Introduction
Broiler welfare is an essential component of the broiler industry and must be taken into account from the time that the chick is hatched until slaughter at the processing plant. Broiler welfare is important because it gives respect to the life of the animal and maximises the quality of the resulting meat. The stunning and harvest procedures also influence animal welfare and meat quality (Kannan and Mench, Reference KANNAN and MENCH1996). For a stunning/harvest method to be humane, it must produce insensibility as rapidly and painlessly as possible. In addition, the stunning method must ensure that the animal is desensitised throughout the slaughter process.
Animal welfare during slaughter was one of the major criteria that led to legislative requirements for stunning across the world. In the United States, the ‘Humane Methods of Slaughter Act’ (1978) mandated humane handling and immobilisation of livestock prior to slaughter. Nevertheless, poultry is not covered under this act, and thereby stunning conditions for poultry are not mandatory as originally dictated (Poultry Products Inspection Act, 1957). In 1993, the European Union Council established a directive to ensure pre-harvest welfare of livestock, including poultry species, and mandates stunning to ensure that birds are rendered insensible to pain, until death by exsanguination (Official Journal of the European Union, Reference OFFICIAL JOURNAL OF THE EUROPEAN UNION2009).
Various stunning methods have been utilised in the poultry industry. An effective stunning procedure instantaneously induces a state of unconsciousness and insensibility to pain that lasts until the death of the animal, immobilises the animal for automated exsanguination, and does not have a negative effect on meat quality (Savenije et al., Reference SAVENIJE, SCHREURS, WINKELMAN-GOEDHART, GERRITZEN, KORF and LAMBOOIJ2002). Bruising, discolorations (Bilgili, Reference BILGILI1992), and broken bones (Gregory and Wilkins, Reference GREGORY and WILKINS1989) are the primary defects often attributed to the stunning-exsanguination stage of harvest. Stunning prior to exsanguination can be accomplished by passing an electrical current through the broiler, modification of the atmosphere by altering the composition of the air, or by decreasing atmospheric pressure. Electrical stunning has conventionally been used in processing facilities which has resulted in automation and rapid processing. Modified atmosphere stun-kill methods have been researched as an alternative to electrical stunning as a means to potentially improve animal welfare, and can be accomplished through gas stunning with carbon dioxide, argon, or nitrogen. Recently, low-atmosphere pressure has been utilised successfully to induce insensibility in broilers without any detrimental effect on meat quality (Thaxton et al., Reference THAXTON, CHRISTENSEN, SCHILLING, R.J. and THAXTON2010).
Electrical stunning, controlled atmosphere stunning and low-atmosphere pressure stunning are all effective at ensuring that the broiler is desensitised to pain and rendered unconscious throughout the harvest process. However, each method has positive aspects and limitations with respect to application, animal welfare, employee welfare, and meat product quality. This paper will focus on these three stunning methods and their impact on animal welfare, physiology, rigor mortis patterns, carcass characteristics, meat quality and application in commercial plant operations.
Electrical stunning
Electrical stunning is the most common stunning method that is utilised in commercial poultry plants in both the United States and Europe (Bilgili, Reference BILGILI1999; Goksoy et al., Reference GOKSOY, MC KINSTRY, WILKINS, PARKMAN, PHILLIPS, RICHARDSON and ANIL1999). Electrical stunning is accomplished by passing a sufficient amount of electrical current through the brain to render the broilers unconscious (Bilgili, Reference BILGILI1992). Heath et al. (Reference HEATH, THALER and JAMES1994) reported that more than 97% of all poultry were subjected to electrical stunning in the United States in the early 1990s. There are two main types of electrical stunning, whole-body stunning and head-only stunning. Whole-body stunning refers to the conventional approach where the head is passed through a water-bath with electrical current. In head-only stunning, current flows through the electrodes placed on both sides of the head (Gregory, Reference GREGORY1989). Head-only stunning is not used in commercial stunning of broilers but is a viable option that has been researched in turkeys. Among the different types of electrical stunning systems that are available, the most common system is electrical water bath stunning (Bilgili, Reference BILGILI1992). Electrical stunning is most often conducted in a water bath stunner that is maintained at constant voltage. The broilers are placed in shackles so that their heads come in contact with the water bath. The electrical current flows through the brain of the broiler causing disruption of brain function.
