Amena-Animal Welfare at Markets and During Transport and Slaughter

This paper summarises some key findings fromrecent research into animal welfare during the preslaughter and slaughter periods. It focuses on injuries and ease of handling, stress effects on subsequent meat quality, and contemporary problems in stunning and slaughter.

Certain breeds, such as Limousin, Red Bororo cattle and Texel sheep, are difficult to handle (Minka & Ayo, 2007; Tompsett &  Gregory, 2008). It is often recommended that such animals should be familiarised with handling procedures, as this makes them easier to manage during the preslaughter period. There is no doubt that familiarisation helps, but in the case of pigs, a potential disadvantage is that familiarised animals have higher counts of enteric bacteria per gram of faeces in their excreta during the presalughter period (Dowd, Callaway, & Morrow-Tesch, 2007). The mechanisms that explain these and other stress-related effects on enteric bacteria and virus populations are not understood, and they need investigating.

It is also widely recognised that preslaughter stress starts as animals are being loaded onto the vehicles that take them to abattoirs. However, there are two recent studies showing that it can start earlier than this. Under Australian conditions, pre-transport stress or underfeeding were present in five out of 13 lamb consignments as determined from depletion of muscle glycogen in biopsies taken before loading (Jacob, Pethick, & Chapman, 2005). 

Previous work by the same group showed there was a linear correlation between muscle glycogen concentration and ME intake, and so it was suggested that improvement in nutritional management should solve a good part of this problem. However, there were four  lamb consignments with lower muscle glycogen concentrations on arrival at the abattoir compared with levels before leaving the farm, and three of those had been fed grain before embarkation. The second study was in New Zealand. When New Zealand lambs are prepared for slaughter they are usually graded and crutched shortly before leaving the farms. When this was done, along with weighing, it was found that it took the lambs more than 3 days to recover a normal pHult in the longissimus dorsi (Devine et al., 2006). The intermediate pHult meat (5.75–6.00) in lambs given insufficient time to recover resulted in tougher meat, but the toughness disappeared if the meat was allowed to age. There are mixed reports about whether handling stress in the abattoir before slaughter is being adequately controlled. In the EU the situation started to deteriorate with the introduction of cattle passports ten years ago. Introducing cattle passports increased the amount of preslaughter handling. Cattle must have their ear tag numbers checked against the number in the passport each time they are sold at markets and when they are presented for slaughter at an abattoir. This involves holding them in a crush, and as with any crush-work, some animals get bruised and others react badly to being confined. In addition, in a study on cattle sent from 30 farms to 10 abattoirs in Scotland, putting cattle through a crush in the lairage was found to increase hide contamination with E. coli O157 (Mather et al., 2007). By contrast, the situation in the USA where passports are not used is improving, in terms of the prevalence of vocalising, thanks to closer attention to welfare auditing (Grandin, 2006; Table 1).

When animals are forced to take strenuous exercise, muscle is prone to forming lipid peroxidation metabolites. The mechanisms that explain this are understood, but there have been few situations where it has been found to affect meat quality (Gregory, 1998, 2007). Ten minutes preslaughter exercise on a treadmill (3.8 km/h) resulted in slightly higher TBARS development in heated pork meatballs, compared to product from unexercised controls, but this must have been quite a severe stress compared with usual practice (Young et al., 2003). Preslaughter heat stress and CO2 stunning could be more common factors leading to oxidative rancidity (Mujahid, Akiba, Warden, & Toyomizu, 2007). TBARS concentration in broiler breast meat was higher in CO2 stunned than electrically stunned birds (Alvarado, Richards, O’Keefe, & Wang, 2007). TBARS formation was particularly pronounced in poorly bled birds (Table 2). CO2 stunning in trout also leads to greater TBARS formation compared to killing by holding in ice (Giuffrida et al., 2007). Whether this was due to their greater exercise or to the potency of carbonate radicals as membrane lipid oxidising agents is not clear.

The way in which pigs are reared can affect ease of handling during the preslaughter period and the extent to which they have to be encouraged to get them to move. Pigs reared on slatted floors were more difficult to load onto vehicles, showing more balking, compared with pigs reared on solid floors. This could have been due to the novelty of the floor type, and because theyseemto bemorereluctant to move generally (Nanni Costa, Tassone, Righetti, Melotti, & Comellini, 2007). They were, however, less likely to slip during loading.

Hambrecht et al. (2005) compared the relative effects of transport stress, lairage duration and rough handling during transfer in the lairage to the stunning point on subsequent meat quality in stress resistant pigs under European conditions. Stressful handling during transfer to the stunner had the biggest effect on pHult and on muscle lactate concentration at 2–3 h post-mortem. 

