Making Slaugherhouses more Humane for Cattle, Pigs, and Sheep

by Temple Grandin

Department of Animal Science, Colorado State University, Fort Collins, CO, 80523


Abstract

When a stunning method is being evaluated, it is essential that the animal-handling and restraint methods that are used with it are also examined. This makes it possible to determine the effect of the entire system on animal welfare. Cattle, pigs, and sheep will move easily through the races at a slaughter plant if visual distractions such as reflections on shiny metal, dangling chains, moving equipment, or people up ahead are removed. The most important scientific research on captive bolt, CO2, and electrical stunning methods is reviewed. A common mistake made by people evaluating insensibility is to misinterpret reflexive leg kicks as a sign of return to sensibility. When religious slaughter is being evaluated, the variable of how the animal is restrained must be separated from the variable of slaughter without stunning. Slaughter can be done with a high level of animal welfare.

Introduction

There is increasing concern about the methods used to handle animals and render them insensible to pain in slaughter plants. The purpose of this paper is to review the most important literature on animal welfare at slaughter plants and combine the scientific review with the authors extensive experience working on handling and stunning methods. The author has visited over 400 slaughter plants in 20 countries and has served as a consultant on the design of handling systems, correct operation of stunning equipment, writing animal welfare guidelines, and training welfare auditors (1). This paper will assist veterinarians, researchers, managers, and inspectors when they evaluate animal welfare at slaughter plants. The scope of this review is animal welfare during preslaughter handling; restraint for stunning; religious slaughter; and stunning methods for cattle, pigs, and sheep.

Preslaughter Handling

Evaluate Both Stunning Method and. Handling

A common mistake is to examine the stunning method but overlook the handling system that is used with it. Handling methods that bring animals up to the stunner, and devices used to restrain animals for stunning or religious slaughter, should also be evaluated. Animal welfare improvements will be greatest when the entire system is examined. For example, the operator of a captive bolt may be failing to render a high percentage of the cattle insensible with a single shot. A common cause of this problem, which is often overlooked, is that animals may become highly agitated as a result of slipping on the floor. Installation of nonslip flooring in the stunbox will solve this problem. Another example is a C02 gas system in which pigs are handled in groups. Handling pigs in groups makes it possible to totally eliminate electric prods, but the pigs may experience some discomfort during anaesthesia induction because loss of consciousness is not instantaneous. A third example is an instantaneous insensibility-—inducing electric stunning system that has to be applied individually to each pig. In large plants, electric prods may be required to move a few pigs up the single-file chute into the restrainer for electric stunning. There may be a trade-off between the stress caused by the handling methods and stress caused by the stunning method itself. Another example is use of a head—h0lding device for captive bolt stunning of cattle. The head-holder will improve stunning accuracy, but it may cause stress if it is designed poorly and if cattle balk and refuse to enter it (2). This is why it is important to evaluate both the stunning method and the systems used to handle and restrain animals as a whole.

Remove Distractions to Improve Animal Movement through Chutes

Cattle, pigs, and sheep will often balk and refuse to move through chutes (races) at slaughter plants, feedlots, or ranches if they see distractions. Some common distractions are: seeing people outside the chute, moving equipment, reflections on shiny metal (3), a chain hanging down, or an entrance to the chute that is too dark (4). Shadows and high contrasts of light and dark will also impede animal movement (5). Because animals tend to move more easily from a darker place toward a more brightly illuminated place (6,7), installation of a lamp at the entrance to a chute will improve animal movement at slaughter plants (8). Livestock are highly influenced by what they see. Addition of a solid panel to prevent cattle from seeing people next to them while they are in a chute has a calming effect (9). Adjusting lighting to eliminate reflections and blocking the view of moving distractions such as people, vehicles, or conveyors also improve animal movement. Another factor that will have a detrimental effect on calm animal movement is air blowing into the faces of approaching animals. Changing the direction of airflow at the stun-box entrance makes it possible to greatly reduce electric prod use by reducing balking and refusal to move. Sudden intermittent noise, such as air hissing from pneumatic valves, rapid motion of people or equipment, and banging metal will frighten animals. Cattle with a more excitable temperament are more likely to become agitated from sudden intermittent stimuli (10) (Figure 1; see sidebar on Animal Behavior Principles).

Are Animals Aware That They Will Die?

This is one of the most common questions people ask. When the author first started working with beef slaughter in the 1970s, she observed that cattle behavior during handling and movement through the chutes (races) was the same both in a slaughter plant and in a squeeze chute at a local feed yard. The amount of balking, refusing to move, and behavioral agitation appeared to be the same in both places.

Fear of Novelty in a New Environment

Fear of novelty may be a major contributor to stress at slaughter. Cattle that were the most fearful of a sudden novel stimulus on the home farm had greater physiological stress reactions at a slaughter plant compared with calmer cattle (1 1). Animal fears are very specific; habitation to a particular novel object, such as a blue and white umbrella, does not transfer to another different novel object, such as an orange tarp (12). Novelty and noise may explain why sheep slaughtered in a quiet research abattoir had lower cortisol levels compared with sheep slaughtered in a large commercial plant (13). Stress reactions at a slaughter plant likely are mainly a result of fear of a new environment rather than fear of death. Further evidence that stress during slaughter is not fear of death is that cortisol levels are similar after both on—farm handling and slaughter (14). However, one study reported that cortisol levels were much higher during on-farm handling compared with slaughter (15). Cortisol levels were 24 mg/ml when cattle were handled calmly, but they doubled when a high percentage of cattle slipped on the floor or balked and refused to enter a head—restraint device (2, 16).

The importance of using animal behavior principles to handle and restrain animals

Many people fail to recognize the importance of using animal behavior principles in the design of equipment for handling and restraining animals. I developed a system called the center-track conveyor restrainer for holding cattle for stunning (Figure 1). Cattle enter it willingly and quietly, if it has a nonslip entrance ramp, a false floor to prevent the incoming animals from seeing the visual cliff effect, and an overhead solid shield that prevents the animals from seeing out until they are restrained fully. In many plants, people have removed cleats on the entrance ramp because they think making animals slip and slide in is more efficient. They have difficulty comprehending the concept of using behavioral principles instead of force. I have returned to many plants to replace and fix modifications that plant manager have made that made the system work poorly. Metal parts that are used to control what an incoming animal can see are often removed because people view the as extra metal that has no purpose. When I replace the nonslip cleats on the ramps, they can see that the cattle enter more easily. This system will work efficiently until a new manager arrives to repeat the same mistakes.

Animals Acclimated to People Easier to Handle

The author has observed that pigs will move through pens and chutes (races) more easily at a slaughter plant if they become accustomed to people walking through their pens on the farm before it is time to load them on a truck for transport to slaughter. This habituates the pigs to a person walking among them so that this experience is no longer novel. Pigs differentiate between a person in their pen and a person in the aisle. For several months before slaughter, a person should walk quietly through the pens in a different random direction each day to train the pigs to move away quietly and walk around the person in an orderly manner. Research supports the idea that contact with people and allowing pigs to run in the aisles at the farm will make them easier to move in the future (17-19). Pigs that had weekly contact with a person in their pens had a lower startle response and were less likely to pile up and squeal when a person suddenly entered their pens (20). Acclimating animals to handling procedures on the farm will reduce the detrimental effect of the sudden novelty of having people walking through them at the slaughter plant. Furthermore, cattle appear to differentiate between a person on foot and a person on a horse (21). The author has observed that cattle that respond calmly to a person on horseback may become highly agitated and have a much bigger Bight zone when they first encounter people on foot at a plant. Cattle should be acclimated to being moved in and out of pens by a person on foot before they go to a slaughter plant. Fortunately, most castle get this experience during normal handling procedures on ranches and feedlots.

