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1.  Transmission routes of African swine fever virus to domestic pigs: current knowledge and future research directions 
The Veterinary Record  2016;178(11):262-267.
African swine fever (ASF) is a major threat to the pig industry in Europe. Since 2007, ASF outbreaks have been ongoing in the Caucasus, Eastern Europe and the Baltic countries, causing severe economic losses for many pig farmers and pork producers. In addition, the number of ASF cases in wild boar populations has dramatically increased over the past few years. Evidence supports direct contact with infectious domestic pigs and wild boars, and consumption of contaminated feed, as the main transmission routes of ASF virus (ASFV) to domestic pigs. However, significant knowledge gaps highlight the urgent need for research to investigate the dynamics of indirect transmission via the environment, the minimal infective doses for contaminated feed ingestion, the probability of effective contacts between infectious wild boars and domestic pigs, the potential for recovered animals to become carriers and a reservoir for transmission, the potential virus persistence within wild boar populations and the influence of human behaviour for the spread of ASFV. This will provide an improved scientific basis to optimise current interventions and develop new tools and strategies to reduce the risk of ASFV transmission to domestic pigs.
PMCID: PMC4819659  PMID: 26966305
2.  Who Is Spreading Avian Influenza in the Moving Duck Flock Farming Network of Indonesia? 
PLoS ONE  2016;11(3):e0152123.
Duck populations are considered to be a reservoir of Highly pathogenic avian influenza (HPAI) virus H5N1 in some agricultural production systems, as they are able to shed the virus for several days without clinical signs. Countries endemically affected with HPAI in Asia are characterised by production systems where ducks are fed on post-harvest spilled rice. During this scavenging process it is common for ducks to come into contact with other duck flocks or wild birds, thereby providing opportunities for virus spread. Effective risk management for HPAI has been significantly compromised by a limited understanding of management of moving duck flocks in these countries, despite of a small number of recent investigations. Here, for the first time, we described the management of moving duck flocks and the structure of the moving duck flock network in quantitative terms so that factors influencing the risk of HPAIV transmission can be identified. By following moving duck flock farmers over a period of 6 months in Java, Indonesia, we were able to describe the movement of flocks and to characterise the network of various types of actors associated with the production system. We used these data to estimate the basic reproductive number for HPAI virus spread. Our results suggest that focussing HPAI prevention measures on duck flocks alone will not be sufficient. Instead, the role of transporters of moving duck flocks, hatcheries and rice paddy owners, in the spread of the HPAI virus needs to be recognised.
PMCID: PMC4809517  PMID: 27019344
3.  A Spatial Analysis of Rift Valley Fever Virus Seropositivity in Domestic Ruminants in Tanzania 
PLoS ONE  2015;10(7):e0131873.
Rift Valley fever (RVF) is an acute arthropod-borne viral zoonotic disease primarily occurring in Africa. Since RVF-like disease was reported in Tanzania in 1930, outbreaks of the disease have been reported mainly from the eastern ecosystem of the Great Rift Valley. This cross-sectional study was carried out to describe the variation in RVF virus (RVFV) seropositivity in domestic ruminants between selected villages in the eastern and western Rift Valley ecosystems in Tanzania, and identify potential risk factors. Three study villages were purposively selected from each of the two Rift Valley ecosystems. Serum samples from randomly selected domestic ruminants (n = 1,435) were tested for the presence of specific immunoglobulin G (IgG) and M (IgM), using RVF enzyme-linked immunosorbent assay methods. Mixed effects logistic regression modelling was used to investigate the association between potential risk factors and RVFV seropositivity. The overall RVFV seroprevalence (n = 1,435) in domestic ruminants was 25.8% and speciesspecific seroprevalence was 29.7%, 27.7% and 22.0% in sheep (n = 148), cattle (n = 756) and goats (n = 531), respectively. The odds of seropositivity were significantly higher in animals sampled from the villages in the eastern than those in the western Rift Valley ecosystem (OR = 1.88, CI: 1.41, 2.51; p<0.001), in animals sampled from villages with soils of good than those with soils of poor water holding capacity (OR = 1.97; 95% CI: 1.58, 3.02; p< 0.001), and in animals which had been introduced than in animals born within the herd (OR = 5.08, CI: 2.74, 9.44; p< 0.001). Compared with animals aged 1–2 years, those aged 3 and 4–5 years had 3.40 (CI: 2.49, 4.64; p< 0.001) and 3.31 (CI: 2.27, 4.82, p< 0.001) times the odds of seropositivity. The findings confirm exposure to RVFV in all the study villages, but with a higher prevalence in the study villages from the eastern Rift Valley ecosystem.
PMCID: PMC4498811  PMID: 26162089
4.  Risk factors associated with Rift Valley fever epidemics in South Africa in 2008–11 
Scientific Reports  2015;5:9492.
