Systematic Review and Meta-Analysis of the Efficacy of Interventions Applied during Primary Processing to Reduce Microbial Contamination on Pig Carcasses.

Interventions from lairage to the chilling stage of the pig slaughter process are important to reduce microbial contamination of carcasses. The aim of this systematic review and meta-analysis was to assess the effectiveness of abattoir interventions in reducing aerobic colony count (ACC), Enterobacteriaceae, generic Escherichia coli, and Yersinia spp. on pig carcasses. The database searches spanned a 30 year period from 1990 to 2021. Following a structured, predefined protocol, 22 articles, which were judged as having a low risk of bias, were used for detailed data extraction and meta-analysis. The meta-analysis included data on lairage interventions for live pigs, standard processing procedures for pig carcasses, prechilling interventions, multiple carcass interventions, and carcass chilling. Risk ratios (RRs) for prevalence studies and mean log differences (MDs) for concentration outcomes were calculated using random effects models. The meta-analysis found that scalding under commercial abattoir conditions effectively reduced the prevalence of Enterobacteriaceae (RR: 0.05, 95% CI: 0.02 to 0.12, I2 = 87%) and ACC (MD: -2.84, 95% CI: -3.50 to -2.18, I2 = 99%) on pig carcasses. Similarly, significant reductions of these two groups of bacteria on carcasses were also found after singeing (RR: 0.25, 95% CI: 0.14 to 0.44, I2 = 90% and MD: -1.95, 95% CI: -2.40 to -1.50, I2 = 96%, respectively). Rectum sealing effectively reduces the prevalence of Y. enterocolitica on pig carcasses (RR: 0.60, 95% CI: 0.41 to 0.89, I2 = 0%). Under commercial abattoir conditions, hot water washing significantly reduced ACC (MD: -1.32, 95% CI: -1.93 to -0.71, I2 = 93%) and generic E. coli counts (MD: -1.23, 95% CI: -1.89 to -0.57, I2 = 61%) on pig carcasses. Conventional dry chilling reduced Enterobacteriaceae prevalence on pig carcasses (RR: 0.32, 95% CI: 0.21 to 0.48, I2 = 81%). Multiple carcass interventions significantly reduced Enterobacteriaceae prevalence (RR: 0.11, 95% CI: 0.05 to 0.23, I2 = 94%) and ACC on carcasses (MD: -2.85, 95% CI: -3.33 to -2.37, I2 = 97%). The results clearly show that standard processing procedures of scalding and singeing and the hazard-based intervention of hot water washing are effective in reducing indicator bacteria on pig carcasses. The prevalence of Y. enterocolitica on pig carcasses was effectively reduced by the standard procedure of rectum sealing; nevertheless, this was the only intervention for Yersinia investigated under commercial conditions. High heterogeneity among studies and trials investigating interventions and overall lack of large, controlled trials conducted under commercial conditions suggest that more in-depth research is needed.

Analysis of bovine postmortem condemnation data in France: Contributions from a comprehensive and standardised information system at the slaughterhouse.

BACKGROUND: The condemnation of carcases and offal unfit for human consumption is a regulatory requirement at the slaughterhouse. Condemnation data, if comprehensive and standardised, can be a valuable source of information for risk-based inspection and decision making. METHODS: The aim of this study was to analyse postmortem condemnation data that were recorded in all bovine slaughterhouses in mainland France from 1 January 2016 to 31 December 2020 in a comprehensive and standardised information system. The rates of and reasons for condemnation, as well as factors influencing rate variation, were investigated through descriptive analysis and multivariable logistic regression models. RESULTS: The global, total and partial condemnation rates were 4.5%, 0.7% and 3.8% for adult cattle and 1.4%, 0.3% and 1.1% for calves, respectively. Reasons for condemnation varied with the animal category; for example, the three main reasons for total condemnation in adult cattle were serous infiltration of connective tissue (49% of condemned animals), congestive peritonitis (12.2%) and fibrinous peritonitis (10.9%), whereas the top three reasons for partial condemnation were unique abscess (21.9%), haemorrhagic infiltration (20.6%) and muscular sclerosis (17.4%). Condemnation rates were influenced by animal-related factors (sex, age, type of breed) and slaughterhouse-related factors (status, type, slaughter volume). CONCLUSION: Our findings could usefully contribute to the continuous improvement of the harmonisation of inspection decisions and support the risk manager's strategy in the modernisation of official controls at the slaughterhouse.

