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Impact of Avian Influenza on Village Poultry Production
Globally
Robyn Alders,
1,2,3,4
Joseph Adongo Awuni,
5
Brigitte Bagnol,
2,3,4,6
Penny Farrell,
1
and Nicolene de Haan
7
1
Faculty of Veterinary Science, University of Sydney, 425 Werombi Road, Camden, NSW 2570, Australia
2
International Rural Poultry Centre, Kyeema Foundation, Brisbane, QLD, Australia
3
International Rural Poultry Centre, Kyeema Foundation, C.P. 1168, Maputo, Mozambique
4
Infectious Disease and Global Health Department, Cummings School of Veterinary Medicine at Tufts University, Grafton, MA
5
Accra Veterinary Laboratory, Veterinary Services Directorate, Box M 161, Accra, Ghana
6
Department of Anthropology, University of the Witwatersrand, Johannesburg, South Africa
7
Food and Agriculture Organization of the United Nations, Rome, Italy
Abstract: Village poultry and their ownerswere frequently implicated in diseasetransmission in the earlydays of the
highly pathogenic avian influenza (HPAI) H5N1 pandemic. With improved understanding of the epidemiology of
the disease, it was recognized that village poultry raised under extensive conditions pose less of a threat than
intensively raised poultry of homogeneous genetic stock with poor biosecurity. This paper provides an overview of
village poultry production and the multiple ways that the HPAI H5N1 pandemic has impacted on village poultry,
their owners, and the traders whose livelihoods are intimately linked to these birds. It reviews impact in terms of
gender and cultural issues; food security; village poultry value chains; approaches to biosecurity; marketing; poultry
disease prevention and control; compensation; genetic diversity;poultry as part of livelihood strategies; and effective
communication. It concludes on a positive note that there is growing awareness amongst animal health providers of
the importance of facilitating culturally sensitive dialogue to develop HPAI prevention and control options.
Keywords: family poultry, food security, gender, genetic diversity, poultry value chain, poultry disease
INTRODUCTION
Highly pathogenic avian influenza (HPAI) was first re-
ported in Italy in 1878 (Stubbs 1965). Up until the late
1800s, the contact structure and small size of extensive and
semi-intensive chicken flocks meant that emerging diseases
could not spread easily (Swayne and Halvorson 2003) and
would therefore burn themselves out in a localized fashion.
Swayne and Halvorson (2003) identified five distinct man-
made ecosystems that have impacted avian influenza (AI)
virus ecology: (1) integrated indoor commercial poultry,
(2) range-raised commercial poultry, (3) live poultry
markets (LPMs), (4) backyard and hobby flocks, and (5)
bird collection and trading systems. In addition, the evo-
lution of HPAI would have faced similar drivers as new
variants of virulent Newcastle disease virus (vNDV) due to
the following characteristics of current poultry production
systems including: (1) host genetic homogeneity (with few
host adaptive bottlenecks), (2) high density rearing
(allowing close animal-to-animal contact and favoring
Correspondence to: Robyn Alders, e-mail: robyn.alders@sydney.edu.au
EcoHealth
DOI: 10.1007/s10393-013-0867-x
Review
2013 International Association for Ecology and Health
transmission of vNDV over low pathogenic NDV), and (3)
intensive vaccination programs (which provide selective
immune pressures and may be executed improperly in
developing countries; Higgins and Shortridge 1988).
In the 1990s, prior to the HPAI H5N1 pandemic, the
world’s poultry population grew by 23% in developed
countries and 76% in developing countries (Branckaert
et al. 2000). This spectacular increase was largely the result
of increased commercial production, notably in the Far
East where growth averaged 90%. Until the 1990s, the
highly pathogenic form of AI had caused sporadic high
mortality in poultry (reported mainly in commercial
chicken units) in a small number of countries (Capua and
Alexander 2009). Since 2003 it has received unprecedented
international attention as outbreaks of HPAI have become
more common (Capua and Alexander 2006).
Village poultry can include a wide range of birds
including indigenous and crossbred breeds of chickens,
quail, mallard and Muscovy ducks, pigeons, guinea fowl,
geese, and turkeys (Alders 2012a). They are raised in vil-
lages for food, eggs, as pets, or for social or religious uses
usually in small flocks usually of 1–50 birds (Alders and
Pym 2009) and with no more than 100 multi-age birds
(Gue
`ye 1998; Martin 1992; Sonaiya 2009; Sultana et al.
2012). Of these birds, chickens, quail, guinea fowl, and
turkeys are highly susceptible to HPAI (Perkins and Swayne
2003). Prior to the emergence of HPAI H5N1, mallard
ducks and pigeons were thought to be resistant to the
disease but recent reports suggest that these birds may
replicate and occasionally succumb to HPAI (Hulse-Post
et al. 2005; Jia et al. 2008; Werner et al. 2007).
In the last decade of the twentieth century, village
poultry production contributed 70% of total poultry
production in most low income, food-deficit countries
(Branckaert et al. 2000). In the twenty-first century, vil-
lage poultry continue to make critically important con-
tributions in many countries to poverty alleviation,
household food security, women’s empowerment, HIV/
AIDS mitigation, and wildlife conservation (Alders and
Pym 2009).
