Trade patterns facilitating highly pathogenic avian influenza virus dissemination in the free-grazing layer duck system in Vietnam

Highly pathogenic avian influenza (HPAI) viruses continue to threaten smallholder poultry producers in several South-east Asian countries, including Vietnam. In particular, the free-grazing duck system has been repeatedly highlighted as a major risk factor for HPAI outbreaks. Free-grazing ducks, which scavenge on rice paddies after the harvest, account for a large proportion of the duck population in Vietnam and the wider South-east Asian region. However, the structure and dynamics of the free-grazing duck production from farm to consumption has not been described for Vietnam. In this study, we used a value chain approach to provide a complete pic-ture of the actors involved in the production and marketing of free-grazing duck eggs and spent layer ducks, as well as to investigate the governance structure of this food system. Group interviews and key informant interviews were conducted in two provinces located in the Mekong River Delta (MRD) and the Red River Delta (RRD). The results presented here highlight similarities and differences in farming and trade practices between the two provinces. The trade of spent layer ducks involved large volumes of live ducks being sent to China and Cambodia for consumption, generating a substantial risk of transboundary spread of pathogens, including HPAI viruses. We describe the major role of “ duck yards ” , which act as hubs in the northbound trade of spent layer ducks. These yards should be considered as essential links in the value chain of spent layer ducks when considering HPAI surveillance and control. The veterinary authorities are only marginally involved in the value chain activities, and their influence could be strengthened by increasing surveillance activities for instance in duck yards. Last, we discuss the dynamics of the duck value chain and further implications for future HPAI management policies.


Trade patterns facilitating highly pathogenic avian influenza virus dissemination in the free-grazing layer duck system in Vietnam
Summary Highly pathogenic avian influenza (HPAI) viruses continue to threaten smallholder poultry producers in several South-east Asian countries, including Vietnam. In particular, the free-grazing duck system has been repeatedly highlighted as a major risk factor for HPAI outbreaks. Free-grazing ducks, which scavenge on rice paddies after the harvest, account for a large proportion of the duck population in Vietnam and the wider South-east Asian region. However, the structure and dynamics of the free-grazing duck production from farm to consumption has not been described for Vietnam. In this study, we used a value chain approach to provide a complete picture of the actors involved in the production and marketing of free-grazing duck eggs and spent layer ducks, as well as to investigate the governance structure of this food system. Group interviews and key informant interviews were conducted in two provinces located in the Mekong River Delta (MRD) and the Red River Delta (RRD). The results presented here highlight similarities and differences in farming and trade practices between the two provinces. The trade of spent layer ducks involved large volumes of live ducks being sent to China and Cambodia for consumption, generating a substantial risk of transboundary spread of pathogens, including HPAI viruses. We describe the major role of "duck yards", which act as hubs in the northbound trade of spent layer ducks. These yards should be considered as essential links in the value chain of spent layer ducks when considering HPAI surveillance and control. The veterinary authorities are only marginally involved in the value chain activities, and their influence could be strengthened by increasing surveillance activities for instance in duck yards. Last, we discuss the 1 | INTRODUCTION Poultry meat and pork are the main sources of animal protein in Vietnam (Le, 2003). The poultry production sector has been targeted by development policies since the late 1990s, in order to improve food security and tackle the widespread nutritional deficiencies in the country (Le, 2003). Among all poultry products, duck meat and duck eggs play an important role in Asia and their production has been increasing throughout the subcontinent (Tai & Tai, 2001). In Vietnam, although the duck production increased at a steady rate between 1990 and 2004, it has been stagnating since 2004 at around 60-80 million head per year (FAOSTAT, 2016). This has been attributed to the severe impact of the highly pathogenic avian influenza (HPAI) outbreaks from 2003 onwards, in particular in the freegrazing duck production systems (Rushton, Viscarra, Guerne Bleich, & McLeod, 2005). The duck egg production, however, has been increasing by 40%  Free-grazing ducks, which are herded on post-harvest rice paddies for scavenging purposes, represent around 73% of the duck population in Vietnam (Bui, 2010) and are widespread in other countries of the region, such as China and Indonesia. Free-grazing ducks can be transported over relatively long distances for grazing and can regularly be in direct or indirect contact with other flocks, themselves coming from different locations (Henning et al., 2013;Meyer et al., 2017). As infected ducks are able to shed HPAI virus without showing clinical signs (Hulse-Post et al., 2005), free-grazing ducks are suspected to play an important role in the maintenance and circulation of HPAI viruses (Gilbert et al., 2006;Songserm et al., 2006;Sturm-Ramirez et al., 2005). This is especially relevant given the fact that various strains of H5N1 and H5N6 viruses continue to circulate in poultry throughout Vietnam, with more than 400 outbreaks having been reported during the last 10 years (EMPRES-i, 2017).
While a few studies described the production of free-grazing ducks in Vietnam (Henning et al., 2013;Minh, Stevenson, Schauer, Morris, & Quy, 2010), none of them considered the other stakeholders involved in the value chain for duck products. Value chain analysis is a key tool to understand the dynamics and drivers of livestock production systems, especially in developing countries where the enforcement of rules and regulations is limited and supply chains are often long and complex (Rich & Perry, 2011). It provides a structured approach to identify disease risks within a food system and to assist the design of health management policies (FAO 2011

