Introduction
Foot-and-Mouth Disease (FMD) is internationally recognised as the most important of the transboundary diseases (TADs) of livestock, impacting negatively on farm incomes, national economies, and severely compromising global food security. FMD has been observed in South-East Asia (SEA) for approximately 150 years and remains endemic, with generally piecemeal control measures until an integrated approach was initiated by OIE (now World Organisation of Animal Health) in 1990 that led to development of the South-East Asia Foot and Mouth Disease (SEAFMD) Campaign, with the first regional meeting held in 1997. This initiative was strengthened by the launch of the Global Framework for the Progressive Control of Transboundary Animal Diseases (GF-TADs) in 2004, aimed at the prevention, detection, and control of TADs, addressing regional and global dimensions, and combining the strengths of the international organisations to achieve agreed common objectives.
SEAFMD, now the South-East Asia and China Foot and Mouth Disease (SEACFMD) campaign with expansion of the original seven countries to 12, facilitates regional alliances in TAD control to collaboratively build capacities of the member countries. This activity now occurs within the Global FMD Control Strategy that was endorsed by representatives from over 100 countries and international and regional partners at the 2nd Global Conference on FMD in Bangkok, Thailand in 2012. SEACFMD and GF-TADs aim to reduce the regional and global burden of FMD and the risks of reintroduction of the disease into free areas, assisting FMD-free countries to maintain their status. The SEACFMD campaign achieves these aims by facilitating a plethora of activities described in the Strategic Plans that have become a series of phased roadmap documents and now using tools that appear to have lifted the momentum of FMD control, including:
There has been substantial progress through the development of the SEACFMD campaign and completion of five phases of implementation from 1997 to 2020: Phase 1 (1997-2001), establishing the Campaign; Phase 2 (2001-2005), refining strategic direction and components of the Campaign; Phase 3 (2006-2010), improving coordination and partnership efforts; Phase 4 (2011-2015), implementation and refining of FMD control strategies with targeted vaccination and enhanced technical coordination; Phase 5 (2016-2020), continuing a sustainable approach to FMD control with expansion of the PCP-FMD; and Phase 6 (2021-2025), proposing a pragmatic and sustainable approach for FMD control and prevention to guide countries in implementation of their national FMD plan on scientific evidence.
The sixth phase also sought an evaluation of the SEACFMD campaign to provide guidance for its future by identifying successes and gaps. I was privileged to have conducted this evaluation in 2022, with assistance from my USYD colleague Harish Tiwari. Unfortunately, shortly after commencing the evaluation, Indonesia became infected with FMD after a period of disease freedom of nearly 40 years; clearly a setback for SEACFMD. Regardless, we progressed the SEACFMD evaluation, with some key findings summarised below.
What happened in Indonesia?
The current outbreak of FMD was reported initially from East Java, where the provincial government stated that between the 28 April 2022 and 3 May 2022, around 1,247 cows in four districts showed clinical signs of FMD. In just three weeks, the FMD outbreak was found to have spread widely across the country, with 24 provinces suspected of having FMD, including the Australian tourist destination island of Bali. Most cases appeared to be concentrated in Java and Sumatra Islands, where 80% of the national beef production and the majority of the dairy production occurs. The rapid spread of FMD was recognised as a significant threat to the livestock industry in Indonesia and neighbouring countries. Reports were that cattle with FMD had anorexia and were rapidly losing weight, resulting in lower incomes for farmers who were unable to sell the infected animals and ceased the purchase of concentrate feed to invest in disinfectants, vitamins, and antibiotics for animal treatment.
I was able to spend a fascinating few days in Malang East Java (via Surabaya) in mid-July 2022, initially revisiting the University of Muhammadiyah Mulang. I previously visited there in February 2020 to commence a nutritional and health intervention collaboration, just as the global COVID-19 pandemic was becoming established. After presenting a guest lecture on cattle health and production including FMD, Lumpy Skin Disease (LSD), and improving cattle nutrition for recovery from oral illnesses, we visited two smallholder (backyard) dairy farms in Ngangtang, both with Friesian cows recovering from FMD. Farm 1 had recently experienced a massive drop in herd daily milk yield from their 18 cows; from 230L/day to 15L/day after FMD hit them in mid-May and now at 100L/day in mid-July (Figure 4). Farm 2 had experienced a complete herd daily milk yield loss from their 29 cows, from 400L/day to almost zero after FMD hit them in mid-June. They were also back to 100L/day by mid-July (Figure 5).
