Guillaume Fournié

Interventions for avian influenza A (H5N1) risk management in live bird market networks

Highly pathogenic avian influenza virus subtype H5N1 is endemic in Asia, with live bird trade as a major disease transmission pathway. A cross-sectional survey was undertaken in northern Vietnam to investigate the structure of the live bird market (LBM) contact network and the implications for virus spread. Based on the movements of traders between LBMs, weighted and directed networks were constructed and used for social network analysis and individual-based modeling. Most LBMs were connected to one another, suggesting that the LBM network may support large-scale disease spread. Because of cross-border trade, it also may promote transboundary virus circulation. However, opportunities for disease control do exist. The implementation of thorough, daily disinfection of the market environment as well as of traders’ vehicles and equipment in only a small number of hubs can disconnect the network dramatically, preventing disease spread. These targeted interventions would be an effective alternative to the current policy of a complete ban of LBMs in some areas. Some LBMs that have been banned still are very active, and they likely have a substantial impact on disease dynamics, exhibiting the highest levels of susceptibility and infectiousness. The number of trader visits to markets, information that can be collected quickly and easily, may be used to identify LBMs suitable for implementing interventions. This would not require prior knowledge of the force of infection, for which laboratory-confirmed surveillance would be necessary. These findings are of particular relevance for policy development in resource-scarce settings.

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.

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.

Temporal characterisation of the network of Danish cattle movements and its implication for disease control: 2000–2009

Social network analysis provides a valuable framework for understanding the dynamics of diseases on networks as well as a means for defining effective control measures. An understanding of the underlying contact pattern for a susceptible population is advisable before embarking on any strategy for disease control. The objective of this study was to characterise the network of Danish cattle movements over a 10-year period from 2000 to 2009 with a view to understanding: (1) cohesiveness of the network, (2) influential holdings and (3) structural vulnerability of the network. Network analyses of data involving all cattle movements in Denmark registered during the period of interest were performed. A total of 50,494 premises participated in 4,204,895 individual movements during the 10-year period. The results pointed to a predominantly scale-free structure of the network; though marked by small-world properties in March-April 2001 as well as in 24 other months during the period October 2006 to December 2009. The network was sparsely connected with markets being the key influential holdings. Its vulnerability to removal of markets suggests that targeting highly connected holdings during epidemics should be the focus of control efforts.

Can closure of live poultry markets halt the spread of H7N9

After isolation of avian infl uenza A H7N9 virus from live poultry markets (LPMs), and reports that several people who were infected with the virus had visited such markets a few days before disease onset, LPMs were suspected to be a main source of human exposure to H7N9 in China. After LPM closure was enforced in several Chinese cities, the incidence of H7N9 human cases rapidly reduced. In The Lancet, Hongjie Yu and colleagues quantify the risk of human infections before and after LPM closure in the Chinese cities of Nanjing, Shanghai, Hangzhou, and Huzhou. The investigators used information about laboratory-confi rmed cases of avian infl uenza A H7N9 virus infection reported in the four cities by June 7, 2013, to fi t a statistical model to assess the daily probability of infection for each susceptible individual before and after LPM closure. They report that closure of LPMs reduced the mean daily number of infections by 99% (95% credibility interval 93–100%) in Shanghai, 99% (92–100%) in Hangzhou, 97% (68–100%) in Huzhou, and 97% (81–100%) in Nanjing. They conclude that LPM closure should be sustained in areas with high risk of disease spread, and implemented in any urban areas where avian infl uenza A H7N9 virus appears in the future. LPMs are known to be a high-risk environment for pathogen transmission between birds and for zoonotic transfer to people. If birds spend a suffi cient amount of time in LPMs to become infected and transmit the virus to other susceptible birds, sustained virus circulation in LPMs can occur. LPMs can then become a permanent source of infection for poultry fl ocks and for people who are in close contact with infected poultry and contaminated fomites. LPM closure would therefore be expected to stop human infections caused by a zoonotic pathogen transmitted within markets. Although LPM closure seems to have had an important eff ect on incidence of avian infl uenza A H7N9 virus infection in people, the underlying epidemiological and socioeconomic system is complex. LPM closure might not have been the most important cause of a reduction in incidence. Indeed, soon after LPM closures in Nanjing, Shanghai, Hangzhou, and Huzhou, human infections were also interrupted in other cities where this measure was not implemented. An example of the complex chain of interacting socioeconomic and epidemiological factors is that reports that poultry is a source of avian infl uenza A H7N9 virus triggered a drop in demand for poultry meat and consequently in poultry prices. Some producers were even forced to destroy their fl ocks because poultry rearing became cost prohibitive, which probably reduced the absolute number of poultry substantially in aff ected areas and reduced viral circulation, irrespective of LPM closure. Strong consumer reactions to zoonotic health hazards are not uncommon. Fears of avian infl uenza A H5N1 virus led to reduced consumption of poultry products in Asia in early 2004. However, these reductions were temporary: consumers’ anxiety decreased rapidly after the fi rst wave of the outbreak. Consumption of poultry products resumed within a few months, sometimes exceeding levels recorded before the outbreak, even though the virus had become endemic and human cases were reported regularly. Reduced consumer demand could have increased the compliance of poultry production stakeholders with LPM closures in China, because informal alternative ways to sell poultry were unavailable. Avian infl uenza A H7N9 virus is probably still circulating in Chinese poultry fl ocks, as suggested by new human cases reported in August, 2013. If poultry consumption resumes, the seasonal increase in poultry production and trading activities that usually occurs in the months preceding Chinese New Year could amplify virus circulation, resulting in a surge in human cases. If this increase occurs and consumer reactions are not as strong as during the spring of 2013, Published Online October 31, 2013 http://dx.doi.org/10.1016/ S0140-6736(13)62109-1

