Volume 90, Issue 3 pp. 307-316
REVIEW ARTICLE
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Cattle stunning with a penetrative captive bolt device: A review

Josef Kamenik

Josef Kamenik

Department of Gastronomy, Faculty of Veterinary Hygiene and Ecology, University of Veterinary and Pharmaceutical Sciences Brno, Brno, Czech Republic

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Vaclav Paral

Vaclav Paral

Department of Anatomy, Histology and Embryology, Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences Brno, Brno, Czech Republic

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Martin Pyszko

Martin Pyszko

Department of Anatomy, Histology and Embryology, Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences Brno, Brno, Czech Republic

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Eva Voslarova

Corresponding Author

Eva Voslarova

Department of Animal Protection, Welfare and Behaviour, Faculty of Veterinary Hygiene and Ecology, University of Veterinary and Pharmaceutical Sciences Brno, Brno, Czech Republic

Correspondence

Eva Voslarova, Department of Animal Protection, Welfare and Behaviour, Faculty of Veterinary Hygiene and Ecology, University of Veterinary and Pharmaceutical Sciences Brno, Brno, Czech Republic.

Email: [email protected]

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First published: 22 January 2019
Citations: 9

Abstract

The captive bolt device has been used for stunning cattle at abattoirs for more than 100 years and is now one of the stunning devices used most widely. The aim of this review article was to assess the effects that are decisive during cattle slaughter on the quality of stunning with the use of a captive bolt stunning device. The basis of effective stunning is the use of a suitable type of device, with the speed of the bolt and the kinetic energy corresponding to the anatomical parameters of the slaughtered animal. The importance of the regular cleaning and maintenance of stunning devices and monitoring of the effectiveness of stunning goes without saying. The immediate loss of sensibility in the animal must occur after the first shot. The effectiveness of the stunning process can be quantified by regular monitoring of the behavior of animals after stunning with an emphasis on the loss of reflexes (corneal reflex, regular breathing, attempts to regain physiological posture) and checks on the shot location on the skulls of slaughtered animals.

1 INTRODUCTION

In 1903, Dr Hugo Heiss invented the device for stunning animals for slaughter that is now known as the penetrative captive bolt stunning device. The veterinarian Dr Heiss worked until 1933 as director of the abattoir in the German town of Straubing (Ring & Schäffer, 2015). During his professional career, he strived to ensure that animals were slaughtered quickly and without suffering or pain at the abattoir. Over the coming decades his invention spread all over the world and is now one of the stunning devices used most widely in cattle slaughter (Oliveira et al., 2018; Terlouw, Bourguet, Deiss, & Mallet, 2015).

According to Council Regulation (EC) No 1099/2009, stunning is understood as every deliberate procedure that leads to the loss of consciousness and sensibility without causing pain. According to Annex I to this Regulation, a penetrative captive bolt device is used at abattoirs in the European Union to stun cattle (Council of the European Union, 2009). The aim of this method of mechanical stunning is to induce a deep and irreversible form of brain concussion (Gregory, Lee, & Widdicombe, 2007; Terlouw et al., 2015; Verhoeven, Gerritzen, Hellebrekers, & Kemp, 2015). Concussion is the short-term disruption of nerve function caused by a sudden acceleration (or deceleration) of the head (Shaw, 2002). The most dramatic aspect of concussion is the sudden loss of consciousness, during which the affected animal falls motionless to the ground. The areas of the brain engaged in consciousness are the cerebral cortex and the thalamus which together make up the thalamocortical complex controlled by the brain stem (Verhoeven et al., 2015). Consciousness arises from the thalamocortical projections (Schwenk et al., 2016). A properly functioning brain stem and thalamus are fundamental to the maintenance of consciousness, and damage to either of these areas may cause a rapid loss of consciousness.

Stunning with a captive bolt causes sudden trauma to the skull, brain, and related blood vessels with a series of subsequent physically manifested symptoms depending on the position, depth, speed, and kinetic energy of the penetration of the bolt into the skull and brain (Atkinson, Velarde, & Algers, 2013; Finnie, 1993). This method of stunning damages the brain structures engaged in the state of wakefulness. Specifically, it involves targeted damage to the reticular formation of the brain or the ascending reticular activating system (Terlouw, Bourguet, & Deiss, 2016). The reticular formation is gray matter in the brain that is made up of more than 50 cerebral nuclei located in the brain stem. It is a system that receives impulses from all specific neural pathways. The brain stem is made up of three parts of the brain—the midbrain, the pons, and the medulla oblongata (Chin & Kumar, 2013). When stunning with a captive bolt device, the device should be placed on the frontal region of the head in such a way that the bolt impacts the brain stem (Fries, Schrohe, Lotz, & Arndt, 2012).

Brain damage caused by mechanical stunning depends on a number of factors. First, it depends on the effect of the shock wave induced in the brain when the bolt impacts the skull. Second, it depends on the effect of mechanical destruction when the bolt penetrates the brain and then on the level of damage to the brain tissue when the bolt is pulled out of the wound, during which bleeding occurs as a result of structural changes. The shot location has a large influence on all these aspects (Terlouw et al., 2015).

