New Patterns for Highly Pathogenic Avian Influenza and Adjustment of Prevention, Control and Surveillance Strategies: The Example of France.

From 2020 up to summer 2023, there was a substantial change in the situation concerning the high pathogenic avian influenza (HPAI) virus in Europe. This change concerned mainly virus circulation within wildlife, both in wild birds and wild mammals. It involved the seasonality of HPAI detections, the species affected, excess mortality events, and the apparent increased level of contamination in wild birds. The knock-on effect concerned new impacts and challenges for the poultry sector, which is affected by repeated annual waves of HPAI arriving with wild migratory birds and by risks due to viral circulation within resident wild birds across the year. Indeed, exceeding expectations, new poultry sectors and production areas have been affected during the recent HPAI seasons in France. The HPAI virus strains involved also generate considerable concern about human health because of enhanced risks of species barrier crossing. In this article, we present these changes in detail, along with the required adjustment of prevention, control, and surveillance strategies, focusing specifically on the situation in France.

Application of Machine Learning Prediction of Individual SARS-CoV-2 Vaccination and Infection Status to the French Serosurveillance Survey From March 2020 to 2022: Cross-Sectional Study.

BACKGROUND: The seroprevalence of SARS-CoV-2 infection in the French population was estimated with a representative, repeated cross-sectional survey based on residual sera from routine blood testing. These data contained no information on infection or vaccination status, thus limiting the ability to detail changes observed in the immunity level of the population over time. OBJECTIVE: Our aim is to predict the infected or vaccinated status of individuals in the French serosurveillance survey based only on the results of serological assays. Reference data on longitudinal serological profiles of seronegative, infected, and vaccinated individuals from another French cohort were used to build the predictive model. METHODS: A model of individual vaccination or infection status with respect to SARS-CoV-2 obtained from a machine learning procedure was proposed based on 3 complementary serological assays. This model was applied to the French nationwide serosurveillance survey from March 2020 to March 2022 to estimate the proportions of the population that were negative, infected, vaccinated, or infected and vaccinated. RESULTS: From February 2021 to March 2022, the estimated percentage of infected and unvaccinated individuals in France increased from 7.5% to 16.8%. During this period, the estimated percentage increased from 3.6% to 45.2% for vaccinated and uninfected individuals and from 2.1% to 29.1% for vaccinated and infected individuals. The decrease in the seronegative population can be largely attributed to vaccination. CONCLUSIONS: Combining results from the serosurveillance survey with more complete data from another longitudinal cohort completes the information retrieved from serosurveillance while keeping its protocol simple and easy to implement.

Avian influenza outbreaks: evaluating the efficacy of cleaning and disinfection of vehicles and transport crates.

In 2021, France faced large avian influenza outbreaks, like in 2016 and 2017. Controlling these outbreaks required the preventive depopulation of a large number of duck farms. A previous study in 2017 showed that the quality of decontamination of trucks and transport crates used for depopulation was often insufficient. A new study was then set up to evaluate cleaning and disinfection (C&D) of trucks and crates used for duck depopulation and whether practices had changed since 2017. Three methods were used to assess decontamination: 1) detection of avian influenza virus (AIV) genome, 2) visual inspection of cleanliness, and 3) microbial counts, considering that 2 and 3 are commonly used in abattoirs. Another objective of the study was to evaluate the correlation between results obtained with the 3 methods. In 5 abattoirs, 8 trucks and their crates were sampled by swabbing to detect AIV genome by rRT-PCR before and after decontamination. Visual cleanliness scores and coliform counts were also determined on crates after C&D. Trucks and crates were decontaminated according to the abattoirs' protocols. Before C&D, 3 quarters of crates (59/79) and 7 of 8 trucks were positive for AIV genome. C&D procedures were reinforced in 2021 compared to 2017; use of detergent solution and warm water were more common. Nevertheless, 28% of the crates were positive for AIV genome after C&D, despite the fact that cleaning scores and microbiological counts were satisfactory for 84% and 91% of the crates, respectively. No correlation was observed between results for AIV genome detection and results from visual control or from coliform counts. Abattoirs are encouraged to use environmental sampling coupled with AIV genome detection to monitor the quality of cleaning and disinfection of trucks and crates during AI outbreaks. Reinforcement of biosecurity measures at abattoirs is still needed to avoid residual contamination of the equipment and cross-contamination during the decontamination process.

