Master Thesis
Environmental Biology
Utrecht University
2013
Euthanasia methods of Rabbits vary
between different contexts: A Review of
Welfare and Ethical considerations
A rabbit is still a rabbit, being
it a pest or a pet
(Modified from Webster, 1994)
Olga Szczodry
9/15/2013
Literature Thesis for the Master Environmental Biology,
track Behavioural Ecology, Utrecht University
Author: Olga Szczodry, BSc.
Student number: 3873048
Supervisor and first examiner: Dr. Saskia Arndt, Department of Animals in
Science and Society, Faculty of Veterinary Medicine, Utrecht University.
Second Examiner: Dr. Franck Meijboom, Ethics Institute, Utrecht University &
Department of Animals in Science and Society, Faculty of Veterinary Medicine,
Utrecht University
September 2013
Abstract
Being pets, animal models, meat and fur producers, rabbits (Oryctolagus cuniculus) are used by
humans in a variety of contexts. Interestingly, the euthanasia methods employed for rabbits appear to
vary between different contexts.
Hence, it appears that a rabbit is not a rabbit, being it a pest or a pet. The latter fact deserves to be
questioned: is the variation of euthanasia methods used between different contexts justified in terms of
welfare? This issue requires, on one hand, a reflection on the biological aspects of welfare, and on the
other hand, an ethical reflection on the moral validity of such a difference.
The present review aims to constitute a first step in the debate by tackling biological aspects of welfare
implicated in each euthanasia method put in its context, and by determining whether such variation in
methods is justified in terms of welfare. As welfare and ethics are intermingled concepts, ethical
implications of different methods and the moral validity of the variation in methods between contexts
is also developed.
After an introduction to the issue, a presentation of the contexts of rabbit use and a brief overview of
the species biology, the present paper examines thoroughly each method, explores its welfare
implications and specifies the context in which it is used. An ethical reflection is then developed
which details the relation between animal welfare, ethics and euthanasia; and explains the key ethical
views on animal use. Finally, the present paper discusses the issue per context and across contexts, and
concludes whether the use of different methods in different contexts is justified from a biological
perspective of welfare, on one hand, and an ethical perspective on the other hand.
The present review comes to the conclusion that from a biological perspective of animal welfare, the
variation of euthanasia methods across contexts is not justified and that from an ethical perspective,
there is a need for further reflection.
Contents
Abstract ..................................................................................................................................................................................... 2
Chapter I: Introduction ........................................................................................................................................................... 5
Chapter II: The rabbit: biology and contexts ........................................................................................................................ 9
I.
CONTEXTS OF RABBIT USE ............................................................................................................................................. 9
1.
Pet rabbit ................................................................................................................................................................ 9
2.
Lab rabbit ............................................................................................................................................................. 10
3.
Meat rabbit ........................................................................................................................................................... 11
4.
Fur rabbit.............................................................................................................................................................. 12
5.
Pest rabbit ............................................................................................................................................................. 13
II.
SIGNS OF PAIN AND DISTRESS IN THE RABBIT ................................................................................................................ 14
Chapter III: Analysis of Euthanasia methods ...................................................................................................................... 15
I.
GENERAL CONSIDERATIONS ......................................................................................................................................... 15
1.
Peri-euthanasia factors ......................................................................................................................................... 16
2.
Recognition and confirmation of death ................................................................................................................. 19
II.
STUNNING ................................................................................................................................................................... 19
III. PHARMACOLOGICAL-CHEMICAL METHOD .................................................................................................................... 21
1.
Pentobarbital Overdose ........................................................................................................................................ 22
O. Szczodry
2013
2.
T61® overdose ...................................................................................................................................................... 24
3.
Volatile inhalant anaesthetics ............................................................................................................................... 25
4.
CO2 ....................................................................................................................................................................... 26
5.
CO ......................................................................................................................................................................... 28
IV. PHYSICAL METHODS .................................................................................................................................................... 29
1.
Captive bolt ........................................................................................................................................................... 30
2.
Electrocution ......................................................................................................................................................... 31
3.
Cervical dislocation .............................................................................................................................................. 31
4.
Decapitation.......................................................................................................................................................... 32
5.
Microwave ............................................................................................................................................................ 33
6.
Kill traps ............................................................................................................................................................... 34
V. METHODS ACCEPTABLE FOR UNCONSCIOUS RABBITS ONLY .......................................................................................... 34
1.
Exsanguination ..................................................................................................................................................... 34
2.
Nitrogen/Argon ..................................................................................................................................................... 34
3.
Potassium chloride (KCl)...................................................................................................................................... 35
4.
Air embolism ......................................................................................................................................................... 35
5.
Chloral hydrate ..................................................................................................................................................... 36
VI. METHODS NOT ACCEPTED FOR RABBITS ....................................................................................................................... 36
Chapter IV: Normative reflection ......................................................................................................................................... 37
I.
ANIMAL WELFARE AND ETHICS................................................................................................................................... 37
II.
PLURALITY IN ETHICAL EVALUATION OF ANIMALS ....................................................................................................... 40
III. DIFFERENT ETHICAL VIEWS ON ANIMAL USE ................................................................................................................. 41
IV. EUTHANASIA AND WELFARE ....................................................................................................................................... 44
V. SUMMARY ................................................................................................................................................................... 45
Chapter V: Discussion............................................................................................................................................................ 47
I.
DISCUSSION PER CONTEXTS OF ANIMAL USE ................................................................................................................. 48
1.
The Rabbit as Meat animal ................................................................................................................................... 48
2.
The Rabbit as Fur animal ..................................................................................................................................... 49
3.
The Rabbit as Lab animal ..................................................................................................................................... 50
4.
The Rabbit as Pet animal ...................................................................................................................................... 52
5.
The Rabbit as wildlife – free-range and pest......................................................................................................... 53
II.
DISCUSSION ACROSS CONTEXTS OF ANIMAL USE .......................................................................................................... 55
III. IMPLICATIONS BEYOND WELFARE ................................................................................................................................ 57
IV. CONCLUSION ............................................................................................................................................................... 58
1.
The challenge of conclusion .................................................................................................................................. 59
2.
Conclusion on Biological basis ............................................................................................................................. 59
3.
Conclusion on Ethical basis .................................................................................................................................. 60
4.
Final statements .................................................................................................................................................... 61
References ............................................................................................................................................................................... 63
Photo Cover: Dutch Ministery of Economic Affairs, Agriculture and Innovation database, 2011.
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Chapter I
Introduction
Humanity has always relied on animals. And it still does. Whether used for food production, clothes,
research or companionship, animals play a crucial role for our species. Rabbits, such as some other
species, are used by humans in very different settings. This context difference has substantial
consequence on their value to humans and thus, ultimately, on their welfare.
Rabbits, with hares, correspond to the Leporidea family in the Lagomorpha order [1], [2]. There are
over 11 genera counting over 50 species [1]. Nowadays, the domestic rabbit, descended from the
European rabbit (Oryctolagus cuniculus), [3] and cottontail rabbit (Sylvilagus sp.) are the most
common [2], [3].
In northern Europe, such as the Netherlands, rabbits are very popular as pets [4]. They are appreciated
for their playfulness, friendliness, and sociability [5]. They are the third most popular mammalian pet
after dogs and cats in the UK, with an estimated number of 2 million in 2010 [6]. In the Netherlands,
their number in 2009 was estimated at 980,000 [5].
These species constitute also an appreciated animal model in scientific research. Their intermediate
body size, ability to breed easily, and their docility are some appreciated features in research [7].
Approximately 314,000 rabbits have been used in research in the European Union (EU) in 2005,
which constitutes 2.6% of all animals used in research in the EU [8].
In the southern part of Europe, such as Italy or Hungary, rabbits are very valued for their meat [4].
Indeed, it is highly digestible, low-caloric and tasty [9]. In Italy, an estimated number of 7.19 million
rabbits are raised in 217 449 farms and slaughtered for meat consumption [10]. This number does not
take into account the substantial number of rabbits raised and slaughtered at home.
Rabbits are also raised for their fur. Whereas some pelts are by-products from meat industry, other
rabbits are raised exclusively for their pelts or hair, namely Rex and Angora rabbits respectively.
Furthermore, the rabbit can be seen as an invasive pest. The common rabbit, Oryctolagus (O.)
Cuniculus, is one of the most ubiquitous existing species. This fact results from introductions to nonendemic areas without natural competitors and predators. In the case of complete lack of population
regulators, the impressive reproductive rate of rabbits accounts for its qualification as invasive pest,
which has harmful consequences on ecology and economy [3].The Australian example is the most
known with rabbits constituting a veritable plague [11]. Surprisingly, in their region of origin, i.e.
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Iberian Peninsula, O. Cuniculus is considered as endangered species. Finally, rabbits are also
considered as game species [3].
The human-rabbit relationship, across contexts, is regularly ended by the death of the animal. Being it
called euthanasia, culling or slaughtering, it appears that the method used to achieve that final aim, i.e.,
death of the animal, differs between contexts [4], [8], [12], [13]. Intuitively, the use of different
methods between contexts for the same species appears to be morally wrong. Beside the fact that
ending life of another being raises per se ethical questioning, a more striking normative issue is
whether it is morally justifiable to use different methods to put down a specific animal species for the
unique reason that the context, and thus the human-animal relationship, differs.
An extensive amount of publications focuses on the biology and welfare of the rabbit without tackling
the process of euthanasia. However, rabbit euthanasia occurs very frequently and constitutes a major
welfare issue [1], [5], [6], [14], [15]. The word “Euthanasia” comes from the Greek “eu” which means
“good” and “thanatos”, meaning “death” [16]. Thus, the etymological meaning of euthanasia is “good
death”. Euthanasia is defined as a “process of inducing death with minimal or no pain or distress in
the animal involved” [17]. The notion of welfare plays therefore a major role in euthanasia and all
methods should strive for the highest welfare standards and social conscience [18]. The euthanasia
method chosen should cause as less pain and suffering as possible and should therefore impair the
welfare of animals to a minimum extent. As stated by the Australian code of Practice for the care and
use of animals for scientific purposes, chosen methods shall kill the animal very quickly or render it
unconscious and thus insensible very rapidly, before the onset of death. All pre-euthanasia stressinducing factors, such as restraint or transport, should be minimized as much as possible and the
technical skills of the operators performing euthanasia should be optimal in order to kill the animal
“humanely” [19].
The fact that across context, different methods are currently used to euthanize rabbits is questionable
in terms of welfare as it would be expected that one method constitutes the “least bad” option. Thus,
the question whether the variation of methods used between contexts is justified in terms of welfare
arises.
From the facts stated above, it can be concluded that the issue of different euthanasia methods between
contexts for the same species, i.e. rabbit, requires, on one hand, a reflection on the biological aspects
of welfare, and on the other hand, an ethical reflection on the moral validity of such a difference.
The present review aims to constitute a first step in the debate by tackling biological aspects of welfare
implicated in each euthanasia method put in its context, and by determining whether such variation in
methods is justified in terms of welfare. As welfare and ethics are intermingled concepts, ethical
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implications of different methods used and the moral validity of the variation in methods between
contexts is also developed.
After an introduction to the issue, a presentation of the contexts of rabbit use and a brief overview of
the species biology, the present paper examines thoroughly each method, explores its welfare
implications and specifies the context in which it is used. An ethical reflection is then developed
which details the relation between animal welfare, ethics and euthanasia; and explains the key ethical
views on animal use. Finally, the present paper discusses the issue per context and across contexts, and
concludes whether the use of different methods in different context is justified, in terms of welfare,
from a biological perspective on one hand, and an ethical perspective on the other hand. The
conclusion defines whether there is a need for further normative reflection.
Box 1: Definition of key concepts
A. Euthanasia
Euthanasia generates a great concern among animal owners, people working with animals or for
animal welfare [12]. As stated earlier, euthanasia means “good death”; it is the act of inducing ‘humane’ death,
gently and painlessly [18], [20].
To achieve minimal pain and distress, many criteria for euthanasia have been defined. One category
focuses on animal welfare: euthanasia methods should avoid stress prior to the process, avoid excitement during
the process, require minimal restraint, induce painless and rapid loss of consciousness followed by irreversible
and reliable Central Nervous System depression, cardiac and respiratory arrest resulting ultimately in death
[17], [18], [21], [22]. The second category focuses on the welfare of the operator of euthanasia: the method
should be simple to administer, safe for the operator and aesthetically acceptable [21]. For laboratory animals or
those earmarked for the food chain, histopathological and biochemical consequences of the euthanasia method
need to be taken into account [17], [22], [23]. Financial costs play also a role in the method chosen [17]
especially in contexts, such as farms, where economic efficiency is sought.
Death should always be confirmed when euthanasia is practised [17] because carcass disposal
procedures, such as freezer placement or skinning and chilling, result in severe degree of suffering if the animal
is still alive [23], [24].
B. Animal Welfare
The main issue with Animal Welfare is that it is difficult to define. Indeed, there is by now, no
consensus about a definition of Animal Welfare. The unique widely-accepted consideration is that a welfare
status lies in the continuum between a negative and a positive affective state. The concept varies with culture,
context, individuals, subjective feelings, time, etc. In addition, different ethical or scientific approaches differ
in their notion of Animal Welfare as well. More importantly, the value of an animal may also depend on the
context. Indeed, a pest animal is regularly valued differently from a pet animal, even though it is the same
species with, thus, identical intrinsic values [25], [26], [27].
A well-known concept of animal welfare is “The Five Freedoms” developed in 1967 and serving as
basis for current guidelines. However, this concept was designed for production animals and its use in different
context is therefore limited. Moreover, the five freedoms concept focuses on the exclusion of negative states,
but this exclusion does not necessarily guarantee a positive welfare state. Besides, the “five freedoms” concept
does not take into account the factor of adaptability to the environment. For instance, being temporarily in a
state of hunger does not impair the welfare status as long as the individual is able to adapt to the situation by
foraging [27].
Thus, over years, and as a response to criticism it faced, the concept has been modified and improved.
A recent adaptation of the five freedoms has been developed by Ohl & Van der Staay (2012) and addresses the
problems mentioned above creating thereby a dynamic concept. The adapted version states: “An animal is in a
positive welfare state when it has the freedom to adequately react to hunger, thirst or incorrect food; thermal
and physical discomfort; injuries or disease; fear and chronic stress; and thus has the freedom to display
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normal behavioural patterns that allow the animal to adapt to the prevailing environmental circumstances that
enable it to reach a state that it perceives as positive”.
From the concept just mentioned that is adopted in the present review, one may state that the welfare
components that are at stake in the context of euthanasia are namely, fear, physical discomfort, injuries, and the
lack of possibility to express behavioural patterns enabling to reach a positive welfare state. The following
analysis will therefore focus on these components.
C. Consciousness
The term consciousness refers to an awake animal or an animal capable of subjective awareness [28].
Kirkwood & Hubrecht (2001) defined consciousness as “the subjective awareness of sensory perceptions,
emotions, and thoughts”. It requires therefore a state of sensibility, i.e. ability to perceive stimuli. Sensibility is
shown by the ability to respond with a species-specific context-relevant behavioural pattern [21], [30].
Following the definition stated above, prerequisite neuronal system are necessary for consciousness
[31] such as the cerebral cortex [32]. Following this line of thoughts, knowledge of neuroanatomy and
physiology across species allow the extension of consciousness to every vertebrate (thus to rabbits as well) and
possibly some invertebrates, such as cephalopods [33].
Unconsciousness in considered as the insensibility to external stimuli [21], [30]. It can thus be
measured by assessing physical or cortical responses, such as electroencephalography (EEG) [21], [34].
D. Distress
Stress is defined as “the effect of physical, physiologic or emotional factors that induce an alteration in
an animal’s homeostasis or adaptive state” [35]. Distress, the negative form of stress, is a general notion
involving different components, such as pain and fear. It includes physiological and psychological states which
result in incapacity to adapt to environmental and internal changes impairing therefore the well-being. Distress
may be assessed trough physiological and behavioural responses to, for instance, noxious stimuli [18], [36],
[37].
Fear and anxiety are two components often confounded because they both increase arousal and
alertness. However, whereas fear is focused on a specific danger and ends when the threat ceases, anxiety is a
“more generalized response to the unknown” and thus lasts longer [38].
Pain has been defined by the international Association for the study of pain (1979) as “An unpleasant
sensory and emotional experience associated with actual or potential tissue damage, or described in terms of
such damage”. The nociceptive mechanisms are nerve impulses provoked by noxious stimuli reaching the
cerebral cortex via ascending neural pathways [18]. Other authors have defined pain as an “aversive sensory
experience that elicits protective motor actions as learned avoidance and modify species-specific behavioural
patterns” [36], [40]. The definitions of pain imply that the is a necessity for conscious awareness of the noxious
stimuli to be in pain, and thus exclude reflex motor responses [21].
Pain, fear and anxiety are interconnected component since “the motivational-affective component of
pain can be modulated by various psychological and environmental stimuli such as anxiety and fear” [41].
Pain is extremely difficult to measure and no consensus exists on an objective method to assess it [42].
Indicators of distress exist, and will be detailed in section Chapter 2, II.
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Chapter II
The rabbit: biology and contexts
Rabbits were first considered rodents. However, because of dentition differences, they now have been
classified in the order of Lagomorpha , family of Leporida [1], [43]. In Europe, the most common
species is the European rabbit (Oryctolagus cuniculus) called also domestic rabbit. In the UnitedStates, cottontail rabbits (Sylvilagus sp.) are more prevalent.