The quality of cattle stunning at abattoirs also depends, however, on the use of an adequate stunning device (Atkinson et al., 2013). In order for the reliable and immediate loss of sensibility to occur, the bolt must be travelling with enough speed to induce extensive concussion in addition to penetrating into the brain (Grandin, 2013). Breaching the cranial cavity is the basic requirement when a penetrative captive bolt device is used. Its effectiveness is heavily dependent on the anatomical features of the animal and on the device itself (Schwenk et al., 2016).

The paramount aim during stunning is for the animal to lose consciousness and sensibility following the first shot (von Holleben, Schneider, & von Wenzlawowicz, 2018). According to Grandin (2013), a score of 95% of animals completely insensible following the first shot can be considered acceptable when using a captive bolt stunning device, whereas 99% represents an excellent result.

The aim of this review article was to assess the effects that are decisive during cattle slaughter on the quality of stunning with the use of a captive bolt stunning device.

2 THE EFFECT OF THE STUNNING DEVICE ON THE QUALITY OF ANIMAL STUNNING

The functional component of a captive bolt stunning device is a retractable metal bolt (captive bolt) which penetrates the skull of the animal causing extensive physical damage to the brain (Grandin, 2013). The energy required to shoot the bolt from the barrel of the stunning device is supplied either by the expansion of gases released from a cartridge in the case of classic stunning devices or by compressed air in the case of pneumatic stunning devices. This energy is converted into the kinetic energy of the moving bolt (Oliveira et al., 2018). Pneumatic stunning devices with a captive bolt of American provenance were first tested in Europe in 1991 (Gregory, 2005).

The cartridge, or the working air pressure in the case of pneumatic devices, is adapted to the size and type of stunned animal (von Holleben et al., 2018). The effectiveness of stunning devices depends on a number of variables:
  • The length and weight of the captive bolt.
  • The type and quality of the cartridges in classic stunning devices.
  • The air pressure in pneumatic stunning devices.
  • The degree of wear and maintenance of stunning devices.

Stunning devices of differing bolt weight, length, and diameter are used for different types and weights of animal (von Holleben et al., 2018). According to Schwenk et al. (2016), conventional stunning devices have a bolt length of 90–120 mm. Pneumatic stunning devices are equipped with bolts of larger diameter and length and, therefore, greater weight (Table 1). They are used extremely widely at large-capacity abattoirs (Oliveira, Gregory, Costa, Gibson, & da Costa, 2017).

Table 1. Summary of cartridge-operated or pneumatically powered captive bolt guns (CBG) used in scientific studies
Manufacturer Gun type Bolt weight (g) Bolt diameter (mm) Bolt length (penetration depth) (mm) Authors
Cartridge-operated CBG
Accles & Shelvoke, UK 0.22 Cash Special 211 11.35 (73 ± 2) Gibson, Mason et al. 2015
0.22 Cash Special Heavy 211 11.35 (72 ± 3)
0.25 Cash Dispatch Kit MB: 215LB: 229 11.3811.38 (70 ± 2)(89 ± 0)
0.25 Cash Euro Stunner 233 11.40 (76 ± 1)
Karl Schermer, GE 6.8/15 KS 242 11.92 (73 ± 1)
Termet, FR 0.25 Matador Super Sécurit 3,000 (6.3/12) 234 11.60 (85 ± 2)
Karl Schermer, GE 6.8/15 KR 230.95 12.00 85 Dörfler et al. (2014)
6.8/15 KS 240.25 12.00 80
6.8/15 KL 259.97 12.00 125
Accles & Shelvoke, UK 0.22 Cash Magnum 9,000 11.91 121 Atkinson et al. (2013)
Termet, FR Super Sécurit 3,000 12.00 90 (bulls); 85 (cows) Terlouw et al. (2015)
EFA Schmid & Wezel, GE 0.22 Cash Magnum 9,000 S 11.40 121 Schwenk et al. (2016)
Karl Schermer, GE 0.27 KL 12.00 125
Pneumatically powered CBG
Jarvis Products, USA USSS-1:CON; MEB; LON ––– ––– 152.4165.1177.8 Martin et al. (2018)
EFA Schmid & Wezel, GE VB 215 12.00 135 Schwenk et al. (2016)
Jarvis Products, USA USSS-1 297 15.9 210 Oliveira et al. (2017)
EFA Schmid & Wezel, GE VB 315 14.5 121 von Holleben et al. (2018)

Dörfler et al. (2013) tested three types of cartridge-fired stunning devices from a single manufacturer, with a captive bolt length of 80, 85, and 125 mm, at an abattoir in Germany. Oliveira et al. (2018) studied the effectiveness of cattle stunning using a pneumatic device with a bolt length of 210 mm. Martin et al. (2018) also tested a pneumatic stunning device with varying bolt length (152.4, 165.1, and 177.8 mm) in the USA. A longer bolt has the potential to penetrate deeper into the brain tissue and cause damage (Figures 1 and 2). On the other hand, longer bolts consume a great deal of energy when retracted back into the barrel of the device (Schwenk et al., 2016).