Do Rubber Floor Mats Prevent Lameness in Gestating Sows Housed in Large Groups? A Field Experiment on Three Commercial Farms in France.

Lameness and foot disorders are major health and welfare issues in intensive swine production systems. They are exacerbated when sows are housed in large groups on slatted concrete floors during gestation. Our study aimed to assess the effect of rubber mats in the lying area of the gestation pen on lameness and leg health in gestating sows housed in large pens in commercial conditions. The study was conducted on three commercial farms over two successive gestations. A total of 582 Large White × Landrace sows, housed in 10 static groups, were enrolled: 5 groups in pens with rubber mats and 5 groups on slatted concrete floors. Lameness, bursitis, leg injuries, claw growth defects and claw lesions were measured at the beginning, middle and end of each gestation period. The rubber mats decreased the risk of suffering from bursitis, but had no effect on the risk of lameness, leg injuries, claw growth defects or claw lesions. Sows housed on rubber mats were heavily soiled compared with those on slatted concrete floors because the mats were not perforated for slurry evacuation. Locomotion disorders and foot lesions remained prevalent despite the rubber mats in the lying area of the gestation pens, but adding rubber mats in service rooms and farrowing crates may produce better results.

Compressed Brown Algae as a Potential Environmental Enrichment Material in Growing Pigs.

In barren housing conditions, enrichment materials are given to pigs to improve their welfare. Here, we assessed the suitability of an algae-based cylinder as an enrichment material on the behavioral, physiological, health and productivity welfare indicators of pigs. Algae was compared with metal chains and wood logs. The study involved 444 pigs from two successive batches on one single farm. During the suckling period, half of the pigs received algae and the control pigs received no material. After weaning and until the end of fattening, algae, wood or chains were equally distributed among the pigs. Consumption of algae cylinders was different between pens and between batches. After weaning and during the fattening period, although the results differed between batches, no significant difference was observed in the object manipulations. Salivary cortisol, used as biomarker to measure the stress levels after pig transfers, were similar between the treatments. Enrichment material made from algae had no negative effect on pig health and no effect on performance and body condition. Regarding their characteristics and according to Commission Recommendation (EU) 2016/336 classification, algae cylinders can be categorized as suboptimal enrichment materials, although the present results suggest that it does not significantly improve pig welfare compared to a metal chain, which is categorized as a material of marginal interest.

Cleaning and disinfection of crates and trucks used for duck transport: field observations during the H5N8 avian influenza outbreaks in France in 2017.

Transport of infected birds is thought to play a key role in the spread of avian influenza (AI) on poultry farms during epizootic outbreaks. Ensuring efficient cleaning and disinfection (C&D) of equipment used for transport is needed to prevent the spread of AI. This study aimed to evaluate the efficacy against the AI virus of C&D protocols applied on trucks and crates used for the transport of ducks during the H5N8 AI outbreaks in France in 2017. In 3 abattoirs, 16 transport vehicles and their crates were sampled by swabbing to detect the influenza type A genome by real-time reverse-transcription polymerase chain reaction. Vehicles were tested before and after decontamination, which was carried out in accordance with the abattoirs' protocols. A total of 86 samples out of 299 collected before C&D were positive for AI (29%); 7 trucks out of 16 transported crates detected positive for AI. After C&D, the AI genome was detected in 56 samples out of 308 (18%). Ten trucks were loaded with a shipment of AI-positive crates. Eight vehicles were detected positive in the cabin, on the truck bed, and/or on the wheels. Despite reinforcement of C&D, the efficacy of decontamination was variable among slaughterhouses. The efficacy seemed to depend on the initial contamination load, C&D protocols, and how the protocol is implemented. Breaks in biosecurity measures led to frequent contamination of trucks after C&D. Observational studies during animal health crises are of interest to analyze practices in emergency conditions and to put forward measures aimed at increased preparedness.

Husbandry Practices, Health, and Welfare Status of Organic Broilers in France.