Vocalization (Moos or Squeals During Handling and Restraint) as an Indicator of Welfare Problems in Beef and Pork Plants

In cattle, vocalization during handling and restraint at a slaughter plant was associated with an adverse event such as sharp edges on restraint equipment, excessive pressure from a restraint device, electric prod use, or inversion for over a minute (22-24). In both cattle and pigs, vocalization (moos, bellows, or squeals) during handling or painful procedures are associated with physiological measures of stress (24-26). Cattle and pig vocalizations in both the chute (race) that leads to the stunner and in the restrainer or stun box can be used as an indicator of handling or equipment problems. Simple improvements in equipment to reduce balking and electric prod use or to reduce pressure applied by a head restrainer greatly reduced the percentage of cattle that vocalized (27). In well-managed slaughter plants, less than 5% of the cattle will vocalize during handling or during holding in a stun box or restrainer (28). In two plants with many distractions, such as people visible up ahead, high electric prod use, and excessive pressure applied by a restraint device, 25-35% of the cattle vocalized (29, 23). Vocalization of animals in the stockyard (lairage) is rarely measured. Vocalizations should be measured at two points: in the stun box or restrainer and when people are actively moving the animals into the stun box or restrainer. Vocalization is not measured in sheep; owing to a species difference, sheep usually do not vocalize when they are hurt.

Physiological Measures of Handling Stress

At the slaughter plant, increased cortisol levels were associated with the use of dogs on sheep and electric prods on cattle (22, 30). Careful handling during the last few minutes before slaughter also can have a beneficial effect on meat quality. Multiple shocks with an electric prod within 5 minutes before slaughter increased meat toughness in cattle (31). In pigs, low lactate levels at bleeding resulted in better pork quality (32, 33). Measuring blood lactate during exsanguination may be an economical method for assessing the quality of handling shortly prior to stunning in pork slaughter plants. Stressful handling within S minutes of slaughter, such as electric prod use or jamming in the chute, greatly increased lactate in pigs (34). Glucose and lactate levels in pigs after stressful handling and multiple electric prod shocks were 215 mg/dl and 32 mM, and after careful, quiet handling with no electric prods, they were 4 mg/dl and 4-6 mM (35). Short-term stresses, such as stressful handling in the stunning chute, will cause glucose and lactate to be higher immediately after a stressful handling event. Long—term stresses such as transport may lower lactate and glucose levels. Therefore, when lactate or glucose is used to evaluate the stressfulness of a handling procedure, the blood sample must be taken immediately after the handling procedure.

Problems with Compromised Animals That Are Difficult to Handle

Quiet, careful handling at the slaughterhouse and transport with an acceptable level of welfare are impossible if animals are very weak or lame. There are four major types of animals that are compromised. They are extremely difficult to move through a slaughter plant in a low-stress, humane manner. The problems discussed in this section must be addressed by producers on the farm.

  1. Newborn Calves: Some newborn calves (Bob veal) of the Holstein dairy breed are almost impossible to handle with low-stress handling methods at a slaughter plant. They are too young to stand and walk easily without assistance from a person. The author has seen newborn Holstein calves thrown, dragged by the ears, and abused by handlers. Newborn calves should not be brought to a slaughter plant until they are old enough to walk and move easily.

  2. Cull Breeding Stock and Old Dairy Cows: A survey of 10 auctions that sold over 9,000 cull dairy cows and over 8,000 beef-breed cull cows showed that 13.3% of the old dairy cows and 3.9% of the beef cows were severely emaciated (36). These extremely thin animals are more likely to become non-ambulatory during transport and handling at a slaughter plant. Most of the cull cows sold at auctions go directly to slaughter. These weak animals make calm, humane handling very difficult. Producers should market their cull cows when they are in better condition.

  3. Feeding Beta—Agonists: The author has observed that the introduction of the beta-agonist ractopamine for increasing lean muscle mass in pigs was associated with a higher incidence of fatigued pigs that were weak and refused to walk. The exact wording on the label from the manufacturer of ractopamine sayes, "Ractopamine may increase the number of injured or fatigued pig during marketing" (37). Pigs fed 9 grams/ton ractopamine were more difficult to handle and had increased hoof cracking (38, 39). Another study showed that ractopamine made gilts more aggressive (40). A common industry practice of reducing the amount of ractopamine to 4.5 gm/ton may help reduce these problems. The anchor has observed some groups of pigs that were so weak that they could not walk off the truck and move through the lairage to the stunner. Reduction of the amount of ractopamine fed reduced this problem. Another factor that may increase handling problems is growing pigs to heavier weights.

There have also been problems with beta-agonists in ruminants. After beta-agonists were approved for feedlot cattle, the main problems observed by the author have been lameness and severe hear stress. The beta-agonists approved for cattle in the United States are ractopamine and zilpaterol. Scientific research has shown that zilpaterol increases the surface body temperature of sheep (41). When summer temperatures rose over 30°C, the author observed sore-footed feedlot cattle and heavy open-mouthed breathing in cattle arriving at five different slaughter planes. Heavy open-mouth breathing is a sign of severe heat stress in cattle (42). After ractopamine was approved, 0pen-mouth breathing was also observed in heat-tolerant Brahman cross-bred cattle. The heat stress symptoms and lameness were variable, and some individual cattle were affected more severely than others. Prior to the introduction of beta-agonists, the author had never observed fully rested, heat-stressed Brahman crossbred cattle with open-mouth breathing. Heat stress symptoms are more likely to occur during hot weather. A dose of 200 mg of ractopamine per steer each day caused some slight changes in the behavior of cattle during handling (43). A preliminary study indicated that certain combinations of implants and beta-agonists may increase panting during hot weather (44).

Foot and Leg Conformation Problems

Another problem that can make animals difficult to handle at a slaughter plant is either poor leg conformation or swollen joints. Certain genetic lines of pigs have poor leg conformation and a high percentage of lame pigs. Calm, careful handling at the slaughter plant is very difficult if the pigs are reluctant to walk.

Training Handlers to Be Quiet

Low-stress handling requires people who are trained in the behavioral principles of animal movement as well as plant management that is committed to humane animal treatment. Handlers need to understand principles such as the flight zone and point of balance (45). Standing in front of an animal while attempting to move it forward in a chute (race) or putting too many cattle or pigs in the crowd pen that leads to the single—file chute are common mistakes made by handlers. Good handling practices require more walking to move smaller groups of pigs and cattle through the chutes. Handlers should he quiet and not yell at livestock. Yelling and whistling are more stressful to cattle than the sounds of gates closing (46). High-pitched, intermittent sounds such as whistling and yelling are also stressful for pigs. High—pitched sounds, especially intermittent sounds, have a greater effect on a pig’s heart rate than low—pitched sounds (47).

Reducing Electric Prod Use

In many large commercial slaughter plants, the author has observed that electric prods have been successfully eliminated (while maintaining commercial production levels) in the following areas:

A total ban on electric prods may be detrimental at the entrance to the stun box or restrainer, because a stubborn animal that refuses to move may be handled abusively by beating, hard tail twisting, or poking sensitive areas such as the anus. In 2010, ten handling audits were clone by restaurant companies in five different pork plants, running 600-900 pigs per hour through a single-file chute. They had highly variable usage of electric prods. Within the same plant, electric prod usage varied from 0% to 23% of the pigs. Some groups of pigs are easier than others to drive through a single-file chute. Electric prod use on groups of easy-to-drive pigs was 4% and 20% on hard-to-drive pigs (48). Problems with groups of difficult-to—drive pigs need to be addressed at the farm. When beef plant management works to eliminate distractions that cause bulking, and trains handlers. Electric prod use can be reduced to 5% of the animals or less (49). Data collected from four years of restaurant audits in over 40 beef plants indicated that the average percentage of cattle moved with an electric prod was 17% (28). In well-managed plants, the handlers are not allowed to constantly carry electric prods. The electric prod can he picked up only to move a stubborn animal, and then it must be put away. Instead, other alternatives, such as flags, plastic paddles, and panels are used as the primary driving aids.

Electric Prod Alternatives

Plant personnel have developed alternative driving tools to reduce electric prod use. Stiff scrub brushes on the end of a stick work well for moving pigs up a single-file race. In many plants, cattle are moved into restrainers and stun boxes with an air—powered prod that creates a very intense vibration. The electric prod substitute was made from a pneumatically powered engraving tool with the sharp end removed. The author has observed that it is an effective electric prod replacement. However, the real electric prod is still needed on approximately 5% of the cattle. The author has applied the vibrating prod to her bare arm, and the vibration was very intense, but it did not hurt. There are a few stubborn animals for which a single buzz with an electric prod is preferable to repeated poking or hitting with other driving aids.