Rabbits are nocturnal animals living in colonies and having a complex social structure [5]. They are
prey species which implies several features such as, being “catecholamine-driven” and thus “stress
easily” [see 44]; possessing an almost 360 degrees field of vision [45]; hiding pain; and showing tonic
immobility known as “ freezing” behaviour when in fear [46]. Despite 2000 years of domestication,
the latter behaviours are still highly conserved is domestic rabbits [43]. Hence, pet rabbits do not
appear to differ much from wild rabbits [47].
Rabbits are very territorial. They have therefore developed good communication means and mark their
territory with scent glands, faeces and urine. Their olfactory sense, hearing and taste are very
developed [46] and they seem capable to recognize individual humans [48]. It is noteworthy that
rabbits have a very light, i.e., 7-8% body weight, and a fragile skeleton [49]. This detail might be of
importance for the choice of euthanasia method.
I.
Contexts of rabbit use
1. Pet rabbit
As mentioned previously, the rabbit constitutes in some countries, the third most popular pet animal
after cats and dogs [4], [5], [6].
Pet rabbits, usually originating from O.cuniculus, are protected by law in several countries. In GreatBritain, the Animal Welfare Act form 2006 defines duties of the owners towards their pets. In the
Netherlands, a new law called the Animals Act (Wet Dieren) came into force the first day of 2013
[50]. It specifies requirements towards the owners and recognises the intrinsic value of animals. At
the European level, the European Convention for the Protection of Pet Animals, defines duties
and conditions in which animals should be kept and killed. Article 11 states: “Only a
veterinarian or another competent person shall kill a pet animal (…). All killing shall be done with the
minimum of physical and mental suffering appropriate to the circumstances. The method chosen,
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except in an emergency, shall either cause immediate loss of consciousness and death, or begin with
the induction of deep general anaesthesia to be followed by a step which will ultimately and certainly
causes death. The person responsible for the killing shall make sure that the animal is dead before the
carcass is disposed of”. The convention also prohibits methods of drowning or suffocation without
induction of deep anaesthesia; use of drugs that cause suffering or electrocution without stunning [51].
Over the last few years, the lifespan of the pet rabbit has been extended from 5-6 to 8-9 years.
Therefore, a new welfare issue arises, namely the palliative care for geriatric rabbits. Some individuals
live comfortably with palliative care until their death and some require human intervention i.e.
euthanasia [52].
Pet rabbits are frequently euthanatized in a caring and respectful manner. It is advised to use
tranquilizers prior to the procedure for some individuals with strong temperaments; it will relax the
animal and give some last quite moments to the owner [12]. According to S. O. Walshaw in the
Manual of rabbit medicine and surgery (2000), the most peaceful method is a two-stage technique with
a sedation or anaesthesia stage where the animal will gradually lose consciousness while receiving
sweets. The second stage is the administration of an euthanasia agent such as sodium pentobarbital or
potassium chloride [12], [52].
2. Lab rabbit
Between 2000 and 2010, 6329 papers containing the keywords “experimental animal model” and
“rabbit” were made available by the Ovid MEDLINE database [3]. In 2002, in Sweden, the rabbit was
the fifth most commonly used mammalian laboratory animal after mice, rats, guinea pigs and pigs. In
2005, 314 600 rabbits were used for scientific research in the EU (see in Lidfors & Edström, 2010).
One can therefore conclude that the rabbit is an appreciated animal model for scientific research.
Currently, the New Zealand white breed of O. cuniculus, is mainly used in scientific research [3] as its
intermediate body size enables an easy application of different techniques. In addition, rabbits are
phylogenetically closer to primates than rodents, which can be beneficial in translational research with
humans being the target species. Moreover, its docility, ability to breed easily in captivity and its short
generation time, explain that the rabbit is appreciated in research [7].
Rabbits are used for in vivo research (e.g. infectious disease research), immunology, vaccine
development, genetics, etc.[3]. To model human diseases, such as arthrosclerosis, hypertrophic
cardiomyopathy or AIDS, transgenic rabbits are created. Transgenic rabbits are also used for
production of pharmaceutical proteins in their milk, blood or urine [7].
Laboratory animals are protected by the European directive 2010/63/EU on the protection of animals
used for scientific purposes [53] . Euthanasia of laboratory animals requires specific consideration
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regarding histological and biochemical consequences of the method used. Indeed, the method may
involve tissue destruction or drug contamination which could interfere with the results [17].
Euthanasia of laboratory rabbits is most commonly done with an overdose of agents such as sodium
pentobarbital which is the only recommended method for this species [30]. Anaesthetic mixtures, such
as halothane or nitrous oxide with other inhalants, or ketamine with premedication (i.e.
acetylpromazine or xylazine) are also commonly used in laboratory rabbit euthanasia but with some
reservations. Captive bolt and exsanguination is sometimes used as well as decapitation with
preceding anaesthesia but this methods are preferred for small specimen (i.e. weighing less than 1kg).
Concussion is only acceptable after anaesthesia [8], [30].
3. Meat rabbit
Whereas rabbits are often considered as pets in northern Europe, they are very appreciated for their
meat in the southern part of Europe. France, Spain, Italy and Portugal produce and consume rabbit
meat on the largest scale within Europe [54]. Rabbit meat is appreciated for its savour, high
digestibility and low amount of calories [9]. Due to its healthy properties, European rabbit meat
processing industry wants to increase its presence in the ready-meal market. This development forces
farms and abattoirs to increase their capacities in rabbit production and slaughtering via automatisation
of the processes. This may put the welfare of animals at stake [23]. While in Italy many rabbits are
home raised and slaughtered, industrial farms exist as well and tend to develop. An estimated number
of 7.19 millions of rabbits are raised and slaughtered each year in intensive production systems in this
country [10]. Rabbit meat is also very popular outside Europe. The world production of rabbit meat
was estimated to 1.5 million tons in 1994, with Hungary and China being the most important
producers and exporters [24]. The New Zealand White breed was originally bred for meat production
before entering the scientific laboratories [55]
European Legislation, i.e. Council directive 93/119/EC, aims to protect farm animals at the time of
slaughter or killing [56], [57]. For the prevention of unnecessary suffering, stunning of animals prior
to slaughter is required to insure unconsciousness and insensibility [54], [58]. In 2006, the European
Food and Safety Authority (EFSA) published an opinion report regarding inter alia killing methods
for production rabbits. This publication recommends the use of captive bolt for killing/stunning for
small numbers of animals, but death must be “confirmed” by another method. The latter method is
also advised for on-farm disease control culling. In commercial slaughter plants, the method of choice
for stunning is electrocution. However, due to lack of data; no recommendation is available regarding
the magnitude and duration of current application. Gaseous stunning is mentioned as a potentially
good alternative but is not recommended yet due to the lack of knowledge regarding welfare
implications during induction phase [54].
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This gap in knowledge is due to the fact that only a very small number of studies have been conducted
on slaughtering methods and their welfare implications in rabbits [4]. Scoring systems to assess the
welfare at slaughter exist. They have been developed by T. Grandin and are successfully used in
abattoirs in United-States and Europe. However, they have been developed for cattle and are thus not
applicable for rabbits [59], [60].
In western commercial abattoirs, the standard procedure of rabbit meat production involves fasting1,
catching, crating, transport, holding at the slaughter plant and ante mortem inspection at a first stage.
This harvesting phase is followed by unloading, stunning, hanging on processing lines and bleeding.
When animals are dead, skinning, evisceration, chilling, packaging and marketing take place in the
order cited [23]. The method used for slaughtering is electrical stunning, followed by hanging by hind
leg and exsanguination. Exsanguination is done by cutting the jugular vein and carotid arteries on left
or both sides of the throat [13], [23]. The loss of the majority of blood produces immediate brain
failure and death [23]. Electrical stunning can produce tonic seizure in the rabbit. Therefore,
exsanguination should be performed only on a well-stunned individual [4], [13].
In the meat production context, a major factor that tends to determine the methods used for
slaughtering, is the meat quality obtained. Legislation requires electrical stunning prior to
slaughtering. However, this welfare disposition conflicts with the marketability of the product. Indeed,
producers ascribe an unpleasant red colour of the carcass to electronarcosis. Purchaser desire bright
colour given by oxymyoglobin which depends on several factors related to stress, such as transport,
restraint, etc. The less the animal is stressed the better its meat will be [61]. The tenderness and
juiciness of the meat is also function of slaughter conditions rigor mortis [24]
4. Fur rabbit
In many countries were meat rabbits are produced and slaughtered in the households, the skin is
marketed but it usually ends up in domestic use because of its poor-quality. At a larger scale, rabbit
skins are also by-product of rabbit meat industry. France appears to be the largest producer of raw
skin. Australia is also a non-negligible producer as rabbits’ skins since they are by-products of their
pest culling campaigns. The best quality fur pelts (less than 50%) go to fur industry for dressing.
Lower quality pelts are used for shorn hair. The market of shorn hair is rather large with 200 Tons
exported from France each year. However, in meat intensive production systems, rabbits are
slaughtered before their coat is complete and stable. Skins are therefore not usable for fur industry and
are usually thrown away or used for fertilization. The inflexible growth cycle of fur and the seasonal
changes it undergoes, make simultaneous meat and fur production unfortunately not realisable, at least
in regions with well-defined seasons, namely temperate regions [24].
1
The shortest time required to empty the digestive track. Concretely, it is the feed withdrawal 8-12h prior to
slaughtering to reduce fecal contamination during evisceration [23].
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Rabbit skins are not only by-products from meat industry. Some breeds are exclusively bred for their
hair or pelt, namely the Angora and Rex Rabbits respectively. The global rabbit pelt production is
estimated to reach 1 billion per year [24].
Angora rabbits produce wool used it the textile industry. European production, which is constantly
growing and was at 300,000 Tons per year in 1997, is mainly located in France, Hungary and Czech
Republic. The hair is collected with scissors, electric or manual shears or by depilation, every 90
to 100 days, when the follicles reach the resting stage and before hair starts falling, which would
cause felting and reduce the hair’s value [24].
Animals raised for fur are also protected by 93/119/EC directive. The Annexe F of the European
directive permits the use several methods for rabbit killing. The following techniques are allowed:
Use of “mechanically-operated instruments which penetrate the brain” which have to be correctly
positioned. The method must be followed by a “death confirmation method”, namely
exsanguination; injection of an overdose of a anaesthetic drug at doses provoking immediate loss
of consciousness; electrocution with cardiac arrest with correctly positioned electrodes and
appropriate electric current as to induce immediate loss of consciousness and cardiac arrest; or
exposure to a 1% prefilled, supervised chamber with carbon monoxide supplied by a source of
100% CO that will produce deep anaesthesia prior to death. Of note, the directive includes the use
or carbon dioxide and chloroform for mustelidae and chinchillas, and mouth-rectum electrocution
for foxes [57].
5. Pest rabbit
At origin, O.cuniculus existed only in the Iberian Peninsula but it constitutes nowadays one of the
most widespread and common species on earth. It has colonized all continents except for Asia and
Antarctica. This outcome is explained by biological features, such as great adaptability to climate,
high reproductive capacity, burrowing behaviour, and various introductions to non-endemic areas.
When the non-endemic areas do not present natural predators or competitors, rabbits’ demography
explodes and they become an invasive pest [3].
Australia is a well-known example in the rabbit pest issue. In 1859, 24 rabbits were released in the
state of Victoria. In 1926, the rabbit population was estimated at 10 billion and farmers were forced to
abandon their cultivation [62] because rabbits were overgrazing the native vegetation. Besides clear
impact on ecology and economy, pest rabbits are the cause of soil erosion and the suppression of
protective ground cover necessary for the survival of indigenous prey species [63]. Additionally, pest
rabbits have an important impact on agriculture because of crop destruction, insect penetration and
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reduction of carrying capacity of grazing areas. Similar scenarios have taken place in Great Britain,
Argentina and New Zealand [64].
For effective rabbit control, the Australian government makes use of a variety of techniques including
poisoning, fumigation, harbour removal, warren destruction, and rabbit proof fencing. Viral agents
have also been used, such as myxomatosis between 1952-1954, which killed 99.8% of the Australian
rabbit population. Rabbit Calicivirus Disease (RCD) has been used in the nineties. It causes acute fatal
disease in the rabbits and it is believed to cause less suffering than other methods [65]. Also, poisoning
is a common method for pest control. Sodium fluoroacetate also named 1080 or pindone, is a poison
acting as anticoagulant and is currently used along with RCD [62]
The Australian Veterinary association published (2011) regarding control of wild rabbits. They
recognize the use of sodium fluoroacetate or anticoagulant but forbid the use of strychnine. Ripping of
warrens is allowed only if used along with other methods to prevent presence of living animals during
the process. Use of explosives, irritant fumigants, steel-jawed traps, is considered as inhumane and
should not be performed. Shooting may be humane but is not effective in population control. The
association recognizes that myxomatosis causes distress but claims that it is a necessary part of an
effective control campaign [65]. This constitutes an ethically questionable position.
II.
Signs of pain and distress in the rabbit
It is difficult to assess pain in animals. Indeed, it will never be possible to ultimately assess the
animal’s perception of a stimulus. However, studies defined behavioural and physiological parameters
that change when the animal is believed to be in pain. For prey species such as the rabbit, it is very
difficult to assess pain behaviourally because they evolved to hide their vulnerability to potential
predators. When in pain, rabbits are likely to respond by “freezing”, also called tonic immobility,
especially in the presence of an observer. Pain scoring system must therefore integrate this “inactive”
pain-related behaviour (see Carmel, 2010).
Behavioural change is considered as the first indication that the welfare status is compromised [66].
Behavioural indicators of distress in rabbits are, inter alia high pitched vocalisations (not always in
the human audible spectrum), freezing behaviours, urination, defecation, evacuation of scent glands,
struggling, aggression, attempts to escape and skeletal muscles reflexes such as shivering, tremors and
spasms [18], [21]. Behavioural aversion or avoidance is also indicators of noxious stimuli.
Physiological signs of distress are high blood pressure, tachycardia provoking changes in the
electrocardiogram (ECG) , sweating, pupillary dilatation, elevation of corticosterone, ACTH, and c-fos
expression [67], [68]. For pet rabbits, information from the owner can give an insight of the normal
behaviour of their pet. It may therefore help to assess a behavioural change that could reflect pain [52].
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Chapter III
Analysis of Euthanasia methods
I.
General considerations
As each species has specific needs and features, animals from different species should not be
euthanized together. To respond to criteria set for euthanasia, i.e. induce “humane” death; the method
should induce loss of consciousness prior to other effects. Euthanasia methods rely on one out of three
possible basic mechanisms. First, death can be caused by direct or indirect hypoxia. With this
technique, convulsions2 can be sometimes seen after loss of consciousness. The second mechanism is
a depression of neurones necessary for life function. The depression of brain neurones induce loss of
consciousness followed by death due to respiratory depression and cardiac arrest. Motor activity may
sometimes be disinhibited causing thus excitement, delirium, and vocalisations. However, those are
not considered as purposeful. The third mechanism causing death is the physical disruption of brain
activity and vital neurones. The midbrain controls cardiac and respiratory activity and its destruction
causes thus immediate stop of these vital functions, leading to death. Here also, convulsions can occur
after the onset of unconsciousness [18], [69].
The euthanasia process has been divided into three phases. Phase I occurs from the initial contact to
the onset of clinical signs. Phase II occurs from clinical signs to recumbence, and phase III from
recumbence to death [70].The euthanasia process may be induced either by a unique agent, or by two
agents. The two-stage euthanasia involves stunning or anaesthesia followed by death induction. The
welfare of the animal is at stake when the two agents have inadequate time points of action. Indeed, if
the onset of the killing mechanism (e.g. asphyxia) occurs before the one inducing unconsciousness,
pain and distress may occur. In addition, the death-inducing agents (e.g. exsanguination) must occur
before the animal regains consciousness [30].
Two types of euthanasia methods can be distinguished, namely pharmacological-chemical and
physical methods. The pharmacological-chemical methods use either injectable or inhalant agents. The
technique consists of administration of an overdose of anaesthetics3 or gases with anaesthetic effect
that cause hypoxia. Some injectable agents contain neuromuscular blocking agents, and are thus
acceptable only under deep-anaesthesia. Physical methods have the advantage of eliminating
pharmacological contamination which is important in certain scientific studies or in the case the
2
Reflex motor reactions. In euthanasia context, they occur during anoxia [231], after decapitation [232] and after
stunning with physical methods [233].
3
Substance that produces in a controllable manner, a drug-induced absence of perception of all sensation [17]
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carcass is meant to enter the food chain [21]. All physical methods used must cause immediate loss of
consciousness which is achieved by physical trauma of the brain [17]. Even though all physical
methods require restrain, they may result in less fear and anxiety and be more rapid and painless death
than pharmaco-chemical methods, provided they are performed by skilled operators using a perfectly
maintained device. Most physical methods are aesthetically unpleasant which could cause distress to
the operator. However, in our opinion, priority should be given to the welfare of euthanized animals
[30].