Rift Valley fever (RVF) is a zoonotic and vector-borne disease, mainly present in Africa, which represents a threat to human health, animal health and production. South Africa has experienced three major RVF epidemics (1950–51, 1973–75 and 2008–11). Due to data scarcity, no previous study has quantified risk factors associated with RVF epidemics in animals in South Africa. Using the 2008–11 epidemic datasets, a retrospective longitudinal study was conducted to identify and quantify spatial and temporal environmental factors associated with RVF incidence. Cox regressions with a Besag model to account for the spatial effects were fitted to the data. Coefficients were estimated by Bayesian inference using integrated nested Laplace approximation. An increase in vegetation density was the most important risk factor until 2010. In 2010, increased temperature was the major risk factor. In 2011, after the large 2010 epidemic wave, these associations were reversed, potentially confounded by immunity in animals, probably resulting from earlier infection and vaccination. Both vegetation density and temperature should be considered together in the development of risk management strategies. However, the crucial need for improved access to data on population at risk, animal movements and vaccine use is highlighted to improve model predictions.
PMCID: PMC4372659  PMID: 25804974
5.  Dynamics of African swine fever virus shedding and excretion in domestic pigs infected by intramuscular inoculation and contact transmission 
Veterinary Research  2014;45(1):93.
African swine fever virus (ASFV) is a highly virulent swine pathogen that has spread across Eastern Europe since 2007 and for which there is no effective vaccine or treatment available. The dynamics of shedding and excretion is not well known for this currently circulating ASFV strain. Therefore, susceptible pigs were exposed to pigs intramuscularly infected with the Georgia 2007/1 ASFV strain to measure those dynamics through within- and between-pen transmission scenarios. Blood, oral, nasal and rectal fluid samples were tested for the presence of ASFV by virus titration (VT) and quantitative real-time polymerase chain reaction (qPCR). Serum was tested for the presence of ASFV-specific antibodies. Both intramuscular inoculation and contact transmission resulted in development of acute disease in all pigs although the experiments indicated that the pathogenesis of the disease might be different, depending on the route of infection. Infectious ASFV was first isolated in blood among the inoculated pigs by day 3, and then chronologically among the direct and indirect contact pigs, by day 10 and 13, respectively. Close to the onset of clinical signs, higher ASFV titres were found in blood compared with nasal and rectal fluid samples among all pigs. No infectious ASFV was isolated in oral fluid samples although ASFV genome copies were detected. Only one animal developed antibodies starting after 12 days post-inoculation. The results provide quantitative data on shedding and excretion of the Georgia 2007/1 ASFV strain among domestic pigs and suggest a limited potential of this isolate to cause persistent infection.
PMCID: PMC4189175  PMID: 25256695
6.  Modular framework to assess the risk of African swine fever virus entry into the European Union 
BMC Veterinary Research  2014;10:145.
The recent occurrence and spread of African swine fever (ASF) in Eastern Europe is perceived as a serious risk for the pig industry in the European Union (EU). In order to estimate the potential risk of ASF virus (ASFV) entering the EU, several pathways of introduction were previously assessed separately. The present work aimed to integrate five of these assessments (legal imports of pigs, legal imports of products, illegal imports of products, fomites associated with transport and wild boar movements) into a modular tool that facilitates the visualization and comprehension of the relative risk of ASFV introduction into the EU by each analyzed pathway.
The framework’s results indicate that 48% of EU countries are at relatively high risk (risk score 4 or 5 out of 5) for ASFV entry for at least one analyzed pathway. Four of these countries obtained the maximum risk score for one pathway: Bulgaria for legally imported products during the high risk period (HRP); Finland for wild boar; Slovenia and Sweden for legally imported pigs during the HRP. Distribution of risk considerably differed from one pathway to another; for some pathways, the risk was concentrated in a few countries (e.g., transport fomites), whereas other pathways incurred a high risk for 4 or 5 countries (legal pigs, illegal imports and wild boar).
The modular framework, developed to estimate the risk of ASFV entry into the EU, is available in a public domain, and is a transparent, easy-to-interpret tool that can be updated and adapted if required. The model’s results determine the EU countries at higher risk for each ASFV introduction route, and provide a useful basis to develop a global coordinated program to improve ASFV prevention in the EU.
PMCID: PMC4112856  PMID: 24992824
African swine fever; Emerging disease; Introduction; European Union; Pigs; Risk assessment; Semi-quantitative framework; Transboundary disease
7.  Spatial and Temporal Pattern of Rift Valley Fever Outbreaks in Tanzania; 1930 to 2007 
PLoS ONE  2014;9(2):e88897.
Rift Valley fever (RVF)-like disease was first reported in Tanzania more than eight decades ago and the last large outbreak of the disease occurred in 2006–07. This study investigates the spatial and temporal pattern of RVF outbreaks in Tanzania over the past 80 years in order to guide prevention and control strategies.
Materials and Methods
A retrospective study was carried out based on disease reporting data from Tanzania at district or village level. The data were sourced from the Ministries responsible for livestock and human health, Tanzania Meteorological Agency and research institutions involved in RVF surveillance and diagnosis. The spatial distribution of outbreaks was mapped using ArcGIS 10. The space-time permutation model was applied to identify clusters of cases, and a multivariable logistic regression model was used to identify risk factors associated with the occurrence of outbreaks in the district.
