This document provides an overview of control measures for Salmonella and Campylobacter in poultry production in the EU and USA. It notes that these bacteria are leading causes of foodborne illness, with poultry implicated as a primary source. Control involves identifying transmission routes, monitoring prevalence data, and evaluating measures. International bodies provide guidance focusing on biosecurity during production and slaughter. Independent scientific bodies advise governments, who establish national control systems based on these recommendations. While regulatory approaches have similarities, differences exist in specific controls implemented. This review aims to compare EU and US control mechanisms.

1. University College of Dublin
A comparison of the control measures targeting Salmonella and Campylobacter in poultry
in the European Union and the USA
Case Study
Supervisors – Dr. Pippa Haughton, Dr. Patrick O’Mahony and Dr. Cormac
Murphy
25th
of August 2015
“I confirm that I have reviewed the UCD policy on Plagiarism and that the work submitted is
my own, except where indicated. I also understand that my work may be checked for
plagiarism and that any false claims for this work will be dealt with in accordance with
University regulations”
James Britton
BIOC40120
MSc Biotechnology, SBBS
James Britton

2. Contents:
Summary……………………………………………………………………………………………………………………….….…1
1. Introduction..……………………………………………………………….……………………………………….………2-7
1.1 Zoonoses and Zoonotic Disease………………..…………………………………………………………………….2
1.2 The Importance of Poultry…………………………………………………………………………………………..2-4
1.3 Salmonella and Salmonellosis……………………………………………………………………….…………….5-5
1.4 Campylobacter and Campylobacteriosis……………………………….……………………….…………….5-7
2. Materials and Methods……………………………………………………………………………………………………8
3. Results………………………………………….…………………………………………………………………………….9-37
3.1 Control of Food Safety ……………………………………………………………………………………….…....9-12
3.1.1 International Food Safety …………………………………………….…………………….………………….9-10
3.1.2 European Food Safety…………………………………………………………………………………….…....10-11
3.1.3 US Food Safety………………………………………….……………………………………………….…………11-12
3.2. Control of Salmonella and Campylobacter in live Poultry………………………….…………...12-17
3.2.1 Sampling and Monitoring………………………………………………………………………….……………….14
3.2.2 Biosecurity……………………………………………………………………………………………………………15-17
3.3 Control during poultry primary production……………………………………………………………..17-35
3.3.1 Feed and water treatment……………………………………………………………………………………17-18

3. 3.3.2 Vaccination…………………………………………………………………………………………………………..19-24
3.3.3 Antimicrobials, Resistance and Monitoring………………………………………..…………………24-35
3.3.4 Competitive Exclusion……………………………………………………………………..…………………………35
3.4 Control during slaughter…………………………………………………………………………………….……36-37
3.4.1 Decontamination.................................................................................................…...36-37
4. Discussion……………………………………………………………………..……………………………………….…38-41
5. Acknowledgements……………………………………………………………………………………………………….42
6. References……………………………………………………………………………………………………………..…43-51

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Summary:
Zoonotic infections are those in which the causative agent is readily transmissible between
animals and humans. Salmonella and Campylobacter are two of the leading causes of
bacterial zoonotic infection in the western world causing an estimated 1.2 and 1.3 million
respective cases per year in the US alone (CDC, 2015). Poultry and poultry related products
have been noted as one of the primary sources of these pathogens for human infection
(WHO, 2009). In order to limit their public health impact, several major steps must be taken.
These include identifying sources and transmission routes, collection and sharing of
prevalence and epidemiological data and evaluation of potential control measures. This
scientific information feeds into developing best practice guidance and legislation. Both
guidance and legislation serve to assist with the control of zoonoses in the EU and the USA.
For example, international bodies such as the world organisation for animal health (OIE) and
the Codex Alimentarius Commission (CAC) have set guideline standards for the control of
these pathogens in poultry. These guidelines focus heavily on biosecurity as a means to
control Salmonella and Campylobacter including precautions for feed and water, the use of
competitive exclusion agents, vaccination and the responsible use of antimicrobials. Control
of zoonotic agents is also assisted by, independent scientific bodies who provide impartial
scientific advice to the governments of respective regions. The legislative bodies may base
their regulations and recommendations on the opinion of the scientific bodies to form
national control systems. While aspects of regulatory systems in the EU and US are similar,
differences do exist in specific control measures. These differences have led to an
interesting situation wherein we may compare and contrast the control mechanisms used in
both countries, that is the aim of this review.

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1. Introduction:
1.1 Zoonosis and Zoonotic diseases
Zoonotic diseases are those which can be readily transmitted between animals and Humans.
There are currently in the region of 1,500 human pathogens and it is estimated that over
60% of these can be transmitted from animals to humans (Cantas and Suer, 2014). Zoonotic
agents can be bacterial, viral, fungal or parasitic in origin. The most common transmission
routes of zoonotic agents from animals to humans are through the ingestion of
contaminated food or water or contact with animals or animal faeces. Advancements in
surveillance, monitoring, diagnostics and control measures have considerably reduced the
public health impact of zoonotic infections in many developed countries, however, they
remain a significant public health risk. Changing practices in farming, food production,
eating habits and other societal behaviour led to increased levels of human salmonellosis
and campylobacteriosis in the EU and US which have, in the last decade, been brought
under control due to the control measures and regulations implemented.
1.2 The Importance of Poultry
Between 1995 and 2005 the global production of primary poultry products (meat and eggs)
increased rapidly with production of chicken meat rising 53% and chicken eggs rising 39%
(Scanes, 2007). Chicken meat production in the EU and US rose 38% and 30% respectively
from 1995 – 2005 (Scanes, 2007). This trend has continued and in 2013 the US processed 8.6
billion chickens resulting in 17.4 million tonnes of chicken meat and 79 billion eggs being
produced (Institute, 2015, Poultry.net, 2014). Meanwhile the EU produced 13.1 million

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tonnes of poultry meat in 2013 (Commission, 2015) and 6.9 million tonnes of Egg and Egg
products in 2012 (Compassioninfoodbusines.com, 2012).
In both the EU and US Salmonella and Campylobacter are the leading causes of zoonotic
bacterial gastroenteritis (EFSA, 2013, CDC, 2015). In 2013 in the EU over 50% of outbreaks of
Salmonellosis and Campylobacteriosis were sourced back to poultry meat, eggs or other
poultry related products (Figures 1 and 2) (EFSA, 2013).
Figure 1. Distribution of food vehicles of foodborne illness outbreaks of salmonellosis in the
EU during 2013. Adapted from EFSA trends of zoonosis, 2013 (EFSA, 2013).

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Figure 2. Distribution of food vehicles of foodborne illness outbreaks of campylobacteriosis in
the EU during 2013. Adapted from EFSA trends of zoonosis, 2013 (EFSA, 2013).
To attempt to lower the levels of salmonellosis and campylobacteriosis in humans it is
necessary and prudent to control the prevalence of Salmonella and Campylobacter early in
poultry production. To this end there have been numerous measures taken by the policy
makers of the EU and US to curb these pathogens at the recommendations of national and
international scientific bodies.
1.3 Salmonella and Salmonellosis
Salmonellosis is a global problem causing over 100+ million illnesses and 350,000 deaths
annually (Gal-Mor et al., 2014, Majowicz et al., 2010, Buckle et al., 2012). Salmonella species
are endemic to the gastrointestinal (G.I) tract of several food producing animal species,
most notably poultry, with over 50% of human salmonellosis cases in the EU associated with
either poultry or egg products (EFSA, 2013).

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Salmonella is a Gram negative bacilli containing two species, S. enterica and S. bongori of
which, S. enterica is the most important in regards to human health. S. enterica is made up
of six subspecies and over 2,600 distinct serovars; many of which can infect and cause illness
in humans. S. enterica sub species account for over 99% of Salmonella strains isolated from
infected patients worldwide(Cantas and Suer, 2014). Salmonella infection usually occurs due
to an individual coming into contact with the organism through either the faecal-oral route
by drinking contaminated water or ingesting contaminated food stuffs. Typhoid and
Paratyphoid fevers are serious illnesses caused by subtypes S. enterica Typhi and Paratyphi
respectively. These fevers are the cause of an invasive enteric, systemic, life threatening
disease which claims over 200,000 lives and causes illness in over 27 million each year
(Buckle et al., 2012). These illnesses are endemic to many parts of Asia but are less common
in the Western World.
Non-typhoidal S. enterica infection causes the highest disease burden in the US and Europe.
Non-typhoidal Salmonella (NTS) cause an estimated 94 million illnesses each year resulting
in over 150,000 deaths (Majowicz et al., 2010, Gal-Mor et al., 2014). While NTS is a problem
globally, high incidences of mortality are largely confined to the developing world due to
poor healthcare systems (Majowicz et al., 2010, Gal-Mor et al., 2014). Studies have shown
that reducing Salmonella prevalence early in the food chain results in a drop in the incidence
of human salmonellosis (Maijala et al., 2005). As such, the control of Salmonella in food
production, particularly in poultry is vital to reduce the risk to human health.
1.4 Campylobacter and Campylobacteriosis
Campylobacter is a Gram negative spiral shaped bacteria. There are 23 known species of
Campylobacter, of which C. jejuni and C. coli cause approximately 80% and 10% of human