Village poultry production was frequently implicated
in the transmission of HPAI N5N1 in the early days of the
pandemic (GRAIN 2006). Subsequently, epidemiological
studies have traced the movement of this virus and dem-
onstrated that this disease, which is highly fatal to poultry,
requires a high density of, and frequent movement be-
tween, susceptible flocks which are more commonly asso-
ciated with intensive production (FAO 2011). Despite this
knowledge, information suggesting the relatively greater
role of extensively raised village poultry, in relation to
intensive, commercial production, in the introduction and
transmission of HPAI persists. This misunderstanding
continues to impact negatively on these birds and their
owners as investment in extensive and semi-intensive
smallholder poultry production reduced considerably
during the years immediately following the H5N1 pan-
demic (Hong Hanh et al. 2007)
In this paper we will provide an overview of the
multiple ways that the HPAI H5N1 pandemic has impacted
on village poultry, their owners, and the traders whose
livelihoods are intimately linked to these birds. It reviews
impact in terms of gender and cultural issues; food security;
village poultry value chains; approaches to biosecurity;
marketing; poultry disease prevention and control; com-
pensation; genetic diversity; poultry as part of livelihood
strategies; and effective communication.
GENDER AND CULTURAL ISSUES
Poultry and people have had a shared history in many parts
of the world and are frequently an essential part of the
fabric of societies across a broad range of cultures (Alders
2012a). Village poultry producers include the men, women,
and children who make up households that raise poultry.
The demography of producers varies globally with women
and children generally being more likely to be in charge of
extensively raised village poultry and men more likely to
own and provide labor in small-scale intensive poultry
production (Alders and Pym 2009; Bagnol 2009a). The
reason for producing poultry also varies from the need to
provide petty cash, household food and for ceremonies to a
primarily commercial venture (Alders and Pym 2009;
Bagnol 2009a; Sonaiya 2009).
In countries where village poultry production pre-
dominates, women, especially those from female-headed
households, frequently derive a significant percentage of
their income from poultry production (Alders and Pym
2009; Bush 2006; Gue
`ye 2005). Some of the most com-
pelling reasons for women to engage in poultry farming are
because of the small size of investment needed, the hardi-
ness of the animal, the limited barriers to entering and
exiting the poultry value chain, and the ease of doing it
from their homes (Alders and Pym 2009; Bagnol 2009a;
Sonaiya 2009; Sultana et al. 2012). Women, who are fre-
quently the primary owners and managers of village
R. Alders et al.
chickens, were considered most adversely affected by HPAI
outbreaks and associated control programs (Bush 2006).
FOOD SECURITY
Approximately 20% of the protein consumed in developing
countries comes from poultry meat and eggs (Branckaert
et al 2000). Indigenous poultry breeds, which have evolved
in village environments, are excellent scavengers, trans-
forming feed resources considered unsuitable for human
consumption into high-quality products such as poultry
meat and eggs. Village poultry production is ideally suited
to rural areas where the conditions for a successful com-
mercial poultry sector are rarely met. The ability of indig-
enous breeds to scavenge, to flee predators, to lay and hatch
their own eggs and to contribute to pest control results in a
production system that complements other farm activities
without directly competing with humans for cereal crops
(Alders 2012a). In some farming systems, they provide vital
support for crop production, by ensuring funds to source
seeds for planting, and labor through feeding neighbors or
laborers during planting and harvesting (Sultana et al.
2012), especially for women who might not have access to
labor or a bank account (Alders et al. 2007). The other
aspect that is often underestimated is the ability of chickens
to produce eggs throughout the year, to fulfill needs,
whereas crops frequently have one specific harvest and
income period.
In the wake of the HPAI H5N1 pandemic, millions of
poultry have been killed or slaughtered to control the
spread of the disease. To date, over 50 million domestic
birds have been slaughtered in Vietnam alone due to HPAI
infection (Gutie
´rrez et al. 2009; Velasco et al. 2008).
Widespread culling of family poultry has impacted on
vulnerable households, including those headed by women,
contributing to increased stunting in children under five in
Egypt (FAO 2009) and decreased enrolment of girls in
school in Turkey post HPAI H5N1 control activities
(Bagnol 2009a). Economic losses in the South East Asia
region have totalled around US $10 billion (Gilbert et al.
2008) which has had direct and indirect effects on food
security.
The HPAI H5N1 pandemic has also highlighted the
readiness of vulnerable households to slaughter and con-
sume either unhealthy birds or carcasses of poultry that
have died of infectious disease because of food insecurity, a
practice which pre-dates the HPAI H5N1 pandemic (Alders
et al. 2012). Improving overall production levels of poultry,
including the effective and efficient prevention and control
of all important poultry diseases, will help to reduce such
practices (Alders et al. 2012; Azhar et al. 2010; Hickler
2007).
UNDERSTANDING VILLAGE POULTRY VALUE
CHAINS
Value chain analysis has proved a crucial tool in the
development of appropriate HPAI prevention and control
strategies (McLeod et al. 2009). A comprehensive analysis
of value chains includes the social and cultural aspects of
the food system and also encompasses the institutional
environment in which food is produced, processed, mar-
keted, retailed, and consumed. The formal rules (public
legislation and private standards) and the informal rules
(social and cultural aspects) and their enforcement impact
on agricultural value chains and their wider innovation
system performance (Taylor and Rushton 2011). The
application of a value chain approach to HPAI risk man-
agement has helped to identify key constraints that, when
addressed, also contribute positively to food security
(Taylor and Rushton 2011).
UNDERSTANDING OF AND APPROACHES TO
BIOSECURITY
Biosecurity is the implementation of measures that reduce
the risk of the introduction and spread of disease agents.
Biosecurity requires the adoption of a set of attitudes,
behaviors (including production systems), and motivation
of people to reduce risk in all activities involving
domestic, captive exotic, and wild birds and their pro-
ducts (FAO 2008). Biosecurity does not start or stop at
the household or farm gate. Considering biosecurity along
the whole value chain is important, including in live bird
markets (FAO 2010), and between markets and the pro-
ducer’s home. Economically sustainable and feasible bio-
security measures need to match the production system
involved and the disease risks inherent in that system.