| Conceptual approach
The working definition of value chain for this study was "the full range of activities, which are required to bring a product or service from conception, through the different phases of production to delivery to final consumers, and final disposal after use" (Kaplinsky & Morris, 2010). We used an institutional and functional analysis (Bockel & Tallec, 2005), which consists in studying the value chain of interest by defining the agents involved and their respective functions (institutional analysis) as well as the various interactions and flows between them (functional analysis). These elements were represented using a commodity flow chart for each of the two commodities studied: duck eggs and spent layer ducks. We explored the vertical and horizontal links (Faße, Grote, & Winter, 2009)

| Data collection and analysis
The study focussed on the layer duck value chain, including table eggs, hatching eggs and spent layer ducks. Duck farms were divided into two groups, raising short-distance free-grazing ducks and longdistance free-grazing ducks, respectively, according to definitions MEYER ET AL.
| 409 previously used (Henning et al., 2013): short-distance free-grazing ducks graze within the home commune and are kept in confinement on the farm at night, while long-distance free-grazing ducks graze on rice paddies within or outside the home commune and do not return to the farm for extended periods of time. In Vietnam, a commune is a small administrative unit encompassing a central village and a varying number of hamlets. The value chains were investigated in the RRD and the MRD, which constitute the two main duck production regions in Vietnam. One province was selected in each region (Hai Phong in the RRD and An Giang in the MRD), based on a higher proportion of free-grazing ducks in the total duck production of the province than other nearby provinces. In order to capture local heterogeneities, six communes within each study province were selected for the study, based on the willingness of the local veterinary services to participate and the presence of long-distance freegrazing ducks at the time of the field activities. Additional stakeholders who were not residing in the study provinces, but who were involved in the value chains under study, were also recruited.
Group interviews were conducted in each study commune, gathering stakeholders involved in the free-grazing layer duck production, from producers to market managers and inspectors. Key informant interviews were also organized in order to characterize the precise role of each agent and triangulate information gathered during the group interviews. Participants of the group discussions were approached to request an individual interview.
Those who accepted were interviewed at their usual workplace.
Additional key agents of the value chain who were not present at the group meetings were identified by the meeting or interview participants and by veterinary officials. One questionnaire per type of agent was designed and refined after pilot interviews. Questions were used to define the main characteristics and functions of each agent (years of experience in the role, sources of inputs, destinations of outputs, etc.), as well as to identify and quantify the product flows in and out of each enterprise for the past year (questionnaire templates are available from the corresponding author on request). The individual interviews were conducted in Vietnamese by two Vietnamese research assistants. The study was initially limited to the value chain of free-grazing ducks, but it was found that only duck producers are specialized in free-grazing ducks, while other actors (e.g., collectors, wholesalers) work with both free-grazing and confined ducks. Consequently, the sample was expanded to include value chain actors that covered both Thematic analysis (Braun & Clarke, 2006) was used in order to analyse the governance structure and dynamics of the value chains. The group interview notes and individual interview notes were reviewed carefully and the data of potential relevance to HPAI epidemiology and management were structured into codes, which were translated into English. The codes identified were sorted into themes that were used to structure the narrative of this analysis.