Both farms lost at least one cow and several calves during their outbreaks. Evidence to support the implementation of many farm-level biosecurity practices was not readily available. On-farm management included frequent use of injectable antibiotics, NSAIDs (flunixin), and vitamins, and widespread use of antibiotic sprays (oxytetracycline as Limoxin) and CuSO4 spray. This reflects the immediate focus of smallholder farmers on treatment of FMD-affected animals and the importance of recent studies confirming the efficacy of pain relief products for therapy ahead of antimicrobials (Windsor, 2001, 2002). In mid-July 2022, despite FMD having been absent from Indonesia since the early 1980s, there were reports of over 300,000 cattle in 19 provinces having been affected in the ~16m cattle population. Frustratingly, less than a million of the three million doses of vaccine that had been ordered had arrived. Received doses were administered from mid-June 2022 to priority animals, particularly the national dairy herd (~200,000 animals) in which nearly all animals had recently been infected with FMD and so were already immune.
SEACFMD Evaluation and Biosecurity deficits
The SEACFMD evaluation commenced in early 2022 with a detailed review of the published roadmaps, PCP-FMD, PVS, previous evaluation documents and scientific literature and other documents, which informed the questionnaire for the extensive stakeholder consultations. Despite the incursion of FMD into Indonesia, we developed the survey tool, including the use of the Organisation for Economic Co-operation and Development (OECD) policy monitoring and evaluation (M&E) criteria:
We conducted online interview testing with an 'expert' group (n=12), followed by distribution of an online comprehensive qualitative survey (n=35 responses). To enhance response rates, an abbreviated quantitative online survey improved the number of responses (n=58 responses). These surveys were followed with face-to face focus group discussions with many respondents (n=34) at the 26th SEACFMD Coordinators Meeting in Bali, 3-5 October 2022 (total responses used, n=92).
There were many and varied strengths and gaps identified in the documents, responses to survey questionnaires and in the focus group discussions, with recommendations offered to address the gaps. Importantly, there was general agreement that the structural expansion of SEAFMD through SEACFMD to involve more countries in the region beyond the Greater Mekong Subregion (GMS) was appropriate and that as increasing interconnectedness of FMD virus pools is occurring, this adaptability should continue. There was also agreement that the evolution of the phases of the SEACFMD Campaign was a robust mechanism that facilitated progress, particularly since the introduction of the PVS and PCP-FMD tools. This agreement was reached despite repeated incursions of FMD, African swine fever, peste des petits ruminates, and other TADs into the region. Further, respondents from all roles and affiliation categories unequivocally agreed that the SEACFMD campaign has been extremely successful in orchestrating solid relationships between technical staff, facilitating fruitful coordination and communication amongst member countries, whereas success in nurturing political and financial commitments for sustainability of the interventions was insufficient.
