ANIMAL WELL-BEING AND BEHAVIOR

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1 ANIMAL WELL-BEING AND BEHAVIOR Broiler chickens dead on arrival: associated risk factors and welfare indicators Leonie Jacobs,, Evelyne Delezie, Luc Duchateau, Klara Goethals, and Frank A. M. Tuyttens,,1 Animal Sciences Unit, Institute for Agricultural and Fisheries Research (ILVO), Scheldeweg 68, 9090 Melle, Belgium; and Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium ABSTRACT The pre-slaughter phase of the production risk factors for DOA% were identified, both related to process has potentially important animal welfare implications, including mortality (recorded as Dead on Arrivals ; DOA). To reduce DOA%, specific risk factors need to be identified. DOA% can also be used as a first and quick screening of pre-slaughter broiler welfare under commercial conditions. The aim of the present study was to identify risk factors for DOA% in commercial broiler flocks and to find associations between DOA% and animal-based indicators of broiler welfare during the pre-slaughter phase. Eighty-one transported flocks to five slaughter plants were assessed. Farmers provided information on the flock and observers gathered data on pre-slaughter factors. DOA% was recorded by slaughter plant personnel. The association between risk factors and DOA% was tested using linear mixed models, with slaughter plant as the random effect. Mean (± SE) DOA% was 0.30 ± 0.05% and median was 0.19% (range 0.04 to 3.34%). Two flock health status during the production phase. Higher DOA% was found when farmers did not check chick qualityuponarrival(p = 0.011), although one extreme DOA% caused this significant effect. In addition, onfarm mortality during production (including selective culling) was negatively associated with DOA% (P = 0.011), potentially due to the selective culling on farm. Further research is needed on the impact of on-farm health status on welfare during the pre-slaughter phase, as the current study provided some evidence that onfarm factors are linked to mortality during the preslaughter phase. No specific characteristics of the preslaughter phase could be identified as risk factor for increased mortality. DOA% was positively associated with five welfare indicators, including indicators of thermal stress, which indicates the potential to use DOA% as a quick, cost-efficient screening tool for those welfare aspects. Key words: broiler welfare, mortality, DOA, risk factor, pre-slaughter phase 2017 Poultry Science 96: INTRODUCTION Globally, 44 billion broiler chickens are produced every year (Compassion in World Farming, 2016), 200 million of which are produced in Belgium. Broilers are processed in Belgium at an average slaughter age of 35 days (thinning) or 41 days (Tuyttens et al., 2014) and then caught and loaded on-farm, transported, unloaded, and kept in lairage at the slaughter plant. This pre-slaughter phase is a critical and stressful phase of the production process, with potentially serious animal welfare problems and economic implications (Nijdam et al., 2004). The pre-slaughter process subjects birds to handling, noise, vibration, thermal challenges, feed and water withdrawal, unfamiliar environments, high stocking density, and social disruption (EFSA, 2011). C 2016 Poultry Science Association Inc. Received March 18, Accepted August 17, Corresponding author: frank.tuyttens@ilvo.vlaanderen.be These potential stressors can result in damage and even death, possibly more so when flocks are in poor health. Mortality during the pre-slaughter phase is usually expressed as percentage dead on arrival (DOA%). Several studies have investigated DOA% as a key indicator of broiler welfare during the pre-slaughter phase (Table 1). Reported risk factors for DOA% include on-farm characteristics such as flock size and vaccination regime, and pre-slaughter characteristics such as catching method, season, weather conditions, and duration of transportation and lairage (Warriss et al., 1992; Nijdam et al., 2004; Ritz et al., 2005; Warriss et al., 2005; Petracci et al., 2006; Vecerek et al., 2006; Haslam et al., 2008; Chauvin et al., 2011; Table 1). DOA% varies considerably between studies, with means ranging from 0.11 to 0.68% (Table 1). This wide range warrants further investigation as the differences might be due to either variation in the health status and condition of the flocks transported, pre-slaughter circumstances, or methods used (e.g., the precise period of the pre-slaughter phase during which DOA% was recorded). 259

