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The international trade of poultry meat:
legislation and requirements for Salmonella
1 - DVM, Ph.D., Professor of Poultry Health,
Dean of the Faculty of Veterinary Medicine,
Federal University of Rio Grande do Sul (UFRGS),
Av. Bento Gonçalves, 9090
Porto Alegre - RS - CEP: 91.540-000 – BRAZIL
2 - DVM, Ph.D., Professor of Poultry Health,
University of Passo Fundo (UPF)
3 - DVM, M.Sc., Professor of Poultry Health
(National University of Colombia); Ph.D. student,
(Faculty of Veterinary Medicine, UFRGS).
4 - DVM, M.Sc., Ph.D. student (Faculty of
Veterinary Medicine, UFRGS).
5 - DVM, Ph.D., Professor of Poultry Health,
Tuiuty-Paraná University (UTP)
[email protected]
Introduction
T
he poultry industry is one of the most
important sectors of the Brazilian agribusiness.
In addition of being extremely important
for economy due to the billions of dollars
generated by exports, the poultry industry has a
very relevant social role as it employs thousands
of people all over the country. Global exports of
chicken meat increased 11.4% in 2007, with 7.2
million metric tons (MT). Brazil had a 45% share in
this international market, maintaining its positions
as the greatest world exporter of chicken meat.
During the period of 1984 to 2007, chicken
meat per capita consumption in Brazil increased
from 7 kg to 38.2 kg. In addition to this significant
growth of the domestic market, the expansion of
production has led Brazil to increase its share in the
foreign market. Chicken meat exports started in
1975, with about 3,500 MT, reached in 2007 the
According to the United States Department of
Agriculture (USDA), global production of chicken
meat increased 6.2% in 2007, from 64 to 68
million MT. Brazilian production in 2007 was 10.2
million MT, maintaining the country in the position
of third largest world producer, following the USA
and China, which produced 16.2 and 11.5 million
MT, respectively. ABEF reported that the exports
of chicken meat cuts summed up 1.8 million MT
with revenues of USD 2.7 billion in 2007. The main
Brazilian chicken cuts markets are Asia (particularly
Japan and Hong Kong) and the European Union
(mainly the Netherlands and Germany). The exports
of whole chickens amounted to 1.1 million MT,
with revenues of USD 1.4 billion, and are mostly
directed to the Middle East (mainly to Saudi Arabia,
Arab Emirates, Yemen, and Kuwait) as well as to
Venezuela, Russia and Angola.
Between January and October of 2008, Brazilian
chicken exports reached 3.1 million MT, representing
a 17% increase compared with the same period in
2007 (during those 10 months of 2008, revenues
totaled USD 6 billion or a 54% increase compared
with 2007) (ABEF, 2008). In order to process most
of its poultry production, Brazil currently has 184
processing plants with federal inspection services.
As mentioned above, it must be highlighted the
poultry production chain has acquired increasing
social and economic importance in Brazil. Taking
the specific case of broiler production in the state
of Rio Grande do Sul (RS), in 2004 the number of
contracted farmers was 10,500 with more than
13,000 broiler houses distributed in 134 counties.
Broilers are produced mainly in small farms
and are an excellent alternative for production
diversification (ASGAV, 2005a,b). In Brazil, UBA
data (2007) indicate a number of 4 million Jobs
linked to poultry production, with obvious social
Area: Food Safety • August 08
V.P. Nascimento, L.R. Santos, L.B. Rodrigues, M.P. Landinez, G. Perdoncini, Y.M. Sierra and A. Borsoi
impressive volume of 3.2 million MT, representing
an increase of more than 91,000% and revenues of
almost USD 5 billion. Despite the increasing share
in the international market, the supply of chicken
meat to the domestic market is still plenty (ABEF Associação Brasileira dos Exportadores de Frango,
2007).
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V.P. Nascimento, L.R. Santos, L.B. Rodrigues, M.P. Landinez, G. Perdoncini, Y.M. Sierra and A. Borsoi
consequences. Because poultry production adopts
associativist or contract systems, it allows farmers
to retain their properties as it makes small farms
economically feasible by providing working capital
and technology and by ensuring the sales of their
flocks. In the state of Rio Grande do Sul, there are
about 40,000 families – mostly small-farm owners –
directly linked to broiler and egg production, which
generate 45,000 direct and 800,000 indirect job
posts.
