Animal health emergencies that affect domestic livestock are a threat to the economy and stability of US animal agriculture. An outbreak of an infectious transboundary or foreign animal disease such as foot and mouth disease would have a severe negative economic effect on US animal agriculture as well as global consequences.1,2 In the event of an epizootic disease outbreak involving a foreign animal disease in the United States, USDA APHIS personnel in conjunction with relevant federal, state, tribal, and local entities will coordinate disease eradication plans in an attempt to prevent widespread losses. Those disease eradication plans may include mass depopulation of large commercial livestock operations. The USDA defines mass depopulation as “a method by which large numbers of animals must be destroyed quickly and efficiently with as much consideration given to the welfare of the animals as practicable.”3 If depopulation is chosen as a method to control or eradicate disease during an AHE, the USDA is committed to complying as closely as possible with the recommendations outlined in the Terrestrial Animal Health Code established by the World Organization for Animal Health4 and the AVMA Guidelines for the Euthanasia of Animals.5
In the United States, a major challenge in preparing and planning for mass depopulation in response to an AHE is the sheer number of cattle on individual farms, ranches, and feedlots. There are currently > 90 million cattle in the United States,6 with more than a third of those cattle maintained on operations with > 1,000 cattle.7 Current technology and traditional approaches to the depopulation of cattle operations may not be adequate to meet the speed and urgency required for a response to an AHE, let alone assure that animals will be euthanized during such a response.8 Thus, a rapid, portable, and consistently effective euthanasia method is an essential requirement for mass depopulation of livestock operations during an AHE response.
A suitable depopulation method must be publicly acceptable, effective, legal, and safe for the personnel involved and cause as little stress as possible to the animals being euthanized. The AVMA Guidelines for the Euthanasia of Animals5 describe 3 acceptable methods for the euthanasia of cattle (barbiturate overdose, gunshot, and captive bolt with ancillary methods to assure death). Gunshot and barbiturate overdose are both 1-step methods for the euthanasia of cattle; however, both have limitations in depopulation situations. Barbiturate overdose involves use of a controlled drug, which requires detailed accounting of each milliliter of drug used and necessitates adequate animal restraint, technical expertise for IV administration of the drug, and safe and environmentally responsible carcass disposal. Gunshot requires either skilled marksmen or proper animal restraint and personnel experienced with firearms to ensure accurate bullet placement and human safety. Additionally, the public may perceive euthanasia by physical methods, whether gunshot or captive bolt, as inhumane. Although use of a penetrating captive bolt is an acceptable method for euthanizing cattle, use of an ancillary, or secondary, method is strongly recommended to ensure death.5,a However, in 1 study,a 28 of 31 adult cattle ≥ 24 months old and 17 of 19 cattle between 5 and 23 months old were euthanized by 1 shot from a penetrating captive bolt and did not require application of a secondary euthanasia method.
The need to implement a secondary euthanasia method to assure death would substantially increase the time required to depopulate a large farm or feedlot. However, use of a penetrating captive bolt with sufficient energy and bolt length might be capable of euthanizing cattle without the use of a secondary method and thereby increase the rate that mass depopulation could be performed. Air-injection captive bolt stunning was used on a limited basis in US slaughterhouses until it was prohibited on January 12, 2004, as part of an interim final ruling issued by the USDA Food Safety and Inspection Service following the detection of a cow with BSE in December 2003.9 That ruling9 designated the brain, trigeminal ganglia, eyes, tonsils, spinal cord, and dorsal root ganglia of cattle as SRMs and prohibited them from the human food supply because those tissues can contain the BSE prion, and humans who consume those tissues might develop variant Creutzfeldt-Jakob disease, which is always fatal.10 Because stunning cattle by use of an air-injection captive bolt might cause dissemination of CNS tissue into other tissues intended for human consumption, use of that device in slaughterhouses was prohibited.9 However, it is unlikely that cattle euthanized during depopulation in response to an AHE would be used for human consumption. The objective of the study reported here was to validate the effectiveness of a penetrating captive bolt device with a built-in low-pressure air channel pithing mechanism as a 1-step method for euthanasia of cattle.
Materials and Methods
Animals
Prior to initiation, all study procedures were reviewed and approved by the Iowa State University Institutional Animal Care and Use Committee (IACUC 2-12-7296-B). Sixty-six feedlot calves (15 heifers and 51 steers) that ranged in age from 6 to 19 months and weight from 227 to 500 kg (500 to 1,100 lb) from Iowa-based feedlot operations were enrolled in the study. Ten calves were individually weighed. The remaining calves were weighed in groups at the source feedlots immediately prior to transport to Iowa State University for euthanasia. For each group, the mean weight was calculated and recorded as the weight for each calf in that group. All calves enrolled in the study were designated by medical or support staff at the source feedlots as unlikely to survive or finish the feeding period with their cohorts. The reasons most frequently cited for such a designation were chronic respiratory tract disease and musculoskeletal disorders.
Study protocol
The study was completed during 7 nonconsecutive days between January and April 2014. Because all calves enrolled in the study were subjected to the same intervention (euthanasia by use of a PCBD), no attempt was made to keep researchers and other study personnel unaware of, or blinded to, any aspect of the study. Calves were transported from the source feedlots to the Iowa State University Lloyd Veterinary Medical Center or Livestock Infectious Disease Isolation Facility, a biosecurity level 2 facility in Ames, Iowa, on the morning they were scheduled to be euthanized.
PCBD
Each calf was euthanized with a PCBD.b The pithing mechanism was designed to inject air at a pressure of approximately 15 psi through the tip of the bolt from the point of full bolt extension to complete retraction back into the captive bolt muzzle and housing. The bolt diameter was 1.6 cm, and the length of the bolt beyond the muzzle was 15.2 cm.