Biosecurity measures have been studied in detail in
commercial poultry because it is an essential component
of the intensive production system where the high density
of genetically uniform birds greatly increases risks of
disease outbreaks.
Impact of Avian Influenza on Village Poultry
In the early days of the HPAI H5N1 outbreak, the
readily available approaches to biosecurity in the com-
mercial sector tended to be applied as a ‘‘one size fits all’’
across all poultry production systems (FAO 2008). How-
ever, it was found that biosecurity measures used for
intensively raised birds are not necessary appropriate for
extensively raised birds. Applying conventional biosecurity
principles to village poultry production is especially chal-
lenging because of the wide range of perceptions about the
origin of disease. Where communities have had limited
access to formal education and are unfamiliar with the
concept that disease is caused by pathogens, most con-
ventional recommendations on disease prevention and
control will be difficult to comprehend (Alders and Bagnol
2007).
The epidemiological unit is a crucial factor when
planning and implementing biosecurity measures. With
commercial poultry, the epidemiological unit is at the level
of the poultry shed or poultry farm. In the early days of the
HPAI H5N1 outbreak, there was an assumption that ‘‘vil-
lage poultry’’ where similar to ‘‘backyard poultry’’ [which
are confined to a defined area and not in contact with other
household flocks (Smith and Dunipace 2011)] and so the
household was chosen as the appropriate unit for family
poultry disease control interventions. Significant progress
in the approaches to the control of HPAI in village poultry
was made when it became widely accepted that the
appropriate epidemiological unit was the village (Alders
and Bagnol 2007; Azhar et al. 2010) and therefore required
investment in developing biosecurity measures in collabo-
ration with communities. Subsequently, initiatives that
involve family poultry producers in discussions on appro-
priate biosecurity measures in Indonesia have yielded
excellent results as demonstrated in the case study below.
EXAMPLES FROM INDONESIA ON BEST
BIOSECURITY PRACTICES FOR VILLAGE
POULTRY
Indonesia’s Village Biosecurity, Education and Communi-
cation (VBEC) programme began in August 2009 with a
qualitative and quantitative socio-cultural assessment in six
pilot villages to assess community understandings, beliefs,
and practices with regards to poultry keeping, poultry
diseases and its movements. The role of the participatory
disease surveillance (PDS) and response (PDSR) team was
to provide technical assistance and improve awareness
about how poultry viruses move and how diseases may be
prevented, helping community members to develop their
own technically sound approach to control and prevent
disease.
The approach was ‘‘bottom up,’’ where the local
community took the initiative of working together to
implement a series of HPAI prevention and control activ-
ities that were realistic and in line with local conditions.
The resulting action plans were agreed in each village with
the involvement of a district livestock services staff member
to ensure continuity, feedback, and technical soundness.
Information, education, and communication activities
targeted existing community groups such as Posyandus
(village integrated health services), religious and devotional
groups, self-help and women’s groups, churches and
mosques, elementary, junior and high-school students, and
other miscellaneous community gatherings. In villages
where commercial poultry producers exist, specific tech-
nical extension messages are provided including technical
discussions covering management issues, poultry anatomy,
and practical biosecurity pertinent to the levels of pro-
duction systems present (FAO 2010).
MARKETING
In many countries where village poultry are important, cold
storage facilities are absent or unreliable and so consumer
preference for live bird markets makes good sense. Family
poultry traders have been dealing with mortality in their
birds due to diseases such as ND for many decades. When
ND control is available in rural areas it benefits both pro-
ducers and traders (Alders 2012b), especially traders that
constantly operate in the same area as the control program.
Traders who knowingly deal in the supply of infected birds
to large markets can only stay in business in large cities
where their identities and reputation are less likely to suffer.
A key lesson from the H5N1 pandemic is that poorly
managed live bird markets and traders’ yards can play a
major role in the persistence and transmission of the AI
virus especially if poultry remain in the market over 24 h,
providing opportunities for transmission within market
stalls (FAO 2011). Market hygiene (cleaning and disinfec-
tion programs) improvements have been introduced in a
number of endemically infected countries which help to
reduce the risk of infection with the AI virus but do not
prevent all cases of infection. Not all live bird markets are
equal in terms of the risk they pose. Small, well-managed
R. Alders et al.
markets that have strict controls over the sources of poultry
do not allow overnight stays from which no live poultry
exit (other than direct to slaughter) represent a very low
risk (FAO 2011). Honhold (pers. comm.) observed that
while it may often be the case that weekly markets at which
live poultry are sold represent a lower risk of disease spread
in poultry than those held every day, it was found in the
field in Nigeria that the poultry traders selling at weekly
markets moved on a daily basis around an established cycle
of such markets, taking stock with them on each day from
one to the next and keeping unsold stock at their perma-
nent bases. This type of trading may present an equivalent
risk to a permanent market in terms of maintaining
infection in stock sold at markets although the environ-
mental contamination should be less. This illustrates the
need to understand clearly the marketing system as well as
the production system in each situation in order to clearly
understand the risks to both poultry and people.
Strict regulation of live bird markets without adequate
consultation with traders has resulted in the parallel trading
of birds which contributed to further spread of the disease
(FAO 2008) (Honhold pers. comm.).
POULTRY DISEASE SURVEILLANCE,
PREVENTION,AND CONTROL:VILLAGE
POULTRY VS.COMMERCIAL POULTRY
As recently as the 1950s, HPAI was known as Fowl Plague
[a term which also included Newcastle disease (which
emerged in 1926) because their clinical signs were so sim-
ilar], until advances in laboratory diagnostic technology
enabled the differentiation of the two causative agents
(Alders 2006).
