An experimental game to assess hunter's participation in zoonotic diseases surveillance.

BACKGROUND: Strengthening the surveillance of zoonotic diseases emergence in the wild meat value chains is a critical component of the prevention of future health crises. Community hunters could act as first-line observers in zoonotic pathogens surveillance systems in wildlife, by reporting early signs of the possible presence of a disease in the game animals they observe and manipulate on a regular basis. METHODS: An experimental game was developed and implemented in a forested area of Gabon, in central Africa. Our objective was to improve our understanding of community hunters' decision-making when finding signs of zoonotic diseases in game animals: would they report or dissimulate these findings to a health agency? 88 hunters, divided into 9 groups of 5 to 13 participants, participated in the game, which was run over 21 rounds. In each round the players participated in a simulated hunting trip during which they had a chance of capturing a wild animal displaying clinical signs of a zoonotic disease. When signs were visible, players had to decide whether to sell/consume the animal or to report it. The last option implied a lowered revenue from the hunt but an increased probability of early detection of zoonotic diseases with benefits for the entire group of hunters. RESULTS: The results showed that false alerts-i.e. a suspect case not caused by a zoonotic disease-led to a decrease in the number of reports in the next round (Odds Ratio [OR]: 0.46, 95% Confidence Interval [CI]: 0.36-0.8, p < 0.01). Hunters who had an agricultural activity in addition to hunting reported suspect cases more often than others (OR: 2.05, 95% CI: 1.09-3.88, p < 0.03). The number of suspect case reports increased with the rank of the game round (Incremental OR: 1.11, CI: 1.06-1.17, p < 0.01) suggesting an increase in participants' inclination to report throughout the game. CONCLUSION: Using experimental games presents an added value for improving the understanding of people's decisions to participate in health surveillance systems.

Environmental and economic determinants of temporal dynamics of the ruminant movement network of Senegal.

Our understanding of the drivers of the temporal dynamics of livestock mobility networks is currently limited, despite their significant implications for the surveillance and control of infectious diseases. We analyzed the effect of time-varying environmental and economic variables-biomass production, rainfall, livestock market prices, and religious calendar on long-distance movements of cattle and small ruminant herds in Senegal in the years 2014 and 2019. We used principal component analysis to explore the variation of the hypothesized explanatory variables in space and time and a generalized additive modelling approach to assess the effect of those variables on the likelihood of herd movement between pairs of administrative units. Contrary to environmental variables, the patterns of variation of market prices show significant differences across locations. The explanatory variables at origin had the highest contribution to the model deviance reduction. Biomass production and rainfall were found to affect the likelihood of herd movement for both species on at least 1 year. Market price at origin had a strong and consistent effect on the departure of small ruminant herds. Our study shows the potential benefits of regular monitoring of market prices for future efforts at forecasting livestock movements and associated sanitary risks.

Elasticity and substitutability of food demand and emerging disease risk on livestock farms.

Disease emergence in livestock is a product of environment, epidemiology and economic forces. The environmental factors contributing to novel pathogen emergence in humans have been studied extensively, but the two-way relationship between farm microeconomics and outbreak risk has received comparably little attention. We introduce a game-theoretic model where farmers produce and sell two goods, one of which (e.g. pigs, poultry) is susceptible to infection by a pathogen. We model market and epidemiological effects at both the individual farm level and the community level. We find that in the case of low demand elasticity for livestock meat, the presence of an animal pathogen causing production losses can lead to a bistable system where two outcomes are possible: (i) successful disease control or (ii) maintained disease circulation, where farmers slaughter their animals at a low rate, face substantial production losses, but maintain large herds because of the appeal of high meat prices. Our observations point to the potentially critical effect of price elasticity of demand for livestock products on the success or failure of livestock disease control policies. We show the potential epidemiological benefits of (i) policies aimed at stabilizing livestock product prices, (ii) subsidies for alternative agricultural activities during epidemics, and (iii) diversifying agricultural production and sources of proteins available to consumers.

