The goat population in the United States totals approximately 2.6 million, according to the National Agricultural Statistics Service census of 2012.1 Although the size of this population as a whole has remained fairly steady over the past decade, the number of goats slaughtered for meat continues to rise, increasing from 558,857 in 2004 to 779,000 in 2010 (an almost 29% increase).2,3 Approximately 80% of goats in the United States are used for meat, whereas a smaller number are used in dairies or kept as pets and exhibition animals.1
The steady state of the US goat population and the increase in the number of goats slaughtered per year stems from the ever-growing ethnic diversity of the US human population.4 Many ethnicities and religious groups such as those from parts of Northern Africa, Greece, the Middle East, Southern Asia, the Caribbean, and South America regularly consume goat meat (chevon or cabrito).5
Captive bolt administration, whether penetrating or nonpenetrating, is an established method of euthanasia for many livestock species. Once fired, a penetrating captive bolt device drives a rod or bolt through the bone of the skull into the brain itself. The portion of the brain that becomes disrupted is dependent on the site of device application. A nonpenetrating captive bolt device ejects a mallet-shaped knocker that leaves a depression in the skull at the site of application while causing considerable damage to the underlying soft tissues of the brain. Because the nonpenetrating captive bolt generally does not break the skin at the site of impact, less opportunity may exist for contamination of the meat with debris from materials potentially hazardous to human health, such as spinal cord and brain.
According to the AVMA, captive bolt devices induce sufficient concussion to render animals unconscious or insensible when applied appropriately to the appropriate species.6 The AVMA euthanasia guidelines also state that neither penetrating nor nonpenetrating captive bolt administration should be used as a sole means of euthanasia and should always be followed by a secondary or adjunctive method, such as exsanguination or pithing.6 A few exceptions exist for pneumatic nonpenetrating captive bolt devices that are designed for use in certain animal groups, including suckling pigs, neonatal ruminants, and turkeys.6 Detailed instructions are provided for use of penetrating captive bolts in the euthanasia of cattle, sheep, goats, horses, and pigs.
Although evidence6–10 exists to support the effectiveness of captive bolt administration in cattle, swine, and sheep, studies of such administration in goats are lacking. Signs of complete concussion, unconsciousness, or insensibility after stunning of livestock species have been reported.9–13 These signs include lack of a corneal reflex, cessation of rhythmic respirations and heartbeat, loss of posture or immediate collapse, lack of righting reflex, lack of vocalization, lack of eye movement, relaxation of the jaw, protrusion of the tongue, convulsions, and lack of response to painful stimuli. In most situations, at least 2 of the signs of complete concussion should be observed to confirm successful stunning.11
Given the demand for goat meat, a method needs to be established for humane stunning and euthanasia of goats. The objective of the study reported here was to use 2 advanced imaging modalities to compare the extent of tissue damage sustained after application of penetrating and nonpenetrating captive bolts to the heads of goats.
Materials and Methods
Animals
Twelve 1- to 5-year-old goats were selected on the basis of availability from an unrelated study that was approved by the University of Tennessee Animal Care and Use Committee (protocol No. 2319-0415). All goats were females with horns and were of meat and dairy breeds. All goats had been euthanized with pentobarbital sodiuma at a dose of 1 mL/4.5 kg in the unrelated study. Death was confirmed through lack of corneal-palpebral reflex and cessation of respiration and heartbeat prior to use in the present study. All procedures and imaging described herein were initiated within 30 minutes after euthanasia.
Captive bolt application
Caprine cadavers were allocated to receive a non-penetrating (n = 6) or penetrating (6) captive bolt. A simple coin toss was used to decide the method of captive bolt administration used for the first cadaver, resulting in selection of a penetrating captive bolt for that cadaver. Bolt administration for subsequent cadavers alternated between nonpenetrating and penetrating. For bolt administration, cadavers were positioned on a table in sternal recumbency with the neck extended to facilitate correct positioning of the captive bolt device. The captive bolt pistolb was used with a 0.25-caliber yellow cartridge and either the knocker head (nonpenetrating) or the standard bolt (penetrating) in accordance with the manufacturer's recommendations.14 The head of 1 goat was removed prior to administration of a penetrating captive bolt, and CT and MRI were performed to serve as a control specimen for comparison purposes.
The location for placing the muzzle of the captive bolt device and the trajectory of the bolt were chosen with consideration of several references.6,15–18 The muzzle was placed flush on the dorsal midline of the head at the level of the external occipital protuberance (poll) and aimed downward toward the cranialmost portion of the intermandibular space (Figure 1).6,16,17 All shots were fired by the same operator for consistency. After captive bolts had been administered, heads were removed from the cadavers at C1 or C2.