The PCBD weighed approximately 13.6 kg (29.9 lb) and was mounted on a hoist system with an ergonomic balancer to assist in maneuvering it to the proper anatomical site during use. Compressed air for use in the PCBD was provided by a 10-hp gas-run air compressorc equipped with a multiset regulator that maintained a constant pressure of air for continuous use. A 300-psi rated high-pressure air hosed (length, 15.2 m [50 feet]) was used to link the compressor and regulator to the PCBD. The compressor and regulator were secured onto an aluminum trailer, which was used to transport all components to the study locations (Figure 1). Once at the study location, the trailer was parked adjacent to a chute equipped with a head catch. The hoist arm was secured on a swivel mount above the head catch in a position that allowed convenient maneuverability of the spring-loaded cable and PCBD to the desired position on the calf's skull.
Photograph depicting the components of a PCBD system used to euthanize 66 feedlot calves, with age ranging from 6 and 19 months and weight ranging from 227 to 500 kg (500 to 1,100 lb), that were considered unlikely to survive or finish the feeding period with their cohorts, generally because of chronic respiratory tract disease or musculoskeletal disorders. A 10-hp gas-run 2-stage air compressor (A) and multiset regulator (B) were mounted on an aluminum trailer that was used to transport the system to the study locations. The black box (C) was used for storage of equipment during transport. Once at the study location, the trailer was parked adjacent to a livestock chute equipped with a head catch, a hoist support arm (D) was secured on a swivel mount above the head catch, a spring-loaded cable (E) was attached to the support arm, and the PCBD (F) was suspended from the cable in a position that allowed convenient maneuverability to the appropriate position on the calf's head. A 300-psi high-pressure air hose (red) was used to link the compressor and regulator to the PCBD.
Citation: Journal of the American Veterinary Medical Association 248, 1; 10.2460/javma.248.1.96
Photograph depicting the components of a PCBD system used to euthanize 66 feedlot calves, with age ranging from 6 and 19 months and weight ranging from 227 to 500 kg (500 to 1,100 lb), that were considered unlikely to survive or finish the feeding period with their cohorts, generally because of chronic respiratory tract disease or musculoskeletal disorders. A 10-hp gas-run 2-stage air compressor (A) and multiset regulator (B) were mounted on an aluminum trailer that was used to transport the system to the study locations. The black box (C) was used for storage of equipment during transport. Once at the study location, the trailer was parked adjacent to a livestock chute equipped with a head catch, a hoist support arm (D) was secured on a swivel mount above the head catch, a spring-loaded cable (E) was attached to the support arm, and the PCBD (F) was suspended from the cable in a position that allowed convenient maneuverability to the appropriate position on the calf's head. A 300-psi high-pressure air hose (red) was used to link the compressor and regulator to the PCBD.
Citation: Journal of the American Veterinary Medical Association 248, 1; 10.2460/javma.248.1.96
Photograph depicting the components of a PCBD system used to euthanize 66 feedlot calves, with age ranging from 6 and 19 months and weight ranging from 227 to 500 kg (500 to 1,100 lb), that were considered unlikely to survive or finish the feeding period with their cohorts, generally because of chronic respiratory tract disease or musculoskeletal disorders. A 10-hp gas-run 2-stage air compressor (A) and multiset regulator (B) were mounted on an aluminum trailer that was used to transport the system to the study locations. The black box (C) was used for storage of equipment during transport. Once at the study location, the trailer was parked adjacent to a livestock chute equipped with a head catch, a hoist support arm (D) was secured on a swivel mount above the head catch, a spring-loaded cable (E) was attached to the support arm, and the PCBD (F) was suspended from the cable in a position that allowed convenient maneuverability to the appropriate position on the calf's head. A 300-psi high-pressure air hose (red) was used to link the compressor and regulator to the PCBD.
Citation: Journal of the American Veterinary Medical Association 248, 1; 10.2460/javma.248.1.96
Immediately prior to use of the PCBD on each day, the device was mounted on a pneumatic stunner testere to determine bolt speed and assure that the device was working properly. The speed of the bolt was determined by measuring the time it took for the bolt to pass 2 proximity switches in the stunner tester. Bolt speed was considered acceptable if the tester measurement was < 1,650 (ie, < 0.00165 seconds).
The PCBD was designed with 2 triggers, a main handle trigger and an auxiliary handle trigger (Figure 2). The PCBD was guided to the proper anatomic site on the calf's skull. The main handle trigger was depressed to load the housing with compressed air and arm the PCBD. Then, the auxiliary handle trigger was depressed to activate the PCBD so that when the spring-loaded head contact was pressed against the calf's skull with sufficient force to compress the spring, the device would fire. The optimal site for application of the PCBD was the midline of the frontal aspect of the skull approximately halfway between an imaginary line drawn from the lateral canthus of 1 eye to the lateral canthus of the opposite eye and another imaginary line drawn parallel to the first across the most dorsal aspect of the head (poll)a (Figure 3).
Photograph of the PCBD used in the system depicted in Figure 1. Depression of the main trigger (A) loads the housing with compressed air and arms the device. Depression of the auxiliary trigger (B) activates the PCBD so that the device will fire when the spring-loaded head contact (C) is pressed against the skull with sufficient force to compress the spring. See Figure 1 for remainder of key.
Citation: Journal of the American Veterinary Medical Association 248, 1; 10.2460/javma.248.1.96
Photograph of the PCBD used in the system depicted in Figure 1. Depression of the main trigger (A) loads the housing with compressed air and arms the device. Depression of the auxiliary trigger (B) activates the PCBD so that the device will fire when the spring-loaded head contact (C) is pressed against the skull with sufficient force to compress the spring. See Figure 1 for remainder of key.
Citation: Journal of the American Veterinary Medical Association 248, 1; 10.2460/javma.248.1.96
Photograph of the PCBD used in the system depicted in Figure 1. Depression of the main trigger (A) loads the housing with compressed air and arms the device. Depression of the auxiliary trigger (B) activates the PCBD so that the device will fire when the spring-loaded head contact (C) is pressed against the skull with sufficient force to compress the spring. See Figure 1 for remainder of key.