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illness, respectively (EFSA, 2011). Campylobacteriosis is the most commonly reported
foodborne illness in the EU and the US, with an estimated 1 million cases in the EU and 1.3
million in the US annually (EFSA, 2010, CDC, 2015). A risk assessment study conducted by
EFSA indicated a linear relationship between the prevalence of Campylobacter in poultry
and the public health risk to the pathogen (EFSA, 2011).
Campylobacteriosis is primarily caused by the ingestion of contaminated food or water or
coming into contact with an infected animal or its faeces. Campylobacter does not readily
reproduce on food kept at room temperature due to their thermophilic and microaerophilic
nature (EFSA, 2011).
Campylobacter species are widely found in many food animals but up to 80% of human
infections are associated with poultry (EFSA, 2011). The infectious dose for Campylobacter is
low (under 800 organisms) and the incubation period lasts from 1-10 days with the majority
of those infected showing symptoms by day 4 (Mahendra H. Kothary, 2001).
Campylobacteriosis typically causes diarrhoea, fever, abdominal pain and nausea. More
serious Infections can result in meningitis and bacteraemia or debilitating long term illnesses
like Reactive Arthritis and Guillain–Barré syndrome (EFSA, 2011).
The most common treatment for campylobacteriosis is rest and fluid intake. Due to the self-
limiting nature of Campylobacter infection antibiotic treatment is rarely prescribed,
however, in cases of invasive disease antimicrobials may be required (EFSA, 2012). There
have been increasing reports of resistance to macrolide and fluoroquinolone antibiotics and
that antibiotic resistant strains have an increased capacity to cause damage in comparison
with antibiotic sensitive strains (Luangtongkum et al., 2009). The occurrence of antibiotic
resistant strains may be a result of the use of antibiotics in animal feed and treatment of

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animals, highlighting the importance of removing or minimizing the use of antibiotics in the
food production process.

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2. Materials & Methods:
Data and information for this report was gathered from many sources. Primary among these
were the guidelines published by the OIE and Codex.
The publications of EFSA and the ECDC in Europe as well as the regulations and directives
issued by the European commission were used to gain information on all EU practices. All
data concerning the EU was gathered from annual reports published by EFSA or the ECDC.
The information used from the US was taken from a wide variety of organizations within the
USA. Data on human illness was provided the CDC, the healthy people 2020 project and the
National Antimicrobial Resistance Monitoring System (NARMS). Data on pathogen
prevalence’s in animals in the US was sourced from FSIS, the national poultry improvement
plan (NPIP), NARMS, the American feed industry association (AFIA), the FDA Centre for
Veterinary Medicine (CVM) and the North American Meat industry association (NAMI).
Legislative data for the US was sourced from www.whitehouse.gov, FSIS publications and
FDA publications.
Other information used in this report was sourced from NCBIs Pubmed literature database.

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3. Results
3.1 Control of Food Safety
3.1.1 International food safety
There are a number of international bodies who provide guidance for the safe production of
food. The most influential of these are the Codex Alimentarius Commission (CAC) and the
World Organisation for Animal Health or Office International des Epizooties (OIE).
The Codex Alimentarius is an international set of food guidelines, standards, and codes of
practice to ensure safe, good food globally. The Codex Alimentarius food standards,
guidelines and codes of practice contribute to the safety, quality and fairness of this
international food trade (WHO)(CAC, 2015b). Codex standards are scientifically based and
cover all areas of food including hygiene, additives, labelling and safety testing for new food
products. The CAC currently contains 185 member countries and one member organisation,
the European Union (EU). These members represent 99% of the worlds population (CAC,
2015a). The Codex is a voluntary reference standard and member countries have no
obligation to adopt its standards; however, Codex is recognised by the World Trade
Organisation (WTO) as an international reference standard.
The OIE is an international organisation tasked with improving animal health worldwide. It
has 180 member countries and is the recognised reference organisation for the WTO. The
OIE has set standards for the safe and humane production of food from animals in their
terrestrial animal health code (OIE, 2015b). These standards and those set out by the CAC
generally complement each other. The EU and the US are members of both the CAC and OIE
and so share a common basis their food safety legislation.

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In addition to the CAC and OIE, the International Organisation for Standardisation (ISO)
provides standards that define the requirements, specifications and characteristics of
products, materials or services which can be used constantly to bring a process to its
required standard. In relation to food production, ISO 9000 for quality management and the
ISO 22000 family of standards for food safety are two of the main food standards which are
internationally recognised (ISO, 2011, ISO, 2005). The ISO also set standard methods for the
detection of microorganisms, such as Campylobacter and Salmonella.
3.1.2 European Food Safety
In the EU, legislation is made by the EU parliament who signs directives and regulations into
law. Directives are legal acts which require the member states to reach a particular result
without prescribing the means to attain it. EU Regulations are legal acts which become
immediately enforceable after signing. All EU member states must comply directly with EU
regulations. The European Food Safety Authority (EFSA), established under European
Commission Regulation No 178/2002, is the keystone of EU risk assessment regarding food
and feed safety. In close collaboration with national authorities and in open consultation
with its stakeholders, EFSA provides independent scientific advice and clear communication
on existing and emerging risks on elements of the food sector including food safety, animal
health, plant protection and nutrition. EFSA’s independent scientific advice underpins the
European food safety system(EFSA, 2013).
The European Centre for Disease Control and Prevention (ECDC) is an agency with the aim of
strengthening Europe’s defences against infectious diseases (ECDC, 2015). ECDC was
established in 2005 under Regulation (EC) No 851/2004 (Commission, 2004a). ECDCs
mission is to identify, assess and communicate current and emerging threats posed by

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infectious diseases. ECDC works in conjunction with EFSA in the preparation of an annual
report on zoonoses and zoonotic disease in Europe. These reports detail the incidence and
relevant information on zoonotic disease including the source, prevalence and levels of
antimicrobial resistance (AMR) at all stages of food production. The data for these reports
are drawn from the data gathered from the regulatory bodies of the individual EU member
states.
3.1.3 United States Food Safety
Food safety in the US is governed at three levels, federal, state and local. At both the federal
and state levels, there are three branches of government involved: legislative, executive and
judicial. The legislative branch is the US congress made up of elected officials who set up US
policy by enacting statutory laws. The executive branch of the US government comprises of
agencies who implement the laws made by the legislative branch. Agencies in this branch
include the Food Safety and Inspection Service (FSIS) and the Food and Drug Administration
(FDA). The Judicial branch of government resolves disputes about the law and interprets the
law (www.WhiteHouse.gov, 2015).
FSIS is an agency within the US Department of Agriculture (USDA) which is responsible for
ensuring the supply of meat, poultry and egg products to the US citizens is safe. All foods
products which contain over 2% poultry or 3% meat are under the jurisdiction of the FSIS
(US Code of Federal Regulations, 1998). FSIS carries out inspections on facilities for animal
slaughter, meat and poultry processing and imports to certify correct practices are being
followed. Inspections include ante and post-mortem examinations of animals to test for
pathogens, sampling antibiotics and chemical residues and inspections to enforce sanitary
conditions.

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The FDA is the national agency responsible for the regulation of all food products other than
meat and poultry. The FDA is a federal agency within the Department of Health and Human
Services. While FSIS is responsible for the regulation and monitoring of meat and poultry
products the FDAs Centre for Food Safety and Applied Nutrition is the branch of the federal
government which deals with the safety in other foods in production and retail. The FDA
Centre for Veterinary Medicine (CVM) is responsible for monitoring AMR in food animals.
The CVM is also responsible for the development and regulation of animal drugs and
additives to animal feed and water(US FDA Centre for Veterinary Medicine, 2015) .
The US Centre for Disease Control and Prevention (CDC) is the national public health
institute of the US. It is a federal agency in the Department of Health and Human Services
and acts to protect public health through the development and implementation of
prevention and control measures for infectious diseases including zoonoses (Centre for
Disease Control and Prevention, 2015).
3.2 Controlling Salmonella and Campylobacter in live Poultry
Although there are discrepancies between the control systems used in the EU and US the
basis of these systems is formed from CAC and OIE guidelines. CAC guidelines on controlling
Salmonella and Campylobacter in chickens (Guideline CAC/GL 78-2011) recommend control
measures at several stages of production from managing grandparent flocks to consumption
of poultry (Figure 1)(CAC, 2011b).