Poultry disease prevention and control is hampered by
inadequate surveillance and under-reporting of poultry
diseases which remain a chronic problem in many coun-
tries, both ‘‘developed’’ and ‘‘developing (Ogundipe et al.
1989; Cattoli et al. 2010). The response to the HPAI H5N1
pandemic does not appear to have significantly strength-
ened poultry disease surveillance as suggested by data
submitted to the World Animal Health Organization’s
(OIE’s) World Animal Health Information Database
(WAHID). While the data submitted to the OIE are not a
reliable way of comparing surveillance activities between
countries, it does serve as an indicator of the importance
given by animal health surveillance systems to poultry
diseases. Sensitive disease surveillance systems that provide
the earliest warnings possible are those which are capable of
detecting diseases which have clinical signs compatible with
priority diseases (Alders 2012a). In the case of HPAI, the
list of differential diagnoses includes ND, acute fowl chol-
era (FC), infectious laryngotracheitis (ILT), and infectious
bursal disease (IBD, Gumboro disease) (Alders and Bagnol
2007; OIE 2012). Each of these diseases also has a signifi-
cant economic impact on poultry production in addition to
presenting a clinical picture similar to HPAI. A summary of
reports to the OIE in 2005 and 2010 for these five poultry
diseases across five countries suggests that surveillance for
poultry diseases remains a significant challenge (Alders
2012a). A complicating factor is that in some countries,
donor support for HPAI control has targeted this disease in
isolation, therefore funds were not made available for
testing for differential diagnoses. This meant that samples
negative for HPAI were not processed further and farmers
were left wondering what caused the mortality in their
birds. This lack of support for the diagnosis of poultry
diseases is likely to have a greater impact on small-holder
producers as in many countries the larger commercial
producers maintain their own diagnostic facilities.
Cost-efficient disease surveillance activities can be en-
hanced by the combination of classical and participatory
epidemiology (PE) methodologies (Azhar et al. 2010; Cat-
ley et al. 2012). The knowledge and perspectives of pro-
ducers and communities obtained through PE activities has
enabled the targeting of more costly classical epidemio-
logical activities, establishes or strengthens linkages be-
tween stakeholders and provides valuable insights into local
perspectives relating to disease prevention and control to
help tailor future interventions (Azhar et al. 2010; Catley
et al. 2012). During HPAI control activities, effective dis-
ease outbreak responses occurred where prior agreements
have been made between producers or their representatives
and relevant government agencies (e.g., the Australian
Veterinary Emergency Plan Avian Influenza Disease Strat-
egy; Australian Animal Health 2011). Such agreements are
usually made with commercial poultry producers with little
attention given to family poultry producers. Control mea-
sures that do not unduly threaten food security or sover-
eignty are more likely to succeed (Alders 2012a). The
inclusion of gender-sensitive methodologies has been rec-
ommended to increase participation and compliance of
both men and women in disease control activities (Bagnol
2009b).
The PDSR approach to HPAI in Indonesia is based
on PE and evolved significantly from the PDS system
Impact of Avian Influenza on Village Poultry
developed for rinderpest eradication in Africa and Paki-
stan (Azhar et al. 2010). However, as noted by Catley
et al. (2012), it is crucial that PE not be regarded as an
adjunct to national surveillance systems which aim to
meet the objectives of the veterinary establishment and
international actors, rather than the priorities of poor
livestock keepers in developing countries. Where sur-
veillance activities focus largely on veterinary and inter-
national objectives, community participation in the
control of HPAI will be limited and surveillance systems
are unlikely to work effectively during projects, or be
sustained when external funding is withdrawn. The cur-
rent global economic slow-down reinforces the challenge
to all countries to ensure that they utilize their available
resources optimally. Flexible PE approaches provide an
opportunity to ensure that disease control programs have
the support of national and local animal owning com-
munities.
COMPENSATION
Where compensation packages do exist, they frequently use
commercial poultry prices as the benchmark for establish-
ing the prices to be paid per bird. Market prices for village
chickens are frequently higher than those obtained for
commercial poultry. In the case of game birds, the value of
individual cocks can be up to 100 times the price of
commercial poultry (Hancock 2006). This disparity is yet
one more reason why village poultry owners are reluctant
to engage with official HPAI control programs. In addition,
criteria for receiving compensation can also be biased
against village poultry producers as illustrated by the case
study from Vietnam below.
COUNTRY CASE STUDY:VIETNAM
The current human HPAI case rate in Vietnam is the third
highest globally, with a fatality rate of 50% (WHO 2012).
According to World Health Organization reports, there
have been 121 confirmed cases and 61 deaths in Vietnam
out of a global 684 cases and 346 deaths (WHO 2012). The
virus is currently endemic in Vietnam (Gleeson 2011) and
is believed to be at high risk of causing a human pandemic
should the H5N1 virus adapt to develop human-to-human
transmission (Velasco et al. 2008; Lockerbie and Herring
2009).
Approximately 80% of rural households in Vietnam
raise poultry, providing food security and nutrition to
many families, with often the poorest families relying on
this resource the most (Hong Hanh et al. 2007; Lockerbie
and Herring 2009).
In November and December 2011, a small research
study was performed in Quang Tri province, Vietnam. The
aim was to explore, at a village level, local understandings
and social aspects of HPAI’s impact, etiology, diagnosis and
differentiation from other poultry diseases, and prevention
and control methods. Collegiality between human and
animal health workers, and their knowledge and percep-
tions of availability of services and reporting systems in this
region were also investigated.
