Humane-Slaughter-Guidelines
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of behavioral assessment and aversion testing and reviewed<br />
in the context of euthanasia. 1 It is important to<br />
understand that aversion is a measure of preference,<br />
and while aversion does not necessarily imply that an<br />
experience is painful, forcing animals into aversive situations<br />
creates distress. The conditions of exposure used<br />
for aversion studies, however, may differ from those<br />
used for stunning or slaughter. One of the characteristics<br />
of anesthesia in humans is the feeling that one<br />
is having an out-of-body experience, suggesting a disconnection<br />
between one’s sense of self and one’s awareness<br />
of time and space. 10 Although we cannot know for<br />
certain the subjective experiences of animals, one can<br />
speculate similar feelings of disorientation may contribute<br />
to the observed signs of distress with inhaled methods.<br />
In addition, agents identified as being less aversive<br />
(eg, Ar or N 2<br />
gas mixtures) can still produce overt signs<br />
of behavioral distress (eg, open-mouth breathing) for<br />
extended periods of time prior to loss of consciousness<br />
under certain conditions of administration (eg, gradual<br />
displacement). 11<br />
Unconsciousness, defined as loss of individual<br />
awareness, occurs when the brain’s ability to integrate<br />
information is blocked or disrupted. In animals, loss<br />
of consciousness is functionally defined by LORR, also<br />
called LOP. 8,12,13 This definition is quite useful because<br />
it is an easily observable, integrated whole-animal response.<br />
Although any physical movement occurring<br />
during anesthesia, euthanasia, slaughter, or depopulation<br />
is often interpreted as evidence of consciousness,<br />
cross-species data from the anesthesia literature suggest<br />
that both memory formation and awareness are<br />
abolished early in the overall process relative to loss of<br />
reflex muscle activity. 8 Thus, vocalization and nonpurposeful<br />
movement observed after LORR or LOP with<br />
properly applied CAS methods are not necessarily signs<br />
of conscious perception by the animal. While generalized<br />
seizures may be observed following effective CAS<br />
methods, these generally follow loss of consciousness;<br />
indeed, anesthesia, coma, and generalized seizures all<br />
represent a loss of consciousness where both arousal<br />
and awareness in humans are low or absent. 14 Loss of<br />
consciousness should always precede loss of muscle<br />
movement.<br />
Although measurements of brain electrical function<br />
have been used to quantify the unconscious state,<br />
EEG data cannot provide definitive answers as to onset<br />
of unconsciousness even when state-of-the-art equipment<br />
is used. At some level between behavioral unresponsiveness<br />
and the induction of a flat EEG (indicating<br />
the cessation of the brain’s electric activity and<br />
brain death), consciousness vanishes. However, current<br />
EEG-based brain function monitors are limited in their<br />
ability to directly indicate unconsciousness, especially<br />
around the transition point. 15,16 Also, it is not always<br />
clear which EEG patterns are indicators of activation by<br />
stress or pain. 17 Reduction in alpha-to-delta brain wave<br />
ratios coincides with LOP in chickens, 18,19 reinforcing<br />
the usefulness of LOP or LORR as an easily observable<br />
proxy for loss of animal consciousness.<br />
Physical methods that destroy or render nonfunctional<br />
the brain regions responsible for cortical integration<br />
(eg, gunshot, captive bolt, cerebral induction<br />
of epileptiform activity in the brain [eg, electric stunning],<br />
blunt force cranial trauma, maceration) produce<br />
instantaneous unconsciousness. When physical methods<br />
directly destroy the brain, signs of unconsciousness<br />
include immediate collapse (LORR or LOP) and<br />
a several-second period of tetanic spasm, followed by<br />
slow hind limb movements of increasing frequency. 20,21<br />
In cattle, however, there is species variability in this response.<br />
The corneal reflex will also be absent. 22 Signs<br />
of effective electric stunning that induces both epileptiform<br />
activity in the brain and cardiac arrest are LORR,<br />
loss of menace reflex and tracking of moving objects,<br />
extension of the limbs, opisthotonos, downward rotation<br />
of the eyeballs, and tonic spasm changing to clonic<br />
spasm, with eventual muscle flaccidity. 21,23 Physical<br />
methods are inexpensive, humane, and minimize pain<br />
if performed properly, and leave no drug residues in<br />
the carcass. Furthermore, animals presumably experience<br />
less fear and anxiety with methods that require<br />
little preparatory handling. However, physical methods<br />
usually require a more direct association of the operator<br />
with the animals, which can be offensive to, and<br />
upsetting for, the operator. Physical methods must be<br />
skillfully executed to ensure a quick and humane death<br />
because failure to do so can cause significant stress, distress,<br />
and pain. Physical disruption methods are usually<br />
followed by exsanguination to ensure death and<br />
improve meat quality. Exsanguination is also a method<br />
of inducing hypoxia, albeit indirectly.<br />
Controlled atmosphere stunning methods also<br />
depress the cerebral cortical neural system, producing<br />
loss of consciousness accompanied by LORR or LOP.<br />
Purposeful escape behaviors should not be observed<br />
during the transition to unconsciousness. Depending<br />
on the speed of onset of unconsciousness, signs associated<br />
with release of conscious inhibition of motor<br />
activity, (such as vocalization or uncoordinated muscle<br />
contraction) may be observed at LORR or LOP. Signs<br />
of an effective stun when the animal is in deep levels<br />
of anesthesia include LORR or LOP, loss of eye blink<br />
(menace reflex) and corneal reflex, and muscle flaccidity.<br />
24 As with physical disruption methods, CAS methods<br />
are usually followed by exsanguination to ensure<br />
death and improve meat quality.<br />
Decapitation and cervical dislocation are physical<br />
methods of slaughter that require separate comment.<br />
The interpretation of brain electric activity, which can<br />
persist for up to 30 seconds following these methods,<br />
25–27 has been controversial. 28 As indicated previously,<br />
EEG cannot provide definitive answers as to the<br />
exact onset of unconsciousness. Other studies 26,27,29–31<br />
indicate such activity does not imply the ability to perceive<br />
pain and conclude that loss of consciousness develops<br />
rapidly.<br />
In summary, the cerebral cortex or equivalent<br />
structures and associated subcortical structures must<br />
be functional for pain to be perceived. If the cerebral<br />
cortex is nonfunctional because of physical disruption,<br />
hypoxia, generalized epileptic seizure, or neuronal depression,<br />
pain cannot be experienced. Motor activities<br />
occurring following LORR or LOP, although potentially<br />
distressing to observers, are not perceived by an unconscious<br />
animal as pain or distress. Reflexive kicking in<br />
8 AVMA <strong>Guidelines</strong> for the <strong>Humane</strong> <strong>Slaughter</strong> of Animals: 2016 Edition