Concerning the choice of a euthanasia method, the European directive 93/119/EC requires that “The
competent authority shall decide on the most appropriate method of killing for the different
species concerned in compliance with the general provisions of Article 3 of this Directive”,
i.e. “Animals shall be spared any avoidable excitement, pain or suffering during movement,
lairaging, restraint, stunning, slaughter or killing” [57]. Hence, the choice of the method should
always prioritize animal welfare aspect [71]. However, due to the lack of data and the subjectivity of
the observational data available, i.e. misinterpretation of reflex movements, emotional and aesthetic
bias, it is impossible to accurately evaluate each method [72]. Despite this fact, methods need to be
somehow evaluated. Thus, they are currently examined regarding their “ability to produce loss of
consciousness and death rapidly and reliably, safety of the personnel, irreversibility, emotional effect
of operators, compatibility with following use of the carcass, compatibility with species and individual
features and ability to maintain equipment” [18]. In practice, the method chosen is determined by the
species, the individual characteristics and needs (e.g. age, health status, habituation to handling), the
skills of the personnel and the equipment available [18], [30]. Emotional and ethical aspects play also
a role in this choice
1. Peri-euthanasia factors
Many factors that surround the process of euthanasia have an influence it and may determine the
extent to which welfare is impaired during the procedure. Indeed, stressor presence prior to euthanasia
determines the state, i.e. the behaviour and physiology, of the animal. This state defines the
smoothness of the proceedings. In addition, long-term pre-euthanasia stressors, such as housing
conditions, have an influence on muscle growth, muscle composition and thus ultimately on meat
quality [23] which is an important aspect in the context of production rabbits. Short-term preeuthanasia stressors i.e. stressors occurring just before killing, are inter alia fasting4, transport to
euthanasia location (e.g. slaughter plant, euthanasia chamber), restraint, unknown environment,
operator attitude and skills, pre-treatment and equipment quality and maintenance [23], [30], [46].
4
Removal of the food some hours in advance to empty the gut and avoid contamination by excreta during
evisceration [23]
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Fasting should be as short as possible. However, 8-12h fasting is believed to not substantially impair
welfare as rabbits are caecotroph and are thus very resistant to hunger [24].
Transport is an important factor as it constitutes a major stressor that can influence slaughter yield and
meat quality [73]. Animals should have a high welfare status before transport. Transport containers are
currently made from metal, fibreglass, plastic, wood or wire mesh. Appropriate bedding is therefore
not guaranteed. For long journeys, i.e. more than 24 hours, it is recommended to separate excreta from
lying areas [74]. At arrival, giving rabbits time for acclimatisation (at least 18 hours) reduces the pH
values of the meat (raised pH values are caused by stress) [75]. The length of the period of
acclimatisation needed depends on the level of stress the animal experienced, which depends on age,
social environment, duration of transport, conditions of transport, etc. [76]. Temperature should be
kept low, as “live shrinkage” is then reduced [23]. Good ventilation is also crucial to maintain an
acceptable welfare level. However, transport appears to be stressful per se since animals do no feed
and lose weight during transport [14].
Another peri-euthanasia factor that causes stress is restraint. Restraint is required is certain euthanasia
methods and can be defined as “the application of just enough force upon the animal to perform
required procedures” [20]. Restraint should be gentle, firm, involve careful handling and performed
preferably by a familiar and skilled operator [21]. The familiarity to the operator prevents additional
stress for the animal especially if it has been habituated to be restrained with the same operator.
Regarding restraint, the European directive 93/119/EC states “Animals must be restrained in an
appropriate manner in such a way as to spare them any avoidable pain, suffering, agitation, injury or
contusions” [57]. However although the latter directive forbids suspending animals before stunning or
killing, it makes an exception for rabbits provided that “appropriate measures are taken to ensure
that, on the point of being stunned, they are in a sufficiently relaxed state for stunning to be carried
out effectively and without undue delay”. This exception creates an “avoidable agitation” which, as
just mentioned, is forbidden by the directive itself. Following the directive, rabbits should not have
their head restraint if stunned or killed by electrical or physical means as this also produces “avoidable
agitation”.
More generally, the environment in which euthanasia is performed plays an important role in the
welfare implications of the procedure. To promote good welfare, overcrowding should be avoided
because animals may become stressed by the manifestations of distress of others. Because rabbits
communicate with inter alia scent, vocalizations non-audible to humans, or behavioural postures,
certain authors recommend to perform the procedure without the presence of dead animals and without
the presence of other alive individuals [18], [20], [30]. Between each euthanasia, the room should be
cleaned in order to minimize all possible cues of euthanasia, i.e. pheromones, urine, blood, faeces, of
the process [18], [20], [21]. The room should also be very silent to promote tranquillity. If injections
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are performed, it should ideally be done in a bright room (for correct administration) followed by a
transfer to a dark, quite room with non-metallic bedding and smooth relaxing music [20]. The attitude
of the personnel plays also an important role in welfare [60]. Operators should be calm, gentle, talk
softly during the process as it has been shown to calm down the animals [12], [20], [21]. The wellbeing of the operators is thereby promoted as well, and this helps to ensure appropriate human
behaviour during the process of euthanasia. Performing euthanasia repeatedly may lead to “profound
dissatisfaction” or even “alienation”. This can lead to “careless handling” and “careless euthanizing”.
Therefore, besides good euthanasia environment, psychological support, good training, short shifts and
frequent breakes, are crucial to maintain high welfare standards in humans and, as a consequence, in
rabbits [18], [77].
The skills of the operators are obviously crucial to insure good welfare standards. As stated in
paragraph 15 of the European directive 2010/106/EC “The level of competence of the person carrying
out this operation is equally important. Animals should therefore be killed only by a competent person
using a method that is appropriate to the species” [53]. Thus, the operators, being preferably familiar
with the animal, need to be certified, well-trained, and possess appropriate knowledge of the speciesspecific features, handling and restraint techniques. Moreover, the operator must master the euthanasia
technique chosen, the device or agent used, and the possible consequences of its effects (e.g.
convulsions) to avoid misinterpretations [18], [20]. Tiredness is another factor that may affect welfare
standards of euthanasia proceedings by affecting the performance of the personnel [4]
The state of the device also impacts the welfare implications of the process of euthanasia. To insure
high welfare standards, the device should be in excellent condition, otherwise it can cause slow and
stressful death (e.g. captive bolt) or it may constitute a danger for personnel and animals (e.g. ether
explosion, carbon monoxide intoxication) [18].
To insure the most humane death, some authors encourage a 2-stage procedure consisting of pretreatment with anxiolytics, sedatives or anaesthetics in a first stage, followed by administration of a
death-inducing method. This pre-treatment will calm down the animals, which is thought to be animalfriendly and which is very beneficial with difficult or dangerous specimens [20], [21]. Some authors
even advise the use of sedatives such as acepromazine maleate (0.7-1.5mg/kg s.c.5) before any
procedure requiring restraint or anaesthesia. This pre-treatment is believed to minimize anxiety and
stress. When butorphanol (0.1mg/kg) is added to acepromazine maleate, peripheral vasodilatation and
slight analgesia occurs in addition to sedation. Another well-known pre-treatment is Hypnorm® which
contains fentanyl and fluanisone (0.3ml/kg s.c.) [12]. As pre-euthanasia anaesthesia, S.O. Walshaw
(2000) recommends ketamine 25mg/kg in combination with xylazine 7mg/kg (PreMix®). Other
combinations for veterinary use exist as well [12], [78]. Sodium pentobarbital can be administered
5
Sub-cutaneous administration
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orally for sedation. It appears that the newest sodium pentobarbital solution FP-3 does not cause
stinging and burning and can be thus administered by intra muscular injection [20] which should be
less distressful as it requires less restraint.
2. Recognition and confirmation of death
As stated previously, the recognition and confirmation of death is crucial to ensure a humane death.
Indeed, animals under deep narcosis may appear death but are still alive. In humans, brain death is
defined as an “irreversible loss of brain function including the brainstem” [79]. When the death of an
animal is questioned, an additional method should be used to ensure that the animal is effectively
killed [18], [20].
Observation of lack of vital signs constitutes the most obvious manner to assess death. Lack of vital
signs includes cessation of heartbeat, cessation of respiration, fall of body temperature and onset of
rigor mortis [20]. Loss of brainstem reflexes, such as pupillary light reflex and corneal reflex, are
indicative of the loss of brain function and are practical to assess stunning and death [80]. In certain
euthanasia methods, reflex convulsions arise. Brain failure is considered to occur simultaneously with
cessation of the convulsions [81].
After euthanasia has been performed and the animal is unconscious, three methods can be used to
assess death. The first one is the cardiac puncture; it is done by inserting a syringe in the heart of the
unconscious animal and observing whether the syringe moves because of cardiac activity. The second
consists of assessing lack of heartbeat and respiration with a stethoscope. The third one is verifying the
onset of rigor mortis after 20 min (partial rigor mortis). However, the best method to assess brain
death is to observe the EEG that measures activity of the cerebral cortex [80]. An isoelectric EEG
characterise brain death [67].
II.
Stunning
Some euthanasia or slaughter methods require stunning prior to death in order to prevent unnecessary
suffering by insuring unconsciousness and insensibility [54], [58]. In all cases, after stunning, death
must be induced, or in other words “confirmed”, by another method. The European directive
93/119/EC defined the permitted methods for stunning [57].
Stunning can be done with a captive bolt pistol, which is described in section IV.1 of the present
chapter. The device must be positioned in a way to enter the cerebral cortex and bleeding must begin
within 15 seconds [4].
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Stunning can also be achieved by electrocution. Electronacrosis with alternative electrical current
(AC) is the most widely used stunning method in rabbit slaughter plants [4] [82]. The European
Directive 93/119/EC and many authors state that electrodes must be applied in a way to pass the
current trough the brain to induce depolarization of neurones and immediate loss of consciousness
[57], [69], [83],[18]. To achieve this, electrodes have to be applied firmly and at a precise location of
the head, i.e. not behind the ears or at the neck. [21]. Special equipment exists for rabbit
electronarcosis and is depicted in figure 1. A system that blocks the device if the minimal required
current is not provided must be present in the basic equipment for electronacosis. Unconsciousness
after current application lasts only 15 to 20 seconds and animals start to breathe again after that period.
The euthanasia method (e.g. exsanguinations) must therefore be applied before the recovery of the
respiratory activity [84].
Figure 1: Diagram of electrodes for stunning rabbits (Anil et al., 2006 )
Several investigations have been performed in abattoirs on the efficiency of electronarcosis (followed
by exsanguinations) in practice. The studies found that in 10% of cases, the position of the electrodes
was incorrect. Electrodes were either too close to the nose or a forelimb was stuck between the head
and the electrode. In 10% of cases, current was applied several times (up to 4) because the first current
application was judged not long enough. At exsanguination, it appeared that 3 animals failed to be
stunned (vocalization, flight reaction) and 18 (1.76%) recovered before exsanguination performance
(head movement, corneal reflex) demonstrating that in practice, electronarcosis is not effective and
thus electrical stunning followed by exsanguination is not a humane euthanasia method, the way it is
currently applied [4].
Concussion is another method for stunning. It is considered quick and humane and involves striking
the base of the head in the occipital region [83]. It should be performed with a mechanical instrument
that induces a blow to the skull. Proper strength and position are crucial. With small batches of rabbits,
concussion without using mechanical device is tolerated provided a sharp blow to the head is
administered [85]. A study showed that a blunt trauma with a heavy instrument did not produce
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apparent signs of pain and cardiac activity started to decrease after 10 seconds [86]. This method must
be performed in a way to render rabbits immediately unconscious until death is induced by another
method (e.g. exsanguination). In the opposite case, the welfare of the animal will be greatly
compromised. In addition to the appalling implications of incorrect application, the method is difficult
to apply consistently and a high level of expertise is required. For these reasons, many authors
concluded that this method is only conditionally acceptable [21].
Exposure to carbon dioxide or other gases constitutes another method for stunning. It appears to have
been accepted by several governments across Europe. Nonetheless, the European directive describes
the use of CO2 exclusively for pigs’ stunning [67] and it thus not recommendable for rabbits.
Independently on which method is used for stunning, it is important to recognize whether the animals
are properly stunned before applying the euthanasia method, especially when the latter requires prior
stunning. In fact, the efficiency of stunning is becoming a societal and political concern [67]. EEG
appears to be the best mean to measure insensibility [80] since a strong reduction of EEG frequency is
considered a reliable indicator of unconsciousness [87], [88]. However, in practice, it is impossible to
use this mean on a large scale. Therefore, the absence of brainstem reflexes, such as pupillary light
reflex and corneal reflex, are used in practice for rabbits, as they are considered reliable indicators of
brain function [80], [89], [90]. In chickens, lack of neck tension has also been described as indicator of
insensibility [91]. Indeed, its onset is synchronized with the loss of brain activity [87]. Sustained
absence of breathing is known as an indicator of “irreversible brain failure and death” [80]. Loss of
visually evoked responses, extension of limbs, opistothotonos6, downward rotation of eyeballs and
convulsions constitute other signs of effective stunning [92], [93]. This is especially true for
electronarcosis [84]. Note that care must be taken when interpreting lack of movement. Indeed, lack of
movement does not necessarily imply lack of consciousness because rabbits, being a prey species, may
“play death” while being conscious [18].
III.
Pharmacological-Chemical methods
The pharmacological-chemical methods involve an overdose of anaesthetic which results in
unconsciousness, followed by respiratory and cardiac arrest that induce death [17]. Pharmacologicalchemical methods should not be used when the carcass is destined to the food chain as the latter can be
contaminated [21]. Two types of methods may be distinguished following their mean of
administration: methods using injectable agents and methods using inhalation agents.
6
Condition of spasm of the muscles of the back, causing the head and lower limbs to bend backward and the
trunk to arch forward [16]
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Injectable agents are considered by some authors as the most preferable mean of euthanasia in terms of
welfare because their administration is reliable, they have an anaesthetic effect and they induce a rapid
and smooth onset of unconsciousness. Nonetheless, using injectable agents requires restraint that may
distress the animals. Intravenous (i.v.) injection is the most desirable as it produces the most rapid
anaesthesia and the most rapid respiratory failure resulting in death [17], [18], [83]. In rabbits, i.v. is
usually performed in the ear vein but this procedure is not easy as rabbits usually struggle at
venipuncture if not pre-treated or pre-trained [78].When i.v. is not practical, intraperitoneal injection
(i.p.) may then be performed. However, i.p. presents the disadvantage that phase I of euthanasia, i.e.
onset of clinical signs, is longer [18], [21], [78], [83].The agent injected i.p. must be non-irritant and
free from neuromuscular blocker [18]. Intracaridiac (i.c.) injection is authorized only on deeply
anaesthetized, sedated or comatose animals [18], [83]. Other methods of administration such as
intrapulmonary, intracephalic, intrahepatic, or sub-cutaneous injections are not advised since they are
either difficult to perform accurately or take too long to produce the desired effects [18], [21].
Generally, those compounds produce respiratory cease when double anaesthetic doses are
administered and cardiac arrest at quadruple anaesthetic dose [21].
Inhalant agents, which induce death via anoxia, require a longer phase I because the gas needs to reach
a certain concentration in the alveoli [18]. The suitability of an inhalant agent is assessed by the
potential distress that may occur during phase I. Rabbits appear to be distressed by inhalants as they
hold their breath and struggle severely [94]. In addition, neonates (up to 16 weeks) appear to be very
resistant to anoxia. Indeed, Glass et al. (1944) reported that new born rabbits (6 days) survived for
13min, rabbits of 14 days survived for 4 min and rabbits older than 18 days lasted 1.5 min. Therefore,
the use of inhalant in rabbits should be avoided whenever possible.
1. Pentobarbital Overdose
Pentobarbital is a drug within the Barbiturates family. Barbiturates depress the central nervous system
(CNS) by interfering with the neurotransmission between the cortex and medulla oblongata. They
induce analgesia evolving in loss of consciousness followed by anaesthesia. At anaesthetic doses, the
drug is metabolized and individuals recover within hours. An overdose produces, after the anaesthetic
stage, a depression of the respiratory system resulting in apnoea followed by cardiac arrest and death
[18], [20].
All barbiturates derivatives, i.e. barbituric acid derivatives, thiobarbiturates, oxybarbiturates, are
considered acceptable euthanasia agents for i.v. application [18], [21]. Preferred compounds are the
ones that are potent, long lasting, stable in solution, and with relatively low financial costs. Sodium
pentobarbital seems to fit these criteria the best [18]. Sodium pentobarbital, besides being the most
cost effective, produces rapid onset of action with reasonable dose, concentration and rate of injection
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required [18], [20]. No particular device is needed for this technique and the latter is applicable to
virtually all mammalian species regardless the health status, age and other features of the individual
[20]. Moreover, the potential welfare consequences of incorrect application of the method are less
appalling than other methods, such as decapitation. The process is aesthetically bearable as it seems to
be smooth and is believed to engender only minimal discomfort [18], [30]. However, this latter belief
is debatable since the aesthetic aspect does not give information about the welfare standard of a
method. The pitfall of the sodium pentobarbital method is that i.v. injection is advised. As previously
mentioned this form of administration requires trained personnel, restraint and implies pain associated
with venipuncture. Gasping7 as well as momentary increase in vital signs have been seen after
administration of lethal doses of sodium pentobarbital [17], [18], [20]. The drug contaminates the
carcass and may cause sedation or even death if the carcass is ingested [18], [20]. An enlargement of
the spleen which can interfere with post mortem analysis is regularly observed [17]. Nevertheless, one
can conclude that since sodium pentobarbital induces the loss of consciousness very rapidly, provokes
analgesia then anaesthesia before death and since the procedure is less risky in terms of potential
welfare implications of poor performance, the advantages outweigh the disadvantages mentioned
above [18]. This explains why many authors conclude that sodium pentobabital constitutes the most
desirable euthanasia technique [17], [18], [21], [83].
