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. 2017 Dec 21;15(12):e05056. doi: 10.2903/j.efsa.2017.5056

Table 5.

Set of behavioural welfare indicators as provided by the applicant. The first column lists the behavioural welfare indicators selected and recorded by the applicant. The second column reports the definition and interpretation of the indicators provided by the applicant. The third column reports EFSA's comments. The last column associates each welfare indicator with the relevant welfare outcome

Applicant's definition and interpretation EFSA's comments Welfare outcomesa
Behavioural indicators
Ataxia Reflects the start of the process of loss of consciousness. Welfare impact of ataxia during LAPS is low, as its duration is relatively short and the birds may be considered not to be fully conscious at this time, however there are likely to be sensations of disorientation during ataxia which may be unpleasant

Defined as an ‘inability to coordinate muscle activity during voluntary (i.e. conscious) movement; most often results from disorders of the cerebellum or the posterior columns of the spinal cord; may involve the limbs, head, or trunk’b

In agreement with applicant definition

Distress and/or Suffering
Clonic/Tonic convulsions Never before LOP. Minimal relevance to welfare

Clonic convulsion is defined as a convulsion in which the contractions are intermittent, the muscles alternately contracting and relaxingc

Tonic convulsion is defined as convulsion with sustained muscle contractiond

Not relevant for welfare as occurring only after LOP

Loss of Consciousness and Sensitivity
Wing flapping Included in clonic convulsions
Deep inhalation

Deep non‐rhythmic inspiration with bill open, may be accompanied by extension of the neck

Deep inhalation has also been termed ‘gasping’ and relates to the birds taking (usually single) deep breaths, often with neck extension. We consider this behaviour to reflect dyspnoea and probably air hunger, and thus reduced welfare during stunning

Deep inhalation has been particularly associated with hyperventilation during CO2 stunning, but it is also seen with inert gases (e.g. McKeegan et al., 2007) and after electrical stunning (Verhoeven et al., 2015). We note that during LAPS, as in CO2 stunning, this behaviour continues after loss of posture indicating that consciousness is not required for its performance (Verhoeven et al., 2014). There is evidence that some dyspnoea occurs in all control atmosphere stunning (CAS) mixtures that have been investigated, including inert gases, however behavioural responses reflecting these have been variously described as ‘gasping’, ‘deep breathing’, ‘respiratory disruption’ (e.g. Gerritzen et al., 2004; Abeyesinghe et al., 2007; McKeegan et al., 2007) making direct comparison with our two behavioural categories more difficult. However, the numbers of bouts of deep inhalation seen during LAPS are in the range of previously reported equivalent values for CAS. In general, we consider that open bill breathing and deep inhalation relate to dyspnoea and associated reduced welfare during hypoxia, as opposed to being responses to reduced atmospheric pressure

In agreement

In agreement

The evidences provided are misleading because McKeegan et al. report deep inhalation to occur mainly in birds that were mostly exposed to CO2 (in agreement with Gerritzen et al., 2004) and more importantly Gerritzen et al. did not investigate effect of hypoxia to make direct comparison with LAPS

EFSA's interpretation is that: (i) the cause of respiratory distress during LAPS is likely to be air hunger; (ii) the cause of respiratory distress during CAS is hypercapnia or hypercapnic hypoxia; (iii) this behaviour has not been described when birds were exposed to hypoxia only. For example, McKeegan et al., (2007) reported 1 or 2 breathing patterns similar to this when chickens were exposed to hypoxia when compared with 9–16 in chickens exposed to CO2 mixtures

Deep inhalation after the electrical water‐bath stunning is the evidence of poor stunning or recovery of consciousness, unless ‘deep breathing’ here refers to agonic gasping

Distress and/or Suffering if it occurs before loss of consciousness
Head shaking Less preferred/novel environment. Awareness by the birds of atmospheric pressure reduction and/or reducing oxygen concentration while conscious. May also relate to auditory stimulation from increased noise levels in the chamber. Reduced welfare during LAPS. Seen in sham LAPS treatments

In addition: possible reaction of the birds in response to pressure reduction recorded by the cochlea and to lack of humidity (dryness of the nasal mucosae)

Based on the video footage: birds started headshaking just after the fogging cleared in the chamber (no more humidity)

Distress and/or Suffering
Jump/Jumping Jumping was generally seen after the onset of ataxia and did not seem to be an entirely voluntary behaviour. The explosive upward movement we termed ‘jump’ appeared to be related to attempts to regain posture during ataxia and may have be caused by involuntary muscle contractions (myoclonic jerks) as loss of muscle control progressed

Because jumping occurs mainly prior to loss of consciousness, it has implications on animal welfare

The wording is ambiguous or imprecise. A movement cannot be partly voluntary: either it is voluntary or it is not. The difficulty might be in differentiating between voluntary and involuntary. An attempt to regain posture cannot be caused by involuntary muscle contractions

Based on the above and considering that during ataxia the animals are conscious, ‘jump’ is a behaviour of welfare concern

Distress and/or Suffering
Loss of posture During LAPS, we considered loss of posture to be the earliest indicator of potential loss of consciousness In agreement Loss of Consciousness and Sensitivity
Lying Lying was adopted after loss of posture, and was never seen prior to this. It reflects the inability of the animal to control its posture and ventral, lateral and dorsal lying was observed In agreement Loss of Consciousness and Sensitivity
Motionless Motionless refers to a limp carcass with the bird being completely still including the cessation of visible breathing movements; it reflects complete and irreversible loss of muscle tone. We considered motionless to confirm the non‐recovery state induced by LAPS

In agreement

Broadly accepted as indicator of death

Death
Open bill breathing Rhythmic breathing with an open bill (distinguished from panting by the fact that the tongue did not protrude) was routinely seen during LAPS and is a response to hypoxia Open bill breathing has never been reported as a response to hypoxia (no reference provided), but rather to hypercapnia (Gerritzen et al., 2000) Distress and/or Suffering if it occurs before loss of consciousness
a

Green = no welfare concern; orange = some degree of welfare concern; red = serious welfare concern (not present in the table).

b

Farlex Partner Medical Dictionary © Farlex 2012 (<a href=“http://medical-dictionary.thefreedictionary.com/ataxia”>ataxia</a>)

c

Farlex Partner Medical Dictionary © Farlex 2012 (<a href=“http://medical-dictionary.thefreedictionary.com/clonic+convulsion”>clonic convulsion</a>)

d

Farlex Partner Medical Dictionary © Farlex 2012 (<a href=“http://medical-dictionary.thefreedictionary.com/tonic+convulsion”>tonic convulsion</a>)