Longitudinal study of the immune response and memory following natural bovine respiratory syncytial virus infections in cattle of different age.

Human and bovine respiratory syncytial virus (HRSV and BRSV) are closely genetically related and cause respiratory disease in their respective host. Whereas HRSV vaccines are still under development, a multitude of BRSV vaccines are used to reduce clinical signs. To enable the design of vaccination protocols to entirely stop virus circulation, we aimed to investigate the duration, character and efficacy of the immune responses induced by natural infections. The systemic humoral immunity was monitored every two months during two years in 33 dairy cattle in different age cohorts following a natural BRSV outbreak, and again in selected individuals before and after a second outbreak, four years later. Local humoral and systemic cellular responses were also monitored, although less extensively. Based on clinical observations and economic losses linked to decreased milk production, the outbreaks were classified as moderate. Following the first outbreak, most but not all animals developed neutralising antibody responses, BRSV-specific IgG1, IgG2 and HRSV F- and HRSV N-reactive responses that lasted at least two years, and in some cases at least four years. In contrast, no systemic T cell responses were detected and only weak IgA responses were detected in some animals. Seronegative sentinels remained negative, inferring that no new infections occurred between the outbreaks. During the second outbreak, reinfections with clinical signs and virus shedding occurred, but the signs were milder, and the virus shedding was significantly lower than in naïve animals. Whereas the primary infection induced similar antibody titres against the prefusion and the post fusion form of the BRSV F protein, memory responses were significantly stronger against prefusion F. In conclusion, even if natural infections induce a long-lasting immunity, it would probably be necessary to boost memory responses between outbreaks, to stop the circulation of the virus and limit the potential role of previously infected adult cattle in the chain of BRSV transmission.

Antimicrobial Resistance in Africa-How to Relieve the Burden on Family Farmers.

Although currently available data indicate that Africa has the lowest usage of antimicrobials in animals in the world (adjusted by animal biomass), data show a high prevalence of antimicrobial resistance in foodborne pathogens isolated from animals and animal products. Apart from the lack of solid data on antimicrobial use in many countries in Africa, different hypotheses could explain this situation. Qualitative interviews of farmers show a lack of knowledge and uninformed use of antimicrobials. Considering the development of animal farming to meet an increasing demand for proteins, this deficiency represents a serious public health issue. We advocate for policies that consider the specific challenges faced by family farmers in Africa, to simultaneously improve access to veterinary drugs while strengthening the regulation of their use. We propose a global approach targeting the agri-food system, offering innovative social and technical interventions on antimicrobial usage, adapted to family farmers.

Poultry farmer response to disease outbreaks in smallholder farming systems in southern Vietnam.

Avian influenza outbreaks have been occurring on smallholder poultry farms in Asia for two decades. Farmer responses to these outbreaks can slow down or accelerate virus transmission. We used a longitudinal survey of 53 small-scale chicken farms in southern Vietnam to investigate the impact of outbreaks with disease-induced mortality on harvest rate, vaccination, and disinfection behaviors. We found that in small broiler flocks (≤16 birds/flock) the estimated probability of harvest was 56% higher when an outbreak occurred, and 214% higher if an outbreak with sudden deaths occurred in the same month. Vaccination and disinfection were strongly and positively correlated with the number of birds. Small-scale farmers - the overwhelming majority of poultry producers in low-income countries - tend to rely on rapid sale of birds to mitigate losses from diseases. As depopulated birds are sent to markets or trading networks, this reactive behavior has the potential to enhance onward transmission.

