Perspectives on progression of transboundary disease, one health and ecosystem health management in the Greater Mekong Subregion and beyond

Introduction

It has been estimated that although family farms produce ~80% of the world’s food on farms of variable size, smallholder farms or those that are smaller than 2 ha, produce only ~32% of the world’s food supply, using ~24% of the world’s agricultural land (Ritchie 2021). Although focused mostly on cropping and traditionally rice cultivation in Southeast Asia (SEA), smallholder farmers also contribute to world meat production and this has been increasing as large ruminants previously used for draft have become available for meat following widespread mechanisation for rice cultivation (Windsor 2011). Approximately 90% of meat is obtained from chickens, pigs and cattle, reaching 357 million tonnes in 2021, compared with 124 million tonnes in 2000 (Food and Agriculture Organisation (FAO) 2023a). The 4% increase in production between 2020 and 2021 was the fastest over the 2000–2021 period. Smallholder farmers also contribute to the global production of bovine milk, although this is a recent development in SEA. Cattle and buffalo contributed 96% of the global milk produced in 2021, increasing to 884 million tonnes. Asia was the largest milk-producing region in 2021, with 44% share of the total, a 142% increase between 2000 and 2021, from 159 million tonnes to 384 million tonnes, although this mostly occurred in India (126 million tonnes), with a 23% share of the global total (Food and Agriculture Organisation (FAO) 2023a).

Increasing the productivity of smallholder farming is considered a crucial step in countries transitioning from poverty to middle incomes (Ritchie 2021). Because these farming families are some of the poorest people in the world, mostly located in developing countries, improving their outputs and incomes is important, even if they are likely to continue to produce less than the non-smallholder farming sector. Enhancing livestock farming in developing countries includes both use of large ruminants for meat and, more recently, milk production from buffalo that are increasingly no longer required for cultivation (Windsor et al. 2021a; Laos Buffalo Dairy (LBD) 2023). Both commodities are now providing important pathways in the amelioration of rural poverty, particularly in the Greater Mekong Subregion region (GMS) of SEA (Windsor 2011). This includes the Lao People’s Democratic Republic (Lao PDR, Laos) and Cambodia, where a majority of the population live in rural communities, often remotely, with minimal services available. These farming families depend on their livestock as ‘cash banks’ and for household food security, providing manure as fertiliser and increasingly for energy through biodigestors, with some large ruminants also being valued for transportation and, more recently, provision of milk for improved childhood development (Laos Buffalo Dairy (LBD) 2023).

Sustained increases in global demand for meat and milk have driven both increasing production and supply via trade, with Asia becoming a net importer of all commodity food groups other than fish in 2021 (Food and Agriculture Organisation (FAO) 2023a). Increases in both imports and local production of livestock and their products to meet increasing demand in the GMS, more broadly in SEA, and, importantly, in countries beyond this region, require improved adoption of existing ‘best practice’ animal-husbandry technologies (Young et al. 2014). This includes improvements in feeding systems, health interventions, reproductive management, housing, manure management and, importantly, marketing and safe processing of livestock and their products (Windsor et al. 2021a). Such improvements have been estimated to potentially assist the global livestock sector to reduce greenhouse-gas emissions (GHGe) by as much as 30% (Food and Agriculture Organisation (FAO) 2018).

Global animal-protein production is associated with total emissions of 6.2 Gt of carbon dioxide equivalents (CO₂eq), or ~12% of the estimated 50–52 Gt CO₂eq of total anthropogenic emissions in 2015 (Food and Agriculture Organisation (FAO) 2023b). Cattle are the largest contributors to GHGe, producing ~3.8 Gt CO₂eq per year, or 62% of all livestock emissions (Food and Agriculture Organisation (FAO) 2023b). Pigs, chickens, buffaloes and small ruminants contribute to 14%, 9%, 8% and 7% respectively, of livestock’s overall emissions. Approximately two-thirds of global emissions are allocated to meat production across all species, with approximately one-third being related to the production of feed inputs, including fertiliser and farm chemical use. It has been noted that variations in emission intensity (EI; kg CO₂eq/kg product) or ‘carbon footprint’ across countries, species and production systems, reflect differences in breeds, management practices, feed quality and environmental conditions. Addressing these differences offers potential pathways for reducing the carbon footprint of the livestock agrifood systems (Food and Agriculture Organisation (FAO) 2023b).