This was not surprising in the case of muscle lactate, but  the 0.13 unit increase in pHult from mishandling immediately before slaughter was unexpected. The general conclusion was that the greatest benefits in terms of meat quality are likely to come from reducing stress in the lairage during the final stages before slaughter.

The importance of exercise and handling stress immediately before stunning could be even greater in hotter climates. The remedy, however, is not always straight-forward. It is recognised that under subtropical conditions, antemortem showering helps to relieve heat stress in pigs, and this should help alleviate the immediate preslaughter acidosis that contributes to PSE meat. In broilers, however, there is a risk that showering birds can lead to a higher proportion of high pHult meat, especially when it is applied too enthusiastically (Guarnieri et al., 2004). 

One of the ugliest aspects of preslaughter handling is the way downer animals are managed at abattoirs. These are animals that are either injured, or are too weak, or too sick to stand and walk. In the US, in 1994 and 1999, 1.15% and 0.8% of cattle waiting in pens at abattoirs were culled because they were in this condition. This amounted to 71,117 and 49,520 cattle, of which 1.1% and 1.5% were dairy cows and 0.7% and 1.1% were beef cattle (Stull, Payne, Berry, & Reynolds, 2007).

We do not have a more recent estimate of the prevalence of this problem. 

International cattle transport has attracted interest on two fronts in recent years. The first has been cattle shipped from Australia for slaughter in the Middle East (Sidhom, 2003). The handling at Cairo abattoir has drawn poor publicity, along with the ways Australian sheep have been managed in Oman. The second area of concern has been with water buffalo and Hariana cattle exported from north India for slaughter in Bangladesh. India has more cattle than any other country and yet, for religious reasons, it does not have a correspondingly high cattle slaughter rate. There are very few recognised beef abattoirs in India, and export agents are thinking of diverting cattle away from Bangladesh to more lucrative markets in the Middle East. There are moves to improve the welfare image of the export trade in Bangladesh to help sustain this important source of dietary protein. The animal welfare problems include ulceration and bleeding where ropes are secured in the noses, broken tails, and skin lacerations and grazing (Table 3).

Many of the injuries were recent injuries and were probably due to contact with the inner walls of the vehicles during transport (Table 4). Some could be corrected through better awareness amongst the stock handlers (Alam, in preparation). Injuries are also common in Nigerian cattle, and it is estimated that 34% of the injuries are due to horns.  Red Bororo cattle are difficult to load onto livestock trailers compared to white Fulani or Sogoto Gudale and they are more prone to injuries. The Red Bororo breed is generally more difficult to handle and this was reflected in the time it took to get them loaded. Red Bororo had more fractures (3%), dislocations (3%), lacerations (20%) and muscle bruising (43%) compared to Sogoto Gudale (2%, 2%, 8%, 23% respectively), which is a placid draught breed (Minka & Ayo, 2007). It is likely that Red Bororo also incurred injuries because of their loose thin skin and long horns. Overall, the prevalence of cattle without any injuries by the end of 10–12 h journeys was 21%, and the prevalence with injuries doubled during the last 6–8 h of the journeys. It is common for journeys to take 2–3 days to reach the slaughter destination.

Temperatures inside the livestock trailer during the hot-dry season vary between 22 and 33 C, and can rise to 35 C when the vehicle stops. Under these conditions, weight loss would be expected during journeys lasting more than a day.

Under central European conditions, 42-day old broilers lose 7 g more weight per bird when transported 1.5 h at a high stocking density (0.0350 m2/broiler) compared to a lower density (0.0575 m2/broiler) (Delezie, Swennen, Buyse, & Decuypere, 2007). The higher density would be typical for present standards, and the saving in weight loss from using the lower density would be equivalent to one bird per module. For a plant processing 200 modules a day this would be equivalent to a saving of 200 birds, which could make the lower density financially attractive. In recent years in the UK, cattle farmers have been using their own vehicles to transport animals instead of hiring professional hauliers. This has cost-saving advantages, provides farmers with more flexibility in deciding when to sell and it gives some farmers an opportunity to hire out vehicles when they are not in use. There may be a food safety advantage as well. Transporting cattle to an abattoir by a haulier is more likely to be associated with contamination of the hide with E. coli O157 compared with transport by the farmer (Mather et al., 2007).