The past few decades have seen the circulation of avian influenza viruses increase in domesticated poultry, regularly creating outbreaks associated with heavy economic loss. In addition, these viruses can sometimes 'jump' into humans, potentially allowing new diseases ­ including pandemics ­ to emerge. The Mekong river delta, in southern Vietnam, is one of the regions with the highest circulation of avian influenza. There, a large number of farmers practice poultry farming on a small scale, with limited investments in disease prevention such as vaccination or disinfection. Yet, it was unclear how the emergence of an outbreak could change the behavior of farmers. To learn more, Delabouglise et al. monitored 53 poultry farms, with fewer than 1000 chickens per farm, monthly for over a year and a half. In particular, they tracked when outbreaks occurred on each farm, and how farmers reacted. Overall, poultry farms with more than 17 chickens were more likely to vaccinate their animals and use disinfection practices than smaller farms. However, disease outbreaks did not affect vaccination or disinfection practices. When an outbreak occurred, farmers with fewer than 17 chickens tended to sell their animals earlier. For instance, they were 214% more likely to send their animals to market if an outbreak with sudden deaths occurred that month. Even if they do not make as much money selling immature individuals, this strategy may allow them to mitigate economical loss: they can sell animals that may die soon, saving on feeding costs and potentially avoiding further contamination. However, as animals were often sold alive in markets or to itinerant sellers, this practice increases the risk of spreading diseases further along the trade circuits. These data could be most useful to regional animal health authorities, which have detailed knowledge of local farming systems and personal connections in the communities where they work. This can allow them to effect change. They could work with small poultry farmers to encourage them to adopt efficient disease management strategies. Ultimately, this could help control the spread of avian influenza viruses, and potentially help to avoid future pandemics.

Social network analysis of practice adoption facing outbreaks of African Swine Fever.

Animal epizootics show widely destructive effect on livestock value chains in sub Saharan Africa, pushing many smallholders into poverty and discouraging investments. Hence, African swine fever (ASF) has been playing a deeply depressing role on swine value chain of Benin since its first occurrence in the country in 1997. Exchanges between actors are fundamental among stakeholders for the overall performance of a value chain and is key in the way these can respond to challenges, as epizootic threats. The present study describes how stakeholders of the swine value chain interact in the diffusion of innovative practices facing an outbreak of ASF. In seven districts, focus groups were first organized with stakeholders to identify changes and other reactions that ensued from a recent ASF outbreak in Benin. In a second step, individual semi-structured interviews were conducted, following a respondent-driven sampling, to collect the contact information needed for social network analysis. The influence of actors' characteristics on their degree centrality was tested through multiple linear regression model. Regulatory requirements and available incomes facilitated practice diffusion among groups of pork butchers, traders/brokers and input suppliers. Stockbreeders displayed passivity in the diffusion of practices whereas they should have the forefront role in addressing the challenge of ASF. Nevertheless, their significant interest in capacity reinforcement, associations, exchange visits and professionalization may lead them to increase their involvement in a joint control of the disease.

Game theory of vaccination and depopulation for managing livestock diseases and zoonoses on small-scale farms.

Livestock producers adapt their farm management to epidemiological risks in different ways, through veterinary interventions but also by modulating their farm size and the removal rate of animals. The objective of this theoretical study was to elucidate how these behavioral adaptations may affect the epidemiology of highly-pathogenic avian influenza in domestic poultry and the outcome of the implemented control policies. We studied a symmetric population game where the players are broiler poultry farmers at risk of infection and where the between-farms disease transmission is both environmental and mediated by poultry trade. Three types of farmer behaviors were modelled: vaccination, depopulation, and cessation of poultry farming. We found that the transmission level of the disease through trade networks has strong qualitative effects on the system's epidemiological-economic equilibria. In the case of low trade-based transmission, when the monetary cost of infection is high, depopulation behavior can maintain a stable disease-free equilibrium. In addition, vaccination behavior can lead to eradication by private incentives alone - an outcome not seen for human diseases. In a scenario of high trade-based transmission, depopulation behavior has perverse epidemiological effects as it accelerates the spread of disease via poultry trade. In this situation, state interventions should focus on making vaccination technologies available at a low price rather than penalizing infected farms.

The RISKSUR EVA tool (Survtool): A tool for the integrated evaluation of animal health surveillance systems.