Organic poultry production has increased sharply with growing consumer demand in the context of sustainable development. A study was conducted in 85 organic broiler flocks between 2014 and 2015 to describe the husbandry practices and the health and welfare status of organic broilers in France, and to study farming diversity by comparing independent farms (Ind farms, n = 15) with direct sales to farms working with companies (Comp farms, n = 70). Each flock was visited at 3 and 11 weeks of age to collect data on farming conditions, health disorders, and mortality. Welfare notation of 30 broilers per flock and parasitic examination of 5 broilers per flock was also performed. Findings showed significantly different farming management between Ind farms and Comp farms, with smaller flocks on the Ind farms (476 broilers/house vs. 3062 broilers/house, p < 0.01) more frequently in mobile houses. The mean mortality rate was 2.8%, mainly involving digestive disorders. Helminths were detected in 58.8% of the flocks. On average, 21.9% and 5.8% of broilers in a flock had footpad dermatitis and dirty feathers, respectively. The health and welfare characteristics of organic broilers on Ind farms vs. Comp farms were not significantly different, except dirtier feathers and more footpad dermatitis on Ind farms (19.1% vs. 2.9%, p = 0.03 and 39.6% vs. 18.1%, p = 0.02, respectively), associated with poultry housing conditions in mobile houses (p < 0.01). This study provides greater insight into farming sustainability aspects related to the husbandry practices, and the health and welfare of organic broilers in France.

Associations between animal welfare indicators and Campylobacter spp. in broiler chickens under commercial settings: A case study.

Few studies have previously investigated how poor animal welfare might be associated with infection of zoonotic pathogens in humans. This paper assesses the predictive value of the presence of Campylobacter spp. in broiler chicken flocks when animal-based measures related to footpad dermatitis, hock burns, body lesions and arthritis are identified under commercial conditions (high density). The study population included 32 flocks analysed on farm and at slaughter, slaughtered between April and August 2008 in six different slaughter plants in Brittany, France. Welfare and health indicators are those indicated by the European legislation and sampling was carried out in the framework of the European baseline survey on the prevalence of Campylobacter in broiler chicken. Caecal contents, sampled both on farm and at slaughter, and carcass skin samples from the neck and breast at slaughter, were investigated for the presence of Campylobacter spp. Logistic models/classification trees were used to estimate the probability of the presence (or absence) of a specific foodborne pathogen in a flock based on specific animal-based measures (or combinations of measures) in order to study the potential relationship between welfare indicators and foodborne pathogen prevalence/incidence levels. On farm, flocks with more than 25% animals with severe lesions on between 25 and 50% of the footpad are predicted to be Campylobacter-positive whereas flocks where less than 13 individuals have arthritis are predicted to be Campylobacter-negative. The error rate on farm and at slaughter was 10 and 4% respectively indicating good predicting abilities. A poor welfare environment may result in stress, which reduces chicken immunocompetence making them more susceptible to Campylobacter spp. An infection with Campylobacter spp may lead to impaired defence and susceptibility to other pathogens which may result in greater intestinal excretion. Poor welfare and high growing rate lead to digestive troubles that lead to litter humidity. Litter humidity that, among other things, causes footpad dermatitis may also influence the horizontal transmission of the Campylobacter spp. infection due to the normal coprophagic behaviour of poultry. Reducing welfare problems by a better management of rearing conditions would not only improve broiler welfare, but it would also decrease the risks of Campylobacter contamination, of carcass condemnations and of economic loss for the poultry industry.

Dust exposure and health of workers in duck hatcheries.

OBJECTIVES: The objectives of this cross-sectional study were to investigate dust exposure and respiratory health of workers in duck hatcheries in western France. MATERIAL AND METHODS: Ninety volunteer workers, who work in sorting rooms and/or incubation rooms, participated in exposure assessments and medical examinations. Medical examinations were performed by occupational health practitioners.They filled-in a questionnaire with the workers, followed by a lung function test on each worker. General characteristics and prevalence of chronic respiratory symptoms were described in each type of working rooms. Associations between symptoms and exposure (working room or dust level) were studied in GEE multivariate models. RESULTS: Overall prevalence of chronic respiratory symptoms (cough, phlegm) and chronic bronchitis were similar or lower than in the reference population. However, prevalence of these symptoms was higher for those working in sorting rooms, that were associated with an increased risk of respiratory symptoms and decreased lung function. Respirable dust was also significantly associated with an increased risk of respiratory symptoms. The prevalence of asthma and rhinitis were well above those in the reference population, but did not vary among working rooms. Descriptive data suggested an occupational origin for some cases. CONCLUSIONS: Hatchery workers were at increased risk of compromised respiratory health due to dust exposure, particularly those who work in sorting rooms. Asthma and rhinitis were in excess in this population of workers. Thorough clinical examination of these workers should be performed and all exposures assessed.

Hens can ingest extruded polystyrene in rearing buildings and lay eggs contaminated with hexabromocyclododecane.