Details are in the caption following the image
View of the right half of the cranial cavity of a cow. Green circle—the ideal shot location, red arrow—the actual shot location, blue line—the boundary between the nasal cavity and cranial cavity (photo by authors Paral and Pyszko)
Details are in the caption following the image
View of the right half of the brain in the cranial cavity of a cow. Median section. Green circle—the ideal shot location, pincers—the actual shot location, green arrows—blood in the subarachnoid space (photo by authors Paral and Pyszko)

One frequently mentioned symptom of effective stunning and loss of consciousness is the collapse of the animal immediately after the first shot. This is the result of damage to the reticular formation which plays a role in maintaining correct posture (Oliveira et al., 2018). The reticular formation represents the central nucleus of the brain stem formed of a large network of nerve tissue (Verhoeven et al., 2015). The reticular formation receives sensory information from the cortex and a number of subcortical areas and its axons project into the cerebral cortex, the thalamus and the spinal cord. The reticular formation plays a role in alertness, muscle tone, motion and various vital reflexes. If the reticular formation ceases to function, the cerebral cortex shuts down. If the cortex is functionally damaged, the neuronal integration of signals from the central nervous system, which is essential to consciousness, cannot take place and subjective experience cannot occur (Verhoeven et al., 2015). It is clear from the above that deeper penetration of the captive bolt into the brain tissue induces potentially greater damage to it. Schwenk et al. (2016) measured distances of 83.0–105.9 mm (median 86.4 mm) from the outside of the bone in the frontal region to the thalamus. A median value for this distance of 84.7 mm was found in young bulls, and a distance of 98.1 mm in bulls older than 30 months. This distance was 101.0–121.0 mm (median 102.0 mm) from the surface of the skin to the thalamus. If stunning devices are used correctly, the captive bolt should, therefore, reach the thalamus itself which is, along with the brain stem, fundamental to maintaining consciousness (Verhoeven et al., 2015). However, the magnetic resonance and computer tomography study conducted by Schwenk et al. (2016) revealed only slight damage to the brain.

Both the neuronal destruction caused by the penetration of the bolt into the brain and neuronal dysfunction resulting from the sudden direct impact of the bolt to the head are important to the effective stunning of cattle at the abattoir (Oliveira et al., 2018). The kinetic energy transferred by the bolt to the skull induces the loss of sensibility; the physical damage to the brain caused by the bolt is responsible for the irreversible loss of sensibility. According to von Holleben et al. (2018), the energy transferred following the discharge of the captive bolt onto the animal's skull is decisive to the effectivity of stunning. There are, however, evidently differences between species of ruminant. During their assessment of the stunning of alpacas (Vicugna pacos), Gibson et al. (2015) determined that shots that missed the brain or caused merely superficial damage to the thalamus and brain stem usually failed to induce complete insensibility. Their results indicated that the kinetic energy acting on the skull following a poor shot did not suffice to induce a complete loss of sensibility as a result of mere brain concussion.

A minimum energy of 200 J is stated for the effective stunning of adult cattle (Oliveira et al., 2018). Dörfler et al. (2013) determined values of kinetic energy from 325.6 to 384.0 J depending on the types of device used when the most powerful cartridges are used. The KL device with a bolt length of 125 mm displayed the lowest value of measured kinetic energy as a result of the greater weight of the bolt. Gibson, Mason, Spence, Barker, and Gregory (2015) tested six captive bolt stunning devices from three manufacturers (United Kingdom, Germany, France). The kinetic energy attained values of 237–443 J when the most powerful cartridges were used and 77–161 J with weaker cartridges, and was therefore beneath the minimum value given in the literature (Oliveira et al., 2018). For effective stunning it is, therefore, necessary to choose both a suitable type of stunning device and also (for classic devices) the right type of cartridge. Dörfler et al. (2013) tested three types (yellow, blue, red) of cartridges of 6.8/15 caliber. The yellow cartridges were designed for stunning sheep, horses, cattle, sows, and boars, the blue cartridges for cows, steers, and bulls, and the red cartridges for heavy bulls and steers. The cartridges differed in terms of the powder content—yellow 260 mg, blue 315 mg, red 320 mg (Dörfler, Troeger, Lücker, Schönekeß, & Frank, 2014). Statistically significant differences (< 0.005) were determined between the measured values of the kinetic energy of the types of cartridge used (Dörfler et al., 2013). The highest values of kinetic energy were determined for the individual stunning devices with the use of the red cartridges. When classic stunning devices with cartridges are used, however, only between one-third and one-half of the potential energy of the cartridge is transformed into the kinetic energy of the captive bolt (Dörfler et al., 2014). The effectiveness of this type of device tends, therefore, to be low. Pneumatic stunning devices are more effective in this respect (Figure 3).