A between-herd data-driven stochastic model to explore the spatio-temporal spread of hepatitis E virus in the French pig production network.

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.

Tackling hepatitis E virus spread and persistence on farrow-to-finish pig farms: Insights from a stochastic individual-based multi-pathogen model.

Hepatitis E virus (HEV) is a zoonotic agent of which domestic pigs have been recognised as the main reservoir in industrialised countries. The great variability in HEV infection dynamics described on different pig farms may be related to the influence of other pathogens, and in particular viruses affecting pigs' immune response. The objective of this study was to develop a multi-pathogen modelling approach to understand the conditions under which HEV spreads and persists on a farrow-to-finish pig farm taking into account the fact that pigs may be co-infected with an intercurrent pathogen. A stochastic individual-based model was therefore designed that combines a population dynamics model, which enables us to take different batch rearing systems into account, with a multi-pathogen model representing at the same time the dynamics of both HEV and the intercurrent pathogen. Based on experimental and field data, the epidemiological parameters of the HEV model varied according to the pig's immunomodulating virus status. HEV spread and persistence was found to be very difficult to control on a farm with a 20-batch rearing system. Housing sows in smaller groups and eradicating immunomodulating pathogens would dramatically reduce the prevalence of HEV-positive livers at slaughter, which would drop from 3.3% to 1% and 0.2% respectively (p-value < 0.01). It would also decrease the probability of HEV on-farm persistence from 0.6 to 0 and 0.34 respectively (p-value < 0.01) on farms with a 7 batch rearing system. A number of farming practices, such as limiting cross-fostering, reducing the size of weaning pens and vaccinating pigs against immunomodulating viruses, were also shown to be pivotal factors for decreasing HEV spread and persistence.

Controlling hepatitis E virus in the pig production sector: Assessment of the technical and behavioural feasibility of on-farm risk mitigation strategies.

Hepatitis E virus (HEV) is a zoonotic agent with pigs as the main reservoir in industrialised countries. Recent studies conducted on pig farms, in experimental conditions or through modelling approaches, have led to a better understanding of the spread of HEV on pig farms. The findings have also made it possible to define a set of measures to reduce HEV prevalence and the risk of marketing contaminated products. The objective of this study was to assess the feasibility of a set of HEV control strategies on pig farms. Individual semi-structured interviews were conducted with farmers, veterinarians and farming advisors to collect general data, their level of knowledge of HEV, their opinion on the technical feasibility of certain changes in practices, their perception of the respective responsibilities of the different stakeholders, and their feelings about the importance of the issue, following the framework of the Theory of Planned Behaviour. The interviews made it possible to highlight potential barriers and preferred motivators for the implementation of on-farm risk mitigation strategies. Barriers included lack of knowledge, scientific gaps, perceived inability to control HEV, and low perception of the importance of the issue. Motivators included professional satisfaction, family recognition, and the opportunity to achieve higher quality standards. Three clusters of stakeholders were also identified, with a group of leaders who could help unlock reluctance and disseminate innovations. This type of behavioural approach appeared useful to help risk managers facilitate zoonotic control on pig farms.

Impact of porcine circovirus type 2 (PCV2) infection on hepatitis E virus (HEV) infection and transmission under experimental conditions.