Design of Stun Boxes and Restrainers

It is beyond the scope of this paper to make extensive recommendations on plant facility design, but a few basic principles are discussed here. One of the single most important design features in a stun box is a flat nonslip floor that is easy for the animal to stand on. Animals panic when they slip. Cattle and other animals are more likely to stand quietly if they have good footing. This makes placement of the captive bolt stunner easier. Cattle standing on a slippery floor often will not stand still because their feet are slipping constantly. If more than 1% of the animals fall during movement into the stunning area, or in the stun box or restrainer prior to stunning, there is a problem that needs to be corrected (48). It is also important that animals entering a stun box cannot see people or moving equipment out on the slaughter floor. Animals may refuse to enter if they see activity up ahead.

In conveyor-restrainer systems that are raised above the plant floor, a false floor is essential. Animals may balk and refuse to enter if they see the visual cliff effect underneath a conveyor restrainer or lose their footing on the slippery entrance ramp (50). Livestock can see depth, and they respond to the visual cliff effect (51). The false floor should be installed so that it is located a few centimeters below the feet of the largest animal. This will facilitate animal entry into both conveyor-restrainers and center-track restrainers because it provides the illusion of a solid floor to walk on.

Highly stressful methods of restraint should not be used on conscious animals. Some examples are shackling and hoisting by the leg, shackling and dragging on the floor, trip floor boxes that make animals fall down before stunning, or religious slaughter or leg clamping boxes. Both industry and international guidelines specify that such methods should not be used (52, 53 ). Sheep that were shackled and hoisted had a higher physiological measurement of stress than sheep held in an upright restraining device (54). Restraining cattle on their backs for over a minute had significantly higher rates of vocalization and cortisol compared with upright restraint (24). Another study showed that restraining veal calves by inverting them in a rotating box compromised welfare (55). Some basic principles of restraint device design are: (a) all parts of the apparatus that contact the animal should move with smooth, steady motion because sudden jerky motion my cause the animal to become agitated; (b) pressure applied by the device must be limited to prevent excessive pressure that causes struggling or vocalization; (c) floors should be slip resistant; (d) stunning or religious slaughter should occur immediately after the animal is fully restrained; and (e) solid panels should be used to prevent entering animals from seeing people or moving equipment (56, 57).

Does Line Speed Affect Welfare?

Problems occur when equipment is pushed beyond its design capacity or when a system is understaffed. The average percentage of electric-prodded cattle was slightly higher and stunning scores were the same in high—line speed plants of over 250 cattle per hour compared with low—line speed plants of fewer than 50 cattle per hour. There were 16 plants in the low-speed category and six in the high-speed category. The average percentages of cattle moved with an electric prod were 19.8% and 25.1%, and the percentage of cattle rendered insensible with a single shot from a captive bolt was 96.2% at low speed and 96.7% at high speed (28).

Captive Bolt Stunning

In this section, only the most important studies and reviews are covered. A penetrating captive bolt gun has a retractable rod that penetrates and does extensive physical damage to the brain. Penetrating captive bolts used in almost all US beef plants that conduct conventional slaughter. Penetrating captive bolt, when it is applied correctly, will induce instant insensibility and unconsciousness, because visually evoked potentials are eliminated from the brain (58, 59). This demonstrates that the brain is totally non-responsive to a light flashed in the eye. To reliably produce instant insensibility, the bolt must have sufficient bolt velocity to cause an extensive concussion in addition to brain penetration (60). The minimum bolt velocity is 55 m/s for steers and 70 m/s for bulls (61, 62). The captive bolt must be placed in the correct location on the animal’s forehead to be effective. In cattle, the frontal position on the forehead is more effective (62). Shooting behind the poll should be used only as a secondary position, because positioning the captive bolt at the correct angle is more difficult. Care must be taken to avoid shooting the nape of the neck, because this position will not reliably induce insensibility (63).

Causes of Captive Bolt Failure

The four main causes of captive bolt failure to render an animal insensible with one shot are: (a) lack of maintenance, (b) damp cartridges in cartridge-fired captive bolts, (c) low air pressure in pneumatic captive bolt guns, or (d) agitated animals that make it difficult to position the stunner. A survey conducted in 10 beef slaughter plants found that lack of daily maintenance was the number one cause of captive bolt failure (64). Both cartridge-fired and pneumatic captive bolt guns have to be cleaned every day and have parts replaced per the manufacturer's instructions. They are manufactured from highly machined parts, and they require the same type of care as firearms. When a major restaurant company started auditing beef slaughter plants, stunning improved owing to better maintenance. Before the restaurant audits started, only three plants out of ten could shoot 95% of the cattle with a single shot (65). In 2010, data collected during animal welfare audits by restaurant companies showed that all 30 of the audited plants were capable of achieving this (66). Most plants now have test stands to measure bolt velocity. This ensures that the captive bolt is operating correctly after it has been serviced in the plant's maintenance shop. On guns powered by compressed air, the air supply must not be neglected. The author has observed plants in which the pneumatic stunner was in good working order, but the air compressor was either undersized or malfunctioning. Another problem is a plant that carefully maintains its main stunners but neglects the guns used out in the lairage to shoot downed, non-ambulatory and compromised animals that arrive on the trucks. When cartridge-fired guns are used, the blank cartridges must be stored in a dry location. Soft-sounding shots caused by damp cartridges or other factors reduce effectiveness (65, 67).

Assessing the Efficacy of Captive Bolt Stunning in Commercial Slaughter Plants

The efficacy of captive bolt stunning can be assessed by scoring the percentage of animals that are rendered completely insensible with a single shot. The voluntary industry standard is that 95% of the animals rendered insensible with a single shot would be an acceptable score and that 99% of the animals rendered insensible with a single shot would be an excellent score (66). Data collected in 66 beef plants showed that the average percentages of cattle, (excluding bulls) rendered insensible with a single shot was 97% (28). None of the plants used ahead restraint. An animal that needs a second shot must be reshot immediately before it is hoisted or has invasive dressing procedures done on it. There is zero tolerance for hoisting or starting dressing procedures such as skinning on any animal that shows any signs of return to sensibility. Rendering bulls and animals with very heavy skulls insensible with a single shot from a captive bolt was shown to be a problem in two studies (62, 65). Some plants have solved this problem by using a large-caliber firearm with a free bullet. The author has observed that this is effective, but there are safety concerns. All the studies, except for data collected in 2010, were conducted before newer, more powerful captive bolt guns, such as the Jarvis pneumatic, became available. The Jarvis pneumatic is used in many large plants that have a center—track conveyor restrainer. The author has observed that it_is more effective than many other cartridge-fired or pneumatic captive bolt guns. Because it is heavy and bulky, head restraint is required when the Jarvis pneumatic is used in a conventional stun box. There is a need for more research on the newer, more powerful captive bolt guns.

Some plants routinely do additional “insurance" shots to make sure an animal will remain unconscious. This is a good practice that will improve animal welfare. When captive bolt stunning is being assessed, the inspector or auditor should examine the animal for insensibility before the second stun is applied. The plant must be able to demonstrate that it is achieving instantaneous insensibility in 95% or more of the animals with a single shot.

Electric Stunning

Electric stunning induces instantaneous unconsciousness by causing a grand mal epileptic seizure (68, 69). To reliably induce a seizure, the electrodes must be placed so that the current flows through the brain (70). The minimum amperages for effective electrical stunning are 1 amp for sheep, 1.25 amps for pigs, and 1.5 amps for cattle (53). Research in four pig slaughterhouses indicated that, because some pigs were not rendered unconscious at the recommended amperages, it is recommended to use outcome measures such as signs of return to sensibility (71). The most effective frequency is the standard 50- or 60-cycle current. High frequencies of 2000 and 3000 hz are not effective (72). Frequencies of 1592 Hz sine wave or 1642 Hz square wave will induce insensibility in small pigs, and the period that the animal remains insensible will be shorter (73). Applying 800 hz to the head followed by a 50 hz electrical current to the body is effective (74). Plant managers are often tempted to use higher frequencies because they reduce blood spotting in the meat.

