salmonella 7
3.1.2 Campylobacter 7
3.2 Processing 8
3.2.1 Salmonella 8
3.2.2 Campylobacter 8
3.3 Distribution, handling and preparation 9
3.3.1 Salmonella 9
3.3.2 Campylobacter 9
 — iv —

4. Examples of specific possible interventions for hazard

reduction 11
4.1 Primary production 12
4.2 Processing 20
4.2.1 Handling of crates and pre-scalding 20
4.2.2 Scalding, de-feathering and evisceration 21
4.2.3 Head pulling 22
4.2.4 Evisceration 22
4.2.5 Crop removal 22
4.2.6 Decontamination (washing) 22
4.2.7 Chilling 25
4.2.8 Storage 28
4.3 Distribution, handling and preparation 29
4.3.1 Temperature control 29
4.3.2 Cross-contamination 29
4.4 Identification of data gaps 30
5. Evaluation of likely outcomes of specific interventions 31
5.1 Step 1: Depopulate and transport to slaughterhouse 31
5.1.1 Salmonella and Campylobacter 31
5.2 Step 2: Scalding, de-feathering and evisceration 31
5.2.1 Salmonella and Campylobacter 31
5.3 Step 3: Washing and chilling 31
5.3.1 Salmonella 31
5.3.2 Campylobacter 32
5.4 Step 4: Storage, retail and consumer handling 32
5.4.1 Salmonella 32
5.4.2 Campylobacter 32
6. Development of a Web-based risk-management tool 33
6.1 Background 33
6.1.1 Examples of tools already extant 34
6.1.2 Prototype tool for a Campylobacter/Salmonella Web-based tool 34
6.2 Suitability of outputs of the meeting for the prototype tool development 36
 — v —

7. Summarized considerations of CCFH request 39

8. References 41
Appendix 45
1. On use of chlorine, from FAO/WHO Consultation 45
2. Hypochlorite in carcass chillers 46
3. Draft summary of expert subgroup discussion on use of chlorine 48
 — vii —

Acknowledgements

The Food and Agriculture Organization of the United Nations and the World Health
Organization would like to express their appreciation to all those who contributed to the
preparation of this document through the provision of their time and expertise, data and other
relevant information and by reviewing the document and providing comments. In particular, the
work of Tina Struve in reviewing and summarizing the information received in response to the
call for data and coordination and technical finalization of the meeting report is acknowledged.
The assistance of José Javier Ocampo Beltrán in collaborating and reviewing data collected and
summarizing available information is also appreciated.

Appreciation is also extended to the meeting chair, the meeting rapporteur, working group
chairs and working group rapporteurs who provided advice and guidance during the preparation
of the final report.

The preparatory work for and implementation of the expert meeting, and the preparation of
this report were coordinated by the Secretariat of the Joint FAO/WHO Expert Meetings on
Microbiological Risk Assessment (JEMRA). This included Sarah Cahill, Maria de Lourdes
Costarrica and Masami Takeuchi in FAO, and Peter Karim Ben Embarek and Kazuko
Fukushima in WHO. Publication of the report was coordinated by Tina Struve and Maria de
Lourdes Costarrica. Final editing for language and style and preparation for publication was by
Thorgeir Lawrence.

This work was supported and funded by the Global Initiative for Food-Related Scientific
Advice (GIFSA).
 — ix —

Contributors (Meeting Participants)

Experts
Vivien ALLEN School of Clinical Veterinary Science, University of Bristol, Langford,
Somerset, United Kingdom
Ayachi AMMAR Laboratory of Microbiology and Immunology, Veterinary Department,
University of Batma. Algeria
Elyakum BERMAN Ministry of Agriculture and Rural Development, Poultry Department, Israel
Veterinary Services, Israel
Dane BERNARD Keystone Foods, United States of America
Marianne CHEMALY HQPAP research unit, AFSSA site de Ploufragan, France
Amir FAZIL Public Health Agency of Canada, Ontario, Canada
Neal GOLDEN Risk Assessment Division, Office of Public Health Science, Food Safety and
Inspection Service, USDA, United States of America
Charles L. HOFACRE Department of Population Health, College of Veterinary Medicine,
University of Georgia, United States of America
Xinan JIAO Laboratory of Zoonosis and Immunology, Yangzhou University, Yangzhou,
Jiangsu, China
Ruwani Sagarika Department of Veterinary Public Health and Pharmacology, Faculty of
KALUPAHANA Veterinary Medicine and Animal Science, University of Peradeniya,
Peradeniya, Sri Lanka
Nuri Sahli MADI Department of Food Science, Faculty of Agriculture, Al-Fateh University,
Libya
Mogens MADSEN DIANOVA, Technical University of Denmark - DTU, Denmark
Geoffrey Charles MEAD Food Hygiene Consultant, United Kingdom (Chair)
Stephen Jon MOORE Faccenda Group Ltd, Telford, United Kingdom
Vladimir Pinheiro do Department of Animal Medicine, Faculty of Veterinary Medicine (FAVET),
NASCIMENTO Federal University of Rio Grande do Sul (UFRGS), Brazil
George NASINYAMA Department of Epidemiology and Food Safety, Faculty of Veterinary
Medicine, Makerere University, Uganda
Maarten NAUTA Department of Microbiology and Risk Assessment, National Food Institute,
Technical University of Denmark - DTU, Denmark.
Alexander PANIN All-Russia State Centre for Quality and Standardization of Veterinary Drugs
and Feed (VGNKI), Russia
Antonia RICCI OIE/National Reference Laboratory for Salmonellosis, Istituto
Zooprofilattico Sperimentale delle Venezie, Italy
Hanne ROSENQUIST Department of Microbiology and Risk Assessment, National Food Institute,
Technical University of Denmark - DTU, Denmark (Rapporteur)
Todd RUTHMAN Risk Sciences International, Ottawa, Canada
 — x —

Marcos X. Inter-American Program for Agribusiness, Trade and Food Safety, Inter-
SANCHEZ-PLATA American Institute for Cooperation on Agriculture, Miami, United States of
America
Jaap WAGENAAR Utrecht University, The Netherlands

Meeting participants – resource persons

Steve HATHAWAY New Zealand Food Safety Authority, Wellington, New Zealand
Judi LEE New Zealand Food Safety Authority, Wellington, New Zealand
Lars Plym FORSHELL National Food Administration, Sweden
Mats LINDBLAD National Food Administration, Sweden
Gillian MYLREA International Trade Department, World Organisation for Animal Health (OIE),
Paris, France
Jeronimas Joint FAO/WHO Food Standard Programme, Rome, Italy
MASKELIUNAS
Sharon WAGENER New Zealand Food Safety Authority, Wellington, New Zealand

Declarations of interest
All participants completed a Declaration of Interest form in advance of the meeting. Eight of the
experts who participated in the meeting declared an interest in the topics under consideration.
• Vivien Allen’s research unit has received support for research on delivery methods for
Salmonella vaccines.
• Ayachi Ammar’s research unit is providing consultancy services and has received research
support from the National Agency for the Development of Research in Health.
• Elyakum Berman’s work is partly funded by the Israel egg and poultry board.
• Dane Bernard is an employee of a food company that includes broiler production operations.
• Charles L. Hofacre provides consulting services to a poultry breeding company.
• Geoffrey Charles Mead provides independent consultancy services as the Chairman of the
technical advisory board for a farm assurance company.
• Stephen Jon Moore is an employee of a poultry processing company.
• Vladimir Pinheiro do Nascimento provides consulting services to a poultry producing
company.
Upon detailed review of these declarations, it was considered that the interests declared by
these experts should not prevent them from participating fully in the deliberations of the
meeting. Their activities were not considered to represent a potential conflict of interest in the
meeting. Nevertheless, for the purpose of transparency, the declarations were made known to all
the participants at the beginning of the meeting. All the experts participated in their individual
capacity and not as representatives of their country, government or organizations.
 — xi —

Abbreviations
ASC Acidified Sodium Chlorite
CAC Codex Alimentarius Commission
CCFH Codex Committee on Food Hygiene
CE Competitive Exclusion
cfu colony-forming units
EU European Union
FAC Free Available Chlorine
FAO Food and Agriculture Organization of the United Nations
FSA Food Standards Agency [United Kingdom]
GHP Good Hygiene Practice
HACCP Hazard Analysis and Critical Control Points
IOBW Inside/Outside Body Wash
JEMRA Joint FAO/WHO Expert Meetings on Microbiological Risk Assessment
MRA Microbiological Risk Assessment
OIE World Organisation for Animal Health
OLR On-line reprocessing
PIF Powdered Infant Formula
ppm parts per million
TSP Trisodium Phosphate
WHO World Health Organization
 — xiii —

Foreword
The Members of the Food and Agriculture Organization of the United Nations (FAO) and of the
World Health Organization (WHO) have expressed concern regarding the level of safety of food
at both the national and international levels due to increasing foodborne disease incidence
caused by microorganisms in food. This concern has been voiced in meetings of the Governing
Bodies of both Organizations and in the Codex Alimentarius Commission. It is not easy to
decide whether the suggested increase is real or an artefact of changes in other areas, such as
improved disease surveillance or better detection methods for microorganisms in foods.
However, the important issue is whether new tools or revised and improved actions can
contribute to our ability to lower the disease burden and provide safer food. Fortunately, new
tools, which can facilitate actions, seem to be on their way.
Over the past decade, Risk Analysis—a process consisting of risk assessment, risk
management and risk communication—has emerged as a structured model for improving our
food control systems, with the objectives of producing safer food, reducing the numbers of
foodborne illnesses and facilitating domestic and international trade in food. Furthermore we are
moving towards a more holistic approach to food safety where the entire food chain needs to be
considered in efforts to produce safer food.
As with any model, tools are needed for the implementation of the risk analysis paradigm.
Risk assessment is the science-based component of risk analysis. Science today provides us
with in-depth information on life in the world we live in. It has allowed us to accumulate a
wealth of knowledge on microscopic organisms, their growth, survival and death, even their
genetic make-up. It has given us an understanding of food production, processing and
preservation, and the link between the microscopic and the macroscopic worlds and how we can
benefit from as well as suffer from these microorganisms. Risk assessment provides us with a
framework for organizing all this data and information and to better understand the interaction
between microorganisms, food and human illness. It provides us with the ability to estimate the
risk to human health from specific microorganisms in foods and gives us a tool with which we
can compare and evaluate different scenarios as well as identify what types of data are
necessary for estimating and optimizing mitigating interventions.
Microbiological risk assessment (MRA) can be considered as a tool that can be used in the
management of the risks posed by foodborne pathogens and in the elaboration of standards for
food in international trade. However, undertaking an MRA, particularly quantitative MRA, is
recognized as a resource-intensive task requiring a multidisciplinary approach. Yet foodborne
illness is among the most widespread public health problems, creating social and economic
burdens as well as leading to human suffering, making it a concern that all countries need to
address. As risk assessment can also be used to justify the introduction of more stringent
standards for imported foods, a knowledge of MRA is important for trade purposes, and there is
a need to provide countries with the tools for understanding and, if possible, undertaking MRA.
This need, combined with that of the Codex Alimentarius for risk-based scientific advice, led
FAO and WHO to undertake a programme of activities on MRA at the international level.
The Nutrition and Consumer Protection Division, FAO, and the Department of Food Safety
and Zoonoses, WHO, are the lead units responsible for this initiative. The two groups have
worked together to develop the area of MRA at the international level for application at both the
national and international levels. This work has been greatly facilitated by the contribution of
 — xiv —

people from around the world with expertise in microbiology, mathematical modelling,
epidemiology and food technology, to name but a few.
This Microbiological Risk Assessment series provides a range of data and information to
those who need to understand MRA. It comprises risk assessment of particular pathogen-
commodity combinations, interpretive summaries of the risk assessments, guidelines for
undertaking and using risk assessment, and reports addressing other pertinent aspects of MRA.
We hope that this series will provide a greater insight into MRA, how it is undertaken and
how it can be used. We strongly believe that this is an area that should be developed in the
international sphere, and have already from the present work clear indications that an
international approach and early agreement in this area will strengthen the future potential of
use of this tool in all parts of the world, as well as in international standard setting. We would
welcome comments and feedback on any document within this series so that we can endeavour
to provide Member States, Codex Alimentarius and other users of this material with the
information they need to use risk-based tools, with the ultimate objective of ensuring that safe
food is available for all consumers.

Ezzeddine Boutrif Jørgen Schlundt

Nutrition and Consumer Protection Department of Food Safety and
Division Zoonoses
FAO WHO
 — xv —

Executive summary
Salmonellosis and campylobacteriosis are among the most frequently reported foodborne
diseases worldwide. While numerous potential vehicles of transmission exist, commercial
chicken meat has been identified as one of the most important food vehicles for these
organisms. Although specific data on the burden of foodborne disease associated with
Salmonella and Campylobacter in poultry is limited, the role of poultry is considered to be
significant in this respect; however, the risk in different countries varies according to control
measures and practices implemented along the chain from primary production to final
preparation of the meat for consumption.
In 2007, the Codex Alimentarius Commission agreed that the development of guidelines for
the control of Salmonella and Campylobacter in poultry was a priority. The elaboration of these
guidelines was initiated at the 39th Session of the Codex Committee on Food Hygiene (CCFH),
in late 2007. The guidelines consist of three sections: one addressing good hygiene practices
(GHP); another covering hazard-based control measures; and a third focusing on risk-based
control measures. In the course of the following year, much work was undertaken on the first
section, and this is nearing completion. Work also began on the hazard-based control measures;
however, the limited availability of data on the quantification of effect and practical
implementation of such measures had implications for this section of the guidelines. The third
section was intended for use in conjunction with a user-friendly Web-based risk-management
decision-support tool, to be developed by the Joint FAO/WHO Expert Meetings on
Microbiological Risk Assessment (JEMRA), which would allow the risk manager to input data
specific to their own production and processing systems and thereby evaluate measures that
might be most effective for risk reduction in those particular conditions.
In order to continue with their work and ensure that it was underpinned with the most robust
scientific data, the 40th Session of CCFH requested FAO and WHO to provide them with the
necessary scientific advice. In response to that request, FAO and WHO convened an ad hoc
Technical Meeting from 4 to 8 May 2009 in Rome, Italy. This report documents the discussions
and the outcome of that meeting.
At the Technical Meeting, the experts carried out an independent assessment and review of
all available scientific information on control of Campylobacter and Salmonella at relevant
stages of the broiler supply chain. This entailed an evaluation of the scientific basis of the
possible control measures described in the draft guidelines as prepared by the CCFH Working
Group to date, and thereafter adding further interventions that had not been included. For every
step of the production chain, an attempt was made to evaluate the interventions in quantitative
terms i.e. according to their likely effects in reducing the prevalence and/or concentration of the
hazard in each case. Particular attention was given to the likely outcome of hazard reduction in a
commercial setting. For this purpose, the Experts decided to draw upon all available and
documented expert data and evidence in support of the interventions described. Thus, the latest
scientific evidence was used to supplement and expand the semi-systematic literature review
that had formed the basis of the draft guidelines developed by the CCFH Working Group.
The Experts found that there were no quantitative data available on the effects of specific
interventions applied during live animal production on the prevalence and/or level of
contamination with Salmonella and Campylobacter. Furthermore, the effects of any
 — xvi —

interventions aimed at primary production had not been validated fully in a commercial setting1.
Therefore, interventions for application in the pre-harvest phase of poultry production were all
classed as GHPs.
The GHP measures described in the Codex draft guidelines regarding scalding, de-feathering
and evisceration were supported by the Technical Meeting. No further scientific data was
presented by the Experts to warrant description of potential hazard-based control measures.
The GHP measures described in the Codex draft guidelines regarding washing and chilling,
and also retail and consumer handling were also supported by the Technical Meeting.
Quantitative data on potential hazard-based controls on account of their likely impact on
prevalence and/or concentration of hazards on the carcass were reviewed and considered
appropriate by the Technical Meeting, with additional data being provided in some cases.
In relation to the risk-management questions posed by CCFH, the feasibility of developing a
Web-based risk-management decision-support tool was discussed and considered to be an
appropriate next step by the Technical Meeting. The primary application of the tool would be to
demonstrate in a simplified manner the relative effects of different control measures, either
alone or in combination, on hazard reduction and consequently relative levels of foodborne
illness. This would enable countries to evaluate combinations of control measures available
within their processing systems using a risk-based approach. The decision tool should also be of
considerable benefit to industry in designing HACCP plans and choosing critical limits for
hazard-based control measures. In order to proceed with the development of the web-based risk-
management tool a subgroup was formed to identify modelling challenges and discuss the
benefits and limitations of different modelling approaches. Development of the prototype is now
in progress, and initial outcomes will be presented at the forthcoming CCFH session.