Compensation of poultry farmers is a key factor in
farmers’ motivation to report suspect cases of HPAI,
therefore rendering it paramount to surveillance and pre-
vention efforts. The pay rate and timeliness of compensa-
tion anticipated varied markedly between study
participants. Some participants stated farmers would only
be compensated if their poultry had already been vacci-
nated against HPAI, as explained by a village animal health
worker in Trieu Do commune, Trieu Phong district, ‘‘If
poultry are already vaccinated (the farmers) get 50% of
market value but if they were not vaccinated they get no
compensation.’’ This was a pertinent finding because most
study participants reported problems with HPAI vaccine
supply (Farrell and Hunter unpublished data).
GENETIC DIVERSITY
Relatively little attention has been paid to the impact of
HPAI on the genetic diversity of poultry. In one study in
northern, northeast and central Thailand, it was found that
outbreaks of HPAI and subsequent restocking activities had
impacted on the genetic resources of indigenous breeds.
The percentage of pure indigenous breeds had decreased
markedly while the percentage of crossbred birds had in-
creased (Duangjinda et al. 2012).
Culling of poultry flocks in HPAI affected regions has
been indiscriminate with little to no attention to or
recording of the genetic stock lost (GRAIN 2006). Given
the homogeneity of commercial poultry stocks, culling in
these settings poses little risk concerning the loss of genetic
resources. However, in the case of heterogenous village
poultry breeds, important genetic resources may be lost
without even being characterized. As farming systems seek
R. Alders et al.
to cope with climate change, having access to resilient and
hardy poultry breeds will be a key aspect of coping strate-
gies.
POULTRY AS PART OF A DIVERSIFICATION
STRATEGY AND IMPLICATIONS ON PERCEIVED
RISK
Although the majority of poultry are found in commercial
settings, the majority of poultry producers are found within
the smallholder section (Alders 2012a). With the onset of
HPAI, this required a renewed understanding of this
smallholder sector. One of the issues that has been eluci-
dated by the global HPAI H5N1 response is that many of
these smallholder farmers have a very diverse portfolio of
activities which make up their livelihoods. In many cases,
smallholders diversify their portfolio to include varying
degrees of all or some of the following: crop production,
livestock, remittances, non-farm self employment, non-
farm wage, farm wage, and gathering. This diversification is
done to mitigate risk (Ellis 2000).
This required survival strategy means that smallholders
with poultry might not be very willing to invest in either
biosecurity and/or any other animal health inputs, since
they have already developed a system where they have
internalized the risk (Bush 2006). Although much work has
been done to date to understand these issues, and work on
looking at the community instead of the household as entry
point provides some options, further research is required to
understand and appropriately influence these dynamics.
EFFECTIVE COMMUNICATION:EASIER SAID
THAN DONE
Understanding who owns and takes care of poultry is
critically important as men, women, and children each have
different linguistic, cultural, and educational backgrounds
and varying access to services (Bagnol 2009a; Alders
2012b). At the beginning of the HPAI outbreak, as many of
the technical recommendations concerning the prevention
and control of the disease were first developed for use in the
intensive commercial poultry industry, these recommen-
dations needed to be adapted for use in rural areas where
village poultry are usually raised extensively (FAO 2010,
2011). Because of time pressures, communication strategies
were frequently developed in a hurry with little consulta-
tion with village poultry producers and inadequate pre-
testing of communication materials (Alders and Bagnol
2007). Currently, the control of HPAI continues to be
hampered by the use of HPAI prevention and control
messages that were developed by technical advisers with
little understanding of the daily reality of village poultry
producers (Table 1).
The good news is that there is a growing awareness
amongst animal health providers of the importance of
developing culturally sensitive dialogue that will identify
appropriate options for HPAI prevention and control as
demonstrated in the Indonesia case study above. The dia-
logue takes into account people’s knowledge and under-
standing (1) of the origin and (2) transmission of the
disease from animals to animals, (3) transmission from
animals to humans, (4) from humans to humans, (5) their
priorities in terms of livelihood strategies, (6) the gender
dynamics of poultry raising activities, and (7) risk aware-
ness and reduction (Alders and Bagnol 2007). Combining
communication activities with PE activities can lead to a
symbiotic relationship that enables farmers and technicians
to better understand each other resulting in feasible and
sustainable disease prevention and control initiatives.
MAIN FINDINGS AND CONCLUSIONS
The HPAI N5N1 pandemic has impacted negatively on
village poultry in many countries but there have also been
some benefits as a result of improved understanding of the
different poultry production systems. The most significant
negative impacts included:
•an adverse effect women as the primary producers of
village poultry;
•increased food and nutrition insecurity at the household
and community levels in countries with endemic HPAI;
•the culling of heterogeneous village poultry without
consideration for the impact on genetic diversity; and
•the use of poorly adapted communication material that
resulted in a loss of credibility of technical recommen-
dations in the eyes of producers and traders.
Key knowledge gained through the implementation of
HPAI prevention and control programs in village poultry
included:
•an improved understanding of the drivers of human
behavior along the value chain and how better manage-
ment of these drivers could also contribute to improved
food security;
Impact of Avian Influenza on Village Poultry
•changing the epidemiological unit from the backyard/
house to the village;
•the importance of working with producers and traders
when designing and implementing HPAI prevention and
control programs; and
•the symbiotic effect of combining communication
activities with PE tools.
HPAI H5N1 remains endemic in a number of countries
where the poultry sector is characterized by a high diversity
of production systems. Compared to the commercial
poultry industry, the family poultry sector has received
limited investment in research, extension, and finance.