In Europe, selling livestock through auction markets (saleyards or salebarns) is losing favour with retailers and governments. This stems from four concerns. Firstly, it has been difficult to trace meat back to the farm of origin when animals have been sold through livestock markets. The worry is that when there is a food safety alert, such as BSE, it will be difficult to identify the source of the problem. That concern is no longer valid in those countries that have introduced cattle passports, as passports now allow an adequate level of traceability. Instead, this concern has been replaced by worries about transmission of disease within markets. This is supported by science-based risk analysis, and it applies particularly to contagious exotic diseases (Bigras-Poulin, Thompson, Chriel, Mortensen, & Greiner, 2006; Robinson & Christley, 2007; Schembri, Hart, Petersen, & Whittington, 2006). In Africa, however, transhumance is probably a greater disease risk than submitting stock for sale in markets (Bonsvoort et al., 2004). The third concern about livestock markets is the effect it has on animal cleanliness. Putting cattle through markets can increase the risk of hide contamination with undesirable bacteria (Collis et al., 2004). The fourth concern is that the welfare of animals sold through markets is poor compared with animals delivered directly to abattoirs (Murray, Davies, Cullinane, Eddison, & Kirk, 2000). 

The welfare concerns with putting fat cattle through markets  include fatigue, fear and distress, fasting, dehydration and injuries. It is well recognised that the prevalence of carcass bruising in cattle sold through markets is higher than for cattle sold direct to abattoirs, and this is cited as evidence that auction marketing is less appropriate than direct sale to abattoirs (Weeks, McNally, & Warriss, 2002). For these reasons, one of the major international restaurant companies no longer allows its European beef burger suppliers to source meat from cattle sold through auction markets. An alternative approach might be to address the welfare concerns by identifying the key issues at the markets and then manage those issues in the most appropriate way.

In a study of 18 cattle markets in the UK, the key welfare issues were found to be slips and falls in fat cattle during unloading, grading, putting-up to and through the sale-ring, impacts during grading and at specific places when passing to and through the ring, slips and falls during loading in calves, and refusal to load amongst cattle after the sale (Table 5; Gregory, Benson, et al., in press). In a comparable study of 24 UK sheep markets, the prevalence of these and other welfare-related problems was very low.

Slips and falls occurred when there was manure plus rain or urine on the concrete floor, especially at bends where running cattle made a turn. When the skid resistance value for wet concrete is greater than 55 British pendulum number (BPN), the prevalence of falls is less than 2% and the prevalence of slips does not exceed 14%. Below 55 BPN, the risks rise. Some cattle markets have installed resin plus grit screeds over concrete in high-risk areas, and they seem to be very effective. Similarly, resin screeds can be applied to metal weighbridges where these pose a problem. 

Many UK cattle markets have two-way gates at the entrance of the holding pens. These have a centre gatepost supporting two gates that open at opposing ends allowing cattle to enter and leave the pen in both directions along the corridor. The disadvantage with these pens is that the entrance can be narrow, and this presents bruising points at the centre and corner posts. The prevalence of impacts from this and other causes when putting cattle up to the sale ring was 12.5% (Gregory, Benson, et al., in press). Impacts were also frequent during grading, and this is a common feature with any work on cattle in crushes, races or other confined spaces.

One way of reducing movement and the likelihood of severe impacts  is to temporarily section the raceway into a series of individual pens using sliding gates. This stops cattle shunting up and down the raceway, and it stops horned cattle burrowing under an animal in front. Not all markets had raceways with a sliding gate system. At some markets, loading is difficult because the loading pen is too wide. Milling and circling occurs when the pens are more than 4 m wide. The height of the loading platform above the vehicle also influences ease of loading. Where it is high, cattle have a clear view downwards into the vehicle and they sometimes refuse to load. This was a serious problem at one market, where the height difference was 93 cm (Gregory, Benson, et al., in press). Applying straw to the loading tailboard was said to make loading easier, but this was rarely used. Placing straw on dry concrete can make the floor slippery and so it is not recommended for unloading.

In the UK study, 11% of calves fell during loading. This usually happened when they failed to raise their feet adequately whilst moving onto the tailboard. Instead, the leading fore leg folded at the knee and was followed by the second fore leg. If the person doing the loading pushed the kneeling calf from behind, it was prone to going over on its side.

Less commonly a calf fell off the side of the tailboard, and became lodged between the tailboard and loading pen side gate. During grading the cattle are usually held in a race or crush, the eartag number is checked against that of the passport, a salelot number is applied to the back and a sale category is registered. Impacts during grading were mainly with gates and other animals, and refusal to enter the crushes was the single most important reason for hindered movement. Slippery floors and lost footing were the main contributors to slips and falls. Other countries have different problems at cattle markets. In Ontario and Quebec the main issue recently has been submission of sick dairy cows, especially when the milk quota has been tightened (Cochrane, personal communication). This has been made worse by a cost-cutting reduction in veterinary livestock inspectors at markets.