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Figure 3. Primary production to consumption of chicken meat. Adapted from Codex
Alimentarius guideline CAC/GL 78-2011 (CAC, 2011b).
As well as the specific guidelines for the control of Salmonella and Campylobacter the Codex
commission has issued more general guidelines for the safe and hygienic production of all
meats (CAC/RCP 58-2005) (CAC, 2005a). Guidelines released by the OIE focuses on the
biosecurity procedures for poultry production and specific guidelines on how to control
Salmonella in poultry (OIE, 2015c, OIE, 2015d). Together, these guidelines from the CAC and
the OIE form the basis for much of the regulation of poultry in the EU and the USA.
3.2.1 Sampling and Monitoring

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An important aspect to the control of any pathogen is monitoring which helps to evaluate
the problem and verify the effectiveness of controls. In both the EU and US sampling of
Salmonella and Campylobacter is carried out according to international guidelines and
standards set out by Codex and the ISO:
 Codex General Guidelines on Sampling CAC/GL 50-2004 (CAC, 2004b)
 ISO 6579:2002 and 10272:2006 (ISO, 2002, ISO, 2006)
European Commission Directive No 2003/99 sets down the requirements for monitoring
zoonoses, zoonotic agents, and AMR in the EU (Commission, 2003a). Zoonosis monitoring in
the EU is carried out by the competent authority in each member state who then report
their findings to EFSA.
EU microbiological limits for Salmonella in foods and during food production are set out in
Regulation (EC) No 2073/2005 (Commission, 2005). The presence of Salmonella at any stage
of food production from slaughter onwards is unacceptable in the EU.
Concerning Campylobacter in the EU there are performance objectives (POs) set by each
member state on its prevalence in the poultry production chain (EFSA, 2005). These POs are
to be reached by following process criteria, control measures designed to reduce
Campylobacter prevalence (EFSA, 2005).
In the US Salmonella and Campylobacter monitoring is carried out by FSIS. For each
establishment 51 samples from the environment and meat are taken and tested, 5 positive
samples is the current acceptable limit for Salmonella and Campylobacter.
3.2.2 Biosecurity

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One important aspect for controlling pathogens is maintaining strict biosecurity in all areas
of primary production. Biosecurity includes many general measures such as ensuring a clean
place of living for the livestock and a clean place of work for production, contamination-free
feed and water and other general hygiene measures (EFSA, 2011).
The OIE terrestrial animal health code gives detailed guidelines on how to set up and
maintain a biosecurity profile in poultry production (OIE, 2015d). These guidelines detail all
aspects of maintaining biosecurity including monitoring flock health, flock production,
mortality, feeding, watering and access to the animals. It is essential that during production
records are kept of all parameters which impact live poultry and poultry meat.
High levels of hygiene should be kept in all production areas at all times. To ensure
adequate levels of hygiene are kept the following precautions must be taken:
 Flock enclosures and meat production areas should be built in such a way as to allow
adequate space, facilities and drainage.
 Flocks enclosures and all production areas must be cleaned and disinfected on a regular
basis.
 All equipment to be used in any stage of production should be thoroughly cleaned and
disinfected both before and after use.
 All persons entering the poultry house should don appropriate clothing as provided by
the establishment.
 Entry and exit of the enclosure/production area must be tightly controlled and secure to
prevent the entry of foreign bodies such as vermin.
 Flocks should be kept separate whenever possible to reduce the chance of spreading
potential pathogens.
 All flocks should have access to sanitary feed and water.

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Prior to slaughter bird flocks are put in crates for transportation and storage. During this
time the birds do not have access to food or water and are in close proximity to other
animals, as this increases the chances of cross contamination this stage should be limited as
much as possible (EFSA, 2011). Moving birds to the slaughterhouse can result in a 20-40%
rise in both Salmonella and Campylobacter prevalence.
To help maintain a strong biosecurity regime the CAC recommends that every food
production establishment make use of a documented process control system in which all
biosecurity measures are recorded (CAC, 2005a). All procedures should follow a Standard
Operating Procedure (SOP) and make use of the Hazard Analysis Critical Control Point
(HACCP) system for identifying and managing potential hazards (CAC, 2005a).
In the US FSIS released compliance guidelines on the control of Salmonella and
Campylobacter in poultry (FSIS, 2010). These guidelines are heavily based on those of these
CAC and OIE and while many of these guidelines are not compulsory by federal law they are
largely adopted by the community (FSIS, 2010).
If a US food producing establishment decides through hazard analysis that either
Salmonella or Campylobacter are likely hazards then a detailed HACCP plan must be put in
place. All birds for use in the food industry must be obtained from hatcheries which follow
the USDAs Animal and Plant Health Inspection Service (APHIS) national poultry
improvement plan (NPIP) (FSIS, 2010). The plan details specific tests and sanitation
procedures that should be undertaken to control the quality of poultry and poultry
products. While NPIP is voluntary it is highly recommended by FSIS. NPIP states that
Salmonella should be monitored by use of environmental sampling of poultry enclosures or
direct cultures from animal carcasses (NPIP, 2014).

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NPIP also gives detailed procedures on how to maintain sanitary conditions throughout the
production process. These procedures are very similar to those given by Codex and the OIE
(FSIS, 2010).
3.3 Controlling Salmonella and Campylobacter during poultry primary production
Primary production ranges from the rearing of grandparent flocks to the eventual slaughter
of the poultry for processing (Figure 3). Both Codex and the OIE have detailed their
recommended control measures targeting both Salmonella and Campylobacter during
primary production of poultry (CAC, 2011b) (OIE, 2015d, OIE, 2015c).
During primary production most control measures relate to the use of good hygiene
practices (GHP) in biosecurity and personal hygiene as described above. However in addition
to this there are a number of methods used to control Salmonella and Campylobacter such
as treatment of feed and water, vaccination (currently only in use for Salmonella),
antibiotics and competitive exclusion.
3.3.1 Feed and water treatment
The CAC and OIE have released guidelines which detail their recommendations on safe and
hygienic treatments of animal feed (OIE, 2015a, CAC, 2004a). All feed ingredients must be
obtained from safe sources and subject to risk analysis. GMP and HACCP should be
implemented throughout feed production to eliminate as many hazards as possible. The OIE
recommends the use of feeds which have been either heat treated or treated with
bacteriostatic or bactericidal additives as this reduces bacterial carriage (OIE, 2015d).
EU animal feed regulations are provided in Regulation (EC) No 183/2005 (Commission,
2003b). In the EU all animal feed producers must follow a HACCP system and all additives to
feed must be approved and documented (Commission, 2003b).

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In 2014 the FDAs Center for Veterinary Medicine (CVM) released the US animal feed safety
system (AFSS) (US Food And Drug Administration, 2014). The AFSS is a set of regulations
similar to those given by the CAC and OIE concerning feed production. In addition to this the
American Feed Industry Association (AFIA) produced guidelines on the Salmonella control
methods in animal feed (AFIA, 2010). AFIA guidance for Salmonella control in feed is similar
to the CAC and OIE guidance with additional recommendations for heat treatment and
pelleting of feed during production to reduce contamination risk (AFIA, 2010).
The use of feed and water additives to combat Campylobacter has also been discussed by
EFSA (EFSA, 2011). The use of both chemicals and biological agents has been considered.
Chlorination has been found to lead to an overall reduced microflora, including
Campylobacter while the addition of organic acids such as monocaprin, formic acid and
butyrate have demonstrated mixed results (EFSA, 2011).
Water treatment with organic acids is also encouraged by FSIS, this reduces the bacterial
load of the animals G.I tract and discourages them from pecking at their droppings (FSIS,
2010).
Adding bacteriocins or bacteriophages to feed or water to reduce Campylobacter
prevalence has also been discussed. Bacteriocins are proteinaceous toxins made by bacteria
to inhibit other closely related bacterial strains. While there have been studies showing
bacteriocins can be highly effective in reducing contamination (Stern et al., 2006), there are
still logistical issues with the production of large amounts of bacteriocins which render the
technology unviable at present. Bacteriophages were also considered and experimental
data seems positive (El-Shibiny et al., 2005) however, problems also exist related to
production and use of bacteriophages which must be overcome prior to their potential use.