Financial motivation to improve the efficiency of cattle and buffalo production has followed an upward trajectory for two decades, particularly in the GMS, where cattle and buffalo liveweight price trends have continued to increase because of growing regional beef consumption (Windsor et al. 2021b). This has created opportunities for some smallholder famers to significantly improve their livelihoods, with fattening operations and small feedlots emerging in some locations. However, many livestock farmers in developing countries have low animal-husbandry skills, minimal nutritional, biosecurity, animal-disease and reproductive management knowledge, have poor access to markets and high rates of illiteracy (Nampanya et al. 2014a; Young et al. 2014; Windsor et al. 2021b). As extension and veterinary services in GMS countries are usually limited, smallholders often have suboptimal abilities for use of the nutritional, health and reproductive interventions that published research has demonstrated can greatly improve efficiency of livestock production. For example, in Laos and Cambodia, fewer than 60% of farmers are using vaccines on cattle and buffalo and these are typically administered to only half the herd or less, preventing the establishment of herd immunity for haemorrhagic septicaemia (HS; Kawasaki et al. 2015) and foot-and-mouth disease (FMD; Rast et al. 2010; Nampanya et al. 2014a, 2014b). This occurs despite the evidence of socioeconomic benefits and successful outcomes from implementation of household and regional vaccination programs (Young et al. 2016; Nampanya et al. 2018).

This paper documents the reflections presented in a plenary talk delivered at the International Conference on Sustainable Animal Agriculture for Developing Countries biennial (SAADC) conference in Vientiane, Laos, 21–24 November 2023. The aim was to provide a perspective on the progress in managing risks of transboundary animal diseases (TADs), plus one-health (OH) and ecosystem-health (EH) concerns in the GMS; however, owing to the increasing inter-connectedness of countries in the SEA region, especially for trade in livestock and their products, the term ‘GMS and beyond’ is preferred (Mekong Livestock Research and Beyond (MLRB) 2023). The paper is informed by ‘hands-on’ experiences in applied research in the region that commenced in 1998, and continues. This work is important because SEA is considered the most likely source of TAD risk to Australia (Blacksell et al. 2019). The objective was to share knowledge of the dynamic nature of both FMD and other emerging infectious diseases (EIDs) including OH and EH concerns of farmed animal populations in the region, plus describe interventions that may assist future progress. It is important to recognise that addressing regional TAD risks requires an understanding that because livestock production systems in SEA remain so very different from those of Australia, progressing TAD control and OH and EH concerns in the GMS and beyond is very challenging.

The persistent challenges of traditional livestock farming in the GMS

Livestock diseases, particularly TADs and zoonoses, increasingly threaten the lives and livelihoods of the often marginalised, smallholder farming communities in the GMS. Diseases pose significant risks to farming families, their livelihoods and, increasingly, the global human population, particularly when animal pathogens cross species barriers into humans as zoonoses. Further, the antimicrobial use (AMU) of therapeutics for livestock disease management, often inappropriately contribute to residues and/or risk of antimicrobial resistance (AMR). These emerging OH threats have been of concern for decades, particularly following emergence of strains of highly pathogenic avian influenza (HPAI) viruses (World Health Organization (WHO) 2017; World Organisation for Animal Health (WOAH) 2023a), henipaviruses (World Health Organization (WHO) 2018) and the SARS-associated coronavirus causing severe acute respiratory syndrome (SARS) in 2003 (World Health Organization (WHO) 2023), suggesting a global pandemic was likely to emerge, possibly in the vicinity of the GMS (World Health Organization (WHO) 2023). These predictions heralded arrival of the most unfortunate of OH coronavirus disasters that emerged just to the north, when covid-19 emerged in Wuhan and rapidly spread globally.

