Do farming conditions influence brominated flame retardant levels in pig and poultry products?

Brominated flame retardants (BFR) are primarily used as flame retardant additives in insulating materials. These lipophilic compounds can bioaccumulate in animal tissues, leading to human exposure via food ingestion. Although their concentration in food is not yet regulated, several of these products are recognised as persistent organic pollutants; they are thought to act as endocrine disruptors. The present study aimed to characterise the occurrence of two families of BFRs (hexabromocyclododecane (HBCDD) and polybrominated diphenyl ethers (PBDE)) in hen eggs and broiler or pig meat in relation to their rearing environments. Epidemiological studies were carried out on 60 hen egg farms (34 without an open-air range, 26 free-range), 57 broiler farms (27 without an open-air range, 30 free-range) and 42 pig farms without an open-air range in France from 2013 to 2015. For each farm, composite samples from either 12 eggs, five broiler pectoral muscles or three pig tenderloins were obtained. Eight PBDE congeners and three HBCDD stereoisomers were quantified in product fat using gas chromatography-high-resolution mass spectrometry, or high-performance liquid chromatography-tandem mass spectrometry, respectively. The frequencies of PBDE detection were 28% for eggs (median concentration 0.278 ng/g fat), 72% for broiler muscle (0.392 ng/g fat) and 49% for pig muscle (0.403 ng/g fat). At least one HBCDD stereoisomer was detected in 17% of eggs (0.526 ng/g fat), 46% of broiler muscle (0.799 ng/g fat) and 36% of pig muscle (0.616 ng/g fat). Results were similar in concentration to those obtained in French surveillance surveys from 2012 to 2016. Nevertheless, the contamination of free-range eggs and broilers was found to be more frequent than that of conventional ones, suggesting that access to an open-air range could be an additional source of exposure to BFRs for animals. However, the concentration of BFRs in all products remained generally very low. No direct relationship could be established between the occurrence of BFRs in eggs and meat and the characteristics of farm buildings (age, building materials). The potential presence of BFRs in insulating materials is not likely to constitute a significant source of animal exposure as long as the animals do not have direct access to these materials.

Feather pecking in laying hens housed in free-range or furnished-cage systems on French farms.

1. Beak trimming is currently used in France to avoid the negative consequences of severe feather pecking (SFP). However, this practice is controversial in terms of animal welfare, and forbidden in some European countries.2. This study aimed to assess the prevalence of SFP in French laying hen farms, to describe how farmers manage this behavioural disorder and to better understand the risk factors involved.3. A study was carried out from April 2015 to June 2016. Visits were paid to 79 flocks kept in furnished cages (FC) and 80 flocks in a free-range (FR) system. All the hens had trimmed beaks and were genotypically brown. The information collected included feather cover, skin damage, beak condition, farm and poultry house characteristics, livestock performance and management.4. The prevalence of SFP in FC flocks was estimated at 32.9% (IC = 95%, [22.5; 43.3]) and the prevalence of cannibalism as 2.5% (IC = 95%, [0.7; 8.8]) at 70 weeks of age. The prevalence of SFP in FR flocks was estimated to be 23.8% (IC = 95%, [14.5; 31.1]) and the prevalence of cannibalism was 8.8% (IC = 95%, [4.3; 17.0]) at 61 weeks of age.5. In FC flocks, SFP was associated with the combination of genotype, type and length of perches, cage area per hen, type of lighting, number of hens per cage and farm location. In FR flocks, feather cover was associated with use of the outdoor run, lighting programme, genotype, farm location and date of house construction.

Exposure to inhalable dust of workers shackling birds frequently exceeds occupational exposure level in abattoirs in Western France.

1. The objectives of this study were to measure the exposure of workers to dust when shackling poultry in abattoirs, and to identify the most effective measures to prevent human exposure to dust. The relationship between respiratory health of workers and their occupational exposure to dust was assessed. 2. Exposure to dust (aerial particles inhaled through the nose and mouth) exceeded the occupational exposure limit (maximum 10 mg/m3 over 8 h) in 65 out of 109 workers from 27 abattoirs, in the context of high levels of ambient aerial dust in small, closed shackling cubicles. Ceiling air ducts for supply of air reduced worker exposure to dust in these buildings. 3. Two-thirds of the 86 workers interviewed reported work-related respiratory symptoms. The self-reported risk of suffering from coughing tended to be associated with the highest exposure to inhalable dust and respiratory dust (aerial particles penetrating up to alveoli) observed in the study. 4. The present study demonstrates that workers may be exposed to considerable amounts of dust when shackling birds before stunning.