Information about infectious diseases at the global level relies on effective, efficient and sustainable national and international surveillance systems. Surveillance systems need to be regularly evaluated to ensure their performance, the quality of the data and information provided, as well as to allocate resources efficiently. Currently available frameworks for evaluation of surveillance systems in animal or human health often treat technical, process and socio-economic aspects separately instead of integrating them. The surveillance evaluation (EVA) tool, a support tool for the evaluation of animal health surveillance systems, was developed to provide guidance for integrated evaluation of animal health surveillance including economic evaluation. The tool was developed by international experts in surveillance and evaluation in an iterative process of development, testing and revision taking into account existing frameworks and guidance, scientific literature and expert opinion. The EVA tool encompasses a web interface for users to develop an evaluation plan, a Wiki classroom to provide theoretical information on all required concepts and a generic evaluation work plan to facilitate implementation and reporting of outputs to decision makers. The tool was tested by planning and conducting epidemiological and economic evaluations of surveillance for classical and African swine fever, bovine virus diarrhoea, avian influenza, and Salmonella Dublin in five European countries. These practical applications highlighted the importance of a comprehensive evaluation approach to improve the quality of the evaluation outputs (economic evaluation; multiple attributes assessment) and demonstrated the usefulness of the guidance provided by the EVA tool. At the same time they showed that comprehensive evaluations might be constrained by practical issues (e.g. confidentiality concerns, data availability) and resource scarcity. In the long term, the EVA tool is expected to increase professional evaluation capacity and help optimising animal health surveillance system efficiency and resource allocation for both public and private actors of the surveillance systems.

Poultry population dynamics and mortality risks in smallholder farms of the Mekong river delta region.

BACKGROUND: Poultry farming is widely practiced by rural households in Vietnam and the vast majority of domestic birds are kept on small household farms. However, smallholder poultry production is constrained by several issues such as infectious diseases, including avian influenza viruses whose circulation remains a threat to public health. This observational study describes the demographic structure and dynamics of small-scale poultry farms of the Mekong river delta region. METHOD: Fifty three farms were monitored over a 20-month period, with farm sizes, species, age, arrival/departure of poultry, and farm management practices recorded monthly. RESULTS: Median flock population sizes were 16 for chickens (IQR: 10-40), 32 for ducks (IQR: 18-101) and 11 for Muscovy ducks (IQR: 7-18); farm size distributions for the three species were heavily right-skewed. Muscovy ducks were kept for long periods and outdoors, while chickens and ducks were farmed indoors or in pens. Ducks had a markedly higher removal rate (broilers: 0.14/week; layer/breeders: 0.05/week) than chickens and Muscovy ducks (broilers: 0.07/week; layer/breeders: 0.01-0.02/week) and a higher degree of specialization resulting in a substantially shorter life span. The rate of mortality due to disease did not differ much among species, with birds being less likely to die from disease at older ages, but frequency of disease symptoms differed by species. Time series of disease-associated mortality were correlated with population size for Muscovy ducks (Kendall's coefficient τ = 0.49, p-value < 0.01) and with frequency of outdoor grazing for ducks (τ = 0.33, p-value = 0.05). CONCLUSION: The study highlights some challenges to disease control in small-scale multispecies poultry farms. The rate of interspecific contact and overlap between flocks of different ages is high, making small-scale farms a suitable environment for pathogens circulation. Muscovy ducks are farmed outdoors with little investment in biosecurity and few inter-farm movements. Ducks and chickens are more at-risk of introduction of pathogens through movements of birds from one farm to another. Ducks are farmed in large flocks with high turnover and, as a result, are more vulnerable to disease spread and require a higher vaccination coverage to maintain herd immunity.

Benefit-Cost Analysis of Foot-and-Mouth Disease Vaccination at the Farm-Level in South Vietnam.