Types of Electric Stunners

There are three basic methods for electric stunning. They are head-only reversible, head-to-body cardiac arrest, and head-only followed by a current applied to the body to stop the heart. A head-only stun is temporary. The animal will return to sensibility and recover completely unless it is bled quickly. Bleeding within 15 s after the head-only stunner is removed is strongly recommended (75). Pigs will return to sensibility within 30 s after head-only stunning (76). Head—only electrical stunning is used on pigs and sheep in many small slaughter plants. The author has observed problems with animals returning to sensibility before bleeding. This is a result of the use of a slow hoist for lifting the animals up after stunning. To prevent return to sensibility, cardiac arrest can be achieved easily by applying the stunning tongs a second time to the side of the body immediately after the head stun (77). This is an easy way to fix a very severe animal welfare problem, and no additional equipment is required. To prevent meat quality problems, the electrode is applied right behind the foreleg. Head-only stunning is also used in plants in New Zealand prior to halal (Muslim) slaughter (48). Some Muslim religious authorities will allow electric head-only stunning because it is completely reversible and because during slaughter the animal dies as a result of bleeding. The author has observed excellent beef and sheep halal plants in Australia and New Zealand, They have high-speed, expensive equipment to facilitate bleeding within 10 s.

Most large US pork and sheep plants use head-to-body cardiac arrest stunning. When this method is used, the current is passed simultaneously through both the brain and the heart to induce both cardiac arrest and instantaneous insensibility (78). In large slaughter plants, the most common causes of return to sensibility after cardiac arrest electric stunning are incorrect electrode placement and poor bleeding (79). Most electrical stunning problems can be solved easily by careful attention to details such as electrode placement. The author has observed also that dehydrated animals are more difficult to render unconscious with electricity.

Out of 19 pork plants that were equipped with a V conveyor restrainer, 13 placed the electric stunner correctly on 100% of the pigs and achieved 100% insensibility (79). From 100 to 200 pigs were assessed in each plant, and all the plants used cardiac arrest stunning during which the current is applied simultaneously to both the head and the body. When a restrainer is used, it is easier to place the electrodes in the correct position on the head and hold them firmly against both the head and the body.

Avoiding Problems with Electric Stunning

When electric stunning fails to induce an unconscious state on the first attempt, it may be highly stressful no the animal. In humans, when electro-convulsive shock therapy (ECT) fails to induce a seizure, it is painful and distressing (80, 81). The ECT device used to induce a seizure in humans has similar electrical parameters of 170-240 volts and 0.85 amps (79). When electrical stunning fails to induce a seizure, the animal will feel the effects of epinephrine secretions and may feel pain (72, 80). When the stunner is applied correctly, the unconscious animal will not feel the effects of epinephrine secretion. When electric stunning is done correctly, sheep will not react with increased heart rate or glucose secretion to a light that has been paired with repeated head-only electrical stuns (83). In humans, 75% of patients who received unmodified ECT without anaesthesia reported that the procedure was not stressful (84). Good electrode contact with the head is essential. Rats that received electro-convulsive shock to wound clips attached to the ears became fear conditioned to the place where the shock was applied (85). The electrodes in the sheep experiment were applied to the temporal fossae on the head and not to the ears.

Monitoring the Quality of Electric Stunning

An electric stunner must reliably induce a tonic (rigid) and a clonic (leg-paddling) phase, which indicates that a seizure was induced. Cardiac arrest stunning masks the clinical signs of a seizure. Usually a weaker attenuated tonic and clonic phase can still be observed (48). The electrodes must be applied firmly to the head before the electric stunner is energized. Energizing the tongs before firm contact is achieved will result in a short squeal from a pig, which probably indicates pain. In 10 of 17 plants in which pigs were held in a V conveyor restrainer, 0% of the pigs squealed when the stunner was applied (27). Research with an oscilloscope showed that failure to press the electrodes firmly against the head will result in a partial current flowing when the electrode first contacts the animal (62). When the electrode is pressed firmly, the entire current passes through the animal. It is possible that the adverse effects reported by some humans owe to poor electrode contact.

CO2 Stunning

CO2 stunning equipment consists of two basic types: small units in which pigs enter a gondola through a single-file race (chute) and large units in which a small group of pigs are moved into a gondola. The group system has no single—file race. In both types of units, the pigs are lowered into a pit containing CO2 gas.

Unlike captive bolt or electric stunning, CO2 gas stunning does not induce instantaneous unconsciousness. Some researchers report that CO2 is extremely aversive to pigs because the excitation phase occurs before loss of sensibility (86, 87). Other research done with the Yorkshire pig breed indicated that the excitation phase occurs after the pigs have become unconscious (88), When CO2 is used, the pigs should be rapidly exposed to 90% CO2 (89). The disagreement in research results may owe to genetic differences in pigs; for instance, there is evidence that pigs that have the halothane stress gene may have a worse reaction (90). Pig reactions to CO2 are highly variable (91), and there is likely a genetic basis. Some pigs had a peaceful induction, and others struggled violently and attempted to climb out the instant the gondola descended to the level of the gas (92). These pigs were definitely reacting to the gas because they did not react to initial gondola movement. In this study, white pigs with Yorkshire breed characteristics had a milder reaction than crossbred pigs with Hampshire coloration. It is likely that the pigs in this study were more genetically diverse because it was conducted before the large breeding companies introduced hybrid lean-type pigs. There is a huge need to conduct studies using objective genetic markers. The author visited Denmark to observe groups of pigs that had a low incidence of the halothane stress gene. They were in a special research CO2 chamber in which it was easy to view the animals walking around in a pen after they had been lowered into the CO2. A few animals backed up and sniffed, and all violent reactions occurred after the pigs had fallen over (loss of posture). After loss of posture, the pigs were probably unconscious when the violent reactions occurred. None of the pigs made an attempt to escape or climb the side of the chamber. Studies in people also have shown that reactions to CO2 are highly variable. Some people have anxiety and panic attacks, and for others there is little reaction (93).

Evaluating Gas Stunning

From a welfare perspective, it is the author’s opinion that the best way to evaluate any gas—stunning method is to observe the animal’s reaction when it is first exposed to the gas. Violent attempts to escape from the chamber before the animal falls over (loses posture) and becomes insensible clearly are not acceptable. However, some mild discomfort might be a reasonable trade-off because the CO2 group handling system reduces handling stress owing to elimination of electric prods. A study with Yorkshire x Landrace crossbred pigs showed that electric shocks were more aversive to pigs than exposure to CO2 (94). One of the most common problems that severely compromise animal welfare is a CO2 stunning machine that is undersized. When the line speed of the plant exceeds the capacity of the CO2 machine, two bad things may happen: The gondolas may be overloaded by forcing the pigs in on top of each other with electric prods, or the conveyor may be speeded up, resulting in exposure to gas that is not long enough to induce insensibility (95). The only way to remedy this problem is to purchase a more expensive, larger machine. Immersing pigs in 90% CO2 for 120 s resulted in only 6 % of the pigs having a corneal reflex compared with 15 % when they were immersed for only 90 s (see discussion of corneal reflex in the section on Determining Insensibility). Monitoring blood in the bleeding area with an ion-sensitive electrode may be used to ensure an adequate depth of anaesthesia (96).

Religious Slaughter: Slaughter Without Stunning

Slaughter without prior stunning for either kosher (Jewish) or halal (Muslim) is highly controversial from an animal welfare standpoint. There are two basic issues that must be examined. They are the method of restraint used to hold the animal and the actual throat cut itself. In the United States, a few small slaughter plants use highly stressful methods of restraint such as shackling and hoisting fully conscious, large cattle. The author has visited plants in which cattle were suspended by one leg, and 30% to 100% of the cattle bellowed and vocalized. It was impossible to observe or measure the animal’s reaction to throat cutting without stunning until it was held in a less stressful manner. When the cattle were restrained in a comfortable upright position, a skillful cut made with the special, long kosher knife caused less behavioral reaction than a hand waved in the face of the animal (97). Waving a hand vigorously in the animal’s face will often cause struggling in the head holder.