Photographs of a caprine cadaver showing preparations made prior to administration of a captive bolt. A—The site of placement of the muzzle of the captive bolt device is identified by the red dot. This site, located on the dorsal midline of the head, corresponds with the poll or the external occipital protuberance of the skull. B—The trajectory of the bolt is shown from the lateral aspect. C—The trajectory is shown from the cranial aspect.
Citation: American Journal of Veterinary Research 78, 2; 10.2460/ajvr.78.2.151
CT and MRI
Heads were submitted to the radiology service at the College of Veterinary Medicine, University of Tennessee, for CT and MRI. The head of the 1 goat from which the head was removed prior to bolt administration was imaged twice (Figure 2). For all CT and MRI scans, the heads were placed to mimic a prone patient position. The CT examination was performed by use of a 40-slice helical CT scanner.c A multidetector helical dataset was obtained, and images were reconstructed in 0.9- and 4-mm transverse slices by means of bone and soft tissue algorithms.
Sagittal T2-weighted MRI (A) and transverse CT (B) views of the head of a caprine cadaver prior to administration of a captive bolt.
Citation: American Journal of Veterinary Research 78, 2; 10.2460/ajvr.78.2.151
The MRI evaluation was performed by use of a 1.5-T superconductive imaging systemd and a designated head coil. Acquired sequences included sagittal T2-weighted spin echo (time of repetition, 5,510 milliseconds; time of echo, 101 milliseconds; slice thickness, 3 mm), transverse T2-weighted spin echo (time of repetition, 4,363 milliseconds; time of echo, 102 milliseconds; slice thickness, 4 mm), transverse T1-weighted spin echo (time of repetition, 391 milliseconds; time of echo, 12 milliseconds; slice thickness, 4 mm), transverse proton density-weighted spin echo (time of repetition, 2,000 milliseconds; time of echo, 13 to 14 milliseconds; slice thickness, 4 mm), transverse fluid-attenuated inversion recovery (time of repetition, 8,000 milliseconds; time of echo, 74 to 77 milliseconds; time of inversion, 2,370 milliseconds; slice thickness, 4 mm), transverse T2*-weighted gradient recalled echo (time of repetition, 889 milliseconds; time of echo, 26 milliseconds; flip angle, 20°; slice thickness, 4 mm), and transverse 3-D T1-weighted gradient recalled echo (time of repetition, 5.41 to 5.84 milliseconds; time of echo, 2.39 milliseconds; flip angle, 10°; slice thickness, 1 mm).
Gross dissection
Once imaging had been performed, a band saw was used to transect the heads longitudinally near or through the captive bolt site and gross photographic images were obtained. Dissection of 1 specimen that received a nonpenetrating captive bolt was performed to assess the fracture sites. An incision was made on the caudal aspect of the head over the site of impact with a scalpel blade, the adnexa were bluntly dissected away from external surface of the calvarium, and facture sites were identified.
Results
Nonpenetrating captive bolt
Heads of goats that received the nonpenetrating captive bolt had consistent evidence of fractures to the occipital bone, interparietal bones, temporal bones, and the basilar portion of the occipital bone (Figures 3 and 4). Damage to the cerebellum and occipital and temporal lobes of the brain was also identified on MRI. Additional damage sustained in some heads included fractures of the parietal bones (n = 5 goats), architectural damage to the parietal lobe (4), architectural damage to the myelencephalon (3), and fractures of the zygomatic arches (1; Table 1).
Representative photograph of the head of a caprine cadaver after administration of a nonpenetrating captive bolt as indicated in Figure 1. Blunt dissection revealed multiple fractures (arrows) as observed from the caudalmost aspect of the cranium.
Citation: American Journal of Veterinary Research 78, 2; 10.2460/ajvr.78.2.151
Sagittal T2-weighted MRI (A) and transverse CT (B and C) views and photograph (D)of the head of a caprine cadaver after administration of a nonpenetrating captive bolt. A—Notice the damage to the architecture of the cerebrum (arrow) and the disruption of the brainstem (asterisk). B—The caudal aspect of the head is shown, revealing multiple fractures of the occipital, interparietal, temporal, and parietal bones. C—Fractures of the basilar portion of the occipital bone (red arrows) and the parietal bones (blue arrows) are evident. D—A gross sagittal view of the head shows fractures at the impact site (arrows).