2 260 JACOBS ET AL. Table 1. Literature overview showing reference, country of study, experimental design (exp. design) with data collection method, sample size (n), mean dead on arrival (DOA) percentage and range, and identified risk factors. Reference (country) Exp. design (data collection) n DOA % (range %) Risk factors identified Visser et al. (2014) (Netherlands) Chauvin et al. (2011) (France) Haslam et al. (2008) (United Kingdom) Petracci et al. (2006) (Italy) Vecerek et al. (2006) (Czech Republic) Ritz et al. (2005) (United States) Warriss et al. (2005) (England) Nijdam et al. (2004) (Netherlands) Warriss et al. (1992) (England) Epidemiological (animal-based measurements) 1 11 flocks 0.11 (0.04 to 0.26) Outside the scope of the study Epidemiological (survey, interviews, 403 flocks 0.18 (0.00 to 1.40) Large flocks; high on-farm measurements) 2 mortality; high and low slaughter weight; mechanical catching (vs. manual); prolonged catching; high crate stocking density; rain and wind; Oct April transportation; prolonged lairage Epidemiological (records, 206 flocks 0.12 (0.00 to 0.64) Hybrid; more small or emaciated measurements) 3 birds; high on-farm mortality; fewer vaccinations; less wheat in the diet; summer transportation Epidemiological (records) million broilers 0.35 (0.04 to 2.00) Summer transportation Epidemiological (records) 3 Unknown 0.25 (unknown) Long-distance transportation; summer and winter transportation Experimental (measurements) 1 24 trucks 0.68 (unknown) Not within their scope Epidemiological (records) 3 60 million broilers 0.13 (0.03 to 3.10) High ambient temperature Epidemiological (unclear) 2 1,907 flocks 0.46 (0.00 to 16.61) Large flocks; hybrid; high slaughter weight; catching crew; high crate stocking density; long transportation; morning and daytime transportation; high and low ambient temperatures; prolonged lairage Epidemiological (records) 3 1,113 trucks 0.19 (0.00 to 15.80) High crate stocking density; long transportation 1 DOAs were counted (from a sample). 2 Not clear how DOA% were obtained. 3 DOA% were collected from slaughter plant records. Flock characteristics and pre-slaughter aspects such as duration of transportation and stocking density can be considered as potential risk factors, while mortality can be considered to be the animal s response to (or the consequence of) these risk factors (EFSA AHAW Panel, 2012). Few pre-slaughter studies have focused on other animal responses or animal-based welfare indicators beyond DOA%, and the link between these responses and mortality is unclear. DOA% could perhaps be used as a first and quick screening of pre-slaughter broiler welfare under commercial conditions, and particularly so if DOA% is linked with other indicators of broiler welfare during the pre-slaughter phase. Furthermore, the relationship between DOA% and these other welfare indicators could reveal potential causes for mortality. Visser et al. (2014) recently assessed the welfare of 11 Dutch broiler flocks from catching until stunning. Panting (1.1 to 6.5% of the birds) and wing fractures (1 to 4.8% of the birds) were the most frequently observed animal-based welfare problems (Visser et al., 2014). However, no associations between DOA% and these welfare indicators were identified. The aim of the current study is to (1) identify flock and pre-slaughter risk factors for DOA% in commercial broiler transportation, and (2) find associations between DOA% and other (animal-based) welfare indicators assessed during the pre-slaughter phase. MATERIAL AND METHODS Study Population In 2013 and 2014, we assessed 81 commercially transported flocks from 52 conventional broiler farms, representing approximately 10% of all Belgian farms, to five slaughter plants in Belgium. Together, these slaughter plants process approximately 60% of the broilers in Belgium (Table 2). Transports took place in spring (n = 14), summer (n = 34), autumn (n = 10), or winter (n = 25), with a mean ambient temperature of 12.4 C (range 0.1 to 33.9 C). Broiler chickens were either Ross (n = 74), Cobb (n = 3), or other or unknown breeds (n = 4). For ease of observation, farms were selected based on the number of broilers transported: at least 3 trucks, ca. 18,000 broilers. The broilers were caught mechanically (n = 8 flocks), manually by professional catching companies (n = 47 flocks), or manually by non-professional acquaintances of the farmer (n = 26 flocks). Broilers were then transported in vehicles with plastic (n = 50 flocks) or metal container modules (n = 31 flocks), which both hold 8 to 12 transportation crates per container, by 1 of 4 transportation companies (company A: n = 13; B: n = 43; C: n = 3; D: n = 22 flocks). Upon arrival at the slaughter plant, the containers were placed outside with or without a cover (n = 36 flocks) or at an inside lairage area (n = 45 flocks).

