Hepatitis E virus (HEV) is the causative agent of hepatitis E in humans, an emerging zoonosis mainly transmitted via food in developed countries and for which domestic pigs are recognised as the main reservoir. It therefore appears important to understand the features and drivers of HEV infection dynamics on pig farms in order to implement HEV surveillance programmes and to assess and manage public health risks. The authors have reviewed the international scientific literature on the epidemiological characteristics of HEV in swine populations. Although prevalence estimates differed greatly from one study to another, all consistently reported high variability between farms, suggesting the existence of multifactorial conditions related to infection and within-farm transmission of the virus. Longitudinal studies and experimental trials have provided estimates of epidemiological parameters governing the transmission process (e.g. age at infection, transmission parameters, shedding period duration or lag time before the onset of an immune response). Farming practices, passive immunity and co-infection with immunosuppressive agents were identified as the main factors influencing HEV infection dynamics, but further investigations are needed to clarify the different HEV infection patterns observed in pig herds as well as HEV transmission between farms. Relevant surveillance programmes and control measures from farm to fork also have to be fostered to reduce the prevalence of contaminated pork products entering the food chain.Electronic supplementary materialThe online version of this article (doi:10.1186/s13567-017-0436-3) contains supplementary material, which is available to authorized users.
Pathogen spread between farms results from interaction between the epidemiological characteristics of infectious agents, such as transmission route, and the contact structure between holdings. The objective of our study was to design network models of pig movements matching with epidemiological features of pathogens. Our first model represents the transmission of infectious diseases between farms only through the introduction of animals to holdings (Animal Introduction Model AIM), whereas the second one also accounts for pathogen spread through intermediate transit of trucks through farms even without any animal unloading (i.e. indirect transmission–Transit Model TM). To take the pyramidal organisation of pig production into consideration, these networks were studied at three different scales: the whole network and two subnetworks containing only breeding or production farms. The two models were applied to pig movement data recorded in France from June 2012 to December 2014. For each type of model, we calculated network descriptive statistics, looked for weakly/strongly connected components (WCCs/SCCs) and communities, and analysed temporal patterns. Whatever the model, the network exhibited scale-free and small-world topologies. Differences in centrality values between the two models showed that nucleus, multiplication and post-weaning farms played a key role in the spread of diseases transmitted exclusively by the introduction of infected animals, whereas farrowing and farrow-to-finish herds appeared more vulnerable to the introduction of infectious diseases through indirect contacts. The second network was less fragmented than the first one, a giant SCC being detected. The topology of network communities also varied with modelling assumptions: in the first approach, a huge geographically dispersed community was found, whereas the second model highlighted several small geographically clustered communities. These results underline the relevance of developing network models corresponding to pathogen features (e.g. their transmission route), and the need to target specific types of holdings/areas for surveillance depending on the epidemiological context.
In developed countries, most of hepatitis E human cases are of zoonotic origin. Swine is a major hepatitis E virus (HEV) reservoir and foodborne transmissions after pork product consumption have been described. The risk for HEV-containing pig livers at slaughter time is related to the age at infection and to the virus shedding duration. Porcine Reproductive and Respiratory Syndrome Virus (PRRSV) is a virus that impairs the immune response; it is highly prevalent in pig production areas and suspected to influence HEV infection dynamics. The impact of PRRSV on the features of HEV infections was studied through an experimental HEV/PRRSV co-infection of specific-pathogen-free (SPF) pigs. The follow-up of the co-infected animals showed that HEV shedding was delayed by a factor of 1.9 in co-infected pigs compared to HEV-only infected pigs and specific immune response was delayed by a factor of 1.6. HEV shedding was significantly increased with co-infection and dramatically extended (48.6 versus 9.7 days for HEV only). The long-term HEV shedding was significantly correlated with the delayed humoral response in co-infected pigs. Direct transmission rate was estimated to be 4.7 times higher in case of co-infection than in HEV only infected pigs (0.70 and 0.15 per day respectively). HEV infection susceptibility was increased by a factor of 3.3, showing the major impact of PRRSV infection on HEV dynamics. Finally, HEV/PRRSV co-infection – frequently observed in pig herds – may lead to chronic HEV infection which may dramatically increase the risk of pig livers containing HEV at slaughter time.Electronic supplementary materialThe online version of this article (doi:10.1186/s13567-015-0207-y) contains supplementary material, which is available to authorized users.
European hygiene regulations require the condemnation of any unsafe food. However, there is little information identifying and quantifying condemnation of poultry carcases at slaughterhouses. We present an in-depth view of rates of and reasons for the condemnation of broiler, turkey, meat and force-feeding duck, guinea fowl carcases in France. The experiment was conducted in 10 slaughterhouses. For one year, all condemnations were recorded on a standard form following a national reference system. The rates of and reasons for condemnation, as well as factors influencing variation were investigated. The global condemnation rates were 1.04 per cent for broilers, 1.85 per cent for turkeys, 1.23 per cent for meat ducks, 1.42 per cent for force-feeding ducks and 1.20 per cent for guinea fowl. Condemnation rates depended on several factors including slaughterhouse, animal gender and season. Reasons for condemnation varied with species, for example, the three main reasons for broilers were cachexia (41.8 per cent of condemned batches), generalised congestion (29.3 per cent) and non-purulent cutaneous lesions (14.2 per cent) versus conformation abnormalities (58.6 per cent), cachexia (14.61 per cent) and ascites (14.56 per cent) for meat ducks. While the condemnation rates can be considered low for all species, the difference between the rates of and reasons for condemnation highlights the need to lead species-specific epidemiological studies to improve the sanitary situation of poultry production.