1. The apparent absence of peer-reviewed scientific publications on the efficacy of specific interventions
in commercial poultry flocks in terms of food safety of broiler meat needs to be seen in context. Such
interventions have been widely used in many countries as part of national control programmes for
Salmonella and, over a period of time, have been associated with significant reductions in prevalence
of pathogens at the pre-harvest stage of broiler production. The countries include Finland, Sweden,
Denmark and The Netherlands, and the effectiveness of their respective control strategies is described
in peer-reviewed scientific publications and in national reports that include surveillance data for
Salmonella in poultry. See, for example, Wegener et al., 2003; Maijala et al., 2005; Van der Fels-
Klerx et al., 2009.
MEETING REPORT
 1. Introduction

1.1 Background
Salmonellosis and campylobacteriosis are among the most frequently reported foodborne
diseases worldwide. While numerous potential vehicles of transmission exist, commercial
chicken meat has been identified as one of the most important food vehicles for these
organisms. In the light of their importance, FAO and WHO have already undertaken risk
assessments on Salmonella and Campylobacter in broiler chickens (FAO, 2003; FAO/WHO,
2002; FAO/WHO, 2009). At the time of their completion, these risk assessments provided both
an overview of the available knowledge on these organisms and a risk assessment framework to
facilitate the evaluation of various interventions to address the risks associated with these
pathogens in broiler chicken meat at the point of consumption.
Although specific data on the burden of foodborne disease associated with Salmonella and
Campylobacter in poultry is limited, it is considered to be significant; however, the risk varies
according to control measures and practices implemented along the chain from primary
production to final preparation for consumption. Furthermore, the presence of these organisms
in poultry is also affecting trade, and recently the detection of Salmonella in poultry products
led to rejection of large consignments of raw poultry meat. While the scientific basis for such
actions is not always clear, the economic impacts can be extensive. Thus the impact on human
health and the associated costs, the trade disruptions and the cost of implementing effective
control measures has meant that the Codex Alimentarius Commission (CAC) in 2007 agreed
that the development of guidelines for the control of Salmonella and Campylobacter in poultry
was a priority. Later that year, at its 39th Session, the Codex Committee on Food Hygiene
(CCFH) agreed on the approach to be taken in the development of the draft guidelines.
Essentially the guidelines are to consist of three sections: one that addresses good hygiene
practices (GHP); one that addresses hazard-based control measures; and a third that focuses on
risk-based control measures. In the past year much work has been undertaken to address the first
section, and this is nearing completion. Work has also begun on the hazard-based control
measures; however, the availability of data on the practical implementation of such measures
has implications for this section of the guidelines. The third section of the guidelines is
envisaged to be used in conjunction with a user friendly Web-based risk-management decision-
support tool, to be developed by the Joint FAO/WHO Expert Meetings on Microbiological Risk
Assessment (JEMRA), which will allow the risk manager to input data specific to their
production and processing system and thereby evaluate measures that might be most effective
for risk reduction in those particular conditions.
In order to continue with their work and ensure that it is underpinned with the most robust
scientific data, the 40th Session of CCFH requested FAO and WHO to provide them with the
necessary scientific advice. In response to that request, FAO and WHO convened an ad hoc
Technical Meeting from 4 to 8 May 2009, in Rome, Italy.
1.2 Scope
The scope of the work to be undertaken by FAO and WHO, through the Technical Meeting, was
defined by the series of issues that CCFH asked both organizations to address, as listed below.
• To carry out an independent assessment and review of available scientific information on
control of Campylobacter and Salmonella at relevant steps through the broiler chain.
2 Introduction

• To evaluate quantitative aspects of hazard reductions in terms of prevalence and

concentration following specific interventions.
• To evaluate likely outcomes in terms of hazard reductions in the commercial setting.
• To assess the feasibility of developing a Web-based risk-management decision-support
tool.
• To develop a framework and identify data needs that might be required for the Web-
based risk-management decision-support tool to be developed by JEMRA.
This Meeting report summarizes the results of the Joint FAO/WHO Technical Meeting on
Salmonella and Campylobacter in Chicken Meat, held at FAO, Rome, from 4 to 8 May 2009,
noting the data sources used and drawing out the main conclusions. In response to the questions
posed by CCFH to FAO and WHO, a number of recommendations were made. Special attention
was drawn to areas where further research and data collection were required for extending the
Web-based risk assessment tool to be more comprehensive and reliable.
1.3 Data sources and objectives
The objective of the meeting was to make an independent assessment of the measures
internationally available for the control of Campylobacter and Salmonella spp. in chicken meat,
based on scientific information on the control of these microorganisms at different steps of the
broiler production chain. The assessment included the review of quantitative aspects of hazard
reduction in terms of prevalence and concentration in the commercial setting, and the
assessment of the feasibility of developing a Web-based risk-management support tool that
could assist managers in the evaluation of measures that might be most effective for risk
reduction in their production and processing systems.
FAO/WHO initiated this assessment through the implementation of an extensive literature
search and by issuing a call for relevant data using various routes, with 24 replies received from
different countries in response. Data and information was submitted by national authorities and
non-governmental organizations, including academic institutions and poultry production groups.
Additionally, data used during this meeting were collected through the review made by the
CCFH Working Group as part of the work carried out for the preparation of the Proposed Draft
Guidelines for the Control of Campylobacter and Salmonella spp. in chicken meat. Furthermore,
specific experts attending the meeting were asked to prepare a short background paper
describing regional differences in chicken meat production, with special emphasis on detection
and control of Salmonella and Campylobacter.
For the Technical meeting to address the request made by CCFH, the Good Hygiene
Practices (GHP) and hazard reduction measures mentioned in the Draft Guidelines provided by
the CCFH Working Group were used as a starting point, with the Experts assessing different
interventions at specific steps in the processing chain. The measures mentioned in the guideline
were assessed from the perspective of their scientific basis. Thereafter, appropriate additional
intervention measures were assessed. Special emphasis was laid on the presence of quantitative
data, which were considered when assessing the feasibility of the Web-based decision tool (See
Chapter 6).
 2. Differences in the nature of chicken meat
production and the implications for Salmonella
and Campylobacter

2.1 General characteristics of chicken meat production and

processing systems
One of the objectives of the request made by the CCFH to FAO and WHO was to investigate
the feasibility of developing a Web-based decision tool that could assist managers in the
evaluation of measures that could be most effective for risk reduction in their production and
processing systems.
In order to meet this request, the Experts had to consider regional differences that could have
critical impacts on the implementation of such a tool. Therefore, the first day of the Technical
Meeting was dedicated to the discussion of these differences.
In spite of the extensive regional differences in broiler production, a substantial part of the
chicken meat production at “industrial level” has some common aspects. For instance, the
breeding stocks used all over the world are produced by a small number of companies, meaning
that these sell to purchasers worldwide. This can lead to the widescale spread of Salmonella if
the breeding stocks are infected. It is therefore especially important to control Salmonella in the
breeder flocks, and as a consequence Salmonella control in primary breeder flocks is of a high
standard (Allen, pers. comm.). Where the aim is to control specific serotypes, a zero-tolerance
policy with respect to these organisms may give a false sense of security, because the
predominant serotypes in poultry flocks are likely to change over time.
The trend seems to be towards production becoming more integrated in the future, and many
small farms will be replaced by fewer, bigger farms, which will allow a greater integration. As
an example, integrated poultry production is very widespread in the United States of America
and in Russia, where the producers also control feed, rearing and processing. This high degree
of integration can therefore lead to better control of Salmonella and Campylobacter. These
control options can also be applied to less integrated systems; it is just more difficult, even
though the principles for control should be the same.
Despite differences between countries, the characteristics of “industrial” broiler chicken
meat production are broadly generic. This facilitates development of a modular risk assessment
that focuses on shared food chain characteristics, but also provides for national inputs where
there may be significant variation, such as in primary processing, distribution pathways, and
handling of products by the consumer. For Salmonella, the peer reviewed literature indicates
that the four most important control measures at primary production are: (1) the elimination of
Salmonella in grandparent and parent flocks; (2) all-in all-out production at the broiler farm, to
avoid any carry over during processing; (3) logistic slaughter planning scheduled to avoid
pathogens being transferred from contaminated processing equipment to another flock; and,
finally, (4) satisfactory cleaning of transport crates. For Campylobacter biosecurity at farm level,
it is reported that prevention of the entry of Campylobacter is the most important control
measure, but it is also important to prevent transfer of the organism from previous flocks. At
present, the epidemiology is not completely clear, and there are also country differences to
consider.
4 Differences in the nature of chicken meat production

During processing, additional interventions can be applied. Application of GHP during

processing helps to ensure that the contamination of broiler carcasses remains as low as
possible. Essential practices include the removal of faecal matter, feathers, etc., from carcasses
and equipment. Most important are procedures that keep the faecal spread to an absolute
minimum.
Operations known to increase the contamination are scalding, plucking and evisceration. The
feather plucker is the most important critical control point in the process in relation to
contamination, but also evisceration can pose a big risk as a consequence of gut rupture. The
problem in this step is that the carcasses are not entirely uniform in size and some may be
damaged by the evisceration machinery. To reduce carcass contamination, decontamination
measures can be applied. These can be physical or chemical, and aim to reduce the
concentration. Contamination of carcasses with Campylobacter can be reduced by dipping or
spraying of carcasses using chlorinated water, acidified sodium chlorite (ASC) or acetic or lactic
acids. Trisodium phosphate (TSP) has also been widely used, but due to processing and
environmental problems its use is now minimal. Regarding these decontamination measures,
there are some regional differences to be considered, since chemical treatment is not accepted in
the EU at the moment, but is widely used in other parts of the world, e.g. in the United States of
America and New Zealand. Physical treatments that reduce Campylobacter counts on carcasses
include freezing; crust freezing; heat treatment; steam-ultrasound; steam or hot water spray;
forced air chilling; and irradiation.
The experts emphasized the differences between countries, and considered the fact that
specific measures taken in one country might not work in another. In a Web-based risk
assessment tool, countries would have to add national data in order to assess the relative risk for
their country.
2.2 Regional perspectives: identification and consideration of
critical differences
The regional differences were too comprehensive to be considered in the present report.
However, this section provides an introduction to some of the critical differences among
countries, for the industrial settings.
2.2.1 Primary production
The most prominent differences presented at the Technical Meeting were found in the primary
production sector. The particular region has a great influence on this matter as well as variation
in the size of broiler production. Thus differences in number of birds produced range from
9.02 billion in the United States of America to 75 million in Sweden. The climate in a region
can have great effect on the type of housing chosen. The housing can be open or closed. Also
the number of birds in the houses varies, since the heat generated by the chickens can be crucial.
Also, other husbandry differences exist, and especially floor type and management can vary. A
further account of these differences will not be given here since it is not the aim of this report,
but the effect on hazard reduction will be reviewed in Chapter 4.
The amount and type of ventilation of the houses differs among the different regions and the
different production types. The type and degree of ventilation used is very much dependent on
the climate and the housing type, since hotter climates and closed houses requires more
ventilation. As will be explained in Chapter 4, the ventilation can be an important source of
Campylobacter introduction, and studies have been made in several Nordic countries on
provision of fly-screens in the ventilation to prevent introduction of Campylobacter with flies.
 Salmonella and Campylobacter in chicken meat 5

Thinning may result in infection of the remaining birds with Campylobacter due to the
temporary breakdown in biosecurity.
2.2.2 Slaughterhouse
Most processing procedures are similar in the different regions, but there are differences in
processing practices, since the product wanted by the consumers can vary a lot between the
different regions. In many places, marketing can be said to drive the production system. This
can reflect differences in legislation. The EU has a top-down approach, whereas in the United
States of America current practice is that the primary control is applied in the processing plant.
As mentioned in the previous section, the decontamination step will also show some differences
among the countries as a result of the local legislation. Thus demands under European Union
legislation differ from that required by, for instance, the United States of America legislation.
2.2.3 Data for risk assessment
Besides the differences mentioned above, there are other challenges to be considered regarding
the Web-based tool. One of the big difficulties is to get data representative for a country, due to
different production systems within the country. For example, in Brazil, the big export
companies are in the south, whereas the smaller companies in the north produce for the home
market. There are challenges when comparing data within a country, but it is far more difficult
to compare data between countries. Another big challenge is that different methods for analysis
in monitoring and research give different results. Furthermore, the legislation and financial
support for additional and systematic sampling will vary greatly within the different country.
Standardized analysis for Campylobacter will pose a special problem in many countries.
 3. Review of available scientific information on
control of Salmonella and Campylobacter:
occurrence and challenges, and state of the
science