3 PRE-SLAUGHTER BROILER MORTALITY 261 Table 2. Means (± SE) or frequency of characteristics of 81 commercially transported flocks per slaughter plant, P-value for slaughter plant effect, with total mean and range. Slaughter plant Total mean 1 (n = 14) 2 (n = 23) 3 (n = 16) 4 (n = 22) 5 (n = 6) P-value (min to max) DOA% 0.54 ± 0.25 a,b 0.44 ± 0.05 a 0.21 ± 0.02 b,c 0.12 ± 0.01 c 0.14 ± 0.02 b,c < (0.04 to 3.34) Carcass rejections (%) 0.56 ± 0.10 a,b 0.30 ± 0.04 a,b 0.56 ± 0.08 a 1.50 ± 0.21 b 0.60 ± 0.13 a,b < (0.06 to 3.77) Slaughter age (d) 41.8 ± 0.3 a 41.3 ± 0.3 a,b 41.9 ± 0.2 a 40.4 ± 0.3 b 40.8 ± 0.6 a,b (38.0 to 45.0) Slaughter weight (kg) 2.73 ± 0.04 a 2.64 ± 0.03 a,b 2.63 ± 0.04 a,b 2.60 ± 0.03 b 2.67 ± 0.06 a,b (1.20 to 3.94) Speed of catching (number of 30.8 ± 5.3 a,b 50.4 ± 17.2 a 22.0 ± 3.6 a,b 19.1 ± 1.7 b 21.2 ± 10.8 a,b (7.4 to 156.1) broilers/catcher/min) Transportation duration (min) 93 ± ± ± ± ± (32 to 300) Lairage duration (min) 291 ± 37 A,B 249 ± 26 A,B 352 ± 35 A 238 ± 27 B 324 ± 59 A,B (15 to 555) Time without feed 1 (min) 972 ± ± ± ± 45 1,095 ± (450 to 1,450) Time without water 2 (min) 477 ± 35 a,c 449 ± 23 a c 524 ± 35 c 348 ± 32 b 428 ± 57 a c (105 to 900) Crate stocking density (kg/m 2 ) 73 ± 2 a,d 61 ± 1 b 72 ± 1 d 66 ± 1 c NA < (52 to 83) Season (freq): spring/summer/ fall/winter 1/7/1/5 5/11/3/4 2/7/4/3 5/5/2/10 1/3/0/2 NA a d Means within a row lacking a common superscript differ (P < 0.05). A,B Means within a row lacking a common superscript tend to differ (P < 0.10). 1 From end of feed provision until start slaughter (some feed may remain in feeders). 2 Equal to the duration of the pre-slaughter phase. After lairage, the containers were tipped over automatically so the birds dropped onto a conveyor belt (n = 31 flocks), or the crates were removed from the container and placed onto a conveyor belt, where birds were manually removed and shackled (n = 50 flocks). Birds were either gas stunned on the conveyor and then their legs were shackled (n = 48 flocks), or they were first shackled and then stunned in an electrified water bath (n = 33 flocks). Data Collection Flock management and pre-slaughter characteristics were recorded for every transported flock of broilers as potential risk factors. The farmer was interviewed during the pre-slaughter process to gather the following information on flock and management characteristics: breed, on-farm mortality (natural mortality and selective culling, %), age (d) at slaughter, and whether day-old chicks had been checked for quality by the farmer upon arrival (yes or no). Furthermore, the following catching, loading, transportation, and lairage conditions were recorded by the observer: slaughter weight (kg), speed of catching and loading (number of broilers per person per min), transportation and lairage duration (min), catching method: professionals catching manually, professionals catching mechanically, or acquaintances catching manually, catching crew (company name), and absence versus presence of farmer during catching. Furthermore, data were collected on the following: on-truck curtain configuration (open, closed, or half open), crate stocking density, feed and water withdrawal duration, lairage ventilation (yes or no), use of water spray and blue light (yes or no), and lairage location (inside or outside). Climatic conditions (ambient temperature, wind speed, sun hours, and precipitation) were obtained from the Royal Meteorological Institute (KMI, Belgium). DOA% and carcass rejections were recorded by slaughterhouse personnel. DOA were defined as birds found dead when removed from the crate at the end of lairage at the slaughter plant. Birds were presumed to have been caught and loaded alive, thus all DOA had presumably died during the pre-slaughter phase. Carcasses unfit for human consumption were removed from the slaughter line by trained veterinary personnel. Reasons for rejection included, but were not limited to, contamination with gut contents, abnormal color, pathological lesions, and emaciation of the carcass. Data on 12 animal-based indicators of broiler