Citation: Journal of the American Veterinary Medical Association 248, 1; 10.2460/javma.248.1.96
Photograph of the frontal aspect of a calf's head illustrating the optimal site (+) for application of the PCB used in this study. The ideal site is on the midline halfway between a line drawn from the lateral canthus of 1 eye to the lateral canthus of the opposite eye and another line drawn parallel to the first at the most dorsal aspect of the head (poll). (Adapted from photograph obtained from Dr. Dee Griffin, Great Plains Veterinary Educational Center, University of Nebraska, Clay Center, Neb. 2015. Reprinted with permission).
Citation: Journal of the American Veterinary Medical Association 248, 1; 10.2460/javma.248.1.96
Photograph of the frontal aspect of a calf's head illustrating the optimal site (+) for application of the PCB used in this study. The ideal site is on the midline halfway between a line drawn from the lateral canthus of 1 eye to the lateral canthus of the opposite eye and another line drawn parallel to the first at the most dorsal aspect of the head (poll). (Adapted from photograph obtained from Dr. Dee Griffin, Great Plains Veterinary Educational Center, University of Nebraska, Clay Center, Neb. 2015. Reprinted with permission).
Citation: Journal of the American Veterinary Medical Association 248, 1; 10.2460/javma.248.1.96
Photograph of the frontal aspect of a calf's head illustrating the optimal site (+) for application of the PCB used in this study. The ideal site is on the midline halfway between a line drawn from the lateral canthus of 1 eye to the lateral canthus of the opposite eye and another line drawn parallel to the first at the most dorsal aspect of the head (poll). (Adapted from photograph obtained from Dr. Dee Griffin, Great Plains Veterinary Educational Center, University of Nebraska, Clay Center, Neb. 2015. Reprinted with permission).
Citation: Journal of the American Veterinary Medical Association 248, 1; 10.2460/javma.248.1.96
Each calf was blindfolded with its head restrained by use of a head gate and 2 halters to minimize any movement that might affect placement of the PCBD. When calf movement or operator error resulted in a misdirected shot from the PCBD, the calf was immediately reshot.
Clinical assessment and data collection
To reduce variability, all clinical evaluations, monitoring, and data recording were performed by the same investigator (KEK). Clinical variables assessed included heartbeat, cardiac electrical activity, corneal reflex, palpebral reflex, righting reflex, vocalization, respiration, and involuntary movement. Each calf was assessed immediately after the PCBD was fired and at 1-minute intervals for a minimum of 10 minutes. Clinical death was defined as lack of an auscultable heartbeat and absence of vocalization, coordinated movements, regular respiration, and discernable corneal, palpebral, and righting reflexes. Cardiac death was defined as ventricular standstill as determined by ECG.
Cardiac variables were assessed with a stethoscopef and a portable ECG monitoring system.g The head of the stethoscope was placed in the left axillary region immediately following use of the PCBD to auscultate the heart. The heartbeat was recorded as present as long as a consistent and rhythmic (ie, a heartbeat originating from the sinus node and occurring at regular intervals) beat was auscultated. The leads of a 4-lead ECG monitor were connected to each calf in a modified base-apex configuration as described,11 and an ECG trace was obtained at least 1 minute before and as soon as possible (within 180 seconds) after the PCBD was fired. Following the shot, the ECG trace was continuously monitored on a laptop computer for at least 10 minutes or until ventricular standstill occurred (cardiac death). Ventricular standstill was defined as cessation of discernable ventricular electrical activity, contractions, and cardiac output.
After calves were shot with the PCBD, corneal reflexes were assessed by gently touching the corneas with a finger. The corneal reflex was defined as present as long as the calf blinked in response to the finger touching the cornea. The palpebral reflex was assessed by gently stroking the dorsal eyelid with a finger; the palpebral reflex was defined as present as long as the calf blinked in response to the eyelid being stroked. A righting reflex was defined as present as long as the calf continued to position itself in sternal recumbency. Vocalization was considered present as long as the calf bawled, bellowed, or made other intentional noises. Involuntary movement was defined as uncoordinated musculoskeletal activity commonly observed when spinal nerves were no longer inhibited by the brain and included movements such as tonic spasms, paddling, flexion and extension of limbs, or other uncoordinated musculoskeletal activity that did not involve the head. Respiration was defined as rhythmic breathing and was assessed by observation of the thorax and placement of a hand in front of the calf's muzzle to detect air movement. An agonal gasp was not considered respiration.
Assessment of skull and brain trauma
After each calf was confirmed dead, its head was removed and the skull and brain were evaluated for location of shot placement and extent of trauma attributable to the PCBD. A veterinary pathologist (RJD) performed all postmortem assessments. The skull was disarticulated from the vertebral column at the atlanto-occipital joint. The entrance site of the bolt into the skull was identified and photographed. The skin was dissected and reflected to expose the frontal portion of the skull at the site of bolt entry. The hole formed by the PCBD was measured to determine the maximum diameter of the skull wound. Each skull was individually weighed, then cut in half along the sagittal plane with a band saw so that the skull thickness at the site of bolt penetration and the depth of bolt penetration could be measured. The brain was then removed from the calvarium and weighed.