3.1 Primary production

The apparent absence of peer-reviewed scientific publications on the efficacy of specific
interventions in commercial poultry flocks in terms of food safety of broiler meat needs to be
seen in context. Such interventions have been widely used in many countries as part of national
control programmes for Salmonella and, over a period of time, have been associated with
significant reductions in prevalence of pathogens at the pre-harvest stage of broiler production.
The countries include Finland, Sweden, Denmark and The Netherlands, and the effectiveness of
their respective control strategies is described in peer-reviewed scientific publications and in
national reports that include surveillance data for Salmonella in poultry. See, for example,
Wegener et al., 2003; Maijala et al., 2005; Van der Fels-Klerx et al., 2008.
3.1.1 Salmonella
In primary production, control of Salmonella within broiler flocks relies on knowledge of the
source of infection (FAO/WHO, 2002). Possible sources include water, feed, litter, farm staff
and the environment, both inside and outside the broiler house (Davies, 2005). Furthermore,
hatcheries are possible sources of infection, as is vertical transmission (FAO/WHO, 2002). Data
on the number of Salmonella organisms in feed, litter, etc., and the numbers of the organism to
which the bird has been exposed, are still limited or unknown. Therefore many of the current
risk assessment models today start at the point of estimating the prevalence of contaminated
Salmonella-positive birds as the birds enter the slaughterhouses, and this means that on-farm
control strategies are very poorly investigated at the present time (FAO/WHO, 2002). In relation
to this meeting, a call for data was sent out, asking inter alia for data regarding prevalence and
effect of on-farm control measures. This call for data did not reveal any new information on the
effect of on-farm interventions as no quantitative information was presented for this step of the
chicken production chain. Enumeration of Salmonella is laborious and time consuming, and is
rarely carried out in practice.
3.1.2 Campylobacter
The principal reservoir of pathogenic Campylobacter spp. is the alimentary tract of wild and
domesticated mammals and birds. Several countries have monitoring programmes to determine
the prevalence of Campylobacter in food producing animals and birds. A seasonality of broiler
flock colonization has been shown in some countries, leading to a peak in the flock prevalence
during the warm summer months (Newell and Davidson, 2003; Kapperud et al., 1993; Jacobs-
Reitsma, Bolder and Mulder, 1994; Rosenquist et al., 2009). However, studies in other parts of
the world (for instance the United Kingdom and North America) have not shown any evidence
of seasonality (Nadeau, Messier and Quessy, 2002). It is believed that the observed influence of
season may be associated with the increased ventilation of houses and the increased numbers of
insects during the warm summer and autumn months. If large volumes of air are introduced, it is
conceivable that flies with Campylobacter from the outside are introduced into the flock. In
Denmark and Iceland, studies have investigated the effect of using fly-screens to prevent the
8 Review of available scientific information

introduction of Campylobacter in the flock. This has shown promising results in lowering the
prevalence of Campylobacter (Hald, Sommer and Skovgard, 2007). However, more
intervention studies must be conducted in order to measure the effect on prevalence and level of
contamination, using also control farms. The efficacy of fly-screens also needs to be tested in
countries with climatic conditions different from those in the Nordic countries.
Campylobacter shed in faeces from the gastrointestinal tract are able to survive for
considerable periods in the environment, but are not known to grow under those conditions.
Survival is enhanced by cool, but not freezing, moist and dark environments. As many
mammals and birds (wild and domestic) are known hosts for Campylobacter, which can be
asymptomatically excreted in significant numbers, then the environment (soil, water, pasture,
etc.) must be frequently contaminated with this organism. A conventional poultry house that is
modern and well maintained and with limited access should be considered a biosecure premise.
Passive transgressions of the biosecurity perimeter in such a house may be by essential
commodities like water, feed and air. Active transgressions require the carriage of
Campylobacter from the external environment, which may occur by vectors such as vermin or
flying and crawling insects, but the most visible vehicles are humans (Ridley et al., 2008).
It is widely assumed that thinning or partial depopulation is a significant risk factor for flock
colonization. The risks include the passive transfer of organisms from previously-visited farms
or the processing plant on clothes, boots, crates and vehicles on to the farm, and subsequently
into the broiler house during catching. Thinning may result in infection of the remaining birds
with Campylobacter within 2 to 6 days due to the temporary breakdown in biosecurity (Allen et
al., 2007).
3.2 Processing
3.2.1 Salmonella
Differences in prevalence resulting from different practices are considered in several studies. In
particular, these studies have focused on differences in water-immersion scalding and chilling
(with and without chemical additives). Those concerned with the effect of chemical additives
generally report a reduction in the prevalence (FAO/WHO, 2002). Data on prevalence and
numbers of organisms are available for individual production steps, but most often using these
data to estimate level of reduction requires additional assumptions since there are differences in
the way the data are obtained. Conducting a baseline study would provide a more certain
estimation (FAO/WHO, 2002). The call for data in support of this meeting provided additional
data on this production step, but, as is the case for previous studies, the data from different
studies are difficult to compare, due to differences in sampling and methods of analysis.
Therefore estimates based on these data sources will also contain a certain level of uncertainty.
Whereas data on the prevalence of Salmonella on poultry meat at the end of processing or at
retail were available, very few surveys have been undertaken where the number of organisms
has been quantified (Anon., 2005). Data provided by Libya in response to the data call describe
the effect of radiation and storage temperature upon growth of Salmonella in fresh chicken
carcasses, but, as is the case with the previously mentioned investigations, more work needs to
be done in order to standardize these studies in a way that renders them comparable among
countries. As a consequence, it is very difficult to combine the existing data in a risk assessment
model to be used when developing the Web-based decision tool.
3.2.2 Campylobacter
Since Campylobacter is a common inhabitant of the intestinal tract of warm-blooded animals,
the organism can be expected to contaminate meat during slaughter and evisceration as a result
 Salmonella and Campylobacter in chicken meat 9

of faecal contamination (FAO, 2003). Therefore, the main goal in controlling Campylobacter
contamination of chicken carcasses during processing is to minimize the spread of faecal
material. The process operations that have been considered in risk assessments are: scalding, de-
feathering, evisceration, washing and chilling (FAO, 2003; Nauta et al., 2009). A study
performed in Denmark on the numbers of Campylobacter during specific slaughter operations
has revealed that the evisceration operation may lead to increased Campylobacter
concentrations on the carcasses, whereas air- and water-chilling can lead to reductions of 0.8–
1.0 log10 cfu/g. Furthermore, it has been shown that freezing causes an additional reduction of
1.4 log10 cfu/g before further frozen storage (Rosenquist et al., 2006). Because scalding washes
much of the dirt and faeces off the carcass exterior, more microorganisms can be removed
during scalding than during any other process step (USDA-FSIS, 2008; Cason and Hinton,
2006; Hinton et al 2004a, 2004b). The scald process cannot eliminate excessively high numbers
of microorganisms entering the process, and the effect of scalding is very dependent on the
method used, since immersion scalding has been shown to increase the level of contamination in
cases where the operating conditions are poor. This was probably caused by an accumulation of
dirt and faeces in the scald water due to an inadequate flow of fresh water into the tank, making
the scald tank a source of cross-contamination for subsequent carcasses (USDA-FSIS, 2008;
Cason and Hinton, 2006; Hinton et al 2004a, 2004b). The scalding process is a major site of
cross-contamination for Salmonella, but is less important in this respect for Campylobacter
because prevalence and numbers of the organism tend to be much higher in positive flocks.
3.3 Distribution, handling and preparation
3.3.1 Salmonella
Most often, interventions at these stages are assessed using growth models that take account of
levels of contamination when carcasses leave the processing plant, thereafter using inputs for
storage time in retail stores, transport time, storage times in homes, and the temperatures
carcasses were exposed to during each of these periods. The presence and level of Salmonella in
this step is very much country specific, since the level of infection when leaving the processing
step will vary between the countries in relation to the methods used at the processing plant.
Therefore national data must be used when estimating levels of contamination (FAO/WHO,
2002).
The call for data sent out in conjunction with the Technical Meeting revealed that many of
the contributors do investigate the prevalence of Salmonella in the chicken meat, but often this
is not done for the level of contamination. Furthermore, the analyses are not done in a
standardized manner and the results will be very hard to use for comparison between countries,
and even within regions of the same country.
3.3.2 Campylobacter
Reports from the European Union (EU), as well as other countries, reveal that fresh poultry
meat is the food vehicle most frequently contaminated with Campylobacter. In some EU
member states in 2007 the prevalence in retail products was as high as 83%. In Iran, a
prevalence of 63% has been reported, and in Japan 45.8% of retail poultry was contaminated
with Campylobacter (FAO, 2003). A study performed in Denmark uses simulations designed to
predict the effect of different mitigation strategies, which showed that the incidence of
campylobacteriosis associated with consumption of chicken meals could be reduced 30 times by
achieving a 2 Log reduction in the number of Campylobacter on the chicken carcasses. To
obtain a similar reduction of the incidence, the flock prevalence should be reduced
approximately 30 times, or the kitchen hygiene improved approximately 30-fold (Rosenquist et
al., 2003). A study from Germany investigated the transfer of Campylobacter, using simulations
10 Review of available scientific information

of some typical situations in kitchens and quantification of the Campylobacter transfer from
naturally contaminated chicken parts most commonly used in Germany. One scenario simulated
the seasoning of five chicken legs and the re-use of the same plate for cooked meat. In another,
five chicken breast fillets were cut into small slices on a wooden board where, without
intermediate cleaning, a cucumber was sliced. Average transfer rates from hands or kitchen
utensils to ready-to-eat foods ranged from 2.9 to 27.5% (Luber et al., 2006). It is generally
believed that cross-contamination, not undercooking, is the dominant route of exposure to
humans (Nauta et al., 2009). However, in some special, minimally processed meat products, this
may be otherwise. Exposure is a consequence of insufficient food hygiene by the person
preparing the food. The vast majority of consumers in a study in the Netherlands have been
shown to be unable to prevent cross-contamination; the effect of consumer information on the
prevention of cross-contamination as a control measure is very small (Nauta et al., 2008).
4. Examples of specific possible interventions for
hazard reduction
One of the objectives of the meeting was to prepare an independent assessment and review of
available scientific information on control measures. This was performed by the Experts
through a review of the scientific basis of the interventions mentioned in the Codex draft
Guidelines (CCFH Draft Guidelines for control of Campylobacter and Salmonella spp. in
chicken meat).2 For each step in the production chain, possible additional interventions were
included.
In support of the meeting's deliberations, reference was made to either information available
on the OIE Web site or to material provided in draft form for the use of the Technical Meeting.
In particular the draft Guidelines on the Detection Control and Prevention of Salmonella spp. in
Poultry were brought to the attention of the meeting3. These have already been considered by
the CCFH working group in their deliberations and both the OIE and Codex documents are
intended to be complementary to each other.
This chapter will follow the process flow outlined in the Codex draft Guideline document
provided by the Codex working group. Comments and Expert Group opinions are given at the
various steps outlined in these draft Guidelines when these are step specific, while comments
and opinions covering several steps of the process (e.g. decontamination) are provided in the
appendix to this report. The relevant text from the Codex draft Guidelines is provided
immediately before the comments of the Experts.
The Experts wish to stress that although individual intervention methods have been reported
to yield scientifically documented reduction effects when applied as the sole measure, multiple
interventions are not always additive.
The Experts identified two horizontal issues with the potential to affect several steps in the
processing segment of the document, the use of chlorination, and, the effectiveness of washing
with water or water containing chemical processing aids.
The Experts drew on all available and documented data and evidence in support of the
interventions described, with the purpose of including up-to-date relevant scientific evidence in
order to supplement and expand the semi-systematic literature review that forms the basis of the
draft Guidelines provided by the Codex working group. This chapter documents the review of
the scientific underpinning of the Codex draft Guidelines. Where the expert meeting considered
that the guidance was appropriate given the current knowledge base and scientific evidence, no
further comment is given. However, in those cases where the guidance was considered to be
incomplete or inappropriate given the available scientific evidence, the basis for such an
opinion is provided.

2. It must be stressed that this was a draft and therefore expected to change in the light of subsequent comments.
The text on which the meeting's deliberations was based can be found at:
ftp://ftp.fao.org/codex/ccfh40/fh40_06e.pdf
3. At the time of the Meeting, the primary OIE document was still technically a draft but due to go for adoption to
be included in the 2009 Terrestrial Animal Health Code at the OIE General Session in the last week of May,
2009. Once adopted it would become part of Terrestrial Animal Health Code. Until that time it would be
available as Annex XIII of the Report of the Terrestrial Animal Health Standards Commission. See pp. 157–162,
in: http://www.oie.int/downld/SC/2009/A_TAHSC_March2009_PartA.pdf
12 Examples of specific possible interventions for hazard reduction

4.1 Primary production

The Experts agreed that control measures applied at primary production are important for the
control of Salmonella and Campylobacter throughout the production process and noted that they
have been undertaken in a number of countries. However, due to the lack of quantification of
the effect on prevalence or level of contamination on broiler carcasses, there are no validated
hazard based control measures for Salmonella or Campylobacter in primary production. All of
the following would be considered as GHPs by the Expert Group.
General control measures for Steps 1 to 11 (Production)
The OIE Terrestrial Animal Health Code (March 2008) Appendix 3.4.1, Annex VI, Hygiene and
Biosecurity Procedures in Poultry Production, provides considerable detail on control measures that
apply to most production steps and should be referred to in application of these more specific
Guidelines. The OIE Terrestrial Animal Health Code (March 2008) Annex V, Guidelines on the
Detection Control and Prevention of Salmonella spp. in Poultry, should be referred to when applying
Steps 1, 9, 10, 11 and 12. Codex draft Guidelines
The Experts were aware that the draft Guidelines on the Detection Control and Prevention of
Salmonella spp. in Poultry has been revised and the new version had been approved by the OIE
Code Commission, and was to be presented to the general meeting of OIE in May 2009.
The Hygiene and Biosecurity Procedures in Poultry Production draft had not yet been
agreed and could be substantially revised.
Further comments are given at relevant steps of relevant interventions.
In addition to following this general guidance, people entering the live bird production areas should
not have close contact with any other birds. If such contact is unavoidable, they should not be
permitted to enter live bird production areas for a specified time after the contact, and then only after
the application of appropriate hygiene measures.
People and vehicles who need to move in reverse of the production flow, i.e. towards Step 1, should
be required to apply sufficient hygiene measures to avoid the introduction of Campylobacter and
Salmonella earlier in production. People and vehicles who need to move to production areas from a
feed mill or processing premises should apply appropriate hygiene measures to minimize the
introduction of Campylobacter and Salmonella into production.
Codex draft Guidelines
The Experts considered this text was appropriate given the current knowledge base and had
no further additions or comments.
Step 1: Manage grandparent flocks
Control of Campylobacter and Salmonella in grandparent flocks is achieved by the application of a
combination of biosecurity and personnel hygiene measures. The particular combination of control
measures adopted at a national level should be determined by the Competent Authority, in
consultation with industry.
Farms should be sited away from other poultry farms, livestock operations, abattoirs and identified
sources of contamination. Pest control programmes, particularly to manage rodents, flies and beetles,
should be in place. Wild birds should be discouraged by immediate clean-up of any feed spills, and
keeping doors closed when not in use.
Equipment and feeders should be designed to minimize contamination from the birds.
Litter should be obtained from an uncontaminated source or be sanitized.
Any equipment taken into a poultry house should be cleaned and sanitized beforehand (including
equipment used for maintenance and repairs). Vehicles should be washed and sanitized at the site
entrance.
 Salmonella and Campylobacter in chicken meat 13

All eggs intended for incubation should be sanitized as soon as possible after lay.
Codex draft Guidelines
In this context, it was the opinion of the Experts that there should be more details on pest
control programmes, e.g. to cover domestic animals, arthropods, reptiles, flies, mites and
wildlife. It was considered that the OIE guidelines covered this appropriately except for the
control of arthropods.
Furthermore, it was the opinion of the Experts that microbiological sampling and testing for
Salmonella was not adequately covered by the Codex draft Guidelines. It was considered that
the OIE guidelines covered this appropriately. Also it was found that drinking water was not
adequately covered in the Codex draft Guidelines, although this was found to be covered
appropriately by the OIE guidelines. It was the opinion of the Experts that sanitization of eggs
can have a negative effect on Salmonella status, chick hatchability and chick quality if the dip
solution becomes contaminated or if improper temperature of the sanitizing solution is used
(Williams and Dillard, 1973; Hutchison et al., 2004).
Strategies to reduce faecal contamination of eggs such as not incubating floor eggs, keeping
nest boxes clean and sanitation of egg trays should be encouraged. The OIE guidelines covered
this appropriately, except for floor eggs (Saeed et al., 1999). The Experts recommend that this
should be considered by the CCFH working group.
When reviewing the Codex draft Guidelines, it was the opinion of the Experts that these
were light on biosecurity measures. However, they found that these were appropriately covered
by the OIE codes, especially for:
• cleaning and disinfection of houses and immediate surrounds or other areas of the farm that
may present a reservoir for Salmonella or Campylobacter;
• staff, visitor and catcher clothing;
• vehicle parking;
• disinfection if it is necessary to enter the farm; and
• restriction on equipment shared between houses.
For Campylobacter: Because of the possibility of vertical transmission, Competent Authorities may
choose to apply preventative measures as a precautionary measure.
Codex draft Guidelines
The Experts agreed that the statement regarding the possibility of vertical transmission of
Campylobacter should be deleted, as at present there is no strong evidence that Campylobacter
is vertically transmitted (Callicott et al., 2006). Campylobacter control prior to broiler farms
was therefore not considered to be necessary.
For Salmonella: The breeder production flock should be kept free from Salmonella to prevent vertical
spread of infection.
Incoming flocks should be screened and monitored according to a statistically-based sampling plan.
Until results are available, the birds may be kept in quarantine. During rearing and production the
birds should be tested according to specified sampling schemes.
Where a flock is found to be Salmonella-positive the houses should be meticulously cleaned and
disinfected before new birds are introduced. Sampling from various locations and equipment should
verify that no Salmonella infection persists.
Feed should be heat-treated or subjected to other bactericidal treatment. Breeder feed should
preferably be delivered in dedicated vehicles used only for feed transport.
Codex draft Guidelines
14 Examples of specific possible interventions for hazard reduction

