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

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

3.3.2 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).

0

10

20

30

40

50

60

70

80

2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014

% P

reva

len

cePrevalence 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

% P

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Percentage of Salmonella positive chickens positive for S. Enteritidis or S. Typhimurium in the EU 2005-2013

S. Enteritidis S. Typhimurium

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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.

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).

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cePrevalence of S. Enteritidis and S. Typimurium in human salmonellosis in

the US 2005 - 2012

Typhimurium Enteritidis

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S. Enteritidis S. Typhimurium

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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

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

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).

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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).

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(A) Antimicrobial resistance in S. Enteritidis isolates from chickens in the EU 2007-2013

Ampicillin Nalidixic Acid Sulfonamides Tetracyclins Ciprofloxacin

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(B) Antimicrobial resistance in S. Typhimurium isolates from chickens in the EU 2007-2013

Ampicillin Nalidixic Acid Sulfonamides Tetracyclins Ciprofloxacin

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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).

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(A) Antimicrobial resistance in S. Enteritids isolates from chickens in the US 2005-2011

Ampicillin Chloramphenicol Tetracycline

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(B) Antimicrobial resistance in S. Typhimurium isolates from chickens in the US 2005-2011

Ampicillin Chloramphenicol Tetracycline

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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).

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(A) Antimicrobial resistance in S. Enteritidis isolates from humans in the EU 2009-2013

Ampicillin Nalidixic Acid Streptomycin

Sulfonamides Tetracyclins Ciprofloxacin

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2008.5 2009 2009.5 2010 2010.5 2011 2011.5 2012 2012.5 2013 2013.5

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(B) Antimicrobial resistance in S. Typhimurium isolates from humans in the EU 2009-2013

Ampicillin Nalidixic Acid Streptomycin

Sulfonamides Tetracyclins Ciprofloxacin

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

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Ampicillin Chloramphenicol Tetracycline

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(A) Antimicrobial resistance in S. Typhimurium isolates from humans in the

US from 2004-2011

Ampicillin Chloramphenicol Tetracycline

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).

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(A) Antimicrobial resistance in C. Jejuni isolates from chickens in the EU 2005-2013

Tetracyclines Quinolones

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(B) Antimicrobial resistance in C. Coli isolates from Chickens in the EU 2005 -2013

Tetracyclines Quinolones

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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.

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Tetracyclines Quinolones

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Antimicrobial resistance in C. Coli isolates from chickens in the US 2004-2011

Tetracyclines Quinolones

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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).

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(A) Antimicrobial Resistance in C. Jejuni isolates from humans in the EU 2009-2013

Tetracyclines Nalidixic Acid Ciprofloxacin Ampicilin

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(B) Antimicrobial Resistance in C. Coli isolates from humans in the EU 2009-2013

Tetracyclines Nalidixic Acid Ciprofloxacin Ampicillin

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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.

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2013

Tetracyclines Nalidixic Acid Ciprofloxacin

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(B) Antimicrobial resistance in C. Coli isolates from humans in the US 2004-2013

Tetracyclines Nalidixic Acid Ciprofloxacin

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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).

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).

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).

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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

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

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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

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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

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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.

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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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CENTRE FOR DISEASE CONTROL AND PREVENTION, C. 2010. Multistate Outbreak of Human

Salmonella Enteritidis Infections Associated with Shell Eggs

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New Animal Drugs with Regard to Their Microbiological Effects on Bacteria of Human Health

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