For rabbits, the preferred mode of administration is i.v. injection as it is very rapid and does not cause
pain except for the venipuncture [18]. I.p. administration is not advised, even if it is easier to
administer and thus less stressful, because the drug can cause irritation of the peritoneum and thus pain
due to its high alkalinity [83], [95]. Some argue that this issue can be overcome by dilution [21], [83].
The administered doses for rabbits range from 100 mg/kg to 200 mg/kg. I.c. injection is only allowed
on fully anaesthetized individuals [17], [21], [96].
Sodium pentobarbital can also be administered in combination with local anaesthetics or cardiotoxic
agents such as lidocaine and phenytoin respectively. Commercially available combinations such as
Beutanasia-D special® or Euthasol® contain phenytoin, but, provided it is not administred i.c., the
onset of unconsciousness occurs prior to cardiac arrest. The use of local anaesthetics may help to
overcome the irritation caused by the drug when administered i.p. [30]. The new FP-3® combination,
commercialized in 2005 contains lidocaine and is thus believed to avoid the burning and stinging
sensations which render it possibly suitable for i.p or even intra-muscular (i.m.) administration. In
some places, sodium pentobarbital plus anaesthtics combinations are easier to obtain than pure sodium
pentobarbital (e.g. United-States). Combinations with neuromuscular blocking agents are unacceptable
since the onset of the neuromuscular action occurs before the loss of consciousness induced by
pentobarbital [18].
7
Abnormal breathing pattern that precedes imminent death and results in terminal apnea. It is caused by cerebral
ischemia [234], [235].
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With rabbits, the procedure of sodium pentobarbital administration involves restraint of the rabbit,
placement of the infusion set, filling of the syringe with the drug, pressure on the base of the ear in
order to distant the marginal ear vein, insertion of the needle into the vein for 1cm, injection,
withdrawing and death confirmation i.e., lack of cardiac pulse, no breathing and absence of pupillary
reflex [96].
2. T61® overdose
T61® is a combination of three drugs namely a curariform drug which acts as muscle relaxant; a local
anaesthetic tetracain HCl; and a hypnotic agent [17], [21], [69], [72]. Besides inducing insensibility,
the local anaesthetic depresses the respiratory centre. The muscle relaxant paralyze the striated
muscles resulting in circulatory collapse and has no influence on the onset of unconsciousness [72].
The muscle relaxant presents the advantage of suppressing the terminal gasp that occurs with other
euthanasia agents such as barbiturates [17], [21]. However, in terms of welfare, there is no
improvement as the terminal gasp is believed to be a reflex response [72]. The mixture has to be
injected i.v. only, because the onset and chronology of actions by other routes is unknown [69]. The
rate of injection must be very slow [17], [21], [83] and pre-treatment with sedatives is advised by
some authors [83].
In the scientific literature over T61, there are conflicting statements regarding the onset of muscle
relaxation and the loss of consciousness. Some authors argue that muscle relaxation occurs after loss
of consciousness [17] others that the onsets are simultaneous [97] and others that muscle relaxation
may occur in a still conscious individual [72]. In the latter case, the welfare would be greatly impaired.
In the study of Hellebrekers et al.(1990) that tested the effects of T61 on dogs, an increased muscle
activity and vocalizations have been observed during injection in 3 out of 8 dogs tested. Different
studies also reported symptoms of distress while using T61 [98]. Some authors believe that it is the
late onset of the hypnotic effect that causes these unpleasant symptoms. The question that needs to be
answered to define on the moral acceptability of the T61 method is whether these “distress symptoms”
occurred in a state of consciousness [72]. Since in the study, animals were sedated, authors believe
that the potential signs of distress are rather reflexes such as the ones provoked by barbiturates [97].
One can conclude that the uncertainty regarding the chronology of the effects of different components
of T61raises concern as it may lead to potentially negative consequences on welfare. In fact, T61® has
been withdrawn from the market and is not manufactured anymore in the United-States [69]. Since
T61 does not present advantages over pentobarbital and raises concern about animal welfare, sodium
pentobarbital should be preferred [17], [72], [99].
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3. Volatile inhalant anaesthetics
Inhalant anaesthetics, i.e. halothane, enflurane and isoflurane, are gases regularly used for euthanasia.
Indeed, they appear to be less aversive than CO2 [100] and have thus been used as pre-treatment to
CO2 euthanasia [18]. These gases have the advantage to be non-flammable and non-explosive.
However they constitute a health hazard for humans [18], [69]. Indeed, congenital abnormalities can
occur if women are exposed to traces of these gases during the first weeks of pregnancy [18]. Hence,
an appropriate gas scavenging apparatus must thus be used to prevent exposure of the operator [83].
The costs and difficulty of application of the euthanasia method using volatile inhalant anaesthetics
restrict its use in larger animals. In smaller animals (less than 7kg), the method is valuable especially
when venipuncture is difficult [18]. Indeed, an important advantage of this method is that it does not
require restraint. However, although rabbits weigh, in most cases, less than 7kg, the use of inhalant
anaesthetics is more than questioned as they seem to react aversively to gases [94].
The euthanasia process using inhalant anaesthetics involves placing the animal into a prefilled
chamber with high gas concentration [17] and waiting until respiration ceases and death occurs [83].
Sufficient air oxygen must be provided to prevent hypoxia [69] and care must be taken to avoid
contact between the individual and the liquid form of the gas since the latter is known to be highly
irritant [83].
Halothane appears to constitute the most desirable inhalant anaesthetic. Indeed, a study showed that
halothane is the least aversive, as compared to isoflurane, enflurane and CO2 [100] because it acts the
most rapidly and effectively as cardiovascular and respiratory depressant [18]. In fact, it was shown to
provoke cardiac arrest in 90 seconds at 4% volume concentration [94] without inducing significant
signs of distress [18]. Obviously the latter observation does not exclude possible negative welfare
implications of a euthanasia method using halothane.
Enflurane has the same effects as halothane but may act slightly slower [18]. The drug appears to be
less metabolized in the liver which may constitute an advantage is certain toxicological studies [21].
Enflurane has a lower vapour pressure potency which counterbalances the fact that it is less soluble in
blood. The induction time may therefore be close to the halothane one. When deeply anaesthetized
with enflurane, individuals have been seen to seizure which is aesthetically unpleasant [18].
Isoflurane can also cause rapid anaesthesia and death but high concentrations are required [18].
Additionally, compared with halothane, it is less soluble in blood and acts therefore more slowly [18],
[83]. A recent study suggested that isoflurane could be used as refinement to CO2 euthanasia method
in rats not previously exposed to inhalant anaesthetics. Indeed, these rats showed less aversion to
isoflurane than to CO2. However, although being less bad, isoflurane induced aversion to re-exposure
[101] and has a pungent odour. For these reasons, isoflurane, such as other anaesthetics, should not be
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used in rabbits because they will hold their breath, delaying thereby the onset of unconsciousness [18],
[21].
4. CO2
CO2 asphyxiation is regularly used in euthanasia of small laboratory animals [69] including rabbits
[82], [102]. CO2 is virtually odourless, non-flammable, non-explosive, and heavier than air [70], [103],
[104]. Its safety, ease of use and inexpensiveness constitutes good advantages [105]. Moreover, it is
believed to have a quick anaesthetic effect when inhaled [70], [103], [104] and is easily applicable for
large numbers of animals [105]. Finally, CO2 does not contaminate the carcass [18] and its application
does not require restraint, which is beneficial in terms of welfare [67].
However, rabbits appear to have long survival times with CO2 induction [106] which might be due to
their breath holding strategy when facing gases [94], [107], [108] or to their physiological ability to
cope with hypercapnia8 [18]. This latter fact questions the use of CO2 in rabbit species. In addition,
CO2 is not physiologically inert [109]. Scientific studies have shown that CO2 provokes salivation,
“pawing at the nose”, vocalizations, defecation, urination, anxiety, tissue lesions in the respiratory
system, and an increase in locomotor activity and rearing behaviours which are signs of arousal.
Moreover, CO2 may induce asphyxia before insensibility. These aversive effects occur in many
species, including rabbits, especially at high concentrations. However, they have been noticed at lower
concentrations, i.e. 40% on as well [17], [30], [110], [111], [112], [113], [114], [115], [116]. Some
authors have hypothesized that distress is provoked by asphyxia and mucosa irritation due to
formation of carbonic acid in the nose [117], [118] which would explain the “pawing at the nose”
behaviour.
Moreover, a substantial body of evidence indicates that CO2 produces pain, i.e. piercing and stabbing,
in humans [109], [110], [118], [119]. The principle of analogy may lead to an extrapolation of those
findings to animals [109], [120]. Indeed, pain is believed to be associated with the presence of nonmyelinated neurones of the nasal mucosa and these neurones are present is virtually all mammals
[121], [122]. Finally, the distress associated with CO2 is emphasized by the fact that the latter gas is
used as pain stimulus in human [118] and animals studies [123].
CO2 has been shown to fail to induce rapid loss of consciousness. Indeed, piglets vocalized in the first
30 seconds and stopped moving after 90 seconds only [111]. However, some studies suggest that
aversive reactions, such as ataxia9, which is symptomatic of CO2 euthanasia [110], [124], [125], might
occur after loss of consciousness [69], [109]. Further research is needed to establish the aversiveness
of such side-effects [109]. Conversely to the studies mentioned above, several investigations did not
8
9
Excessive CO2 concentration in the blood [16]
Lack of voluntary coordination of muscle movements [16]
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find any sign of distress associated with CO2 [22], [42], [109], [125], [126]. A study form Hackbarth et
al. (2000) assessed behavioural and hormonal markers of distress between a sedated group and a nonsedated one. No between-group differences were found suggesting that CO2 exposure was not
stressful. This is in line with other studies that found no significant effect of anaesthesia prior to CO2
induction [22], [127]. This goes against the substantial amount of studies showing that CO2 is aversive.
For instance, a recent study of Wong et al. (2013) showed that rats tested is a light-dark box presented
aversion to CO2.
Many studies suggest that the greater the concentration, the faster the loss of consciousness [18].
However, it also appears that the greater the concentration, the greater the distress [110], [111], [112].
Nonetheless, as suggested earlier, distress has also been seen at CO2 concentration of 25% in pigs, rats
and mice [100], [128]. A 35% concentration of CO2 has been shown to change respiration rythm,
blood pressure, heart rate, and HPA-axis activity [42], [129], [130]. At concentration of 60% or above,
hyperventilation and loss of consciousness take place. At CO2 concentrations above 70%, respiratory
and cardiac failure occur [83], [131]. These high concentrations are generally recommended as they
induce rapid loss of consciousness before the onset of hypoxia (e.g. in J. K. Blackshaw et al., 1988 a
concentration of 97% is recommended for euthansia of rats and mice). Some authors recommend even
higher concentrations (see Close et al., 1996). However, Van Zutphen et al. (1993) have shown that
100% CO2 provokes breathlessness causing thereby distress. This conclusion has been supported by
Leach et al (2002). On the whole, one can conclude that different authors recommend conflicting
strategies, i.e. some advertising low concentrations and others high concentrations [124], [133].
Whether the chamber should be prefilled (PF) with the CO2 concentration desired or whether a gradual
induction (GI) should take place after the animal is placed in the chamber constitutes an ongoing
debate. With GI, death takes longer to occur [18]. Indeed, it takes more time for blood pressure and
heart rate to collapse [134]. The American Veterinary Medicine Association (2007) suggests a CO2
flow rate of 20% of the volume of the chamber per minute but it has been seen that a high flow rate,
i.e. 15L per minute or above, may cause a distressing noise [127]. The latter problem is obviously nonexistent in PF chambers. Nevertheless, Britt et al.(1987) concluded that GI was preferable since, even
if the process was slower, fewer signs of distress were uncovered. Other studies are in line with this
statement [126]. Some authors recommended therefore the GI strategy [115], [135]. Other authors opt
for the PF technique as it is more rapid [113], [124], [134]. Finally, certain authors did not find any
significant difference between both techniques, which were both very slow, namely induced
unconsciousness after 30 seconds and death after 5.4 minutes in PF [134].
Another issue without consensus is whether mixing CO2 with O2 is more beneficial in terms of
welfare. Mixing with O2 is believed to produce death by narcosis and not anoxia [113]. However,
some authors advertised that suffering was reduced with O2 although the processing of euthanasia took
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longer [113], [124]. Conversely, other authors did not report any advantage for welfare as no
behavioural change was observed [18], [133], [136].
Mixing CO2 with gases such as Argon or Halothane has also been investigated. Mixing low
concentrations of CO2 with inert gases such as Argon (60%) is acceptable in poultry as has been
shown to cause rapid brain failure. However, this combination may cause excitement during induction
and convulsions after loss of consciousness, and some authors concluded that it should be avoided in
larger species [30], [137]. Clifford et al. (1985), suggested to combine CO2 with Halothane. However,
this mixture is expensive and presents substantial danger to personnel [134].
Studies found that 1min before the failure of the circulatory system, animals appeared dead. It is
therefore advised to maintain CO2 flow for an additional minute [18], [134]. Moreover, literature
shows that the time for unconsciousness varies greatly form one situation to another (e.g. J. K.
Blackshaw et al., 1988) which questions the humanity of the method. There is no consensus regarding
the latter [134] and further research is needed in order to provide adequate knowledge about the use of
the CO2 method for euthanasia and about possible refinements available [139].
In conclusion, some authors recommend CO2 [22], even for rabbits [140] as handling may be more
stressful than CO2 exposure [114]. Conversely, other authors do not recommend the latter method (e.g.
Ewbank, 1983; Green et al., 1981) because of the welfare issues detailed above. Given the incoherence
found in the literature, it would be wise to avoid the use of CO2 without anaesthesia, especially in
rabbits as they are sensitive to gases and survive for a relatively long period after CO2 exposure [30],
[94], [106], [107], [108], [109]. The questionability of the humanity of the CO2 euthanasia method
made the Canadian Council for Animal Care (CCAC) to recommend other methods for euthanasia,
especially for rodents [141].
5. CO
Carbone monoxide (CO) is an odourless, colourless, non-explosive and non-flammable (below 10%
concentration) gas [18]. Due to its non-detectability, it is usually not accepted as euthanasia mean
because it represents a substantial danger for the personnel [83]. Indeed CO is a “cumulative poison”
which means that clinical signs of poisoning are visible very late. For humans, these clinical signs
appear at CO concentration of 0.2% [142] whereas a person may die after 1 hour exposure to 0.45%
CO [143]. Moreover, chronic exposure to CO has teragenic effects and may increase cardiovascular
disease prevalence [144], [145]. However, when using appropriate gas scavenging devices and safety
measures (e.g. presence of CO monitors, outdoor euthanasia performance) CO appears to constitute a
humane way to euthanize animals [83], [146]. Indeed, its undetectably helps to prevent distress during
induction [131], [147] and animals appear to be unaware of occurring hypoxemia insuring thus a
humane death [18].
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CO can be obtained by three different means: chemical reaction of sodium formate with sulphuric
acid, incomplete combustion engines, or commercially compressed cylinders. Only the latter source is
authorized for euthanasia as the other means are believed to provoke irritation of the respiratory track,
to produce other gases and might cause problems with cooling [18], [83].
CO has a greater affinity to haemoglobin than oxygen. Consequently, it combines with haemoglobin to
form carboxyhaemoglobin which blocks the uptake of oxygen by the erythrocytes. This causes
hypoxemia that is followed by death [18], [148]. Some reflex motor activity, i.e. convulsions, may
occur during unconsciousness as CO appears to stimulate motor centres in the brain [18], [21].
Studies showed that minks became comatose after 21seconds at 3.5% CO concentrations [146].
Ramsey ant Eilman (1932) studied guinea pigs subjected to 8% CO exposure. They noted a comatose
state after 2 minutes and death within 6 minutes. Dogs exposed to 6% CO vocalized and became
agitated before losing consciousness. EEG showed abnormal brain activity that may have provoked
this abnormal behaviour. The latter is therefore not believed to be a manifestation of distress [148].
This belief is in line with the fact that humans do not report substantial distress while exposed to CO
[142] as the symptoms preceding loss of consciousness, i.e. headaches, dizziness, weakness followed
by decrease in visual acuity, nausea, confusion [150], are relatively mild. However, use of
tranquilizers decreases behavioural and physiologic response in dogs [151] suggesting that they might
experience distress when non-treated.
With this method, it is advised to euthanize animals one by one and to ensure a flow rate that rapidly
reaches 6% CO concentration. For rabbits, some authors consider this method acceptable without
anaesthesia but this is not the case of the whole scientific community [18], [30].
IV.
Physical methods
Physical methods, if well-performed, are considered by some authors to be more humane than the
pharmacological-chemical ones because they involve immediate death. They have also the advantage
to not contaminate the carcass which may be desired for meat consumption or scientific research.
However, the methods involve usually tissue destruction which may be unwanted for particular
research questions. Physical methods are usually aesthetically unpleasant and may have psychological
repercussions on the operators. Moreover, a number of factors may put animal welfare at stake, such
as the necessity for restraint, the incorrect application of the device used, the lack of experience and
expertise of the operator or the mechanical inefficiency of the device conditioned its maintenance [30].