The Experts wanted to emphasize the value of culling positive flocks, and it was found that
the OIE document covers this appropriately.
The Experts agreed that feed should be heat treated and could be subjected to other
bactericidal treatment.
For Salmonella: Other measures that have been evaluated in experimental or very limited commercial
settings include vaccines, competitive exclusion, and feed or water additives. A Competent Authority
may need to validate such measures in the national setting before advocating their use. Such measures
must however not be seen as alternatives to good hygienic practices. Codex draft Guidelines
There are live vaccines and killed vaccines that can be used.
It was the opinion of the Experts that live Salmonella vaccines demonstrate non-serotype-
specific and rapid protection for breeder pullets. Live vaccines also give immunity against
specific serotypes. The inactivated Salmonella vaccines produce immunity only against specific
serotypes. Combination of live and killed vaccines gives protection to the hen and maternal
antibodies to the broiler. All of these are widely used commercially. Despite this, the Experts
did not consider it to be a hazard control measure as the effect had not been well enough
quantified regarding the impact on the resulting broilers.
The Experts stated that probiotics are defined products, whereas competitive exclusion (CE)
mixtures are undefined intestinal flora. It was the opinion of the experts that the use of
undefined CE products could be effective for Salmonella control in combination with other
interventions. It decreases or prevents Salmonella colonization of other birds in the flock and
results in a decreased concentration of Salmonella in caecal contents of birds that become
colonized. It was accepted by the meeting that CE was in wide commercial use.
Probiotics are live microbial feed supplements that are not pathogenic for the host and able
to modulate the immune response and change or stabilize microbial activities. Prebiotics are
non-digestible substances with a beneficial physiological effect on the host due to the beneficial
effect on the gut flora of the host. There are many publications on pre- and probiotics. Currently,
there was no evidence that they could be commercially developed as effective intervention
agents for Salmonella.
There is a great variety of feed and water additives, including organic acids, plant derivatives
and enzymes (e.g. xylanase). For Salmonella control, there are numerous feed and water
additives that have been successful when used experimentally. The opinion of the Experts was
that these were not currently effective commercially, with the exception of organic acids or
formaldehyde in feed. The use of organic acids in water (Dibner and Buttin, 2002) and organic
acids and formaldehyde in feed reduces the concentration of Salmonella in the water, and also
reduces the risk of contamination of feed post-heat treatment (Davies and Hinton, 2000).
It was noted that the effects of organic acids in feed are not apparent until the treated feed
has been consumed by the bird and wetted in the crop.
The experimental results of bacteriocin controls for Salmonella looked very promising, but
there had been no published field trials, so the experts considered it too early to recommend it as
an effective intervention in a commercial setting. Also, the experimental results for
bacteriophage therapy for Salmonella looked very promising, but there had been no published
field trials. There were commercial companies investigating this, but it was too early to
recommend it as an effective intervention in a commercial setting (Atterbury et al., 2007).
Research into genetic resistance to Salmonella colonization showed that this had some
effectiveness, but it was not a viable, cost-effective option in the near future (Wigley et al.,
2006).
 Salmonella and Campylobacter in chicken meat 15

There had been limited experimental success for Salmonella control using immuno-
stimulators, but it was still too early to give a recommendation as to whether this could be used
as an effective intervention in a commercial setting.
The Experts furthermore stated that antimicrobials do decrease Salmonella concentration
both in the gut and systemically, but that it would not always completely eliminate
contamination. They should not be used as a Salmonella control measure in breeders except for
salvaging valuable genetic lines, due to the risk of development of resistant Salmonella strains.
In such cases, it should be followed by a CE product to restore the micro flora (Goren, 1993;
Reynolds, 1997).
Negative air ionization had been demonstrated in research to be effective in reducing the
level of Salmonella in the air in breeder houses, but it had not yet been applied successfully in a
commercial setting.
There were many commercially available treatments to acidify the litter. Research had
shown that short-term reduction in bacterial populations could be achieved. It appeared to have
a limited long-term effect. The experts were not aware of any current commercial use for
Salmonella control.

Step 2: Transport eggs to hatchery

For Salmonella: Egg trolleys should be cleaned and sanitized before use. They should be stored in an
enclosed storage area.
Vehicles used for transporting eggs should preferably be dedicated for that purpose. The driver should,
on arrival, wear protective clothing, use the boot dips provided and should not enter any livestock
buildings.
Eggs from each flock should be packed into separate trays and should be identifiable. Egg trays should
be labelled with the appropriate flock code and date.
Only eggs from Salmonella-negative flocks should be sent for incubation. When this is not feasible
eggs from Salmonella-positive flocks should be transported well separated from eggs from negative
flocks. Codex draft Guidelines
The Experts were in agreement with the appropriateness of the above guidance; however
they noted that although it is common practice to use foot dips they are not always effective,
especially in the presence of organic matter. This organic matter can result in inactivation of the
disinfectant and subsequent boots can become contaminated with Salmonella. It might be better
to suggest a change of footwear when entering the house (Amass et al., 2000).

Step 3: Parent hatchery

For Salmonella: The control measures as described at Step 1 also apply at this Step where relevant to a
hatchery.
Each setter or hatcher should only contain eggs from one flock.
If possible, only eggs from Salmonella-negative flocks should be incubated as it has been scientifically
demonstrated that only one Salmonella-contaminated egg can contaminate all eggs and newly hatched
chicks within a hatching cabinet.
Where the use of eggs from flocks that are known to be contaminated is unavoidable, they should be
kept separate and hatched separately from eggs from other flocks. Trace-back of infection to the
contaminated breeding flocks should be performed and control measures should be reviewed.
Sampling programmes for detection of Salmonella, including testing dead chicks, chicken fluff,
meconium and shells, should be in place. Codex draft Guidelines
16 Examples of specific possible interventions for hazard reduction

The Experts suggested revising the text so that the types of samples listed were shown as
options rather than inclusive, this meaning that at least one of the listed options should be used
to monitor for Salmonella from the hatchery.
UV irradiation of hatching eggs has been very effective for Salmonella control under
experimental conditions as a way to sterilize the surface of the egg. There is no commercial
application as yet, probably due to staff safety issues and the negative effect on plastics.
Air sanitation in hatchers using ozone, hydrogen peroxide and phenol is effective
experimentally against Salmonella, but commercial use is limited due to other practical
concerns. Formaldehyde is still commonly used as long as staff precautions are taken.

Step 4: Transport day-old chicks to parent farm

For Salmonella: Personnel should follow the same hygiene routine as for collection of hatching eggs.
Transport of day-old chicks should be in vehicles or containers preferably used only for that purpose.
Chicks should be traceable to a hatchery. The driver should not enter any livestock buildings.
Codex draft Guidelines

Step 5: Manage parent flocks

For Salmonella: The control measures described at Step 1 apply at this Step.
Codex draft Guidelines

Step 6: Transport eggs to hatchery

For Salmonella: The control measures described at Step 2 apply at this Step.
Codex draft Guidelines

Step 7: Hatchery
For Salmonella: The control measures described at Step 3 apply at this Step.
Codex draft Guidelines
The Experts considered that the guidance provided is Steps 4 – 7 was appropriate given the
current knowledge base, and had no further additions or comments.

Step 8: Transport day-old chicks to grower sheds

For Salmonella: The control measures described at Step 4 apply at this Step.
Codex draft Guidelines
While the Experts were in agreement that the guidance provided was appropriate they also
highlighted the need to address traceability from breeder farms to hatchery.

Step 9: Manage chickens

The control measures described at Step 1, where relevant to growing farms, apply at this Step.
Unusually high levels of mortality or morbidity should be investigated.
Stand down periods for personnel are advisable during which there is no contact with birds of any
type. Personnel protective clothing should be under the control of the company.
Any equipment that must be taken into a shed should be cleaned and sanitized beforehand (this
includes equipment used for repairs and maintenance).
 Salmonella and Campylobacter in chicken meat 17

Pest control programmes should be used outside sheds and inside the annex as necessary. Specific
pests such as flies and litter beetles should be controlled to the highest level practicable. Where
practicable, fly-screens may be useful in reducing the prevalence of Campylobacter or Salmonella
contamination in flocks. Doors should be kept closed.
Sheds should be single purpose - single species operations, and ideally an all-in all-out single-age-
group principle should be adopted. Where several flocks are maintained on one farm, the individual
flocks should be managed as separate epidemiological units.
Where there is a detection of pathogen-positive flocks, control measures applied at processing should
be considered, e.g. heat treatment or freezing of chicken meat derived from positive flocks to reduce
the concentration of Salmonella and/or Campylobacter.
For Salmonella: Feed and water additives have been used (alone or in combination with competitive
exclusion) in experimental or very limited commercial settings to reduce colonization of the chickens.
A Competent Authority may need to validate such measures in the national setting before advocating
their use. Codex draft Guidelines
While agreeing on the appropriateness of the above guidance, the Experts noted that
mortality during the first two weeks could be indicative of Salmonella infection from the
breeder farms. Furthermore, the Experts were concerned at the possible effect of litter moisture
on Salmonella (Eriksson et al., 2001) but considered this to be appropriately covered under the
OIE text.
It was the opinion of the Experts that the guideline was light on biosecurity measures.
However, they found that biosecurity was appropriately covered by the OIE codes, especially
for:
• cleaning and disinfection of houses, their immediate surrounds and other areas of the
farm that might present a reservoir for Salmonella or Campylobacter;
• staff, visitor and catchers’ clothing;
• vehicle parking, and disinfection if necessary to enter farm; and
• restriction on equipment shared between houses.
For Salmonella: Competitive exclusion treatments may reduce Salmonella flock prevalence by up to
70–85% or more. Codex draft Guidelines
While the Experts were in agreement with the intent of the above guidance on the utility of
competitive exclusion, it was considered that it would benefit from greater clarity in terms of the
efficacy of such a treatment and suggested a more appropriate statement would be “Competitive
exclusion may reduce the prevalence of Salmonella-positive flocks and / or levels of intestinal
colonisation, but the extent of any reduction can vary”. Furthermore it was advised that CE be
administered after antimicrobials are used for treatment of other diseases, to restore the normal
gut flora (Smith and Tucker, 1975).
In addition to the GHP measures mentioned above, the meeting considered other potential
interventions for implementation during broiler growing in terms of their potential practical
utility in reducing Campylobacter and Salmonella. The outcome of these deliberations is
documented below.
Several potential Campylobacter vaccines had been tested but the results were poorly
reproducible. Obviously, new approaches were needed to develop effective vaccines. The
opinion of the Experts was that it would take many years before a commercial vaccine would be
available. There were live vaccines that could be used to control Salmonella in broilers, but
these had not proven to be effective commercially.
18 Examples of specific possible interventions for hazard reduction

Experimental studies on CE for control of Campylobacter showed contradictory results:

some of them claimed effectiveness while others did not. Furthermore, the Experts raised the
concern that there might be an under-reporting of studies showing no effect. Currently there was
little evidence that CE would work against Campylobacter, and to the current knowledge of the
Experts there was no expectation that products used against Campylobacter would be developed
in the near future.
Organic acids appeared to be a promising feed or water additive for control of
Campylobacter. However, large-scale field trials had yet to be performed to assess effectiveness
on-farm. Other substances (e.g. monocaprin and caprylic acid, some enzymes and egg yolk
powder) did not give reproducible results. The Experts concluded that the effect of these
required field trials.
For Salmonella control, there were numerous feed and water additives that had been
successful when used experimentally. At the time of writing these were not used commercially,
with the exception of organic acids in pre-slaughter drinking water, and organic acids or
formaldehyde in feed. The organic acids in pre-slaughter drinking water have been shown
experimentally to decrease Salmonella concentration in crop and caeca, which may result in
lower contamination on the carcass. The use of organic acids or formaldehyde in feed reduces
the concentration of Salmonella in the feed and reduces the risk of post-heat-treatment
contamination (Dibner and Buttin, 2002).
Bacteriocins are substances produced by bacteria, having anti-bacterial activity against
specific other bacterial species. One research group reported promising results using these
peptides against Campylobacter (Stern et al., 1995). There is an Intellectual Property dimension
to these findings (i.e. patents). To the meeting's knowledge, only experimental data had been
published. The studies to date looked very promising, but on-farm trials were needed to
investigate efficacy and reproducibility under commercial conditions.
Experimental results for Salmonella control looked very promising, but on-farm studies had
yet to be published, so it was too early to recommend it as an effective intervention in a
commercial setting.
Bacteriophages are viruses able to kill specific bacterial species. Experimental studies from
different research groups have shown the effectiveness on Campylobacter and Salmonella. Due
to their short-term effect, the application would be limited to a small time window just before
slaughter. There is only proof of principle, and on-farm studies had not yet been performed.
Practical application might be hampered by lack of broad-host phages, resistance and
environmental contamination issues. Phage therapy was promising, but development and
application of a commercial product would need much extensive research (Atterbury et al.,
2007)
There had been limited experimental success for control of Campylobacter or Salmonella
using immunostimulators, but it was too early to recommend it as an effective intervention in a
commercial setting.
There was no role for the use of antimicrobials in the control of Campylobacter. First,
because of the issue of the threat of increasing antimicrobial resistance and hence the need for
restricted use, and, second, because of the impossibility of practical application with regard to
residues (when treatment is close to slaughter) and re-infection when the withdrawal period is
respected.
The opinion of the Experts was that antimicrobials decrease Salmonella concentration in the
gut and systemically, but would not always completely eliminate contamination. It should not
be used as a Salmonella control measure in broilers.
 Salmonella and Campylobacter in chicken meat 19

Housing conditions and biosecurity are a form of prevention, controlling the introduction of
infectious agents by use of hygiene measures, for example. Increasing biosecurity has
definitively a role in the prevention of Campylobacter colonization of broilers. However,
quantifying the effect is difficult and most probably dependent on regional and seasonal
differences. In northern European countries (e.g. Denmark, Iceland) there is a strong suggestion
that improvement of biosecurity resulted in a reduction of Campylobacter prevalence. However,
control groups are lacking. The effect of specific measures such as fly-screens has been reported
from Denmark, and is very promising. The effect of this approach in other geographical areas
(e.g. other climates or ventilation systems) should be confirmed.
In the meeting's opinion, biosecurity had a (major) role to play in the reduction of the
prevalence of Campylobacter and Salmonella, but quantitative prediction of the effect was
difficult to ascertain.
Although various litter treatments had been used in experimental trials, in the case of
Campylobacter there appeared to be no reduction of microbial load on the final product. The
conclusion of the Experts was that there was insufficient evidence that this approach would be
effective.
There are many commercially available treatments to acidify the litter. Research has shown
that short-term reduction in bacterial populations can be achieved. It appears to have a limited
long-term effect. The Experts were not aware of any commercial use for Salmonella control.