Host selection and parasite infection in Aedes taeniorhynchus, endemic disease vector in the Galapagos Islands

Host selection in blood-sucking arthropods has important evolutionary and ecological implications for the transmission dynamics, distribution and host-specificity of the parasites they transmit. The black salt-marsh mosquito (Aedes taeniorhynchus Wiedemann) is distributed throughout tropical to temperate coastal zones in the Americas, and continental populations are primarily mammalphilic. It is the only indigenous mosquito in the Galápagos Islands, having colonised the archipelago around 200,000 years ago, potentially adapting its host selection, and in the process, altering the dynamics of vector mediated pathogen interactions in the archipelago. Here, we use blood-meal analysis and PCR-based parasite screening approach to determine the blood-feeding patterns of A. taeniorhynchus in the Galápagos Islands and identify potential parasite transmission with which this mosquito could be involved. Our results show that A. taeniorhynchus feeds equally on mammals and reptiles, and only one avian sample was observed in 190 successful PCR amplifications from blood meals. However, we detected endemic filarial worms and Haemoproteus parasites known to infect various Galápagos bird species in mosquito thoraces, suggesting that feeding on birds must occur at low frequency, and that A. taeniorhynchus may play a role in maintaining some avian vector-borne pathogens, although more work is needed to explore this possibility. We also isolated three different DNA sequences corresponding to hemogregarine parasites of the genus Hepatozoon from mosquito and iguana blood samples, suggesting that more than one species of Hepatozoon parasites are present in Galápagos. Phylogenetic analysis of Hepatozoon 18sRNA sequences indicates that A. taeniorhynchus may have facilitated a recent breakdown in host-species association of formerly isolated Hepatozoon spp. infecting the reptile populations in the Galápagos Islands.

Potential risk of regional disease spread in West Africa through cross-border cattle trade.

Background Transboundary animal movements facilitate the spread of pathogens across large distances. Cross-border cattle trade is of economic and cultural importance in West Africa. This study explores the potential disease risk resulting from large-scale, cross-border cattle trade between Togo, Burkina Faso, Ghana, Benin, and Nigeria for the first time. Methods and Principal Findings A questionnaire-based survey of livestock movements of 226 cattle traders was conducted in the 9 biggest cattle markets of northern Togo in February-March 2012. More than half of the traders (53.5%) operated in at least one other country. Animal flows were stochastically simulated based on reported movements and the risk of regional disease spread assessed. More than three quarters (79.2%, range: 78.1–80.0%) of cattle flowing into the market system originated from other countries. Through the cattle market system of northern Togo, non-neighbouring countries were connected via potential routes for disease spread. Even for diseases with low transmissibility and low prevalence in a given country, there was a high risk of disease introduction into other countries. Conclusions By stochastically simulating data collected by interviewing cattle traders in northern Togo, this study identifies potential risks for regional disease spread in West Africa through cross-border cattle trade. The findings highlight that surveillance for emerging infectious diseases as well as control activities targeting endemic diseases in West Africa are likely to be ineffective if only conducted at a national level. A regional approach to disease surveillance, prevention and control is essential.