The overall concentration of hexabromocyclododecane (HBCDD) in eggs is low although abnormally high concentrations exceeding 3000 ng g-1 lw have been reported. In order to test whether these contaminations may originate from the ingestion of insulating materials in rearing buildings, a group of 55 hens raised in a collective cage was provided with a 64-g piece of extruded polystyrene (XPS, 2.59% HBCDD of which 75, 15 and 10% as α-, ß- and γ-HBCDD, respectively). Hens entirely consumed the piece within 3 days, leading to a mean daily exposure of 4.7 mg HBCDD per kg body weight. Whole egg HBCDD concentration reached a maximum of 1037 ng HBCDD g-1 fresh weight (fw), recorded 2 days after the piece had disappeared, and decreased down to 86 ng g-1 fw within the 19 following days. In all these samples, HBCDD was made of 98.7 ± 0.7 and 1.3 ± 0.6% α- and ß-HBCDD, respectively, and 0.1% γ-HBCDD when quantified; it was enriched in (-)α- and (+)ß-HBCDD with enantiomeric fractions of 0.438 ± 0.009 and 0.579 ± 0.030, respectively. HBCDD was quantified in all the individual eggs collected the last day of experiment at concentrations ranging between 0.47 and 1361 ng g-1 fw, according to a lognormal distribution. The ingestion of XPS in degraded rearing buildings is thus a plausible cause of on-farm egg contamination by HBCDD which should be strictly avoided.

Effect of Feed Additives on Productivity and Campylobacter spp. Loads in Broilers Reared under Free Range Conditions.

The poultry reservoir, especially broiler meat, is generally recognized as one of the most-important sources for human Campylobacteriosis. The measures to control Campylobacter targeted essentially the primary production level. The aim of this work was to evaluate the effectiveness of different treatments against natural Campylobacter colonization in a French experimental farm of free-range broilers during the whole rearing period. Five commercial products and a combination of two of them were tested and all the products were added to feed or to water at the dose recommended by the suppliers. Campylobacter loads in caeca and on carcasses of broilers at the slaughter were determined by culture methods. Natural contamination of the flock occurred at the end of the indoor rearing period between day 35 and day 42. At day 42, the multispecies probiotic added to the feed reduced the contamination of 0.55 log10 CFU/g (p = 0.02) but was not significant (p > 0.05) at the end of rearing at day 78. However, another treatment, a combination of a cation exchange clay-based product in feed and an organic acid mixture (formic acid, sodium formate, lactic acid, propionic acid) in water, led to a slight but significant reduction of 0.82 ± 0.25 log10 CFU/g (p = 0.02) compared to the control group at day 78. Testing this combination in field conditions in several flocks is needed to determine if it is biologically relevant and if it could be a valuable measure to reduce Campylobacter in broiler flocks.

Enantiomer-specific accumulation and depuration of α-hexabromocyclododecane (α-HBCDD) in chicken (Gallus gallus) as a tool to identify contamination sources.

A LC-ESI(-)-HRMS method dedicated to the analysis of 6 HBCDD enantiomers at trace levels in animal matrices was developed, using a cellulose based stationary phase with a particle size of 2.5 µm. This method was applied to a sample set derived from a kinetic study of α-HBCDD previously conducted in fast- and slow-growing chickens (Gallus gallus domesticus, n = 49, plus controls), in order to study the enantiomer specific accumulation and depuration of α-HBCDD in various tissues. Regarding abdominal adipose tissue, muscle and liver, the average enantiomeric fractions of α-HBCDD (EFα) for continuously exposed groups ranged between 0.434 and 0.467, with standard deviations below 0.014, showing a significant enrichment in (-)α enantiomer even accentuated for slow growing individuals during depuration with EFα reduced by about 0.020. Similar trends were observed for pooled plasma. Then, EFα of circulating plasma α-HBCDD appeared to closely reflect EFα in storage tissues and liver, suggesting some equilibrium. The racemic elimination of α enantiomer in excreta during the contamination phase indicated that no preferential gastrointestinal absorption took place. By contrast, preferential excretion of (-)α-HBCDD from the circulating compartment to the intestinal lumen occurred during the depuration. Finally, the method was applied to samples collected in three chicken farms, selected for total HBCDD levels in muscle in the ng/g range, as a tool to determine whether the contamination occurred ante- or post-mortem, according to the chiral signature. Ante-mortem contamination was hypothesised for 2 farms, with feed being excluded as contamination source.