Step 10: Depopulate (full or partial)

Full depopulation should be carried out where possible. Where this is not practicable and partial
depopulation is practised, particular attention should be paid to strict biosecurity and general hygiene.
This includes the prior cleaning of equipment such as transport vehicles and their tyres, forklifts,
pallets/modules, catcher’s boots, and transport crates. It is preferable that sheds being partially
depopulated are scheduled for catching prior to those being fully depopulated on the same day. This
may assist in minimizing contamination of remaining birds. Catching crews should adopt good
biosecurity practices and facilities should be provided to enable them to do so.
When feed withdrawal is practised, water additives such as lactic acid that may lower post-harvest
crop contamination may be considered. Codex draft Guidelines
The Experts were in agreement with the appropriateness of the above guidance.
An agreed microbiological testing regime followed by scheduled slaughter (with positive
flocks being processed separately or after negative flocks to reduce cross-contamination) or sent
for further treatment post-slaughter will significantly reduce the microbial load and/or the
prevalence on the carcass. Sampling should be carried out as close to slaughter as possible,
taking into account the time for results to be available. This can only be done for
Campylobacter if the flock prevalence is sufficiently low (EFSA, 2009).

Step 11: Transport to slaughterhouse

Stress to live birds increases shedding of Salmonella and Campylobacter and should be minimized
during transport by:
- Giving each bird sufficient space to rest and stand up without restriction.
- Protecting birds from undue fluctuations in temperature, humidity or air pressure.
- Sheltering birds from extremes of weather.
All live bird transport vehicles, crates, modules and associated equipment should:
- Be designed, constructed and maintained to allow effective cleaning.
20 Examples of specific possible interventions for hazard reduction

- Be effectively washed and sanitized, away from processing and bird holding areas so as to minimize
cross-contamination, and be visibly clean.
- Be dried if practical and achievable before use in the case of crates and modules.
Codex draft Guidelines
While agreeing with the appropriateness of the above guidance, the Experts suggested that
air velocity may be a more fitting term to use than air pressure.

4.2 Processing
4.2.1 Handling of crates and pre-scalding
Information on flocks presented for slaughter should be provided in a timely manner to enable optimal
slaughter and processing procedures. Supplier statements or supplier guarantees covering information
on flock health, e.g. relating to the use of veterinary drugs or ante-mortem inspection results, should be
required upon receipt of flocks and any other materials received by the slaughterhouse.
Stress to birds should be minimized, e.g. by dim lighting, minimal handling and avoiding delays in
processing. Information on flocks presented for slaughter should be provided in a timely manner to
enable optimal slaughter and processing procedures
For Salmonella: If flocks are known positive for Salmonella, they should be presented for slaughter in
a manner that minimizes cross-contamination to known negative flocks, e.g. by slaughtering them at
the end of the day, or all on one day and preferably the last day(s) of the week. Codex draft Guidelines
While agreeing with the intent and to a large extent the appropriateness of the above
guidance, the Experts considered the section on supplier statements or guarantees might not be
necessary.
Furthermore, emphasis is put on the importance of scheduling based on information on feed
withdrawal period, due to its impact on the level of carcass contamination during slaughter.
Thus slaughtering flocks 8 to 12 hours after feed withdrawal will reduce likelihood of
contamination of carcasses by faecal material and\or ingesta. Flock information should include
details on feed withdrawal period for appropriate scheduling purposes (Northcutt, Savage and
Vest, 1997; Wabeck, 1972, 1992; Warriss et al., 2004).
Step 13: Ante-mortem inspection
Moribund, unhealthy or otherwise unsuitable poultry should not be processed.
Where numbers of birds that are dead on arrival, moribund, unhealthy or otherwise unsuitable for
processing exceed expected levels, the processor should notify the relevant responsible person, e.g. the
farmer, veterinarian, catcher or transportation company, so that appropriate preventative and/or
corrective action can be taken. Codex draft Guidelines
The Experts considered that the guidance provided was appropriate given the current
knowledge base, and had no further additions or comments.
Step 14: Slaughter
Where practicable, known positive flocks may be diverted for specific processing and/or treatment
according to national food safety policies.
Measures should be taken to minimize bird stress at hanging, e.g. use of blue light, breast comforter,
suitable line speed.
Bleeding should be substantially completed before scalding in order to prevent inhalation of scald
water and to reduce the amount of blood entering the scalder. Codex draft Guidelines
 Salmonella and Campylobacter in chicken meat 21

While agreeing with the appropriateness of the above guidance, the Experts highlighted that
minimizing stress at hanging applied only to live hanging-on operations, and did not cover, for
example, controlled atmosphere stunning/killing.
Step 15: Dress
So as to minimize contamination4 of carcasses, control measures can include:
– Washing at key process steps to minimize attachment of Campylobacter and Salmonella to
carcasses.5
– Trimming, to minimize visible contamination.
– Other approved chemical6 and physical methods.
These methods can be applied alone or in combination at different process steps during processing.
Where re-hang of carcasses is necessary, it is preferable that this is done mechanically so as to reduce
cross-contamination.
All birds which drop on the floor should be condemned, or reprocessed under specific conditions as
determined by the Competent Authority. Any dropped products should trigger corrective actions as
appropriate. Codex draft Guidelines
Washing at key process steps will reduce contamination by Campylobacter and Salmonella,
but the Experts disagreed that this applied specifically to attachment. Trimming, washing or
other measures applied to minimize visible contamination with faecal materials or ingesta on
carcasses should be initiated by inspection, be it visual or automated inspection, which is
becoming more common practice in industry.

4.2.2 Scalding, de-feathering and evisceration

Contamination during scalding can be minimized by:
– the use of counter-current flow;
– addition of as much fresh water as possible;
– having the scald temperature as high as possible to minimize levels of Campylobacter and
Salmonella; and
– use of approved7 chemicals, e.g. pH regulators.
Other factors that should be taken into account when designing process control systems that minimize
contamination during scalding include:
– degree of agitation;
– use of multi-staged tanks;
– pre-scald brush and wash systems;
– raising the temperature of scald tanks to 70°C at breaks;
– tanks being emptied and cleaned at end of a processing period; and
– hygiene measures applied to re-used/recycled water. Codex draft Guidelines

4. Decontamination of carcasses will probably reduce, but not eliminate Salmonella and Campylobacter
bacteria on broiler carcasses and broiler meat.
5. Washing with water alone may achieve a decrease in Campylobacter and Salmonella but has little
effect on cells attached to the carcass surface. Further, the extent of the decrease may depend on the
efficacy of previous washes.
6. Chemical decontaminants should be approved by the Competent Authority.
7. Processing aids should be approved by the Competent Authority.
22 Examples of specific possible interventions for hazard reduction

Addition of as much fresh water as possible is a vague statement, and also counteracts water
conservation measures by industry. It was suggested that the process should instead be specified
as: High flow rates of water with adequate agitation. Raising the temperature of scald tanks at
breaks is a sound measure, but various temperatures are applied in the industry according to
plant, company and region. So the specific recommendation of 70°C is too rigorous, but could
be used as an example. It should be clear that the purpose is to raise water temperature high
enough for a long enough time to kill Salmonella and Campylobacter in the scalders.
Cross-contamination at de-feathering can be minimized by:
– guarantee of appropriate fasting of birds prior to slaughter;
– prevention of feather build-up on equipment;
– continuous rinsing of equipment and carcasses;
– regular adjustment and maintenance of equipment;
– particular attention to cleaning moving parts; and
– regular replacement of plucker fingers. Codex draft Guidelines
While agreeing with the appropriateness of the above guidance the Experts noted that the
first bullet was already covered under Step 12 Receipt at slaughterhouse. Furthermore the
importance of appropriate feed withdrawal time for impact on carcass contamination should be
stressed.

4.2.3 Head pulling

Head pulling should be carried out in such a manner that leakage from the crop is prevented. Heads
should be pulled downwards to reduce contamination due to crop rupture. Codex draft Guidelines

4.2.4 Evisceration
Rupture of the viscera and spread of faeces can be minimized by:
– limiting size variation in batches so that birds of similar size are processed together; and
– careful adjustment and regular maintenance of machinery. Codex draft Guidelines
The Experts considered that the guidance provided on head pulling and eviceration was
appropriate given the current knowledge base, and had no further additions or comments
4.2.5 Crop removal
Where possible, crops should be extracted in a manner that is likely to reduce/limit carcass
contamination. Codex draft Guidelines
The Experts found that there was no scientific evidence supporting the statement that
specific methods for the removal of the crop would reduce carcass contamination.

4.2.6 Decontamination (washing)

Washing/rinsing with abundant potable water may be sufficient to reduce cross-contamination with
Campylobacter and Salmonella. Codex draft Guidelines
The Experts questioned the use of the word sufficient, considering that there was not an
established level for cross-contamination reduction. It was suggested that “may assist in
reducing” might be more appropriate. Also, the group suggested the word contamination to
replace cross-contamination. In addition, it was the opinion of the group that this was a GHP
measure rather than a specific control measure.
 Salmonella and Campylobacter in chicken meat 23

Chlorination of water used for carcass washing, e.g. 25 ppm, has been shown to reduce
Campylobacter levels on skin by 0.5 log10 cfu/g. Codex draft Guidelines
The Experts questioned whether the reported reduction is due to presence of chlorine in the
wash water. The draft report of the FAO/WHO Expert Consultation on the benefits and risks of
the use of chlorine-containing disinfectants in food production and food processing (See
Appendix) noted that the removal of pathogenic bacteria from poultry carcasses during physical
washing procedures on an industrial scale is predominantly a feature of the physical action of
the water rather than the use of hypochlorite in the water.8"
Dipping of carcasses in solutions containing processing aids, e.g. 10% solution of trisodium phosphate
(TSP) at pH 12 for 15 seconds, has been shown to reduce Campylobacter levels on skin by up to 1.7
log10 cfu/g. Codex draft Guidelines
It was the opinion of the Experts that references to the use of TSP should be removed from
the document, considering that TSP was rarely used in commercial poultry processing. Some
arguments include the negative environmental impacts of phosphates and the counteracting
effect of the alkaline compound on the effectiveness of chlorine in chillers, e.g. chlorine
performs better in pH lower than 7 (Smart, 2009).
For Salmonella: Multiple-sequential washing steps have been shown to reduce the Salmonella
incidence on broiler carcasses by 40 to 90%, the proportion depending on number and nature of
washing interventions. Codex draft Guidelines
It was the opinion of the Experts that the quoted 40 to 90% was overly optimistic. However,
between 4 to 8% reductions were reported in the same document for each individual washer. In
two other studies, Lillard (1989, 1990) (discussed in the Appendix) showed that reductions from
sequential washing steps are not additive, since limited effects of sequential washings were
obtained.
The experts recommended that the Codex working group refer to reductions at individual
steps when redrafting the document.
On-line reprocessing of contaminated carcasses using TSP can significantly reduce the presence of
Salmonella, with some reports of almost 100% of carcasses being test negative.
Codex draft Guidelines
It was the opinion of the Experts that references to the use of TSP should be removed from
the document, considering that TSP was rarely used in commercial poultry processing.
Step 16: Inside/outside body wash
It was the view of the experts that On-line reprocessing should be dealt with as a subset of
washing.
The inside and outside of all carcasses should be thoroughly washed, using pressure sufficient to
remove visible contamination. Appropriate equipment should be used to ensure direct water contact
with the carcass. Codex draft Guidelines
The Experts were in agreement with the appropriateness of the above guidance but noted that
in commercial practice, the physical force needed to remove visible contaminants may be aided
by the use of brushing apparatus installed in line with the inside/outside body wash (IOBW).

8. The report of the Expert meeting on the benefits and risks of the use of chlorine-containing
disinfectants in food production and food processing is being finalized and minor wording changes
may occur during technical editing.
24 Examples of specific possible interventions for hazard reduction

For Campylobacter: Washing systems. Using water alone has been shown to reduce levels of
Campylobacter by up to 0.5 log10 cfu/ml of whole carcass rinse sample.1) Codex draft Guidelines
This statement is incorrect according to the reference cited as it includes 3 sequential
washings with 25 ppm chlorinated water.
Use of an inside/outside wash followed by an on-line spray system incorporating a processing aid, e.g.
acidified sodium chlorite (ASC) and citric acid9, has been shown to reduce Campylobacter in the
whole carcass rinse sample by 1.7 log10 cfu/ml.
1)
Washing systems using TSP or ASC may further reduce average Campylobacter levels by 1.0 log10
cfu/ml of whole carcass rinse sample. Codex draft Guidelines
As noted previously it was the opinion of the expert meeting that references to the use of
TSP should be removed from the document, considering that TSP was rarely used in
commercial poultry processing. Further, it was suggested to review the second sentence as
footnote 1) was incorrectly placed according to the literature provided. The sentence belongs to
the previous section.
The Experts found that the reference to 1.7 log10 reduction is not correct, and this statement
should be reviewed by the Codex working group.
For Salmonella: Use of an inside/outside wash, including processing aids as desired has been shown to
reduce Salmonella-positive carcases by up to 60%. Codex draft Guidelines
The Experts suggested revising the statement to include conditions of application and
specific agents to support it.
Inside/outside washing using a spray application of 20–50 ppm chlorinated water may reduce the
prevalence of Salmonella-positive broiler carcasses by 20%. A second inside/outside washing
following immediately upon the first may result in a further 25% reduction. Codex draft Guidelines
In the opinion of the Experts a new section should be added to include practices known as
On-line reprocessing (OLR) to replace the above paragraph.
To clarify the OLR process: it occurs that in certain areas of the world an additional washing
step has been added following the Inside/Outside Body Wash (IOBW). This has been
designated as "On-line reprocessing" and, where permitted by National Authorities, this may be
used in lieu of trimming or washing off-line as a remediation for faecal or ingesta contamination.
The concept was described by Blankenship et al. (1993). Kemp et al. (2001) demonstrated a
better level of microbial control than that provided by Off-line reprocessing when using ASC in
OLR.
Hazard-specific control for Salmonella: Unpublished data were presented to and accepted by
the Expert Group that validated the use of ASC (750 ppm, pH ~2.5, spray application) in an
OLR application. In plant trials, reductions in Salmonella prevalence from 48% to zero and 56%
to zero were achieved (Bernard and Natrajan, pers. comm.). Another unpublished data
submission indicated 18.4% reductions of Salmonella prevalence by the use of ASC spray
washes at 700–900 ppm, pH ~2.5 (Sanchez-Plata, pers. comm.).
Step 17: Postmortem inspection
Line speeds should be appropriate for effective post mortem inspection of carcasses for visible
contamination, organoleptic defects and relevant gross pathology.
Codex draft Guidelines

9. Reported specifications are: 15-second on-line spray system incorporating ASC at 1100 ppm and
citric acid at 9000 ppm giving a pH of 2.5 at 14–18ºC.
 Salmonella and Campylobacter in chicken meat 25

The Experts were in agreement with the appropriateness of the above and had no further
additions or comments.