The discharge of electricity from electrical stunning into animals causes the release of excitatory amino acid neurotransmitters, accompanied by epileptiform activity, as demonstrated in sheep research (Meldrum, Reference MELDRUM1975), that results in disruption of the central nervous system. Using an electroencephalogram to measure the electrical activity of the brain of broilers, it has been indicated that prior to stunning the electrical brain activity is very rhythmic and steady. However after stunning, unipolar, high amplitude, and low frequency electrical activity is observed in broilers (Raj, Reference RAJ1998), and manifested as an epileptic state. The cause of the tonic-clonic seizure is thought to be due to the release of excitatory amino acid neurotransmitters, more specifically glutamate and aspartate as observed in sheep (Cook et al., Reference COOK, DEVINE, TAVENER and GILBERT1992; Cook, Reference COOK1993). Glutamate has an excitatory effect on ligand-gated ion channels which increases sodium and calcium conductance and various other regulatory interactions that result in exitoxicity (Chapman et al., Reference CHAPMAN, VANDONGEN and VANDONGEN1997). After electrical stunning, aspartate reacts with acetyl-CoA to form N-Acetyl-aspartate. The complete function of N-Acetyl-aspartate is not fully known to date. However, it is believed to be a major osmolyte (which are responsible for fluid balance in the brain). The release of glutamate due to electrical stunning can then bind to the newly formed N-Acetyl-aspartate and further disrupt brain function. A third amino acid, γ amino-4-butyric acid (GABA) has been reported to increase in concentration after electrical stunning. γ- amino-4-butyric acid receptors are ligand-activated chloride channels that are located on the neurons. When activated by the binding of GABA, the receptors shuttle chlorine ions across the neuron membrane (Olson, Reference OLSON2002). It is speculated that the activation of the GABA receptor has an analgesic effect on animals after electrical stunning (Cook et al., Reference COOK, DEVINE, GILBERT, SMITH and MAASLAND1995). The unconsciousness of broilers after electrical stunning is thought to be related to neural disruption of various nuclei and structures of the brain such as the intralaminar nuclei located within the thalamus, which are essential for maintaining the waking state (Butler and Cotterill, Reference BUTLER and COTTERILL2006). This disruption is driven by both the initial application of electricity to the brain and the release of the neurotransmitters that are released due to electrical stunning.
Electrical stunning results in brain function disturbances in the form of a general epileptiform insult. The physiological responses of electrical stunning have been researched by various investigators (Richards and Sykes, Reference RICHARDS and SYKES1967; Gregory and Wotton, Reference GREGORY and WOTTON1989, Reference GREGORY and WOTTON1990). Inhibition of the reticular activating system (RAS) and somatosensory impulses have been attributed to the occurrence of unconsciousness (Heath et al., Reference HEATH, THALER and JAMES1994). RAS is nonspecific, while the somatosensory impulse is specific. Further research focused on the role of somatosensory evoked potentials (SEP) utilising EEG and concluded that loss of SEPs could be related to brain failure and absence of pain perception (Gregory and Wotton, Reference GREGORY and WOTTON1989; Reference GREGORY and WOTTON1990). During electrical stunning, death may occur due to cardiac arrest and loss of oxygen to the brain (Turcsan et al., Reference TURCSAN, VARGA, SZIGETI, TURCSAN, CSURAK and SZALAI2003). In their investigations on the comparison of amperages (60 versus 110 mA) used for electrical stunning, Gregory and Austin (Reference GREGORY and AUSTIN1992) observed about a five-fold increase in ventricular fibrillation at greater amperage, thereby inhibiting the recovery of chickens subjected to stunning and consequently leading to death. However, insufficient currents may not prevent the perception of pain, stress or discomfort even though the broiler is physically immobilized (Bilgili, Reference BILGILI1999). Low voltage stunning (US) is utilised in the United States, and high current stunning is used in Europe that results in electrocution (EU) (Bilgili, Reference BILGILI1999).
effects on carcass characteristics
Electrical stunning (EU) is utilised in the European Union during neck cutting to induce unconsciousness and bleeding for reasons of animal welfare or to facilitate automatic neck cutting in the U.S. through immobilisation (Lambooij et al., Reference LAMBOOIJ, GERRITZEN, ENGEL, HILLEBRAND and PIETERSE1999). To ensure an irreversible stun, high amperage current (120 to 150 mA per bird) is utilised in Europe, so that the birds are stunned to death (Fletcher, Reference FLETCHER1999). High voltage stunning procedures have been linked to broken bones (Gregory and Wilkins, Reference GREGORY and WILKINS1989), breast meat haemorrhages (Veerkamp and de Vries, Reference VEERKAMP and DE VRIES1983; Veerkamp, Reference VEERKAMP1988), separation of shoulder muscle tendons, and split tendons (Sams, Reference SAMS1996). No clear relationship exists between stunning amperage and whole carcass quality attributes (Griffiths, Reference GRIFFITHS1985; Bilgili, Reference BILGILI1992), but high stunning amperages have been associated with haemorrhaging in deep breast muscles (Veerkamp, Reference VEERKAMP1988; Gregory and Wilkins, Reference GREGORY and WILKINS1989).