Poultry production also contributes to improve
soil physical and chemical qualities, as a considerable
volume of organic fertilizer is added to crops in small
farms, increasing the production of crops. In addition,
cooperatives and poultry companies provide the
farmers with cutting-edge genetic, nutrition and
health technologies. Another important aspect is
that poultry production supplies an affordable food
source for low-income populations.
When considering the current global scenario,
together with the remarkable progress in
technology, there is a growing public concern with
food quality and safety. This concern is evident
not only in the so-called developed countries, but
also those still developing as a result both of the
improvement of the social and economic conditions
of their populations and of the expansion of the
access to information (CAC, 2001).
For decades, food microbiological safety was
exclusively based on complying with pre-established
microbiological standards and criteria. This
required food safety surveillance agencies and food
companies to conduct microbiological analyses to
determine the compliance with those criteria and
standards, and therefore, if products were safe
for human consumption. However, it was soon
perceived that those analyses were limited as tools
Risk analysis
Risk
assessment
Risk
management
Risk communication
Figure 1 - Risk analysis structure (CAC, 1999).
2
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to ensure food safety, particularly when there are
low contamination levels. For instance, when there
is one contaminated unit in a batch of 200 food
products (0.5%), even if 100 units are analyzed,
the probability of mistakenly approve the batch
is 61% (ICMSF, 2002). In addition to sampling
method and size, there are other issues involved,
such as method of analysis, microbiological limits
of each pathogen, and microbial ecology in the
product. Microbiological standards and criteria can
be applied to finished products, but make little or
no contribution to solve contamination issues in the
processing line (Reij and Schothorst, 2000).
The international trade of food is growing,
bringing economic and social benefits. Also feedings
habits have changed in many countries during the
last two decades, inspiring the development of
new food production, preparation, and distribution
techniques (CAC, 2001). This has required a proactive attitude from food producers, using other
tools to ensure food safety. One of these tools is the
HACCP system (Hazard Analysis and Critical Control
Points) applied to food processing lines. However,
its efficacy requires the previous implementation
of good hygiene practices (Whiting and Buchanan,
1997). The main focus of the HACCP system is to
identify and control process steps that influence the
production of safe food. This system has proven
to be very effective for the control of physical,
chemical, and biological hazards in foods. However,
one of its main disadvantages is that it is difficult to
compare different HACCP plans as it is not possible
to assess if they provide the same level of protection
to the final consumer (ICMSF, 1998; ICMSF, 2002).
The existence of these limitations, together with
the need of properly estimating potential food safety
impacts on public health as well as the economic
costs associated to foodborne diseases, resulted in
the development of this new safety management
tool called Risk Analysis (Whiting and Buchanan,
1997). The concept of microbiological risk analysis
has been increasingly accepted for the management
of microbiological hazards in food. A risk analysis is
a structured and systematic process that integrates
information from several sources on the origin and
destruction of pathogens along the production
chain and that determines the magnitude of public
health risks (Lammerding, 2006).
According to the internationally accepted
concept, the Risk Analysis process consists of three
components: Risk Assessment, Risk Management,
and Risk Communication (CAC, 1999; ICMSF, 2002;
Schlundt, 2002), as shown in Figure 1.
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Salmonella in poultry and
its importance in food
processing and public health
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V.P. Nascimento, L.R. Santos, L.B. Rodrigues, M.P. Landinez, G. Perdoncini, Y.M. Sierra and A. Borsoi
Risk analysis
There
are
interactions among
the elements of Risk
Analysis
(Figure
2). In this structure,
5. Risk
the
individual
4. Risk
assessment
characterization
responsible for risk
management
(risk
manager) determines
6. Options
4. Risk
assessment
which hazard is
2. Hazart
characterization
3. Exposure
under consideration
characterization
assessment
(Figure 2, item 1),
7.
2. Options
Hazart
3. Exposure
whereas the person
implementation
1. Hazard assessment
characterization
responsible
for
identification
Risk Analysis (risk
8. Monitoring
assessor)
provides
Risk assessment
and review
Risk
assessment
information
on
the behavior and
other
important
characteristics
of
Risk communication
the selected hazard
(Figure 2, item 2).