Citation: American Journal of Veterinary Research 78, 2; 10.2460/ajvr.78.2.151
Summary of damage to the heads of caprine cadavers identified via MRI, CT, and gross dissection following administration of a nonpenetrating captive bolt.
| Goat | Structures with soft tissue damage | Structures with skeletal damage |
|---|---|---|
| 1 | Cerebellum, occipital lobe, and temporal lobe | Fractured occipital and interparietal bones, fractured temporal and parietal bones bilaterally, and fractured basilar portion of the occipital bone |
| 2 | Cerebellum and occipital, temporal, and parietal lobes | Fractured occipital and interparietal bones, fractured temporal bones bilaterally, fractured right parietal bone, and fractured basilar portion of the occipital bone |
| 3 | Cerebellum, myelencephalon, and occipital, temporal, and parietal lobes | Fractured occipital and interparietal bones; fractured temporal, parietal, and zygomatic bones bilaterally; and fractured basilar portion of the occipital bone |
| 4 | Cerebellum and occipital, temporal, and parietal lobes | Fractured occipital and interparietal bones, fractured temporal and parietal bones bilaterally, and fractured basilar portion of the occipital bone |
| 5 | Cerebellum, occipital lobe, temporal lobe, and myelencephalon | Fractured occipital and interparietal bones, fractured temporal bones bilaterally, and fractured basilar portion of occipital bone |
| 6 | Cerebellum, myelencephalon, and occipital, temporal, and parietal lobes | Fractured occipital and interparietal bones, fractured temporal and parietal bones bilaterally, and fractured basilar portion of the occipital bone |
Blunt dissection of 1 head that received a non-penetrating captive bolt revealed fractures involving the occipital, interparietal, and temporal bones (Figure 4). Nineteen fragments of bone were identified on the caudal aspect of the head over the external occipital protuberance. Hemorrhage was also noted at the impact site. The architecture of the soft tissues including the cerebellum, occipital and temporal lobes, and myelencephalon were disrupted as well.
Penetrating captive bolt
Heads of goats that received the penetrating captive bolt had consistent evidence of fractures to the occipital and interparietal bones. Computed tomography revealed a bony fragment (probably from the external occipital protuberance or poll) embedded in the deep tissues of the brain within each head (Figure 5). In 5 heads, this fragment was in the mesencephalon; in the remaining head, it was in the area of the diencephalon. Soft tissue damage included architectural damage to the cerebellum and mesencephalon (n = 5 goats), myelencephalon and diencephalon (3), and occipital (2) and frontal lobes (1; Table 2). A considerable amount of hemorrhage was identified associated with the underlying soft tissues of the brain (caudal portion of the cerebrum and cerebellum primarily).
Transverse CT and sagittal T2-weighted MRI images and photograph of the head of a caprine cadaver after administration of a penetrating captive bolt. A—Notice the bony fragment (arrow) located in the area of the mesencephalon. B— Notice the tract of the bolt depicted by the blue line. C—Notice the bony fragment (arrow) at the level of the mesencephalon.
Citation: American Journal of Veterinary Research 78, 2; 10.2460/ajvr.78.2.151
Summary of damage to the heads of caprine cadavers identified via MRI, CT, and gross dissection following administration of a penetrating captive bolt.
| Goat | Structures with soft tissue damage | Structures with skeletal damage |
|---|---|---|
| 1 | Cerebellum, diencephalon, and mesencephalon | Fractured occipital and interparietal bones and bony fragment embedded in the area of the mesencephalon |
| 2 | Cerebellum, occipital lobe, mesencephalon, and diencephalon | Fractured occipital and interparietal bones and bony fragment embedded in the area of the mesencephalon |
| 3 | Cerebellum, myelencephalon, and mesencephalon | Fractured occipital and interparietal bones, fractured basilar portion of the occipital bone, and bony fragments embedded in the area of the mesencephalon |
| 4 | Cerebellum, myelencephalon, and mesencephalon | Fractured occipital and interparietal bones and bony fragment embedded in the area of the mesencephalon |
| 5 | Occipital lobe, diencephalon, and frontal lobe | Fractured interparietal bone, fractured parietal bones bilaterally, and bony fragment embedded in the area of the diencephalon |
| 6 | Cerebellum, myelencephalon, and mesencephalon | Fractured interparietal bone, possible fracture of right temporal and parietal bones, and bony fragment in the area of the mesencephalon |
Discussion
The results of the present study indicated that administration of either a penetrating or nonpenetrating captive bolt to the head of caprine cadavers could effectively induce brain trauma potentially sufficient to result in stunning and unconsciousness of live goats7,19–21 We were unable to assess damage to the brainstem in 3 goats to which the nonpenetrating captive bolt was administered because of the lack of hemorrhage and edema in the area of the brainstem visible on MRI scans. The lack of noticeable hemorrhage and edema on MRI scans was attributable to the use of cadavers rather than live subjects. Despite the lack of hemorrhage on MRI scans, considerable disruption of the underlying soft tissues was identified after transection and blunt dissection of head specimens that received the nonpenetrating captive bolt.