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3.3.2 Vaccination
Vaccines are biological preparations which provide an organism with an acquired immunity
to a particular microbial disease. Typically vaccines are made from weakened or killed forms
of the microbe in question, its surface proteins or toxins. Currently the most utilized vaccine
types in poultry are live attenuated vaccines due to their efficiency and longevity (C.
Gamazo, 2007).
Vaccination of farm animals is recommended by both the OIE and CAC as a method of
controlling pathogens during production (OIE, 2015c, K. Videnova, 2012, OIE, 2010b, CAC,
2011b). The OIE has set standards which should be met when creating, authorizing and
administering vaccines to animals (OIE, 2010b). The use of vaccines for controlling
Salmonella infection is well established throughout the world, the OIE has detailed
guidelines on the use of Salmonella vaccines in chapter 2.9.9 of the manual of diagnostic
tests and vaccines for terrestrial animals (OIE, 2010a). Vaccines are usually administered to
large numbers of animals through their feed or water, or alternatively by spray application.
EFSA has recommended the use of vaccines to control Salmonella in poultry since 2004
(EFSA, 2004c). The European Commission has declared the use of Salmonella vaccines in
poultry as mandatory if the member state has a high prevalence of the organism
(Commission, 2006). Vaccines must be approved by the European Medicines Agency (EMA)
and subsequently the competent authority in individual member states prior to use
(Commission, 2006).
The use of these vaccines in the EU has had a great impact on the levels of poultry and
poultry product associated Salmonellosis (EFSA, 2010). For example, after Salmonella
Enteritidis vaccination in poultry was implemented in Belgium in 2004 the cases of human
salmonellosis dropped from over 12,000 in 2003, of which 89% were due to S. Enteritidis, to

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under 4,000 in 2008 (EFSA, 2010). Similarly in Denmark where vaccination was first
introduced in 1996 the proportion of salmonellosis cases associated with egg products
dropped from 60% in 1996 to 5% in 2006 (EFSA, 2010).
Vaccines against Salmonella usually target specific serovars. Of particular concern are
serovars S. Enteritidis and S. Typhimurium, together they were identified in almost 60% of
human salmonellosis isolates in 2013 (Figure 4). Of the six Salmonella targeting poultry
vaccines currently licensed in the EU four target S. Enteritidis (Table 1). The positive effects
of these vaccines is clearly shown in Figure 4 as the percentage of human salmonellosis
caused by S. Enteritidis has dropped from 76% in 2004 to 39.5% in 2013. The effect of
vaccines has also been shown in poultry directly with a drop in the prevalence of S.
Enteritidis from over 37% of Salmonella isolates in 2005 to 15% in 2013 (Figure 5).

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Figure 4. The prevalence of the two most common Salmonella serovars, S. Enteritidis and S.
Typhimurium as a percentage of all human salmonellosis in the EU from 2004 – 2013. Data
gathered from EFSA annual zoonosis reports 2004 – 2013 (EFSA, 2013)
Figure 5. The prevalence of the two most common Salmonella serovars, S. Enteritidis and S.
Typhimurium as a percentage of Salmonella positive isolates from live Gallus gallus chickens
in the EU from 2005 – 2013 Data gathered from EFSA annual zoonosis reports 2005 – 2013
(EFSA, 2013).
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80
2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014
%Prevalence Prevalence of S. Enteritidis and S. Typimurium as a percentage of all
human salmonellosis in the EU 2004 - 2013
S.Enteritidis S. Typhimurium
0
5
10
15
20
25
30
35
40
2005 2006 2007 2008 2009 2010 2011 2012 2013 2014
%Positive
Percentage of Salmonella positive chickens positive for S. Enteritidis or S.
Typhimurium in the EU 2005-2013
S. Enteritidis S. Typhimurium

25. 22 | P a g e
Product Name Manufacturer Year of approval Serovars targeted
AviPro Salmonella
Vac T
Lohmann Animal
Health
1994 S. Typhimurium
AviPro Salmonella
Vac E
Lohmann Animal
Health
1999 S. Enteritidis
Gallivac SE Merial 2002 S. Enteritidis
Gallimune Se + St Merial 2007 S. Enteritidis,
S. Typhimurium
Nobilis Salenvac Intervet 1996 S. Enteritidis
Nobilis Salenvac T Intervet 2004 S. Typhimurium
Table 1. Vaccines targeting Salmonella serovars S. Typhimurium and S. Enteritidis for use in
poultry which have been approved for use in the EU. Data gathered from (K. Videnova, 2012,
Paul-Ehrlich-Institute, 2015).
In the US, vaccination is recommended by FSIS and the FDA to control the spread of
Salmonella in poultry. Even though vaccination of poultry for Salmonella isn’t mandatory in
US law, it was estimated that in 2010 that 78-79% of poultry producers vaccinated their
flocks (FSIS, 2010). Although vaccines are encouraged by the FDA their use in the US has
only recently become widespread after an outbreak of salmonellosis linked to egg shells
caused approximately 2,000 illnesses in 2010 (Centre for Disease Control and Prevention,
2010). Similarly to the EU most of the approved vaccines in the US target either S.
Enteritidis, S. Typhimurium or both, however due to the lack of enforcement of vaccine use
there has been no significant drop in the prevalence of these serovars in human
salmonellosis or their identification in poultry.

26. 23 | P a g e
Figure 6. The prevalence of the two most common Salmonella serovars, S. Enteritidis and S.
Typhimurium as a percentage of all human salmonellosis in the US from 2005 – 2012. Data
gathered from the US national enteric disease surveillance program (CDC, 2012).
Figure 7. Percentage of Salmonella positive Gallus gallus chickens found positive for either S.
Enteritidis or S. Typhimurium in the US from 2004-2012. Data gathered from (NPIP, 2014).
0
10
20
30
40
50
60
70
2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014
%Prevalence Prevalence of S. Enteritidis and S. Typimurium in human salmonellosis in
the US 2005 - 2012
Typhimurium Enteritidis
0
5
10
15
20
25
30
2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014
% of Salmonella positive chickens positive for S. Enteritidis or
S. Typhimurium in the US 2004-2012
S. Enteritidis S. Typhimurium

27. 24 | P a g e
There are currently no vaccines targeting Campylobacter on the market. Past studies have
shown that vaccination can have protective properties in chickens (Stern et al., 1990),
however these have been poorly reproducible (de Zoete et al., 2007). It may be possible to
use vaccination as a prevention method in the future, however efficacy in the field is hard to
predict due to the natural exposure of animals to Campylobacter in their environment
(EFSA, 2011).
3.3.3 Antimicrobials, Resistance and Monitoring
The CAC provides guidelines to the use of antimicrobials in food producing animals in
CAC/RCP 61-2005 and CAC/GL 77-2011 (CAC, 2005b, CAC, 2011a). These documents aim to
reduce the public health burden resulting from the use of antimicrobials in food producing
animals, namely antimicrobial resistance (AMR). This CAC guideline is supplements
guidelines by the OIE terrestrial animal health code in chapters 6.6-6.10 (OIE, 2015b). The
CAC guideline CAC/RCP 61-2005 describes the recommended practices for to contain and
minimize the spread of AMR. This guide covers all aspects of the regulation of antimicrobials
for use in animals from regulatory approval to responsible use. The CAC concludes that
antimicrobials are an important tool in controlling infectious disease. OIE terrestrial animal
health code chapter 6.9 provides details on the responsible use of antimicrobials in animals
(OIE, 2015e). The competent authority of a region must first give a substance market
authorization and have the necessary evidence to deem it safe and efficacious.
Antimicrobials are recommended by both the CAC and OIE to be used as part of an overall
biosecurity plan and not as a sole method of control.
In the EU the use of antimicrobials and other additives in animal feed is governed by
Regulation (EC) No 1831/2003 (Commission, 2003b). The use of all antibiotics other than

28. 25 | P a g e
coccidiostats and histomonostats has been banned under this legislation since the 1st of
January 2006. This is intended to reduce AMR in food animals. Rather than using
antimicrobials to reduce pathogen load, the focus is now on preventing pathogens from
entering the food chain through rigorous control methods.
In the past decade the FDA has updated its legislation concerning the use of antimicrobials
in food. The documents that have been released aim to phase out the unnecessary or
inappropriate use of medically significant antimicrobials in food animals, either for
enhancing growth or increasing feed efficiency (Centre for Veterinary Medicine, 2013). In
2003, GFI #152 was released (Centre for Veterinary Medicine, 2003). This document details
a risk based analysis for evaluating the potential for antimicrobial animal drugs to induce
AMR. The FDA advises that antimicrobials only be used in animals for the prevention,
treatment or control of disease (Centre for Veterinary Medicine, 2012). This is in contrast to
the absolute ban on antibiotics in the EU. The FDA has also released documents which
provide guidance to drug manufacturers who want to remove their antimicrobials indication
in animal use (Centre for Veterinary Medicine, 2013).
Both the OIE and CAC recommend using detailed post-marketing surveillance strategies to
monitor AMR while a product is being sold. OIE Ch. 6.10 details the risk analysis for the rise
of AMR in food animals (OIE, 2015f).
Monitoring and reporting of AMR in the EU is regulated by Directive 2013/652 EU
(Commission, 2013). This directive details the procedures for sampling live animals, food
during production and at retail for AMR for a variety of pathogens. Monitoring is carried out
by the competent authority in each member state and data is reported to EFSA. This report
must contain all details about the monitoring procedure and the samples taken. The first

29. 26 | P a g e
published specifications for the harmonized monitoring of AMR in Salmonella and
Campylobacter isolates in animals and food was released in 2007 (2007/407/EC)
(Commission, 2007).
The ECDC protocol for harmonised monitoring of AMR in human Salmonella and
Campylobacter isolates was released in March 2012 (EFSA, 2012). This details the methods
necessary for monitoring the occurrence of antibiotic resistance in humans. This includes
details on the type of resistance encountered and how to test for antimicrobial
susceptibility.
In the US AMR monitoring is carried out by the National Antimicrobial Resistance
Monitoring System (NARMS) which was established in 1996 in a collaboration between the
CDC, FDA and USDA (CDC, 2015). NARMS monitors AMR trends in bacteria isolated from
humans, retail meats and food animals.
In 2013 the CDC reported 310,000 cases of drug resistant campylobacteriosis and 100,000
cases of drug resistant salmonellosis (CDC, 2015). In the EU the ECDC reported
Both the US and EU list the threat of AMR in Salmonella isolates as serious, in the US alone
over 100,000 AMR Salmonella infections occur per annum (CDC, 2015).
Figures 8 – 15 show the recent prevalence of AMR in Salmonella and Campylobacter in both
chickens and humans in the EU and US.
In the EU resistance to ampicillin and Nalidixic Acid is widespread in S. Enteritidis, however it
has yet to become widespread in the US (Figures 8A, 9A). Resistance to multiple antibiotics,
in particular ampicillin and tetracycline is common in S. Typhimurium in both the EU and US
(Figures 8B, 9B).