Figure 2 - Structure of Risk Assessment as defined by the Codex Alimentarius (FAO/
The risk assessor
WHO, 1997).
then
determined
the level of hazard
exposure using both
used as a tool to analyze which are the best way(s)
product analysis and the complete description of the
to reduce this risk (Hope et al., 2002).
path followed by the raw material from transport,
processing, and storage up to consumption (Figure
2, item 3). Therefore, the different hazard levels
can be estimated under several situations and/or
circumstances, as well as the probability of public
exposure. Finally, the risk assessor combines the
hazard exposure data with information on the doseresponse ratio and severity of the effects to provide
a final risk estimate (Figure 2, item 4). Based on
Avian salmonellosis is a term that designates a
this estimate, the task of the risk manager is to
group of acute or chronic diseases caused by one
evaluate the risk considering not only its scientific
or more species of the genus Salmonella, which
characteristics, but also its social, ethic and economic
belongs to the family Enterobacteriaceae. More
consequences to decide which actions are needed
than 2,500 serovars belong to that genus and are
to be implemented (Figure 2, items 6 and 7). The
differentiated based on chemical and serological
estimated risk, therefore, must be clearly presented;
reactions (Popoff and Le Minor, 1997). Several
for instance, “the risk of an immunocompromised
species can be isolated from poultry, which are the
individual to become severely ill due to listeriosis
largest individual reservoir of Salmonella in nature
acquired by the consumption of 100g of vacuum(Snoeyenbos and Williams, 1991) and are important
packed salami is lower than 1 in one million.”
vectors of foodborne Salmonella infections in
Moreover, the entire system must be constantly
humans.
monitored and regularly reviewed (Figure 2, item
8) (Reij and Schothorst, 2000).
According to Todd (1989), economic losses due
to food poisoning in the USA and Canada amount
This model is also very useful for pathogen
to USD 8.4 billion and approximately 50% of this
reduction programs and implementation of Hazard
cost is due to diseases caused by Salmonella. Pivinick
Analysis and Critical Control Points (HACCP),
(1978) showed that the incidence of Salmonella in
because the primary objective of a Risk Analysis of
poultry carcasses in Canada increased from 15% to
foodborne pathogens with no or few epidemiological
39% during the period of 1970 to 1977.
data should not be to predict the risk; rather, to be
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V.P. Nascimento, L.R. Santos, L.B. Rodrigues, M.P. Landinez, G. Perdoncini, Y.M. Sierra and A. Borsoi
According to WHO, the genus Salmonella is
the most frequent microorganism implicated in
foodborne diseases of bacterial origin around the
world. That agent is typically transmitted to humans
by the consumption of animal food products, such
as meat, eggs, and milk.
There are several studies on the incidence of
Salmonella in the meat of poultry collect in retail
stores. Straver et al. (2007) quantified Salmonella
in 220 chicken breast fillet samples collected in
retail stores and determined that 19 samples (8.6%)
had Salmonella counts higher than 10 MPN (most
probable number) and only 0.8% samples presented
counts higher than 3 log10.
Trajkovic et al. (2007), analyzing 90 fresh meat
samples from retail stores in Serbia, determined that
3.3% of the poultry samples were contaminated
with Salmonella. According to Varnam and Evans
(1991), the infecting dose for healthy persons is
105-107 colony-forming units (CFU). Nascimento
and Silva (1994) observed that literature indicates
that a small number of Salmonella microorganisms
is sufficient to infect humans and a single
microorganism can trigger food poisoning.
Salmonella infection in humans is influenced
by serovar, strain, infecting dose, nature of the
contaminated food, and host’s health status.
Children, immunocompromised patients and those
infected with blood diseases are more susceptible
to Salmonella infection than adult humans. Some
serovars are highly pathogenic for humans, but the
virulence of some rare serovars is still unknown.
Also, strains belonging to the same serovar may
present different pathogenicity.
In a study on the incidence of Salmonella in five
different fresh meat products sold at retail in New
Zealand, Wong et al. (2007) found 3% prevalence
in poultry meat and one of serotypes isolated,
Salmonella typhimurium PT1, was phenotypically
and serologically similar to the attenuated serotype
used in the poultry vaccine MeganVac1.
As to the influence of environmental factors
on carcass contamination, the study of Arsenault
et al. (2007) should be mentioned. Those authors
analyzed the prevalence and risk factors of broiler
carcasses contamination with Salmonella. A
prevalence of 21.2% was determined, and the
following risk factors were identified: birds with cecal
culture positive for Salmonella, low rainfall during
transport to the processing plant, temperatures
higher or equal to 0 °C during transport to the
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processing plant and lairage times longer than 4
hours.
In the state of Rio Grande do Sul, Brazil,
Nascimento et al. (2003) described the prevalence
of Salmonella in broiler carcasses and cuts and
the main serovars isolated. Out of the sampled
carcasses, 15.1% whole carcasses and 26.1% cuts
(drumette: 25.6%, breast meat: 25.6%, leg: 30.3%
and back: 31.0%) were positive. The main serovars
identified were S. Enteritidis (51%), S. Hadar (26%)
and S. Heidelberg (11%).