Principal Findings
RVF outbreaks were reported between December and June in 1930, 1947, 1957, 1960, 1963, 1968, 1977–79, 1989, 1997–98 and 2006–07 in 39.2% of the districts in Tanzania. There was statistically significant spatio-temporal clustering of outbreaks. RVF occurrence was associated with the eastern Rift Valley ecosystem (OR = 6.14, CI: 1.96, 19.28), total amount of rainfall of >405.4 mm (OR = 12.36, CI: 3.06, 49.88), soil texture (clay [OR = 8.76, CI: 2.52, 30.50], and loam [OR = 8.79, CI: 2.04, 37.82]).
RVF outbreaks were found to be distributed heterogeneously and transmission dynamics appeared to vary between areas. The sequence of outbreak waves, continuously cover more parts of the country. Whenever infection has been introduced into an area, it is likely to be involved in future outbreaks. The cases were more likely to be reported from the eastern Rift Valley than from the western Rift Valley ecosystem and from areas with clay and loam rather than sandy soil texture.
PMCID: PMC3934866  PMID: 24586433
8.  Spatial multi-criteria decision analysis to predict suitability for African swine fever endemicity in Africa 
African swine fever (ASF) is endemic in several countries of Africa and may pose a risk to all pig producing areas on the continent. Official ASF reporting is often rare and there remains limited awareness of the continent-wide distribution of the disease.
In the absence of accurate ASF outbreak data and few quantitative studies on the epidemiology of the disease in Africa, we used spatial multi-criteria decision analysis (MCDA) to derive predictions of the continental distribution of suitability for ASF persistence in domestic pig populations as part of sylvatic or domestic transmission cycles. In order to incorporate the uncertainty in the relative importance of different criteria in defining suitability, we modelled decisions within the MCDA framework using a stochastic approach. The predictive performance of suitability estimates was assessed via a partial ROC analysis using ASF outbreak data reported to the OIE since 2005.
Outputs from the spatial MCDA indicate that large areas of sub-Saharan Africa may be suitable for ASF persistence as part of either domestic or sylvatic transmission cycles. Areas with high suitability for pig to pig transmission (‘domestic cycles’) were estimated to occur throughout sub-Saharan Africa, whilst areas with high suitability for introduction from wildlife reservoirs (‘sylvatic cycles’) were found predominantly in East, Central and Southern Africa. Based on average AUC ratios from the partial ROC analysis, the predictive ability of suitability estimates for domestic cycles alone was considerably higher than suitability estimates for sylvatic cycles alone, or domestic and sylvatic cycles in combination.
This study provides the first standardised estimates of the distribution of suitability for ASF transmission associated with domestic and sylvatic cycles in Africa. We provide further evidence for the utility of knowledge-driven risk mapping in animal health, particularly in data-sparse environments.
PMCID: PMC3918235  PMID: 24406022
African swine fever; Knowledge-driven risk mapping; Multi-criteria decision analysis
9.  Calf-Level Factors Associated with Bovine Neonatal Pancytopenia – A Multi-Country Case-Control Study 
PLoS ONE  2013;8(12):e80619.
Bovine neonatal pancytopenia (BNP), a high fatality condition causing haemorrhages in calves aged less than 4 weeks, was first reported in 2007 in Germany and subsequently observed at low incidence in other European countries and New Zealand. A multi-country matched case-control study was conducted in 2011 to identify calf-level risk factors for BNP. 405 BNP cases were recruited from 330 farms in Belgium, France, Germany and the Netherlands by laboratory confirmation of farmer-reported cases. Up to four calves of similar age from the same farm were selected as controls (1154 calves). Risk factor data were collected by questionnaire. Multivariable modelling using conditional logistic regression indicated that PregSure®BVD (PregSure, Pfizer Animal Health) vaccination of the dam was strongly associated with BNP cases (adjusted matched Odds Ratio - amOR 17.8 first lactation dams; 95% confidence interval – ci 2.4, 134.4; p = 0.005), and second or more lactation PregSure-vaccinated dams were more likely to have a case than first lactation vaccinated dams (amOR 2.2 second lactation; ci 1.1, 4.3; p = 0.024; amOR 5.3 third or more lactation; ci 2.9, 9.8; p = <0.001). Feeding colostrum from other cows was strongly associated with BNP if the dam was not PregSure-vaccinated (amOR 30.5; ci 2.1, 440.5; p = 0.012), but the effect was less if the dam was PregSure-vaccinated (amOR 2.1; ci 1.1, 4.0; p = 0.024). Feeding exclusively dam’s milk was a higher risk than other types of milk (amOR 3.4; ci 1.6, 7.5; p = 0.002). The population attributable fractions were 0.84 (ci 0.68, 0.92) for PregSure vaccination, 0.13 (ci 0.06, 0.19) for feeding other cows’ colostrum, and 0.15 (ci 0.08, 0.22) for feeding dam’s milk. No other calf-level factors were identified, suggesting that there are other important factors that are outside the scope of this study, such as genetics, which explain why BNP develops in some PregSure-colostrum-exposed calves but not in others.