4.2.7 Chilling
Poultry meat should be chilled as quickly as possible to limit the growth of microorganisms on the
carcass.10 Chemicals that may be added to the chiller water should be approved by the Competent
Authority and include, among others: Codex draft Guidelines
The Experts suggested that the footnote at this stage needs to be deleted because conditions
of application affect the performance of chlorination. Without specifying the conditions of use,
the reference is incomplete.
– Chlorine
– Chlorine dioxide and other chlorine derivatives (in the form of sodium-hypochlorite, calcium
hypochlorite tablets or chlorine gas or electrolytically generated hypochlorous acid) – TSP
– Organic acids (e.g. lactic acid). Codex draft Guidelines
The Experts suggested revision of the list of actual organic acids, to include citric acid,
which is more frequently used commercially. See previous comments about TSP used in
commercial settings.
4.2.7.1 Air Chilling
Prior to air chilling, carcasses may be sprayed or dipped, e.g. chlorinated water, lactic acid or TSP, to
assist cooling.
During air chilling, carcasses may be sprayed with chlorinated water, lactic acid or TSP to assist
cooling and reduce the level of contamination. Spraying cabinets should be installed in downflow
chilling tunnels. Codex draft Guidelines
The Experts recommended the deletion of the two above paragraphs as there was no
evidence to indicate that the use of water sprays, with or without chemicals, had a beneficial
effect, and could be in fact detrimental. Added water sprays are likely to retain enough moisture
during the storage to allow for survival of Campylobacter and withstand the drying process of
the chiller (Mead et al., 2000; Allen et al., 2000a, b, 2007).
The Experts did recognize that the process of air chilling, in the reduction of the carcass
temperature, would minimize the likely growth of Salmonella if present. The meeting asked the
CCFH working group to consider the findings of the Joint FAO/WHO Expert meeting on the
benefits and risks of the use of chlorine-containing disinfectants in food production and food
processing (FAO/WHO, 2008)
4.2.7.2 Immersion Chilling
Water (including recirculated water) should be potable and the chilling system may comprise one or
more tanks. Chilled water can be used or ice may be added to it. Water flow should be counter-current
and may be agitated to assist cooling.
Immersion chilling of carcasses should incorporate:
– total available chlorine maintained at 50–70 ppm, and available free chlorine maintained at 0.4–5.0
ppm; and
– pH maintained at 6.0–6.5.

10. The time necessary to eliminate Salmonella or Campylobacter in the chiller water increases with
decreasing free available chlorine, e.g. it takes 120 minutes to eliminate both organisms at 10 ppm but
only 6 minutes at 50 ppm total available chlorine.
26 Examples of specific possible interventions for hazard reduction

Following chilling, any excess water should be allowed to drain away from the carcasses to minimize
cross-contamination of carcasses at subsequent steps in the processing chain.
Codex draft Guidelines
The Experts disagreed that chlorine should always be used with immersion chilling. Where
necessary for control of Salmonella and Campylobacter, processing aids (e.g. chlorine
compounds, acidulants and other approved agents) may be considered.
It was the opinion of the Experts that the GHP as written was too prescriptive and parameters
should be validated in the particular circumstances (See Appendix).
For Campylobacter: Air chilling may significantly reduce numbers of Campylobacter depending on
chilling rate and humidity.11 Codex draft Guidelines
Forced air chilling (Blast chilling) can be a hazard control measure for Campylobacter due to
the drying out of the surface. The Experts recommended that this paragraph be moved to a new,
hazard-based control section within air chilling.
For Salmonella: Immersion chilling using water with antimicrobial agents may decrease the
prevalence of Salmonella-contaminated carcasses by up to 50%. Codex draft Guidelines
The subgroup did not find substantiation for the stated reduction and suggested removing "by
up to 50%" from the statement.
The Experts spent much time discussing the role of processing aids in reducing the levels of
contamination with Salmonella and Campylobacter on broilers during the immersion chilling
operation. To support the discussion, the draft report of the Joint FAO/WHO Expert meeting on
the benefits and risks of the use of chlorine-containing disinfectants in food production and food
processing (FAO/WHO, 2008) were used in addition to other relevant references and personal
comments.
The Experts did not reach agreement on the necessity for use of processing aids for control
of Salmonella and Campylobacter on broilers during the chilling process.
Points were brought forward in support of the use of chlorine or other derivatives as
inactivating agents in the chiller, but questions remained as to whether the noted effects were
the result of the chlorine or the physical removal of contaminants by washing.
There was general agreement among the experts that the addition of chlorine at a level
sufficient to maintain a residual in the water would inactivate pathogens washed off during the
chilling process, preventing re-attachment and cross-contamination.
The point of controversy remains whether the use of chlorine in the chill tank does or does
not act as a decontaminating agent by acting directly on the surface of contaminated carcasses.
The same applies to application of processing aids during what has been referred to earlier as
OLR.
For Campylobacter and Salmonella: A pre-chill 15-second spray or 5- to 8-second immersion dip in
acidified ASC has been shown to reduce Campylobacter and Salmonella on poultry carcasses by
greater than 2 log10 cfu per ml of whole carcass rinse sample. Reductions of 2.6 log10 cfu per ml of
whole carcass rinse sample can be achieved if the spray or dip is preceded by a freshwater wash.
Codex draft Guidelines
This statement describes a processing step related to the previous section; there is no chilling
done at this stage and it should be considered in the IOBW or OLR section.

11. Campylobacter spp. are relatively sensitive to drying and low humidity and die as a result of
desiccation of the carcass surface.
 Salmonella and Campylobacter in chicken meat 27

Use of an 8 to 12% solution of TSP in pre- or post-chiller baths has been shown to reduce
Campylobacter and Salmonella by 1 to 2 log10 cfu per ml of whole carcass rinse sample.
Codex draft Guidelines
As noted previously it was the opinion of the expert meeting that references to the use of
TSP should be removed from the document, considering that TSP was rarely used in
commercial poultry processing.
For Campylobacter: Immersing whole carcasses in ASC immediately after the chiller has been shown
to reduce Campylobacter by 2.6 log10 cfu/ml of whole carcass rinse sample.12 In other commercial
applications, ASC applied by dipping carcasses after exiting a screw chiller has been shown to reduce
the prevalence of contaminated carcasses by up to 80%.
Codex draft Guidelines
These interventions should be considered as Post-Chill applications. The Codex working
group should consider placing this as a separate section in the revised document.
In addition, the Experts asked the Codex working group to go back to the original references,
as the citations in terms of reported Log reduction for Campylobacter were incorrect.
For Salmonella: Use of chlorine dioxide in chiller water at a level of 5 ppm (0.5–1.0 free residual
chlorine dioxide) may reduce Salmonella on broiler carcasses by 2 log10 cfu per ml of whole carcass
rinse sample. Codex draft Guidelines
The Experts noted that there was no such thing as free residual chlorine dioxide; it should be
free residual chlorine.
The following hazard-specific control measure should go into the post-chill section.
Unpublished data were presented to and accepted by the Expert Group that the use of ASC
(750 ppm, pH ~2.5, immersion dip, post-chill application) in a plant trial gave a reduction in
Salmonella prevalence from 16% to zero (Bernard and Natrajan, pers. comm.). Another
unpublished data submission indicated 15–25% reduction in Salmonella prevalence by the use
of a chlorine dioxide generating system applied as a dip at 5 ppm post-chill (Sanchez-Plata, pers.
comm.).
Chilled carcasses should be held in temperature controlled environments and processed as soon as
possible, or with the addition of ice to minimize the growth of Campylobacter and Salmonella.
Codex draft Guidelines
The Experts suggested that the reference to Campylobacter should be removed, as
Campylobacter will not grow below 32°C (ICMSF, 1996).
The Experts considered that the addition of the following hazard-based control section for
Campylobacter was necessary as a consequence of recent published information:
"For Campylobacter: Crust freezing using continuous CO2 belt freezing of portions, skinless
breast fillets, provided a reduction in Campylobacter of 0.42 Log (Boysen and Rosenquist,
2009). The effect of crust freezing of whole birds on reducing Campylobacter is supported
by work carried out by Corry et al. (2003)."
Step 20: Pack
Chilled carcasses should be held in temperature-controlled environments and processed as soon as
possible, or with the addition of ice to minimize the growth of Campylobacter and Salmonella.

12. Reported specifications are: Immersion of whole carcasses in 600 to 800 ppm ASC at pH 2.5 to
2.7 for 15 seconds.
28 Examples of specific possible interventions for hazard reduction

Care should be taken when packaging to minimize external contamination of the pack. Leakproof
packaging, where possible, should be leakproof. Codex draft Guidelines
The Experts suggested that the reference to Campylobacter should be removed as
Campylobacter will not grow below 32°C (ICMSF 1996).
The Experts agreed that minimizing cross-contamination was an important aspect of
packaging and could be achieved in several ways, e.g. leakproof packaging or absorbent pads.
However, it was not advocated that leakproof packaging should be applied in all situations.
For Campylobacter: If modified atmosphere packs are used, the atmosphere chosen should not
enhance the survival of Campylobacter. Codex draft Guidelines
A high oxygen concentration (70%) reduced the survival of Campylobacter during chilled
storage by 2.0 to 2.6 Log over 8 days of storage (Boysen, Knøchel and Rosenquist, 2007). The
Experts recommended that the Codex working group consider this as a hazard-based control
option. As this is being drafted, the Codex working group should take care that new measures
do not create other hazards.
For Salmonella: Products should at all times be stored at temperatures preventing growth of
Salmonella.13 Codex draft Guidelines
While scientifically correct, the Experts considered that this text should be moved to Section
9.11 of the Codex draft Guidelines as it refers to storage.
For Campylobacter and Salmonella: Gamma rays or electron beams14 applied to warm, chilled, or
frozen carcasses has been shown to be effective at eliminating Campylobacter and Salmonella. Where
permitted, irradiation levels should be approved by the Competent Authority. Radiation at doses of 3–
5 kGy for frozen poultry and 1.5–2.5 kGy for chilled poultry has been shown to eliminate Salmonella
and Campylobacter. Codex draft Guidelines
The Experts noted that a range of doses had been reported, and should therefore be validated
in the particular situation.
Step 21: Chill/freeze
Measures based on GHP are provided in the Code of Hygienic Practice for Meat, CAC/RCP 58-2005
[CAC, 2005] with further guidance in the International Code of Practice for the Processing and
Handling of Quick Frozen Foods, CAC/RCP 8-1976, Rev. 2-2008 [CAC, 2008].
Codex draft Guidelines
It was considered that such general statements should be included in the introduction to the
draft document.
For Campylobacter: Freezing of naturally contaminated carcasses followed by 31 days of storage at -
20°C has been shown to reduce Campylobacter by 0.65 to 2.87 log10 cfu/g.
Codex draft Guidelines
The Experts agreed with the note that freezing will reduce Campylobacter contamination
(Rosenquist et al., 2006).

4.2.8 Storage
Measures based on GHP are provided in the Code of Hygienic Practice for Meat, CAC/RCP 58-2005
[CAC, 2005] with further guidance in the International Code of Practice for the Processing and
Handling of Quick Frozen Foods, CAC/RCP 8-1976, Rev. 2-2008 [CAC, 2008].

13.Packaging in modified atmosphere does not prevent growth of Salmonella if temperature abuse occurs.
14. Refer to Codex Standard 106-1983, Rev. 1-2003, General Standard for Irradiated Foods.
 Salmonella and Campylobacter in chicken meat 29

Codex draft Guidelines

It was considered that this was a general statement rather than specific guidance and should
go in the introduction to the draft document.
For Salmonella: Products should at all times be stored at temperatures preventing growth of
Salmonella.15 Codex draft Guidelines
The Experts agreed with the appropriateness of the guidance that products should be stored
below temperatures allowing growth of Salmonella. The Experts could not agree on the need for
application of this criterion at all times. Growth is time and temperature dependent; there are
disagreements as to the exact temperatures to prevent growth, as well as questions regarding the
impact of short periods at higher temperatures (Ingham et al., 2004).

4.3 Distribution, handling and preparation

4.3.1 Temperature control
The requirements for temperature control during transportation and storage of the product are
covered adequately by the Code of Hygienic Practice for Meat, CAC/RCP 58-2005 (CAC,
2005).
In relation to cooking of raw chicken, the NACMCF (2007) review specifies that cooking to
a minimum internal temperature of 74°C will give a 7 log10 reduction in Salmonella and a
50 log10 reduction in Campylobacter. However, the data available to the Experts for both
pathogens was based on extrapolation of data from lower temperatures and different kinds of
meat. Nevertheless, it should be noted that ready-to-eat meat and poultry products sampled at
manufacturing plants for regulatory compliance during 2001 and 2002 yielded only 23 samples
positive for salmonellae in over 14 000 tested (Dreyfuss et al., 2007) using the mentioned
temperature of 74°C.
For Campylobacter, there is published data on fried chicken breast (Bergsma et al., 2007)
and unpublished data on Campylobacter and Salmonella on chicken breast fillets showing
unusual heat resistance. It was the opinion of the Experts that further work was needed to verify
this. Commercial cooking practices following the guidelines in the document have a proven
performance history of minimizing the risk of Salmonella and Campylobacter. However, studies
on home cooking practices were not definitive at that time.
Factors that could affect heat resistance, such as: presence of chemical additives; size and
conformation of the product; type of cooking process; water activity; fat content; and pH, must
be taken into account to establish a heat regime. The variable nature of survival curves is
recognized in the FAO/WHO document (FAO/WHO, 2002).
4.3.2 Cross-contamination
The requirements for meat handling at retail, as specified in the Codex Draft guidelines Section
10.4.1.1) were acceptable. In relation to food service operators, it was recommended that
hygiene measures should be aimed at minimizing cross-contamination between raw chicken and
hands, contact surfaces and utensils, but should prevent contamination of other foods.
Information to consumers on food safety requirements given by the CCFH Guidelines should
also be channelled through relevant national media.