Details are in the caption following the image
Pneumatic captive bolt stunning devices are used today in a number of industrial cattle abattoirs in Europe (photo by author Kamenik)

Oliveira et al. (2018) measured a bolt kinetic energy of 448 J using a pneumatic stunning device. The energy of the bolt, as well as its speed, depend on the operating pressure of the compressed air. Oliveira et al. (2017) tested pneumatically controlled stunning devices with low operating pressure (1.10 MPa/160 psi; 1.21 MPa/175 psi) and high operating pressure (1.31 MPa/190 psi) at two abattoirs in Brazil. The weight of the bolt was constant (0.297 kg). While the bolt attained a speed of 47.7–48.8 m/s at low operating air pressure, it was significantly higher (54.6 m/s; < 0.01) at a higher pressure. The same was also true of the kinetic energy (338–356 J as opposed to 448 J; < 0.01).

The kinetic energy transferred to the head of the stunned animal is affected to a far greater degree by differences in the speed of the captive bolt than by its weight (Gibson, Mason et al. 2015). The recommended minimum speed of the bolt is generally 55 m/s for steers, heifers, and cows (Gibson, Mason et al. 2015) and 70 m/s for bulls (Grandin, 2013). Daly, Gregory, and Wotton (1987) stated two factors for the effective stunning of adult cattle—the speed of the captive bolt and the weight of the stunned animals. According to these authors, bolt speeds of 55 and 58 m/s significantly increase the extent of damage to the brain in comparison with speeds of 41 and 47 m/s. As stated by Oliveira et al. (2017), the limit values given above are based on classic stunning devices using a cartridge.

As the speed of the bolts is associated with their kinetic energy, it is also strongly affected by the use of cartridges in classic stunning devices. During their tests on stunning devices, Gibson, Mason et al. (2015) determined bolt speeds of between 46.20 and 61.53 m/s with the strongest cartridges, as compared to between 27.16 and 38.75 m/s with the weakest cartridges. This study also included tests on 30 stunning devices used by the government agencies of the United Kingdom. The average speed of the captive bolt was 46.66 m/s (SD ±1.72). Eighty-seven percent had a speed of 46.0–48.9 m/s. Three devices were of low performance with average speeds of 42.70 m/s (SD ±0.59), 40.30 m/s (SD ±0.56), and 44.97 m/s (SD ±0.61). The failure to observe the values of the recommended minimum speed of the captive bolt during shooting does not, however, automatically mean ineffective stunning. Von Holleben and her colleagues determined a bolt speed of 42–44 m/s during the use of a pneumatic stunning device. The effectiveness of stunning was, however, extremely high and all the animals were stunned with the first shot (von Holleben et al., 2018).

In addition to the selection of the appropriate type of stunning device and the right kind of cartridge (or the appropriate air pressure in pneumatic devices), attention must also be paid to the regular cleaning and maintenance of the device and the prompt replacement of worn parts. According to Grandin (2013), monitoring at 10 cattle abattoirs in the USA showed that the failure to perform daily maintenance was the number one cause of the failure of stunning devices. Captive bolt stunning devices should be regularly checked for their state of wear and cleaned to maintain their performance after every 500 shots (Gibson, Mason et al. 2015). Grandin (2013) recommends daily cleaning of both pneumatically controlled stunning devices and cartridge devices. Captive bolt stunning devices have parts that must be replaced in accordance with the instructions of the manufacturer. They demand the same care as firearms (Grandin, 2013). Compressed air devices demand checks of the air intake (including the proper functioning of the compressor).

3 EVALUATION OF THE EFFECTIVENESS OF CATTLE STUNNING AT ABATTOIRS

Following stunning, it is essential to confirm that the animal is insensitive to pain and in a permanent state of unconsciousness before it is hoisted onto the bleeding line (Grandin, 2013). The most important outcome of the process of stunning an animal is it being made insensible to pain. The following symptoms of a return to consciousness, and thereby sensibility, may not be present if stunning is to be considered effective (Grandin, 2002, 2013):
  • Rhythmic breathing: the ribs move in and out at least twice. Do not confuse with gasping for air like a fish out of water.
  • Natural autonomic blinking or a response to a hand moving in front of the eyes without touching the animal. Do not confuse with nystagmus (vibrating eyelid). It is a good idea to observe animals in stalls before slaughter to recognize what natural blinking looks like.
  • Vocalizations—mooing, bellowing, groaning. Isolated mild groaning as a result of the sudden release of air may appear immediately after stunning. No other vocalizations may occur.
  • An attempt to regain posture or raise the head. As soon as the animal is hoisted onto the line, its head must be hanging loose and floppy.
  • Reaction to a pinprick to the inner skin of the nostril.
  • The eye following a moving object.

Atkinson et al. (2013) categorized three levels of stun quality (Stun Quality Rating, SQR) on a total of 998 cattle at an abattoir with an average daily capacity of 200 cattle. Adequate (deep) stunning (SQR0) was characterized by the immediate collapse of the animal (Figure 4), a tonic phase followed by a clonic phase with spasms and involuntary limb movements, the cessation of rhythmic breathing, no attempt to regain posture, the absence of vocalization, the absence of pain perception, and the absence of corneal reflex or eyeball movements.