International food trade
As mentioned above, during the last few years
Brazil has consolidated its position at the world
largest food exporter, including animal proteins.
Simultaneously, new restrictions emerge in the
international food trade. According to Milner
(1997), the increase in the volume of manufactured
products submitted to non-tariff controls – from
less than 1% in 1974 to about de 20% in 1985
– significantly enhanced the importance of healthregulating agencies. That author showed that as
tariff restrictions were reduced in international
trade, there was a significant increase in application
of non-tariff restrictions, particularly those related
to health issues.
In an attempt to change this scenario, the World
Trade Organization (WTO) organized a negotiation
round among the member countries to regulate the
main aspects of international trade. The principle
of equivalence was then adopted by the WTO
to facilitate trade while protecting consumers’
health (Codex Alimentarius, 2007b). During these
meetings, known as the Uruguay Round, norms for
the Application of Sanitary and Phytosanitary (SPS)
measures by the involved countries.
Those measures determined that, although the
nations have the right to adopt measures to protect
the health of their populations, these measures
should mainly:
a. be applied only to the extent necessary to
protect human health;
b. be based on scientific principles;
c. not be maintained without sufficient scientific
evidence;
d. be based on internationally agreed
recommendations.
In addition, the agreement recommends that a
country should consider measures taken by another
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country as equivalent, provided they ensure the
same safety level to the final product (CAC, 2007b).
Therefore, since the agreement became effective
in 1995, the importance of Risk Analysis has
significantly increased (FAO, 2002) because it allows
comparing two different systems to determine if
they provide the same protection level to the final
consumer (ICMSF, 2002).
In terms of health, microbiological hazards need
to be effectively controlled in order to prevent risks
to consumers’ health and to allow food trade among
countries. In this sense, it should be mentioned that
foodborne disease outbreaks may cause severe
social and economic damage, with losses in terms
of trade and tourism, unemployment and increased
health care costs (CAC, 2001).
Some countries and international agencies,
aiming at minimizing those losses, developed some
microbiological risk analysis studies on some foodpathogen combinations (USDA, 1998; FAO/WHO,
2002; FSANZ, 2005). However, the management of
microbiological hazard risk control is technically very
complex. The food industry has had the responsibility
of providing food safety by operating a set of control
measures related to food hygiene according to
official regulations. Risk Analysis and its components
(risk assessment, management, and communication)
has been recently introduced as a new tool for the
assessment and control of microbiological hazards,
aiming at helping to protect consumers’ health and
to ensure fair international trade practices. It may
also aid the judgment of equivalence of food safety
control systems (FAO/WHO, 1997). According
to the general aspects determined by the Codex
Alimentarius, the main objective of risk analysis
applied to food safety is to ensure human health
In the scenario of products analyzed for Salmonella
spp by third countries, the recommendation of the
WTO for fresh chicken products (whole carcasses
and parts) is that these products should not be
tested at the border as a health barrier against the
entrance of fresh products, because the presence
of Salmonella is allowed in fresh meat products.
However, some countries require a certificate of the
absence of Salmonella spp or of some Salmonella
species in these products, such as the case of the
largest poultry meat importer, Russia, as well as
Singapore and some European Union (EU) countries,
including Sweden, Finland and Denmark.
Processed products not submitted to heat
treatment (salted and seasoned chicken products)
also have specific sanitary certification requirements
by some EU countries. These products account for
a significant number of rapid alerts received by
Brazil due to sampling made at reception in third
countries. Cooked products, because they are
submitted to heat treatment, have low detection
risk, and there has been no record of Salmonella in
these exported products.
Processed chicken products had a participation
in the portfolio of exports of 155,000 MT in 2007,
with revenues of USD 402 million, whereas salted
meats accounted for 124,000 MT and USD 356
million in revenues during the same period. The EU
was the main customer of both segments.
In Brazil, a recent study carried out by the
National Agency of Health Surveillance (Agência
Nacional de Vigilância Sanitária – ANVISA) showed
the presence of Salmonella spp. in 3.03% of frozen
poultry carcasses collected in retail stores of 13
states and Federal District between 2004 and 2006
(Brasil, 2008).