Specific regions of the brain including the cerebrum, cerebellum, midbrain, pons, thalamus and hypothalamus, and medulla and spinal cord were assessed for tissue damage and hemorrhage. The extent of tissue damage and hemorrhage caused by the PCBD was scored on a scale of 0 to 3 as described in a study12 that involved water buffalos. Briefly, within each region of the brain evaluated, 0 = no tissue damage or disruption and no parenchymal hemorrhage, 1 = mild damage limited to hemorrhage or tissue displacement in < 25% of the region, 2 = moderate damage with tissue destruction in 25% to 75% of the region, and 3 = severe damage with > 75% of the region affected. After each region was scored, the scores for the thalamus and hypothalamus, midbrain, pons, and medulla were combined to calculate a consolidated brainstem damage score, which was reported on a scale of 0 to 4 (1 = combined score of 1 to 3, 2 = combined score of 4 to 6, 3 = combined score of 7 to 9, and 4 = combined score of 10). For total brain damage, the cerebrum damage score (all calves had a cerebral damage score of 1) was added to the total brainstem score to achieve a total brain damage score that ranged from 1 to 5. The extent of hemorrhage within each region was scored on the basis of the estimated percentage of subdural area affected on a scale of 0 to 3 (0 = no hemorrhage, 1 = > 0 to 25% hemorrhage, 2 = > 25% to 75% hemorrhage, and 3 = > 75% hemorrhage). Each region of the brain was evaluated for the presence of bone fragments, and if bone fragments were present, they were removed and counted. For each calf, the observed bolt path and extent of tissue damage were subjectively sketched by hand onto photocopies of brain and skull images in the dorsal, lateral, and sagittal planes obtained from an atlas of bovine anatomy.13
Statistical analysis
The unit of analysis for the study was each individual calf. Observations and assessments were recorded in either a spreadsheet or text document. Electrocardiographic data were saved in a commercially available ECG software programh and analyzed and interpreted as described.11 A commercially available statistical software programi was used to generate descriptive data for heartbeat, corneal reflex, palpebral reflex, righting reflex, vocalization, respiration, involuntary movement, brain regions damaged, number and location of skull fragments within the brain, and brain trauma scores. Linear regression was used to assess the coefficient of determination between body weight and head weight, head weight and time to clinical death (absence of an auscultable heartbeat), head weight and skull thickness, head weight and depth of bolt penetration, and skull thickness and time to clinical death. One-way ANOVA was used to evaluate the respective associations between trauma score and head weight, skull thickness, and time to clinical death. Finally, calves were categorized into 2 groups on the basis of whether the PCBD caused trauma to the brainstem, and the survival curves were compared between those 2 groups. The linear regression, ANOVA, and survival curve analyses were performed with another commercially available statistical software program,j and values of P < 0.05 were considered significant.
Results
Calves
All calves were successfully euthanized with the PCBD without the need for an ancillary method of euthanasia. However, 2 shots had to be applied to 2 calves and 3 shots had to be applied to another 2 calves to achieve successful euthanasia. Thus, the PCBD had to be fired 72 times to successfully euthanize 66 calves. On the basis of postmortem examination, all PCBD shots that entered the cranial vault were sufficient to cause death (ie, kill shots), and each calf received only 1 kill shot.
Corneal reflexes, righting reflexes, vocalization, and respiration were not observed in any of the calves after application of a kill shot. The mean time to clinical death (ie, no auscultable heartbeat) was 440 seconds (7.3 minutes; range, 92 to 865 seconds [1.5 to 14.4 minutes]). The mean time to cardiac death was determined for only 55 calves and was 501 seconds (8.3 minutes; range, 176 to 886 seconds [2.9 to 14.8 minutes]). Detailed results regarding the time to death on the basis of absence of an auscultable heartbeat and ECG data for a subset (n = 22) of the study population are reported elsewhere.11
For the 10 calves that were individually weighed, there was a significant (P < 0.004) positive correlation (R2 = 0.664) between live body weight and weight of the head. For all calves, the weight of the head was not significantly correlated with time to clinical death (R2 = 9.487 × 10−4; P = 0.806), skull thickness at the site of bolt penetration (R2 = 3.253 × 10−5; P = 0.964; Figure 4), or bolt penetration depth (R2 = 2.387 × 10−3; P = 0.699). Skull thickness at the site of bolt penetration was not significantly (P = 0.296) correlated with time to clinical death (R2 = 0.017).
Scatterplots of the weight of the head versus skull thickness at the site of bolt penetration (A), weight of the head versus brain trauma score (B), skull thickness at site of bolt penetration versus brain trauma score (C), and time to clinical death (absence of an auscultable heartbeat) versus brain trauma score (D) for the calves of Figure 1. Each dot represents 1 animal. Within each region of the brain evaluated, 0 = no tissue damage or disruption and no parenchymal hemorrhage, 1 = mild damage limited to hemorrhage or tissue displacement in < 25% of the region, 2 = moderate damage with tissue destruction in 25% to 75% of the region, and 3 = severe damage with > 75% of the region affected. After each region was scored, the scores for the thalamus and hypothalamus, midbrain, pons, and medulla were combined to calculate a consolidated brainstem damage score, which was reported on a scale of 0 to 4 (1 = combined score of 1 to 3, 2 = combined score of 4 to 6, 3 = combined score of 7 to 9, and 4 = combined score of 10). For total brain damage, cerebrum damage was added to the total brainstem score to achieve a total trauma score that could range from 1 to 5. Within each trauma score column in panels B–D, the middle horizontal line represents the mean and the outer horizontal lines represent the SEM for the variable on the y-axis. *The mean for the y-axis variable differs significantly between trauma scores linked by a bracket. See Figure 1 for remainder of key.
Citation: Journal of the American Veterinary Medical Association 248, 1; 10.2460/javma.248.1.96
Scatterplots of the weight of the head versus skull thickness at the site of bolt penetration (A), weight of the head versus brain trauma score (B), skull thickness at site of bolt penetration versus brain trauma score (C), and time to clinical death (absence of an auscultable heartbeat) versus brain trauma score (D) for the calves of Figure 1. Each dot represents 1 animal. Within each region of the brain evaluated, 0 = no tissue damage or disruption and no parenchymal hemorrhage, 1 = mild damage limited to hemorrhage or tissue displacement in < 25% of the region, 2 = moderate damage with tissue destruction in 25% to 75% of the region, and 3 = severe damage with > 75% of the region affected. After each region was scored, the scores for the thalamus and hypothalamus, midbrain, pons, and medulla were combined to calculate a consolidated brainstem damage score, which was reported on a scale of 0 to 4 (1 = combined score of 1 to 3, 2 = combined score of 4 to 6, 3 = combined score of 7 to 9, and 4 = combined score of 10). For total brain damage, cerebrum damage was added to the total brainstem score to achieve a total trauma score that could range from 1 to 5. Within each trauma score column in panels B–D, the middle horizontal line represents the mean and the outer horizontal lines represent the SEM for the variable on the y-axis. *The mean for the y-axis variable differs significantly between trauma scores linked by a bracket. See Figure 1 for remainder of key.