30. 27 | P a g e
Figure 8. The change in the percentage of (A) S. Enteritidis and (B) S. Typhimurium isolates
taken from Gallus Gallus chickens which were resistant to the antibiotics Ampicillin, Nalidixic
Acid, Sulphonamides, Tetracyclines and Ciprofloxacin in the EU. Data gathered from EFSA
reports on AMR and zoonoses (EFSA, 2015).
0
5
10
15
20
25
30
35
2006 2007 2008 2009 2010 2011 2012 2013 2014
%isolatesshowingresistance
(A) Antimicrobial resistance in S. Enteritidis isolates from chickens in the
EU 2007-2013
Ampicillin Nalidixic Acid Sulfonamides Tetracyclins Ciprofloxacin
0
10
20
30
40
50
60
70
80
90
100
2006 2007 2008 2009 2010 2011 2012 2013 2014
%isolatesshowingresistance
(B) Antimicrobial resistance in S. Typhimurium isolates from chickens in
the EU 2007-2013
Ampicillin Nalidixic Acid Sulfonamides Tetracyclins Ciprofloxacin

31. 28 | P a g e
Figure 9. The change in the percentage of antimicrobial resistance seen in (A) S. Enteritidis
and (B) S. Typhimurium isolates taken from Gallus gallus chickens which were resistant to
the antibiotics Ampicillin, Tetracycline and Chloramphenicol in the US (CDC, 2013).
-0.5
0
0.5
1
1.5
2
2.5
3
3.5
2004 2005 2006 2007 2008 2009 2010 2011 2012
%Isolatesshowingresistance (A) Antimicrobial resistance in S. Enteritids isolates from chickens in the
US 2005-2011
Ampicillin Chloramphenicol Tetracycline
0
10
20
30
40
50
60
70
80
90
2004 2005 2006 2007 2008 2009 2010 2011 2012
%Isolatesshowingresistance
(B) Antimicrobial resistance in S. Typhimurium isolates from chickens in
the US 2005-2011
Ampicillin Chloramphenicol Tetracycline

32. 29 | P a g e
Figure 10. The prevalence of resistance to Ampicillin, Nalidixic Acid, Streptomycin,
Sulphonamide, Tetracycline and Ciprofloxacin antibiotics in (A) S. Enteritidis and (B) S.
Typhimurium in European human isolates from 2009 – 2013 (EFSA, 2015).
0
5
10
15
20
25
2008.5 2009 2009.5 2010 2010.5 2011 2011.5 2012 2012.5 2013 2013.5
%Isolatesshowingresistance (A) Antimicrobial resistance in S. Enteritidis isolates from humans in the
EU 2009-2013
Ampicillin Nalidixic Acid Streptomycin
Sulfonamides Tetracyclins Ciprofloxacin
0
10
20
30
40
50
60
70
2008.5 2009 2009.5 2010 2010.5 2011 2011.5 2012 2012.5 2013 2013.5
%Isolatesshowingresistance
(B) Antimicrobial resistance in S. Typhimurium isolates from humans in
the EU 2009-2013
Ampicillin Nalidixic Acid Streptomycin
Sulfonamides Tetracyclins Ciprofloxacin

33. 30 | P a g e
Figure 11. The change in the percentage of antibiotic resistance in (A) S. Enteritidis and (B) S.
Typhimurium isolates taken from humans (CDC, 2013).
As shown in figures 10 and 11 the highest levels of resistance seen in human isolates S.
Enteritidis is against Nalidixic acid in the EU. This correlates well with the Nalidixic acid
resistance seen in European chicken flocks, it seems Nalidixic acid resistance has yet to
0
1
2
3
4
5
6
7
2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014
%Isolatesshowingresistance (A) Antimicrobial resistance in S.Enteritidis isolates from humans in the US
from 2004-2011
Ampicillin Chloramphenicol Tetracycline
0
5
10
15
20
25
30
35
40
2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014
%Isolatesshowingresistance
(A) Antimicrobial resistance in S. Typhimurium isolates from humans in the
US from 2004-2011
Ampicillin Chloramphenicol Tetracycline

34. 31 | P a g e
reach the US. Resistance to ampicillin, sulphonamides, tetracycline and streptomycin is
prevalent in human isolates of S. Typhimurium in the EU, resistance to sulphonamides and
streptomycin has not yet been recorded in human isolates in the US.
Figure 12. The change in the percentage of (A) C. Jejuni and (B) C. Coli isolates taken from
Gallus Gallus chickens which were resistant to the tetracycline and quinolone antibiotics.
Data gathered from EFSA reports on AMR and zoonoses (EFSA, 2015).
0
10
20
30
40
50
60
2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014
%Isolatesshowingresistance
(A) Antimicrobial resistance in C. Jejuni isolates from chickens in the
EU 2005-2013
Tetracyclines Quinolones
0
10
20
30
40
50
60
70
80
90
2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014
%Isolatesshowingresistance
(B) Antimicrobial resistance in C. Coli isolates from Chickens in the EU
2005 -2013
Tetracyclines Quinolones

35. 32 | P a g e
Figure 13. The change in the percentage of (A) C. Jejuni and (B) C. Coli isolates taken from
Gallus Gallus chickens which were resistant to the tetracycline and quinolone antibiotics
(CDC, 2013).
Resistance to both tetracycline and quinolone antibiotics is widespread in the EU in C. Jejuni
and C. Coli. Resistance to Tetracyclines is prevalent across the US but resistance to the
quinolones is considerably lower than in the EU.
0
10
20
30
40
50
60
2003 2004 2005 2006 2007 2008 2009 2010 2011 2012
%Isolatesshowingresistance
Antimicrobial resistance in C. Jejuni isolates from chickens in the US 2004-
2011
Tetracyclines Quinolones
0
10
20
30
40
50
60
70
2003 2004 2005 2006 2007 2008 2009 2010 2011 2012
%Isolatesshowingresistance
Antimicrobial resistance in C. Coli isolates from chickens in the
US 2004-2011
Tetracyclines Quinolones

36. 33 | P a g e
Figure 14. The prevalence of resistance to Tetracycine, Nalidixic Acid, Ciprofloxacin and
Ampicillin antibiotics in (A) C. Jejuni and (B) C. Coli S in European human isolates from 2009 –
2013(EFSA, 2015).
0
10
20
30
40
50
60
2008.5 2009 2009.5 2010 2010.5 2011 2011.5 2012 2012.5 2013 2013.5
%Isolatesshowingresistance (A) Antimicrobial Resistance in C. Jejuni isolates from humans in the EU
2009-2013
Tetracyclines Nalidixic Acid Ciprofloxacin Ampicilin
0
10
20
30
40
50
60
70
80
2008.5 2009 2009.5 2010 2010.5 2011 2011.5 2012 2012.5 2013 2013.5
%Isolatsshowingresistance
(B) Antimicrobial Resistance in C. Coli isolates from humans in the EU
2009-2013
Tetracyclines Nalidixic Acid Ciprofloxacin Ampicillin

37. 34 | P a g e
Figure 15. The prevalence of resistance to Tetracyclines, Nalidixic acid and Ciprofloxacin
antibiotics in (A) C. Jejuni and (B) C. Coli in US human isolates from 2004 – 2013(CDC, 2013).
AMR in human isolates of Campylobacter from the EU have showed the highest prevalence
of resistance to Nalidixic acid and the quinolone Ciprofloxacin with lower prevalence’s of
resistance to tetracyclines and ampicillin being shown. Conversely, in the US human isolates
were more commonly found with tetracycline resistance than Nalidixic acid or Ciprofloxacin.
0
10
20
30
40
50
60
2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014
%IsolatesshowingResistance (A) Antibiotic resistance in C.Jejuni isolates from humans in the US 2004-
2013
Tetracyclines Nalidixic Acid Ciprofloxacin
0
10
20
30
40
50
60
2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014
%Isolatesshowingresistance
(B) Antimicrobial resistance in C. Coli isolates from humans in the US 2004-
2013
Tetracyclines Nalidixic Acid Ciprofloxacin

