Anthropogenic factors and the risk of highly pathogenic avian influenza H5N1: prospects from a spatial-based model

Beginning in 2003, highly pathogenic avian influenza (HPAI) H5N1 virus spread across Southeast Asia, causing unprecedented epidemics. Thailand was massively infected in 2004 and 2005 and continues today to experience sporadic outbreaks. While research findings suggest that the spread of HPAI H5N1 is influenced primarily by trade patterns, identifying the anthropogenic risk factors involved remains a challenge. In this study, we investigated which anthropogenic factors played a role in the risk of HPAI in Thailand using outbreak data from the “second wave” of the epidemic (3 July 2004 to 5 May 2005) in the country. We first performed a spatial analysis of the relative risk of HPAI H5N1 at the subdistrict level based on a hierarchical Bayesian model. We observed a strong spatial heterogeneity of the relative risk. We then tested a set of potential risk factors in a multivariable linear model. The results confirmed the role of free-grazing ducks and rice-cropping intensity but showed a weak association with fighting cock density. The results also revealed a set of anthropogenic factors significantly linked with the risk of HPAI. High risk was associated strongly with densely populated areas, short distances to a highway junction, and short distances to large cities. These findings highlight a new explanatory pattern for the risk of HPAI and indicate that, in addition to agro-environmental factors, anthropogenic factors play an important role in the spread of H5N1. To limit the spread of future outbreaks, efforts to control the movement of poultry products must be sustained.     

The spread of highly pathogenic avian influenza (subtype H5N1) clades in Bangladesh, 2010 and 2011

Since the global spread of highly pathogenic avian influenza H5N1 during 2005–2006, control programs have been successfully implemented in most affected countries. HPAI H5N1 was first reported in Bangladesh in 2007, and since then 546 outbreaks have been reported to the OIE. The disease has apparently become endemic in Bangladesh. Spatio-temporal information on 177 outbreaks of HPAI H5N1 occurring between February 2010 and April 2011 in Bangladesh, and 37 of these outbreaks in which isolated H5N1 viruses were phylogenetically characterized to clade, were analyzed.     

Metapopulation dynamics and determinants of H5N1 highly pathogenic avian influenza outbreaks in Indonesian poultry

In 2008, the Indonesian Government implemented a revised village-level Participatory Disease Surveillance and Response (PDSR) program to gain a better understanding of both the magnitude and spatial distribution of H5N1 highly pathogenic avian influenza (HPAI) outbreaks in backyard poultry. To date, there has been considerable collection of data, but limited publically available analysis. This study utilizes data collected by the PDSR program between April 2008 and September 2010 for Java, Bali and the Lampung Province of Sumatra. The analysis employs hierarchical Bayesian occurrence models to quantify spatial and temporal dynamics in backyard HPAI infection reports at the District level in 90 day time periods, and relates the probability of HPAI occurrence to PDSR-reported village HPAI infection status and human and poultry density. The probability of infection in a District was assumed to be dependent on the status of the District in the previous 90 day time period, and described by either a colonization probability (the probability of HPAI infection in a District given there had not been infection in the previous 90 day time period) or a persistence probability (the probability of HPAI infection being maintained in the District from the previous to current 90 day period). Results suggest that the number of surveillance activities in a district had little relationship to outbreak occurrence probabilities, but human and poultry densities were found to have non-linear relationships to outbreak occurrence probabilities. We found significant spatial dependency among neighboring districts, indicating that there are latent spatial processes that are not captured by the covariates available for this study, but which nonetheless impact outbreak dynamics. The results of this work may help improve understanding of the seasonal nature of H5N1 in poultry and the potential role of poultry density in enabling endemicity to occur, as well as to assist the Government of Indonesia target scarce resources to regions and time periods when outbreaks of HPAI in poultry are most likely to occur.     

Risk factors and characteristics of H5N1 Highly Pathogenic Avian Influenza (HPAI) post-vaccination outbreaks

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.     

Use of personal protective measures by Thai households in areas with avian influenza outbreaks

Thailand has had multiple poultry outbreaks of highly pathogenic avian influenza (HPAI) H5N1 since its first emergence in 2004. Twenty-five human cases of HPAI H5N1 avian influenza have been reported in the country, including 17 fatalities, and contact with infected dead or dying poultry has been identified as a risk factor for human infection. This study assessed the use of protective equipment and hand hygiene measures by Thai poultry-owning households during activities involving poultry contact. Surveys conducted in 2008 included questions regarding poultry-related activities and protective measures used during an HPAI outbreak (2005) and 3 years after the study location's last reported outbreak (2008). For both time periods, poultry owners reported limited use of personal protective equipment (PPE) during all activities and inconsistent hand washing practices after carrying poultry and gathering eggs. This is the first time that PPE use in Thailand has been quantified for a large study group. These data are important for ongoing characterization of HPAI risk and for the crafting of educational messages.     