Investigation of a type C/D botulism outbreak in free-range laying hens in France.

In 2014, a botulism outbreak in a flock of laying hens was investigated in France. In the flock of 5020 hens, clinical signs of botulism occurred at 46 weeks of age. A type C/D botulism outbreak was confirmed using the mouse lethality assay for detection of botulinum toxin in serum and a real-time PCR test to detect Clostridium botulinum in intestinal contents. The disease lasted one week with a mortality rate of 2.6% without recurrence. Botulism in laying hens has rarely been reported. Five monthly visits were made to the farm between December 2014 and May 2015 for a longitudinal study of the persistence of C. botulinum in the poultry house after the outbreak, and to assess egg contamination by C. botulinum. Several samples were collected on each visit: in the house (from the ventilation circuit, the egg circuit, water and feed, droppings) and the surrounding area. Thirty clean and 30 dirty eggs were also swabbed at each visit. In addition, 12 dirty and 12 clean eggs were collected to analyse eggshell and egg content. The samples were analysed using real-time PCR to detect type C/D C. botulinum. The bacterium was still detected in the house more than 5 months after the outbreak, mostly on the walls and in the egg circuit. Regarding egg contamination, the bacteria were detected only on the shell but not in the content of the eggs. Control measures should therefore be implemented throughout the egg production period to avoid dissemination of the bacteria, particularly during egg collection.

Aerial dust concentration in cage-housed, floor-housed, and aviary facilities for laying hens.

Agricultural workers, and pig and poultry farmers in particular, are exposed to airborne contaminants including organic dusts, gases, fungi, bacteria, and endotoxins that can have adverse effects on their respiratory health. To date, data comparing the aerial dust concentrations in the different hen-housing systems used by commercial poultry farmers are scarce. An epidemiological study was conducted in commercial housing facilities for laying hens, half of which were housed in a cage system without litter and the remaining half on an on-floor system with litter. The aims were to measure and compare the ambient dust concentrations in the different housing systems and identify any factors in building design and hen management that could influence the dust burden. An average concentration of respirable ambient dusts (≤4 µm) of 0.37 mg/m(3) (95% CI [0.31-0.42]) was measured in the on-floor system, and this value was higher than average values in the cage system {0.13 mg/m(3) (95% CI [0.11-0.14]) P = 0.01}. The highest dust concentration was observed in aviaries (1.19 mg/m(3) [0.80-1.59]). The type of housing and the presence of litter therefore had a preponderant effect on air quality. Dust concentrations in caged buildings were influenced by cage design and rearing practices, whereas litter management, the age of hens, and temperature control were determining factors for dust levels in on-floor houses. This study underlines the need for information and preventive measures to reduce the exposure of poultry workers to bioaerosols, particularly in alternative systems where high levels of ambient dust were observed.

Risk factors for the introduction of avian influenza virus in breeder duck flocks during the first 24 weeks of laying.

A study was carried out in French breeder duck flocks in 2008 and 2009 to identify practices and events related to the introduction of avian influenza viruses (AIVs). The status of flocks was assessed using serological methods for all subtypes of AIV without typing. Flocks managed with both natural mating and artificial insemination were investigated every 4 weeks from the beginning of the laying period up to seroconversion or for a maximum of 6 months. A questionnaire was completed with the farmer during each visit and 20 female ducks were randomly sampled for blood testing. Only flocks that tested seronegative at the first visit were included in the study (n =151 flocks managed with natural mating or artificial insemination). Data were analysed using survival analysis to identify factors influencing the time to seroconversion. Three separate models were constructed: one for the whole sample, one for natural mating flocks, and one for artificial insemination flocks. Factors related to the time to introduction of AIV included the type of production system linked to artificial insemination practices, the neighbourhood, poor disinfection practices, liquid manure management, presence of wildlife, and vehicles entering the building. No clear relationship could be observed in the serological status of male and female ducks in farms keeping male ducks separately from female ducks for artificial insemination. By respecting carefully biosecurity measures, it should be possible to decrease AIV infection of breeder duck flocks.

Bayesian network as an aid for Food Chain Information use for meat inspection.