38. 35 | P a g e
Interestingly resistance to Nalidixic acid was not found in chicken flocks in either the EU or
US indicating it comes from another source.
3.3.4 Competitive Exclusion
Competitive exclusion (CE) is the process of inoculating a flock with another organism or a
culture of organisms which out-competes the pathogen. Competitive exclusion is
recommended by both the OIE and Codex for use in Salmonella control. However, there has
been difficulty in obtaining approval for CE products due to their complex nature. The main
concern, in the US especially, is the fact that many CE cultures being marketed are largely
undefined in their content. There are concerns regarding their safety and potential to
spread antibiotic resistance genes through the environment (Doyle and Erickson, 2012). For
this reason, the FDA in the US has not approved the use of CE or probiotic products in
animals (Doyle and Erickson, 2012). In the EU however the use of probiotic products is
permitted under Regulation (EC) No 1831/2003 which allows for the use of microbes as gut
flora stabilizers, i.e. products which have a positive effect on the animals gut flora
(Commission, 2003b). To gain approval probiotic products destined for animals must prove
their identity, safety and show efficacy under field trials (Anadon et al., 2006).
Although a 2004 report by EFSA recommended competitive exclusion for the control of
Salmonella (EFSA, 2004b), there is no legislation as of yet relating to this control measure.
The use of competitive exclusion for Campylobacter in the EU is not currently considered as
a viable control method due to the lack of evidence of efficacy and standardization of the
organisms to be used (EFSA, 2011). For exclusion to be most effective it the excluding agent
should be administered as soon before pathogen exposure as possible (EFSA, 2004b).

39. 36 | P a g e
3.4 Control during Slaughter
Control of both Salmonella and Campylobacter during slaughter and meat processing is
mainly carried out by maintaining a strict biosecurity profile as detailed by the OIE and CAC
(OIE, 2015d, CAC, 2011b).
To ensure lower bacterial loads during slaughter it is necessary that all areas and equipment
which the birds come into contact with are sanitized both before they enter and after they
come into contact (FSIS, 2010).
The way in which slaughter and processing is carried out should be carefully monitored.
Most of the slaughter and processing process is mechanized, machines used should be
adapted to deal with any variation in carcass size. This is to ensure the intestines are not
ruptured during evisceration as they are a plentiful source of bacteria (EFSA, 2011). The
withdrawal of feed prior to slaughter is recommended by FSIS and the EFSA as it reduces
fecal load. If the feed is withdrawn too late the G.I tract of the carcass may rupture, while if
feed is withdrawn too early, the internal organs become fragile. Therefore, care must be
taken in timing the animals last meal (FSIS, 2010).
3.4.1 Decontamination
Decontamination is the process of reducing the microbial load of a carcass; it may be carried
out by either physical or chemical means. Codex guideline CAC/GL 78-2011 recommends
washing carcasses with water, trimming carcasses and disposing of those with considerable
faecal contamination. Codex also recommends the use of physical or chemical methods
when approved by the competent authority (CAC, 2011b). Water is used in both the EU and
US as it can physically remove microorganisms from carcasses, reducing microbial load
(EFSA, 2011).

40. 37 | P a g e
European Commission Regulation No 853/2004 allows chemical decontamination to be
considered if the substance is proven safe and effective, however, currently no chemical
decontamination treatments approved are in Europe (EFSA, 2011, Commission, 2004b). In
contrast the FDA has approved the use of a number of chemical agents for
decontamination, however, use of these is at the discretion of the manufacturer (FSIS,
2010).

41. 38 | P a g e
4. Conclusion
Since the turn of the century there has been multiple changes to the legislation in both the
EU and US concerning the control of Salmonella and Campylobacter in poultry. The impact
of the implementation and standardisation of biosecurity procedures as recommended by
the OIE and CAC is difficult to determine. This is due to the fact that prior to the release of
the CAC and OIE guidelines biosecurity measures of varying effectiveness were
implemented in the US and some of the current EU member states (CAC, 2005a, OIE,
2015d).
Similarly the impact of recent feed treatment legislation in the EU and US is difficult to
determine as many of the measures described in these regulations had been implemented
to different degrees across the EU and US.
Arguably most impactful change in the past decade has been the implementation of
Salmonella targeting vaccines in poultry in the EU. The rate of salmonellosis in the EU
dropped from over 40 cases per 100,000 of the population to under 25 between 2004 and
2012 (Figure 16).
As shown in table 1, the majority of vaccines available in the EU target S. Enteritidis, the
most prevalent cause of human salmonellosis. In 2004 S. Enteritidis was the cause of 76% of
human salmonellosis and was present in almost 40% of chicken flocks contaminated with
Salmonella, by 2013 S. Enteritidis was the cause of 39.5% of human illness and its
prevalence in chickens was reduced to 15% of all Salmonella isolates (Figures 4 and 5).
The rate of salmonellosis in the US seems to have stayed relatively constant compared to
the EU, this could be linked to the differences in reporting procedures. There is a

42. 39 | P a g e
considerable spike in the prevalence of salmonellosis in the EU in 2004. Interestingly this
corresponds with a period of expansion in the EU as the A10 countries, many of which were
former eastern bloc countries of the Soviet Union joined the EU. Many of these had
underdeveloped systems to deal with zoonotic pathogens (EFSA, 2004a).
Figure 16. Rates of human salmonellosis in the EU and US from 2002-2012 per 100,000
population (CDC, 2012, EFSA, 2013).
In contrast the rates of campylobacteriosis in the EU has risen from 47 cases per 100,000 to
65 from 2004 – 2012 (Figure 17). This is likely a result of increased reporting rather than
increased disease prevalence as the harmonized guidelines for the reporting of
campylobacteriosis in the EU was released in 2005 (EFSA, 2005). Rates of
campylobacteriosis in the US have stayed relatively constant in the past decade, this again
may be due to the low levels of reporting of Campylobacter infection.
0
5
10
15
20
25
30
35
40
45
2000 2002 2004 2006 2008 2010 2012 2014
Rate of salmonellosis per 100,000 population 2002-2012 in the
EU and US
EU US

43. 40 | P a g e
Figure 17. Rate of Human Campylobacteriosis in the EU and US per 100,000 population
2004-2012 (EFSA, 2013, CDC, 2013).
Rates of AMR in both the US and EU in Salmonella and Campylobacter in both human
isolates and animals have fluctuated in the past decade. Since the implementation of
Regulation (EC) 1831/2003 which came into effect in 2006 no antibiotics have been used on
poultry in the EU. This however has not led to reduced levels of resistance to many
antibiotics in Salmonella and Campylobacter species. This is likely due to the antibiotic
resistance genes not being detrimental to the organisms fitness in antibiotic free
environments (EFSA, 2015). Similarly in the US since the FDAs recommendations on the
limited use of antibiotics on poultry and other food animals there has been no significant
decline shown in AMR of Salmonella or Campylobacter (Centre for Veterinary Medicine,
2003, FSIS, 2010). To fully experience the effects of removing antibiotics from animal use,
we must look towards the next generation of antibiotics to combat Salmonella or
0
10
20
30
40
50
60
70
80
2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013
Illnessrateper100,000 Rate of human campylobacteriosis per 100,000 population EU and US
EU US

44. 41 | P a g e
Campylobacter and determine the effect not using antibiotics in animals had on the growth
of resistance to these.
Overall it seems vaccination has the greatest effect on the prevalence of Salmonella in
poultry and the resulting salmonellosis in humans. Along with the use of all other methods
described herein, the creation of a viable vaccine against Campylobacter should be
encouraged.

45. 42 | P a g e
6. Acknowledgements
I would like to thank both Dr. Pat O’Mahony and Dr. Pippa Haughton of the Food Safety
Authority of Ireland for allowing me to conduct this project under their supervision in their
place of work. I would also like to extend my gratitude to all the staff of the FSAI who made
me feel very welcome at all times and helped me with any queries I had over the course of
the project.