Issues with biosecurity mean vaccination is critical
The increasing literature on FMD control in SEA includes: in-country history of FMD (Nampanya et al., 2016), virology and immunology (Buckle et al. 2021), epidemiology (Miller et al. 2018), socio-economic impacts (Nampanya et al.. 2016), vaccination strategies and impacts (Nampanya et al., 2018; Rast et al. 2010), biosecurity and strategic disease control (Windsor et al. 2011), with the regional history of FMD in SEA summarised (Blacksell et al. 2019). The literature has increasingly emphasised that more effective FMD control requires the development of improved regional biosecurity and reduced movement of livestock and their products throughout the GMS. However, because of this widespread failure to improve regional biosecurity, including a reduction in livestock and animal product movement, a critical issue in the interim has been the importance of increasing FMD vaccination, focusing on vaccine serotypes and matching, strategies and efficacy, and delivery logistics and capacities. Important logistical lessons were learned from delivering an extensive FMD vaccination program between 2012 and 2016 in northern Lao PDR relevant to future FMD vaccination programs, ensuring the momentum of FMD control with vaccination is sustainable (Nampanya et al., 2018). These include:
i. Continuation of the vaccination program every 5-6 months for several years is required, particularly in targeted FMD high-risk areas,
ii. Increasing vaccination days from one to 2-3 days per village to enable most adult cattle and buffalo in the village to be vaccinated with the aim to increase vaccination coverage (as observations were that a field vaccination day would vaccinate a maximum of 100-200 animals per day),
iii. increasing FMD vaccine availability and vaccination coverage by providing FMD vaccines for village veterinary workers to continue vaccination in their villages (one or two 100cc FMD vaccine bottles),
iv. provision of improved animal restraint facilities to supplement the use of bleeding poles with portable yards and animal crushes and superior vaccination equipment, including vaccine guns with protective sheaths to minimise self-administration, is required for staff conducting vaccinations,
v. consideration of payment of vaccinating staff based on the number of animals vaccinated per day or per trip (rather than a set per diem as used currently),
vi. improving the current data management system (i.e., the number of adult animals vaccinated in each village and district) to produce more accurate data on FMD vaccination coverage,
vii. accompanying vaccination with information and training on improving animal movement controls and biosecurity practices, including compliance activity targeted at illegal movement of live animals and their products,
viii. strengthening active and passive disease surveillance and disease reporting at the village, district, provincial and national levels through public awareness campaigns,
ix. continuation of regular two-stage random sampling serosurveys to provide increasing evidence of FMD control, eventually supporting a potential FMD-free zone with vaccination application to WOAH,
x. continuation of sampling and testing strategies to evaluate post-vaccination responses and ensure vaccine matching against emerging isolates is maintained,
xi. continuation of training programs for vaccination staff and farmers on essential biosecurity to limit the risk of FMD transmission, preferably delivered separately from vaccination days (due to time constraints),
xii. Improving public awareness of FMD risks, transmission, and prevention along with training on production improvement (e.g., forage plantation and utilisation, parasite control, and knowledge of good husbandry practices) to enhance livelihoods.
xiii. promote understanding of disease risk management at all levels of the livestock husbandry system.
FMD vaccination suppresses signs temporarily
Despite the apparent, albeit temporary, success of this northern Lao PDR FMD vaccination program, outbreaks returned within a year of cessation, suggesting that the vaccination program suppressed clinical expression of FMD at the village level but was insufficient to eliminate FMD clinical outbreak risk. Following the cessation of the northern Lao PDR FMD vaccination program (Nampanya et al. 2018), a cross-sectional seroprevalence study in nine northern Lao provinces was conducted in early 2019, sampling large ruminants (n = 602) and goats (n = 19) from 30 villages (MacPhillamy et al. 2022). A seroprevalence of 43.7% and 90% was found in the sampled villages with at least one seropositive animal. Notably, an examination of current reporting behaviours of farmers, village veterinary workers and district and provincial officials found that individuals were using their discretion on whether disease events required reporting along the chain of command. This study confirmed the likelihood of foot-and-mouth disease virus (FMDv) transmission despite a failure to detect and report clinical cases. It highlighted the necessity of public awareness programs to increase the reporting of both the presence and absence of clinical disease, similar to the so-called 'FMD negative reporting' that was introduced in the Philippines FMD eradication program (Windsor et al. 2011).
FMDv transmission in the absence of clinical detection was further evaluated in a study using serum and dry mucosal swabs. Samples collected from the nasal, oral, and dorsal nasopharyngeal mucosal surfaces of healthy cattle (n = 84 in Laos; n = 125 in Myanmar) and buffalo (n = 48 in Laos; n = 5 in Myanmar) immediately after slaughter in three slaughterhouses were evaluated for the presence of viral RNA (Buckle et al, 2021). Testing of swabs using pan-serotypic real-time reverse transcription-PCR (rRT-PCR) and serum using the FMD PrioCHECK non- structural protein (NSP) ELISA found 7.3% of animals had detectable FMDv RNA in one or more of the three sites (5.3% of nasopharyngeal, 2.3% of oral, and 1.5% of nasal swabs) with no FMDv RNA detected in serum. A third (37.8%) of animals were positive for NSP antibodies, indicating likely past natural exposure to FMDv. Results were comparable for Laos, Myanmar, cattle, and buffalo, with no significant difference between age groups. The presence of FMDv RNA on the oral and nasal mucosa of clinically healthy large ruminants in Laos and Myanmar demonstrates the importance of sampling asymptomatic animals during FMD surveillance programs. It suggests that subclinical infections may have a role in the epidemiology of FMD.