Current ante mortem inspection involves a check of relevant Food Chain Information (FCI) transmitted by the farmer to the slaughterhouse on a regulatory FCI document. Since 2000, a farm sanitary form with FCI data has been used for all consignments of broiler chickens in France. However, the FCI needs to be standardized for the collection and interpretation of data. A study was conducted to develop an expert system, undertaken to elaborate on a simple decision support system capable of predicting whether the flocks will present a high condemnation risk, based on FCI. For this, 'optimal' (i.e. on-farm survey data) and 'worthy' (i.e. farmers' declaration on existing farm sanitary form) data quality conditions were considered to estimate the lower and upper reference bounds of the confidence that the decision-makers could have in such a tool. Chicken broiler flocks (404) were randomly selected in 15 slaughterhouses located in Western France in 2005. Condemnation proportion and farm sanitary form were collected for each selected flock. Information about health history and technical performances were also specifically collected on farm. Condemnation risk category was modelled from the on-farm collected information, using a Bayesian network and assuming this represented the optimal data quality conditions. Corresponding information declared by the farmer on the existing farm sanitary form was secondly used in the network to evaluate the impact of the uncertainty of such information on the condemnation classification obtained with the expert system. The learnt Bayesian network had 16 explanatory variables pertaining to technical characteristics and sanitary features of the flock. Using a threshold of 1% of condemned carcases to define high risk, the network sensitivity and specificity were 55% and 93%, respectively, corresponding to positive and negative predictive values of 70% and 87%. When declared existing information was used in the network, the sensitivity and specificity were 16% and 96%, respectively, corresponding to positive and negative predictive values of 57% and 80%. Results suggested that the predictive network developed may be insufficient for correctly classifying chicken flocks for targeting of management procedures, and in its current form, the expert system may be unlikely to be implemented in the field. However, it could help to improve the standardization of both form design and FCI interpretation at a national level.

Endotoxin concentration in poultry houses for laying hens kept in cages or in alternative housing systems.

Endotoxins as components of organic dust may have adverse effects on the respiratory health of workers in poultry buildings. The move towards more welfare-friendly housing systems for layers may increase worker exposure to air contaminants due to the use of litter. The endotoxin concentrations in the inhalable fraction of airborne dust (below 100 µm) from cage and alternative system houses (on-floor, free range and aviaries) were compared under both experimental and commercial conditions. The endotoxin concentration was higher in experimental aviaries (median: 565 EU/m³, range: 362-1491 EU/m³) than in cage housing (98 EU/m³ (51-470)). In field conditions, the endotoxin concentration in the air of 13 alternative houses was higher (35 to 3156 EU/m³) than in cage system buildings (n = 8, 78-576 EU/m³). It was correlated to the respirable dust concentration (fraction below 5 µm) and to the temperature inside the hen house but no seasonal variation was observed. The present study emphasises that considerable worker exposure to endotoxins may occur in laying houses, especially in alternative systems.

Factors associated with mortality of broilers during transport to slaughterhouse.

In recent years, broiler mortality during transport to the slaughterhouse has become a cause for concern because of animal welfare considerations and associated economic losses. A descriptive and analytical epidemiological study was carried out to estimate the extent of DoA in poultry broiler production in the main producing regions of France and to determine factors influencing the DoA rate. Data regarding animal characteristics and rearing, catching, transport and lairage conditions were collected on farm and at the slaughterhouse for 404 chicken broiler flocks processed during 2005. The average DoA rate was 0.18% (from 0% to 1.4%). Variables found to be associated (P < 0.05) with the DoA rate in a multivariable negative binomial model were flock cumulative mortality on farm, the catching system (mechanical being more at risk than manual), the density in crates (more space allowance being associated with less mortality) and climatic conditions (rain and wind being associated with more DoA). Mortality during transport is thus related to all production steps from the farm to the slaughterhouse. Efforts have therefore to be made by all professionals to contain mortality on farm and during catching and transportation.

Factors influencing bacterial eggshell contamination in conventional cages, furnished cages and free-range systems for laying hens under commercial conditions.