Low voltage electrical stunning (US) is an effective method for immobilizing broilers (Bilgili, Reference BILGILI1999). Heath et al. (Reference HEATH, THALER and JAMES1994) reported that low voltage (10 to 25 V) and high frequency (500 Hz) systems are used in 77.4% of U.S poultry plants. Low voltage electrical stunning can decrease the incidence of carcass quality damage and haemorrhaging that is associated with high voltage electrical stunning. However, a bird will regain consciousness if not exsanguinated within approximately two minutes of stunning. Low voltage electrical stunning has been shown to negatively affect early blood loss, in comparison with high amperage electrical stunning, but does not affect total blood loss after the 90 to 120 second exsanguination period (Gregory, Reference GREGORY1993; Papinaho and Fletcher, Reference PAPINAHO and FLETCHER1995). Craig and Fletcher (Reference CRAIG and FLETCHER1997) evaluated the effects of high and low frequency currents on stunning, and reported that high frequency (500Hz) currents have a greater effect on the central nervous system when compared to low frequency (50 to 60 Hz), which may also impact the muscular system. High frequency current is predominantly associated with decreased muscular damage. Similarly, Gregory et al. (Reference GREGORY, WILKINS and WOTTON1991) documented fewer incidences of broken bones during electrical stunning at high frequency (1500 Hz) than at low frequencies (50 Hz). The European Union recommended a minimum stunning current of 120 mA (EU) that induces unconsciousness and cardiac arrest, and assures an onset to an unrecoverable death by hypoxia leading to anoxia (Gregory, Reference GREGORY1992). But these high amperages can cause muscle contractions that lead to muscle fibre damage and subsequent haemorrhaging in muscle tissue. (Gregory and Wilkins, Reference GREGORY and WILKINS1989; Hillebrand et al., Reference HILLEBRAND, LAMBOOIJ and VEERKAMP1996a; Kranen et al., Reference KRANEN, SCHEELE, VEERKAMP, LAMBOOIJ, VAN KUPPEVELT and VEERKAMP1998). Haemorrhaging is due to a sharp increase in intravascular pressure (Kranen et al., Reference KRANEN, LAMBOOIJ, VEERKAMP, VAN KUPPEVELT and VEERKAMP2000), as a result of which blood capillaries may rupture and cause bleeding.
When comparing electrical stunning (EU, 100 V, 80 mA) with concussion stunning in a research trial, Goksoy et al. (Reference GOKSOY, MC KINSTRY, WILKINS, PARKMAN, PHILLIPS, RICHARDSON and ANIL1999) observed a higher incidence of broken bones, and bone (coracoid, furculum)- and muscle-haemorrhages in electrically stunned birds when compared to their counterparts stunned by concussion stunning. In contrast, electrically stunned birds exhibited a lower incidence of red wing tips and shoulder haemorrhages when compared to birds that were stunned by concussion. Nevertheless, the authors reported a rapid rate of blood loss in electrically stunned (non-fibrillated) birds when compared to concussion stunning. In a recent investigation, Lambooij et al. (Reference LAMBOOIJ, REIMERT and HINDLE2010) observed that in birds subjected to head-only electrical stunning, the percentage of fillets free of blood splashes was 80%, compared to 16% in conventional electrical stunning. However, the authors reported that head-only stunning resulted in wing flapping which could be a disadvantage as it may lead to broken bones and subsequent haemorrhages. Recent advances in electrical stunning systems focus on ‘tailor-made’ head-only stunning, which delivers the stunning current based on individual head resistance, and offers minimal carcass and meat defects (Bal, Reference BAL2011). Such systems utilise a restrainer cone to minimise carcass movements. However, additional research needs to be conducted on ‘tailor made’ head-only stunning since the above mentioned research was a small scale study with limited sample size. Such stunning would need to be conducted in commercial applications to verify the advantages that have been reported for this method.
effect on rigor mortis and meat quality
Low voltage (LV) and modified atmosphere stunning (MAS) have similar effects on rigor development and meat quality, but use of MAS may potentially allow processors to reduce deboning time for broiler breast meat when compared to LV electrical stunning (US) since the onset of rigor mortis occurred more rapidly in broilers subjected to modified atmosphere stunning in comparison to broilers subjected to LV electrical stunning (US) (Poole and Fletcher, Reference POOLE and FLETCHER1998; Papinaho et al., Reference PAPINAHO, FLETCHER and BUHR1995). Raj et al. (Reference RAJ, GREGORY and WILKINS1992) reported that EU electrical stunning can potentially cause tonic seizures that have a detrimental effect on breast meat quality such as haemorrhages. These tonic seizures or super contractions can lead to ruptured blood vessels that cause a high incidence of haemorrhages in breast muscle (Hillebrand et al., Reference HILLEBRAND, PIETERSE and LAMBOOIJ1996b). European Union electrical stunning (EU) can suppress the peri mortem struggle which delays post mortem glycolysis and minimises lactic acid accumulation early in post mortem (Papinaho et al., Reference PAPINAHO, FLETCHER and BUHR1995). Electrical stunning (50 mA and 125 mA) slows the onset of rigor mortis by about four hours when compared to birds that were not stunned (Papinaho and Fletcher, Reference PAPINAHO and FLETCHER1996). Broiler meat tends to become tough if it is deboned before the development of rigor mortis due to physical stimulation during cutting and stripping, cold shortening, and the absence of skeletal framework to restrain shortening (Sams, Reference SAMS1999).