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6. References:
AFIA, A. F. I. A. 2010. American Feed Industry Association Salmonella Control Guidelines 2010 AFIA
http://ucfoodsafety.ucdavis.edu/files/172958.pdf.
ANADON, A., MARTINEZ-LARRANAGA, M. R. & ARANZAZU MARTINEZ, M. 2006. Probiotics for animal
nutrition in the European Union. Regulation and safety assessment. Regul Toxicol
Pharmacol, 45, 91-5.
BUCKLE, G. C., WALKER, C. L. F. & BLACK, R. E. 2012. Typhoid fever and paratyphoid fever: Systematic
review to estimate global morbidity and mortality for 2010. Journal of Global Health, 2,
010401.
C. GAMAZO, J. M. I. 2007. Salmonella Vaccines http://www.formatex.org/microbio/pdf/Pages518-
524.pdf.
CAC, C. A. C. 2004a. Code of Practice on Good Animal Feeding CAC/RCP 54-2004
http://www.fao.org/docrep/012/i1379e/i1379e06.pdf.
CAC, C. A. C. 2004b. General Guidelines on Sampling CAC/GL 50-2004
CAC, C. A. C. 2005a. Code of Hygenic Practice for Meat CAC/RCP 58-2005
http://www.foodsafety.govt.nz/elibrary/industry/code-of-hygienic-practise-meat.pdf.
CAC, C. A. C. 2005b. CODE OF PRACTICE TO MINIMIZE AND CONTAIN ANTIMICROBIAL RESISTANCE
CAC/RCP 61-2005
http://www.codexalimentarius.net/input/download/standards/10213/CXP_061e.pdf.
CAC, C. A. C. 2011a. GUIDELINES FOR RISK ANALYSIS OF FOODBORNE ANTIMICROBIAL RESISTANCE
CAC/GL 77- 2011
http://www.codexalimentarius.net/input/download/standards/11776/CXG_077e.pdf.
CAC, C. A. C. 2011b. Guidelines for the control of Campylobacter and Salmonella in chicken meat
www.codexalimentarius.org/input/download/standards/.../CXG_078e.pdf.
CAC, C. A. C. 2015a. Codex Alimentarius Web Page - Members and Observers,
http://www.codexalimentarius.org/members-observers/en/.

47. 44 | P a g e
CAC, C. A. C. 2015b. Codex Alimentarius Website - About Codex,
http://www.codexalimentarius.org/about-codex/en/.
CANTAS, L. & SUER, K. 2014. Review: the important bacterial zoonoses in "one health" concept.
Front Public Health, 2, 144.
CDC, C. F. D. C. A. P. 2012. National Enteric Disease Surveillance: Salmonella Surveillance
CDC, C. F. D. C. A. P. 2013. National Antimicrobial Resistace Monitoring System (NARMS): Enteric
Bacteria 2013. Human Isolates Final Report http://www.cdc.gov/narms/pdf/2013-annual-
report-narms-508c.pdf.
CDC, C. F. D. C. A. P. 2015. Antibiotic Resistance Threats in the United States, 2013
http://www.cdc.gov/drugresistance/pdf/ar-threats-2013-508.pdf.
CENTRE FOR DISEASE CONTROL AND PREVENTION, C. 2010. Multistate Outbreak of Human
Salmonella Enteritidis Infections Associated with Shell Eggs
http://www.cdc.gov/salmonella/enteritidis/index.html.
CENTRE FOR DISEASE CONTROL AND PREVENTION, C. 2015. CDC Organisation and mission statement
Web page - http://www.cdc.gov/about/organization/cio.htm.
CENTRE FOR VETERINARY MEDICINE, C. 2003. CVM GFI #152 Evaluating the Safety of Antimicrobial
New Animal Drugs with Regard to Their Microbiological Effects on Bacteria of Human Health
Concern
http://www.fda.gov/downloads/AnimalVeterinary/GuidanceComplianceEnforcement/Guida
nceforIndustry/UCM052519.pdf.
CENTRE FOR VETERINARY MEDICINE, C. 2012. Guidance for Industry #209 The Judicious Use of
Medically Important Antimicrobial Drugs in Food-Producing Animal
http://www.fda.gov/downloads/AnimalVeterinary/GuidanceComplianceEnforcement/Guida
nceforIndustry/UCM216936.pdf.
CENTRE FOR VETERINARY MEDICINE, C. 2013. Guidance for Industry #213 New Animal Drugs and
New Animal Drug Combination Products Administered in or on Medicated Feed or Drinking

48. 45 | P a g e
Water of FoodProducing Animals: Recommendations for Drug Sponsors for Voluntarily
Aligning Product Use Conditions with GFI #209
http://www.fda.gov/downloads/AnimalVeterinary/GuidanceComplianceEnforcement/Guida
nceforIndustry/UCM299624.pdf.
COMMISSION, E. 2003a. Directive 03/99/EC OF THE EUROPEAN PARLIAMENT AND OF THE COUNCIL
of 17 November 2003 on the monitoring of zoonoses and zoonotic agents, amending Council
Decision 90/424/EEC and repealing Council Directive 92/117/EEC
https://www.fsai.ie/uploadedFiles/Legislation/Food_Legisation_Links/Zoonoses/Directive_2
003_99_EC.pdf.
COMMISSION, E. 2003b. REGULATION (EC) No 1831/2003 OF THE EUROPEAN PARLIAMENT AND OF
THE COUNCIL of 22 September 2003 on additives for use in animal nutrition
https://www.agriculture.gov.ie/media/migration/agri-
foodindustry/feedingstuffs/feedadditives/RegulationAdditives(1831_2003).pdf.
COMMISSION, E. 2004a. Regulation (EC) No 851/2004 of the European Parliment and of the council
of 21 April 2004 establishing a European centre for disease prevention and control
http://ecdc.europa.eu/en/aboutus/Key%20Documents/0404_KD_Regulation_establishing_E
CDC.pdf.
COMMISSION, E. 2004b. REGULATION (EC) No 853/2004 OF THE EUROPEAN PARLIAMENT AND OF
THE COUNCIL of 29 April 2004 laying down specific hygiene rules for food of animal origin
https://www.fsai.ie/uploadedFiles/Food_Business/Reg853_2004.pdf.
COMMISSION, E. 2005. COMMISSION REGULATION (EC) No 2073/2005 of 15 November 2005 on
microbiological criteria for foodstuff
https://www.fsai.ie/uploadedFiles/Consol_Reg2073_2005.pdf.
COMMISSION, E. 2006. COMMISSION REGULATION (EC) No 1177/2006 of 1 August 2006
implementing Regulation (EC) No 2160/2003 of the European Parliament and of the Council
as regards requirements for the use of specific control methods in the framework of the

49. 46 | P a g e
nationalprogrammes for the control of salmonella in poultry http://eur-lex.europa.eu/legal-
content/EN/TXT/PDF/?uri=CELEX:32006R1177&from=en.
COMMISSION, E. 2007. COMMISSION DECISION of 12 June 2007 on a harmonised monitoring of
antimicrobial resistance in Salmonella in poultry and pigs 2007/407/EC http://eur-
lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32007D0407&from=EN.
COMMISSION, E. 2013. COMMISSION IMPLEMENTING DECISION of 12 November 2013 as regards a
Union financial aid towards a coordinated control plan for antimicrobial resistance
monitoring in zoonotic agents in 2014 http://eur-lex.europa.eu/legal-
content/EN/TXT/PDF/?uri=CELEX:32013D0653&from=EN.
COMMISSION, E. 2015. European Commission for Agriculture and Rural Development, Poultry Meat.
http://ec.europa.eu/agriculture/poultry/index_en.htm.
COMPASSIONINFOODBUSINES.COM 2012. Egg Production in the EU
http://www.compassioninfoodbusiness.com/media/5789260/laying-hens-egg-production-
in-the-eu.pdf.
DE ZOETE, M. R., VAN PUTTEN, J. P. & WAGENAAR, J. A. 2007. Vaccination of chickens against
Campylobacter. Vaccine, 25, 5548-57.
DOYLE, M. P. & ERICKSON, M. C. 2012. Opportunities for mitigating pathogen contamination during
on-farm food production. Int J Food Microbiol, 152, 54-74.
ECDC, E. C. F. D. C. A. P. 2015. ECDC Web page - About us,
http://ecdc.europa.eu/en/aboutus/Pages/aboutus.aspx.
EFSA, E. F. S. A. 2004a. EU Summary Report on antimicrobial resistance in zoonotic and indicator
bacteria from humans, animals and food in 2004
EFSA, E. F. S. A. 2004b. Opinion of the Scientific Panel on Biological Hazards on the request from the
Commission related to the use of antimicrobials for the control of Salmonella in poultry.
http://www.efsa.europa.eu/sites/default/files/scientific_output/files/main_documents/bio
haz_opinion16_ej115_antimicr_salmonella_en1%2C5.pdf.