About 20 years ago it was thought that electronic marketing would displace traditional live auction markets. This has not happened, but there are some feedlot regions where first-price sealed-bid auctions have become common (Crespi & Sexton, 2004). Feedlot operators provide weekly show lists of lots of cattle available for sale, and abattoir representatives may visit the feedlot to inspect these cattle. Bids are submitted as sealed bids by phone or fax, and competing abattoirs do not know who has bid on the various lots and at what price. The feedlot accepts or refuses a bid, and usually the first bidder is given an opportunity to revise his bid in the event that someone offers a higher price. This system works well where there are many feedlots and processors using the system simultaneously.

About 30% of cattle in the USA are now sold through a grid pricing system. This method has been controversial because it is thought to aid price control by a declining number of abattoirs, and it relies on meat and carcass quality assessments made on the slaughterline which are thought to be too subjective (Schroeder, Mintert, Ward, & Wheeler, 2003; Whitley, 2002). Confidence in the quality-related criteria needs to be improved. 

When cattle are slaughtered without stunning some animals take a long time to lose brain function and die. This has been shown experimentally using somatosensory evoked responses in the brain and from the delay before the animal collapses (Blackmore, 1984; Daly, Kallweit, & Ellendorf, 1988). It is thought that the delay is due to a combination of false aneurysms in the severed carotid arteries plus sustained flow of blood to the brain through a plexus connecting the vertebral arteries with the carotid rete (Baldwin, 1960). False aneurysms are also known as ballooning. The severed artery retracts within its surrounding connective tissue sheath, the connective tissue becomes impregnated and swollen with blood and this can occlude flow from the cut artery. About 8% of cattle slaughtered by shechita and halal, without stunning, develop false aneurysms in both carotid arteries (Gregory, von Wenzlawowicz, et al., 2008). When this happens there is a risk that blood flow from the severed caudal ends of the arteries stops and the animal takes longer than usual to lose consciousness and die. The next piece of work that needs to be done is to find ways of avoiding false aneurysm formation.

Some authorities claim that aspiration of blood into the upper respiratory tract and lungs causes suffering during slaughter without stunning (Von Wenzlawowicz & von Holleben, 2007; Webster, 1994). Others take the view that there will be no suffering because afferent signals activated by lung irritation are conveyed by neurones within the vagus nerves (King, 1999), and these are severed during slaughter without stunning. More recently, it has been shown in a range of laboratory animal species that there is a collateral spinal afferent pathway between the lower respiratory tract and the brain, which passes through the cervicothoracic (syn. stellate) ganglia and the dorsal root ganglia at T2–4 (Qin, Foreman, & Farber, 2007). This pathway could relay signals that are interpreted in humans as tickling, tearing or burning sensations provoked by chemical and physical stimuli in the alveoli of the lungs (Hummel, Sengupta, Meller, & Gerhart, 1997). About 19% of 123 cattle slaughtered by shechita in the upright position were found to have  blood in the trachea (covering >10% of the inner surface area), and 36%  had blood in the bronchi (Gregory, in press). These prevalences were similar to those in 103 cattle shot by captive bolt and gash stuck whilst in the same upright position (21% and 31%). Ten percent of the shechita cattle had bright red blood foam in the trachea, whereas none of the secular cattle showed this effect. Taken together this information suggests that the welfare concerns about blood aspiration during shechita are warranted.

In the UK there are about 2 million Muslims, and yet it is said that there are 6 million consumers of halal meat. This claim has not been authenticated, but the reasoning behind it has a logical basis. It is claimed that there is a perception that halal meat carries less risk of transmitting BSE. This is consistent with the fact that captive bolt stunning introduces a risk of brain emboli embedding in the edible carcass. However, that view is not consistent with recent reports from Turkey, where two separate studies showed that 9% and 10% of retail meat products contained central nervous system (CNS) tissue, as determined with the glial fibrillary acidic protein ELISA test (Nazli, Colak, Hampikyan, & Bingol, 2006). Since the main slaughter methods in Turkey are halal and shechita, it is highly unlikely that the CNS material arose from brain emboli developing after shooting by captive bolt. Instead it is likely that the CNS tissue arose from the spinal cord during carcass splitting (Lim, Erwanto, & Lee, 2007). Carcass splitting is probably the single biggest risk factor in transferring the BSE prion to edible meat in an infected carcass, and it can occur independently of the stunning or slaughter method.

Most meat scientists would accept that meat quality in stunned cattle and sheep is comparable to that from animals slaughtered without stunning. There has, however, been a recent exception. When 25 kg lambs were slaughtered without stunning, their meat developed less drip before cooking, and had less cooking loss, compared with meat from electrically or CO2 stunned lambs (Linares, Bórnez, & Vergara, 2007; Table 6). Whether this was sufficient to influence meat succulence was not tested.