Citation: Journal of the American Veterinary Medical Association 248, 1; 10.2460/javma.248.1.96
Scatterplots of the weight of the head versus skull thickness at the site of bolt penetration (A), weight of the head versus brain trauma score (B), skull thickness at site of bolt penetration versus brain trauma score (C), and time to clinical death (absence of an auscultable heartbeat) versus brain trauma score (D) for the calves of Figure 1. Each dot represents 1 animal. Within each region of the brain evaluated, 0 = no tissue damage or disruption and no parenchymal hemorrhage, 1 = mild damage limited to hemorrhage or tissue displacement in < 25% of the region, 2 = moderate damage with tissue destruction in 25% to 75% of the region, and 3 = severe damage with > 75% of the region affected. After each region was scored, the scores for the thalamus and hypothalamus, midbrain, pons, and medulla were combined to calculate a consolidated brainstem damage score, which was reported on a scale of 0 to 4 (1 = combined score of 1 to 3, 2 = combined score of 4 to 6, 3 = combined score of 7 to 9, and 4 = combined score of 10). For total brain damage, cerebrum damage was added to the total brainstem score to achieve a total trauma score that could range from 1 to 5. Within each trauma score column in panels B–D, the middle horizontal line represents the mean and the outer horizontal lines represent the SEM for the variable on the y-axis. *The mean for the y-axis variable differs significantly between trauma scores linked by a bracket. See Figure 1 for remainder of key.
Citation: Journal of the American Veterinary Medical Association 248, 1; 10.2460/javma.248.1.96
Assessment of skull and brain trauma
The mean skull thickness at the site of bolt penetration was 16.4 mm (range, 10.0 to 25.0 mm). The mean diameter of the bolt penetration site was 16.9 mm (range, 10.0 to 25.0 mm). The mean bolt penetration depth was 14.1 cm (range, 9.8 to 17.5 cm), and the presphenoid, sphenoid, and occipital bones were the bones most frequently fractured by the PCBD (Figure 5).
Photograph of a sagittal section of the skull and brain of a representative calf described in Figure 1 following euthanasia with a PCBD. The skull thickness at the site of bolt penetration (white bar) was measured. Notice that the sphenoid and occipital bones were fractured (arrow) in this calf. See Figure 1 for remainder of key.
Citation: Journal of the American Veterinary Medical Association 248, 1; 10.2460/javma.248.1.96
Photograph of a sagittal section of the skull and brain of a representative calf described in Figure 1 following euthanasia with a PCBD. The skull thickness at the site of bolt penetration (white bar) was measured. Notice that the sphenoid and occipital bones were fractured (arrow) in this calf. See Figure 1 for remainder of key.
Citation: Journal of the American Veterinary Medical Association 248, 1; 10.2460/javma.248.1.96
Photograph of a sagittal section of the skull and brain of a representative calf described in Figure 1 following euthanasia with a PCBD. The skull thickness at the site of bolt penetration (white bar) was measured. Notice that the sphenoid and occipital bones were fractured (arrow) in this calf. See Figure 1 for remainder of key.
Citation: Journal of the American Veterinary Medical Association 248, 1; 10.2460/javma.248.1.96
Frequency distributions of scores for the extent of tissue damage and hemorrhage in various regions of the brain were summarized (Table 1). The PCBD caused damage to the brainstem (thalamus, hypothalamus, midbrain, pons, and medulla) in 55 calves. The calculated composite brainstem damage score was 0 for 11 (16.7%) calves, 1 for 30 (45.5%) calves, 2 for 17 (25.8%) calves, 3 for 6 (9.1%) calves, and 4 for 2 (3%) calves. Survival to clinical and cardiac death did not differ significantly between calves with and without brainstem damage (Figure 6). The trauma score was not significantly associated with the weight of the head or the time to clinical death (Figure 4). However, the trauma score was significantly associated with skull thickness at the site of bolt penetration; the mean skull thickness at the site of bolt penetration for calves that had cerebral damage only (total brain damage score, 1) was significantly greater than that for calves that had minor brainstem trauma (total brain damage score, 2) and those that had major brainstem trauma (total brain damage score, 5).
Survival curves for clinical (absence of an auscultable heartbeat; A) and cardiac (ventricular standstill as determined by ECG; B) death for the calves of Figure 1 that did (dashed line; n = 55) and did not (solid line; 11) have damage to the brainstem (thalamus, hypothalamus, midbrain, pons, and medulla) following euthanasia with a PCBD. See Figure 1 for remainder of key.
Citation: Journal of the American Veterinary Medical Association 248, 1; 10.2460/javma.248.1.96
Survival curves for clinical (absence of an auscultable heartbeat; A) and cardiac (ventricular standstill as determined by ECG; B) death for the calves of Figure 1 that did (dashed line; n = 55) and did not (solid line; 11) have damage to the brainstem (thalamus, hypothalamus, midbrain, pons, and medulla) following euthanasia with a PCBD. See Figure 1 for remainder of key.
Citation: Journal of the American Veterinary Medical Association 248, 1; 10.2460/javma.248.1.96
Survival curves for clinical (absence of an auscultable heartbeat; A) and cardiac (ventricular standstill as determined by ECG; B) death for the calves of Figure 1 that did (dashed line; n = 55) and did not (solid line; 11) have damage to the brainstem (thalamus, hypothalamus, midbrain, pons, and medulla) following euthanasia with a PCBD. See Figure 1 for remainder of key.