Considering meat quality, Craig and Fletcher (Reference CRAIG and FLETCHER1997) reported no difference in breast meat colour and ultimate meat pH in birds stunned by high amperage (EU) or low voltage (US). In addition, the observed difference in tenderness was not commercially significant. In fact, many investigations concluded that different systems of electrical stunning do not have a significant influence on ultimate broiler meat quality, including ultimate pH, ultimate blood loss, meat colour, and tenderness (Papinaho and Fletcher, Reference PAPINAHO and FLETCHER1995; Craig and Fletcher, Reference CRAIG and FLETCHER1997; Lambooij et al., Reference LAMBOOIJ, REIMERT and HINDLE2010). Although, stunning method did have an influence on initial blood loss rate (Craig and Fletcher, Reference CRAIG and FLETCHER1997), initial pH (Papinaho and Fletcher, Reference PAPINAHO and FLETCHER1996; Craig and Fletcher, Reference CRAIG and FLETCHER1997), and rigor mortis development (Papinaho and Fletcher, Reference PAPINAHO and FLETCHER1996). Electrical stunning systems can potentially induce stress due to the uncrating and shackling of live broilers prior to stunning, potential pre-stunning electric shocks that may occur as in turkey (Wotton and Gregory, Reference WOTTON and GREGORY1991) when the wings contact the water bath prior to their heads, and variation in electrical impedance among broilers which may prevent cardiac arrest when a constant voltage stunner is used (Raj, Reference RAJ1998).
Gas stunning
Modified atmosphere stunning utilising CO2 (MA-CO2) has been researched since the 1950s (Kotula et al., Reference KOTULA, DREWNIAK and DAVIS1957). Modified atmospheric stunning involves controlled changes in the atmosphere surrounding a broiler such that the broiler loses consciousness due to lack of oxygen (hypoxia), excess CO2 (hypercapnic hypoxia), a combination of these two methods (hypercapnic anoxia) (Hoen and Lankhaar, Reference HOEN and LANKHAAR1999), use of oxygen with inert gases such as nitrogen or argon (Hypercapnic hyper oxygenation) or by atmospheric depressurisation (low atmosphere pressure stunning). The stunning gas or gas mixture should not be aversive to the broilers, and the induction of unconsciousness should be rapid (Raj, Reference RAJ1998). Carbon dioxide induces unconsciousness by reducing the pH of the cerebrospinal fluid (Eisele et al., Reference EISELE, EGER and MUALLEM1967). When the pH of blood falls below the normal level (7.4) to 7.1, it induces unconsciousness by influencing vital enzyme reactions, membrane permeability, and electrolyte imbalance. Even though these methods are effective and yield acceptable quality meat, an increased concentration of CO2 in combination with a lack of oxygen may cause excitation or convulsions in the broilers (Turcsan et al., Reference TURCSAN, SZIGETI, VARGA, FARKAS, BIRKAS and TURCSAN2001).
Several researchers have indicated that there are advantages to stunning with gases. One particular advantage includes the acceleration of rigor mortis (Raj et al., Reference RAJ, GREY, AUDSELY and GREGORY1990a; Raj et al., Reference RAJ, WILKINS, RICHARDSON, JOHNSON and WOTTON1997). Stunning and exsanguination by gas is effective at improving carcass quality by reducing bloodspots, especially those on the thighs and breasts, when compared to electrical stunning (EU electrocution) (Hoen and Lankhaar, Reference HOEN and LANKHAAR1999). Other benefits include reduction in pre-harvest stress due to eliminating the added excitement that is associated with shackling of live broilers during electrical stunning (Lambooij et al., Reference LAMBOOIJ, GERRITZEN, ENGEL, HILLEBRAND and PIETERSE1999; Gerritzen et al., Reference GERRITZEN, LAMBOOIJ, HILLEBRAND, LANKHAAR and PIETERSE2000). However, minimal research could be located on blood corticosterone levels from broilers subjected to MAS and compared to broilers that were electrically stunned (US and EU). Small scale studies (Xu et al., Reference XU, JI, YUE, WU, ZHANG, ZHANG and QI2011a; Reference XU, ZHANG, YUE, WU, ZHANG, JI and QI2011b) indicated that plasma corticosterone levels were comparable between MAS and ES stunned broilers. However, these were small scale pilot studies and further research would need to be conducted to determine if the use of MAS could lead to decreased corticosterone concentration, thus indicating lower stress. The results from the pilot studies above indicate that the death struggle from MAS may be equally as stressful to broilers as the shackling that occurs during ES stunning. One potential limitation with modified atmosphere stunning is that broilers may regain consciousness rapidly on exit from the gaseous atmosphere (Raj, Reference RAJ1998). To avoid this problem, Raj and Gregory (Reference RAJ and GREGORY1990) recommended that the broilers should be killed during stunning to prevent the broilers from regaining consciousness and to allow for easier handling.