However, the rearing of family poultry persists because it is
inherently low-input and extremely cost-efficient. The
development and introduction of economically feasible and
culturally acceptable interventions focusing on the factors
limiting productivity within the different production sys-
tems, and optimizing the efficiency of their associated value
chains, must be tailored according to country and local
conditions. It is likely that significant gains will be made in
these countries when the social and cultural aspects of
poultry production are addressed in harmony and coher-
ence with the technical disease control measures.
Poultry production has been an integral part of small
farms for centuries and will continue to be for the fore-
seeable future. As we seek to achieve food security and
safety, it is essential that we understand the people behind
the animals better. Unfortunately because of the short
timeframes of most HPAI control projects, there has not
always been adequate time given to completely under-
standing value chains and developing and trialing local and
culturally appropriate approaches. Understanding the hu-
man dimension of emerging infectious disease and taking a
broader systems approach will help in dealing with a dis-
ease like HPAI, which ultimately affects us all, including
smallholders, commercial companies, and consumers.
Table 1. Comments on two of the four key messages relating to the control of HPAI promoted by multi-lateral agencies in the early
stages of the response to the H5N1 pandemic (adapted from Alders 2006)
Message Comments
Report sick birds Given the need to ensure that birds infected with HPAI are handled safely, this was a sound
recommendation. In many cases it was not clear to whom or how farmers should report.
Even where a message is sent to the appropriate authorities, it may take days for a response
to be mounted. If farmers and communities are not adequately informed, they will continue
to eat and sell sick and dead birds and, by so doing, facilitate the spread of the disease
Farmers have seen their chickens dying every year of ND and were never asked to report.
In addition, even when their children or they themselves are sick they do not report and often
have difficulty accessing health services. This special request regarding the health of chickens
was seen as very awkward
Another complication was that compensation packages were rarely in place for farmers whose
birds were slaughtered as part of control packages. Therefore farmers rarely reported
a second time and other farmers learnt not to report at all
Separate types of birds and poultry The promotion of the confinement of village poultry without due attention to nutrition
and sanitation should be considered a temporary measure only. If birds are to be enclosed
for long periods they will need:
Access to clean water and feed that has an appropriate balance of protein, energy, vitamins,
and minerals (supplied by either commercial ration or from locally available feed);
To be kept in an environment that is frequently cleaned (with the removal of manure); and
Regular de-worming and vaccination against the common killer diseases
The benefit–cost of these measures should be made clear to farmers
The recommendation could have been adapted for village production systems by encouraging
farmers to provide separate overnight housing for each type of poultry and to house poultry
separately from pigs
R. Alders et al.
ACKNOWLEDGMENTS
The authors would like to acknowledge the support given
to village poultry research and development by the
Australian Centre for International Agricultural Research
(ACIAR), the Australian Agency for International Devel-
opment (AusAID), the Food and Agriculture Organization
of the United Nations (FAO), the International Livestock
Research Institute (ILRI), and the International Network
for Family Poultry Development (INFPD). Furthermore,
our gratitude is extended to the veterinarians, extension
specialists, researchers, traders, and farmers in many parts
of the world who have given freely of their time and
expertise.
REFERENCES
Alders R (2006) Information, education and communication
(IEC) challenges and gaps in HPAI control. In: Avian Influenza
Rapid Appraisal and Pro-Poor Livelihoods Agenda Consulta-
tion—Preliminary Assessment of Lessons Learned, Omore A
(editor), Nairobi, Kenya: International Livestock Research
Institute
Alders RG (2012a) Challenges and opportunities for small-scale
family poultry production in developing countries. Proceedings
of the XXIV World Poultry Congress, Salvador, Bahia, Brazil, 5–
9 Aug 2012. World’s Poultry Science Journal 68(Suppl 1):153
Alders RG (2012b) Analysis of science and innovation in the poultry
value chain: lessons for African countries. Paper commissioned by
the Technical Centre for Agricultural and Rural Cooperation
(CTA) for their Knowledge for Development website. Available:
http://knowledge.cta.int/en/Dossiers/Commodities/Livestock/
Enhancing-competitiveness-in-the-ACP-poultry-value-chain/
Feature-articles/Science-and-Innovation-in-Family-Poultry-Value-
Chain-Development-Lessons-for-African-countries. Accessed 7
October 2012
Alders RG, Bagnol B (2007) Effective communication: the key to
efficient HPAI prevention and control. World’s Poultry Science
Journal 63:139–147
Alders RG, Bagnol B, Farrell P, Fornace K, Gleeson L, Kock R,
Rushton J, Rushton R (2012) The human dimensions of food
safety and biosecurity with special emphasis on chronic
food and financial insecurity. Emerging Infectious Diseases
Symposium Abstract Booklet, CSIRO, Geelong, 22–23 October
2012, p 57
Alders R, Bagnol B, Harun M, Young M (2007) Village poultry,
food security and HIV/AIDS mitigation. LEISA Magazine
23(3):20–21
Alders RG, Pym RAE (2009) Village poultry: still important to
millions, eight thousand years after domestication. World’s
Poultry Science Journal 65(02):181–190
Animal Health Australia (2011) Disease Strategy: Avian Influenza
(Version 3.4). Australian Veterinary Emergency Plan (AUSVET-
PLAN), 3rd ed., Canberra, ACT: Primary Industries Ministerial
Council. Available: http://www.animalhealthaustralia.com.au/
wp-content/uploads/2011/04/AI3_4-06FINAL16Feb11.pdf. Ac-
cessed 27 March 2013
Azhar M, Lubis AS, Siregar ES, Alders RG, Brum E, McGrane J,
Morgan I, Roedar P (2010) Participatory disease surveillance
and response in Indonesia: strengthening veterinary services and
empowering communities to prevent and control highly path-
ogenic avian influenza. Avian Diseases 54(s1):749–753
Bagnol B (2009a) Gender issues in small-scale family poultry
production: experiences with ND and HPAI control. World’s
Poultry Science Journal 65:231–240
Bagnol B (2009b) Improving village chicken production by
employing effective gender sensitive methodologies. In: Village
Chickens, Poverty Alleviation and Sustainable Control of New-
castle Disease, Alders RG, Spradbrow PB, Young MP (editors),
Canberra: Australian Centre for International Agricultural Re-
search. ACIAR Proceedings No. 131, pp 35–42
Branckaert RDS, Gaviria L, Jallade J, Seiders RW (2000) Transfer
of technology in poultry production for developing countries.