Citation: Journal of the American Veterinary Medical Association 248, 1; 10.2460/javma.248.1.96
Frequency distribution of scores for the extent of tissue damage and hemorrhage in various regions of the brain for 66 feedlot calves that were euthanized with a PCBD.
| Tissue damage score | Hemorrhage score | ||||||||
|---|---|---|---|---|---|---|---|---|---|
| Brain region | 0 | 1 | 2 | 3 | 0 | 1 | 2 | 3 | Bone fragments |
| Cerebrum | — | 66 (100.0) | — | — | — | 7 (10.6) | 35 (53.0) | 24 (36.4) | 61 (92.4) |
| Cerebellum | 52 (78.8) | 11 (16.7) | 3 (4.5) | — | — | 4 (6.1) | 30 (45.5) | 32 (48.5) | 6 (9.1) |
| Thalamus and hypothalamus | 31 (47.0) | 14 (21.2) | 10 (15.2) | 11 (16.7) | 1 (1.5) | 1 (1.5) | — | 64 (97.0) | 11 (16.7) |
| Midbrain | 48 (72.7) | 10 (15.2) | 3 (4.5) | 5 (7.6) | — | 1 (1.5) | 1 (1.5) | 64 (97.0) | 12 (18.2) |
| Pons | 16 (24.2) | 19 (28.8) | 24 (36.4) | 7 (10.6) | 1 (1.5) | 1 (1.5) | 1 (1.5) | 63 (95.5) | 1 (1.5) |
| Medulla | 55 (83.3) | 6 (9.1) | 4 (6.1) | 1 (1.5) | — | 1 (1.5) | 1 (1.5) | 64 (97.0) | 2 (3.0) |
| Spinal cord | 65 (98.5) | 1 (1.5) | — | — | — | 1 (1.5) | 1 (1.5) | 64 (97.0) | 1 (1.5) |
Values represent the No. (%) of calves. All calves ranged in age from 6 to 19 months and weight from 227 to 500 kg (500 to 1,100 lb) and were considered unlikely to survive or finish the feeding period with their cohorts, generally because of chronic respiratory tract disease or musculoskeletal disorders. Within each region of the brain, the extent of tissue damage (0 = no tissue damage or disruption and no parenchymal hemorrhage, 1 = mild damage limited to hemorrhage or tissue displacement in < 25% of the region, 2 = moderate damage with tissue destruction in 25% to 75% of the region, and 3 = severe damage with > 75% of the region affected) and hemorrhage (0 = no hemorrhage, 1 = > 0 to 25% hemorrhage, 2 = > 25% to 75% hemorrhage, and 3 = > 75% hemorrhage) were scored on a scale of 0 to 3. Within a row and score type, the percentages may not total to 100 because of rounding.
— = Not applicable.
Discussion
Results of the present study indicated that all calves were successfully euthanized by the PCBD evaluated, and an ancillary method of euthanasia was not required for any calf. Observational techniques commonly used to assess animals for unconsciousness and death (eg, corneal and palpebral reflexes, vocalization, righting reflex, and respiration) were absent immediately after the brain was penetrated by the PCBD. After calves were shot with the PCBD, a heartbeat was auscultable for a mean of 7.3 minutes and cardiac electrical activity was present for a mean of 8.3 minutes. In horses euthanized with an overdose of pentobarbital, residual cardiac electrical activity has been recorded for as long as 12 minutes.14
After being shot with the PCBD, the majority (55/66 [83%]) of calves in the present study had trauma to the brainstem (thalamus, hypothalamus, midbrain, pons, and medulla), which influences cardiac and respiratory functions. Rhythmic respiration is controlled by the pons and medulla via feedback from the lungs and chemoreceptors, whereas voluntary nonrhythmic breathing is directed by the cerebral cortex. The brainstem affects cardiac function primarily through the parasympathetic nervous system and secondarily through peripheral vascular resistance and cessation of respiration, which leads to hypoxia.15,16 All 66 study calves had damage to the cerebrum. Following proper application of the PCBD (ie, penetration of the cranial vault), it was expected that the cerebrum would be damaged directly by the captive bolt with additional trauma resulting from pressure from the air channel pithing mechanism and unconsciousness would be immediate and complete.
In contrast to standard penetrating captive bolt devices that often require the use of an ancillary method to achieve death,a the PCBD evaluated in the present study rendered all calves unconscious immediately after penetration of the cranial vault, and death resulted shortly thereafter. The time to death did not differ significantly between calves that did and did not have grossly evident brainstem damage, which most likely was a reflection of the widespread pressure trauma induced by the air channel pithing mechanism. Although standard penetrating captive bolt devices must be accurately applied to the head to elicit unconsciousness and death, the air channel pithing component of the PCBD effectively caused unconsciousness and death as long as the bolt entered the cranial vault, even in calves in which the shot was not optimally placed to produce maximum brainstem damage. This suggested that the target area for bolt placement was larger for the PCBD than that for a standard penetrating captive bolt device, which would be advantageous if the PCBD is to be used for depopulation of large cattle herds because personnel assigned or deployed for euthanasia administration, though adequately trained, might lack extensive experience with penetrating captive bolt devices. Additionally, the PCBD with its larger latitude for placement on the skull might allow depopulation procedures to proceed at a faster rate, compared with other penetrating captive bolt devices that require more precise placement on the skull.
In the present study, the weight of the head was not correlated with skull thickness at the site of bolt penetration and was not associated with the extent of brain trauma induced by the PCBD. This suggested that the PCBD can be used to euthanize cattle of various weights and sizes. However, the largest calf (weight, 509 kg [1,120 lb]) euthanized with the PCBD in this study was not representative of the upper size limit for feedlot cattle, and validation of the device in larger cattle is necessary if it is to be used for depopulation of commercial feedlots.
Contrary to the weight of the head, skull thickness at the site of bolt penetration for calves that had mild (calculated total brain damage score, 2) or maximum (calculated total brain damage score, 5) trauma to the brainstem was significantly less, compared with that for calves that had trauma to the cerebrum only. In larger cattle, placement of the captive bolt on the skull becomes increasingly important because the sinuses enlarge with age, with the frontal sinus continuing to enlarge throughout life.17 Despite this negative association between skull thickness and extent of brain trauma, there was no correlation between time to death (clinical or cardiac) and extent of trauma to the brain, skull thickness, or weight of the head.