Details are in the caption following the image
The collapse of the animal and the loss of consciousness and sensibility facilitate further handling up to the moment of slaughter by bleeding (photo by author Kamenik)

Any symptoms outside the above criteria were recorded. Symptoms including failure to collapse, vocalizations, blinking, corneal reflex, pain response, an attempt to regain posture or rhythmic breathing were considered signs of sensibility or imminent recovery of consciousness. In such case the stun quality was graded SQR3. Nystagmus and full eyeball rotation were reason for classification as SQR2. Category SQR1 symptoms (partial eyeball rotation, gasping, groaning, strong reaction to pricking, ears backwards or tongue retained in the mouth following sticking) were not considered direct indicators of sensibility. Cattle rated as either SQR2 or SQR3 were considered inadequately stunned and the repeat use of the stunning device followed. Of the 998 cattle assessed, 84.1% were correctly stunned (SQR0). The percentage of inadequately stunned cattle recorded was 12.5% (7.7% SQR2, 4.8% SQR3). An uncertain stun quality (SQR1) was observed in 3.3% of cases. 16.7% of bulls were inadequately stunned, in comparison with 6.5% of other classes of cattle (< 0.0001). Category SQR3 was also far more frequent in bulls (6.9%) than in other classes of cattle (2.1%; < 0.0011) (Atkinson et al., 2013).

Dörfler et al. (2013) categorized stun quality parameters into three groups (categories I–III). Animals collapsing immediately after stunning, with tonic spasms, without regular respiration, without a corneal reflex, without eye movement or vocalizations, with a straight top line without movement and with a protruding tongue belonged to category I. Animals in category II displayed nystagmus or eyeball rotation and atypical movements, or lacked typical spasms. Other symptoms were in agreement with category I. Animals in category III showed an attempt to regain posture, regular respiration, blinking, corneal reflex, vocalizations, curving of the top line, and reaction to pain from a pinprick to the inner skin of the nostril. At abattoir A (n = 694 animals), 5.7% inadequately stunned animals were recorded, with a figure of 8.1% recorded for bulls, with the use of a KS device (80 mm bolt). The proportion of inadequately stunned animals was considerably lower (1.6% KR and 1.9% KL) when the other two devices were used (KR: 85 mm bolt; KL: 125 mm bolt). At abattoir B (n = 1,244 animals), the proportion of inadequately stunned animals was 1.7% with a KS device and 0.9% with a KR device (Dörfler et al., 2013).

In their experiment, Terlouw et al. (2015) studied the possible effect of the gender (class) of cattle on stun quality. Their evaluation was performed on 40 animals (20 cows, 20 bulls). A device with a bolt length of 90 mm was used on the bulls, whereas a length of 85 mm was used on the cows. The bolt diameter was 12 mm. None of the animals displayed a corneal reflex after stunning. Fifteen of the 20 bulls evaluated showed signs of eye rotation or rhythmic breathing. These symptoms were not observed in any of the cows. Two bulls were shot a total of three times (both displayed eye rotation and rhythmic breathing), whereas one bull was shot twice (with manifestations of eye rotation). When these animals were hoisted for bleeding, they began to show signs of neck movement. This was followed by clonic spasms of the forelimbs and hindlimbs and movements of the neck and back. Circular movements of the head were recorded in six cows, though this type of movement was not observed in bulls. Sideward movements of the head occurred in all 20 cows, and this head position was recorded in 13 bulls. Four bulls did not display any movement at all. Movements of the fore limbs were observed in 13 cows and 7 bulls, movements of the hind limbs in 16 cows and 12 bulls (Terlouw et al., 2015). Grandin (2013) considers the interpretation of reflex kicking motions with the limbs as a return to a state of sensibility a mistake made by many people at abattoirs in the evaluation of the loss of consciousness. Reflex kicking motions of the limbs may be a sign of correct stunning in animals in a state of unconsciousness. According to the Terlouw et al. (2015), the presence of limb movements or turning of the head cannot be considered an indicator of the degree of consciousness. Structures in the brain stem and spinal cord are engaged in the autonomic production of rhythmic motor activity which results in the occurrence of uncontrolled movements of the limbs or neck independently of consciousness. Such movements have even been recorded in stunned animals in which the connection between the brain and the spinal cord has been interrupted at the level between the foramen magnum and the first vertebra (Terlouw et al., 2015).

Martin et al. (2018) studied whether a longer bolt serves as a tool to suppress limb movements following stunning as a consequence of greater brain damage at commercial abattoirs in the USA. They studied 2,850 animals stunned with the use of captive bolts of three lengths (standard: 152.4 mm, medium: 165.1 mm, and long: 177.8 mm).

Analysis of limb movement after stunning showed that the increasing length of the captive bolt was not accompanied by a reduction to motor activity in the limbs following animal stunning. When a longer captive bolt was used, the slaughtered cattle displayed increased kicking with the fore limbs. More frequent kicking with the hind limbs was also observed in the Holstein breed. This may have been associated with greater brain damage caused by a longer bolt. Greater brain damage with an elongated captive bolt could lead to greater damage to the deeper areas of the brain that control motion—the basal ganglia which help control coordination and movement or the cerebellum which suppresses involuntary movements and receives proprioceptive signals from the spinal cord. Connecting neurons which create a network controlling motor output are at the heart of the motor system of the spinal cord. The lumbar section of the spinal cord contains neuronal elements that determine the timing and activation of the muscles of the hind limbs designed for motion. The cervical section of the spinal cord controls the movement of the fore limbs. Synaptic interactions across these different pathways create basic neural circuits that create intersections between higher brain function and executive spinal circuits (Martin et al., 2018).