Differences Between Cattle and Sheep

Sheep become unconscious more quickly after slaughter without stunning compared with cattle owing to differences in anatomy. In cattle, the vertebral arteries can still supply blood to the brain after the carotids are cut. Sheep get almost all their blood supply to the brain via the carotids (98, 99), Sheep will lose sensibility and the ability to stand within 2 to 14 s, and most cattle lose sensibility and stop attempts to stand in 17-85 s (59, 100-105 ). Potential welfare issues during religious slaughter are greater for cattle than sheep. Good technique can greatly shorten the time required to lose sensibility. When good technique is used, over 90% of the cattle will collapse and lose sensibility within 30 s (Erika Voogd, personal communication, 2009). A European research study showed a similar result (106). In both studies, the cattle were held in an upright standing position. Some of the factors that shorten the time for cattle to collapse are: (a) a calm animal, (b) swift knife strokes, (c) release of pressure applied by the restraint device immediately after the cut, (d) a cut performed within 10 s after the head is restrained, and (e) avoidance of bending the neck with the head holder and keeping the bovine’s forehead parallel with the floor (107).

One of the causes of prolonged sensibility in cattle is a result of scaling off of the artery ends (false aneurysms) after the cut (108-1 10). Research has shown that sealing off of the arteries can be reduced by cutting the neck in the C1 (cervical one) position (111). The cut should be made posterior to the larynx and directed toward C1. Sealing off of the artery ends, which can reduce blood flow, does not occur in sheep (Neville Gregory, personal communication, 2011). Cutting cattle in the C1 position also cuts a sensory nerve, which may prevent the animals from experiencing discomfort caused by aspiration of blood (112). When an animal was restrained in a good upright restraint device, 36% (kosher) to 69% (halal) of the cattle aspirated blood (113). In a rotating box in which the animal is held on its back, the author has observed many animals aspirating blood.

The big issue is: Does the cutting of the throat without prior stunning cause pain? One research group reported that the pain of the throat cut was comparable with dehorning a calf (114). They used a 24.5-cm/mg knife on 109-107 kg veal calves, which may have been too short. It had been sharpened on a mechanical grinder instead of the hand whetstone that is used on kosher knives (115). The author has observed violent struggling in both sheep and cattle when the knife tip on a short knife gouges into the throat or when the wound is allowed to close back over the knife. Further observations by the author indicated that the only knife that is long enough to prevent gouging in adult cattle is the special, long kosher knife.

A correct kosher or halal cut is made by cutting across the throat and simultaneously cutting the carotid arteries, jugular veins, and trachea. Stab-type cuts must never be used for slaughter without stunning. Jewish texts have strict rules for knife length, not allowing the wound to close over the knife, and not hesitating during the cut (116). The knife is checked for nicks after each cut because nicks can cause pain. Research is needed to determine cutting positions and angles that induce rapid collapse and loss of sensibility more precisely. The use of different types of blades and sharpening methods also needs to be investigated.

Determining Insensibility

It is essential to confirm that an animal is insensible to pain and permanently unconscious before hoisting, skinning, or other invasive dressing procedures. The most important outcome of all stunning procedures is to produce insensibility to pain. After all types of stunning, the following signs of return to sensibility must be absent before dressing procedures begin (117):

The mistake made by many people when they evaluate insensibility is confusing reflexive kicking with return to sensibility. Kicking reflexes may be present after all types of proper stunning in unconscious animals (48). A total absence of kicking reflexes after captive bolt stunning may be an indicator of a poor stun with a shallower depth of insensibility (67). When electrical stunning successfully induces an epileptic seizure, there is a tonic (rigid) phase followed by a clonic (paddling»kicking) phase. When cardiac arrest electric stunning is used, the current that stops the heart will greatly reduce or eliminate the tonic and clonic spasm. Usually a feeble tonic and clonic phase can still be observed. A total absence of the tonic and clonic phase will owe to either failure to induce insensibility or very long stun times of over 5 s (48). The paddling reflexes occur because the circuits for reciprocal leg movements for walking are located in the spinal cord (118). When the brain is incapacitated, the walking circuit becomes over-active.

Because electric stunning and CO2 stunning do not physically destroy the brain, an animal that is completely unconscious may have a weak corneal reflex (77). Corneal reflexes may be present in electrically stunned sheep when visual and somatosensory responses are abolished. Evoked responses are measured by recording electrical signals from the brain that occur in response to light or touch. When evoked responses are absent, the animal is unconscious. After correctly applied electric stunning, the pupil may still respond to light (77). The secondary step of applying the electrode to the body cc stop the heart abolishes the following signs of return to sensibility: vocalization, rhythmic breathing, eye tracking, natural spontaneous blinking, and the righting reflex (77). The corneal reflex and pupil response to light are brain stem reflexes, and they occur when either an animal or a person is in a state of surgical anaesthesia (119).

Captive bolt or gunshot physically damages the brain, and the corneal reflex must be absent (67). The eyes must be opened and have a wide blank stare. Nystagmus (vibrating eye) or a rotated eye must be absent after captive bolt or gunshot (6 7). Gasping like a fish out of water or nystagmus may be present after properly done electric or C02 stunning.

Auditing Programs to Maintain High Standards

People manage the things they measure. Animal welfare specialists recommend the use of animal-based outcome measures to evaluate welfare (120). To keep handling and stunning at a high standard requires the continuous attention of the plant managers to prevent practices from deteriorating. Objective numerical scoring makes it possible for a manager to determine whether handling or stunning practices are improving or deteriorating. When major meat buyers use their economic power wisely, large changes can be made. For instance, audits conducted by major restaurant chains such as McD0na1d’s and Wendy’s International have resulted in major improvements (121, 122).

To pass a welfare audit, a plant must achieve an acceptable score on all five numerically scored outcome variables on the voluntary industry guideline (52). In each plant, either 100 animals or one hour of production is observed. Tested outcomes include:

For religious slaughter without stunning, the stunning scores are omitted. There are also acts of abuse, which would be an automatic failure of an audit. They are: dragging non-ambulatory animals, poking sensitive parts of the animal, deliberately slamming gates on animals, deliberately driving an animal on top of another animal, and beating animals. All signs of return to sensibility must be absent before invasive dressing procedures such as skinning or leg removal are started. Even though an animal with a corneal reflex is probably unconscious, dressing procedures should be delayed until all eye reflexes are absent.

Remote Video Auditing

The newest tool to maintain high standards during handling and stunning is remote video auditing. When this system is used, auditors outside the plant can watch stunning, handling, and truck unloading over an internet link. This system solves the problem of people putting on a show and behaving correctly when they know somebody is watching. The Cargill Operation and JBS Swift have installed these systems in all of their North American beef plants (Mike Siemens, Cargill Corporation, personal communication, 2011). To use this technology in a positive manner, all of the Cargill plants receive all of the data. This creates competition to be the best plant. Each month the plant with the lowest electric prod scores gets a pizza party or other reward.

Are Slaughterhouses Humane? Future Directions for the Industry

The author is asked all the time, are all slaughterhouses as terrible as the ones shown in some of the videos taken by undercover investigators? Audits started by restaurant companies have resulted in great improvements, though there are still problems when nobody is watching. Further improvements have been brought about by the stepped-up enforcement of the Humane Slaughter Act with a directive to US Department of Agriculture/Food Safety and Inspection Service inspectors in 2011 (123). The plants most likely to have serious welfare issues are often small plants that are not audited by a customer. Some of these problems are a result of a lack of knowledge, and some owe to management having a poor attitude. One of the biggest frustrations during the author's long career is that everything can be working perfectly when the author is present and deteriorate after she leaves. Commitment to humane slaughter has to start with top management.

In conclusion, slaughterhouses can be operated with a high level of humane treatment. The author has taken many people on tours. When the plant is operating correctly, most people respond by saying they are surprised at how calm the animals are as they walk up the race to the stunner. Procedural details are very important. For example, the author has been in several plants in which cattle entered the restrainer very quietly when the entrance was illuminated with a lamp. When the lamp broke, the plant employees failed to replace it. This resulted in increased electric prod usage because the cattle refused to enter a dark chute. Management has to be attentive to such details. The meat industry has done a poor job communicating the improvements that have been made with the public. Plants chat are doing a good job should show what they are doing. Opening the doors electronically would be very easy with video streamed out to web pages.

Summary Points

  1. For best overall animal welfare, both the stunning method and the methods used to handle and restrain the animals should be evaluated as a whole system.