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1. Captive bolt
The captive bolt gun is a mechanical device powered with gun powder or compressed air that can be
either penetrating or non-penetrating. For the penetrating one to be effective, the bolt must penetrate
sufficiently into the skull to destroy the brain inducing immediate loss of consciousness and even
death [18]. The bolt penetration produces severe concussion, focal injury around the wound and tissue
damage of the cerebral hemispheres, the brain stem and cerebellum [152], [153], [154]. It has been
suggested that the extensive brain damage found in areas non-adjacent to the wound, resulted in strong
pressure changes provoked by penetration of the bolt [155]. Besides the brain destruction, a study
showed that the impact of the bolt itself on the cranium may be determinant for effective stunning
[152].
For effective use of the technique, the correct positioning of the captive bolt is crucial [156]. To
achieve this, restraint is unavoidable. Operators must therefore master the restrain technique of the
specific species, have sufficient knowledge about the species specific skull features, be experts in the
device manipulation and be psychologically well-prepared to the non-aesthetic result of the method
[18], [83], [156].
Each device is species-specific as the size of the bolt and the strength of the shot delivery must be
adapted to the skull features. For rabbits, spring-operated penetrating captive bolt guns are used. The
technique is especially used in large rabbits, namely more than 4kg [30], [156], [157]. In young
animals, the skull may be too soft for effective stunning and this technique should be thus avoided
[155], [157].
Figure 2 : Spring operated captive bolt guns used for rabbits (EFSA, 2006)
Since the captive bolt gun may either stun (especially the non-penetrating) or directly kill the animal,
death induction by another mean is compulsory [18], [83]. The maintenance of the device is also
crucial for the efficiency and humanity of the process [18]. When performed correctly, the loss of
consciousness, the loss of reflexes and the respiratory failure are immediate [30], [155]. The heart rate
and pulse decrease slowly [155]. Virtually no vocalization or struggling are seen and EEG stops after
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1 minute in rabbits [30]. In calves, captive bolt appears to be an effective stunning technique as no
behavioural response occurs when exsanguinations takes place [155].
Because the present technique requires restraint, high-level skills, good device maintenance and is
non-pleasant aesthetically, it is only conditionally recommended [18], [30]. However, the captive bolt
technique is useful in slaughterhouses or other contexts where pharmacological-chemical methods
need to be avoided. That is why the technique is recommended by the American Veterinary Medical
Association [18].
2. Electrocution
Electrical stunning is the most widely used technique in rabbits abattoirs [4]. This technique may also
be used as a proper euthanasia method. Electrocution causes death by the induction of cardiac
fibrillation causing cerebral hypoxia [158], [159]. However, in animals weighing less than 5 kg, such
as the majority of rabbits, cardiac fibrillation does not necessarily imply long-lasting circulatory
collapse. Furthermore, it has been shown to be more aversive than 90% CO2 application [160].
Animals may remain conscious for up to 30 seconds after electrical application. That is why animals
must be rendered unconscious before being subjected to electrocution [18]. Unconsciousness should
be achieved by electronarcosis, i.e. application of current to the brain (see Chapter 3.II). Other
methods such as head-to-tail or head-to-foot current application, are not acceptable as they do not
induce immediate unconsciousness [82].
For correct electrocution, removing hair, wool or wetting the fur may be necessary. Also, the correct
positioning of the electrodes, the correct power and length of the current application must be ensured
to preserve the welfare of the animal. Therefore, the device used should display the power and
duration of the current application and the operator should be an expert in this method [161].
To conclude, one can say that electrocution alone is not advised as the method appears aversive and
does not ensure proper circulatory collapse in rabbits, which disqualify its use on stunned animals. The
use of electrocution for stunning only was shown to impair animal welfare and to be not efficient
enough in practice (see Chapter 3.II). Moreover, although financially inexpensive, the method requires
restraint, specialist skills and much time per individual. Also, it may be dangerous for the operators
and is aesthetically unpleasant [18]. For all these reasons electrocution as a mean of euthanasia is not
recommended for rabbits and other methods should be preferred [18].
3. Cervical dislocation
Cervical dislocation (CD) involves severing of the spinal cord from the brain which damages the brain
stem and induces immediate loss of consciousness [17], [83], [113]. This method is only conditionally
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accepted but is, in practice, regularly used in neonatal rabbits [162] or adult rabbits weighting less than
1kg. For instance, in the fur industry, cervical dislocation routinely follows electrical stunning [163].
The heavier the animal, the greater the strength that needs to be applied to perform the procedure. In
rabbits, the muscle mass concentrated in the cervical region complicates the performance of CD.
Moreover, the operator has to be well-trained and experienced as this operation is not easy to perform
[17], [18], [30], [83].
There are several methods for CD [164]. One manner consists in stretching the animal, hyper
extending its neck and twisting it at 30 degrees in order to separate the C2 cervical vertebra from the
skull [102], [165]. Another manner involves suspension of the rabbit by the hind legs, grasping of both
hocks with one hand and administrating a sharp blow at the base of the skull while blocking the chest
[30].A third manner consists of pulling the head until feeling that the skull and the spinal cord are
severed. However, the latter is a slow process that may greatly compromise the welfare of a not
anaesthetized animal [18]. Prior sedation, anaesthesia or stunning is advised and even mandatory in
some guidelines in order to facilitate the process and minimize the distress experienced [21], [30],
[83]. Although this method is supposed to kill the animal, studies found that CD could carry high
failure rate [164] and death confirmation is thus recommended [83], [147].
A worrying fact regarding the method of CD is that the EEG appears to be still active until 13 seconds
after dislocation [166], [167]. Moreover, studies performed on mice found that 21% continued to
breath until 15min after CD and that almost all mice presented unwanted thoracic and lumbar lesions.
Other studies are in line with the latter findings (e.g. Carbone et al., 2012). Erasmus et al. (2010)
compared different CD methods with captive bolt and blunt trauma in turkeys and found that the two
latter euthanasia ways caused immediate unconsciousness whereas all CD methods failed to induce
loss of consciousness. Therefore, Erasmus and colleagues (2010) as well as Carbone and colleagues
(2012), concluded that CD resulted in unsuccessful euthanasia.
In the light of the facts cited above, one can conclude that this method not easy to apply [30] and
appears to endanger the welfare of the animals. Because the humanity of the method is not yet proven,
other methods should therefore be preferred [18]. Note that some authors stated that is method is
conditionally acceptable provided the animals are anaesthetized beforehand [30], [164].
4. Decapitation
Decapitation is a “method severing the neck of the animal close to the head with a sharp instrument”
[21]. This method presents the advantage to leave the brain undamaged [18]. Decapitation by
guillotine is used in rabbits provided they are weighing less than 1kg which insures a sufficiently
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fragile skeleton [17], [21]. Compared with scissors, guillotine is a more rapid and precise device for
decapitation. Sedation or anaesthesia is recommended for easier handling [17], [30].
An important disadvantage of the decapitation method lies in the high risk of inaccurate performance
of the operator, even if the latter is an experienced professional. Moreover, the maintenance of the
guillotine plays a crucial role in the process of decapitation and constitutes thus an additional risk for
welfare impairment [18], [109]. Finally, the method requires a certain degree of restraint which is
distressing for the animals. Note that the use of restraint plastic cones appears to be less distressing
and enhances the position on the guillotine [18].
An ongoing debate on the humanity of decapitation regards the duration of consciousness after
decapitation [69], [147], [162]. Several authors suggest that warm-blooded animals, such as rabbits,
lose consciousness very rapidly after decapitation because of the immediate lack of circulation to the
brain provoking thereby rapid cerebral anoxia. A rat’s head was estimated to become anoxic, and thus
unconscious, in 2,7 seconds [166]. This time period is substantially shorter compared to the CO2
method [109]. Conversely, some studies showed EEG traces 13.6 seconds after decapitation [168]. In
addition, a visually evoked response was found up to 30 seconds after decapitation. However, it is
important to bear in mind that the presence of an EEG activity does not infer the presence of
sensibility to pain, especially when the onset of unconsciousness occurs rapidly [166], [167]. Because
of the contradictory results found in the literature, some guidelines favour other euthanasia methods
over decapitation [18], [21], [109] but the welfare implications of decapitation and the meaning of an
active EEG remain to be studied further.
5. Microwave
This technique is mainly used in neurobiology to fix brain metabolites while maintaining the
anatomical integrity of the brain [169], [170]. The mechanism involved in the microwave euthanasia
technique is the interruption of brain enzymatic activity. The efficiency of the interruption depends on
the size of the head, the ability to tune the resonance cavity and the features of the specific apparatus.
The latter must be specifically designed for euthanasia purpose and cannot be replaced by any
domestic appliance. In rabbits, the method is accepted only for individuals weighing less than 300g
[83], [171]. The method requires specialist skills as the beam needs to be directed to a specific brain
area to ensure rapid death. In fact, when correctly applied death can be achieved in less than 1second
[69], [172]. However, because of the difficulty of correct application of the method and because
devices are intended for smaller species, i.e. mice and rats, the use of the microwave as a routine
euthanasia mean for rabbits should be avoided [173].
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6. Kill traps
Kill traps are generally used for catching and killing free-ranging small mammals. They are therefore
used in the context of rabbits as game species or pest. The advantage of kill traps is that they do not
involve handling or restraint, which cause substantial amount of distress, especially in wild animals.
However, kill traps cannot guarantee a quick and distress-free death, which violates the criteria set for
euthanasia [18] (see Box 1. A). Moreover, they are very variable in their efficiency as various factors,
such as trigger type, size, or location influence the effectiveness of the method. In fact, steel-jaw traps
are rejected by the Australian veterinary association [65].
For free-ranging animals, live traps followed by another euthanasia method are preferable compared to
kill traps, but provoke distress as well since the animal is trapped and starved [18]. In conclusion, kill
traps do not constitute an advisable euthanasia method and should be therefore used only when no
other mean is possible.
V.
Methods acceptable for unconscious rabbits
only
1. Exsanguination
Exsanguination involves removing the major part of the blood contained in the body, which causes
rapid loss of consciousness. The onset of unconsciousness varies between species and may be function
of body weight as well [174]. In rabbits, exsanguination may be performed either by cutting the deeper
blood vessels of the neck, i.e. carotid artery and jugular vein, or inserting a syringe at the base of the
sternum at 30 to 45 degree and aspirate the blood [21], [96]. Cutting the deeper vessels or inserting a
syringe is obviously very painful if not performed on an anaesthetized animal. Moreover,
hypovolaemia10 and hanging the animal by the hind leg induces stress. Therefore, exsanguinations is
accepted only on fully-anaesthetised, sedated or stunned animals [21], [96], [175], [176].
2. Nitrogen/Argon
Nitrogen or Argon are odourless, colourless, inert and non-explosive gases [71], [109]. Their
inhalation may constitute a euthanasia method as these gases induce hypoxia by oxygen displacement
[21], [83]. However, this method fails to provoke rapid loss of consciousness which is an important
criterion for euthanasia [18]. A study showed that 39 % of rats became comatose only after 3 minutes
and some young animals did not die at all [22], [69], [129], [177], [178]. Moreover, signs of panic and
10
Reduced blood volume [16].
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distress such as attempts to escape, hyperventilation and convulsions, were observed in several species
[69], [127], [179]. Conversely, some studies testing pigs and chicken with argon did not find any sign
of distress because the animals were unconscious when convulsions and death took place [111], [180].
Note that after loss of consciousness, some animals euthanaized with Nitrogen presented convulsions,
gasps, vocalizations and tremors, which are aesthetically undesired [181].
Argon appears to be less aversive than CO2, which is a method accepted without anaesthesia [109],
[128]. As it appears to be non-distressful for some species and as it provokes death rather rapidly (e.g.
66sec for chickens) it is recommended by some authors [109], [111], [180]. Argon is heavier than air
and is thus safe for the personnel. It is however more expensive than other gases used for euthanasia,
such as CO2 [18], [109].
Nitrogen was found to induce death after 5 min in dogs and rats. Prior to unconsciousness, behavioural
signs of distress, such as vocalizations, were noticed. The same is true for rabbits [127], [181], [182].
However, other studies concluded that nitrogen is not aversive to cats and dogs since no fear response
was found when placed in the cage where induction occurred.
To conclude, one can say that the method using nitrogen of argon is not acceptable without
anaesthesia or prior sedation since several studies showed that it is distressful in some species [18],
[21]. However, sedation or anaesthesia may delay death and a small volume of O2 induces immediate
recovery [18]. These facts account for a total disqualification of the argon/nitrogen method.
3. Potassium chloride (KCl)
Potassium chloride is the unique agent used exclusively for euthanasia [17]. It is a cardiotoxic
substance provoking cardiac failure and death triggered by potassium ion [17], [183], [184]. Death is
accompanied by gasps, vocalizations, and convulsions [83], [183] which may occur shortly after
injection [18] and are aesthetically unpleasant [21]. In some cases, enlargement of organs is observed
[17].
This method is appreciated in livestock or free-ranging animals since no risk of intoxication due to
carcass consumption is present with this technique [183], [184]. However, because of the unpleasant
side-effects cited above, the method should be applied only in fully-anaesthetized animals. The
operator must be experienced in assessing surgical plane of anaesthesia, i.e. loss of consciousness, lack
of reflex motor response, lack of response to noxious stimuli [18].
4. Air embolism
This method consists of i.v. injection of 5-50ml/kg of air [21], [83] and has been used in the rabbit
[90]. This procedure causes rapid death but convulsions, opisthotonos and vocalizations occur
35 Master Thesis, Utrecht University
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regularly which suggest that the procedure is painful [21], [83]. Additionally, the procedure appears to
be an unreliable way of inducing death [21].
5. Chloral hydrate
This compound involves gradual depression of the respiratory centres and leads ultimately to death by
hypoxemia. As vocalizations, gasps, muscle spasms may occur prior to the onset of unconsciousness,
animals need to be anaesthetized or sedated beforehand. Note that several guidelines completely reject
the use of this method [83] and that this technique involves aesthetically unwanted side-effects [18].
VI.
Methods not accepted for rabbits
Some killing methods are rejected as euthanasia means because they do not comply with the criteria
set for euthanasia and induce distress. The following methods are not accepted for rabbits: ether
inhalation, as it is slow acting, irritant, explosive and flammable [30], [38]; rapid freezing, since death
is not immediate [21]; chloroform, as rabbits react aversively [30]; hydrogen cyanic gas, as it may
cause very strong convulsions and seizures and is dangerous for the personnel [30], [83];
metoxyflurane as its induction is very slow and chances of recovery are very high [18], [83].
Cyclopropane appears to be a quick and humane method but is very hazardous for the operators [83].
Nitrous oxide is sometimes accepted with reservation in rabbits [30] but should be rejected as it does
not induce any form of anaesthesia and hypoxemia may occur prior to cardiac and respiratory arrest
causing thereby anxiety [18], [83]. Similarly, Ketamine hydrochloride which produces “extensive
muscle contraction” and vocalizations, is accepted with reservations provided the rabbit is correctly
pre-treated with sedatives [30] but should be rejected on welfare grounds.
The use of ketamine alone, magnesium sulphate, potassium chloride without anaesthesia is not
acceptable for rabbit euthanasia [30]. Trichloroethylene, hypothermia, magnesium sulphate,
decompression, asphyxia, neuromuscular blocking agents, drowning, hydrogen cyanide gas,
hydrocyanic acid, nicotine and strychnine, are additional methods considered as non-acceptable for
euthanasia of rabbits [83].
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Chapter IV
Normative reflection
When euthanizing healthy but unwanted animals in laboratory settings or abattoirs, ethical
considerations need to be addressed. Firstly, because professionals involved with animal killing such
as farmers, zoo technicians or veterinarians have profound ethical concerns about the act of
euthanasia. Secondly, because if judgments of what is right and wrong remain non-reflected and are
based on feelings only, these moral judgments will not be stable and univocal. This latter fact leads to
the problem of double standards. Such standards are “morally objectionable and logically
indefensible” [185]. Moreover, although prior to the 20th century people showed poor concern for
animals suffering because of inter alia their own sufferings [186] and poorer biological knowledge,
the current society shows greater concern for animal welfare including animal euthanasia, slaughtering
and culling [12], [187], [188]. The concern is even stronger among animal owners and animal welfare
professionals [12]. One of the reasons put forward by certain authors for this increase in animal
welfare concern is the decreased occurrence of human suffering in modern western societies [186].
However, it is believed that the change in the moral standing of animals constitutes the main
underlying reason. Indeed, in the 18th century, the philosopher J. Bentham already questioned the
linguistic and reasoning abilities as criteria for moral consideration taking infants as counter-example.
He suggested the criterion of sentience allowing thereby animals entering the moral circle. His
argument is very well phrased is his famous quote: “The question is not, Can they reason?, nor, Can
they talk? but Can they suffer?” [185]. As a consequence of the latter shift of criteria, an improved
economical situation and a substantially deeper knowledge on the biology of animals, the public
concern about animal welfare increased. This increase results in new questions and problems of how
to assess welfare and weigh this value against other moral and societal values. Therefore, there is a
pronounced societal call for an ethical framework that would be action guiding for animal welfarerelated cases, including issues regarding euthanasia, slaughtering or culling of animals.
I.