To control animal diseases, implementation of disease-control policies that facilitate programs focusing on promoting positive behavioural change by individual smallholder farmers is required. The aim is to use knowledge-based and other interventions to encourage adoption of disease prevention, through vaccination and biosecurity, and other disease-management interventions, including parasite control. Unfortunately, these programs often fail or deliver suboptimal outcomes (Windsor and Hill 2022).

Why has improved livestock health, productivity and welfare for food security and rural poverty alleviation continued to be so difficult to deliver in developing countries? Although management of TADs/OH/EH is strongly inter-related, these require effective disease surveillance and efficient response capacities. Attempts to continually improve these capabilities have been numerous, with a long list of research and development programs having been delivered. However, it is likely that the generally piecemeal improvements of in-country and regional disease-management mechanisms and capacities has largely failed to keep pace with the rapid increases in risks to food security and health in the GMS and beyond. These have emerged following both the impressive economic development in the region (Miller et al. 2018; Blacksell et al. 2019) and the increasing vulnerability of livestock production to climate-change crisis risks, including episodes of severe hypothermia (Khounsy et al. 2012).

Although it is apparent that the increasing TAD/OH/EH risks reflect the rapid rise in consumer demand from changing dietary preferences, driving increased animal and product movement, this has been accompanied by climate-change impacts, driving increased vulnerability of livestock agrifood production systems to both ecosystem and disease shocks. Epidemics of African swine fever (ASF; Matsumoto et al. 2021), incursions of new FMD virus strains (Blacksell et al. 2019), occurrence of lumpy skin disease (LSD; Ratyotha et al. 2022) and risk of peste petits ruminants (PPR; Burns et al. 2019) with persistent outbreaks of HPAI in the GMS and beyond (Pfeiffer et al. 2013) appear to both threaten food insecurity and are likely to increasingly be caused by it. This increasingly complex situation is now confounded with an expectation that the high-EI livestock agrifood systems of the GMS will need to find means of amelioration of the GHGe that result from the mostly inefficient smallholder farms (Windsor et al. 2021a; Windsor and Hill 2022). The EIs of meat production from cattle in Laos, Cambodia and Indonesia at 102.9, 88.51, 58.72 respectively, are comparatively much higher than the EIs of global average and Australian beef meat production systems at 30.28 and 22.01 respectively (Food and Agriculture Organisation (FAO) 2023a).

Problem definition in the GMS livestock systems

Ongoing applied field research has been conducted by our Mekong Livestock Research and Beyond (Mekong Livestock Research and Beyond (MLRB) 2023) team for over one and a half decades in Laos and Cambodia, documenting the systematic constraints that influence the understanding by farmers of disease-related risks, plus the household-level decisions involved in investing in animal-disease control. The work has involved numerous longitudinal livestock production and health studies and participatory observations, accompanied by in-depth interviews and focus-group discussions, involving farming families in numerous research-site villages in both countries (Nampanya et al. 2014a, 2014b, 2014c; Young et al. 2014). Although there were many partners involved, progress depended on key relationships in both countries, particularly Dr Syseng Khounsy of the Department of Livestock and Fisheries in Laos (DLF) and Dr Suon Sothoeun of the General Directorate of Animal Health and Production in Cambodia (GDAHP). Numerous collaborations with sharing of insights and training materials with other research teams and international agencies, especially WOAH and FAO, have also contributed to the learning that has informed this process (Australian Centre for International Agricultural Research (ACIAR) 2012, 2013; Nampanya et al. 2014c, 2017, 2018).