| RESULTS
A total of 12 group interviews were conducted in each study province in 2015, with a total of 188 stakeholders from different levels of the value chain (Table 1) Phong and tended to sell them earlier than farmers in Hai Phong did. Among An Giang participants, short-distance farmers had smaller flocks and sold them earlier than long-distance farmers did.

| Collectors, retailers and wholesalers
A number of agents were involved in the trade of ducks eggs and spent layer ducks in both provinces: collectors, retailers, local wholesalers, inter-province wholesalers and duck yard owners. These agents are hereafter collectively referred to as "intermediaries." Collectors purchase live ducks mainly at farm gate and sell them to other agents in the value chain, but not directly to the consumers.
The retailers purchase ducks from farmers or other intermediaries and sell them to the end consumers, either as live ducks or as fresh carcasses. All retailers in the survey used motorbikes to transport ducks. They traded smaller volumes than the other agents did, with an average of 1,300 heads per month, respectively (Table 3). Retailers were mainly women in both provinces. Both genders were represented among collectors and wholesalers in Hai Phong, but mainly men had these functions in An Giang. Retailers operated within a smaller geographic area than collectors did; the average distance travelled from their residence to buy ducks was 9 and 43 km, respectively, while the average distance travelled from their residence to sell ducks was 2 and 70 km, respectively (data not shown).
Wholesalers generally bought larger quantities of live ducks at once, directly from farms or from local collectors, and sold them to other agents further along the value chain, but not directly to the con- local topography and to their higher loading capacity, boats constituted the most common mode of duck and duck egg transportation in An Giang. Three types of wholesalers were identified: local wholesalers, inter-province wholesalers and duck yard owners (see following section). Local wholesalers worked within their province of origin while inter-province wholesalers conducted their activities over at least two provinces. Inter-province wholesalers handled larger volumes of spent layer ducks (up to 150,000 heads per month) than retailers or local wholesalers did (Table 3).

| Owners of duck yards
The so-called duck yards are facilities in the northern provinces of Vietnam that serve as exchange hubs for wholesalers trading spent layer ducks, which might have travelled hundreds of kilometres to reach the duck yard. The ducks present in the yards are owned by the yard owners, who are in charge of feeding the ducks with concentrates until they reach the minimum weight required by the buyers. Yard owners reported that up to 30% of the ducks delivered on their yards were underweight and had to be fed. The ducks were kept on the yards for an average of 2.7 days before being collected (data not shown). The yard owners recruited in the study traded on average 67,300 spent layer ducks per month ( and 100%, respectively), but trucks and boats were also used (data not shown).

| Destinations of duck eggs from the farms
In Hai Phong, only 12% of farmers sold eggs to a hatchery while most farmers sold table eggs to intermediaries (Table 5)