In: Proceedings of the XXI World Poultry Congress, Montreal,
Canada, 20–24 Aug 2000
Bush J (2006) The threat of avian flu: predicted impacts on
rural livelihoods in SNNPR (Ethiopia). The Food Economy
Group. Available: http://www.feg-consulting.com/resource/
reports/Avian_Flu_Livelihoods_Final_Report.pdf. Accessed 7
October 2012
Capua I, Alexander DJ (2006) The challenge of avian influenza to
the veterinary community. Avian Pathology 35(3):189–205
Capua I, Alexander DJ (2009) Avian influenza infection in birds:
A challenge and opportunity for the poultry veterinarian.
Poultry Science 88:842–846
Catley A, Alders RG, Woods J (2012) Participatory epidemiology:
approaches, methods, experiences. The Veterinary Journal
191:151–160
Cattoli G, Fusaro A, Monne I, Molia S, Le Menach A, Maregeya B,
Nchare A, Bangana I, Garb Maina A, N’goran Koffi JN, Thiam
H, Bezeid OEMA, Salviato A, Nisi R, Terregino C, Capua I
(2010) Emergence of a new genetic lineage of Newcastle disease
virus in West and Central Africa—implications for diagnosis
and control. Veterinary Microbiology 142(3–4):168–176
Duangjinda M, Choprakarn K, Suwanlee S, Amnueysit P, Thieme
O (2012) Impact of the avian influenza outbreak on indigenous
chicken genetic resources in Thailand. World’s Poultry Science
Journal 68:503–512
Ellis F (2000) The determinants of rural livelihood diversification
in developing countries. Journal of Agricultural Economics
51(2):289–302
FAO (2008) Biosecurity for highly pathogenic avian influenza:
issues and options. FAO Animal Production and Health Paper
No. 165
FAO (2009) Highly pathogenic avian influenza: a rapid assessment
of its socio-economic impact on vulnerable households in
Egypt. Food and Agriculture Organization of the United Na-
tions, Rome
FAO (2010) Guide de Bonnes Pratiques sur les Marche
´s de Vol-
ailles Vivantes. Food and Agriculture Organisation, Bamako.
Available: http://www.fao-ectad-bamako.org/fr/Guide-des-
bonnes-pratiques. Accessed: 7 October 2012
FAO (2011) Approaches to controlling, preventing and elimi-
nating H5N1 highly pathogenic avian influenza in endemic
countries. Food and Agriculture Organisation, Rome. Animal
Production and Health Paper No. 171
Impact of Avian Influenza on Village Poultry
Gilbert M, Xiao X, Pfeiffer DU, Epprecht M, Boles S, Czarnecki C,
Chaitaweesub P, Kalpravidh W, Minh PQ, Otte MJ, Martin V,
Slingenbergh J (2008) Mapping H5N1 highly pathogenic avian
influenza risk in Southeast Asia. PNAS 12:4769–4774
Gleeson L (2011) Fourth Report Global programme for the pre-
vention and control of highly pathogenic avian influenza. Food
and Agriculture Organisation of the United Nations. Available:
http://www.fao.org/docrep/014/i2252e/i2252e00.pdf. Accessed 6
October 2012
GRAIN (2006) Fowl play: the poultry industry’s central role in the
bird flu crisis. Genetic Resources Action International. Avail-
able: http://www.grain.org/briefings/?id-194. Accessed 7 Octo-
ber 2012
Gue
`ye EF (1998) Village egg and fowl meat production in Africa.