15.Packaging in modified atmosphere does not prevent growth of Salmonella if temperature abuse occurs.
30 Examples of specific possible interventions for hazard reduction

4.4 Identification of data gaps

Main data gaps for primary production were:
• Salmonella and Campylobacter prevalence information was available for some countries
worldwide, but many of these studies gave limited details of study design.
• Data were limited or missing from most countries in Africa, Asia, Latin America and the
Caribbean.
• There were very limited data on the concentration of Salmonella on positive birds.
• The effect on Salmonella and Campylobacter prevalence and concentration of specific risk
reduction interventions needs to be evaluated.
Main data gaps for processing were:
• Quantitative data were limited for several steps of processing.
• There was limited information on processing practices used in different countries.
• Many studies were old; more recent information on changes in prevalence and numbers
would be beneficial.
Main data gaps for cooking and handling were:
• Quantitative data regarding cooking practices and handling are needed.
• Systematic investigations are needed of the prevalence or level of contamination in this step.
 5. Evaluation of likely outcomes of specific
interventions

5.1 Step 1: Depopulate and transport to slaughterhouse

5.1.1 Salmonella and Campylobacter
The Experts found that there were no current quantified effects on prevalence or level of
contamination of Salmonella and Campylobacter on broiler carcasses, and that the effect of any
interventions made in the primary production stage had not been validated in a commercial
setting. Therefore the evaluation of likely outcomes would not be measured as a reduction in
prevalence or level of contamination, but have instead to be considered as a GHP, as described
in Section 4.1, above. As mentioned in Section 4.4, Data gaps, there was a need for these
measures to be quantified in order to consider these interventions as hazard reductions.
5.2 Step 2: Scalding, de-feathering and evisceration
5.2.1 Salmonella and Campylobacter
The measures mentioned in the Codex draft Guideline were found to cover the step adequately.
No further data or interventions were presented at the Technical Meeting, and the interventions
mentioned in the Codex draft Guidelines were not qualitative in regards to measuring the effect
before and after the intervention.
5.3 Step 3: Washing and chilling
5.3.1 Salmonella
A study (Stopforth et al., 2007) showed 4–8% reduction in connection with sequential washing
steps. However two other studies by Lillard (1989, 1990) (see Appendix) showed that
reductions from sequential washing steps are not additive, since limited effects were obtained
from sequential washings.
Furthermore, there was a documented effect of up to 100% when dipping the carcass in
solutions containing a 10% solution of TSP at pH 12 for 15 seconds (Codex draft Guidelines).
Unpublished data were presented and validated at the FAO/WHO Technical Meeting,
concerning the use of ASC (750 ppm, pH~2.5 spray application) in an OLR application. In plant
trials, the reduction was a decrease the prevalence from 48% or 56% to zero. Additional
unpublished data showed reductions of 18.4% in Salmonella prevalence by the use of ASC
spray wash (700–900 ppm, pH ~2.5).
ASC can also be used as a pre-chill 15-second spray washing or a 4–8-second immersion dip,
which has shown to reduce Salmonella on poultry carcasses by more than 2 log10 cfu/ml of
whole carcass rinse sample. If this is preceded by a freshwater wash, reduction can be increased
to 2.6 log10 cfu/ml whole carcass rinse sample.
The use of air chilling can minimize the growth of Salmonella if present, possibly due to a
reduction in the carcass temperature. In the case of water chilling, use of chlorine in the water at
a level of 5 ppm may reduce the Salmonella on broiler carcasses by 2 log10 cfu/ml whole-
carcass rinse sample.
Additional data were presented at the Technical Meeting, showing a reduction in Salmonella
prevalence from 16% to 0% when using ASC (750 ppm, pH ~2.5, immersion dip, post-chill
32 Evaluation of likely outcomes of specific interventions

application) (Bernard and Natrajan, pers. comm.), and a 15–25% reduction in Salmonella
prevalence by the use of a chlorine dioxide generating system applied as a dip at 5 ppm post
chill (Sanchez-Plata, pers. comm.).
5.3.2 Campylobacter
Campylobacter prevalence will be reduced by each individual wash step. Chlorinating the wash
water, e.g. 25 ppm, has been shown to reduce Campylobacter levels on skin by 0.5 log10 cfu/g.
Campylobacter levels on the carcass can be reduced by a pre-chill 15-second spray washing or
4–8-second immersion dip. Reductions for Campylobacter can be up to 2 log10 cfu/ml of whole-
carcass rinse sample, and 2.6 log10 cfu/ml whole-carcass rinse sample if the spray is preceded by
a freshwater wash.
Forced air chilling can also be a hazard reducing control measure for Campylobacter due to
the drying out of the surface. This measure can reduce Campylobacter by 0.4 log10 cfu/g.
Besides the abovementioned interventions, new studies have shown that crust freezing using
CO2 as mentioned in Chapter 4 could reduce Campylobacter by 0.42 log10/g (Boysen and
Rosenquist, 2009; Corry et al., 2003)
5.4 Step 4: Storage, retail and consumer handling
5.4.1 Salmonella
Cooking to a minimum internal temperature of 74°C will give a 7 log10 reduction in Salmonella.
5.4.2 Campylobacter
No specific hazard reducing measures have been described in the Codex draft Guidelines
regarding this step, but the Experts recommended the Codex working group to consider a study
showing that the use of high oxygen concentration (70%) reduced the survival of
Campylobacter during chilled storage by 2.0 to 2.6 log10 over 8 days of storage (Boysen,
Knøchel and Rosenquist, 2007). Also, freezing followed by 31 days of storage at -20°C has
shown to have a reducing effect on Campylobacter prevalence in naturally contaminated
carcasses (by 0.65 to 2.87 log10 cfu/g) (Codex draft Guidelines).
Cooking to a minimum internal temperature of 74°C has shown to give a 7 log10 reduction in
Campylobacter.
6. Development of a Web-based risk-management
tool

6.1 Background
In response to the risk-management questions posed by CCFH, the primary application of a
risk-management decision tool would be to demonstrate in a simplified manner the proportional
effect of different control measures, either alone or in combination, on likely reductions in
foodborne illness. This should allow countries to evaluate combinations of control measures by
applying a risk-based approach. This decision tool should also be of considerable benefit to
industry in designing HACCP plans.
Requested features of the web-based tool specified by CCFH were:
• simplified modelling of risks associated with final product without selected interventions;
• simplified modelling of risks associated with final product with selected interventions;
• comparison of different food chain scenarios;
• the proportionality of risk reduction associated with various control measures; and
• modelling of “what-if” scenarios.
In order to meet this request, an electronic discussion group was formed by FAO/WHO prior
to the Technical Meeting. The aim of this e-group was to discuss the possibilities for
development of a prototype user-friendly risk-assessment tool for Salmonella and
Campylobacter in chicken meat. While the technology exists to develop these tools, there are a
number of questions to be addressed in relation to their scope and limitations, functionality and
performance.
Specifically, the following questions were considered by the electronic discussion group:
• Is this really a feasible list of requirements?
• How "simplified" would such a tool have to be to meet these requirements, and would it
ultimately still have a value?
• Should we be considering this as one unique tool covering the whole chain, or a series of tools
that focus on one segment of the chain, e.g. one for production, one for processing, etc., which
may or may not be linked?
Based on discussions in the electronic discussion group, the following were put forward at
the Technical Meeting:
• It is a feasible list of requirements.
• The level of simplification required and appropriate is still under consideration.
• The tool will consist of one unique tool.
• The tool will deal only with industrial processing.
• There are many existing detailed and complex risk assessment models (e.g. FAO,
Netherlands, UK, Canada).
• The goal for this tool is to create a user friendly risk-management tool suitable for use via the
Web.
34 Development of a Web-based risk management tool

• The model should be developed in such a manner so as to:

– Enable users to input initial contamination levels at a common starting point.
– Allow exploration of various assumptions about what happens during evisceration and
chilling (and other specific steps to be named).
– Provide default values for certain interventions.
– Allow the user to override these with their own data or assumptions.
– Provide only relative risk reduction compared to a baseline scenario.
– Allow the user to compare or rank the effectiveness of different intervention options.
6.1.1 Examples of existing tools
Two recently developed Web-based tools were briefly introduced to the group.
• Food Standards Agency (FSA) Slaughterhouse Hygiene Assessment Tool.
• FAO/WHO (JEMRA) Risk Assessment for Cronobacter spp. in Powdered Infant Formula
Tool.
6.1.1.1 Food Standards Agency (FSA) Slaughterhouse Hygiene Assessment Tool
The tool would be used to record measures in place to control Salmonella and Campylobacter
from farm to carcass chill. It was developed by the FSA in consultation with the United
Kingdom industry, to be used by United Kingdom poultry processors as a self audit. The tool
was still in development, and only a limited example was seen by the group. The tool sets
specific questions at each process step and the user had a choice of possible interventions. The
questions were based on interventions for which there is literature support for controlling
Salmonella and/or Campylobacter. The scores given for each answer reflect the degree of
control. The total score for each set of questions within a section are multiplied by a “stage
multiplier”. The value of the multiplier is a reflection of the degree of risk at that step. Access
through the Web would be linked directly to literature that supports each intervention, when the
tool came online.
6.1.1.2 FAO/WHO (JEMRA) Risk Assessment for Cronobacter spp. in Powdered Infant
Formula
This is an online risk assessment tool. The tool explicitly examines the impact of different
preparation and handling strategies on Cronobacter spp. in Powdered Infant Formula (PIF) and
describes the outputs in terms of the relative risk posed to infants. In addition to explicitly
considering the preparation and handling of PIF, it provides tools to explore the possible impact
of microbiological criteria through the specification of sampling plans for Cronobacter spp in
PIF. The microbiological criteria can be explored in isolation or in combination with the
preparation and handling tools to determine the impacts upon risk.
Users enter parameters such as concentration values, preparation and handling, and sampling
plan information. The tool then uses a risk assessment model to produce a report showing the
relative risk of the scenarios provided.
The tool is publicly available at www.mramodels.org/esak.
6.1.2 Prototype tool for a Campylobacter/Salmonella Web-based tool
An early prototype was presented to the experts for the purpose of generating discussion. The
prototype included a few sample processing steps with options to input initial concentration and
prevalence levels, identify process changes such as growth and cross-contamination, and
introduce interventions.
The main features demonstrated by the prototype tool were:
 Salmonella and Campylobacter in chicken meat 35

• a user friendly interface (Web-based) for the end user; and

• a user friendly model development tool for the risk modeller.
The user would have the option to use default data, where available, based on the CCFH
document and other literature. The user could also override those inputs with their own data.
The software then uses those inputs to produce a risk-based report.
The prototype tool models changes in concentration and prevalence during processing. It
currently starts after de-feathering, but this could be changed if found appropriate. The final
concentration is used to compute two doses: one considering the interventions selected and a
baseline dose assuming no interventions. These doses were applied to a dose-response model.
The relative risk reduction between the result with interventions and without interventions is
reported back to the user, as well as the mean concentration and prevalence values at each step.
Comments from individual experts on what the model developers should consider in the
further development of the prototype tool included the following:
• It should make recommendations on sampling schemes and microbiological methods for
users to determine input data so that inputs are comparable between users.
• The model should start further up the chain (e.g. pre-harvest) to expand the choices of
management options.
• The model should be expanded to include consumer handling (e.g. cooking, cross-
contamination).
• Have the model account for interactions between applying multiple interventions (synergistic,
antagonistic, reduced effectiveness).
• The model should account for cross-contamination.
• The model should account for multiple flocks (e.g. cross-contamination between flocks).
• The implication of uneven carcass size within a flock should be considered.
• The model should account for the use of different scalding procedures.
• Different products should be included – e.g. cut-up products.
The following concerns from individual experts were raised:
• Who will be using the model? Will it be used by industry, government, and/or risk managers,
and for what purpose?
• Which questions will the tool ask the users in order to provide input to the model?
• There is currently a lack of data (e.g. concentration data for Salmonella) to fill into the model.
Would this prevent the tool from being usefully used?
• How will the model be validated?
• There is currently no consensus model on which to build the tool.
• Will the tool be updated as new information becomes available?
• It is difficult to rely on one model covering all plants with all the different machinery and
GHPs in place.
• The Campylobacter issue is much more complicated than the Cronobacter spp issue, thus the
model will be more complicated.
• Could the model be used for comparisons between countries?
• Different serovars may require different dose-response models.
36 Development of a Web-based risk management tool

Mechanisms by which to address some of these concerns include the following:

• The tool will provide default data, which can be used if the user has no data of their own. The
data will be based on the best available information.
• The same dose response model will be used for all Salmonella serovars. Statistically, there are
no differences between dose response models for different Salmonella serovars.
• Using relative risk makes the influence of the dose response less important.
• The model will be designed to compare different scenarios. Countries can add input data
sampled for different situations, such as climate.
• The tool can be updated with new information when available and models can be adjusted if
necessary.
6.2 Suitability of outputs of the meeting for the prototype tool
development
The Experts agreed that the prototype tool was feasible and that the work on further
development of a prototype should continue, based on the following arguments:
• We need this kind of tool for risk-based management.
• There are potential users, both governments and stakeholders. For developing countries, the
tool would also be of value. It can be used to train industry and government at the same time
used to encourage discussion of risk management.
• The tool will help countries that have targets or market demands, to explore which
interventions could be applied.
• The tool might help with trade situations by providing a common framework.
• The tool will be useful for ranking the effectiveness of interventions.
• The tool will be useful for exploring the combining effects of interventions.
• A model is never complete as is it always a simplification that uses science, assumptions and
expert opinions, but it is the best that can be provided to assist management decisions.
Countries cannot do experiments with all interventions and so models are useful to help
evaluate interventions.
• The model captures the best consensus knowledge on the processes and the interventions.
Next steps:
• A prototype tool will be delivered to the CCFH working group through the JEMRA process.
• The current version of the prototype tool will be expanded to start at the entry to slaughter and
include all processing steps described in the Codex draft guidelines. It will allow for the
hazard-based controls agreed upon in the CCFH document and other hazard-based controls
compatible with the model to be compared for their impact on relative risk reduction.
• The modellers need to consider
– how to model microbiological effects that may occur at each step (e.g. cross-
contamination, growth, and inactivation);
– how to model synergistic, antagonistic and reduced effectiveness of multiple
interventions; and
– can an effective model for Salmonella be developed using only prevalence data?
Salmonella and Campylobacter in chicken meat 37

• The prototype requires inputs for initial carcass-level contamination (Log cfu/carcass);
between-flock prevalence; and within-flock prevalence. The modellers will not provide
guidance on determining those inputs from sample data.
• The prototype should provide estimated default values for microbiological effects (e.g. Log
reduction; cross-contamination during scalding) for the prototype to assist the evaluation of
the model.
• Evaluation of the scientific data of baseline values and other interventions not currently
included as hazard-based controls should be determined by subject-matter experts, and should
not be the responsibility of the modellers.
• Model development will require interaction with risk managers and subsequent peer review.
 7. Summarized considerations of CCFH request
In response to the request made by the CCFH to FAO/WHO, this chapter summarizes
considerations agreed on by the invited experts during the Joint FAO/WHO Technical Meeting
on Salmonella and Campylobacter in chicken meat.
Independent assessment and review of available scientific information on
control measures
• Relevant literature was reviewed in Chapter 3. The information received as a response to the
call for data preceding the Technical Meeting was of critical value for this report, with
additional references provided by the experts attending the meeting.
Evaluate quantitative aspects of hazards reduction in terms of prevalence and
concentration (specific interventions)
• The Experts evaluated and commented on the interventions identified in the Codex draft
Guidelines. In Chapter 4, more interventions were added where data were available. These
should not be considered as standalone interventions, and not all of the mentioned
interventions will be effective for both pathogens.
Primary production
• The Experts considered the control measures mentioned in the primary production part of the
production chain to be a part of GHP. Additional measures were added, but the group
emphasized that the impact of these must be further investigated in order to quantify their
effect.
Additional measures
• Increased pest control.
• Treatment of drinking water.
• Sanitation of eggs.
• Biosecurity measures.
• Culling of Salmonella-positive flocks.
• Heat treatment of feed.
• Vaccination.
• Probiotics.
• Competitive exclusion (CE).
• Feed and water additives.
• Bacteriocins.
• Bacteriophages.
• Negative air ionization.
• UV irradiation of hatching eggs.
• Scheduled slaughter.
Processing
The following measures were proposed as additional interventions to the CCFH document:
• Use of ASC (acidified sodium chlorite) in On-line reprocessing (OLR).
40 Summarized considerations of CCFH request

• Air chilling as a measure to reduce carcass temperature.*

• Forced air chilling (Blast chilling).*
• Crust freezing.
• High oxygen concentration during chilled storage.
NOTE: * Effective for Campylobacter due to drying, but not effective for Salmonella reduction.
Distribution and Preparation
• No additional hazard reducing measures were mentioned during the Technical Meeting, but
the Experts stated that further studies were needed in order to determine the effect of heat
treatment and home cooking practices.
• Some specific interventions could not be executed in all regions due to legislation differences.
With regard to this, see Appendix concerning washing with water and use of chemical
additives.
Evaluate likely outcomes in terms of hazard reductions in the commercial setting
• The outcomes of the specific interventions have been mentioned in regard to their scientific
validity and their quantitative effect on level of contamination and prevalence. The repetition
of these can be found as Chapter 5, above.
Assess the feasibility of developing a Web-based risk-management decision-
support tool
• The Web-based risk-management tool was discussed by the Experts, and was found to be
feasible. A subgroup was formed to help the developers of the Web-based tool regarding the
limitations and the modelling, and aspects of developing this prototype tool were discussed.
The Experts agreed on the terms described in Chapter 6. The subgroup was to work with the
tool developers on the production of the prototype Web-based tool, and this work was to be
presented at the next CCFH meeting.
Develop a framework and identify data needs for the Web-based risk-
management decision-support tool
• Prior to the Technical Meeting, a subgroup of experts was invited to participate in a Web
discussion forum set up by the JEMRA Secretariat. This forum was used prior to the meeting
to discuss both feasibility and the advantages and limitations of such a tool. During the
Technical Meeting this subgroup of experts continued their work on the terms of
development. After the decision in plenum that the prototype tool was found to be feasible,
this subgroup continued their work on the development of the model and the Web tool. The
electronic discussion forum will remain one possible way of communication, but e-mail will
also be used as a means of communication. The data needs to develop a prototype Web-based
tool have been described in Section 4.4, above.
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 Salmonella and Campylobacter in chicken meat 43

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 APPENDIX
The draft report of the Joint FAO/WHO Expert meeting on the benefits and risks of the use of
chlorine-containing disinfectants in food production and food processing. (Ann Arbor, USA,
27–30 May 2008) was made available to the Technical Meeting to facilitate its discussion, in
addition to other relevant references and comments from the experts attending the meeting. The
text below reflects the outcome of the discussions during the current Technical Meeting, taking
into account information from the expert meeting on the use of chlorine-containing disinfectants.