| Governance
Two main themes linked to the governance of the spent layer duck value chain were identified during the group and individual interviews: the major role of collectors and wholesalers, respectively. As insufficient data were collected on the governance of the egg value chain, they are not presented here.
In both provinces, collectors have access to essential information about both the current availability of and demand for spent layer ducks and duck eggs in terms of volume, location and timing. Collectors may have trade contacts with wholesalers and retailers in the provincial urban centres where the demand is higher than it is in rural areas. They have an important role as brokers, influence the product prices and form a key link between the farmers and other actors such as wholesalers in terms of sharing of information on demand and supply.
Wholesalers are able to purchase large quantities of ducks within a short period, thus being able to buy ducks for a smaller price than local intermediaries are. They had the longest experience in duck trade ( Table 3  Average proportion of spent duck production sold to each agent among farmers selling to that agent (%) Intermediaries in the province 87 87 95 Intermediaries outside the province 32 58 75 Slaughter points and retailers 15 q 2 r NA Other 3.5 2 NA Figures on the same line not sharing any superscript letter were statistically significantly different (p < .05). LD, long-distance; SD, short-distance; NA, not applicable. Intermediaries: collectors, retailers, local wholesalers, inter-province wholesalers and duck yard owners. The lines "Farmers selling duck eggs to each agent" and "Farmers selling spent layer duck to each agent" refer to proportions of agents, while the other two lines refer to proportions of production sold to specific agents among farmers for whom this proportion is not null.
all post-farm gate actors work with both free-grazing and confined ducks, it was not possible in this study to obtain figures specific to free-grazing ducks when characterizing the trade volumes beyond the production level. However, we believe that the figures presented here accurately reflect the trading patterns of duck eggs and spent layer ducks from free-grazing systems during the study period. As the participants were recruited in a subset of communes only, it is possible that we did not capture all the relevant actors from the free-grazing duck value chains. However, we interviewed all the actors whose names were provided by the animal health official services and we recruited further actors who were mentioned during the interviews. As such, we believe that the description of the value chains provided here is sufficiently complete so that meaningful inferences can be drawn.
The trade of live poultry has long been recognized as a major route for HPAI virus dissemination in Asia (Fourni e, de Glanville, & Pfeiffer, 2012). As they bring together various susceptible bird species coming from various locations, live bird markets are known to contribute to the spread of HPAI viruses and have regularly been found contaminated in endemic contexts (Amonsin et al., 2008;Chen et al., 2014;Indriani et al., 2010;Negovetich et al., 2011;Nguyen et al., 2005). Similarly, we believe that the duck yard system may be involved in the epidemiology of avian influenza viruses, and HPAI viruses specifically, for various reasons. First, we found that a large number of HPAI-susceptible ducks are collected from the entire country and gathered in the yards, where flocks from different origins often mingle for several days. Second, long-distance transport is a stressful event and has been previously reported as a risk factor for avian influenza infection (Beaudoin et al., 2014)  share taken by supermarkets in food retailing (Reardon, Peter Timmer, Barrett, & Berdegu e, 2003) suggests that the demand for chilled and frozen poultry will increase in the near future. The characteristics of the duck value chains presented here, in particular the important role of the inter-province wholesalers and yard owners, also have implications in terms of HPAI surveillance.
The veterinary authorities have a role in the trade of spent layer ducks as they issue movement certificates when ducks are transported across province borders (for instance from the MRD to the duck yards). The wholesalers from the MRD recruited in our study reported that all the northbound trucks were inspected and sealed before departure. However, the ducks collected in the RRD were mainly transported by motorbike without veterinary inspection (data not shown). The duck yards in the RRD are under the jurisdiction of the provincial veterinary services, whose offices are located distant from the yards. In addition, most transactions from and to the duck yards occur at night-time, in order to minimize the stress for the animals. Consequently, the likelihood of effective inspection by the veterinary services in the duck yards was reported as low. Most importantly, the active surveillance for HPAI viruses in Vietnam is mostly implemented in live bird markets (Nguyen et al., 2014). Freegrazing ducks represent around 73% of the total duck production in the MRD (Bui, 2010), and our study showed that over 98% of them did not transit through live bird markets in 2015. Therefore, a considerable proportion of the HPAI at-risk population bypasses the traditional surveillance activities implemented in LBMs. In the light of the results of this value chain analysis, we strongly recommend to monitor the HPAI status of duck yards as a complement to LBM surveillance.
Management practices of free-grazing duck farmers differed between the two provinces. First, all farmers in An Giang practised free grazing with their flocks all year round, but 67% of farmers from Hai Phong kept their flocks confined on the farms for a substantial part of the year. This is consistent with previous studies reporting that free-grazing duck practices differ between agro-ecological regions in Vietnam (Desvaux, Ton, Phan Dang, & Hoa, 2008;Edan, 2006). Second, the production cycle of layer duck flocks was longer in Hai Phong than it was in An Giang (median of 24 and 15 months, respectively) ( The value chains presented here were subjected to fluctuation in demand and product availability, linked not only to seasons, but also to climatic, disease and cultural events. Therefore, trade agreements between stakeholders are essential for the survival of their businesses during difficult periods. According to the participants in this study, the export of the spent layer ducks produced in Vietnam is dependent on the demand abroad and on the ease of border crossing. The decrease in prices linked to incidents with the custom officers early 2016 leads to a significant re-routing of the products towards local consumption and export to Cambodia. Implications for surveillance and control of highly pathogenic avian influenza (HPAI/H5N1