Highly pathogenic avian influenza H5N1 virus in cats and other carnivores

The Asian lineage highly pathogenic avian influenza (HPAI) H5N1 virus is a known pathogen of birds. Only recently, the virus has been reported to cause sporadic fatal disease in carnivores, and its zoonotic potential has been dominating the popular media. Attention to felids was drawn by two outbreaks with high mortality in tigers, leopards and other exotic felids in Thailand. Subsequently, domestic cats were found naturally infected and experimentally susceptible to H5N1 virus. A high susceptibility of the dog to H3N8 equine influenza A virus had been reported earlier, and recently also HPAI H5N1 virus has been identified as a canine pathogen. The ferret, hamster and mouse are suitable as experimental animals; importantly, these species are also kept as pets. Experimental intratracheal and oral infection of cats with an HPAI H5N1 virus isolate from a human case resulted in lethal disease; furthermore, cats have been infected by the feeding of infected chickens. Spread of the infection from experimentally infected to in-contact cats has been reported. The epidemiological role of the cat and other pet animal species in transmitting HPAI H5N1 virus to humans needs continuous consideration and attention.     

Association between outbreaks of highly pathogenic avian influenza subtype H5N1 and migratory waterfowl (family Anatidae) populations

Highly pathogenic avian influenza (HPAI) virus subtype H5N1 threatens poultry production and human health. Understanding the role that migratory waterfowl play in introducing and maintaining this infection is critical to control the outbreaks. A study was conducted to determine if the occurrence of HPAI subtype H5N1 outbreaks in village poultry in Romania, 2005-2006, was associated with proximity to populations of migratory waterfowl. Reported outbreaks--which could be grouped into three epidemic phases--and migratory waterfowl sites were mapped. The migratory waterfowl site closest to each outbreak was identified. The distances between outbreaks occurring in phase 1 and 2 of the epidemic and the closest migratory waterfowl site were significantly (P<0.001) less than in phase 3, but these distances were only useful in predicting when outbreaks occurred during phase 1 (October-December, 2005) of the epidemic. A spatial lag (rho=0.408, P=0.041) model best fit the data, using distance and [distance]*[distance] as predictors (R2=0.425). The correlation between when outbreaks were predicted to occur and when they were observed to occur was 0.55 (P=0.006). Results support the hypothesis that HPAI virus subtype H5N1 infections of village poultry in Romania during the autumn of 2005 might have occurred via exposure to migratory populations of waterfowl.     

Legislation for the control of avian influenza in the European union

In the light of experience gained with avian influenza (AI) outbreaks in Europe and elsewhere in the world, the European Union (EU) legislation has recently been updated. The strategy to control the introduction and spread of AI relies on rapid disease detection, killing of infected birds, movement restrictions for live birds and their products, cleaning and disinfection and vaccination. Measures are not only to be implemented in case of outbreaks of highly pathogenic AI (HPAI), but are now also directed against occurrence of low pathogenic AI of H5 and H7 (LPAI) subtypes in poultry, albeit in a modified manner proportionate to the risk posed by these pathotypes. Enhanced surveillance in poultry holdings and wild birds, as well as preventive vaccination, has also been introduced. EU Measures are flexible and largely based on risk assessment of the local epidemiological situation. The occurrence of HPAI H5N1 of the Asian lineage in the EU and its unprecedented spread by wild migratory birds necessitated the adoption of additional control measures. Although HPAI H5N1 has affected wild birds and poultry holdings in several EU Member States, EU legislation and its implementation in Member States has so far successfully limited the impact of the disease on animal and human health.     