1. The aim was to assess eggshell contamination in various laying hen-housing systems and to identify factors influencing this contamination. 2. Fifty-eight laying hen farms in France were studied, including 21 flocks housed in conventional cages, 7 in furnished cages and 30 kept on-floor. 3. Sixty eggs per flock were analysed to obtain counts of the total mesophilic flora. Data on equipment and hen management were collected. 4. Mean bacterial count on eggshells tended to be higher in on-floor systems (4.82 +/- 0.51 log CFU/eggshell) than in cage systems (4.57 +/- 0.58 log CFU/eggshell, P = 0.09). 5. Contamination increased with age of the hens, airborne dust concentration, manual packing of the eggs, and packing in plastic rather than in recycled-pulp egg-flats. 6. The effect of the housing system on eggshell contamination, previously described in experimental assays, was confirmed under production conditions.

Evaluation of common cleaning and disinfection programmes in battery cage and on-floor layer houses in France.

1. The aim in this study was to evaluate cleaning and disinfection programmes in battery cage and on-floor layer houses in France. 2. Cleaning and disinfection efficiency was assessed by a visual evaluation of cleaning and a bacteriological monitoring of surface contamination from counts of thermotolerant streptococci on contact agar plates. 3. In battery cage houses, dropping belts, manure conveyors, and house floors remained highly contaminated due to poor cleaning in half of the buildings examined. 4. In on-floor houses, a high standard of cleaning was achieved but errors in the planning of cleaning and disinfection operations sometimes led to a high residual contamination of nest boxes and egg sorting tables.

Risk and indicators of condemnation of male turkey broilers in western France, February-July 2006.

A field study was conducted to estimate the sanitary condemnation proportion in male turkey broiler flocks, to describe the reasons for condemnation and the related macroscopic lesions, and to investigate whether primary production information would predict the risk of condemnation. Male turkey standard broiler flocks (117) were randomly selected in the 13 slaughterhouses located in Western France, from February to July 2006. The flocks were monitored from their arrival at the slaughterhouse until the results of the post mortem sanitary inspection. Information about rearing conditions, health history, catching and loading conditions, transportation to the slaughterhouse and slaughtering was also collected. Sampling design was considered in the calculations and the condemnation proportion was modelled using a negative binomial regression, accounting for clustering within slaughterhouse. The within-flock weighted average condemnation proportion was 1.8% (95% confidence interval, 1.3-2.3%). Emaciation, arthritis-polyarthritis and congestion were the main reported official reasons for condemnation, representing 76% of the condemned carcases. Three variables were significantly associated with increased risk of condemnation: observed locomotor disorders on the farm, high cumulative mortality 2 weeks before slaughter, and clinical signs observed by the Veterinary Services during the ante mortem inspection at the slaughterhouse. The final model explained 35% of the total variation in condemnation risk. Half of this explained variation could be attributed to locomotor disorders observed during rearing. The sensitivity and specificity of the model to predict a high flock condemnation risk were 80% and 74%, respectively, when using an optimum threshold of 0.95% to define high risk. The results of this study suggested that the variables found to be associated with condemnation proportion were markers of increased risk and could be used as indicators. These risk indicators can easily be retrieved from the pre-existing regulatory document transmitted before flock arrival at the slaughterhouse and could be used to screen flocks before slaughter, according to their expected risk of condemnation.

Risk factors for sanitary condemnation in broiler chickens and their relative impact: application of an original multiblock approach.

An innovative and well-adapted statistical method, called multiblock redundancy analysis, is proposed for a complex health-event analysis to account for the thematic block organization of variables. The outcome block contained the condemnation rates of 404 broiler chicken flocks, distinguishing infectious and traumatic condemnation categories. Explanatory variables were organized in blocks related to the different production stages (farm structure and routine husbandry practices; on-farm flock history and characteristics; catching, transport and lairage conditions; slaughterhouse and inspection features). The aim was to determine risk factors for both condemnation categories, and the relative impact of the different production stages on the whole condemnation rate. Results showed that significant factors were either specific to one condemnation category or related to both categories, and each of the explanatory blocks was involved in the explanation of infectious and traumatic condemnation rates. On-farm flock information explained 40% of the overall condemnation process whereas the other explanatory blocks had similar relative impacts.

Feasibility of screening broiler chicken flocks for risk markers as an aid for meat inspection.

