Pig traders’ networks on the Kenya-Uganda border highlight potential for mitigation of African swine fever virus transmission and improved ASF disease risk management

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Highlights

  • Pig trade is important in ASF transmission in sub Saharan Africa where smallholder pig farming is a livelihood strategy.

  • Traders knew early of outbreaks because farmers sought to sell their pigs as soon as they suspected an outbreak.

  • The structure of pig trade networks suggests traders may contribute to rapid dissemination of the virus.

  • Cross border harmonization of approaches to manage ASF is critical in this transboundary region.

  • Institutional changes, infrastructure improvements and collaboration between traders and governments is important.

Abstract

We applied social network analysis to pig trader networks on the Kenya-Uganda border. Social network analysis is a recently developed tool, which is useful for understanding value chains and improving disease control policies. We interviewed a sample of 33 traders about their experiences with trade and African swine fever (ASF), analyzed the networks they generated in purchasing pigs and selling pork and their potential contribution to modulating dissemination of the ASF virus (ASFV). The majority of the traders were aware of clinical signs of ASF and the risk of trade transmitting ASFV. Most said they avoided buying pigs from ASF outbreak villages or sick pigs but their experiences also indicated that inadvertent purchase was relatively common. Traders had early knowledge of outbreaks since they were contacted by farmers who had heard rumours and wanted to sell their pigs to avoid the risk of them dying. Individual traders bought pigs in up to nine villages, and up to six traders operated in a village. Although each trade typically spanned less than 5 km, networks of the various traders, comprising movements of pigs from source villages to slaughter slabs/sites and retail outlets, and movement of pork to villages where it was consumed, linked up indirectly across the 100 km × 50 km study area and revealed several trade pathways across the Kenya-Uganda border. ASF could potentially spread across this area and beyond through sequential pig and pork transactions.

Regulation of the pig and pork trade was minimal in practice. The risk of ASFV being spread by traders was compounded by their use of poorly constructed slaughter slabs/sites with open drainage, ineffective or non-existent meat inspection services, lack of provision for biosecurity in the value chain, and sales of pork to customers who were unaware of the risks to their own pigs from contact with ASF infected pork. More effective regulation is warranted. However, limitations on government capacity, together with the strong self-interest that established traders have in reducing the disruption and financial losses that outbreaks cause, highlight the importance of governments and traders co-developing an approach to ASF control. Formation of trader organizations or common interest groups warrants government support as an important step in engaging traders in developing and implementing effective approaches to reduce the risk of ASF outbreaks.

Introduction

Social network analysis can help to reveal which nodes in a value chain are critical for disease spread. Understanding the structure of traders’ livestock buying and selling networks can inform the design of control strategies and prevent access to potential transmission pathways (Dube et al., 2009). Livestock convergence sites such as market-places typically have large numbers of incoming and outgoing connections (Christley et al., 2005) making them critical nodes, and therefore potentially important, in disease spread. Identification of such nodes in advance of disease incursions (Bigras-Poulin et al., 2006, Bigras-Poulin et al., 2007) makes it more feasible to target them for rapid intervention during epidemics for information dissemination, including education relating to biosecurity measures to prevent disease transmission and measures for implementation of rapid response to outbreaks (Robinson and Christley, 2007). However where trade does not involve livestock converging at market-places, critical nodes or hubs for transmission of disease may not be readily apparent. Such is the case with husbandry and trade of pigs by small-holder farmers in regions of Kenya and Uganda where African swine fever virus (ASFV) is prevalent resulting in intermittent, but regular ASF disease outbreaks (Lichoti et al., 2016).

African swine fever is a contagious fatal disease of pigs with no effective treatment or vaccine for prevention. It is a major limiting factor for pig production in most African countries and has impacts on pig production in other regions, currently including Russia and parts of eastern Europe, with the potential risk of global spread, (Penrith et al., 2013, Oura, 2013, Gallardo et al., 2015, Gavier-Widén et al., 2015).

Many smallholder farmers in Uganda and Kenya have adopted small-scale pig keeping to improve their living standards (FAO, 2012, Pezo, 2013, Chenais et al., 2017). However, the potential contribution of pig keeping to enhanced food security in vulnerable households is limited by ASF, or the perceived risk of ASF outbreaks. For example, in northern Uganda more than two thirds of a sample of pig keeping farmers stated that they had been affected by ASF outbreaks in which 80% of their pigs had died (Chenais et al., 2017). Along the Kenya-Uganda border, half of the pig-keeping households do not keep pigs continuously and mortality of pigs due to ASF was the main reason they provided for discontinuous pig-keeping (Nantima et al., 2015a).