The weight and size of the PCBD used in the present study were considerably greater than those for standard penetrating captive bolt devices and may present operational challenges during a depopulation event. Thus, in addition to proper training, the physical fitness and upper body strength required for repetitive use of the PCBD should be considered when personnel are assigned to use the device during a depopulation event. In this study, the PCBD was attached to a spring-loaded cable to partially offset its weight (13.6 kg), facilitate its maneuverability, and reduce operator fatigue. However, variable tension on the back of the PCBD created an additional challenge in physically maneuvering the device in the settings in which it was used during this study. This challenge was compounded if the calf was not adequately restrained. Although adequate restraint of cattle is always recommended during euthanasia procedures regardless of the method used, it is especially critical when the PCBD is used because its size and weight makes quick maneuvering of the device challenging. The issue regarding adequate restraint of cattle can be alleviated by the use of chutes with head restraints such as neck extenders or sweeps. During a depopulation event, many of the challenges associated with cattle restraint could be met by the use of a center-track restrainer like that used in many slaughterhouses, which provides personnel operating captive bolt devices better access to the animal's skull to facilitate shot placement.
Another challenge of the PCBD evaluated in the present study was that the structure and function of the apparatus necessitated that the operator be positioned at a location where visual observation of the calf's forehead and the optimal site for bolt application was hindered. Although all personnel who operated the PCBD had considerable experience euthanizing cattle with penetrating captive bolt devices, in this study, instead of being positioned to the side of the calf with an unobstructed view of its forehead, they were positioned in front of the calf directly behind the PCBD. This impaired the visibility of the calf's forehead, and the time required to complete the euthanasia procedure was slightly prolonged, compared with that for standard penetrating captive bolt devices. Consequently, in 4 calves, the initial shot fired by the PCBD was off center and penetrated the sinus instead of the cranial vault, which necessitated that those calves be shot again. Calves that required an additional shot from the PCBD were easy to identify because they did not go down or lose consciousness immediately after the first shot. In the present study, the overall mean number of shots from the PCBD required to euthanize each calf was 1.09. Even though that number does not seem excessive, a small commercial feedlot with 1,000 cattle would require 1,090 shots from the PCBD to depopulate the herd. However, the additional time required to shoot occasional cattle with the PCBD more than once is offset by the fact that a secondary method of euthanasia such as pithing, exsanguination, or IV administration of a saturated solution of potassium chloride is not required. Nevertheless, the estimated number of shots required from the PCBD should be accounted for when planning for the labor and time necessary to depopulate a large herd of cattle. Additionally, the psychological strain for operators of the PCBD who might have to reshoot approximately 6% of cattle should be considered.
In 2004, the USDA prohibited the use of air channel pithing devices in slaughterhouses because brain tissue, which is designated as a SRM for BSE, was identified in the ventricles of the heart and arteries of the lungs of cattle following their use.9 Prior to the ban, most air channel pithing devices used air pressures of approximately 175 psi. The PCBD evaluated in the present study used an air pressure of approximately 15 psi, and we did not attempt to ascertain whether that low pressure caused dissemination of brain tissue to other parts of the body. Regardless, it is currently illegal to use a PCBD to euthanize cattle intended for human consumption in the United States. Also, the potential for dissemination of SRM throughout the body after use of an air channel pithing device limits carcass disposal options for older cattle. In the United States, cattle > 30 months old must have SRM such as CNS tissue removed prior to being processed in a rendering facility. The location of the CNS tissue can be assumed and the SRM removed in cattle that die or are euthanized by conventional methods. Cattle > 30 months old in which the SRM has been disseminated to other tissues cannot be rendered if any of the rendered products might be used for animal feed.
Because the objective of the present study was to validate the effectiveness of a PCBD as a 1-step method for euthanasia of cattle, the procedure did not take place at a typical rate, and the exact amount of time required to euthanize each study calf was not representative of the amount of time required to euthanize a calf under field conditions. Accurate estimation of the time required to euthanize an animal with the PCBD under field conditions is necessary to determine how efficiently this method can be used for depopulation of large feedlots. Although results of this study indicated that the PCBD was 100% effective in rendering calves unconscious and inducing death, restraining a calf in a squeeze chute, application of the PCBD, and removing the calf from the chute take time. Therefore, even though use of the PCBD did not require implementation of a secondary euthanasia method, it will still require a substantial amount of time to depopulate a large herd of cattle.
Overall, the PCBD evaluated in the present study was an effective 1-step method for the euthanasia of feedlot calves weighing between 227 and 500 kg. In all calves, penetration of the cranial vault by the PCBD resulted in immediate unconsciousness with death soon thereafter. Following euthanasia, evaluation of the skull and brain revealed that the combination of the captive bolt and air pithing resulted in lethal tissue damage. The PCBD might be suitable for depopulating cattle herds in the event of an AHE; however, additional efforts to make the device more user-friendly and develop accompanying paraphernalia or procedures to increase the euthanasia rate are warranted. The workforce needed to depopulate cattle herds in high-density livestock regions such as the central portion of the United States is a particular concern. Results of a foot and mouth disease exercise18 in the Texas Panhandle indicated that depopulation and disposal of cattle within 72 and 96 hours, respectively, were not feasible because of the high livestock density. The number of individuals available during an AHE and the type of herds affected will have a role in determining the appropriate control methods implemented. Comparison of the euthanasia efficiency of the PCBD with that of other captive bolt methods is warranted. The number of cattle to be depopulated and ease of use, efficiency, portability, and accessibility of each euthanasia method will be important considerations during selection of a depopulation method in an AHE. Therefore, knowledge of the performance characteristics of various euthanasia methods for cattle is fundamental to protecting the US livestock and food supply during an AHE.
Acknowledgments
The study was conducted at Iowa State University's research facilities.
Supported by USDA APHIS grant 11-9200-1357-CA.