Investigating poultry trade patterns to guide avian influenza surveillance and control: a case study in Vietnam

Live bird markets are often the focus of surveillance activities monitoring avian influenza viruses (AIV) circulating in poultry. However, in order to ensure a high sensitivity of virus detection and effectiveness of management actions, poultry management practices features influencing AIV dynamics need to be accounted for in the design of surveillance programmes. In order to address this knowledge gap, a cross-sectional survey was conducted through interviews with 791 traders in 18 Vietnamese live bird markets. Markets greatly differed according to the sources from which poultry was obtained, and their connections to other markets through the movements of their traders. These features, which could be informed based on indicators that are easy to measure, suggest that markets could be used as sentinels for monitoring virus strains circulating in specific segments of the poultry production sector. AIV spread within markets was modelled. Due to the high turn-over of poultry, viral amplification was likely to be minimal in most of the largest markets. However, due to the large number of birds being introduced each day, and challenges related to cleaning and disinfection, environmental accumulation of viruses at markets may take place, posing a threat to the poultry production sector and to public health.

When private actors matter: Information-sharing network and surveillance of Highly Pathogenic Avian Influenza in Vietnam

The effectiveness of animal health surveillance systems depends on their capacity to gather sanitary information from the animal production sector. In order to assess this capacity we analyzed the flow of sanitary information regarding Highly Pathogenic Avian Influenza (HPAI) suspicions in poultry in Vietnam. Participatory methods were applied to assess the type of actors and likelihood of information sharing between actors in case of HPAI suspicion in poultry. While the reporting of HPAI suspicions is mandatory, private actors had more access to information than public actors. Actors of the upstream sector (medicine and feed sellers) played a key role in the diffusion of information. The central role of these actors and the influence of the information flow on the adoption by poultry production stakeholders of behaviors limiting (e.g. prevention measures) or promoting disease transmission (e.g. increased animal movements) should be accounted for in the design of surveillance and control programs.

Analysis of Swine Movements in a Province in Northern Vietnam and Application in the Design of Surveillance Strategies for Infectious Diseases

While swine production is rapidly growing in South-East Asia, the structure of the swine industry and the dynamic of pig movements have not been well-studied. However, this knowledge is a prerequisite for understanding the dynamic of disease transmission in swine populations and designing cost-effective surveillance strategies for infectious diseases. In this study, we assessed the farming and trading practices in the Vietnamese swine familial farming sector, which accounts for most pigs in Vietnam, and for which disease surveillance is a major challenge. Farmers from two communes of a Red River Delta Province (northern Vietnam) were interviewed, along with traders involved in pig transactions. Major differences in the trade structure were observed between the two communes. One commune had mainly transversal trades, that is between farms of equivalent sizes, whereas the other had pyramidal trades, that is from larger to smaller farms. Companies and large familial farrow-to-finish farms were likely to act as major sources of disease spread through pig sales, demonstrating their importance for disease control. Familial fattening farms with high pig purchases were at greater risk of disease introduction and should be targeted for disease detection as part of a risk-based surveillance. In contrast, many other familial farms were isolated or weakly connected to the swine trade network limiting their relevance for surveillance activities. However, some of these farms used boar hiring for breeding, increasing the risk of disease spread. Most familial farms were slaughtering pigs at the farm or in small local slaughterhouses, making the surveillance at the slaughterhouse inefficient. In terms of spatial distribution of the trades, the results suggested that northern provinces were highly connected and showed some connection with central and southern provinces. These results are useful to develop risk-based surveillance protocols for disease detection in the swine familial sector and to make recommendations for disease control.

Epidemiology of Highly Pathogenic Avian Influenza Virus Strain Type H5N1

Highly pathogenic avian influenza (HPAI) is a severe disease of poultry. It is highly transmissible with a flock mortality rate approaching 100% in vulnerable species (Capua et al. 2007a). Due to the potentially disastrous impact the disease can have on affected poultry sectors, HPAI has received huge attention and is classified as a notifiable disease by the World Organisation for Animal Health (OIE).