  2. At the slaughter plant, fear of a novel environment and not fear of death may be the main stressor to the animals. Animals often refuse to move through chutes if the entrance is too dark, if they see reflections on wet floors, or if they see moving people or machinery up ahead.

  3. In cattle and pigs, vocalization (moos, bellows, or squeals) in the stunning area are associated with obvious aversive events and physiological measures of stress.

  4. Compromised animals such as newborn calves, emaciated old cull animals, and weak animals that have difficulty walking are a major welfare problem and make humane slaughter difficult.

  5. Research validating the efficacy of different types of stunning methods and determining insensibility are covered in detail.

  6. When slaughter without stunning(kosher, halal,or on-farm) is evaluated from an animal welfare perspective, stressful methods of animal restraint may make it impossible to evaluate the animal’s reaction.

  7. It is important to use objective, outcome-based assessments of welfare, such as numerical scoring of the percentage of animals stunned incorrectly, percentage vocalizing, percentage falling during handling, and percentage moved with an electric prod.

  8. Maintaining high standards of animal welfare requires management commitment to welfare. Remote video auditing by auditors over the Internet is recommended strongly to prevent the problem of bad practices occurring when auditors are absent.

Disclosure Statement

The author is not aware of any affiliations, memberships, funding, or financial holdings that might be perceived as affecting the objectivity of this review.

Literature Cited

1. Grandin T. 2007. Handling and welfare of livestock in slaughter plants. In Livestock Handling and Transport, ed. T Grandin, pp. 329-53. Oxfordshire, UK: CABI Int.

2. Ewbank R, Parker MJ, Mason CW. 1992. Reactions of cattle to head restraint at stunning: a practical dilemma. Anim. Welf. 1:55-63.

3. Klingimair K, Stevens KB, Gregory NG. 2011. Luminare and glare in indoor handling facilities. Anim. Welf. 20:263-69.

4. Grandin T. 1980. 0bservations of cattle behavior applied to the design of cattle—handling facilities. Appl. Anim. Ethol. 6:19-31.

5. Tanida HA, Miura A, Tanaka T, Yoshimoto T. 1996. Behavioral response of piglets to darkness and shadows. Appl. Anim. Behav. Sci. 40:173-83.

6, Grandin T. 1996. Factors that impede animal movement at slaughter plants. J. Am. Vet. Med. Assoc. 209:757-59.

7. Van Putten G, Elshof WJ. 1978. Observations on the effects of transportation on the well-being and lean quality of slaughter pigs. Anim. Regul. Stud. 1:247-71.

8. Grandin T. 1982. Pig behavior studies applied to slaughter plant design. Appl. Anim. Ethol. 9:141-51.

9. Miller R, Schwartzkopf-Genswein, Shah MA, von Keyserlingk MA. 2008. Effect of neck injection and handling visibility on behavioral reactivity of beef steers. J. Anim. Sci. 86:1215-22.

10. Lanier JL., Grandin T, Green RD, Avery D, McGee K. 2000. The relationship between reaction to sudden intermittent movements and sounds and temperament. J. Anim. Sci. 78:1467-74.

11. Bourquet C, Deiss V, Grobert M, Durand D, Boissey A, Terlouw EMC. 2010. Characterizing the emotional activity of cows to understand and predict stress reactions to the slaughter procedure. Meat Sci. 125:9-21.

12. Leiner L, Fendt M. 2011. Behavioral fear and heartrate responses of horses after exposure to novel objects: effects of habituation. Appl. Anim. Behav. Sci. 131:104-9.

13. Pearson AJ, Kilgour R, de Langen H, Payne E. 1977. Hormonal responses of lambs to trucking, handling, and electric stunning. Proc. N. Z. Soc. Anim. Prod. 37:243-49.

14. Grandin T. 1997. Assessment of stress during handling and transport. J. Anim. Sci. 75:249-57.

15. Mitchell G, Hattingh J, Gahoe M. 1988. Stress in cattle assessed after handling, after transport and after slaughter. Vet. Rec. 123:201-5.

16. Cockram MS, Corley KTT. 1991. Effect of preslaughter handling on the behavior and blood composition of beef cattle. Br. Vet. J. 147:444-54.

17. Abbott TA, Hunter EJ, Guise JH, Penny RH. 1987. The effect of experience of handling pigs on willingness to move. Appl. Anim. Behav. Sci. 54:371-75.

18. Geverink NA, Kappers A, van de Burgwal JA, Lambooij E, Blockhuis JH, Wiegant VM. 1998. Effect of regular moving and handling on the behavior and physiological response of pigs to preslaughter treatment and consequences for subsequent meat quality. J. Anim. Sci. 76:2080-85.

19. Krebe N, McGlone JJ. 2009. Effects of exposing pigs to moving and odors in a simulated slaughter chute. Appl. Anim. Behav. Sci. 16:178-85.

20. Grandin T. 1987. Animal handling. Vet. Clin. N. Am. 3:323-38.

21. Grandin T, Deesing M. 2008. Humane Livestock Handling. Amherst, MA: Storey. 229 pp.

22. Hemsworth PH, Ric M, Karlen MG, Calleja L, Barnett JL., et al 2011. Human-animal interactions at the abattoir: relationships between handling and animal stress in sheep and cattle. Appl. Anim. Behav. Sci. 135:24-33.

23. Grandin T. 1998a. The feasibility of using vocalization scoring as an indicator of poor welfare during slaughter. Appl. Anim. Behav. Sci. 56:121-25.

24. Dunn CS. 1990. Stress reactions of cattle undergoing ritual slaughter using two methods of restraint. Vet. Rec. 126:22-25.

25. Warriss PD, Brown S, Adams SJM, 1994. Relationship between subjective and objective assessment of stress at slaughter and meat quality in pigs. Meat Sci. 38:329-40.

26. White RG, Deshazer JA, Tressler CJ, Borcher GM, Davey S, et al. 1995. Vocalizations and physiological responses of pigs during castration with and without anaesthetic. J. Anim. Sci. 73:381-96.

27. Grandin T. 2001. Cattle vocalizations associated with handling and equipment problems in slaughter plants. Appl. Anim. Behav. Sci, 71:191-201.

28. Grandin T. 2005. Maintenance of good animal welfare standards in beef slaughter plants by use of auditing programs. J. Am. Vet. Med. Assoc. 225:370-73.

29. Bourquet C, Deiss V, Tannugi CC, Terlouw EM. 2012. Behavioral and physiological reactions of cattle in a commercial abattoir: relationships with organizational aspects of the abattoir and animal characteristics. Meat Sci. 68:158-68.

30. Kilgour R, de Langen H. 1970. Stress in sheep from management practices. Proc. N.Z. Soc. Anim. Prod. 30:65-76.

31. Warner RD, Ferguson DM, Cottrell JJ, Knees BW. 2007. Acute stress induced by preslaughter use of electric prodders, causes tougher meat. Aust. J. Exp. Agric. 47:782-88.

32. Hambrecht E., Essein JJ, Newman DJ, Smits CHM, den Hartog LA, Verstegen MWA. 2005. Negative effects of stress immediately before slaughter on pork quality are aggravated by suboptimal transport and lairage conditions. J. Anim. Sci. 83:440-48.

33. Edwards L, Engle TE, Correa JA, Paradis MA, Grandin T, Anderson DB. 2010. The relationship between exsanguination blood lactate concentration and carcass quality in slaughter pigs. Meat Sci. 85:435-45.

34. Edwards LN, Grandin T, Engle TE, Porter SP, Ritter MJ, et al 2010. Use of exsanguination blood lactate to assess the quality of preslaughter handling. Meat Sci. 86:384-90.

35. Benjamin ME, Gonyou HW, Ivers DL, Richard LF. 2001. Effect of handling method on the incidence of stress response in market swine in a model system. J. Anim. Sci. 79(Suppl. 1):279.

36. Ahola JK, Foster HA, VanOverbeke DL, Jensen KS, Wilson RL, et al. 2011. Survey of quality defects in market beef and dairy cows and bulls sold through auctions in the Western United States: I. Incidence rates. J. Anim. Sci 89:1474-83.

37. Elanco APO602-25BPaylean 9 (label). Indianapolis, In: Elanco Anim. Health. http://www.elancocentral.com/paylean_label.pdf.