effect on carcass characteristics
Modified atmosphere stunning with CO2 has been successfully utilised in pork slaughter for many years and has been investigated for possible uses in the poultry industry since the 1950s (Drewniak et al., Reference DREWNIAK, BAUSH and DAVIS1955; Kotula et al., Reference KOTULA, DREWNIAK and DAVIS1957). Kotula et al. (Reference KOTULA, DREWNIAK and DAVIS1961) developed an inline CO2 immobilisation system for chickens by using 33 to 36% CO2. Researchers have reported that stunning with CO2 increased initial blood loss compared to non-stunned birds (Kotula et al., Reference KOTULA, DREWNIAK and DAVIS1957), resulted in less muscle haemorrhaging and broken bones when compared to electrocution (Raj et al., Reference RAJ, GREGORY and AUSTIN1990b), and increased breast meat tenderness when compared to electrocution when stunning was conducted at levels of 40 or 45% CO2 (Raj et al., Reference RAJ, GREY, AUDSELY and GREGORY1990a; Fleming et al., Reference FLEMING, FRONING, BECK and SOSNICKI1991). Kang and Sams (Reference SAMS1999) observed a lower incidence of carcass damage in broilers that were stunned with CO2 when compared to those subjected to water-bath electrical stunning (35 mA, US), and attributed this to the broilers being calmer when stunned using modified atmosphere stunning. Poole and Fletcher (Reference POOLE and FLETCHER1998) concluded that stunning of broilers with 30% carbon dioxide and up to 5% residual oxygen in argon improved the quality of breast meat, when compared to electrical stunned broilers, which was attributed to the milder convulsions during gas stunning (Turcsan et al., Reference TURCSAN, SZIGETI, VARGA, FARKAS, BIRKAS and TURCSAN2001).
effect on rigor mortis and meat quality
With respect to tenderness, no differences were observed in shear values for breast fillets from broilers receiving no stun versus CO2 stun (Sams and Dzuik, Reference SAMS and DZUIK1995). When compared to electrical stunning, CO2 stunning has been reported to produce lower breast meat shear values at 1 h post-mortem than US electrical stunning (Veeramuthu and Sams, Reference VEERAMUTHU and SAMS1993). The death struggle induced by carbon dioxide stunning accelerates rigor development, as indicated by a more rapid onset of post mortem pH decline than occurs with US electrical stunning. This reduces the length of aging time (4 h vs. 7 h) required to ensure meat tenderness (Raj, Reference RAJ1994). Although the exact mechanism is not known, the increased anoxic convulsions (increased wing flapping) that have been observed in CO2 stunned broilers accelerates rigor development which leads to a more rapid utilisation of adenosine triphosphate (ATP) by the muscles when compared to muscles from electrically stunned broilers (Raj et al., Reference RAJ, WILKINS, RICHARDSON, JOHNSON and WOTTON1997). In addition, Kang and Sams (Reference SAMS1999) reported that even though breast meat pH decline did not differ between ES (US) and CO2 stunned broilers, the R-value was greater in CO2 stunned birds, thus indicating that the onset of rigor mortis was quicker.
Even though gas stunning has some advantages over electrical stunning with respect to avoiding bird handling stress and allowing earlier deboning, there are some distinct disadvantages: 1) Gaseous stunning involves an induction phase that can be stressful to the broilers (Lambooij et al., Reference LAMBOOIJ, GERRITZEN, ENGEL, HILLEBRAND and PIETERSE1999). 2) Carbon dioxide can cause breathlessness prior to the loss of consciousness (Raj, Reference RAJ1998). 3) Gases used in MASK are dangerous to humans. Inhalation of 30% carbon dioxide by humans causes a low level of pungency and breathlessness (Gregory et al., Reference GREGORY, RAJ, AUDSLEY and DALY1990). These limitations hinder the broad acceptance of gas stunning in the poultry industry.
Modified atmosphere - inert gas stunning
The use of a mixture of inert gases in combination with oxygen or carbon dioxide is an alternative approach for controlled atmosphere stunning. Oxygen deprivation in the body is termed hypoxia or anoxia. Inhalation of elevated concentrations of the inert gases (argon and nitrogen) causes hypoxia which eventually leads to anoxia (complete absence of oxygen). The brain is the most sensitive organ to a physiologic reduction in blood oxygen concentration and when the oxygen supply is insufficient for normal brain functioning, it will lead to unconsciousness and subsequent death (Guyton and Hall, Reference GUYTON. A.C. and HALL2010). In poultry, unconsciousness was observed when the concentration of oxygen was reduced below 5% O2 by volume (Woolley and Gentle, Reference WOOLLEY and GENTLE1988), whereas for anoxic stun-to-kill systems, less than 2% O2 by volume could be used (Raj, Reference RAJ1998). The commonly used gases are nitrogen and argon with or without CO2 for broilers and nitrogen with CO2 for turkey, which results in anoxic loss of sensibility. In commercial situations, Hoen and Lankhaar (Reference HOEN and LANKHAAR1999) reported that a few abattoirs use 90% argon in air, 60% argon in air with 30% carbon dioxide, or a mixture of 40% carbon dioxide, 30% oxygen, and 30% nitrogen. Argon is heavier than air and also tasteless and odourless, which makes it easier to administer during gas stunning. A combination of argon with carbon dioxide in gas stunning resulted in rapid cessation of brain functions (absence of SEP in about 24 seconds) in broiler chicken (Raj et al., Reference RAJ, WOTTON, MCKINSTRY, HILLENBRAND and PIERTERSE1998). In commercial situations, gas stunning minimises the handling of birds (uncrating/shackling) prior to stunning, thereby reducing pre-harvest stress. On the other hand, gas stunning can also lead to some distress in birds as exhibited by wing flapping, gasping and head shakes (Lambooij et al., Reference LAMBOOIJ, GERRITZEN, ENGEL, HILLEBRAND and PIETERSE1999). In addition, the oxygen-replacers like argon demonstrate decreased efficacy in chicks (Woolley and Gentle, Reference WOOLLEY and GENTLE1988), which would also likely be true for carbon dioxide and nitrogen.