Hepatitis E virus is a zoonotic pathogen for which pigs have been identified as the main reservoir in industrialised countries. HEV infection dynamics in pig herds and pigs are influenced by several factors, including herd practices and possibly co-infection with immunomodulating viruses. This study therefore investigates the impact of porcine circovirus type 2 (PCV2) on HEV infection and transmission through experimental HEV/PCV2 co-infection of specific-pathogen-free pigs. No statistical difference between HEV-only and HEV/PCV2-infected animals was found for either the infectious period or the quantity of HEV shed in faeces. The HEV latency period was shorter for HEV/PCV2 co-infected pigs than for HEV-only infected pigs (11.6 versus 12.3 days). Its direct transmission rate was three times higher in cases of HEV/PCV2 co-infection than in cases of HEV-only infection (0.12 versus 0.04). On the other hand, the HEV transmission rate through environmental accumulation was lower in cases of HEV/PCV2 co-infection (4.3·10-6 versus 1.5·10-5 g/RNA copies/day for HEV-only infected pigs). The time prior to HEV seroconversion was 1.9 times longer in HEV/PCV2 co-infected pigs (49.4 versus 25.6 days for HEV-only infected pigs). In conclusion, our study shows that PCV2 affects HEV infection and transmission in pigs under experimental conditions.

Natural viral co-infections in pig herds affect hepatitis E virus (HEV) infection dynamics and increase the risk of contaminated livers at slaughter.

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.

Persistent viremia and presence of hepatitis E virus RNA in pig muscle meat after experimental co-infection with porcine reproductive and respiratory syndrome virus.

Although hepatitis E virus (HEV) transmission has been demonstrated after consumption of products containing infected pig liver, human cases can be also associated with other pig meat products, such as sausages. Data on HEV viremia and dissemination in muscle meat of infected animals are still sparse, especially during long-term infection. Previously, we have shown that experimental co-infection of pigs with HEV and porcine reproductive and respiratory syndrome virus (PRRSV) lengthens HEV infection up to 49 days and increases the likelihood of the presence of HEV RNA in the liver of the pig at a later stage of infection. In the present study, we show that during experimental HEV-PRRSV co-infection, prolonged HEV viremia, up to 49 days post-inoculation (dpi), is detected. The long-term viremia observed was statistically associated with the absence of HEV seroconversion. HEV RNA was also frequently detected, at a late stage of infection (49 dpi), in the three different types of muscle tested: femoral biceps, psoas major or diaphragm pillar. The HEV RNA load could reach up to 1 ·â€¯106 genome copies per gram of muscle. Detection of HEV in muscle meat was statistically associated with high HEV loads in corresponding liver and fecal samples. The presence of HEV in pig blood, femoral biceps and major psoas, corresponding to ham and tenderloin muscles respectively, is of concern for the food industry. Hence, these results indicate new potential risks for consumers and public health regarding pork products.

Are French pig farmers and veterinarians knowledgeable about emerging foodborne pathogens? The case of hepatitis E virus.

Hepatitis E virus (HEV) is an emerging zoonotic pathogen mainly transmitted via food in developed countries, and for which domestic pigs are recognised as the main reservoir. To implement an efficient HEV surveillance and control plan in the pig production sector, it is first necessary to assess the level of knowledge of pig-farming main actors about this pathogen. To this aim, an online survey was conducted between September and October 2017 to evaluate pig farmers' and veterinarians' knowledge about HEV epidemiology and its zoonotic potential. The questionnaire was filled in by 383 pig farmers and 46 pig veterinarians. Of this population, 77.8% of farmers and 8.7% of veterinarians had never heard of HEV. Our results highlight knowledge gaps among responding farmers, especially regarding the clinical and epidemiological features of HEV, while veterinarians appear to be well-informed about this pathogen. These findings indicate significant room for further improvement and the need for more information aimed at French pig farmers, with veterinarians acting as a priority channel through which information may be transferred from scientists to farmers. These educational efforts will facilitate farmers' involvement in future HEV surveillance and control plans.

Combining network analysis with epidemiological data to inform risk-based surveillance: Application to hepatitis E virus (HEV) in pigs.

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.

Pig movements in France: Designing network models fitting the transmission route of pathogens.

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.

From the epidemiology of hepatitis E virus (HEV) within the swine reservoir to public health risk mitigation strategies: a comprehensive review.

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.

Hepatitis E virus chronic infection of swine co-infected with Porcine Reproductive and Respiratory Syndrome Virus.

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.