The causal agent for ASF is a large DNA virus classified in the monotypic family Asfaviridae, genus Asfivirus (Dixon et al., 2005). The virus is very stable, persisting for weeks in pig faeces, dead pigs, offal, and perhaps most importantly in pig meat products (Wilkinson, 1989, Montgomery, 1921). The virus is shed in body secretions and faeces and may be transported over hundreds of kilometers on clothing and equipment used by people involved in trade and slaughter (FAO, 2000). The virus can be found in all tissues and body fluids of infected pigs, but during the acute phase of infection, particularly high levels are found in the blood. Environmental contamination during slaughter can facilitate virus spread on fomites (Oura, 2013, de Carvalho Ferreira et al., 2013).

The behavior of smallholder pig farmers along the Kenya-Uganda border indicated that trader networks were potentially important to the spread of ASF. Farmers quickly decided to sell their pigs if they saw or heard about other pigs getting sick even though the cause of illness or death might not be ASF (Lichoti et al., 2016). If pigs were infected with ASF at the time of sale, spread of the disease would likely be facilitated by trade-associated movement of pigs and pig products between farms, slaughter slabs, butcheries and homes and farms owned by consumers of pig products. Traders have a key role in facilitating these movements. Accordingly, this study was undertaken to understand what pig traders in the region knew about ASF and the structure of their trading networks. Our goal was to complement other epidemiological and diagnostic studies by informing strategies for ASF prevention, surveillance and impact reduction in sub-Saharan Africa.

Section snippets

Selection strategy

The traders considered for this study were a subset of those who bought pigs in 2011–2012 from a clustered random sample of small-holder pig-keeping farmers in 38 randomly sampled villages in Busia and Teso Districts (now Busia County) in Kenya, and Tororo and Busia Districts in Uganda. The farmers were interviewed in 2012 as part of an earlier study about pig keeping and pig health (Lichoti et al., 2016, Nantima et al., 2015a, Nantima et al., 2015b) and were asked about the life history of

How and why traders purchased pigs

Traders bought pigs not only for slaughter but also for rearing, as shown in Fig. 1. About 40% of Kenyan traders bought pigs solely for slaughter and a similar proportion coupled slaughter with finishing. A slightly smaller proportion of Ugandan traders bought pigs solely for slaughter and 25% bought them for a combination of slaughter, finishing and sale. Pigs were either slaughtered at the traders’ premises (butchery) or at a slaughter slab. The pork was subsequently sold to people from the

Discussion

Trade of infected pigs undoubtedly facilitates ASF spread, as other studies have reported (Chenais et al., 2017, Costard et al., 2009, Randriamparany et al., 2005). More than half the traders who participated in our study stated that they were aware of this. These traders were more likely than others to say that during the most recent outbreak they experienced, they only purchased pigs from villages that had no outbreak or closed their business. The results suggest these traders may have been

Conclusion

The contribution of pig trade to ASF transmission has had comparatively little attention in regions of sub-Saharan Africa where ASF is endemic and smallholder pig farming is important to livelihoods. Our aim was to complement other epidemiological and diagnostic studies by informing ASF surveillance, prevention and control policies for reduction of its impact with generic implications for sub-Saharan Africa. The structure of pig trade networks indicates the potential for traders to contribute

Conflict of interest

None.

Research ethics approval

Participation of, and collection of data from, people in the project was governed by ethics approval from Commonwealth Scientific Research and Industrial Organization (CSIRO)-Social Science Human Research Ethics Committee (CSSHREC), approval 059/11, Australia.

Acknowledgements

The research was conducted as part of the Africa Food Security Initiative funded by the Australian Government as part of its overseas development assistance program. We also thank the partners who managed the research program: CSIRO, the Biosciences East and Central Africa (BecA) Hub and the Animal Biosciences program at the International Livestock Research Institute, Nairobi. We are grateful to members of pig keeping households and traders in Kenya and Uganda for contributing information that

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    Equal contributors.

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    Formerly Commonwealth Scientific and Industrial Research Organization, Land and Water, Australia.

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    Formerly, International Livestock Research Institute and Biosciences Eastern and Central Africa, P.O. Box 30709, 00100 Nairobi, Kenya.

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