With respect to carcass quality, Raj et al. (Reference RAJ, GREGORY and WILKINS1992) observed a higher incidence of wing damage in poultry subjected to inert gas stunning in comparison to electrical stunning (EU electrocution) which was attributed to the severe convulsions during inert gas stunning. In one experiment, Raj and Gregory (Reference RAJ and GREGORY1991) concluded that argon stunning resulted in fewer muscle haemorrhages, a more rapid decrease in early post mortem pH, and an earlier deboning time for breast meat when compared to electrocuted broilers. The rapid decline in pH was attributed to the peri mortem struggle during argon stunning and subsequent accelerated glycolysis. In another investigation, Raj (Reference RAJ1994) compared high frequency electrical stunning (electrocution) with argon stunning and reported less bleed-out in argon stunned birds. The difference in meat quality due to different stunning methods was documented by Uijttenboogaart (Reference UIJTTENBOOGAART1997). Modified atmosphere gas stunning resulted in darker and redder liver in comparison with electrocution stunning. Furthermore, breast meat colour was darker in argon and electrically stunned (EU) birds when compared to carbon dioxide stunned counterparts (Uijttenboogaart, Reference UIJTTENBOOGAART1997). A combination of greater L* value (above 60) and lower ultimate meat pH indicates the occurrence of pale meat with lower water holding capacity (Van Laack et al., Reference VAN LAACK, LIU, SMITH and LOVEDAY2000).
In their investigations to determine the effectiveness of gas mixtures for modified atmosphere stunning under commercial conditions utilising approximately 19,000 carcasses, McKeegan et al. (Reference MCKEEGAN, ABEYESINGHE, MCLEMAN, LOWE, DEMMERS, WHITE, KRANEN, VAN BEMMEL, LANKHAAR and WATHES2007) concluded that a combination of CO2 and O2 provided an advantage to poultry processors since there are a lower percentage of fractured wings (1.6 vs. 6.8) as compared to broilers subjected to stunning with argon + CO2. Furthermore, through a series of studies in laboratory and commercial settings, McKeegan et al. (Reference MCKEEGAN, ABEYESINGHE, MCLEMAN, LOWE, DEMMERS, WHITE, KRANEN, VAN BEMMEL, LANKHAAR and WATHES2007) suggested that a biphasic hypercapnic hypoxygenation approach, which utilises 40% CO2, 30% O2, 30% N2 (unconscious phase) and 80% CO2, 5% O2, 15% N2 (death phase) would ensure broiler welfare and carcass quality (Abeyesinghe et al., Reference ABEYESINGHE, MCKEEGAN, MCLEMAN, LOWE, DEMMERS, WHITE, KRANEN, BEMMEL, LANKHAAR and WATHES2007). McKeegan et al. (Reference MCKEEGAN, ABEYESINGHE, MCLEMAN, LOWE, DEMMERS, WHITE, KRANEN, VAN BEMMEL, LANKHAAR and WATHES2007) also reported greater susceptibility of the birds to exhibit agitated behavioural responses, including wing-flapping, jumping, twitching, and paddling along with severe convulsions, when stunned by a gas mixture containing argon, which could lead to carcass quality defects such as fractured wings and fillet haemorrhages.
Regarding the effect on rigor mortis and meat quality, Savenije et al. (Reference SAVENIJE, SCHREURS, WINKELMAN-GOEDHART, GERRITZEN, KORF and LAMBOOIJ2002), in a small-scale research trial, investigated the effect of stunning methods on muscle metabolism and reported that head-only stunning (electrocution) resulted in the greatest metabolic rate, which was indicated by a faster decrease in muscle pH, glycogen, and ATP and increase in R-value and lactate concentration at 2 h post mortem. Stunning with argon/ CO2 yielded intermediate rates, while the lowest rate was reported for birds subjected to water bath-electrocution and modified atmosphere stunning with CO2/O2/N2. The authors reported differences for haemorrhage scores, water holding capacity (up to 8 h post mortem), and meat colour (L*, a*, b* values) with respect to different stunning systems. Gas stunning (Inert and CO2) and captive needle stunning resulted in fillets with the lowest haemorrhage scores (1.8), while water bath stunned birds had the highest scores (3.6). Nevertheless, the authors utilised restraining funnels (bleeding cones) in head-only and captive-needle- stunned broilers, while the gas-stunned carcasses were not restrained and the water-bath stunned birds were in shackles. L* value (lightness) for breast meat was similar for fillets from gas stunned birds (60.5), captive needle stunning (59.7), and electrical stunning (58.7). Electrical stunning in water bath exhibited breast meat with similar a* values (redness) (4.5), when compared to captive needle stunning (3.3), and stunning by gas (3.5 in argon/ CO2, 3.2 in CO2/O2/N2). Considering yellowness, b* values were 11.7, 11.3, 11.1, and 10.9 respectively for gas stunning (CO2/O2/N2), captive needle stunning, electrical stunning and argon stunning. In addition, no differences were observed in tenderness and water holding capacity for breast meat after 24 h post mortem among the stunning systems.