V.P. Nascimento, L.R. Santos, L.B. Rodrigues, M.P. Landinez, G. Perdoncini, Y.M. Sierra and A. Borsoi
In a document published in 1997, FAO/WHO
recommends that countries use the approach of Risk
Analysis to ensure the perfect allocation of resources
to programs controlling foods and foodborne
diseases. Moreover, Risk Analysis can be used as
a major determining factor in the development of
any scientifically based system for the control and
prevention of microbiological hazards (Hope et
al., 2002). Risk Analysis has been for more than a
decade a structural model to improve food control
systems aiming at producing safe food, reducing
the number of foodborne diseases, and facilitating
domestic and international food trade. In addition,
this system provides a more comprehensive food
safety approach, as the entire chain needs to be
considered for the production of safe foods (FAO,
2002).
protection (CAC, 2007a). Therefore, the application
of Risk Analysis will support the presence of the
Brazilian government in international negotiation
rounds and reinforce the credibility and acceptance
of its management system of food safety control,
aiming at maintaining the position of Brazil in the
chicken meat international trade.
Aiming at determining the prevalence and
monitoring the incidence of Salmonella spp. to
enhance the efficiency of the control measures in
order to ensure adequate consumers’ protection,
the Brazilian Ministry of Agriculture (MAPA)
established in 2003 the Program for Pathogen
Reduction and Microbiological Monitoring and
Control of Salmonella spp. in Chicken and Turkey
Area: Food Safety • August 08
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Carcasses, applied to poultry and rabbit processing
plants under federal inspection (Brasil, 2003).
V.P. Nascimento, L.R. Santos, L.B. Rodrigues, M.P. Landinez, G. Perdoncini, Y.M. Sierra and A. Borsoi
Applicability
of
Risk
Analysis for Salmonella
and other pathogens in
poultry meat
6
One of the strengths of Risk Analysis (RA) is the
practical applicability of its principles, methodology,
and communication of results. This applicability
includes governmental agencies, processing and
its entire production chain, and reaches household
consumption by informing the risk to the final
consumer, having immediate consequences in
international trade.
At government level, RA provides well-structure
information, allowing the official agencies that
manage risks to identify possible interventions in
the production chain that improve public health
controls. These official interventions include
regulations, revision of the applicable legislation,
development of policies emphasizing public health
education, and to guide new research projects on
areas considered critical. RA is extremely useful for
research because it is flexible and dynamic, allowing
health authorities to direct research lines to sectors
that most affect public health. In summary, RA of
Salmonella spp in poultry meat opens a wide field
of concrete opportunities to establish public policies
that directly affect food safety, and consequently,
the health of the final consumer.
In the poultry meat processing, which is typically
done by private companies, RA also provides many
practical applications for the processing line; health
control along the production chain, particularly at
farm level; and finished product packaging and
labeling, providing clear and precise information
on the risks to the final consumer. Risk analysis
allows processing plants to develop more effective
and efficient HACCP plans by providing them with
technical and scientific foundation. Processing
plants that use RA as a tool to identify risk inherent
to processing can classify risks no longer in
qualitative scales (high, intermediate or low), but in
more accurate terms focused on the final consumer.
The advantage of this change is that the risk will
be defined according to the negative impacts on
human health, instead of according to the possibility
of carcass or finished product contamination as it is
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applied today. Consequently, the process risk can
be measured taking into account the consumption
of the product by the last link of the production
chain, i.e. the final consumer, and no longer the
product itself.
The greatest practical beneficiary of RA is, after
all, the final consumers, as they will be clearly and
objectively informed of the actual possibility of a risk
that is inherent to the product they are purchasing
for consumption. Risk analysis allows informing the
consumers that, when purchasing chicken meat and
consuming a determined amount of this product,
they will be exposed to a controlled risk within an
acceptable safety margin.
Another practical consequence of RA for
Salmonella spp in poultry meat is relative to
international trade. As a tool currently recommended
by the CODEX Alimentarius, RA has an important role
in the meat international trade because countries
that use it to implement food safety governmental
policies are aligned with the technical and scientific
principles determined by international bodies.
Moreover, the principle of equivalence determines
that the health requirements used as reference in
a country can be required by it when importing the
same products from third countries. Therefore, by
adopting the most modern and innovative food
safety governmental policies, Brazil is safeguarded
from possible trade and/or health barriers that may
compromise its chicken meat exports.
If there is no systematic risk analysis, importing
countries can establish barriers not related to food
safety, as previously mentioned, creating artificial
limitations to international trade. Acknowledging
the importance of a scientific-based perspective for
fair trade, WTO recommends that every country
adopts food safety measures based on Risk Analysis.
The CODEX Alimentarius has already determined
the principles to be followed when conducting RA,
and has indicated it may be included as a standard
tool for establishing food safety public policies.
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