50. 47 | P a g e
EFSA, E. F. S. A. 2004c. Opinion of the Scientific Panel on Biological Hazards on the requests from the
Commission related to the use of vaccines for the control of Salmonella in poultry
http://www.safe-
poultry.com/documents/opinion_biohaz15_ej114_vacc_salminpoultry_v2_en1.pdf.
EFSA, E. F. S. A. 2005. Opinion of the Scientific Panel on Biological Hazards on the request from the
Commission related to Campylobacter in animals and foodstuff
http://www.efsa.europa.eu/sites/default/files/scientific_output/files/main_documents/bio
haz_ej173_op_campylobacter_en1_0,7.pdf.
EFSA, E. F. S. A. 2010. Scientific Opinion on a quantitative estimation of the public health impact of
setting a new target for the reduction of Salmonella in laying hens
http://www.efsa.europa.eu/sites/default/files/scientific_output/files/main_documents/154
6.pdf.
EFSA, E. F. S. A. 2011. Scientific Opinion on Campylobacter in broiler meat production: control
options and performance objectives and/or targets at different stages of the food chain.
EFSA, E. F. S. A. 2012. Technical specifications on the harmonised monitoring and reporting of
antimicrobial resistance in Salmonella, Campylobacter and indicator Escherichia coli and
Enterococcus spp. bacteria transmitted through food.
EFSA, E. F. S. A. 2013. The European Union summary report on trends and sources of zoonoses,
zoonotic agents and food-borne outbreaks in 2013
EFSA, E. F. S. A. E. 2015. EU Summary Report on antimicrobial resistance in zoonotic and indicator
bacteria from humans, animals and food in 2013
http://ecdc.europa.eu/en/publications/Publications/antimicrobial-resistance-zoonotic-
bacteria-humans-animals-food-EU-summary-report-2013.pdf.
EL-SHIBINY, A., CONNERTON, P. L. & CONNERTON, I. F. 2005. Enumeration and diversity of
campylobacters and bacteriophages isolated during the rearing cycles of free-range and
organic chickens. Appl Environ Microbiol, 71, 1259-66.

51. 48 | P a g e
FSIS, U. F. S. A. I. S. 2010. Compliance guideline for Controlling Salmonella and Campylobacter in
Poultry Third Edition May 2010 http://www.fsis.usda.gov/wps/wcm/connect/6732c082-
af40-415e-9b57-
90533ea4c252/Compliance_Guide_Controling_Salmonella_Campylobacter_Poultry_0510.pd
f?MOD=AJPERES. FSIS.
GAL-MOR, O., BOYLE, E. C. & GRASSL, G. A. 2014. Same species, different diseases: how and why
typhoidal and non-typhoidal Salmonella enterica serovars differ. Frontiers in Microbiology, 5,
391.
INSTITUTE, N. A. M. 2015. The United States Meat Industry at a glance - NAMI Web page
https://www.meatinstitute.org/index.php?ht=d/sp/i/47465/pid/47465%20Meat%20industr
y%202013.
ISO, I. O. F. S. 2002. ISO 6579:2002 Microbiology of food and animal feeding stuffs -- Horizontal
method for the detection of Salmonella spp. .
ISO, I. O. F. S. 2005. ISO 22000 - Food Safety Management.
ISO, I. O. F. S. 2006. ISO 10272:2006 Microbiology of food and animal feeding stuffs -- Horizontal
method for detection and enumeration of Campylobacter spp
http://www.iso.org/iso/catalogue_detail.htm?csnumber=37091.
ISO, I. O. F. S. 2011. ISO 9000 Family http://www.iso.org/iso/iso_9000.
K. VIDENOVA, D. K. J. M. 2012. Availability of vaccines against major animal diseases in the European
Union http://web.oie.int/boutique/extrait/22videnova971978.pdf.
LUANGTONGKUM, T., JEON, B., HAN, J., PLUMMER, P., LOGUE, C. M. & ZHANG, Q. 2009. Antibiotic
resistance in Campylobacter: emergence, transmission and persistence. Future Microbiol, 4,
189-200.
MAHENDRA H. KOTHARY, U. S. B., US FOOD AND DRUG ADMINISTRATION FDA 2001. Infective Dose
of Foodborne Pathogens In Volunteers: A Review

52. 49 | P a g e
MAIJALA, R., RANTA, J., SEUNA, E. & PELTOLA, J. 2005. The efficiency of the Finnish Salmonella
Control Programme. Food Control, 16, 669-675.
MAJOWICZ, S. E., MUSTO, J., SCALLAN, E., ANGULO, F. J., KIRK, M., O'BRIEN, S. J., JONES, T. F., FAZIL,
A. & HOEKSTRA, R. M. 2010. The global burden of nontyphoidal Salmonella gastroenteritis.
Clin Infect Dis, 50, 882-9.
NPIP, U. A. A. P. H. I. S. 2014. National Poultry Improvement Plan Program Standards August 2014
https://www.poultryimprovement.org/documents/ProgramStandardsAugust2014.pdf.
OIE, W. O. F. A. H. 2010a. Manual of Diagnostic Tests and Vaccines for Terrestrial Animals CHAPTER
2.9.9. SALMONELLOSIS
http://www.oie.int/fileadmin/Home/eng/Health_standards/tahm/2.09.09_SALMONELLOSIS.
pdf.
OIE, W. O. F. A. H. 2010b. Manual of Diagnostic Tests and Vaccines for Terrestrial Animals
http://www.oie.int/manual-of-diagnostic-tests-and-vaccines-for-terrestrial-animals/.
OIE, W. O. F. A. H. 2015a. OIE Terrestrial Animal Health Code Chapter 6.3 The control of hazards of
animal health and public health importance in animal feed
http://www.oie.int/fileadmin/Home/eng/Health_standards/tahc/2010/chapitre_control_fe
ed_hazard.pdf.
OIE, W. O. F. A. H. 2015b. OIE Terrestrial Animal Health Code http://www.oie.int/international-
standard-setting/terrestrial-code/access-online/.
OIE, W. O. F. A. H. 2015c. Terrestrial Animal Health Code Ch.6.5 Pevention, detection and Control of
Salmonella in poultry
OIE, W. O. F. A. H. 2015d. Terrestrial Animal Health Code Ch. 6.4 Biosecurity procedures in poultry
production
http://www.oie.int/index.php?id=169&L=0&htmfile=chapitre_biosecu_poul_production.ht
m.

53. 50 | P a g e
OIE, W. O. F. A. H. 2015e. Terrestrial Animal Health Code Chapter 6.9 RESPONSIBLE AND PRUDENT
USE OF ANTIMICROBIAL AGENTS IN VETERINARY MEDICINE
http://www.oie.int/fileadmin/Home/eng/Health_standards/tahc/2010/chapitre_antibio_us
e.pdf.
OIE, W. O. F. A. H. 2015f. Terrestrial Animal Health Code Chapter 6.10 RISK ANALYSIS FOR
ANTIMICROBIAL RESISTANCE ARISING FROM THE USE OF ANTIMICROBIAL AGENTS IN
ANIMALS
http://www.oie.int/fileadmin/Home/eng/Health_standards/tahc/2010/chapitre_antibio_ris
k_ass.pdf.
PAUL-EHRLICH-INSTITUTE 2015. Paul-Ehrlich Institute Web Page - Vaccines for Poultry
http://www.pei.de/EN/medicinal-products/vaccines-veterinary/poultry/poultry-node.html.
POULTRY.NET, W. 2014. Current trends in US egg industry
http://www.worldpoultry.net/Layers/Markets-Trade/2014/1/Current-trends-in-the-US-egg-
industry-1422034W/.
SCANES, C. G. 2007. The Global Importance of Poultry. Poultry Science, 86, 1057-1058.
STERN, N. J., MEINERSMANN, R. J. & DICKERSON, H. W. 1990. Influence of antibody treatment of
Campylobacter jejuni on the dose required to colonize chicks. Avian Dis, 34, 595-601.
STERN, N. J., SVETOCH, E. A., ERUSLANOV, B. V., PERELYGIN, V. V., MITSEVICH, E. V., MITSEVICH, I. P.,
POKHILENKO, V. D., LEVCHUK, V. P., SVETOCH, O. E. & SEAL, B. S. 2006. Isolation of a
Lactobacillus salivarius strain and purification of its bacteriocin, which is inhibitory to
Campylobacter jejuni in the chicken gastrointestinal system. Antimicrob Agents Chemother,
50, 3111-6.
US CODE OF FEDERAL REGULATIONS, C. 1998. AGENCY ORGANIZATION AND TERMINOLOGY;
MANDATORY MEAT AND POULTRY PRODUCTS INSPECTION AND VOLUNTARY INSPECTION
AND CERTIFICATION http://www.ecfr.gov/cgi-bin/text-

54. 51 | P a g e
idx?SID=cdc009ebf3bf8fe6572252c3ec3ea154&mc=true&tpl=/ecfrbrowse/Title09/9chapterI
II.tpl.
US FDA CENTRE FOR VETERINARY MEDICINE, C. 2015. Approved Animal Drug Products (Green Book)
http://www.fda.gov/AnimalVeterinary/Products/ApprovedAnimalDrugProducts/default.htm
.
US FOOD AND DRUG ADMINISTRATION, F. 2014. Overview of FDA’s Animal Feed Safety System
http://www.fda.gov/downloads/AnimalVeterinary/SafetyHealth/AnimalFeedSafetySystemA
FSS/UCM277673.pdf.
WHO, W. H. O. 2009. Salmonella and Campylobacter in chicken meat. Meeting Report
http://apps.who.int/iris/bitstream/10665/44211/1/9789241547901_eng.pdf?ua=1.
WWW.WHITEHOUSE.GOV 2015. Whitehouse.gov Web page - The Judicial Branch
https://www.whitehouse.gov/1600/judicial-branch.