Environmental and anthropogenic risk factors for highly pathogenic avian influenza subtype H5N1 outbreaks in Romania, 2005−2006

The association between highly pathogenic avian influenza (HPAI) subtype H5N1 outbreak risk in poultry in 161 Romanian villages (October 2005 to June 2006) and environmental and anthropogenic factors was investigated. Village outbreak risk was associated with a village being <5 km from a major road (odds ratio [OR] 5.27, 95% confidence interval [CI] 1.21–22.9) or a river/stream (OR 1.97, 95% CI 1.06–3.72). Outbreak risk in the first part of the epidemic was associated with a village being <5 km from a major road (OR 3.31, 95% CI 1.10–9.98) or a regularly flooded land area (OR 5.08, 95% CI 1.08–23.9); whereas outbreak risk in the second part of the epidemic was associated with a village being <5 km from a river/stream (OR 5.5, 95% CI 1.69–18.9). Results suggest that both environmental and anthropogenic factors influence the risk of HPAI subtype H5N1 outbreaks in village poultry populations.     

Geostatistical visualisation and spatial statistics for evaluation of the dispersion of epidemic highly pathogenic avian influenza subtype H5N1

The aim of this study was to evaluate a range of statistical and geostatistical methods for their usefulness in providing insights into how highly pathogenic avian influenza (HPAI) subtype H5N1 might spread through a national population of village poultry. The insights gained allow the generation of disease dispersion hypotheses. The case study data set consisted of 161 outbreaks of HPAI subtype H5N1 in village poultry reported in Romania between October 2005 and June 2006. Reports of village outbreaks (%) occurred in three waves: October-December (14%), February-March (16%), and May-June (68%). Risk mapping - based on variography and kriging - was used to visualize the evolution of the epidemic. Outbreaks first appeared in eastern and southern Romania, particularly within an area that forms part of the Danube River Delta. The largest phase of the epidemic affected villages in all parts of central, southern, and eastern Romania, but outbreaks were clustered in central Romania. Outbreaks spread in an east to west direction. By using geostatistical visualisation and spatial statistics, the evolution of the epidemic could be characterised into two parts: disease introduction, local spread, and sporadic outbreaks, and long-distance disease spread with rapid epidemic propagation. This is consistent with the hypothesis that the environment and landscape (specifically the Danube River Delta) played a critical role in the introduction and initial spread of HPAI subtype H5N1 during the autumn and winter of 2005, and that the movement of poultry might have introduced the infection into central Romania during the spring and summer of 2006. Further research focusing on the spatio-temporal interface between the two parts of the epidemic might reveal how and why it progressed from a confined, local epidemic to a large, national epidemic. Such information would assist efforts to limit the global spread of HPAI subtype H5N1.     

Spatial transmission of avian influenza (type H5) in birds

Highly pathogenic avian influenza (HPAI) H5N1 continues to threaten domestic and wild birds, as well as human health. However, the mechanism of spatial transmission of HPAI is still unclear. We analyzed the current distribution of HPAI occurrences based on World Organization for Animal Health reported data from 3049 sites in the world from December 2003 to June 2006, and found that these sites were spaced at distances with a frequency peak of 100–200 km. We built a cellular automata model to simulate the spatial transmission process of HPAI as a function of transmission distance, variance of the transmission distance, infection rate, and transmission times (how many times HPAI transmits from one host to another before suppression). We determined that the transmission distance between HPAI occurrences is approximately 100 km on the basis of historical HPAI occurrences from 2003 to 2006 in both wild and domestic birds. To effectively reduce the long‐distance spreading of HPAI, preventing close contact between domestic birds and waterfowl within a radius of 100 km around HPAI occurrence sites is essential.     

Risk signals of an influenza pandemic caused by highly pathogenic avian influenza subtype H5N1: spatio-temporal perspectives

Highly pathogenic avian influenza (HPAI) subtype H5N1 is a trans-boundary animal disease that has crossed the animal-human species barrier and over the past decade has had a considerable impact on the poultry industry, wild bird populations and on human health. Understanding the spatio-temporal patterns of H5N1 outbreaks can provide visual clues to the dynamics of disease spread and of areas at risk, and thus improve the cost-effectiveness of disease control and prevention. This study describes the characteristics and investigates the temporal, spatial and space-time dynamics of H5N1 outbreaks in domestic poultry between December 2003 and December 2009 using a global database. The study found that the start date of the epidemic wave was postponed, the duration of the epidemic was prolonged and its magnitude reduced over time, but the disease transmission cycle was not efficiently interrupted. Two 'hot-spot' regions of H5N1 outbreaks were identified: well-documented locations in East and Southeast Asia, as well as a novel location at the boundaries of Europe and Africa, where enhanced surveillance should be conducted. The risk of a pandemic due to H5N1 remains high.     