PMCID: PMC3846664  PMID: 24312485
10.  Risk factor modelling of the spatio-temporal patterns of highly pathogenic avian influenza (HPAIV) H5N1: a review 
Highly pathogenic avian influenza virus (HPAIV) H5N1 continues to impact on smallholder livelihoods, to constrain development of the poultry production sector, and to cause occasional human fatalities. HPAI H5N1 outbreaks have occurred in a variety of ecological systems with economic, agricultural and environmental differences. This review aimed to identify common risk factors amongst spatial modelling studies conducted in these different agro-ecological systems, and to identify gaps in our understanding of the disease’s spatial epidemiology. Three types of variables with similar statistical association with HPAI H5N1 presence across studies and regions were identified: domestic waterfowl, several anthropogenic variables (human population density, distance to roads) and indicators of water presence. Variables on socio-economic conditions, poultry trade, wild bird distribution and movements were comparatively rarely considered. Few studies have analysed the HPAI H5N1 distribution in countries such as Egypt and Indonesia, where HPAIV H5N1 continues to circulate extensively.
PMCID: PMC3389348  PMID: 22749203
Spatial epidemiology; avian influenza; H5N1
11.  Understanding and Managing Zoonotic Risk in the New Livestock Industries 
Environmental Health Perspectives  2013;121(8):873-877.
Background: In many parts of the world, livestock production is undergoing a process of rapid intensification. The health implications of this development are uncertain. Intensification creates cheaper products, allowing more people to access animal-based foods. However, some practices associated with intensification may contribute to zoonotic disease emergence and spread: for example, the sustained use of antibiotics, concentration of animals in confined units, and long distances and frequent movement of livestock.
Objectives: Here we present the diverse range of ecological, biological, and socioeconomic factors likely to enhance or reduce zoonotic risk, and identify ways in which a comprehensive risk analysis may be conducted by using an interdisciplinary approach. We also offer a conceptual framework to guide systematic research on this problem.
Discussion: We recommend that interdisciplinary work on zoonotic risk should take into account the complexity of risk environments, rather than limiting studies to simple linear causal relations between risk drivers and disease emergence and/or spread. In addition, interdisciplinary integration is needed at different levels of analysis, from the study of risk environments to the identification of policy options for risk management.
Conclusion: Given rapid changes in livestock production systems and their potential health implications at the local and global level, the problem we analyze here is of great importance for environmental health and development. Although we offer a systematic interdisciplinary approach to understand and address these implications, we recognize that further research is needed to clarify methodological and practical questions arising from the integration of the natural and social sciences.
PMCID: PMC3734490  PMID: 23665854
emerging diseases; integrated ecology and human health; livestock production; risk characterization; risk management; zoonoses
12.  Transmission Potential of Rift Valley Fever Virus over the Course of the 2010 Epidemic in South Africa 
Emerging Infectious Diseases  2013;19(6):916-924.
A Rift Valley fever (RVF) epidemic affecting animals on domestic livestock farms was reported in South Africa during January–August 2010. The first cases occurred after heavy rainfall, and the virus subsequently spread countrywide. To determine the possible effect of environmental conditions and vaccination on RVF virus transmissibility, we estimated the effective reproduction number (Re) for the virus over the course of the epidemic by extending the Wallinga and Teunis algorithm with spatial information. Re reached its highest value in mid-February and fell below unity around mid-March, when vaccination coverage was 7.5%–45.7% and vector-suitable environmental conditions were maintained. The epidemic fade-out likely resulted first from the immunization of animals following natural infection or vaccination. The decline in vector-suitable environmental conditions from April onwards and further vaccination helped maintain Re below unity. Increased availability of vaccine use data would enable evaluation of the effect of RVF vaccination campaigns.
PMCID: PMC3713830  PMID: 23735606
Rift Valley fever; South Africa; epidemic; likelihood functions; viruses; Rift Valley fever virus; zoonoses; transmission
13.  The incidence of feline injection site sarcomas in the United Kingdom 
Feline injection site sarcomas (FISS) are aggressive neoplasms that have been associated with vaccination. In North America the incidence estimates have varied from 1 case of FISS per 1,000-10,000 cats vaccinated. The aim of this study was to estimate the incidence of FISS in the United Kingdom (UK) in 2007. The ratio of FISS to vaccines sold in the UK was also estimated.
Fourteen FISS were diagnosed by a convenience sample of 34 small animal veterinary practices in the United Kingdom in 2007 and were used as the numerator for the incidence estimates. Denominator data was obtained from the computer systems of each practice. Considering that a single cause relationship with vaccination is not proven, three different denominators (number of cats registered, the number of cat consultations undertaken and the number of vaccination visits for cats at the practices) were used to express the potential variation in risk.
The incidence risk of FISS per year was estimated to be 1/16,000 -50,000 cats registered by practices, 1/10,000-20,000 cat consultations and 1/5,000-12,500 vaccination visits.
When interpreting these findings, it needs to be taken into consideration that this sample of practices and their cats may not be representative of veterinary practices and cats at risk of FISS in the UK. However it can still be concluded with reasonable certainty that the incidence of FISS in the UK is very low.
PMCID: PMC3608079  PMID: 23339769
Feline injection site sarcomas; Incidence; Risk
14.  Rinderpest Virus Sequestration and Use in Posteradication Era 
Emerging Infectious Diseases  2013;19(1):151-153.