Hepatitis E virus (HEV) is a zoonotic pathogen, in particular genotype 3 HEV is mainly transmitted to humans through the consumption of contaminated pork products. This study aimed at describing HEV infection patterns in pig farms and at assessing the impact of immunomodulating co-infections namely Porcine Reproductive and Respiratory Syndrome Virus (PRRSV) and Porcine Circovirus Type 2 (PCV2), as well as other individual factors such as piglets' immunity and litters' characteristics on HEV dynamics. A longitudinal follow-up was conducted in three farrow-to-finish farms known to be HEV infected. Overall, 360 piglets were individually monitored from birth to slaughter with regular blood and faecal sampling as well as blood and liver samples collected at slaughterhouse. Virological and serological analyses were performed to detect HEV, PCV2 and PRRSV genome and antibodies. The links between 12 explanatory variables and four outcomes describing HEV dynamics were assessed using cox-proportional hazard models and logistic regression. HEV infection dynamics was found highly variable between farms and in a lower magnitude between batches. HEV positive livers were more likely related to short time-intervals between HEV infection and slaughter time (<40 days, OR = 4.1 [3.7-4.5]). In addition to an influence of piglets' sex and sows' parity, the sequence of co-infections was strongly associated with different HEV dynamics: a PRRSV or PCV2/PRRSV pre-or co-infection was associated with a higher age at HEV shedding (Hazard Ratio = 0.3 [0.2-0.5]), as well as a higher age at HEV seroconversion (HR = 0.5 [0.3-0.9] and HR = 0.4 [0.2-0.7] respectively). A PCV2/PRRSV pre-or co-infection was associated with a longer duration of shedding (HR = 0.5 [0.3-0.8]). Consequently, a PRRSV or PCV2/PRRSV pre-or co-infection was strongly associated with a higher risk of having positive livers at slaughter (OR = 4.1 [1.9-8.9] and OR = 6.5 [3.2-13.2] respectively). In conclusion, co-infections with immunomodulating viruses were found to affect HEV dynamics in the farrow-to-finish pig farms that were followed in this study. K E Y W O R D S hepatitis E virus, infection dynamics, PCV2, PRRSV, public health, risk factors | 1931 SALINES Et AL.
Hepatitis E virus is a zoonotic pathogen for which pigs are recognized as the major reservoir in industrialised countries. A multiscale model was developed to assess the HEV transmission and persistence pattern in the pig production sector through an integrative approach taking into account within-farm dynamics and animal movements based on actual data. Within-farm dynamics included both demographic and epidemiological processes. Direct contact and environmental transmission routes were considered along with the possible co-infection with immunomodulating viruses (IMVs) known to modify HEV infection dynamics. Movements were limited to 3,017 herds forming the largest community on the swine commercial network in France and data from the national pig movement database were used to build the contact matrix. Between-herd transmission was modelled by coupling within-herd and network dynamics using the SimInf package. Different introduction scenarios were tested as well as a decrease in the prevalence of IMV-infected farms. After introduction of a single infected gilt, the model showed that the transmission pathway as well as the prevalence of HEV-infected pigs at slaughter age were affected by the type of the index farm, the health status of the population and the type of the infected farms. These outcomes could help design HEV control strategies at a territorial scale based on the assessment of the farms’ and network’s risk.
Animal movements between farms are a major route of pathogen spread in the pig production sector. This study aimed to pair network analysis and epidemiological data in order to evaluate the impact of animal movements on pathogen prevalence in farms and assess the risk of local areas being exposed to diseases due to incoming movements. Our methodology was applied to hepatitis E virus (HEV), an emerging foodborne zoonotic agent of concern that is highly prevalent in pig farms. Firstly, the pig movement network in France (data recorded in 2013) and the results of a nation-wide seroprevalence study (data collected in 178 farms in 2009) were modelled and analysed. The link between network centrality measures of farms and HEV seroprevalence levels was explored using a generalised linear model. The in-degree and ingoing closeness of farms were found to be statistically associated with high HEV within-farm seroprevalence (p<0.05). Secondly, the risk of a French département (i.e. French local administrative areas) being exposed to HEV was calculated by combining the distribution of farm-level HEV prevalence in source départements with the number of movements coming from those same départements. By doing so, the risk of exposure for départements was mapped, highlighting differences between geographical patterns of HEV prevalence and the risk of exposure to HEV. These results suggest that not only highly prevalent areas but also those having at-risk movements from infected areas should be monitored. Pathogen management and surveillance options in the pig production sector should therefore take animal movements into consideration, paving the way for the development of targeted and risk-based disease surveillance strategies.
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