Animal Welfare and Ethics
Before starting with the ethical reflection about euthanasia and how the method chosen differs
between contexts for a single species, it is important to clarify the relationship between welfare and
ethics since both are intermingled [189], [190].
First of all, the fact of being concerned by animal welfare and focusing on the issue already
acknowledges the moral importance of the latter concept, which shows a first link between animal
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welfare and ethics. From this latter statement, one may wonder why animal welfare should be
considered morally important [189].
A second link between animal welfare and ethics is that the concept of animal welfare has a normative
aspect. Indeed, it varies according to different factors, and inter alia the factor of ethical views that
moral agents hold on animal use (see box 1.B). Different agents will conceptualize animal welfare
differently. Some may define animal welfare on a functional basis, i.e. determined by the ability of an
animal to cope with a situation. Others may ground their assessment of welfare on feelings, i.e. how an
animal will feel in a given situation. Finally, some moral agents will believe that animal welfare is
nature-based, thus, what is in nature is the reference for the assessment of animal welfare [191].
Bovenkerk and Meijboom (2013) showed that next to the normative aspect of animal welfare
definition, the process of measuring and weighing animal welfare (against other interests) also
involves normative aspects. Indeed, measuring welfare relies on empirical data. The manner these data
are acquired is influenced by the normative assumptions and personal ethical framework that the
scientist has. One scientist will focus on certain parameters and another on different parameters (e.g.
stress for feeling-based assumptions, or natural behaviour for nature-based assumptions) in order to
measure the same matter, namely animal welfare. Finally, one’s ethical framework will also determine
one’s duty of care for the welfare of an animal which constitutes another example of the connection
between animal welfare and ethics [189].
The animal welfare field is also intermingled with ethics because it faces moral dilemmas very
regularly [189] (e.g the issue of euthanasia). Moreover, some freedoms which insure welfare, may
conflict with each other (e.g. exploring a new territory is stressful) [27]. An ethical framework is
therefore needed to structure ethical discussions. The Dutch Animal welfare council (RDA) recently
developed such a framework [192]. The latter aims to identify relevant ethical issues and what should
be done from a moral perspective to resolve these issues.
As suggested in Ohl & Van der Staay (2012), ethical consideration of animal welfare is influenced by
scientific knowledge and the morality of the society. Public morality is based on three elements. First,
morality often starts with moral intuitions, i.e. feelings or emotions that, for instance, mistreating is
bad or that animals can be harmed [189]. The importance of moral intuition is debated in ethical
theory. Authors, such as Frey or Singer, stand against including moral emotion into ethics [193].
Secondly, morality consists of facts, e.g. people being confronted with suffering of animals and
empirical proofs that animals can experience pain. Finally, morality is based on ethical principles,
such as the principle of respect for animals’ inherent worth [194], the principle of integrity, or the
principle of respect for life [195]. However, one can easily recognize that the question about which
principles should included in the moral discussion about animal use and which not; may be subject to
debate. Facing this debate, one could conclude that there is a need for a consensual societal moral
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guidance regarding animal use. To achieve this consensus, it is important to develop theoretical ethical
frameworks such as the RDA’s one, and it is also worth looking at general principles such as the one
developed by The National Aeronautics and Space Administration (NASA) from the United-States,
namely principles of Respect for life, Societal benefit and Non-Maleficence11 [196].
Principles, intuition and facts are interacting with each other in a process of moral reflection. In fact,
they are discussed prior moral judgments are achieved [197]. An ethical issue, such as different
methods of animal euthanasia across contexts of animal use, often starts with the intuition that
“something is wrong”. It is the first sign of a potential normative problem. The moral principles and
values that a person has, can justify the first intuition. Afterwards, it is worth looking at facts, and
whether the intuition is adequate to the facts and whether the facts do violate important societal values
and principles. The process where these three elements interact is a triangle of moral reflection and is
depicted in Figure 3. In order to conclude on a critical moral judgement, a so-called “Reflective
Equilibrium” needs to be reached [197] after moral reflection. This triangle of moral reflection can
raise fundamental moral questions: Do we have to care about animal welfare? If yes, is it conflicting
with other interests? If yes, How to weight interests? (see Fig 1 in Ohl & Van der Staay, 2012). With
respect to these questions, several ethical views exist to define our duties to animals and they can help
us to weight interests in moral dilemmas regarding animal welfare (see section Chapter IV.III).
Figure 3: Reflective Triangle showing the interrelations between Intuitions, Facts ant Principles (Dutch Ministry of Economic
Affairs, Agriculture and Innovation, 2011)
11
Minimization of pain, distress and suffering is a moral imperative [196]
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Finally, the ambivalence of the concept of animal welfare creates an urge for common action
guidelines. To achieve this aim, empirical scientific research about animal welfare needs a normative
framework showing thereby a last connection between animal welfare and ethics [189].
All in all, the process of euthanasia, being a matter of animal welfare, is therefore intermingled with
ethics as well. This latter fact explains thus that besides the biological analysis of different euthanasia
methods across contexts, a normative discussion about the assumptions of euthanasia takes place in
the present review.
II.
Plurality in ethical evaluation of animals
The major issue with the concept of animal welfare is that, the moral evaluation of welfare differs
between, inter alia culture, regions, time [25], [26]. In the previous section, it has been shown that the
concept of animal welfare and ethics are closely connected. Because one may argue that each person
has its own personal ethical framework, one may argue that the concept of animal welfare varies also
from one person to another. The latter variability leads to a certain plurality of moral evaluation
concerning animals. Consequently, animals will be evaluated on normative grounds differently from
one country to another or one decade to another, which seems intuitively aberrant. Certain species will
also be valued differently than others. However, the most striking ethical aberration is that within one
animal species, members will be valued differently across contexts [198]. As ethical evaluation varies
between contexts, the duty to maintain high welfare status may vary accordingly. Hence, the method
of preference for euthanasia may vary across contexts as well.
However, being it a pest or a pet animal, the intrinsic value of the animal is identical. Webster (1994)
phrased it well: “a rat is a rat whether we define it as vermin or as pet”. Intuitively, it appears to be
morally wrong to use different methods of euthanasia in different contexts for the same animal
species. This negative intuition is the first sign of an ethical issue that needs to be tackled.
In the contexts of euthanasia methods, one could more generally ask “Do we have to care about the
animals we kill? To answer this question another more fundamental question needs to be resolved:
Should we morally consider non-human beings and thus recognize that these beings can be wronged
morally ?[200]. Indeed, the issue about euthanasia methods across contexts is connected, via its
interaction with ethics, to the basic ethical considerations about the moral status of animals [189].
Several ethical views on the moral status of animals that are relevant to the present issue are developed
in the following section.
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III.
2013
Different ethical views on animal use
The very influential christian theologian Thomas Aquinas stated that animals have no moral status and
are to be used by humans [201]. This anthropomorphic view where “man has no duties towards
animals” was confirmed in the 19th century by the Pope Pius IX. Therefore, most of the European
societies with catholic background have a more instrumental view about animals compared to AngloSaxon societies with protestant background, which were the first to care about animal welfare [186].
According to Aquinas’ view, animals have no moral status, it is thus not morally wrong to kill them in
whichever manner possible. A lack of coherence in the manner used for euthanasia across contexts is
thus unlikely to be problematic neither.
The Kantian view suggests that the personhood, i.e. the representation of “I”, is the criterion to enter
the circle of moral consideration [202]. A modern Kantian view suggests that the reflective structure
of consciousness, thus the fact of facing the problem of normativity, constitutes the criterion and thus,
does not include non-humans in the moral circle [203]. However Kant introduced the concept of
deontology which sets some moral principles independently to the whole group’s welfare [196]. Such
a moral principle could be, for instance, the life-centred Respect for Nature [204] that would be
relevant to the issue of this paper, namely variation in euthanasia methods across contexts for
members of the same species. However, the Kantian view does not attribute moral status to animals,
therefore, whichever principle is set in deontology, it does not apply for animals. Hence, there is no
duty to preserve their life or welfare status and inconsistency, again, does not appear to be
problematic.
Contractarianism sets another criterion. “Morality is defined as a sort of agreement among selfinterested persons, who have something to gain from entering into such agreement ” (see Sandøe,
2013a). Animals cannot keep agreements, so they do not enter the moral community. However, people
may behave nicely to animals because they like them, and it is in their interest to preserve what they
like. This latter fact explains why people will tend to be troubled by the suffering or euthanasia of their
favourite species (e.g. dog) and completely indifferent to the suffering of other (e.g. pigs). The way
animals are treated in many societies, i.e. as a mean to fulfil human interests, is reflected by the
contractarian view [185]. Going one step further, one may justify different euthanasia methods for the
same species across contexts. Indeed, people may be emotionally positively involved with pet rabbits;
be totally indifferent to rabbits housed in barren, overcrowded cages where they are considered merely
as commodities and may “hate” pest rabbits that destroy their garden or field. Therefore, applying
welfare-friendly euthanasia methods in context where people like the animal and let euthanasia
methods be driven by other interests than welfare in other contexts, seems consistent with
contractarianism.
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Nevertheless, the problem with the aforementioned criteria to enter the moral circle, i.e. capacity to
reflect morally, capacity to keep agreements, is that they exclude also the so-called “marginal
humans”, i.e. humans without self-reflective capacities, such as children, autisms or persons with
cognitive disorders. Therefore, utilitarians rejected these criteria. As cited earlier, Jeremy Bentham the father of utilitarianism- stated “The question is not, Can they reason? Nor, Can they talk? But,
can they suffer? [205]. The criterion set by utilitarians is sentience, and since animals are
acknowledged to be capable to feel pain, they are thus able to enter the moral circle. Sentient beings
have an interest to not suffer [206], and as they have an interest, it should be taken into account and
deserve equal consideration as the interests of humans [200]. In the utilitarian view, in order to
determine an ethically justifiable action, what matters in not the individual benefit but the overall
benefit of the group. Utilitarianism is coined an “action-oriented ethical theory” because as it may be
noticed, it focuses on the consequences of actions [196]. Therefore, the strength and nature of interests
matters, not whose interest they are [185], [200]. For utilitarians, the fact of killing an animal is not
morally wrong - provided it has lived and it is killed without suffering –because animals, which were
believed incapable of self-consciousness, do not have a personal interest in continuing their life. Their
interest is therefore not violated by death [185]. Following the utilitarian view, the method to kill an
animal has to have the highest welfare standards. Thus, applying different methods for euthanasia
across contexts does not seem morally right. Of course, one could argue that there is a conflict
between the method used for euthanasia and the interest of other moral agents. Indeed, if one method
would be recognised to have the highest welfare standards (let’s take pentobarbital as example) but
would contaminate the carcass, conflict between the animal’s interest in a painless death and the
humans’ interest to eat its meat could arise. The strength of each party’s interest and the number of
beneficiaries is both parties should be weighed in a moral reflection process.
A further approach starts at the rights of animals. This account is strongly connected to the writings of
Tom Regan, who integrates the notion of inherent value, dignity and inviolability of living beings
[206]. Animal rights supporters give inherent value to animals because animals experience life, and
their life and welfare matters to them. The principle of inherent and intrinsic value implies the
principle of respect and thus, subjects to life cannot be harmed. Death harms the subjects by depriving
them from what is good in life. The respect principle implies also that subjects have certain rights that
cannot be overweighed by the interest of the group [206]. Hence, the animal rights view considers that
animals should be treated as an end and not as a mean and reject thus all forms of animal use; they are
so-called “abolitionists” [185], [206]. The question of different euthanasia methods across contexts
does not hold in this view, as euthanasia per se is condemned.
A final and very relevant view for the issue of using different euthanasia method across contexts for a
single species is the relational view. It states that the value - and thus the treatment we reserve to an
animal and the duty of care we feel towards it - depends on our relationship with the animal. We won’t
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accept to kill our pet, but it is commonly accepted that farm animals are being killed. Animals differ in
their moral status according to the relationship they maintain with humans. The more intimate the
relationship, the stronger the care for the animal’s interest should be. This latter statement is in line
with the fact that, in our societies, we tend to care more about pets, especially our own pet, than farm
or laboratory animals [207]. This view is challenged by the issue of competing interests of animal
owners and animals. However, according to relational view defenders, caring for our animal is caring
for our own good. Indeed, caring for a cow is economically beneficial as it will live longer and be
more fertile. Caring for a dog provides us with good feelings when the dog is joyful in return. As
caring for animals we have a close relationship with, is in our self-interest, no conflict of interest exists
[185]. The relational view is somehow linked to the concept of sociozoological scale. In this concept,
animals are morally more or less important depending on many factors, such as their usefulness,
cuteness, their harmfulness or cultural and religious beliefs. This sociozoological scale plays the role
of defining the attitudes of humans towards animals and may ultimately lead to determine what
humans will feel to owe to a specific animal species. Nowadays, pets, i.e. dogs and cats, are on the top
of the scale. Indeed there are given names, whereas poultry is expressed as weight per area (e.g.
kg/m2). This scale is based on old tradition and prejudice, and is very objectionable ethically and
scientifically, but, unfortunately, it is part of social reality [207]. The fact of placing different species
above other and the human at the very top without a valid normative reason, has been called
“speciesism”. The idea of speciesism was developed by Peter Singer, a contemporary utilitarian
philosopher [185], [196]. The sociozoological scale tends to attribute different moral value to different
species. Our argument is that within each species, there is what one could call as “Intra-specific
contextual scale” where within a single species; an individual will be valued differently than another,
according to the context of the human-animal relationship. Following the relational view, it is clear
that the aspect of welfare will play a more important role in the choice of euthanasia method of pets
than in the choice of euthanasia method of pest rabbits. In our current way of dealing with farm
animals, i.e. without close human-animal relationship, welfare aspect may play a role in the euthanasia
methods chosen, but only when it is economically beneficial (e.g. better meat quality, meeting
consumer demand for high welfare standards, etc.). When it is not economically beneficial, the welfare
aspects will be overweighed by other aspects driven by other interests, such as rapidity of the
slaughtering method for an increased productivity.
Beyond the factor of human-animal relationship, some authors have noticed that humans’ attitudes
towards animals vary also with circumstances, such as inter alia the animal species, human features
(e.g. age, level of education, values, beliefs), the function of the animal and emotions (e.g. empathy,
identification, fear) [186], [208]. In each contexts of animal use, either beliefs, emotions or function
are the explanatory factors of one’s attitude toward animals. For instance, farm animals are considered
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for their purpose, pets are considered for the emotional relationship with humans, and sacred animals
such as cows in India, or unclean pork, are considered due to people’s beliefs [186].
Of note, Animal philosophers such as Midgley and Sapontzis presented some “mixed” theories.
Midgley’s view is that animals’ interests count but only when all the humans ones are satisfied.
Indeed, she recognizes that “we are bond-forming creatures” [209] and suggests that “the needs of the
closer to us, have moral priority over the needs on those less close“ [206]. However, considering the
degree of bondedness as the factor determining the degree of moral consideration presents the danger
of unjust discrimination (e.g. racism).
The idea of degrees of moral status is well present in our society. Indeed, foetuses or animals are
considered to possess a moral status but to a less important degree than adult persons and that is why
abortion or animal use is tolerated. After an analysis on the “conceptual and normative options
regarding moral status”, DeGrazia concludes that the assumption that moral status is an “all-ornothing” concept has to be abandoned [210] and stands in favour of an “unequal consideration view”
[211]. In this view, the obligations towards certain beings may be lesser than to others. However,
which factors determine the degree of one’s moral status remains an ongoing debate. As shown with
the example of human foetuses, moral consideration within one species may differ according to
different factors (e.g. age or unborn status), thus within the species of rabbits it is not surprising that
some people attribute degrees of morality according to the context. Because criteria determining the
degree of moral status to be attributed to an individual are not consensual, one could set the degree of
human-rabbit relationship as the main factor correlating with the degree of morality attributed.
Following this line of thought it would be justified to apply different euthanasia methods across
contexts but the latter criterion is more than arguable.
IV.
Euthanasia and Welfare
Euthanasia of healthy but unwanted animals, violating moral principles such as “respect for life” or
“intrinsic value of living beings”, appears to certain individuals to be, by intuition, morally wrong
[212]. It is the first step of a needed moral reflection. A question that could be asked within this
process of moral reflection is whether death is a welfare issue. It is commonly agreed that death is not
a welfare issue [199], [213]. Indeed, being death is not per se a welfare issue as opposed to antemortem processes inducing death, i.e. euthanasia, that may result is substantial impairments in the
welfare of a still-alive, dying animal [26]. According to certain authors, as animals are believed to lack
time conceptualization, being euthanized sooner or later has no importance to them [214]. This
constitutes another argument that death is not a welfare issue.
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Conversely, certain philosophers such as Sapontzis, are persuaded that life is of crucial value for
living beings with interests [215]. Also, authors such as Yeates (2010) or Bruijnis (2013) stand for the
claim that death is a welfare issue. Yeates (2010) using a wide concept of welfare, i.e. welfare issues
being referred to animals’ interests, states that “an animal’s death may be a welfare issue insofar as it
leads to the exclusion of relevant positive states”. The latter statement depends on contexts and is thus
relevant in the present paper. Indeed, if the expected life was supposed to be characterized by positive
welfare states, death may frustrate animal’s interest by exuding the expected positive states and thus
be a welfare issue. However, if the expected life would be characterised by negative welfare states,
euthanasia may prevent further welfare impairments that would occur if the animal was not killed.