The higher frequency of eye movement and rhythmic respiration in bulls in comparison with cows evidently reflects differences in brain damage in cattle of different sexes during stunning with a captive bolt. The absence of a corneal reflex is a sign that the reticular formation is no longer functioning properly. The absence of a corneal reflex is therefore an indication of the loss of consciousness. The absence of a corneal reflex contrasted in the experiment (studying the effectiveness of stunning in 20 cows and 20 bulls) by Terlouw et al. (2015) with the presence of eye movement or rhythmic breathing in bulls. This meant that the depth of unconsciousness in bulls did not attain the standard of stun quality in cows. The absence of rhythmic breathing is a sign of the fact that the respiratory function of the medulla oblongata is no longer apparent. The presence of rhythmic breathing casts the state of unconsciousness into doubt and is an indication for the repeated use of the stunning device.

Nystagmus is considered a less reliable indicator (Terlouw et al., 2015). According to Grandin (2013) a correctly stunned animal must have its eyes open with a wide empty expression. Nystagmus or eye rotation must not be evident. Gregory et al. (2007) recorded nystagmus in 3.2% of cases during their assessment of the effectiveness of stunning on 1,608 animals at cattle slaughter. Inadequate stunning (low depth of concussion) was interpreted during the manifestation of one or more of the following symptoms immediately after shooting (the animal did not collapse, normal rhythmic breathing, eye rotation, positive corneal reflex). Such states were found in 140 animals (8.7%).

Dörfler et al. (2013) defined the degree of flawed stunning as the frequency of the necessity of repeated use of the stunning device due to animals not being adequately stunned following the first shot. According to the data in the literature, the degree of flawed stunning at abattoirs during cattle slaughtering ranges between 4 and 9%. Flawed stunning occurs twice as often in bulls in comparison with cows and heifers. Oliveira et al. (2018) assessed the effectiveness of stunning on 455 animals with the use of a pneumatic device (bolt length 210 mm). 99% of animals collapsed following the first shot. Nevertheless, 12% of animals had to receive two or more shots. Rhythmic breathing was observed following the first shot in 8% of animals, an attempt to stand in 1%, a corneal reflex in 1% of animals, and eye rotation in 1%. Tonic spasms were seen in 62% of stunned animals.

4 THE EFFECT OF THE SHOT LOCATION ON THE QUALITY OF CATTLE STUNNING

The ideal place to position a penetrative device lies in the frontal region of the head at the point of intersection of two imaginary lines connecting the base of the horns with the opposite eyes (von Holleben et al., 2018; Oliveira et al., 2018). It has been found that if the shot location lies more than 2 cm from this ideal position there is a greater risk that the concussion caused will not be sufficiently deep (Figures 5-7). The angle at which the penetrative device is held to the plane of the frontal region is also important and should be 90° (Fries et al., 2012).

Details are in the caption following the image
Top view of the right half of a cattle brain. Green circle—the ideal shot location, red arrow—the actual shot location, blue line—the boundary between the nasal cavity and the cranial cavity (photo by authors Paral and Pyszko)
Details are in the caption following the image
View of the right half of the cranial cavity of a cow. Green circle—the ideal shot location, red arrow—the actual shot location, blue line—the boundary between the nasal cavity and the cranial cavity (photo by authors Paral and Pyszko)
Details are in the caption following the image
(a, b) View of the right half of the brain in the cranial cavity of a cow. Paramedian section. Green circle—the ideal shot location, pincers—the actual shot location, green arrows—blood in the subarachnoid space (photo by authors Paral and Pyszko)

The bones of the frontal region, where the captive bolt device is placed during stunning, are formed by both frontal bones, or more precisely their frontal scale—the squama frontalis. The sutura sagitalis (interfrontalis) join both frontal bones in the median plane. In the studied region, the squama frontalis consists of two lamellae of compact bone—the facies externa and facies interna, between which a large paranasal frontal cavity called the sinus frontalis is located. A tough meninx (dura mater encephali) is attached to the periosteum of the inner surface of the bone whose duplicature forms the cerebral falx (falx cerebri) in the median plane. There is an unpaired cerebral sinus (sinus sagitalis) inside the falx cerebri. With its continuous layer, it adjoins the solid meninx of the arachnoid mater which creates small pins—granulationes arachnoideales—in the falx cerebri region. These pins penetrate the sinus sagitalis. Fine fibers of arachnoid mater are located in the space between the tough and the soft meninx. They start from a continuous layer and terminate in the soft meninx (pia mater) which is attached directly to the surface of the brain. The space between the arachnoid mater and the soft meninx is called the cavum subarachnoideale and, in addition to arachnoid fibers, is filled with cerebrospinal fluid—liquor cerebrospinalis.