World’s Poultry Science Journal 54:73–86
Gue
`ye EF (2005) Gender aspects in family poultry management
systems in developing countries. World’s Poultry Science Journal
61:39–46
Gutie
´rrez RA, Naughtin MJ, Horm SV, San S, Buchy P (2009)
Influenza A(H5N1) virus evolution in South East Asia. Viruses
1:335–361
Hancock J (2006) Report on an electronic consultation on com-
pensation and HPAI. ECTAD Socioeconomic Group, 18
October 2006, FAO, Rome, Italy
Hickler B (2007) Bridging the gap between HPAI ‘awareness’ and
practice in Cambodia. Food and Agriculture Organization of
the United Nations, Bangkok. Available: http://www.fao.org/
docs/eims/upload//241483/ai301e00.pdf. Accessed 6 October
2012
Higgins DA, Shortridge KF (1988) Newcastle disease in tropical
and developing countries. In: Developments in veterinary virol-
ogy: Newcastle disease, Alexander DJ (editor), Dordrecht,
Netherlands and Boston, USA: Kluwer Academic Publishers,
pp 272–302
Hanh PTH, Burgos S, Ronald-Holst D (2007) The poultry sector in
Viet Nam: prospects for smallholder producers in the aftermath of
the HPAI crisis. Pro-Poor Livestock Policy Initiative Research
Report. Available: http://www.fao.org/ag/againfo/programmes/
en/pplpi/docarc/rep-hpai_vietnampoultryquality.pdf. Accessed
27 March 2013
Hulse-Post DJ, Sturm-Ramirez KM, Humberd J, Seiler P, Gov-
orkova EA, Krauss S, Scholtissek C, Puthavathana P, Buranathai
C, Nguyen TD, Long HT, Naipospos TSP, Chen H, Ellis TM,
Guan Y, Peiris JSM, Webster RG (2005) Role of domestic ducks
in the propagation and biological evolution of highly patho-
genic H5N1 influenza viruses in Asia. Proceedings of the National
Academy of Sciences USA 102:10682–10687
Jia B, Shi J, Li Y, Shinya K, Muramoto Y, et al. (2008) Patho-
genecity of Chinese H5N1 highly pathogenic avian influenza
viruses in pigeons. Archives of Virology 153:1821–1826
Lockerbie S, Herring DA (2009) Global panic, local repercussions:
economic and nutritional effects of bird flu in Vietnam. In:
Anthropology and Public Health, Hahn R, Inhorn M (editors),
Oxford: Oxford University Press, pp 566–587
Martin PAJ (1992) The epidemiology of Newcastle disease in
village chickens. In: Newcastle disease in village chickens, con-
trol with thermostable oral vaccine. Spradbrow, PB (editor).
Proceedings of an International Workshop, Kuala Lumpur,
Malaysia, 6–10 October 1991. ACIAR Proceedings No. 39:40–45
McLeod A, Morgan N, Prakash A, Hinrichs J (2012) Economic
and social impacts of avian influenza. Available: http://www.fao.
org/avianflu/documents/Economic-and-social-impacts-of-avian-
influenza-Geneva.pdf. Accessed 6 October 2012
McLeod A, Kobayahsi M, Gilman J, Siagian A, Young M (2009)
The use of poultry value chain mapping in developing HPAI
control programmes. World’s Poultry Science Journal 65:217–224
Ogundipe GAT, Oluokun SB, Esuruso GO (1989) The develop-
ment and efficiency of the Animal Health Information System
in Nigeria. Preventive Veterinary Medicine 7:121–135
OIE (2012) OIE World Animal Health Information Database
Interface. World Animal Health Organization, Paris. Available:
http://web.oie.int/wahis/public.php. Accessed 29 October 2012
Perkins LEL, Swayne DE (2003) Comparative susceptibility of
selected avian and mammalian species to a Hong Kong-origin
H5N1 high pathogenicity avian influenza virus. Avian Diseases
47(s3):956–967
Smith G, Dunipace S (2011) How backyard poultry flocks influ-
ence the effort required to curtail avian influenza epidemics in
commercial poultry flocks. Epidemics. 3(2):71–75
Sonaiya EB (2009) Fifteen years of family poultry research and
development at Obafemi Awolow University, Nigeria. In: Alders
R.G., Spradbrow P.B. and Young M.P. (eds) Village chickens,
poverty alleviation and the sustainable control of Newcastle
disease. Proceedings of an international conference held in Dar
es Salaam, Tanzania, 5–7 October 2005. ACIAR Proceedings No.
131:15–26
Stubbs EL (1969) Fowl Plague. In: Diseases of Poultry, 5th ed.,
Bisester HE, Schwarte LH (editors). Ames: Iowa State University
Press, pp 813–822. Cited by Easterday BC, Hinshaw VS, Hal-
vorson DA (1997) Influenza. In: Diseases of Poultry, 10th ed.,
Ames: Iowa State University Press, pp 583–605
Sultana R, Nahar N, Rimi NA, Azad S, Islam MS, Gurley ES, Luby SP
(2012) Backyard poultry raising in Bangladesh: a valued resource
for the villagers and a setting for zoonotic transmission of avian
influenza—a qualitative study. Rural and Remote Health Journal
12:1927. Available: http://www.rrh.org.au/publishedarticles/article
_print_1927.pdf. Accessed 25 March 2013
Swayne DE, Halvorson DA (2003) Influenza. In: Diseases of
poultry, Saif YM (editor), 11th ed. Ames, A Blackwell Publishing
Company: Iowa State Press, pp 135–158
Taylor N, Rushton J (2011) A value chain approach to animal
diseases risk management—Technical foundations and practical
framework for field application. Animal Production and Health
Guidelines No. 4, Rome. Available: http://www.fao.org/docrep/
014/i2198e/i2198e00.htm. Accessed 29 October 2012
Velasco E, Dieleman E, Supakankuti S, Phuong TTM (2008) Gender
aspects of the avian influenza crisis in Southeast Asia: Laos, Thailand
and Vietnam. European Commission Directorate General External
Relations. Available: http://ec.europa.eu/world/avian_influenza/
docs/gender_study_0608_en.pdf.Accessed6October2012
Werner O, Starick E, Teifke J, Klopfleisch R, Prajitno TY, et al.
(2007) Minute excretion of highly pathogenic avian influenza
virus A/chicken/Indonesia/2003 (H5N1) from experimentally
infected domestic pigeons (Columbia livia) and lack of trans-
mission to sentinal chickens. Journal of General Virology
88:3089–3093
WHO (2012) Cumulative number of confirmed human cases for
avian influenza A (H5N1) reported to WHO, 2003–2012. World
Health Organisation. Available: http://www.who.int/influenza/
human_animal_interface/EN_GIP_20120208CumulativeNumber
H5N1cases.pdf. Accessed 8 November 2012
R. Alders et al.