This study aimed to analyze the financial impact of foot-and-mouth disease (FMD) outbreaks in cattle at the farm-level and the benefit-cost ratio (BCR) of biannual vaccination strategy to prevent and eradicate FMD for cattle in South Vietnam. Production data were collected from 49 small-scale dairy farms, 15 large-scale dairy farms, and 249 beef farms of Long An and Tay Ninh province using a questionaire. Financial data of FMD impacts were collected using participatory tools in 37 villages of Long An province. The net present value, i.e., the difference between the benefits (additional revenue and saved costs) and costs (additional costs and revenue foregone), of FMD vaccination in large-scale dairy farms was 2.8 times higher than in small-scale dairy farms and 20 times higher than in beef farms. The BCR of FMD vaccination over 1 year in large-scale dairy farms, small-scale dairy farms, and beef farms were 11.6 [95% confidence interval (95% CI) 6.42-16.45], 9.93 (95% CI 3.45-16.47), and 3.02 (95% CI 0.76-7.19), respectively. The sensitivity analysis showed that varying the vaccination cost had more effect on the BCR of cattle vaccination than varying the market price. This benefit-cost analysis of biannual vaccination strategy showed that investment in FMD prevention can be financially profitable, and therefore sustainable, for dairy farmers. For beef cattle, it is less certain that vaccination is profitable. Additional benefit-cost analysis study of vaccination strategies at the national-level would be required to evaluate and adapt the national strategy to achieve eradication of this disease in Vietnam.

Linking disease epidemiology and livestock productivity: The case of bovine respiratory disease in France.

Concerns are growing over the impact of livestock farming on environment and public health. The livestock industry is faced with the double constraint of limiting its use of natural resources and antimicrobials while ensuring its economic sustainability. In this context, reliable methods are needed to evaluate the effect of the prevention of endemic animal diseases on the productivity of livestock production systems. In this study, an epidemiological and productivity model was used to link changes in Bovine Respiratory Disease (BRD) incidence with the productivity of the beef and dairy cattle sectors in France. Cattle production parameters significantly affected by BRD were selected through literature review. Previous field study results and national cattle performance estimates were used to infer growth performances, mortality rates and carcass quality in the cattle affected and not affected by BRD. A steady-state deterministic herd production model was used to predict the productivity of the dairy and beef sector and their defined compartments (breeding-fattening, feedlot young bulls, and feedlot veal) in case of BRD incidence reduction by 20%, 50% or 100%. Results suggested that BRD should be controlled at a priority in beef breeding farms as eradication of BRD in beef calves would increase the whole beef sector's productivity by 4.7-5.5% while eradication in other production stages would result in lower productivity gain in their respective sectors. However, the analysis performed at compartment level showed that, in both the beef and dairy sector, young bull and veal feedlot enterprises derive more economic benefits from BRD eradication for their own compartment (increase in productivity of 8.7-12.8% for beef young bulls) than the breeding farms (increase in productivity of 5.1-6% for beef calves), which may limit the investments in BRD control.

Economic factors influencing zoonotic disease dynamics: demand for poultry meat and seasonal transmission of avian influenza in Vietnam.

While climate is often presented as a key factor influencing the seasonality of diseases, the importance of anthropogenic factors is less commonly evaluated. Using a combination of methods - wavelet analysis, economic analysis, statistical and disease transmission modelling - we aimed to explore the influence of climatic and economic factors on the seasonality of H5N1 Highly Pathogenic Avian Influenza in the domestic poultry population of Vietnam. We found that while climatic variables are associated with seasonal variation in the incidence of avian influenza outbreaks in the North of the country, this is not the case in the Centre and the South. In contrast, temporal patterns of H5N1 incidence are similar across these 3 regions: periods of high H5N1 incidence coincide with Lunar New Year festival, occurring in January-February, in the 3 climatic regions for 5 out of the 8 study years. Yet, daily poultry meat consumption drastically increases during Lunar New Year festival throughout the country. To meet this rise in demand, poultry production and trade are expected to peak around the festival period, promoting viral spread, which we demonstrated using a stochastic disease transmission model. This study illustrates the way in which economic factors may influence the dynamics of livestock pathogens.