After the 2011 declaration of rinderpest disease eradication, we surveyed 150 countries about rinderpest virus stocks. Forty-four laboratories in 35 countries held laboratory-attenuated strains, field strains, or diagnostic samples. Vaccine and reagent production and laboratory experiments continued. Rigorous standards are necessary to ensure that stocks are kept under safe conditions.
PMCID: PMC3557999  PMID: 23260811
Rinderpest; eradication; virus sequestration; viruses; ruminants; vaccine
15.  Live Poultry Trade in Southern China Provinces and HPAIV H5N1 Infection in Humans and Poultry: The Role of Chinese New Year Festivities 
PLoS ONE  2012;7(11):e49712.
The number of outbreaks of highly pathogenic avian influenza virus of the H5N1 subtype (HPAIV H5N1) over the past 5 years has been drastically reduced in China but sporadic infections in poultry and humans are still occurring. In this study, we aimed to investigate seasonal patterns in the association between the movement of live poultry originating from southern China and HPAIV H5N1 infection history in humans and poultry in China.
Methodology/Principal Findings
During January to April 2010, longitudinal questionnaire surveys were carried out monthly in four wholesale live bird markets (LBMs) in Hunan and Guangxi provinces of South China. Using social network analysis, we found an increase in the number of observed links and degree centrality between LBMs and poultry sources in February and March compared to the months of January and April. The association of some live poultry traders (LPT’s) with a limited set of counties (within the catchment area of LBMs) in the months of February and March may support HPAIV H5N1 transmission and contribute to perpetuating HPAIV H5N1 virus circulation among certain groups of counties. The connectivity among counties experiencing human infection was significantly higher compared to counties without human infection for the months of January, March and April. Conversely, counties with poultry infections were found to be significantly less connected than counties without poultry infection for the month of February.
Our results show that temporal variation in live poultry trade in Southern China around the Chinese New Year festivities is associated with higher HPAIV H5N1 infection risk in humans and poultry. This study has shown that capturing the dynamic nature of poultry trade networks in Southern China improves our ability to explain the spatiotemporal dissemination in avian influenza viruses in China.
PMCID: PMC3500328  PMID: 23166751
16.  Exploratory Space-Time Analyses of Rift Valley Fever in South Africa in 2008–2011 
Rift Valley fever (RVF) is a zoonotic arbovirosis for which the primary hosts are domestic livestock (cattle, sheep and goats). RVF was first described in South Africa in 1950–1951. Mechanisms for short and long distance transmission have been hypothesised, but there is little supporting evidence. Here we describe RVF occurrence and spatial distribution in South Africa in 2008–11, and investigate the presence of a contagious process in order to generate hypotheses on the different mechanisms of transmission.
Methodology/Principal Findings
A total of 658 cases were extracted from World Animal Health Information Database. Descriptive statistics, epidemic curves and maps were produced. The space-time K-function was used to test for evidence of space-time interaction. Five RVF outbreak waves (one in 2008, two in 2009, one in 2010 and one in 2011) of varying duration, location and size were reported. About 70% of cases (n = 471) occurred in 2010, when the epidemic was almost country-wide. No strong evidence of space-time interaction was found for 2008 or the second wave in 2009. In the first wave of 2009, a significant space-time interaction was detected for up to one month and over 40 km. In 2010 and 2011 a significant intense, short and localised space-time interaction (up to 3 days and 15 km) was detected, followed by one of lower intensity (up to 2 weeks and 35 to 90 km).
The description of the spatiotemporal patterns of RVF in South Africa between 2008 and 2011 supports the hypothesis that during an epidemic, disease spread may be supported by factors other than active vector dispersal. Limitations of under-reporting and space-time K-function properties are discussed. Further spatial analyses and data are required to explain factors and mechanisms driving RVF spread.
Author Summary
The factors explaining Rift Valley fever (RVF) spread in domestic livestock during an epidemic are attributed to short and long distance mechanisms, including active vector dispersal, passive vector dispersal and movements of infectious animals. However, because of data scarcity, quantifying and disentangling these mechanisms remains challenging. Here, we generate hypotheses on the possible mechanisms involved in RVF spread in South Africa between 2008 and 2011. We use descriptive statistics and estimate the space-time K-function to explore the presence of space-time interactions, being interpreted as an indicator of an underlying transmission process. Our results confirm the presence of an intense, short, initial transmission process that could be attributed to active vector dispersal; but also highlight the presence of another transmission mechanism of a lower intensity and over further distances that could be explained by the movements of infectious animals, passive vector dispersal or emergence of other foci. Further data collection and modelling tools are required to confirm these hypotheses.
PMCID: PMC3429380  PMID: 22953020
17.  Identifying Live Bird Markets with the Potential to Act as Reservoirs of Avian Influenza A (H5N1) Virus: A Survey in Northern Viet Nam and Cambodia 
PLoS ONE  2012;7(6):e37986.