As far as the brain is concerned, there are dorsal surfaces of both hemispheres of the cerebrum (telencephalon) in the described area. This is exactly the dorsal section of the convex plane (facies convexa) which forms the parietal lobe (lobus parietalis) in the neocortex of the cerebrum. The area sensitiva is located right in the lobus parietalis, caudally behind the sulcus ansatus. Between the hemispheres there is a deep longitudinal groove called the fissura longitudinalis cerebri, into which the falx cerebri is inserted. The medial surface of the hemisphere—facies medialis—is oriented toward the fissura longitudinalis. A blunt dorsal border—the margo dorsalis—separates this area from the convex plane.

Fries et al. (2012) examined a total of 8,879 cattle skulls at two cutting plants in Germany. They studied the accuracy of use of the stunning device from three perspectives: the number of shots to the skull, the placement of the shot on the skull, and the direction of the shot (angle) in respect to the plane of the skull. They assigned the results to one of three categories. In the case of category I, the shot location was a maximum of 2.5 cm from the point of intersection of lines connecting the eyes and the bases of the opposite horns. The maximum deviation from the vertical direction was at an angle of 0–10°. In such case, there is a good expectation of hitting the brain stem with high probability. Category II represented deviation from the correct shot position of 3.0–4.5 cm and a deviation in the shot angle of 10–20° from the vertical direction. Finally, category III meant a deviation from the correct position of more than 5 cm and an angle of deviation from the vertical direction greater than 20°.

At plant 1, there were 4,399 skulls with a single shot out of a total of 4,592 skulls. Of these skulls, 64.7% were assigned to category I and 31.3% to category II. 4.0% of skulls fell outside this range. More than one shot was found on 192 skulls (4.2%), and in one case not a single shot was found on the skull. Of the total number of 4,592 skulls, 367 (7.8%) belonged to category III or displayed more than one shot. 4,287 skulls were examined at plant 2. 4,191 had a single shot. 65.3% of skulls were assigned to category I and 31.5% to category II. 3.1% of skulls were assigned to category III. Two shots were found on 92 skulls, and three shots on four skulls (2.2% with more than one shot). A total of 227 skulls (5.3%) were either assigned to category II or showed more than one shot (Fries et al., 2012).

According to von Wenzlawowicz, von Holleben, and Eser (2012), the correct shot location, including the standard angle at which the stunning device is placed to the planes of the skull, can be improved with the use of fixation of the head of the animal. Atkinson et al. (2013) determined 8.0% of cases of inaccurate shooting (outside a circle of a diameter of 2 cm from the point of intersection of lines connecting the base of the horn or the upper edge of the ear with the opposite eye) from their analysis of the heads of 998 cattle after slaughter and carcass processing. The authors did not evaluate either the angle or depth of penetration of the bolt into the brain. Fourteen bulls included in the study were shot more than three times, with one being shot as many as five times (Holstein breed). None of the cows, steers, or calves were shot more than twice. Gregory et al. (2007) described a high proportion of inaccurate shot locations in their study. Their analysis was performed on 1,608 animals slaughtered at a cattle abattoir, with stunning being performed by three experienced shooters. Forty-three percent of the bulls were shot more than 2 cm from the ideal position. The figure for the other categories was 53%.

von Wenzlawowicz et al. (2012) stated that it is often difficult to achieve the right shot location with the use of a powerful pneumatic stunning device, though in such cases slight deviations do not influence the effectiveness of stunning. The results of Oliveira et al. (2017, 2018), who did not determine a significant relationship between the shot position or the distance from the ideal location and clinical symptoms of consciousness/unconsciousness in slaughtered animals, agree with this contention. Tests were performed on 455 animals. The correct position during stunning with a pneumatic penetrative device with a captive bolt (up to 2 cm from the correct position) was recorded in 34.7% of animals. During their assessment of the effectiveness of stunning with the use of a pneumatic stunning device (n = 397 animals), von Holleben et al. (2018) recorded the incorrect positioning of the stunning device (more than 2 cm from the ideal position) in nine cattle. Deviations of 15 or more degrees from the perpendicular line were found in a total of 16 cases of stunned animals. A deviation in the positioning of the stunning device in terms of both its position (2.5 cm to the right) and angle of direction (20° to the right) was found in just a single cow.

Grandin (2013) stated an agitated animal, which makes it difficult to place the stunning device in the right position in the frontal region, as one of four main reasons for the inadequate stunning of cattle following the first shot (the other three reasons were associated with the stunning device itself). Placing the stunning device in the correct position also depends on the experience of the person performing stunning. Dörfler et al. (2013) recorded differences in the effectiveness of stunning depending on whether stunning at commercial slaughter was performed by an experienced shooter or by a stand-in. Similarly, Atkinson et al. (2013) found the most frequent occurrence of imprecise stunning in a shooter who had worked at the abattoir for just a few months in comparison with another four people with at least 3 years of experience. A shooter with 15 years of experience recorded the smallest number of imprecise shots.