38. Marchant-Forde JN, Lay DC, Pajor JA, Rickert BT, Schinckel AP. 2003. The effects of ractopamine on the behavior and physiology of finishing pigs. J. Anim. Sci, 81:416-22.

39. Poletto R, Rostagno MH, Richert BT, Marchant-Forde JN. 2009. Effects of a "step up" ractopamine feeding program, sex, and social rank on growth performance, beef lesions, and Enterobacteriaceae shedding in finishing pigs. J. Anim. Sci. 87:304-11.

40. Poletto R, Cheng HW, Meisel RL, Garner JP, Richert BT, Marchant-Forde JN. 2010. Aggressiveness and brain amine concentrations in dominant and subordinate finishing pigs fed the B-adrenoreceptor agonist ractopamine. J. Anim. Sci. 88:3107-20.

41. Macias-Cruz U, Alveraz—Valenzuela FD, Torrentera-Olivera G, Velazquez—Morales JV, Correa-Calderon A, et al. 2010. Effect of zilpaterol hydrochloride on feedlot performance and carcass characteristics of ewe lambs during heat-stress conditions. Anim. Prod. Sci. 50:983-89.

42. Mader TL, Davis MS, Brcwn-Brandl T. 2005. Environmental factors influencing hear stress in feedlot cattle. Anim. Sci. 84:712-19.

43. Baszcazk JA, Grandin T, Gruber S, Engle TE, Platter WJ, et al. 2006. Effects of ractopamine supplementation on behavior of British, Continental, and Brahman crossbred steers during routine handling. J. Anim. Sci. 84:3410-14.

44. Vogel K. 2011. Investigating the impact of husbandry and management practices on the interaction of animal well-being and product quality in beef, swine, and dairy systems. PhD Diss. Colo. State Univ.

45. Grandin T. 1998. Handling methods and facilities to reduce stress on cattle. Vet. Clin. N. Am. Food Anim. Pract. 14:325-41.

46. Waynert NE, Stookey JM., Schwartzkopf-Genwein JM, Watts CS, Waltz CS. 1999. Response of beef cattle to noise during handling. Appl. Anim. Behav. Sci. 62:27-42.

47. Talling J, Warren NK, Wather CM. 1992. Behavioral and physiological responses of pigs to sound. Appl. Anim. Behav. Sci. 48:187-202.

48. Grandin T. 2010a. Improving Animal Welfare: A Practical Approach. Oxfordshire, UK: CABI.

49. Grandin T, Vogel KD. 2010. Restaurant Animal Welfare and Humane Slaughter Audits by U.S. Federally inspected Beef and Pork Slaughter Plants. http://www.grandin.com/survey/2011.restaurant.audits.html.

50. Grandin T. 2003. Transferring results of behavioral research to industry to improve animal welfare on the farm, ranch and the slaughter plant. Appl. Anim. Behav. Sci. 81:215-28.

51. Lemmon WB, Patterson GH. 1964. Depth perception in sheep: effects of interrupting the mother-neonate bond. Science 145:835-36.

52. Grandin T. 2012. Recommended Animal Handling Guidelines and Audit Guide. Washington, DC: Am. Meat Inst. Found. http://www.animalhandling.org.

53. OIE. 2009. Guidelines for the Slaughter of Animals for Human Consumption. Paris: World Organ. Anim. Health.

54. Westervelt RG, Kinsman D, Prince RP, Giger W Jr. 1976. Physiological stress measurements during slaughter of calves and lambs. J. Anim. Sci. 42:831-34.

55. Lambooji B, van der Werf JTN, Reimert HGM, Hindle VA. 2011. Restraining and neck cutting or stunning and neck cutting of veal calves. Meat Sci. 91:22-28

56. Grandin T. 1992. Observations of cattle restraint devices for stunning and slaughtering. Anim. Welf. 1:85-91.

57. Grandin T. 1991. Double rail restrainer for handling beef cattle. Paper No.. 91-5004. St. Joseph, MI: Am. Soc. Agric. Eng.

58. Daly CC, Gregory NG, Wotton SB, Whittington PE. 1986. Concussive methods of pre—slaughter stunning of sheep: assessment of brain function using cortical evoked responses. Res. Vet. Sci. 41:349-52.

59. Daly CC, Kallweit E, Ellendorf F. 1988. Cortical function in cattle during slaughter: conventional captive bolt stunning followed by exsanguination compared to shechita slaughter. Vet. Rec. 122: 325-29.

60. Daly CC, Whittington PE. 1989. Investigation into the principal determinants of effective captive bolt stunning in sheep. Res. Vet. Sci. 46:406-8.

61. Daly CC, Gregory NG, Wotton SE. 1987. Captive bolt stunning of cattle: effects on brain function and role of bolt velocity. Br. Vet. J. 143:574-80.

62. Gregory NG. 2007. Animal Welfare and Meat Production. Oxfordshire, UK: CABI International. 299 pp. 2nd ed.

63. Lambooy E, Spanjaard W. 1981. Effect of shooting position on stunning calves captive bolt. Vet. Rec. 109:359-61.

64. Grandin T. 1998e. Objective scoring of animal handling and stunning practices in slaughter plants. J. Am. Vet. Med. Assoc. 212:36-39.

65. Grandin T. 2002. Return to sensibility problems after penetrating captive bolt stunning of cattle in commercial plants. J. Am. Vet. Med. Assoc. 221:1258-61.

66. Grandin T, Vogel KD. 2010. 2010 Restaurant Welfare and Human Slaughter Audits in Federally Inspected Beef and Pork Slaughter Plants http://www.grandin.com/survey/2010.restaurant.audits.html.

67. Gregory NG, Lee CJ, Widdicombe JP. 2007. Depth of concussion in cattle shot by penetrating captive bolt. Meat Sci. 77:499-503.

68. Croft PS. 1952. Problems with electric stunning. Vet. Rec. 64:255-58.

69. Lambooij E. 1982. Electrical stunning of sheep. Meat Sci. 6:123-35.

70. Anil MH, McKinstry JJ. 1998. Variation of electrical tong placements and relative consequences in slaughter pigs. Vet. J. 155:85-90.

71. Végh A, Abonyi—Toth Z, Rafai P. 2010. Verification of the technical parameters of head-only electrical stunning of pigs under commercial conditions. Acta Vet. Hung. 58:147-58.

72. Warrington PD. 1974. Electrical stunning: a review of literature. Vet. Bull. 44:617-33.

73. Anil AM, McKinstry JL. 1994. The effectiveness of high frequency electrical stunning in pigs. Meat Sci. 31:481-91.

74. von Wenzlawowicz M, Schutte A, von Hollenbon K, von Altrock AV, Bostelmann N, Roeb S. 1999. Field study on the welfare and meat quality aspects of Midas-pig-stunning device. Fleischwirtschaft 2:8-13.

75. Blackmore DK, Newhook JC. 1981. Insensibility during slaughter of pigs in comparison to other domestic stock. N. Z. Vet. J. 29:219-22.

76. Hoenderken R. 1983. Electrical and carbon dioxide stunning of pigs for slaughter. In Stunning of Animals for Slaughter, ed. G Eikelenboom, pp. 59-63. Boston: Martinus Nijhoff.

77. Vogel KD, Badtram G, Claus JR, Grandin T, Turpin S, et al. 2011. Head only followed by cardiac arrest electrical summing in an affective alternative to head only electrical stunning in pigs. Meat Sci. 89:1412-18.

78. Lambooy E, Spanjaard W. 1982. Electrical stunning of veal calves. Meat Sci. 6:15-25.

79. Grandin T. 2001. Solving return to sensibility problems after electrical stunning in commercial pork slaughter plants. J. Am. Vet. Med. Assoc. 219:608-11.

80. Zivotofsky AZ, Strous RD. 2011. A perspective on the electrical stunning of animals: Are there lessons to be learned from human electroconvulsive therapy (ECT)? Meat Sci. 90:956-61.

81. Chanpattana W. 2001. Seizure threshold in electroconvulsive therapy: effect of instrument titration schedule. German J. Psychiat. 4(3):51-56.

82. Weaver LA Jr, Williams RW. 1986. Stimulus parameters and electroconvulsive therapy. Ann. N.Y. Acad. Sci. 462:174-85.

83. Leach TM, Warrington R, Wotton B. 1980, Use of conditioned stimulus to study whether the initiation of electrical pre-slaughter stunning is painful. Meat Sci. 4:203-8.