Wet markets are common in many parts of the world and may promote the emergence, spread and maintenance of livestock pathogens, including zoonoses. A survey was conducted in order to assess the potential of Vietnamese and Cambodian live bird markets (LBMs) to sustain circulation of highly pathogenic avian influenza virus subtype H5N1 (HPAIV H5N1). Thirty Vietnamese and 8 Cambodian LBMs were visited, and structured interviews were conducted with the market managers and 561 Vietnamese and 84 Cambodian traders. Multivariate and cluster analysis were used to construct a typology of traders based on their poultry management practices. As a result of those practices and large poultry surplus (unsold poultry reoffered for sale the following day), some poultry traders were shown to promote conditions favorable for perpetuating HPAIV H5N1 in LBMs. More than 80% of these traders operated in LBMs located in the most densely populated areas, Ha Noi and Phnom Penh. The profiles of sellers operating at a given LBM could be reliably predicted using basic information about the location and type of market. Consequently, LBMs with the largest combination of risk factors for becoming virus reservoirs could be easily identified, potentially allowing control strategies to be appropriately targeted. These findings are of particular relevance to resource-scarce settings with extensively developed LBM systems, commonly found in South-East Asia.
PMCID: PMC3366999  PMID: 22675502
18.  BPEX Pig Health Scheme: a useful monitoring system for respiratory disease control in pig farms? 
Respiratory diseases account for significant economic losses to the UK pig industry. Lesions indicative of respiratory disease in pig lungs at slaughter e.g. pneumonia and pleuritis are frequently recorded to assess herd health or provide data for epidemiological studies. The BPEX Pig Health Scheme (BPHS) is a monitoring system, which informs producers of gross lesions in their pigs' carcasses at slaughter, enabling farm-level decisions to be made. The aim of the study was to assess whether information provided by the BPHS regarding respiratory lesions was associated with respiratory pathogens in the farm, farm management practices and each other.
BPHS reports were obtained from a subset of 70 pig farms involved in a cross-sectional study conducted in 2008-09 investigating the epidemiology of post-weaning multi-systemic wasting syndrome. The reports were combined with data regarding the presence/absence of several pathogens in the herd and potential farm-level risk factors for respiratory disease. Principal component analysis (PCA) performed on BPHS reports generated three principal components, explaining 71% of the total variance. Enzootic pneumonia score, severe pleurisy and acute pleuropneumonia had the highest loadings for the principal component which explained the largest percentage of the total variance (35%) (BPHS component 1), it was thought that this component identifies farms with acute disease. Using the factor loadings a score for each farm for BPHS component 1 was obtained. As farms' score for BPHS component 1 increased, average carcass weight at slaughter decreased. In addition, farms positive for H1N2 and porcine reproductive and respiratory disease virus (PRRSV) were more likely to have higher levels of severe and mild pleurisy reported by the BPHS, respectively.
The study found statistical associations between levels of pleurisy recorded by BPHS at slaughter and the presence H1N2 and PRRSV in the herd. There is also some evidence that farms which submit pigs with these lesions may have reduced productivity. However, more research is needed to fully validate the scheme.
PMCID: PMC3285094  PMID: 22208847
19.  Spatial Distribution and Risk Factors of Highly Pathogenic Avian Influenza (HPAI) H5N1 in China 
PLoS Pathogens  2011;7(3):e1001308.
Highly pathogenic avian influenza (HPAI) H5N1 was first encountered in 1996 in Guangdong province (China) and started spreading throughout Asia and the western Palearctic in 2004–2006. Compared to several other countries where the HPAI H5N1 distribution has been studied in some detail, little is known about the environmental correlates of the HPAI H5N1 distribution in China. HPAI H5N1 clinical disease outbreaks, and HPAI virus (HPAIV) H5N1 isolated from active risk-based surveillance sampling of domestic poultry (referred to as HPAIV H5N1 surveillance positives in this manuscript) were modeled separately using seven risk variables: chicken, domestic waterfowl population density, proportion of land covered by rice or surface water, cropping intensity, elevation, and human population density. We used bootstrapped logistic regression and boosted regression trees (BRT) with cross-validation to identify the weight of each variable, to assess the predictive power of the models, and to map the distribution of HPAI H5N1 risk. HPAI H5N1 clinical disease outbreak occurrence in domestic poultry was mainly associated with chicken density, human population density, and elevation. In contrast, HPAIV H5N1 infection identified by risk-based surveillance was associated with domestic waterfowl density, human population density, and the proportion of land covered by surface water. Both models had a high explanatory power (mean AUC ranging from 0.864 to 0.967). The map of HPAIV H5N1 risk distribution based on active surveillance data emphasized areas south of the Yangtze River, while the distribution of reported outbreak risk extended further North, where the density of poultry and humans is higher. We quantified the statistical association between HPAI H5N1 outbreak, HPAIV distribution and post-vaccination levels of seropositivity (percentage of effective post-vaccination seroconversion in vaccinated birds) and found that provinces with either outbreaks or HPAIV H5N1 surveillance positives in 2007–2009 appeared to have had lower antibody response to vaccination. The distribution of HPAI H5N1 risk in China appears more limited geographically than previously assessed, offering prospects for better targeted surveillance and control interventions.