The feasibility of using risk markers to screen broiler chicken flocks and anticipate their risk of condemnation at meat inspection was examined in 404 randomly selected flocks in 15 French slaughterhouses in 2005. Condemnation rate and information about rearing conditions, health history, catching and loading, transport and slaughtering were collected. The Poisson regression model of the condemnation rate consisted of six simple and biologically relevant predictors: production type, frequency of farmer's visits during the starting period, health disorders during rearing, on-farm mortality, mortality during transport, and slaughter-line speed. Although accurate prediction of the condemnation rate for a given flock was not feasible, flocks with low or high risk of condemnation could be distinguished. These findings could be useful at various stages of chicken production, to monitor and improve farm husbandry practices, minimize the impact of transport conditions, and optimize meat inspection procedures.

Diversity of pulsed-field gel electrophoresis profiles of Campylobacter jejuni and Campylobacter coli from broiler chickens in France.

In 2003 to 2004, 26 free-range broilers flocks excreting Campylobacter were studied for identification of Campylobacter species and genotype diversity. Seventeen flocks were sampled at the end of the indoor rearing period and 9 before departure to the slaughterhouse after access to an open area. Out of 513 isolates, 315 were identified as Campylobacter jejuni and 198 as Campylobacter coli. Pulsed-field gel electrophoresis analysis revealed 35 genotypes for C. jejuni and 43 genotypes for C. coli; 38.4% of the isolates were clustered into 16 genetic groups. This kind of poultry production system is characterized by a large number of Campylobacter coli isolates. Flocks sampled during the indoor phase were predominantly contaminated by C. jejuni, whereas those sampled during warm months were predominantly contaminated by C. coli. The Campylobacter population was genetically highly diverse: multiple genotypes were detected in a single flock. Six flocks were each found to harbor a mixture of genotypes; these isolates were genetically closely related and were grouped into clusters of at least 80% genetic similarity. Isolates with genotypes found in different flocks and strains, but sharing the same genetic clusters, were detected in different farms and at different times in the year. Flocks sampled during the indoor rearing period and when farmers use fresh farm-made litter were associated with a small number of clusters. In conclusion, Campylobacter species were genetically highly diverse. Our findings suggest the presence of genomic rearrangements in Campylobacter colonizing the chick intestine and that some Campylobacter strains are adapted to poultry. In addition, the species diversity in the flocks was affected by season and cloistering measures. Litter and exposure to an open area were likely sources of flock Campylobacter contamination.

Postmortem condemnations of processed broiler chickens in western France.

A total of 404 broiler chicken flocks processed in 15 slaughterhouses in western France were studied to estimate the condemnation prevalence and describe the official reasons for condemnation and the main macroscopic lesions observed in a sample of the condemned carcases. The condemnation rate was 87 per 10,000 birds slaughtered (95 per cent confidence interval 79 to 95 per 10,000) but differed significantly according to the type of poultry produced (standard, light, heavy or certified). The main reasons for condemnation were emaciation and congestion, with rates of 30 and 22 per 10,000 birds slaughtered, respectively. Congestion was significantly associated with arthritis and ascites, whereas infected skin lesions were associated with bruises and abnormalities of colour, odour or conformation.

Risk factors for Campylobacter spp. colonization in French free-range broiler-chicken flocks at the end of the indoor rearing period.

The aim of this cross-sectional survey was to identify risk factors for Campylobacter spp. colonization in French free-range broiler flocks at the end of the indoor rearing period (between 35 and 42 days old). Seventy-three broiler farms were studied from March 2003 to March 2004 in France. A questionnaire was administered to the farmers and samples of fresh droppings were taken to assess the flocks'Campylobacter status by bacteriology. Campylobacter species were determined by PCR. A logistic regression analysis was used to assess the influence of various factors on flocks'Campylobacter status. 71.2% of the sampled flocks excreted Campylobacter spp. before going out on the range. The risk of a flock being colonized with Campylobacter was increased in the spring/summer period (RR=1.8, p=0.02) and autumn (RR=2.2, p=0.02) compared to winter, on total freedom rearing farms (RR=3.3, p=0.04) in comparison with farms with a fenced run, when the first disinfection of the poultry-house was performed by the farmer (RR=2.4, p=0.04) instead of a hygiene specialist, when rodent control was carried out by a contractor (RR=1.8, p<0.01) and not by the farmer and when the farmer came into the house twice a day as opposed to three time a day or more (RR=1.5, p=0.02). Use of a specific gate for chick placement decreased the risk of a flock being colonized with Campylobacter (RR=0.5, p=0.01) in comparison with using the gate for manual disposure or the door of the change room.