Further lessons on FMD vaccination
A survey was conducted on the implementation of FMD vaccination programmes in SEACFMD countries (OIE, 2021), yielding valuable information on the status, challenges, strategies, and practices adopted by the various SEACFMD member countries with endemic FMD. The findings provide a useful baseline indicator to measure the progress of Output 1.3 of the SEACFMD Roadmap of 2021-2025, described as a 'robust vaccination strategy developed, including access to quality vaccines and vaccination data management and analyses.' The main recommendations of this study addressed to member countries include:
i. Follow a vaccination protocol based on scientific evidence, including the use of a two-dose primary course consisting of a first dose at the age of three to four months and a second vaccination at least three to four weeks after the first dose; and vaccination of animals at six monthly intervals.
ii. Develop or strengthen partnerships with the private sector, such as cattle owners, dairy/beef associations, private veterinarians, and veterinary paraprofessionals to implement FMD vaccination following the OIE PPP Handbook: Guidelines for Public-Private Partnerships in the veterinary domain.
iii. Monitor the vaccination campaign to review the success of vaccine delivery, the level of induced immunity, and their impact on disease and infection. A systematic investigation of reported outbreaks in vaccinated herds following FAO/OIE Guidelines on FMD vaccination and post-vaccination monitoring is mandatory.
iv. Use vaccines that follow OIE standards (for those countries in PCP-FMD Stage 3 and above) and vaccine types based on circulating FMDv strains.
v. Procure vaccines from qualified FMD vaccine manufacturers based on The European Commission for the Control of Foot-and-Mouth Disease pre-qualification criteria for FMD and similar TADs.
vi. All FMD-free countries should identify a vaccine compliant with OIE standards and detailed vaccination plans for implementation during FMD incursions.
Summarised Outcomes of the SEACFMD Evaluation
Of the many suggestions offered during the extensive stakeholder consultations during the SEACFMD evaluation, the 13 key recommendations were that future SEACFMD activities should:
Conclusions
FMD control in SEA, and Indonesia in particular, is unlikely to be achievable without greater regional commitment to collaborative integration and resourcing of disease control activities. Almost insurmountable challenges remain despite the progress of SEACFMD, including: insufficient biosecurity practices with unregulated animal movements between and within infected countries; difficulties of vaccine resourcing, application and delivery, compromising its efficacy; low-level field technical capacity to deliver adequate surveillance and response; low levels of local engagement of smallholders in disease control awareness; lack of national emergency disease response capacities; and difficulties in co-ordination of national and international control programs. Continued funding of FMD control programs in endemically-infected countries is required, particularly to improve technical capabilities in the field and improve the implementation of disease control tools, including biosecurity, compliance with movement controls, vaccine delivery, surveillance, and public awareness programmes for FMD control. Increased emphasis on effective advocacy and governance is urgently required.
FMD control and freedom will likely remain difficult to achieve in the short- to medium-term in most endemically infected countries as each has its own national disease control and resource allocation priorities and modernisation of livestock production systems remains surprisingly slow. For example, one country will have its own policy on live animal imports or frozen meat that may well not align to those of others participating in the trading bloc. Potentially, the government of China will have an increasingly important role in FMD stewardship, although complicated by China not being an Association of Southeast Asian Nation member state and the slowing of momentum on FMD control in China since the beginning of the COVID-19 pandemic.
FMD control and freedom is a step-by-step process that requires continued international integration of efforts, especially in facilitating trade, managing risk and implementing biosecurity. If regional/transnational trade systems become more formalised, then it may be possible to reduce the current risks from trading patterns in cattle and animal products that facilitate FMDv transmission. All factors discussed in this paper are of relevance to control of FMD in SEA for the foreseeable future and are arguably, critical for Australia if we are serious in reducing the risk of TAD incursions into Australia, including provision of vaccines and pain-relief therapy (Figures 6,7,8) for addressing welfare concerns of FMD.
References