welfare during the pre-slaughter phase were collected using a newly developed assessment protocol (Table 3). Indicators from the protocol were based on literature (Welfare Quality R, 2009; EFSA, 2011; Visser et al., 2014) and evaluated for feasibility, validity, and reliability. Welfare was assessed before and after specific stages during the pre-slaughter phase: on-farm just before catching and loading (pre-catch baseline value), on-farm just after catching and loading (post-catch), at the slaughter plant at the end of lairage (ante-mortem), and at the slaughter line after plucking (post-mortem). Most measurements (indicators 1 to 4, 6 to 12) were assessed more than once (Table 3). All indicators were assessed either on the day of slaughter or the night before by 1 of 4 trained observers. Measurements at crate level were performed for 44 ± 3 crates (mean ± SD) per assessment; on average 88 ± 6 crates per transported flock. Containers were randomly selected and marked with tape. All crates from these selected containers were assessed. Crates were observed from at least two sides to record the number of birds showing a certain behavior or condition within the crate (indicators 7 to 12; Table 3).

4 262 JACOBS ET AL. Table 3. Welfare indicators assessed on farm before catching and loading (pre-catch), on farm after catching and loading (post-catch), at the slaughter plant at the end of lairage (ante-mortem), and at the slaughter line (post-mortem). The measurement level and unit is given per indicator. Time of assessment No Indicator Measurement level (unit) pre-catch post-catch ante-mortem post-mortem Physical condition 1 Wing 1 or leg fractures Animal & flock (%) x x x x 2 Lesions on vent and thighs 1 Animal & flock (%) x x x x 3 Plumage cleanliness 1 Animal x x x 4 Discharge or blood from beak, Flock (%) x x x nasal cavities or auditory meatus 2 5 Bruising on legs, wings, breasts 1 Flock (%) x Thermal stress 6 Body temperature 2 Animal ( C) x x x 7 Panting or huddling 1 Flock & crate (%) x x x In-crate welfare 8 Prostration 2 Crate (%) x x 9 Splayed legs 3 Crate (%) x x 10 Crowding 3,4 Crate (%) x x 11 Supine birds 3 Crate (%) x x 12 Toes, wings or heads stuck in the crate 3 Crate (%) x x 1 Original indicator from Welfare Quality R (2009). 2 Original indicator from EFSA (2011). 3 Original indicator from Visser et al. (2014). 4 Crowding prevalence per crate was assessed as % of birds that had another bird on top of them. Measurements on individual animals (at animal level) were performed on a different sample of 44 ± 1birds per moment of assessment (on average 132 ± 3birds per transported flock). Before catching, these birds were chosen randomly from 10 locations in the poultry house (on the side or in the middle of the house, ca. 5 birds per location). After catching and at the end of lairage, the birds were chosen randomly from the same marked containers (one bird from all crates in the marked containers). Post-mortem measurements were performed at the slaughter line after plucking. The number of birds showing indicators 1, 2, or 5 (Table 3) was counted during a 10-min period and prevalence was estimated based on the line speed (on average 10,710 ± 199 birds/h) as described in the Welfare Quality R poultry protocol for bruising (Welfare Quality R 2009). Statistical Analysis Data were analyzed using SAS 9.2 (SAS Institute Inc., Cary, NC) with transported flock as the experimental unit. The DOA% was log transformed, as is commonly done for percentages to obtain data that can be modeled through the normal distribution. First, the association between 29 potential risk factors and DOA% was tested using a univariate linear mixed model, with slaughter plant as the random effect. Risk factors significant at a 10% significance level were considered for inclusion in a multivariate linear mixed model, with slaughter plant as the random effect. Additionally, the association between welfare indicators and DOA% was tested using univariate linear mixed models with the slaughter plant as the random effect. RESULTS Risk Factors for DOA% Mean (± SE) DOA% was 0.30 ± 0.05% (range 0.04 to 3.34%; n = 79), and median DOA% was 0.19%. One flock had a DOA% that was extremely high (3.34%) compared to the other flocks. For two transports, no information on DOA% was provided. DOA% (P < 0.001) and transportation characteristics differed per slaughter plant, for instance mean amount of time without water (P = 0.003), crate stocking density (P < 0.001), slaughter age (P = 0.003), and weight (P = 0.093; Table 2). The multivariate analysis resulted in a model with two flock or management-related risk factors for DOA%, indicative of physical condition of the flock during the production phase. Higher DOA% were found when farmers had not checked chick quality upon arrival (1.20 versus 0.26%; P = 0.011). Notably, the one transported flock with extremely high mortality (3.34%) was part of one subset (no check of chicks at arrival), which skewed the average mortality upwards. When this transportation was excluded from the dataset, the effect of the farmer s check was no longer significant (P = 0.69). In addition, on-farm mortality during production (including culling; P = 0.011) was negatively associated with DOA%, with every 1% increase in on-farm mortality, DOA% decreased by 9%. No pre-slaughter phase risk factors could be identified for DOA%. Broiler Welfare Indicators and DOA% DOA% was significantly associated with 5 out of 12 indicators of broiler welfare during the pre-slaughter

5 PRE-SLAUGHTER BROILER MORTALITY 263 Table 4. Significant associations between animal-based welfare indicators (at flock level) and DOA% (n = 79). The estimates and P-value are given. Welfare indicator Slaughter phase Mean ± SE Estimate P-value Lesions on vent and thighs (%) Ante-mortem 4.66 ± Plumage cleanliness score Pre-catch 1.18 ± Ante-mortem 1.31 ± Body temperature ( C) Post-catch ± Ante-mortem ± Panting (%) Post-catch 1.93 ± Ante-mortem 2.32 ± <0.001 Supine birds (%) Post-catch 0.04 ± phase (Table 4). DOA% was positively associated with the percentage of birds with lesions on the vent and thighs (ante-mortem P = 0.005), plumage cleanliness (pre-catch P = 0.039; ante-mortem P = 0.056), body temperature (post-catch P = 0.003; ante-mortem P = 0.007), panting prevalence (post-catch P = 0.022; ante-mortem P < 0.001), and prevalence of birds supine in-crate (post-catch P = 0.030). DISCUSSION The current study showed a mean DOA% of 0.30% and a median of 0.19%, ranging from 0.04 to 3.34% between flocks. Sudden death syndrome and traumatic lesions, including fractures and liver ruptures, have recently been identified as the most common causes of death in broilers during the pre-slaughter phase (Kittelsen et al., 2015). Infectious diseases have been reported to be another main cause of DOA (Nijdam et al., 2006). Furthermore, heat stress is a major cause of mortality (Bayliss and Hinton, 1990; Ritz et al., 2005). In the current study no post-mortem analysis of DOA carcasses was performed, as the focus was on identifying risk factors and associated welfare indicators. Risk Factors for DOA% A variety of mean DOA% have been reported in the literature (Table 1); our findings are within the range of those results. This wide range of DOA% might indicate either a difference in pre-slaughter circumstances or a difference in method of assessment, but could also be due to flock health status. It should be noted that DOA% were recorded differently in different studies: by slaughter plant personnel or by researchers, possibly explaining a part of the variation in DOA% (Table 1). Additionally, dissimilarities could also be due to methodological differences in research. For instance, a Czech study (Vecerek et al., 2006) showed an effect of transportation distance and season on DOA% but did not consider other flock or pre-slaughter aspects. Neither factor affected DOA% in the current study. Lack of a distance effect could be due to the relatively short duration of transports within Belgium (mean of 113 min, range of 32 to 300 min). Lack of a seasonal effect could possibly be due to either limited sample size or the moderate climatic conditions during the