This research identified the ongoing structural constraints of low health and husbandry knowledge, weak veterinary health and rural extension systems, poor supply-chain infrastructure plus limited access of farmers to markets and low-interest credit. These and other constraints prohibit more progressive farmers from gaining the necessary knowledge for application of disease-prevention practices, inhibiting abilities to invest in risk management and increasing their economic vulnerability. Such constraints drive behaviours that are often recognised as ‘high risk’ for disease emergence and spread, including sale and purchase of diseased stock, lack of vaccination, failure to implement quarantine and hygiene, failure to report disease outbreaks to animal-health authorities, inadequate use of anthelmintics and, importantly, excessive and inappropriate use of antimicrobials (Windsor et al. 2020). These behaviours lead to many small- and medium-scale farmers in the GMS and beyond remaining trapped in a cycle of poverty, poor productivity and, commonly, ill health for both animals and humans (Windsor 2011; Nampanya et al. 2014a, 2014b, 2014c; Young et al. 2015).

Whereas it is challenging to address the complexities of these issues, if production deficits and disease impacts are to be sustainably ameliorated, it has been important to understand the motivations and resistance characteristics of smallholder farmers in the GMS. Many farmers still consider disease outbreaks as an ‘act of god’ and that disease control is either unmanageable or a government responsibility. We have learned that whereas the knowledge required to control disease mostly requires implementation of risk-management interventions, particularly vaccination and biosecurity, these strategies are not recognised by farmers as ways for them to generate income, or more importantly, decrease their workloads, particularly when their thinking is that disease is something that is to be treated, rather than prevented. This means that many disease-control advisory programs have and will continue to fail because they are considered unaffordable.

Recognising motivations and resistance to change

Our initial work identified that successful implementation of animal-health and -production programs required farmer learning that is both participatory and motivational (Nampanya et al. 2012). This was assumed to be the introduction of interventions that assisted smallholder farmers to recognise socioeconomic improvements, particularly increased household income. Because this often involves work that is outside of the immediate disciplines of the animal-health personnel, it required larger teams with nutritional, marketing and social science expertise, including gender-focused strategies (Bush et al. 2014a, 2014b; Nampanya et al. 2014c; Mekong Livestock Research and Beyond (MLRB) 2019). The experiential learning acquired was that once money was being made and workloads decreased by smallholder farmers from feeding their animals properly using forage plantations and more recently molasses blocks, they then began to understand that they should protect this ‘investment’ of labour and they became more receptive to the necessity of adopting health interventions. Of importance was that the successful adoption of some interventions was due to motivations other than income generation, particularly the ‘time-savings’ acquired, enabling more time for other farming activities and improved education of children now spending less time seeking feed for the animals. The introduction of forages decreased the labour required to provide adequate ‘cut and carry’ feed and, recently, the availability of molasses blocks ensured easier animal management of animals with more rapid return from open grazing to access the blocks (Mekong Livestock Research and Beyond (MLRB) 2023). Clearly, understanding the implementation of animal production- and health-improvement programs is the recognition that motivations and resistance assumptions may not always be what was initially expected.

This experience was first observed in the successful FMD eradication program in the Philippines in 1998–99, where it was found that although training on FMD and biosecurity was considered important, the majority of farming households mainly wanted to know how to improve the feeding of their pigs. Supplementing their use of kitchen waste or swill enabled them to obtain more money from their pigs and the cooking of the kitchen waste created a biosecurity intervention that prevented FMD virus transmission (Windsor et al. 2011). Similarly with Cambodian cattle from 2007, forages were introduced for feeding and fattening of cattle, taking several years to establish. These plantations eventually proved to be very successful in motivating farmers to adopt change (Nampanya et al. 2012), resulting in the development of a robust market for forages for cattle feeding. Of importance were the socioeconomic impacts of forages for rural families, with time saved in efficiently feeding their animals and more readily available collection of manure for fertiliser and/or energy. Numerous families in our research programs are now able to afford to send their children to university from the additional funds achieved from moving from subsistence smallholder ‘keepers’ to more productive small–medium cattle-raising enterprises (Mekong Livestock Research and Beyond (MLRB) 2018).

What are the solutions?