Poole and Fletcher (Reference POOLE and FLETCHER1998) utilised 70:30 argon/CO2 in a modified atmosphere stunning-killing system and reported that this system produced comparable effects on meat quality and rigor development, with respect to low voltage electrical stunning, while the benefit of accelerated development could be minimal when compared to high current electrical stunning. Modified atmosphere inert gas stunning could result in broken wing bones caused by severe convulsions during stunning. In addition, availability and expense of the inert gases make it difficult for processors to adopt this technology. However, researchers (Raj, Reference RAJ1998; McKeegan et al., Reference MCKEEGAN, ABEYESINGHE, MCLEMAN, LOWE, DEMMERS, WHITE, KRANEN, VAN BEMMEL, LANKHAAR and WATHES2007; Coenen et al., Reference COENEN, LANKHAAR, LOWE and MCKEEGAN2009) concluded that modified atmosphere stunning with CO2 or inert gases could improve broiler welfare by minimising handling of live birds when compared to electrical stunning (EU).
Low Atmospheric Pressure Stunning (LAPS)
Unlike other methods of modified atmosphere stunning, LAPS does not displace oxygen with another gas or use CO2 to produce insensibility. LAPS or atmospheric depressurisation reduces atmospheric partial pressure of oxygen by evacuating air from an air tight chamber. Broilers are placed in an air tight decompression chamber and pressures of 0.20 to 0.29 atmospheres have previously been utilised to stun the broilers. Though minimal research has been performed on low atmospheric stunning, Purswell et al. (Reference PURSWELL, THAXTON and BRANTON2007) reported that LAPS appeared to be an effective method for humane stunning and exsanguination of chickens.
Low atmospheric pressure stunning has been in the development and implementation stages in commercial broiler abattoirs since 2005. This technology controls the atmosphere through anoxia by using a vacuum pump to reduce oxygen tension in the atmosphere. Italy allows the use of a vacuum chamber for harvest of farmed game species (European Commission, Reference EUROPEAN COMMISSION2003). In the U.S., decompression as a method of euthanasia has been ruled unacceptable by the American Veterinary Medical Association for multiple reasons, such as improper equipment design and operation as agents of pain (AVMA, 2007). The question of when chickens lose consciousness during the process of reducing atmospheric pressure was addressed by Guyton and Hall (Reference GUYTON. A.C. and HALL2010) in the Textbook of Medical Physiology. Guyton and Hall (Reference GUYTON. A.C. and HALL2010) explain that most tissues of the body can go without oxygen for several minutes and some for as long as 30 minutes. During which the cells obtain energy through anaerobic metabolism. The brain is minimally capable of anaerobic metabolism since neurons have only a minimal reserve of glycogen. The metabolic rate of neurons is much higher than most other tissues, thus glucose is continuously being metabolised and storage simply does not occur. Additionally, storage of oxygen in neurons is also very minimal. Therefore, most neuronal activity depends on second-to-second delivery of glucose and oxygen from the blood. Thus, a sudden cessation of blood flow to the brain or a sudden drastic decrease in oxygen in the blood will result in unconsciousness in five to ten seconds (Guyton and Hall, Reference GUYTON. A.C. and HALL2010).
Purswell et al. (Reference PURSWELL, THAXTON and BRANTON2007) reported that blood oxygen concentration decreased from the normal value of 80 mmHg to 23 mmHg, when measured immediately after the birds were removed from the LAPS chamber. This represents a drastic reduction in blood oxygen concentration of approximately 85%. These results support the determination that broilers exhibited a 90% reduction in electrical activity of the brain (determined by direct electroencephalography) within 32 seconds in an atmosphere of 20 Kpa. Previous research showed that loss of consciousness of broilers, as indicated by at least 90% reduction in electrical brain activity, occurred when blood oxygen levels were drastically reduced by exposure to atmospheres of rare gases (Raj et al., Reference RAJ, WOTTON, MCKINSTRY, HILLENBRAND and PIERTERSE1998) which was also supported by Dell et al. (Reference DELL, HUGELIN and BONVALLET1961) and Ernsting (Reference ERNSTING1965).
The American Veterinary Medical Association (AVMA) lists four primary objections to adopting decompression for euthanasia, which include ‘the use of very rapid systems which resulted in pain and distress due to expansion of gas trapped in body cavities; tolerance of hypoxia by immature animals that require longer periods of decompression for respiration to cease; various aesthetically unpleasant reactions by the animals such as bleeding, vomiting, convulsions, and defecation; and finally the potential for accidental recompression’ (AVMA, 2007). Purswell et al. (Reference PURSWELL, THAXTON and BRANTON2007) demonstrated that all these factors could be eliminated by a controlled decompression using a single bird chamber, and that Low Atmospheric Pressure could be a humane method of slaughter and potentially useful for commercial harvest. Purswell et al. (Reference PURSWELL, THAXTON and BRANTON2007) reported that the speed of pressure reduction is critical to reduce discomfort reactions from the birds and that this could be achieved through precision in the controls of the equipment. This finding was in agreement with previous research that used vacuum as a means of euthanasia of mammals (Smith, Reference SMITH1965).