data collection period, as the mean transportation temperature was 10.5 C with a range of 0.1 to 25.7 C. In the current study, no risk factors inherent to the pre-slaughter phase were found for DOA%, while other researchers did find pre-slaughter risks (Table 1). The flocks in our study were transported to five slaughter plants. Many pre-slaughter characteristics such as slaughter age, weight, and pre-slaughter phase duration were strongly linked to the slaughter plant. Furthermore, in most cases transportations to a particular slaughter plant were conducted by a single transportation company and lairage conditions were similar within slaughter plants as well. As the slaughter plant was included as a random effect in the model, the likelihood of identifying such risk factors that strongly co-vary with slaughter plant was low. Potentially, only a complex combination of different environmental factors result in higher DOA%, instead of single, specific characteristics of the pre-slaughter phase. The current study shows that two flock management factors, indicative of the physical condition of the flock, were related to mortality during the pre-slaughter phase. Other studies have also indicated that flock characteristics are of importance (Table 1). In the multivariate analysis, a farmer check of chick quality upon arrival was associated with DOA%. However, the farmer s check effect was due to one extreme DOA%. Only 5% of the sampled flocks were not checked by the farmers. These results are therefore inconclusive. The possibility that the farmer s check reflects chick quality, health status and good management skills requires further investigation. The other identified risk factor for DOA% was onfarm mortality, which included selective culling by the farmer. Other studies (Haslam et al., 2008; Chauvin et al., 2011) have identified a positive relationship between on-farm mortality and DOA%, which contrasts with our findings. The difference is most likely due to the inclusion of selective culling by the farmer in the current study. On-farm mortality can be an indicator of overall flock health, with high percentages related to poor health (Haslam et al., 2008). However, when selective culling is included, a high percentage could indicate a careful selection by the farmer, with only healthy birds being transported. This could explain the negative relationship found in the current study and indicates

6 264 JACOBS ET AL. the potential importance of a fit-for-transportation inspection. Such an inspection is required by EU law (EU Council Regulation no 1/2005), and currently consists of a signature by the farmer indicating that the entire flock is fit to be transported. Further research should focus on developing a practical method for a proper fit-for-transportation assessment. Broiler Welfare Indicators and DOA% There were several animal-based welfare indicators assessed during the pre-slaughter phase which were positively associated with DOA%. The association between pre-catch welfare indicator plumage cleanliness and DOA% supports the findings that risk factors for the transports assessed in the current study relate to the on-farm phase. Flocks with a poor health status, reflected in our study as birds with soiled plumage, increased body temperature, and heat stress before transportation, may be at greater risk for DOA. Although no causal relationships were determined, results do show that flocks with high DOA% were found to have increased body temperature, more lesions, soiled plumage, panting, and more supine birds. Routine monitoring of a large number of broiler welfare indicators as was done for the current study is poorly feasible in commercial conditions. We therefore recommend using DOA%, which is already collected routinely, as a first and quick screening of broiler welfare under commercial conditions. If DOA% reaches a certain threshold, further investigation of the welfare problems should be performed on future shipments from the same farmer. Theoccurrenceofskinlesionsonventandthighs was fairly high (4.7%) compared to other welfare indicators, but