As other studies have shown, considerable differences can exist among species with regard to the evaluation of captive bolt as a euthanasia technique, and it is important to establish efficacy of these methods. In 2 such studies, one involving pigs22 and the other involving lambs,23 the presence of amyloid precursor protein was examined in histologic samples of brain tissues to determine whether the nonpenetrating captive bolt caused traumatic brain injury. Investigators in those studies22,23 were successful in establishing the efficacy of nonpenetrating captive bolt administration in sheep; however, the traumatic brain injury induced in pigs (body weight, 15 to 18 kg) was insufficient to cause death. This lack of injury in pigs was speculated to have been attributable to the anatomy of the skull and increased cervical musculature of pigs of this size. Another study7 of penetrating captive bolt administration involved use of various charges and placements of the bolt, with the objective of developing recommendations regarding the appropriate cartridge size and target to ensure death of both polled and horned sheep. In that study,7 complete concussion or unconsciousness was obtained in 94% of sheep regardless of cartridge used.
Although the sample size in the present study was fairly small, the authors do not believe this was a limitation. Imaging revealed that all 6 caprine cadavers evaluated for each type of captive bolt had trauma sufficient to induce stunning and unconsciousness.7,19–21 Use of cadavers provided some valuable information; however, physiologic effects such as hemorrhage and edema, which are used to assess completeness of concussion and successful stunning, could not be assessed.
Administration of a penetrating or nonpenetrating captive bolt appeared to cause sufficient tissue damage to render horned goats unconscious, but additional research is necessary in live subjects to validate either method as an effective means of euthanasia. A possible next step would be to euthanize goats with a nonpenetrating or penetrating captive bolt while anesthetized and monitor brain and electroencephalographic activity, as has been done in sheep and cattle.11,24–28 This procedure could be followed with MRI to determine the extent of soft tissue damage, particularly to the brainstem. Another next step would be to assess stun quality at abattoirs through observation of goats for signs of incomplete concussion.
Acknowledgments
The authors declare that there were no conflicts of interest. The authors thank Drs. David Anderson and Madhu Dhar for providing the caprine cadavers and Gordon Conklin and Dr. Chase Constant for their help with imaging.
Footnotes
Beuthanasia-D Special, Merck Animal Health, Madison, NJ.
Cash Special captive bolt pistol, Accles and Shelvoke Ltd, Sutton Coldfield, West Midlands, England.
Philips Brilliance-40, Amsterdam, The Netherlands.
Siemens Magnetom Espree, Erlangen, Germany.
References
1. USDA National Agricultural Statistics Service. 2012 census of agriculture full report. Washington, DC: USDA, 2012.
2. USDA APHIS. The goat industry: structure, concentration, demand, and growth. Fort Collins, Colo: APHIS, 2004;1–25.
3. USDA Food Safety and Inspection Service. Goat from farm to table. Available at: www.fsis.usda.gov/wps/portal/fsis/topics/food-safety-education/get-answers/food-safety-fact-sheets/meat-preparation/goat-from-farm-to-table/ct_index. Accessed Jul 9, 2015.
4. Geisler M. Ethnic foods market profile. Available at: www.agmrc.org/markets-industries/food/ethnic-foods-market-profile. Accessed Jul 7, 2015.
5. Isaacs JS. Meat for ethnic markets. Available at: www.agmrc.org/commodities-products/livestock/meat-for-ethnic-markets. Accessed Jul 7, 2015.
6. Leary S, Underwood W, Anthony R, et al. AVMA Guidelines for the euthanasia of animals: 2013 edition. Schaumburg, Ill: AVMA, 2013.
7. Gibson TJ, Ridler AL, Lamb CR, et al. Preliminary evaluation of the effectiveness of captive-bolt guns as a killing method without exsanguination for horned and unhorned sheep. Anim Welf 2012; 21: 35–42.