Since limited data on carcass characteristics and meat quality could be obtained from a single bird unit, Thaxton et al. (Reference THAXTON, CHRISTENSEN, SCHILLING, R.J. and THAXTON2010) utilised a research model (TechnoCatch LLC, Kosciusko, MS) that held one commercial cage unit and later a two cage system with automatic controls. After test runs were completed at both a University and commercial processing plant setting, the authors reported that the research prototype provided satisfactory results on poultry welfare. LAPS-stunned birds demonstrated significantly lower blood corticosterone levels (755 pg/ml) when compared to electrically stunned birds (1642 pg/ml), thus indicating lower stressfulness in broilers that were stunned using the LAPS system, likely through minimised handling of the live birds in comparison to shackling with electrical stunning (Kannan and Mench, Reference KANNAN and MENCH1996). The authors suggested that decreased corticosterone levels could minimise meat quality defects under stressful conditions, such as elevated temperature in the summer. On the other hand, LAPS-stunned birds demonstrated 3.2% greater wing damage than electrically stunned birds. The authors also verified the absence of recovery in birds subjected to low atmosphere pressure stunning and utilising behavioural evaluation (absence of bill-breathing and mandibulation), blood analysis and histopathological examination (absence of haemorrhagic lesions in tissues), they concluded that LAPS is a humane system of stunning with potential application in the poultry industry.
In another investigation, Battula et al. (Reference BATTULA, SCHILLING, THAXTON, BEHRENDS, WILLIAMS and SCHMIDT2008) compared the effect of LAPS and electrical stunning (US) on broiler breast meat quality and consumer acceptability. The birds were stunned by exposing them to a low atmospheric pressure (proprietary information with patent pending) an airtight decompression chamber. Meat quality parameters including colour, pH, cook loss, and shear force values were measured on breasts at different deboning times. The authors reported similar L* values (56.1) in breast meat from LAPS birds deboned after 4 h post mortem, compared to those from electrically stunned (US) birds (L* value = 57.3). The a* value (redness) was 1.6 and 1.3 in LAPS and electrically stunned (US) carcasses respectively, while the b* value (yellowness) was 1.8 and 2.1. No differences were observed in shear force (19.9N - 20.6N), pH 24 h post mortem (5.99 – 5.95), and consumer acceptability among breast meat from electrically stunned (US) or LAPS birds and the authors concluded that both stunning methods yield high-quality breast meat with minimal product differences. Even though 24 h pH was similar between breast meat from ES and LAPS stunned birds, the rate of rigor mortis was more rapid in LAPS stunned broilers when compared to ES stunned broilers (Battula et al., Reference BATTULA, SCHILLING, THAXTON, BEHRENDS, WILLIAMS and SCHMIDT2008, Radhakrishnan, et al., 2010). Radhakrishnan et al. (Reference RADHAKRISHNAN, SCHILLING, THAXTON and CHRISTENSEN2010) reported that even though final product pH was similar between breast meat from ES and LAPS stunned broilers, the pH at 15 minutes post mortem was between 6.1 and 6.2 for breast meat from LAPS stunned broilers and approximately 6.5 for ES stunned broilers. In addition, these researchers reported that the pH from LAPS stunned broilers was approximately 6.0 by 30 min post mortem, but the pH did not reach 6.0 until 4 h post mortem for ES stunned broilers. However, pH of breast meat from both ES and LAPS stunned broilers was approximately 5.8 at 24 h post mortem (Radhakrishnan et al., Reference RADHAKRISHNAN, SCHILLING, THAXTON and CHRISTENSEN2010). These differences in pH early post mortem could either be due to a death struggle during LAPS and/or a different pattern of post mortem muscle metabolism since blood corticosterone levels are low in the LAPS stunned broilers when compared to ES stunned broilers. More research is necessary to make conclusive remarks about whether pH differences are due to a death struggle and/or rigor mortis. With respect to deboning time, the authors recommended an aging period of 4 h, regardless of the stunning method, as this contributes to meat tenderness. On the other hand, poultry processing plants with electrical stunning usually age broilers for 4 to 7 h to ensure that the product is tender (Lyon and Lyon, Reference LYON and LYON1990; Schilling et al., Reference SCHILLING, SCHILLING, J.R., MARRIOTT, DUNCAN and WANG2003) and to meet customer specifications.
Conclusions
The goal of stunning is to render birds/animals insensible to pain rapidly, thereby ensuring humane slaughter and improved safety of the personnel. Each system varies in its mode of operation and offers distinct merits and limitations. The selection of a stunning system depends on factors such as animal welfare, cost and ease of operation, effect on meat quality, and safety of operators. Animal welfare should be considered while designing and implementing poultry stunning systems. Electrical, controlled atmosphere, and low atmosphere pressure stunning all produce high quality broiler meat, but controlled atmosphere and low atmosphere pressure stunning also potentially reduce stressfulness by enabling shackling of post-stunned broilers. Although electrical, controlled atmosphere and low atmosphere stunning are all acceptable methods for slaughter when conducted correctly, low atmosphere pressure stunning is currently utilised in the broiler industry and may provide benefits with respect to animal welfare due to lower blood corticosterone levels.