much lower than the prevalence of 30% reported by Feddes et al. (2002). Lesions could result in contamination of the meat and could affect slaughter yield because damaged skin or meat has to be trimmed from the carcass. The prevalence of supine birds in-crate was lower than the 0.14% reported by Visser et al. (2014). The catching procedure is the most likely cause of birds lying in this position, the result of being placed or tossed into the crates. Anecdotes from farmers and slaughter plant personnel suggest that birds lying supine are unable to turn over unassisted, and are thus likely to die during the pre-slaughter phase. A positive association between cleanliness and DOA% was found. The plumage cleanliness scores found before and after transportation were partly comparable to scores reported by Wilkins et al. (2003). Their potential scores ranged from 0 to 7, with their highest 4 scores (score 4 to 7) being similar to our scores from 0 to 3. Soiled plumage could result in hygiene problems at the slaughter plant, with potential contamination of equipment (Wilkins et al., 2003). The link between plumage cleanliness and DOA% is not clear, but could potentially be due to thermal comfort, gut health, or management during the growing period (e.g., ventilation). The positive association between post-catch and ante-mortem body temperature, panting, and DOA% also indicates a link between heat stress and mortality. Thermal stress could be affected by many factors, such as ambient temperature, stocking density, and curtain configuration on trucks, but also body weight, feather coverage, cleanliness, and other animal-based aspects. Although no climate-related risk factors of the pre-slaughter phase were significantly associated with DOA%, the link between animal-based indicators for heat stress and DOA% do indicate that heat stress may result in DOA. In addition, it suggests that assessing animal-based indicators is more reliable to evaluate thermal stress than the assessment of the studied management-based risk factors. The microclimate in transportation containers, and how it affects the birds thermal comfort, depends on an interaction of factors. It is well recognized that heat stress is a major threat to broiler welfare (EFSA, 2011). Ritz et al. (2005) found the pre-transportation and post-transportation phases may cause heat stress, in accordance with the present study. Adjustment of the ventilation to the climatic conditions could help to solve these temperature-related problems (EFSA, 2011). In conclusion, two risk factors for DOA% were identified. However, the farmer s check effect was due to one extreme DOA% and the on-farm mortality effect may have been due to selective culling. Further research is needed on the relationship between on-farm health status and welfare during the pre-slaughter phase, as the current study provided some evidence that on-farm health and welfare is linked to mortality during the preslaughter phase. No specific, separate characteristics of the pre-slaughter phase could be identified as risk factor for increased DOA%. Because DOA% was found to be positively associated with other welfare indicators (lesions on vent and thighs, plumage cleanliness, body temperature, panting, supine birds), including indicators of thermal stress, DOA% could be used as a first and quick screening for pre-slaughter broiler welfare impairment, with the aim of identifying commercially transported flocks whose welfare is most at risk. ACKNOWLEDGMENTS The authors thank the Federal Public Service (FPS) for Health, Food Chain Safety and Environment and the Department of the Environment, Nature and Energy of the Government of Flanders for funding this research (RT12/1 WELLTRANS). The authors thank the farmers, transportation companies, and slaughterhouses for their cooperation. In addition, the authors thank the animal technicians, fellow PhD students, and interns at ILVO for help with the data collection. The authors also thank Miriam Levenson (ILVO) for English language correction.

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