1. On use of chlorine, from FAO/WHO Consultation

Washing with hypochlorite
Industrial studies by Stopforth et al. (2007) and Villarreal, Baker and Regenstein (1990)
demonstrated an effect of washing carcasses in hypochlorite solution on the prevalence of
Salmonella. However, other studies (Northcutt et al., 2005; Yang, Li and Johnson, 2001)
showed that washing in water alone resulted in most of the reductions in Salmonella on poultry.
Therefore, it is not possible to make a definitive statement on the effectiveness of hypochlorite
against Salmonella during carcass washing on an industrial scale based on these studies. It is
likely that washing in water alone is a moderately effective intervention and that hypochlorite
does not provide a significant additional effect.
Laboratory based experiments have shown reductions in Campylobacter on carcasses of less
than 2 Log units but only over extended washing times (up to 30 min). Other experiments using
more practical conditions show reductions of less than 1 Log unit on Campylobacter in
comparison with no washing. However, when compared to washing in water alone there was no
additional effect on Campylobacter for carcasses washed in water with hypochlorite (Northcutt
et al., 2005). Therefore, as with Salmonella, it is likely that washing in water alone is a
moderately effective intervention and that hypochlorite does not provide a significant additional
effect.
Summary Statement
The removal of pathogenic bacteria from poultry carcasses during physical washing procedures
on an industrial scale is predominantly a feature of the physical action of the water rather than
the use of hypochlorite in the water.
References cited
Stopforth. J.D., O’Connor, R., Lopes, M., Kottapalli, B., Hill, W.E. & Sampadpour, M. 2007. Validation
of individual and multiple-sequential interventions for reduction of microbial populations during
processing of poultry carcasses and parts. Journal of Food Protection, 70(6): 1393–1401.
Villarreal, M.E., Baker, R.C. & Regenstein J.M. 1990. The incidence of Salmonella on poultry carcasses
following the use of slow release chlorine dioxide (Alcide). Journal of Food Protection, 55(6): 465–
467.
Northcutt, J.K., Smith, D.P., Musgrove, K.D., Ingram, K.D. & Hinton, A. Jr. 2005. Microbiological
impact of spray washing broiler carcasses using different chlorine concentrations and water
temperatures. Poultry Science, 84: 1648–1652.
Yang, H., Li, Y. & Johnson. M.G. 2001. Survival and death of Salmonella Typhimurium and
Campylobacter jejuni in processing water and on chicken skin during poultry scalding and chilling.
Journal of Food Protection, 64(6): 770–776.
46 Appendix

2. Hypochlorite in carcass chillers

Hypochlorite is routinely used in poultry process lines in countries where chilling by water
immersion is allowed. It is added to the chill water to prevent the build up of bacteria in the
water during processing.
Studies evaluating the numbers of Salmonella on carcasses before and after chilling are few.
However, Russell and Axitall (2005) noted a reduction in Salmonella numbers per carcass
caused by the physical movement of carcasses in the chiller tank rather than the presence of
hypochlorite in the chiller water. Overall the studies show that if chlorine is not present in
chiller water then the prevalence of Salmonella increases on carcasses because of cross-
contamination. Lillard (1980) also showed that the prevalence of Salmonella in chiller water
treated with chlorine at 20 ppm and 34 ppm was reduced from 41.7% (untreated water) to
17.3% and ‘not detected’, respectively. Yang, Li and Johnson (2001) and Stopforth et al. (2007)
demonstrated the effectiveness of chlorine in killing Salmonella in chill water, but not on
carcasses.
The effects of chlorinated chill water on Campylobacter seemed to be greater than the effect
on Salmonella, but reports are inconsistent. Small reductions in both numbers and prevalence of
Campylobacter on carcasses were observed when chill water was chlorinated. In a 2004 study
by Bashor et al. a reduction in Campylobacter of 0.13 log10 cfu/carcass was achieved after
chilling in water with 25 ppm chlorine, and the prevalence of Campylobacter positive carcasses
was reduced from 80% post-wash to 73.3% post-chill. In a second plant, using a chill tank with
a higher level of chlorinated water, at 35 ppm, a reduction in Campylobacter of 0.25 log10
cfu/carcass was observed after chilling. The prevalence of Campylobacter-positive carcasses
was reduced from 80% post-wash to 70% post-chill.
In another study on naturally contaminated poultry in a commercial plant, a chiller with
chlorinated water resulted in a Campylobacter reduction of 1.09 log10 cfu/carcass (statistically
significant) and 1.3 log10 cfu/carcass (statistically significant) in two experiments. Prevalence of
Campylobacter-contaminated carcasses was not affected in the first experiment, but reduced
from 95% to 77.5% in the second experiment (Oyarzabal et al., 2004). However no un-
chlorinated water chill controls were evaluated.
The effect of chlorine in chill water on the death kinetics of inoculated Campylobacter jejuni
was studied on chicken skin (Yang, Li and Johnson, 2001). Chilling in chlorinated water with
50 ppm added chlorine (20–30 ppm residual chlorine) resulted in inactivation rate of
Campylobacter on skin of D-value 73 minutes. However, using older chill water initially with
50 ppm chlorine, where organic material had built up, the residual concentration of free chlorine
was approximately zero. Chilling in this water resulted in a D-value for Campylobacter on
chicken skin of 344.8 minutes. A similar result was seen with Salmonella, confirming the need
to maintain residual chlorine levels in chill water during processing. However, Yang, Li and
Johnson (2001) showed that chlorine was effective at killing Campylobacter in chill water, but
did not examine the effect this might have had on prevalence.
Summary Statement
The use of chlorine in the chill tank may not act as a decontaminating agent by acting directly
on the contaminated carcass; however, there would be a washing-off effect by the water itself,
and the addition of chlorine at a level sufficient to maintain a free residual in the water would
then inactivate pathogens washed off, preventing re-attachment and cross-contamination.
 Salmonella and Campylobacter in chicken meat 47

References cited
Bashor, M.P., Curtis, P.A., Keener, K.M., Sheldon, B.W., Kathariou, S. & Osborne, J.A. 2004. Effects of
carcass washers on Campylobacter contamination in large broiler processing plants. Poultry Science,
83: 1232–1239.
Lillard, H.S. 1980. Effect on broiler carcasses and water of treating chiller water with chlorine and
chlorine dioxide. Poultry Science, 59: 1761–1766.
Oyarzabal, O.A., Hawk, C., Bilgili, S.F., Warf, C.C. & Kemp, G.K. 2004. Effects of postchill application
of acidified sodium chlorite to control Campylobacter spp. and Escherichia coli on commercial
broiler carcasses. Journal of Food Protection, 67(10): 2288–2291.
Russell, S.M. & Axitall, S.P. 2005. Monochloramine versus sodium hypochlorite as antimicrobial agents
for reducing populations of bacteria on broiler carcasses. Journal of Food Protection, 68(4): 758–763.
Stopforth, J.D., O’Connor, R., Lopes, M., Kottapalli, B., Hill, W.E. & Sampadpour, M. 2007. Validation
of individual and multiple-sequential interventions for reduction of microbial populations during
processing of poultry carcasses and parts. Journal of Food Protection, 70(6): 1393–1401.
Yang, H., Li, Y. & Johnson. M.G. 2001. Survival and death of Salmonella Typhimurium and
Campylobacter jejuni in processing water and on chicken skin during poultry scalding and chilling.
Journal of Food Protection, 64(6): 770–776.
48 Appendix

3. Summary of expert subgroup discussion on use of chlorine

The following scientific discussion was in relation to Section 9.7.1.2 of the proposed draft
Guidelines for Control of Campylobacter and Salmonella spp. in Chicken Meat, where it states:
“Immersion chilling of carcasses should incorporate: Total available chlorine maintained at 50–
70 ppm, available free chlorine maintained at 0.4–5.0 ppm, and pH maintained at 6.0–6.5.”
Immersion chilling of carcasses is believed to result in limiting cross-contamination and/or
reduction of pathogens if managed properly. However, a scientific discussion developed around
the following: Is there scientific evidence supporting whether the observed reduction was due to
water alone (dilution, removal of loosely attached organisms) or due to the addition of chlorine
(bactericidal, decreased re-attachment/cross-contamination of bacteria) in the chiller?
The draft report of the Joint FAO/WHO Expert meeting on the benefits and risks of the use
of chlorine-containing disinfectants in food production and food processing [in preparation]
supports that chlorine has a measurable benefit when used in the immersion chilling process.
The extent of any effect of chlorine may depend on the precise condition of chilling16.
The scientific basis for reduction due to chlorine is as follows: Chlorine is bactericidal and
functions as a strong oxidizing agent. When in contact with bacteria, cell damage occurs at
many sites. Chlorine is most effective when there is a measurable quantity of free available
chlorine (FAC) to convert to its most active form. However, chlorine readily reacts with organic
matter, which may partly result in a high concentration of combined available chlorine,
especially during operations such as the immersion chilling process. During processing of
broilers, significant amounts of organic matter are introduced and chlorine will need to be
continually added to the chillers otherwise no FAC will be available. Furthermore, the reaction
resulting in production of FAC is favoured by a pH below 7.0. As the pH of the solution is
reduced below 7, the reaction is driven further in the direction of production of FAC as long as
the chlorine in solution is not already organically bound. The reaction toward FAC can also be
driven through higher concentrations of chlorine. If the immersion chiller is maintained to have
free and combined available chlorine and the pH is adequately controlled, it is the scientific
view of this expert panel that chlorine use will be optimized as a bacteriocide that will inactivate
both Salmonella and Campylobacter. The number of cells inactivated and the rate of
inactivation depends on several factors, including the FAC content, contact time, temperature,
and probably other factors not completely defined.
The supporting literature is the draft report of the Joint FAO/WHO Expert meeting on the
benefits and risks of the use of chlorine-containing disinfectants in food production and food
processing [in preparation]16.
Alternatively, removal of bacteria, including pathogens, in the immersion chiller may be due
to physical removal of bacteria by water, a dilution effect, and/or flow rate that decreases the
opportunity for attachment/re-attachment (cross-contamination). Therefore, antimicrobials, such
as chlorine, may not be needed in the immersion chiller to achieve a low level of pathogens in
the birds exiting the chiller. It is the scientific evaluation of this expert panel that water alone in
the immersion chiller can reduce pathogen(s) levels on the carcass, but without the aid of an
intervention designed to inactivate planktonic bacteria, including Campylobacter and
Salmonella, cross contamination will be a concern. In this case, the removal of pathogens from

16. The report of the Expert meeting on the benefits and risks of the use of chlorine-containing
disinfectants in food production and food processing is being finalized and minor wording changes
may occur during technical editing.
 Salmonella and Campylobacter in chicken meat 49

chicken carcasses and the minimization of cross-contamination will depend on a sufficiently

high water flow rate.
The supporting literature is listed below. In a pilot plant, Buhr et al. (2005) state that the
water alone in the immersion chiller results in a Campylobacter reduction of 1.9 log10 and
addition of chlorine had no additional effect.
Annotated bibliography
Buhr, R.J., Bourassa, D.V., Northcutt, J.K., Hinton, A. Jr., Ingram, K.D. & Carson, J.A. 2005. Processing,
products and food safety. Bacteria recovery from genetically feathered and featherless broiler
carcasses after immersion chilling. Poultry Science, 84: 1499–1504.
Lillard, H.S. 1989. Incidence and recovery of salmonellae and other bacteria from commercially
processed poultry carcasses at selected pre-evisceration and post-evisceration steps. Journal of Food
protection, 52: 88–91.
NOTE: This paper discusses the use of decontamination agents against salmonella.
Lillard, H.S. 1990. The impact of commercial processing procedures on the bacterial contamination and
cross-contamination of broiler carcasses. Journal of Food Protection, 53(3): 202–204.
NOTE: This paper discusses the use of continuous washes (up to 40) on attached bacteria on carcass
surfaces.
McMeekin T.A., Thomas, C.J. and Pennington P.I. 1984. Contamination and decontamination of poultry
carcass neck tissue. Journal of Food Safety, 6(2): 79–88.
NOTE: This paper discusses attachment of pathogens on chicken skin and the challenges of removal by
washing only.
 FAO/WHO MICROBIOLOGICAL RISK ASSESSMENT SERIES

1 Risk assessments of Salmonella in eggs and broiler chickens: Interpretative Summary, 2002

2 Risk assessments of Salmonella in eggs and broiler chickens, 2002

3 Hazard characterization for pathogens in food and water: Guidelines, 2003

4 Risk assessment of Listeria monocytogenes in ready-to-eat foods: Interpretative Summary,

2004
5 Risk assessment of Listeria monocytogenes in ready-to-eat foods: Technical Report, 2004

6 Enterobacter sakazakii and microorganisms in powdered infant formula: Meeting Report,

2004
7 Exposure assessment of microbiological hazards in food: Guidelines, 2008

8 Risk assessment of Vibrio vulnificus in raw oysters: Interpretative Summary and Technical
Report, 2005
9 Risk assessment of choleragenic Vibrio cholerae 01 and 0139 in warm-water shrimp in
international trade: Interpretative Summary and Technical Report, 2005
10 Enterobacter sakazakii and Salmonella in powdered infant formula: Meeting Report, 2006

11 Risk assessment of Campylobacter spp. in broiler chickens: Interpretative Summary, 2009

12 Risk assessment of Campylobacter spp. in broiler chickens: Technical Report, 2009

13 Viruses in food: Scientific Advice to Support Risk Management Activities: Meeting Report, 2008

14 Microbiological hazards in fresh leafy vegetables and herbs: Meeting Report, 2008

15 Enterobacter sakazakii (Cronobacter spp.) in powdered follow-up formula: Meeting Report, 2008

16 Risk assessment of Vibrio parahaemolyticus in seafood: Interpretative Summary and Technical

Report, 2009
17 Risk characterization of microbiological hazards in food: Guidelines, 2009.

18 Enterohaemorragic Escherichia coli in meat and meat products: Meeting report. 2009

19 Salmonella and Campylobacter in chicken meat: Meeting Report. 2009