Hence, death would not be a welfare issue and would even be positive regarding welfare. As one can
see, the welfare implication of euthanasia depends on the surrounding framework because it is
determined by the welfare implications the extended life would have. The same way of thinking may
be applied for the euthanasia methods within contexts. Indeed, the welfare implications of one
euthanasia method could be evaluated in reference to the welfare implications if other methods were
used.
Bruijnis et al. (2013) addressed specifically the welfare issue of prolonged longevity when the
extended life is characterized by negative welfare states. Next to longevity being a partial indicator of
good welfare, Bruijnis et al. [212] showed that being alive is a prerequisite for experiencing welfare,
and that longevity is a preference that should be satisfied to ensure positive welfare. Indeed, longevity
“should be considered as a constitutive element of animal welfare”. This approach to moral reflection
enables to understand the prima facie intuition that killing is morally wrong. Animal welfare should be
handled in a way that integrates biological knowledge, moral norms, notion of time and future
opportunities for an animal to prosper [212].
The latter view raises a more general question regarding the morality of the practice of euthanasia in
rabbits in the context of production, research and pest control. Indeed, those animals have
opportunities to flourish if their life is extended. Pet rabbits are usually put down because of severe
health problems and they constitute the unique context where euthanasia is worth debating, according
to the latter view.
V.
Summary
In the present chapter it has been shown that animal welfare has become a societal concern over the
last years, which creates a need for societal guidelines concerning animal welfare. Besides a biological
analysis of a welfare issue, it has been shown that a strong normative reflection is needed since animal
welfare and ethics are intermingled concepts. The basic three components involved in the process of
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moral reflection have been detailed, namely intuition, facts and principles (see figure 3). Because of
the interconnection between ethics and animal welfare and because of the lack of consensus around the
latter concept, it has been demonstrated that a plurality of moral considerations of animals arises. This
includes variation in the values attributed to a single species across contexts which constitute an
intuitive moral aberration tackled in the present review. The moral consideration of animals is
different from one ethical view of animal use to another, as the criteria for acknowledging moral status
to animals differs. Different ethical views on animal use were detailed, outlining the relevance for the
topic of the present paper. Finally, a reflection on the morality of euthanasia and its relation to animal
welfare was developed.
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Chapter V
Discussion
The present review attempts to provide an overview of euthanasia methods used in rabbits, across
contexts, and to explore the issue of using different euthanasia methods for rabbits according to the
context. We have chosen to focus on the main euthanasia methods and the key contexts, which does
consequently not cover all existing methods in every single context. Also, due to the scarcity of
scientific information available regarding rabbit euthanasia in specific contexts, several parts of the
review rely on legislative texts or institutional guidelines. We are aware that these latter facts limit our
approach and we have taken it into account in our reflection and discussion. Note that for the sake of
intelligibility only euthanasia methods regarding adult rabbits are discussed.
Box 2: Discussion about key concepts
A. Animal Welfare concept
Although a specific definition of the concept of welfare has been chosen in section I.2 of the present
review, it was also mentioned that no consensus on a single definition of animal welfare has been reached. In
our opinion, this may be due to the fact that the concept of Animal Welfare maybe linked to the moral standing
attributed to animals, which is suggested to be, at least partly, determined by personal background and beliefs.
This later fact introduces thus a certain degree of variability in the Animal Welfare conceptualization. For
instance, one may notice a within-individual, variation in attitudes depending on the context and emotion
involved. This ambiguity gives rise to double-standards [185]. Animals perceived as “cute” are often more
valued than the ones that are seen dirty or ugly by humans, even if they are members of the same species. For
instance, a rat in his home cage will more often be considered cute whereas a rat foraging in the garbage will
disgust many people. On the whole, the variability around conceptualization of Animal Welfare leads to
instances of discrimination based on rather morally arguable criteria namely aesthetics or context. This fact
underlines the need for a common societal moral towards animals and a more consensual concept of Animal
Welfare.
Another consequence of the plurality of Animal Welfare conceptualization is that it gives rise to debate
about concepts that are connected with it. For instance, the issue of euthanasia depends on the definition of
Animal Welfare and since some authors, such as Fraser (1997) or Musschenga (2002) advocate a broader view
of welfare than the one used in the present review (see section I.2), the discussion around euthanasia changes.
Their view holds that, to the current concept of Animal Welfare (labelled “feeling well and functioning well”),
the concept of “living natural lives” should be integrated. According to them, Naturalness is a part of the
integrity of the animal and may be a reason for moral action; it is thus a component of Animal Welfare [216],
[217]. Following the latter line of thought and as the concept of welfare is involved in the euthanasia process; it
would be coherent to integrate “Naturalness” to the euthanasia process. However, in the nature, dying may be a
violent, stressful and painful process, and it is not clear whether the latter process is better, from a welfare
perspective, than euthanasia in artificial settings. To answer this, a more profound ethical reflection is needed
and the unique clear statement that can be made is that euthanasia is a welfare issue and its evaluation will
depend on the definition of welfare employed.
B. Insensibility and unconsciousness
These concepts are used in an exchangeable manner in the literature. However, it is questionable whether
unconsciousness implies insensibility in every case, since during sleeping –a form of unconsciousness– a part
of the brain is still sensible to external stimuli. The relationship between both concepts would need some
clarification since unconsciousness is the key criterion in “humane” euthanasia process, but this is beyond the
scope of this paper.
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C. Humane killing
Note that throughout the present review, the word “humane” was used as referring to the most desirable in
terms of welfare. However, since the Cambridge Advanced Learner’s Dictionary defines it as “showing
kindness, care, and sympathy towards others, especially to those who are suffering” [218], it appears difficult
to show kindness and sympathy in killing without consent. Indeed, without consent, it is difficult to decide
whether an animal’s need to avoid suffering outweighs its need to avoid death. Another view holds that
“humane” implies fitting our humanity, or in other words, fitting our human morality. Therefore, the
underlying question is whether animals are included in one’s moral reasoning. If the answer is no, then killing
animals may be humane. If the answer is yes, then, at least, welfare should be a criterion in the process of
killing [219]
I.
Discussion per contexts of animal use
1. The Rabbit as Meat animal
As explained in the chapter III where electronarcosis (see chapter 3.II), electrocution (see chapter
3.IV.2) and exsanguination (see Chapter 3.V.1) were tackled, the euthanasia method commonly used
in the meat industry, i.e. electronarcosis followed by exsanguination, does not seem worse than others
in terms of welfare. Indeed, except the restraint that can impact very badly the welfare of rabbits, the
correctly-applied method induces unconsciousness instantaneously and exsanguination provokes
immediate death. That is the theory. In practice, many factors contribute to systematic welfare
impairments.
Firstly, the restraint technique used consists of hanging rabbits by the hind leg. It is undoubtedly very
stressful and questions arise on the reasons why this restraint method is authorized for rabbits, while it
is forbidden for other species by the council directive for the protection of animals at the time of
slaughter or killing [57]. As it is shown in the chapter 3.I.1, pre-euthanasia factors are crucial for the
welfare of animals. Hence the practice of hanging by the hind leg goes against the purpose of the EC
Directive. What is more, stress has a negative impact on meat quality [23], thus hanging the rabbits
prior stunning is not economically optimal neither.
Secondly, electrodes use for stunning were found to be incorrectly applied in 10% of cases and rabbits
recovered before being exsanguinated, in 2% of cases, rabbits. Also, 10% of animals were
electrocuted several times [4]. This latter fact may be explained by a conflict that arises between
operators’ safety and the welfare of rabbits. The V-shaped electrodes used for the rabbit should
provide a very high voltage electrical current to surmount the isolation characteristics of fur and to
reach immediate insensibility in the rabbit. However, the greater the voltage used, the greater the
danger for the operator [54].
The incorrect application of the electronarcosis & exsanguination technique questions the level of
knowledge and skilfulness – mandatory by Article 7 of the Council directive 93/119/EC – of the
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operators [57]. The fact that some animals had forelimbs stuck between the head and the electrode
confirms the poor performance of the operators or even a lack of care which may reflect a low moral
consideration given to animals [207].
As large numbers of rabbits are slaughtered using this technique, even low percentages of incorrect
application of the method represents a very large number of animals that suffered severe pain and
distress just before death. The latter fact completely discredits this currently used method. However,
despite the high degree of procedural errors with terrible welfare implications uncovered [4],
electrical stunning with exsanguination remains the method of choice in the context of meat
production. This illustrates that other factors outweigh animal welfare in the choice of euthanasia
method in this context, and suggests that animals in this context may have a devalued moral status to
the level of “commodities”. This is debatable and we believe that this debate goes beyond welfare.
This idea is developed later on.
2. The Rabbit as Fur animal
Fur rabbits are commonly slaughtered by electronarcosis and CD [163]. In chapter 3 section IV.3, it
has been shown that CD is not a satisfying method for euthanasia, since it carries a high percentage of
failures [18], [30], [164].
As explained previously, the carcass of fur rabbits is not used for its meat. This would allow for the
use of injectable drugs such as pentobarbital overdose – identified by some authors as the most
desirable euthanasia method [17], [18], [21], [83]. Thus, the question arises why the industry does not
switch to methods with supposedly higher welfare standards.
The answer may lie in the conflict that exists between rabbits’ interests and legitimate human interests
such as economic value. From the current practice used for fur rabbit euthanasia, it is clear that animal
welfare is not the major determinant of the euthanasia method chosen, and other factors outweigh
rabbits’ interest for high welfare standards. However, in our view, animal welfare should drive the
practices in the context of animal use because animals are sentient beings and have thus a moral
standing; and a great extent of their interests is already violated by their use per se. The use of
animals, especially for questionable human interests such as fur wearing, is debatable and deserves a
more profound ethical reflection which is beyond the scope of the present review. Because of the
intrinsic moral standing of fur rabbits, because of the questionability of the purpose of animal use and
because of a lower societal acceptance of the fur industry practices, we suggest to diminish the
numbers of rabbits used and, more importantly, to refine currently used euthanasia methods to insure
high welfare standards.
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An idea would be to merge the rabbit meat and fur industry and to agree on a euthanasia method that
preserves high welfare standards and that does not contaminate the carcass. This method could be
captive bolt stunning followed by potassium chloride administration. Indeed, given that rabbits
possess a fragile skeleton [220] the use of captive bolt seems an appropriate way for stunning as it
requires only correct restrain and positioning as opposed to electronarcosis, which depends on many
other factors such as amperage, voltage, duration, etc. Moreover, it supposedly kills the animal so
there is no chance for recovery from stunning before induction of death by another method. After
stunning, potassium chloride could be administered because it is a very reliable death induction
method and does not contaminate the carcass [183], [184].
In every scenario, there is still an urge to drastically improve current practices in the fur and meat
industry. Whatever method is chosen, a strong focus shall be put on the quality of operators’
performance in order to comply in practice with what the procedures foresee in theory. For instance,
regarding electronarcosis with exsanguination, the theory foresees to put only the head of the rabbit
between the electrodes. In practice, a forelimb or an ear are regularly stuck there as well [4], and this
should be prevented. Additionally,an effort shall be made regarding the peri-euthanasia stressors (e.g.
limit transport by choosing local abattoirs).
In conclusion, the fur industry presents the same dangers as the meat industry regarding the potential
consideration of animals as commodities, depriving them, at least partly, from the moral standing
attributed nowadays to sentient beings. As mentioned above, in the context of factory farming for fur
or meat, animal welfare does not appear to play a prevailing role in the choice of the euthanasia
method in daily practice, as it conflicts with other human interests. Similarly to the context of meat
production, we believe that for fur rabbits, the issue of animal welfare at the time of slaughter goes
beyond the method chosen for euthanasia. This view will be developed in a following section.
3. The Rabbit as Lab animal
Animal use in laboratories is an ongoing debate between different views in the ethics of animals use
because it is a moral dilemma [221]. Although animal testing - at least to some extent - is approved by
the part of the population that adopts a utilitarian-like view or a deontological view (i.e. using animals
is the lesser evil), people are extremely concerned by the fact of using millions of animals four our
own interest [207], especially as it results very often in very poor outcomes. Moreover, some authors
argue that in the biomedical field, there is a “political culture in which many or most animal
researchers and their supporters do not engage in sustained critical thinking about the moral status of
animals and their basic justification for animal research”. Most of animal ethics philosophers
criticize the latter tendency concluding that the use of animal for scientific research is objectionable
[211]. If the latter tendency is true, than it is crucial that lab animals benefit from a protection at the
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legislative level (e.g. Directive 2010/63/EU, Good Laboratory Practice of United-States Food and
Drug Administration, etc.) and that much effort is put in the implementation of the 3Rs, namely
Replacement, Reduction and Refinement [222]. Clearly, the complete replacement of animals by
other techniques for scientific experimentation would dismiss the ethical issue of euthanasia of lab
animals, such as rabbits. However, this is not the current reality, yet. A reduction of the number of
animals being used is of course desirable, but affecting the welfare of less animals is not “less bad” in
terms of welfare, and does not constitute a solution. Thus, the focus must hold principally on
refinements of the procedures used, including refinement of euthanasia methods.
Nowadays, the methods used for euthanasia of small lab animals vary largely between laboratories
and biotechnicians as no consensus has been reached on the welfare implications of each method and
contradictory findings about each method are present in the literature (e.g. pre-filled chambers versus
gradual induction chamber CO2).
This variability is also explained by the fact that the choice of the method is also driven by inter alia,
the research question, experimental procedures (e.g. animals habituated to injections), devices
available. Although the methods described below are the most regularly used in the laboratory
context, they may potentially apply to other contexts. Similarly, the methods described in the previous
section may also be used in the present context (e.g. cervical dislocation).
Performing euthanasia using CO2 is very common in laboratory settings. However, although many
conflicting results are found in the literature, we conclude that CO2 euthanasia should not be used in
rabbits since they were seen to react aversively to gases and may cope with hypercapnia. This would
thus result in a painful and slow death. The same holds for other gases, such as inhalant anaesthetics,
namely Nitrogen or Argon.
Although Carbon Monoxide (CO) is a gas, it is worth to study it further for rabbit euthanasia purpose
because it appears to be undetectable for several animal species. Also, very low concentrations are
needed for euthanasia (around 4-6%) which may constitute an advantage for non-detectability.
Additionally, CO is a cumulative gas thus clinical signs appear with delay limiting thereby aversive
reactions [18], [131], [147]. Carbon monoxide would enable euthanasia in the home cage and solve
the issue of restraint which greatly impairs rabbits’ welfare since, being prey species; rabbits are
genuinely uncomfortable with restraint. However, the use of CO as euthanasia method is often
discarded by many authors because it represents a substantial danger to the personnel as it is virtually
undetectable. To us, this kind of rejection appears wrong because the welfare of the animal should
prevail in the choice of the method when solutions to control safety of the personnel are available (e.g.
concentration monitors, ventilation systems, etc).
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Decapitation is not advised in rabbits because these are often larger than1kg and have a very muscular
neck [223]. Moreover there is a clear lack of knowledge about its welfare implications (see Chapter 3.
IV. 4) and future investigations on, for instance, the meaning of an active EEG after decapitation, are
needed.
Overdose of sodium pentobarbital is also regularly used and further described in the following
section. It is especially advised when subjects are habituated to injections and venipuncture.
Air embolism and chloral hydrate, even if performed on unconscious rabbits, should be totally
abandoned since they carry the risk of using it on a not-well-anaesthetised animal and other methods,
such as pentobarbital injection, have been proven to provide higher welfare standards.
In conclusion, we can state that although lab animals are clearly considered instrumentally [186], i.e.
to provide reliable results during experimentation, the welfare aspects of these animals are taken more
and more into consideration. Besides the greater societal concerns, scientists recognized that “most
humane possible treatments (…) are a prerequisite for successful animal experiments” [222].
Therefore, where possible, the method used for euthanasia tries to impair to a minimum extent the
welfare of animals being it for moral reasons, or for more reliable experimental outcomes.
4. The Rabbit as Pet animal
As stated in the book Ethics of Animal Use, “the purpose of pet ownership is to have a life with the
animal where the animal is happy”. However, good intentions do not prevent welfare and moral
problems to arise in pet animals [207] and one moral problem might be euthanasia. The particularity
of this type of human-animal relationship is the strong emotional attachment that humans have
towards their companion [186], [207]. This leads us to assume that the welfare of one particular
animal will be an important factor driving the euthanasia method chosen by its owner.
Sodium pentobarbital injection is considered by many authors as the least welfare-impairing
euthanasia method as it induces a rapid loss of consciousness, analgesia followed by anaesthesia and a
wrong application of the methods does not put tremendously the welfare at stake [17], [18], [21], [83].
The fact that this drug is used in humans, i.e. physician-assisted suicide or capital punishment [224],
[225], accounts for the view that this euthanasia method is the most desirable in terms of welfare.
Moreover, sodium pentobarbital appears to induce some emotionally positive effects as it is subject to
human drug-abuse because it produces effects similar to ethanol intoxication (inter alia euphoria and
decreased anxiety).
Interestingly, sodium pentobarbital overdose injection is the most common method to put down pet
animals. Because sodium pentobarbital is believed by many to be the animal-friendliest method, this
illustrates that in the context of pets, animal welfare plays a major role. For pet rabbits, this method
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seems appropriate as these animals are habituated to humans, to restraint, and hopefully, to medical
care. Moreover, the presence of the owner during the injection can, in certain cases, further decrease
the amount of stress induced by the procedure.