Author Summary
The geographical distribution of highly pathogenic avian influenza (HPAI) H5N1 and agro-ecological risk factors have been studied in a number of countries in Southeast Asia. However, little is know of its distribution in China where HPAI H5N1 first emerged in 1996, evolved, and spread throughout Asia and the western Palearctic in 2004–2006. This study analyzes separately the distribution, in domestic poultry, of HPAI virus (HPAIV) H5N1 isolated from active risk-based surveillance sampling and HPAI H5N1 clinical disease outbreaks. These data are analyzed in relation to the distribution of chicken and domestic waterfowl population density, proportion of land covered by rice or surface water, cropping intensity, elevation, and human population density. HPAI H5N1 viruses identified by risk-based surveillance are found to be associated with domestic waterfowl density, human population density, and the proportion of land covered by surface water. In contrast, HPAI H5N1 clinical disease outbreak occurrences were mainly associated with chicken density, human population density, and low elevation. These results show that the distribution of HPAI H5N1 risk in China appears more limited geographically than previously assessed, offering prospects for better targeted surveillance and control interventions.
PMCID: PMC3048366  PMID: 21408202
20.  Recent advances in the analysis of behavioural organization and interpretation as indicators of animal welfare 
While the incorporation of mathematical and engineering methods has greatly advanced in other areas of the life sciences, they have been under-utilized in the field of animal welfare. Exceptions are beginning to emerge and share a common motivation to quantify ‘hidden’ aspects in the structure of the behaviour of an individual, or group of animals. Such analyses have the potential to quantify behavioural markers of pain and stress and quantify abnormal behaviour objectively. This review seeks to explore the scope of such analytical methods as behavioural indicators of welfare. We outline four classes of analyses that can be used to quantify aspects of behavioural organization. The underlying principles, possible applications and limitations are described for: fractal analysis, temporal methods, social network analysis, and agent-based modelling and simulation. We hope to encourage further application of analyses of behavioural organization by highlighting potential applications in the assessment of animal welfare, and increasing awareness of the scope for the development of new mathematical methods in this area.
PMCID: PMC2817160  PMID: 19740922
fractal analysis; Theme; Markov chains; social networks; modelling; animal behaviour
21.  African swine fever: how can global spread be prevented? 
African swine fever (ASF) is a devastating haemorrhagic fever of pigs with mortality rates approaching 100 per cent. It causes major economic losses, threatens food security and limits pig production in affected countries. ASF is caused by a large DNA virus, African swine fever virus (ASFV). There is no vaccine against ASFV and this limits the options for disease control. ASF has been confined mainly to sub-Saharan Africa, where it is maintained in a sylvatic cycle and/or among domestic pigs. Wildlife hosts include wild suids and arthropod vectors. The relatively small numbers of incursions to other continents have proven to be very difficult to eradicate. Thus, ASF remained endemic in the Iberian peninsula until the mid-1990s following its introductions in 1957 and 1960 and the disease has remained endemic in Sardinia since its introduction in 1982. ASF has continued to spread within Africa to previously uninfected countries, including recently the Indian Ocean islands of Madagascar and Mauritius. Given the continued occurrence of ASF in sub-Saharan Africa and increasing global movements of people and products, it is not surprising that further transcontinental transmission has occurred. The introduction of ASF to Georgia in the Caucasus in 2007 and dissemination to neighbouring countries emphasizes the global threat posed by ASF and further increases the risks to other countries.
We review the mechanisms by which ASFV is maintained within wildlife and domestic pig populations and how it can be transmitted. We then consider the risks for global spread of ASFV and discuss possibilities of how disease can be prevented.
PMCID: PMC2865084  PMID: 19687038
African swine fever; molecular epidemiology; transmission; arthropod vectors; pigs
22.  Evaluating the control of HPAIV H5N1 in Vietnam: virus transmission within infected flocks reported before and after vaccination 
Currently, the highly pathogenic avian influenza virus (HPAIV) of the subtype H5N1 is believed to have reached an endemic cycle in Vietnam. We used routine surveillance data on HPAIV H5N1 poultry outbreaks in Vietnam to estimate and compare the within-flock reproductive number of infection (R0) for periods before (second epidemic wave, 2004-5; depopulation-based disease control) and during (fourth epidemic wave, beginning 2007; vaccination-based disease control) vaccination.
Our results show that infected premises (IPs) in the initial (exponential) phases of outbreak periods have the highest R0 estimates. The IPs reported during the outbreak period when depopulation-based disease control was implemented had higher R0 estimates than IPs reported during the outbreak period when vaccination-based disease control was used. In the latter period, in some flocks of a defined size and species composition, within-flock transmission estimates were not significantly below the threshold for transmission (R0 < 1).
Our results indicate that the current control policy based on depopulation plus vaccination has protected the majority of poultry flocks against infection. However, in some flocks the determinants associated with suboptimal protection need to be further investigated as these may explain the current pattern of infection in animal and human populations.
PMCID: PMC2898779  PMID: 20525380
23.  Risk factors and characteristics of H5N1 Highly Pathogenic Avian Influenza (HPAI) post-vaccination outbreaks 
Veterinary Research  2008;40(3):15.