84. James BO, Morakinyo O, Lawani AO, Oroeregba JO, Oloto OS. 2010. Unmodified electro-convulsive therapy: the perspective from patients in a developing country. J. ECT 26:218-22.

85. Friedman MH. 1953. Electroconvulsive shock as a traumatic (fear-producing) experience in the albino rat. J. Abnorm. Soc. Psychol. 48:555-62.

86. Hoenderken. 1976. Improved design for guiding pigs to the restrainer. Die Fleischwirstch. 56:838-39.

87. Rodriguez P, Dalmau A, Ruiz—de—la-Torre JL, Manteca X, Jensen EW, et al. 2008. Assessment of unconsciousness during carbon dioxide stunning in pigs. Anim. Welf. 17:341-49.

88. Forslid A. 1987. Transient neocortical hippocampal and amygdaloid EEG silence induced by one minute inhalation of high concentration CO2 in swine. Acta Physiol. Scand. 130:1-10.

89. Becerril-Herrera M, Alonso»Spilsbury M, Lemus-Flores C, Guerrero-Legarreta I, Olmos-Hernandez A, et al. 2009. CO2 stunning may compromise swine welfare compared to electrical stunning. Meat Sci. 81:233-37.

90. Troeger K, Wolsterdorf W. 1991. Gas anaesthesia of slaughter pigs. Fleischwirstch. Int. 4:43-49.

91. Dodman NH. 1977. Observations on the use of the Werberg dip—lift carbon dioxide apparatus for - preslaughter anaesthesia of pigs. Br. Vet. J. 133:71-80.

92. Grandin T. 1988. Possible generic effect on pig’s reaction to CO2 stunning. Proc. 34th Int. Congr. Meat Sci Technol., Brisbane, Aust., pp. 96-97. Clayton, Aust.: CSIRO. 93. Griez E., Zandbergen J, Pols H, et al. 1990. Response to 35% CO2 as a marker for panic and severe anxiety. Am. J. Psychiatry 147:796-97.

94. Jongman EC, Barnett H., Hemsworth PH. 2000. The aversiveness of carbon dioxide stunning in pigs and a comparison of CO2 system vs. the V-restrainer. Appl. Anim. Behav. Sci. 67:67-76.

95. von Wenzlawowicz M, von Hollenben K and Eser E. 2012. Identifying reasons for stun failures in slaughter houses for mule or pigs: a field study. Anim. Welf. 21(52):51-60.

96. Hartmann H, Siegling-Vitakis C, Rinderman G, Fries R. 2009. Different CO2 stunning procedures and post mortem obtained lung lesions in response to the corneal reflex and parameters in blood of slaughtered pigs. Berl. Munich. Tierarztl. Wochenschr. 122:333-40.

97. Grandin T. 1994. Euthanasia and slaughter of livestock. J. Am. Vet. Med. Assoc. 204:1354-60.

98. Baldwin BA, Bell FR. 1963. The effect of temporary reduction in cephalic blood flow on the EEG of sheep and calf. Electroencephalogr. Clin. Neurophysiol. 15:465-73.

99. Baldwin BA, Bell FR. 1963. The anatomy of the cerebral circulation of the sheep and ox: the dynamic distribution of the blood supplied by the carotid and vertebral arteries to cranial regions. J. Anat. 97:203-15.

100. Blackmore DK. 1984. Differences in behavior between sheep and cattle during slaughter. Res. Vet. Sci. 37:223-36.

101. Nangeroni LI, Kennett PD, 1963. An electroencephalographic study of the effects of shechita slaughter on cortical function in ruminants, Report, Dept. Physiol., NY State Vet. Coll., Cornell Univ.

102. Newhook JC, Blackmore DK. 1982. Electroencephalographic studies of stunning and slaughter in sheep and calves: part I -- the onset of permanent insensibility in sheep during slaughter. Meat: Sci. 6:295—300.

103. Schulz W, Schulze-Petxold H, Hazam AS, Grass R. 1978, Experiments for the objectification of pain and consciousness during conventional (captive bolt stunning) and religiously mandated ("ritual cutting") slaughter procedures for sheep and calves. Dtsch. Tierarztl. Wochenschr. 85:41-76.

104. Gregory NG, Wotton SB. 1984. Time to loss of brain responsiveness following exsanguination in calves. Res. Vet. Sci. 37:141-43.

105. Blackmore DK, Newhook JC, Grandin T. 1983. Time of onset of insensibility in four- to six-week-old calves during slaughter. Meat Sci. 9:145-49.

106. Gregory NG, Fielding HR, von Wenzlawowicz M, von Hollenben KV. 2010. Time to collapse following slaughter without scanning of cattle. Meat Sci. 85:66-69.

107. Grandin T, Regenstein JM. 1994. Religious slaughter and animal welfare: a discussion for meat scientists, In Meat Focus International, pp. 115-23. Oxfordshire, UK:CABI.

108. Gregory NG, von Wenzlawowicz M, Alam RM, Anil HM, Yesildere T, Silva-Fletcher A. 2008. False aneurysms in carotid arteries of cattle and water buffalo during shechita and halal slaughter. Meat Sci. 80:2-11.

109. Anil MH, McKinstry JL, Wotton SB, Gregory NG. 1995. Welfare of calves -- 1. Investigation into some aspects of calf slaughter. Meat Sci. 41:101-12.

110. Anil MH, McKinstry JL, Gregory NG, Woman SB, Symonds H. 1995. Welfare of calves -- 3. Increase in vertebral artery blood flow following exsanguination by neck sticking and evaluation of chest sticking as alternative slaughter method. Meat Sci. 41:113-23.

111. Gregory NG, Schuster P, Mirabito I., Kolesar R, McManus T. 2012. Arrested blood flow during false aneurysm formation in the carotid arteries of cattle slaughtered with and without stunning. Meat Sci. 90:368-72.

112. Gregory NG, von Wenzlawowicz M, von Hollenben K, Fielding HR, Gibson TJ, er al. 2012. Complications during shechita and halal slaughter without stunning in cattle. Anim. Welf. 21(Suppl.2):81-86.

113. Gregory NG, von Wenzlawowicz M, von Hollenben KV. 2008. Blood in the respiratory tract during slaughter without stunning in cattle. Meat Sci. 82:13-16.

114. Gibson TJ, Johnson CB, Murrell JC, Hulls CM, Mitchinson SL, et al. 2009. Electroencephalographic responses of halothane-anaesthetised calves to slaughter by ventral-neck incision without prior stunning. N. Z. Vet. J. 57:77-85.

115. Gibson TJ, Johnson CB, Murrell JC, Chambers JP, Stafford KJ, Mellor DJ. 2009b. Components of electroencephalographic responses to slaughter in halothane-anaesthetized calves. Effects of cutting neck tissues compared to major blood vessels. N. Z. Ven J. 57:84-89.

116. Epstein L, ed. 1943. The Babyonian Talmud. London: Socino.

117. Grandin T. 2010b. Auditing animal welfare at slaughter plants, Meat Sci. 86:56-65.

118. Grillner S, 2011. Human locomotion circuits conform. Science 334:912-13.

119. Rumpl E, Gerstenbrand F, Hackl JM, Prugger M, 1982. Some observations on the blink reflex in post-traumatic coma, Electroencephalogr. Clin. Neurophysiol. 54:406-17

120. Wray HR, Main DCJ, Green LE, Webster AJF. 2003. Assessment of the welfare of dairy cattle using animal-based measurements: direct observations and investigation of farm records. Vet. Rec. 153:197-202.

121. Grandin T, 2000. Effect of animal welfare audits by a major fast food company on cattle handling and stunning practices. J. Am. Vet. Med. Assoc. 216:848-51.

122. Grandin T. 2006. Progress and challenges in animal handling and slaughter in the U.S. Appl. Anim. Behav. Sci. 100:129-39.

123. US Dept. Agric. Food Saf. Insp. Serv. 2011. Directive 6900.2: Humane Handling and Slaughter of Livestock, Revision 2. Washington, DC: US Dept. Agric. Food Saf. Insp. Serv.


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