Risk factors for Listeria monocytogenes contamination in French laying hens and broiler flocks.

The objective of this study was to identify potential risk factors for Listeria monocytogenes contamination in French poultry production. Eighty-four flocks of layer hens kept in cages and 142 broiler flocks were included in this study. For each production type, a questionnaire was submitted to farmers and fecal samples were taken to assess the L. monocytogenes status of the flocks during a single visit to the farm. Two logistic regression models (specific to each production) were used to assess the association between management practices and the risk of L. monocytogenes contamination of the flock. The prevalence of L. monocytogenes-positive flocks was 30.9% (95% CI: 21.0; 40.9) and 31.7% (95% CI: 24.0; 39.4) for cage-layers and broiler flocks, respectively. For layer flocks, the risk of L. monocytogenes contamination was increased when pets were present on the production site. When droppings were evacuated by conveyor belt with deep pit storage, the risk of L. monocytogenes contamination decreased significantly. Feed meal was found to be associated with a higher risk of L. monocytogenes contamination than feed crumb. For broiler flocks, the risk of L. monocytogenes contamination was increased when farmers did not respect the principle of two areas (clean and dirty) at the poultry house entrance. A first disinfection by thermal fogging and the absence of pest control of the poultry house before the arrival of the next flock was found to increase the risk of contamination. When litter was not protected during storage and when farm staff also took care of other broiler chicken houses, the risk of L. monocytogenes contamination increased significantly. In the case of the watering system, nipples with cups were found to decrease the risk of contamination.

Isolation of Salmonella enterica in laying-hen flocks and assessment of eggshell contamination in France.

The present investigation was conducted in conjunction with the European Union baseline study for the estimation of Salmonella prevalence in laying-hen flocks. It aimed at evaluating eggshell contamination in farms positive for Salmonella, characterizing the genetic patterns of Salmonella strains and identifying the factors associated with Salmonella contamination of eggshells. For this purpose, a total of 4,200 eggs were collected from 28 positive flocks and analyzed according to draft Annex D of International Organization for Standardization Method 6579. Molecular characterization of the Salmonella strains was obtained by the pulsed-field gel electrophoresis method with two restriction enzymes, XbaI and BlnI. The relationship between the presence of Salmonella on eggshells and rearing practices was studied by using multiple correspondence analysis. Results showed that 39.3% of the positive flocks had at least one positive eggshell, with a total of 1.05% of eggshells testing positive for Salmonella. We detected the same serovars on samples taken from the farm and from eggshells within a given flock, with isolates sharing the same genetic pattern in 7 of 11 flocks. Eggshells tested positive for Salmonella in flocks (i) located where delivery trucks pass near air entrances of the poultry house, (ii) with high holding capacity (>30,000 laying hens), and (iii) with more than five positive samples coming from the farm environment, as well as in cases of flocks with a maximum egg-laying rate of >96% and in cases where farmers worked in other animal production. This study provided valuable information that could be used for risk management and risk assessment studies.

Risk factors for Salmonella enterica subsp. enterica contamination in 519 French laying hen flocks at the end of the laying period.

A cross-sectional study was carried out to identify risk factors for Salmonella spp. contamination in French laying hen flocks at the end of the laying period. Five hundred and nineteen flocks were studied between October 2004 and September 2005. The Salmonella status of the flocks was assessed from 5 faeces samples (pooled faeces samples from cage flocks and foot swabs from flocks kept on the floor, i.e. in a barn, outdoors and on organic farms) and 2 dust samples analysed using a classical bacteriological method. At least one contaminated sample was found in 93 flocks and the apparent prevalence of Salmonella was 17.9% (CI 95%=14.5, 21.3). Prevalence was significantly higher in caged flocks than in on-floor flocks and logistic-regression models were built for each subpopulation. Associations between farm characteristics, managerial practices and the presence of one or more Salmonella-positive samples in a flock were assessed using a mixed logistic-regression model with a flock-specific random effect. In caged flocks (n=227) the risk of Salmonella contamination increased with flock size and when delivery trucks passed near poultry-house entrances. The risk of detecting a positive sample was lower with pooled faeces samples than with dust samples. In on-floor flocks (n=292), a higher risk of contamination was associated with multistage management (presence of hens of different ages on the farm) and contamination by Salmonella Enteritidis of a previous flock kept on the farm. However, the use of a container for dead bird disposal was a protective factor.