Reflections from the learning acquired during the studies conducted by our team members, collaborators and the findings of others working in the GMS livestock sector, as briefly described above, has led to the conclusion that future efforts require delivery of the following three major strategies:

Discussion

This paper has provided a perspective on progressing TAD/OH/EH in the smallholder livestock farming system in the GMS and more broadly in SEA. It confirmed that the concepts and practices of improved animal production, health and welfare have been slow to gain traction, despite rapidly improving economies in the region that has created a sustained increase in demand for livestock and their products. The surging demand has increased both TAD, EID and OH risks from extended informal movements of livestock and their products. There has been slow adoption of OH concepts and practices, with increased AMR risk from unregulated antimicrobial use and minimal AMR stewardship. Further, EID risks from substandard slaughtering facilities and unhygienic ‘wet markets’ where the sale of wildlife adjacent to livestock is often still tolerated, persists. Changed management efforts are required to improve regional biosecurity, yet motivating governments and farmers and others in the value chain to adopt these interventions, is very challenging (Young et al. 2015).

The use of highly visible interventions capable of creating rapid system change by motivated farmers and other stakeholders and that overcome resistance to change, are urgently required. Access to ECBs to increase productivity and improve management, accompanied by leveraging targeted health surveillance and preventive strategies, including vaccination and endoparasite control to reduce disease risk, have the potential to help drive these practice changes. It has been suggested that the apparent awakening to the importance of biosecurity in the post-covid pandemic era may convince many that TAD/OH/EH should be a collaborative priority for all medical, veterinary and animal-production authorities (Windsor and Hill 2022). There is a desperate need to create a more receptive environment for the change management required to progress both animal health and welfare through productivity innovations, assisting GHGe mitigation from the currently inefficient livestock systems, particularly in developing countries in the GMS and beyond.

The reflections documented here suggest that international development projects are important because they can contribute significantly through upscaling livestock husbandry and health knowledge, practices and infrastructure, addressing weaknesses in the value chain and creating a more sustainable food-security system. However, the multiple benefits of leveraging from commercial investments in climate-smart livestock systems is an interesting new development in Laos, and potentially Cambodia, Indonesia and beyond. This initiative requires governance, advocacy and policy settings that encourage both cross-sectoral collaborations and reputable international trading systems, particularly for carbon credits. However, because it provides a pathway for adoption of improved livestock dietary and health initiatives that reduce high levels of methane EI and potentially diminish TAD/OH/EH risks in the smallholder production systems in the GMS and beyond, it should be encouraged and facilitated.

Currently, SEA farming systems are dominated by the inefficient smallholder ‘animal-keeper’ system, compromising low-level literacy, very limited resource availability and an historical preference for unhygienic ‘wet-market’ processing and trading that avoids refrigeration and, often, food safety and quality assurance. Further, the ineffective development of local and regional biosecurity and other disease-prevention services by under-funded national and international livestock services persists, with any improvements being only slowly adopted, particularly in the GMS. That these and other risk factors have persisted for decades, despite evidence of a sustained period of rapidly expanding regional demand for animal-sourced foods, is frustrating.

The increasing risks of TAD incursions and OH and EH concerns are clearly evident from recent disease-surveillance information. Regular arrival of new strains of FMD in SEA has accompanied persistent circulation of endemic strains, with loss of general population immunity following the inevitable replacement by vulnerable animals. Similarly, there have been repeated occurrences of HPAI, accompanied by arrival of epidemics of ASF, porcine reproductive and respiratory syndrome (PRRS), LSD and PPR in SEA and beyond. That the covid pandemic emerged in the vicinity of SEA reflects that these factors are of relevance to managing OH concerns, including EIDs, zoonoses and increasing AMR. Further, the slow adaption to increasingly deleterious climate impacts is apparent in countries where increasingly severe floods, droughts, hyperthermia and hypothermia episodes are emerging, albeit in countries with some of the highest EIs of ruminant animal production. The observations reviewed here indicate the severity of these issues in the near neighbourhood of Australia. The importance of both maintaining vigilant national biosecurity and increasing engagement with the GMS and beyond to more directly address regional TAD/OH/EH challenges, is emphasised.