8. Atkinson S, Velarde A, Algers B. Assessment of stun quality at commercial slaughter in cattle shot with captive bolt. Anim Welf 2013; 22: 473–481.
9. Gouveia K, Ferreira PG, Roque da Costa JC, et al. Assessment of the efficiency of captive bolt stunning in cattle and feasibility of associated behavioural signs. Anim Welf 2009; 18: 171–175.
10. Gregory NG, Lee CJ, Widdicombe JP. Depth of concussion in cattle shot by penetrating captive bolt. Meat Sci 2007; 77: 499–503.
11. Verhoeven MT, Gerritzen MA, Hellebrekers LJ, et al. Indicators used in livestock to assess unconsciousness after stunning: a review. Animal 2015; 9: 320–330.
12. Gibson TJ, Whitehead C, Taylor R, et al. Pathophysiology of penetrating captive bolt stunning in alpacas (Vicugna pacos). Meat Sci 2015; 100: 227–231.
13. von Wenzlawowicz M, von Holleben K, Eser E. Identifying reasons for stun failures in slaughterhouses for cattle and pigs: a field study. Anim Welf 2012; 21: 51–60.
14. Accles and Shelvoke. CASH Special Captive Bolt Available at: www.qcsupply.com/media/pdf/CashSpecialProductDataSheet.pdf. Accessed Jul 1, 2015.
15. Gilliam JN, Shearer JK, Woods J, et al. Captive-bolt euthanasia of cattle: determination of optimal-shot placement and evaluation of the Cash Special Euthanizer Kit for euthanasia of cattle. Anim Welf 2012; 21: 99–102.
16. Shearer JK, Ramirez A. Procedures for humane euthanasia. Ames, Iowa: Iowa State University, 2012. Available at: vetmed.iastate.edu/sites/default/files/vdpam/Extension/Dairy/Programs/Humane%20Euthanasia/Download%20Files/EuthanasiaBrochure20130128.pdf. Accessed Jul 1, 2015.
17. Walz P, Lin H. Farm animal anesthesia. Danvers, Mass: Wiley Blackwell, 2014;278.
18. Iowa State University. Anatomic landmarks webpage. Available at: vetmed.iastate.edu/vdpam/about/production-animal-medicine/dairy/dairy-extension/humane-euthanasia/humane-euthanasia/anatomical-landmarks. Accessed Jul 14,2015.
19. Casey-Trott TM, Millman ST, Turner PV, et al. Effectiveness of a nonpenetrating captive bolt for euthanasia of 3 kg to 9 kg pigs. J Anim Sci 2014; 92: 5166–5174.
20. Concha-Albornoz I, Stieger-Vanegas SM, Cebra CK. Computed tomographic features of the osseous structures of the external acoustic meatus, tympanic cavity, and tympanic bulla of llamas (Lama glama). Am J Vet Res 2012; 73: 42–52.
21. Svendsen O, Jensen SK, Karlsen LV, et al. Observations on newborn calves rendered unconscious with a captive bolt gun. Vet Rec 2008; 162: 90–92.
22. Finnie JW, Manavis J, Summersides GE, et al. Brain damage in pigs produced by impact with non-penetrating captive bolt pistol. Aust Vet J 2003; 81: 153–155.
23. Finnie JW, Blumbergs PC, Manavis J, et al. Evaluation of brain damage resulting from penetrating and non-penetrating captive bolt stunning using lambs. Aust Vet J 2000; 78: 775–778.
24. Blackmore DK, Newhook JC. Electroencephalographic studies of stunning and slaughter of sheep and calves—part 3: the duration of insensibility induced by electrical stunning in sheep and calves. Meat Sci 1982; 7: 19–28.
25. Newhook JC, Blackmore DK. Electroencephalographic studies of stunning and slaughter of sheep and calves—part 2: the onset of permanent insensibility in calves during slaughter. Meat Sci 1982; 6: 295–300.
26. Newhook JC, Blackmore DK. Electroencephalographic studies of stunning and slaughter of sheep and calves—part 1: the onset of permanent insensibility in sheep during slaughter. Meat Sci 1982; 6: 221–233.
27. Gibson TJ, Johnson CB, Murrell JC, et al. Electroencephalographic responses of halothane-anaesthetised calves to slaughter by ventral-neck incision without prior stunning. N Z Vet J 2009; 57: 77–83.
28. Sánchez-Barrera IC, Albarracin W, Rojas MJ. Electroencephalographic spectrum power of sheep's brain after stunning. J Appl Anim Res 2013; 42: 73–76.