Highly pathogenic avian influenza (HPAI) virus H5N1 is now endemic in South-East Asia but HPAI control methods differ between countries. A widespread HPAI vaccination campaign that started at the end of 2005 in Viet Nam resulted in the cessation of poultry and human cases, but in 2006/2007 severe HPAI outbreaks re-emerged. In this study we investigated the pattern of this first post-vaccination epidemic in southern Viet Nam identifying a spatio-temporal cluster of outbreak occurrence and estimating spatially smoothed incidence rates of HPAI. Spatial risk factors associated with HPAI occurrence were identified. Medium-level poultry density resulted in an increased outbreak risk (Odds ratio (OR) = 5.4, 95% confidence interval (CI): 1.6–18.9) but also climate-vegetation factors played an important role: medium-level normalised difference vegetation indices during the rainy season from May to October were associated with higher risk of HPAI outbreaks (OR = 3.7, 95% CI: 1.7–8.1), probably because temporal flooding might have provided suitable conditions for the re-emergence of HPAI by expanding the virus distribution in the environment and by enlarging areas of possible contacts between domestic waterfowl and wild birds. On the other hand, several agricultural production factors, such as sweet potatoes yield, increased buffalo density, as well as increased electricity supply were associated with decreased risk of HPAI outbreaks. This illustrates that preventive control measures for HPAI should include a promotion of low-risk agricultural management practices as well as improvement of the infrastructure in village households. Improved HPAI vaccination efforts and coverage should focus on medium poultry density areas and on the pre-monsoon time period.
PMCID: PMC2695038  PMID: 19081006
avian influenza; H5N1; poultry; risk factor; HPAI outbreak
24.  Risk mapping of Rinderpest sero-prevalence in Central and Southern Somalia based on spatial and network risk factors 
In contrast to most pastoral systems, the Somali livestock production system is oriented towards domestic trade and export with seasonal movement patterns of herds/flocks in search of water and pasture and towards export points. Data from a rinderpest survey and other data sources have been integrated to explore the topology of a contact network of cattle herds based on a spatial proximity criterion and other attributes related to cattle herd dynamics. The objective of the study is to integrate spatial mobility and other attributes with GIS and network approaches in order to develop a predictive spatial model of presence of rinderpest.
A spatial logistic regression model was fitted using data for 562 point locations. It includes three statistically significant continuous-scale variables that increase the risk of rinderpest: home range radius, herd density and clustering coefficient of the node of the network whose link was established if the sum of the home ranges of every pair of nodes was equal or greater than the shortest distance between the points. The sensitivity of the model is 85.1% and the specificity 84.6%, correctly classifying 84.7% of the observations. The spatial autocorrelation not accounted for by the model is negligible and visual assessment of a semivariogram of the residuals indicated that there was no undue amount of spatial autocorrelation. The predictive model was applied to a set of 6176 point locations covering the study area. Areas at high risk of having serological evidence of rinderpest are located mainly in the coastal districts of Lower and Middle Juba, the coastal area of Lower Shabele and in the regions of Middle Shabele and Bay. There are also isolated spots of high risk along the border with Kenya and the southern area of the border with Ethiopia.
The identification of point locations and areas with high risk of presence of rinderpest and their spatial visualization as a risk map will be useful for informing the prioritization of disease surveillance and control activities for rinderpest in Somalia. The methodology applied here, involving spatial and network parameters, could also be applied to other diseases and/or species as part of a standardized approach for the design of risk-based surveillance activities in nomadic pastoral settings.
PMCID: PMC2873515  PMID: 20426843
25.  Associations between attributes of live poultry trade and HPAI H5N1 outbreaks: a descriptive and network analysis study in northern Vietnam 
The structure of contact between individuals plays an important role in the incursion and spread of contagious diseases in both human and animal populations. In the case of avian influenza, the movement of live birds is a well known risk factor for the geographic dissemination of the virus among poultry flocks. Live bird markets (LBM's) contribute to the epidemiology of avian influenza due to their demographic characteristics and the presence of HPAI H5N1 virus lineages. The relationship between poultry producers and live poultry traders (LPT's) that operate in LBM's has not been adequately documented in HPAI H5N1-affected SE Asian countries. The aims of this study were to document and study the flow of live poultry in a poultry trade network in northern Vietnam, and explore its potential role in the risk for HPAI H5N1 during 2003 to 2006.
Our results indicate that LPT's trading for less than a year and operating at retail markets are more likely to source poultry from flocks located in communes with a past history of HPAI H5N1 outbreaks during 2003 to 2006 than LPT's trading longer than a year and operating at wholesale markets. The results of the network analysis indicate that LPT's tend to link communes of similar infection status.
Our study provides evidence which can be used for informing policies aimed at encouraging more biosecure practices of LPT's operating at authorised LBM's. The results suggest that LPT's play a role in HPAI H5N1 transmission and may contribute to perpetuating HPAI H5N1 virus circulation amongst certain groups of communes. The impact of current disease prevention and control interventions could be enhanced by disseminating information about outbreak risk and the implementation of a formal data recording scheme at LBM's for all incoming and outgoing LPT's.
PMCID: PMC2837645  PMID: 20175881

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