Classic fowl plague--a review

Highly pathogenic avian influenza (HPAI) represents a severe form of generalized avian influenza which is characterized by a rapid and severe course of disease and a very high mortality. All poultry species are susceptible. Turkeys and chickens are most vulnerable. There are no pathognomonic symptoms or specific pathological alterations. The disease is caused by avian influenza virus strains of the subtypes H5 or H7. These viruses arise spontaneously from apathogenic progenitors by insertional mutation in the HA gene. Until recently, outbreaks of HPAI were rare events, however, they have been found to cause increasing losses over the past few years. Since 2003, a widespread occurrence of HPAI has been registered in southeast Asia, and some countries are endemically infected with HPAIV strain H5N1. In six countries this virus has also caused fatal human infections. This has sparked fears that this agent may be the progenitor of a new pandemic influenza virus. During summer 2005 the disease has slowly spread westward. Isolated outbreaks have been reported from Kazakhstan, Russia, Romania, Turkey, Croatia and Ukraine. Migratory birds have been tentatively accused for spreading the infection along their flyways.     

Modeling the dynamics of backyard chicken flows in traditional trade networks in Thailand: implications for surveillance and control of avian influenza

In Southeast Asia, traditional poultry marketing chains have been threatened by epidemics caused by the highly pathogenic avian influenza H5N1 (HPAI H5N1) virus. In Thailand, the trade of live backyard chickens is based on the activities of traders buying chickens from villages and supplying urban markets with chicken meat. This study aims to quantify the flows of chickens traded during a 1-year period in a province of Thailand. A compartmental stochastic dynamic model was constructed to illustrate trade flows of live chickens from villages to slaughterhouses. Live poultry movements present important temporal variations with increased activities during the 15 days preceding the Chinese New Year and, to a lesser extent, other festivals (Qingming Festival, Thai New Year, Hungry Ghost Festival, and International New Year). The average distance of poultry movements ranges from 4 to 25 km, defining a spatial scale for the risk of avian influenza that spread through traditional poultry marketing chains. Some characteristics of traditional poultry networks in Thailand, such as overlapping chicken supply zones, may facilitate disease diffusion over longer distances through combined expansion and relocation processes. This information may be of use in tailoring avian influenza and other emerging infectious poultry disease surveillance and control programs provided that the cost-effectiveness of such scenarios is also evaluated in further studies.     

Identification of risk factors associated with highly pathogenic avian influenza H5N1 virus infection in poultry farms, in Nigeria during the epidemic of 2006-2007

We conducted a matched case-control study to evaluate risk factors for infection with highly pathogenic avian influenza (HPAI) H5N1 virus in poultry farms during the epidemic of 2006-2007 in Nigeria. Epidemiologic data were collected through the use of a questionnaire from 32 case farms and 83 control farms. The frequency of investigated exposure factors was compared between case and control farms by using conditional logistic regression analysis. In the multivariable analysis, the variables for (i) receiving visitors on farm premises (odds ratio [OR]=8.32; 95% confidence interval [CI]=1.87, 36.97; P<0.01), (ii) purchased live poultry/products (OR=11.91; 95% CI=3.11-45.59; P<0.01), and (iii) farm workers live outside the premises (OR=8.98; 95% CI=1.97, 40.77; P<0.01) were identified as risk factors for HPAI in poultry farms. Improving farm hygiene and biosecurity should help reduce the risk for influenza (H5N1) infection in poultry farms in Nigeria.     

A Bayesian model for spatial wildlife disease prevalence data

The analysis of the geographical distribution of disease on the scale of geographic areas such as administrative boundaries plays an important role in veterinary epidemiology. Prevalence estimates of wildlife population surveys are often based on regional count data generated by sampling animals shot by hunters. The observed disease rate per spatial unit is not an useful estimate of the underlying disease prevalence due to different sample sizes and spatial dependencies between neighbouring areas. Therefore, it is necessary to account for extra-sample variation and spatial correlations in the data to produce more accurate maps of disease incidence. The detection of spatial patterns is complicated by missing data in many of the geographical areas as the complete coverage of all areas is nearly impossible in wildlife surveys. For this purpose a hierarchical Bayesian model in which structured and unstructured over dispersion is modelled explicitly in terms of spatial and non-spatial components was implemented by Markov chain Monte Carlo methods. The model was empirically compared with the results of a non-spatial beta-binomial model using surveillance data of pseudorabies virus infections of European wild boars (Sus scrofa scrofa L.) in the Federal State of Brandenburg, Germany.