The authors declare that there were no conflicts of interest.
Presented in part as an oral presentation at the 47th Annual Conference of the American Association of Bovine Practitioners, Albuquerque, September 2014, and the Animal Welfare Symposium 2014: Humane Endings, Rosemont, Ill, November 2014; and as a poster at the Iowa State University College of Veterinary Medicine Research Day, January 2015.
ABBREVIATIONS
| AHE | Animal health emergency |
| BSE | Bovine spongiform encephalopathy |
| PCBD | Pneumatic captive bolt device |
| SRM | Specified risk material |
Footnotes
Gilliam JN, Shearer JK, Bahr RJ, et al. Evaluation of brainstem disruption following penetrating captive bolt shot in isolated cattle heads: comparison of traditional and alternative shot placement landmarks (abstr), in Proceedings. 4th International Symposium on Beef Cattle Welfare 2014. Available at: www.extension.iastate.edu/registration/events/conferences/beefwelfare/pdf/posters/Gilliam%20John%20-%20Evaluation%20of%20Brainstem%20Disruption%20Following%20Penetrating%20Captive%20Bolt%20Shot%20in%20Isolated%20Cattle%20Heads.pdf. Accessed Oct 8, 2015.
Model number USSS-3, Jarvis Products Corp, Middleton, Conn.
ML Series pressure-lubricated, 2-stage air compressor, FS Curtis Co, St Louis, Mo.
300 psi (2068427.2 Pascals) high pressure Adaptaflex air hose, Gates Corp, Denver, Colo.
Pneumatic stunner tester, Jarvis Products Corp, Middleton, Conn.
Littman Classic II SE stethoscope, 3M Center, Saint Paul, Minn.
Televet 100, version 5.0.0 veterinary telemetric ECG system, Engel Engineering Services GmbH, Offenbach, Germany.
Televet 100, version 5.0.0 software, Engel Engineering Services GmbH, Offenbach, Germany.
SAS, version 9.3, SAS Institute Inc, Cary, NC.
GraphPad Prism, version 5.04, GraphPad Software, Inc, La Jolla, Calif.
References
1. Paarlberg PL, Lee JG, Seitzinger AH. Potential revenue impact of an outbreak of foot-and-mouth disease in the United States. J Am Vet Med Assoc 2002; 220: 988–992.
2. Knight-Jones TJ, Rushton J. The economic impacts of foot and mouth disease—what are they, how big are they and where do they occur? Prev Vet Med 2013; 112: 161–173.
3. Foreign ADP, Plan R. National Animal Health Emergency Management System, NAHMES guidelines: mass depopulation and euthanasia. May 2011. Available at: www.prpc.cog.tx.us/Programs/RegionalServices/Calf-Ranch-Industry/PRPC_CalfRanch/bioref/63%20-%20BG%20-%20NAHEMS%20Mass%20Depopulation%20and%20Euthanasia.pdf. Accessed Sep 15, 2015.
4. Killing of animals for disease control purposes. In: Terrestrial Animal Health Code. 18th ed. Paris: World Organisation for Animal Health, 2009; 369–392.
5. AVMA. AVMA guidelines for the euthanasia of animals: 2013 edition. Available at: www.avma.org/KB/Policies/Documents/euthanasia.pdf. Accessed Sep 22, 2015.
6. USDA National Agricultural Statistics Service. US Cattle Inventory. July 25, 2014. Available at: usda.mannlib.cornell.edu/usda/nass/Catt//2010s/2014/Catt-07-25-2014.pdf. Accessed Sep 22, 2015.
7. USDA National Agricultural Statistics Service. Cattle operations and inventory by size group, US. 2013. Available at: www.nass.usda.gov/Charts_and_Maps/Cattle/inv_ops.asp. Accessed Sep 22, 1015.
8. McReynolds SW, Sanderson MW. Feasibility of depopulation of a large feedlot during a foot-and-mouth disease outbreak. J Am Vet Med Assoc 2014; 244: 291–298.
9. USDA Food Safety and Inspection Service. 9 CFR Parts 309, 310, 311, 318, and 319 Prohibition of the Use of Specified Risk Materials for Human Food and Requirements for the Disposition of Non-Ambulatory Disabled Cattle. Fed Regist 2004; 69: 1862–1874.
10. Wells GA, Hawkins SA, Green RB, et al. Preliminary observations on the pathogenesis of experimental bovine spongiform encephalopathy (BSE): an update. Vet Rec 1998; 142: 103–106.
11. Dewell RD, Moran LE, Kleinhenz KE, et al. Assessment and comparison of electrocardiographic and clinical cardiac evidence of death following use of a penetrating captive bolt in bovines. Bov Pr 2015; 49: 32–36.
12. Gregory NG, Spence JY, Mason CW, et al. Effectiveness of poll stunning water buffalo with captive bolt guns. Meat Sci 2009; 81: 178–182.
13. Pasquini C. Atlas of bovine anatomy. Eureka, Calif: Sudz, 1983; 47, 49.
14. Buhl R, Andersen LO, Karlshoj M, et al. Evaluation of clinical and electrocardiographic changes during the euthanasia of horses. Vet J 2013; 196: 483–491.
15. Stephenson RB. Neural and hormonal control of blood pressure and blood volume. In: Klein BG, ed. Cunningham's textbook of veterinary physiology. 5th ed. St Louis: Elsevier, 2013; 243–250.
16. Robinson NE. Control of ventilation. In: Klein BG, ed. Cunningham's textbook of veterinary physiology. 5th ed. St Louis: Elsevier, 2013; 529–530.
17. Dyce KM, Sack WO, Wensing CJG. The head and ventral neck of the ruminant. Textbook of veterinary anatomy. 4th ed. St Louis: Elsevier, 2010; 651–652.
18. Texas Animal Health Commission. Operation Palo Duro February 21–23, 2007. Available at: www.tahc.state.tx.us/emergency/May2007_OperationPaloDuro.pdf. Accessed Sep 22, 2015.