5 OTHER ASPECTS OF THE USE OF A CAPTIVE BOLT STUNNING DEVICE

The beginning of the millennium saw increased attention focused on the possible effect of the use of captive bolt stunning devices on the distribution of abnormal prions from the brains of cattle affected by bovine spongiform encephalopathy (BSE) to edible tissues (Lim, Erwanto, & Lee, 2007; Pitardi et al., 2013; Prendergast, Sheriadan, Daly, McDowell, & Blair, 2003). This was associated with the finding that pieces of brain tissue are disseminated to the blood vessels following traumatic brain injury. As the heart is still active in stunned animals, particles of brain tissue can travel as far as the lungs through the vascular system (Gregory, 2005). Brain tissue also gets into the area around the wound through the opening at the shot location, as has been confirmed by the study conducted by Prendergast et al. (2003). Nevertheless, the comparison of two methods of stunning cattle at abattoirs (penetrative with a captive bolt and a nonpenetrative mechanical method) conducted by Lim et al. (2007) in Korea did not find any difference in the frequency of contamination of carcasses by particles of central nervous system tissue (CNST), although the level of contamination with CNST was higher with the use of a captive bolt stunning device (< 0.001). A higher level of contamination was found on the interior of carcasses in comparison with their exterior which pointed to a strong effect of halving of the body through the middle of the spinal canal on the transmission of pieces of CNST (Lim et al., 2007). Pitardi et al. (2013) also consider the halving of cattle carcasses a key step in contamination by particles of CNST. In general terms, however, in view of the significant decline in the number of new cases of BSE in Europe and around the world, the issue of contamination by particles of CNST at abattoirs has escaped the attention of inspection bodies and operators.

The open wound in the frontal region of a slaughtered cow resulting from the application of a captive bolt stunning device may also be a route for the bacterial contamination of the carcass. Buncic, McKinstry, Reid, and Anil (2002) performed abattoir tests during the slaughter of lambs with a captive bolt stunning device. They used artificial contamination with a strain of Escherichia coli K12 and Pseudomonas fluorescens in their experiments. In both cases, the strains used were resistant to nalidixic acid. When the stunning device was contaminated by contact with an artificially contaminated brain and subsequently used to stun other lambs, the bacterial strains used were found in 100% of stunning wounds, in the blood of 30% of lambs and on the carcass surface of 40% of slaughtered animals. The bacterial strains used were not detected in the organs or meat. When the stunning wounds were inoculated immediately after stunning, the bacteria used were then found in 80% of samples of lung and spleen, 30% of lymph nodes and 20% of samples of meat in the lambs artificially inoculated in this way. The bacterial strains were found in 50% of cases on the carcass surface. The authors deduced from the results that the use of a captive bolt stunning device may present the risk of internal and external microbial contamination of eatable tissues and organs (Buncic et al., 2002).

Another aspect of the use of a captive bolt stunning is its acceptability for religious communities, namely Muslims and Jews. One of the basic requirements for halal slaughter practiced by Muslims is that the animal has to be slaughtered alive, and concerns have been raised about the likelihood of some animals dying as a result of stunning (Fuseini, Knowles, Hadley, & Wotton, 2016). However, preslaughter stunning that does not stop the heart before the start of exsanguination should be acceptable and encouraged (Anil et al., 2006). Halal Certification Bodies generally accept simple or reversible stunning (Fuseini et al., 2016) but penetrative (captive bolt) stunning is unacceptable because the animal will not make a complete recovery if the stunning is not followed by a slaughter (Farouk, 2013; Nakyinsige et al., 2013). Another objection to stunning methods concern the claim that it prevents all of the blood draining from the animal and the carcass. Anil et al. (2006) compared captive bolt stunning followed by neck cutting with the halal slaughter method without stunning. Their results showed that captive bolt stunning followed by a neck cut did not impede exsanguination in terms of the rate of blood loss and total blood loss when compared with halal slaughter without stunning. In addition, meat quality parameters determined as pH, packed cell volume, and color were not affected. On the other hand, the kosher requirement that the animal not only be alive but conscious prior to slaughter would render any methods of stunning now or in the future unacceptable for Jews (Farouk, 2013).

6 CONCLUSION

The captive bolt device has been used for stunning cattle at abattoirs for more than 100 years. In addition to classic devices, in which the energy for expelling the captive bolt is supplied by gases released by the activation of the cartridge's percussion cap, pneumatic stunning devices are finding increasing use under industrial conditions. The basis of effective stunning is the use of a suitable type of device, with the speed of the bolt and the kinetic energy corresponding to the anatomical parameters of the slaughtered animal. The importance of the regular cleaning and maintenance of stunning devices and monitoring of the effectiveness of stunning goes without saying. The immediate loss of sensibility in the animal must occur after the first shot. The effectiveness of the stunning process can be quantified by regular monitoring of the behavior of animals after stunning with an emphasis on the loss of reflexes (corneal reflex, regular breathing, attempts to regain physiological posture) and checks on the shot location on the skulls of slaughtered animals.

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