However, the stress could be even further decreased, and thus the welfare further enhanced, by
replacing injectable solutions with other forms of administration that exist for this drug (e.g. drinkable
solution for human physician-assisted suicide [224] or powders to be mixed with food). One can
wonder why these means of administration, which would solve the major flaw in this method, i.e.
need for restraint and pain due to venipuncture, are currently not used. One hypothesis is that the dose
administered is less controllable, but, according to us, several procedures (e.g. mixing the required
dose with high amount of very attractive food) could overcome the problem. Therefore, it appears that
although welfare is an important factor in the method chosen for euthanasia in the context of pet
animals, it is not the unique driver of the choice since other ways of administration that appear less
aversive than injection, exist and are applied in humans (e.g. drinkable solution).
We can thus conclude that due to a stronger emotional human-rabbit bond in the context of pet
rabbits, animal welfare plays, in this context, a more important role in the euthanasia method chosen
than in other contexts. We believe that this latter statement may be, at least partly, explained by the
fact that in the context of pets, human interests (e.g. companionship) are somehow linked to the
welfare of the animal. Because welfare is not the unique determinant factor for euthanasia method, we
account for a relational view of animal use in the context of pet animals, indeed, the between-human
relationship in stronger than human-pets ones, thus the importance of welfare as factor seem to vary
accordingly.
5. The Rabbit as wildlife – free-range and pest
Wild rabbits may be hunted, considered as pest or games species. However, in some cultures, respect
for nature and thus alls its creatures, is part of societal values and beliefs. In the western modern
societies, there is an increasing fascination for nature. This fascination may be due to an emotional
factor of identification or empathy [186] or to the notion that nature has an intrinsic worth [195].
Hence, there is a growing concern about how the wild populations are regulated and how “pest”
populations are controlled. The particularity of this context is that animals are not accustomed to
human contact, and restraint is thus even more aversive in wildlife, than in other contexts.
A method that does not require restraint is poisoning [65]. However, some substances, such as sodium
pentobarbital, present the risk to poison the animal that consumes the carcass of the animal targeted.
Moreover, sodium pentobarbital is further discarded because of its current form of administration, i.e.
injection that requires restraint. Poisons such as pindone, sodium fluoroacetate of strychnine have
been used for population management, but as stated previously, these drugs have very negative
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welfare implications and they should not be used. Potassium chloride (KCl) is appreciated because it
does not present the risk of intoxication of other animals. However, this substance is cardiotoxic, it is
thus very distressful when administered without anaesthesia, which is the case with free-range
animals.
Kill traps, a common mean of killing wildlife, preserve animals from human contact but cases of noneffective killing leading to severe distress question the latter method. Live traps are often considered
better, in terms of welfare, but being trapped and starved, sometimes to death, involves a very large
amount of distress and accounts for the dismissal of this technique.
Two culling techniques that have not yet been mentioned in the present review are worth to be
discussed in the context of pest management, namely blow to the head and gun shooting. Provided it
is adequately adapted to the anatomical features, the blow to the head technique may be humane as a
single strong blow can produce immediate depression of the CNS. This technique requires a
sufficiently fragile skull and it is thus accepted for neonatal animals only [18]. Besides being nonsuited for adult rabbits, the major pitfalls of the method are the necessity for restraint and the
necessity for well-trained operators. Gun shooting presents the advantage of avoiding restraint. The
principle is similar to the one of captive bolt, i.e. penetration of the bullet with immediate destruction
of the brain and CNS depression. The drawback of this method is that it requires very high precision if
the shooting takes place from a certain distance. Moreover, no control whatsoever on the power of the
shot is available [18]. Finally, as gunshot is not a discrete method. This may induce a substantial
amount of fear in the whole rabbit population. All in all, the two latter techniques present important
welfare flaws if not correctly applied, and are not efficient for population control as they kill animals
one by one [65].
A method that has been showed to be efficient in population control is the use of myxomatosis virus
that culled 99.8% of Australian rabbit population. However, although efficient, not requiring any
restraint, and believed to be rabbit-specific, this method has been recognized to be painful. Nowadays,
the RCD virus – believed less painful –is used. Despite recognizing the bad welfare consequences of
myxomatosis virus, the Australian Veterinary Association (AVA) argued that it is a necessary part of
an active control campaign [65].
The latter statement deserves to be discussed. The question whether it is morally right to tolerate a
certain amount of distress in order to achieve a goal already morally questionable, i.e. killing large
numbers of animals, needs to be addressed.
Firstly, it has to be borne in mind that the concept of “pest species” is not absolute. In our view, it is
rather relative since our judgement of value of a species remains subjective. For instance, what is
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considered as pest by (some) humans will not be considered as pest by a species living in symbiosis
with it.
Secondly, it is needed to reflect on the moral standing of pest animals. Although moral standing is
intrinsically independent of societal acceptance [219], in practice much is defined by societal
acceptance of one’s moral status. From what has been seen from the different techniques used, not
much attention is paid to animal welfare within the context of pest rabbits, the public acceptance of
the moral status of pest animals appears to be rather low. This is corroborated by the fact that
companies specialized in pest management do not advertise much the “humanity” of their methods
(with the exception of live traps), and we believe that if they do not, it is because there is no strong
consumer’s demand for it. This appears to us pretty aberrant when the pest control is about the same
species as people’s beloved pet. In our opinion, this reflects a relational view of animal use. AVA in
its declarations adopts a more utilitarian approach by weighting the interests of both parties and
concluding that some amount of suffering for rabbits is a necessary evil in their population control.
In conclusion, it appears that, what is in a human perspective considered as pest, does not deserve, in
a relational view, a high moral status. Therefore, the methods used do not take the welfare aspect
much into consideration. In a more utilitarian view, the moral status of the pest species is recognized
but humans’ interests outweigh rabbits’ ones and the end justifies the means.
II.
Discussion across contexts of animal use
One of the criteria for euthanasia is to produce an immediate loss of consciousness and the quickest
death possible. One can wonder whether this criterion is desirable in terms of welfare. Indeed, certain
methods inducing gradual, and thus slower death, appear to be potentially less distressful (e.g. gradual
induction of CO2 in the chamber; mixing CO2 with O2) [71]. Hence, rapidity of action as criterion for
euthanasia should be reconsidered. Indeed, rapidity can cause violent onset of effects which prevents
smoothness of the procedure and may be anxiogenic. In our view, when the welfare implications of a
slow method are “less bad” than the ones causing rapid death, the criterion of rapidity should not
disqualify them from being “humane”. However, this matter is debatable.
More generally, the humanity of each method developed in the present paper is debatable since, as
mentioned before, science is intermingled with ethics. In fact, ethics is inherent to the concept of
euthanasia and play a role at three different levels in the present debate.
First, it has to be determined whether humans should care about the interests of the animals and if so,
why. This question is clearly related to the view on the moral standing of animals. Because there is a
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plurality of answers to this question, the importance granted to animal welfare will be variable which
will result in a variety of “preferred euthanasia methods”.
When moral standing is recognized in animals, then ethics play a role at a second level: what are the
duties implied by morally considering animals? In the frame of the present topic, humane killing in
general and animal welfare aspects during euthanasia in particular, are relevant to the discussion.
Clearly, science faces the complex challenge of determining a preferred method, in terms of welfare,
for euthanasia. However, many experimental studies find different or even conflicting results, which
complicates the task. To us, this different results are due to the multiplicity of factors and
combinations (e.g. transport, familiarity with the handlers, testing environment, etc.) that affect the
experimental outcomes.
When one recognizes that animal welfare aspect should be considered in the choice of euthanasia
method, ethics play a role at a third level, namely in the reflection whether it is possible to
euthananise an animal without harming its interests. At that level, an ethical reflection on the value of
the aim for which the animals are killed takes place as well. Due to the interrelationship between
science and ethics, a large variety of conclusions can be drawn as to the preferred euthanasia method.
It is noteworthy that the notion of what can currently be the best practice12 (e.g. the best euthanasia
method), changes with scientific knowledge and societal ethics and those factors are time-dependent.
Hence, it has to be borne in mind that our current belief about which method is the best, is relative,
and what is currently considered the best method for euthanasia can degrade in the future [20]. In
conclusion, it is difficult to find an absolute preferred method in terms of welfare. However, for the
purpose of the present paper, an attempt is made.
An interesting way to assess the method that is considered the most “humane” is to look at the ones
that are used in humans, i.e. capital punishment, euthanasia, and physician-assisted suicide. It is seen
that in Europe and United-States, the most common method consists of barbiturate injection possibly
followed by administration of pancuronium, a paralyzing drug resulting in cardiac arrest. In some
states of America, such as Ohio, sodium pentobarbital is the unique drug used for capital punishment
since 2011 [226]. In the Netherlands, a drinkable solution of barbiturate is offered for physicianassisted suicide [227]. These facts account for the idea that the use of barbiturate is one of the most
compassionate ways to put down animals, including humans. Many experts agree with the latter
statement [17], [18], [21], [83]. Indeed, besides the rapidity, sodium pentobarbital fulfils other criteria
for euthanasia. One of them is the ease of administration and the lack of important detrimental
consequences of a poor performance of the operator. Sodium pentobarbital needs a simple i.v.
injection compared to other methods such as cervical dislocation, that requires expert skills, and
12
Practice that apply the state-of-art techniques and methodologies and is usually better than the industry and
societal standards [20].
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where the suffering engendered by an operating error is obvious. Another criterion fulfilled is
aesthetics. However, it has to be borne in mind that what appears aesthetic does not imply that it is
better for animal welfare [30]. Aesthetics is a relevant criterion only because it may influence the
behaviour and care of operators and change their relationship with animals, with thus possible welfare
implications. The major flaw of the method is the contamination of the carcass and the need for
restraint in case of injectable solutions. To make it usable in other contexts than pet animals, more
research is needed on the application of alternative means of administration. Also, barbiturate drug
mixtures, such as PF-3, should be further evaluated.
If sodium pentobarbital is considered the euthanasia method of choice in terms of welfare, one can
easily conclude that in the majority of contexts, the process of euthanasia is not the most animalfriendly since other euthanasia methods are employed. Of course, different factors (e.g. habituation to
restraint) and interests (e.g. economic efficiency, scientific results) define each contexts and whether a
euthanasia method is applicable. For instance, in meat production, sodium pentobarbital is naturally
discarded because it would contaminate the carcass. As meat is the raison d’être of this context of
animal use, it will logically outweigh any other factor in the choice of the euthanasia method. Not
only between contexts, but also within context, many aspects will influence the choice of the
euthanasia method. For instance, in the context of research animals, drug contamination of the carcass
may constitute a problem is some experiments but not in others.
The section above, i.e. discussion per context of animal use, aimed to establish the importance granted
to animal welfare in the choice of the euthanasia method within each context. One can easily conclude
that there is a difference between contexts regarding the importance of animal welfare. Although a
logical explanation as to why certain methods are discarded in certain contexts (e.g. sodium
pentobarbital in meat production) may be found, it is unclear why the importance of animal welfare as
a factor determining the choice of the euthanasia method, differs so much from one context to
another. According to us, this is certainly linked to the fact that the moral standing of animals differs
from one context to another, which seems aberrant to us when the species remains the same across
contexts. Here, we recognize a relational approach to animal use, which, although generating some
support, appears to us to be morally wrong since we recognize the inherent worth of animals.
III.
Implications beyond welfare
Some items discussed in the present chapter, such as the use of rabbits for production, lead us to
believe that some aspects of the debate go beyond welfare. The use of animals, such as rabbits, in the
context of farming has always been instrumental [186]. This is not an issue when humanity does not
show care about animals for their own sake. However, two major changes occurred over years.
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Firstly, scientific advances have triggered a change in the view on the moral standing of animals. The
capacity of sentience is currently acknowledged in animals and a part of humanity does care about
animals for their own sake.
Secondly, the way of farming dramatically changed over the last decades in our societies. It passed
from a traditional system where “humans were in a contractual, symbiotic relationship with farm
animals” where “the producer did well if and only if the animal did well” insuring thereby a certain
level of welfare for the animals [207], [228]; to an intensive system dictated by efficiency to produce
meat at the lowest cost. Via technological innovation (e.g. preventive use of antibiotics) it was
practically possible to increase the size of farms and automatise certain procedures in order to cut the
cost of labour [207], [229]. This shift of approach to farming is illustrated by the shift in the
sociozoological scale, which shows how people evaluate animals. Indeed, several decades ago, cattle
were at the top of the sociological scale and sits low on the latter scale nowadays. This two major
changes lead to moral questions. The ever-growing size of farms and the constant search for cost
reduction may have detrimental consequences on animal welfare in the case animals are considered
merely as commodities [207] despite their acknowledged capacity of sentience. However, a recent
report of the Netherlands Council for Animal Affairs (2012) shows that an economy-driven
production does not systematically imply detriments to animal welfare. Indeed, in the current market,
animal welfare may become a desired added-value to the product.
In this economy-driven climate, it is not surprising – but certainly not ethically defensible - that the
choice of euthanasia method may appear to be more driven by factors such as financial costs than
welfare implications. In conclusion, the issue of animal welfare at the time of slaughter goes far
beyond the method chosen for euthanasia and lies principally in the system that governs the profitdriven modern industrial agriculture. We believe that, without changing the latter, it will be difficult
to reconsider the currently used methods for rabbit slaughter although there is clearly room for
refinement, in terms of welfare, of the currently used methods. For now, the focus must thus hold
principally on refinements of the currently used methods.
IV.
Conclusion
As detailed earlier, the view on the moral status of animals changed over years. Indeed, with scientific
advances that enabled to recognize animals as sentient beings, animals became morally considerable
for their own sake. The recent changes in the way of keeping animals i.e. from traditional agriculture
to factory farming challenge the traditional idea that “the producer did well if and only if the animal
did well“ [228], which constrained human action towards animals independently of whether they are
morally considered. As a consequence of these two latter changes, different animals are valued
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differently. This is illustrated by the sociozoological scale that makes people be very concerned about
pet euthanasia but less concerned by slaughtering of farm animals and even less by culling of “pest”
animal. This view is challenged by the criterion of logical consistency when, in similar circumstances,
the same species is treated differently across different contexts.
1. The challenge of conclusion
Many matters tackled in this review present conflicts which prevents any clear-cut conclusion on what
is the best for animal welfare. For instance, sedation is advised to relax the individual before
euthanasia but as it is usually administered by injection, it might in fact increase stress [21]. Similarly,
guidelines about animal euthanasia advice to euthanize each animal separately but several authors
identified isolation in social animals as a major stressor. Consequently, all methods are questions of
trade-off. Within one method, when one factor is positive for welfare (e.g. smooth induction of
unconsciousness) another appears negative (e.g. restraint for injection) and it is a challenge to
determine which outweigh the other in the animal’s perception.
These conflicts are reflected in the relatively large amount of contradictory literature available. This
complicates even more any conclusion drawing. These contradictions shed light on the crucial role of
peri-euthanasia factors in the euthanasia process. Indeed, two experiments may test an identical
method on identical species and end up with opposite results because of factors such as transport, food
deprivation, familiarity of the handler, etc. Moreover, even within each context, the constraints on the
euthanasia method may be different (e.g. different research questions in the context of lab animals).
Hence, each situation is unique and presents a distinctive combination of factors determining the
choice of the euthanasia method.
Because each single situation constitutes a context on its own, the ethical questions that are inherent to
it, are different. Moreover, these questions are answered differently by each individual. Therefore, it is
very difficult to draw a general and absolute conclusion about a preferred method that should be
applied in each context or to conclude whether is it is justified to use different methods across
contexts for a single species. However, as a result of the information gathered and the ethical
reflection that was developed in the present paper, a conclusion is stated in the following section. It
has to be borne in mind that the latter does not pretend to be an absolute and unalterable answer, but a
sensible inference from the facts and ideas presented throughout the review.
2. Conclusion on Biological basis
The present paper provided an overview of the welfare implications of each euthanasia method and
described each context, specifying the most common euthanasia methods used within it. From the
present review, it appears that different methods, with thus different welfare standards are used in
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different contexts. In pest rabbits, although there is an increasing concern about wildlife, the methods
currently used do not appear to take welfare implications much into account which may reflect a poor
acknowledgment of the moral status of animals seen as pest. In rabbits used for production, i.e. meat
and fur, individuals are submitted to a procedure that impairs their welfare (e.g. hanging, inefficient
stunning or recovery before death induction) although some measures for better welfare standards are
taken. In laboratory settings, the welfare of animals is thoroughly scrutinised by ethical committees
and laboratory animal specialists, but the purpose of the experiment outweighs welfare implications.
Welfare appears to play the most leading role in the context of pet animals.
Therefore, the question whether it is scientifically justified to use different methods in different
contexts for rabbit euthanasia, arises. It has to be borne in mind that the ontogeny of the individual
plays an important role in the determination of the most welfare-friendly method (e.g. whether
animals are habituated to handling). In a biological approach towards animal welfare, our conclusion
is that it is not justified to consider rabbits differently across contexts, and thus use different
euthanasia methods, since members of the same species have identical biological features and needs.
This holds unless the ontogeny of the individual justifies the use of a different euthanasia method.
Unfortunately, in the real world and as mentioned earlier, the raison d’être of the context will always
outweigh the welfare implications of the euthanasia method required for the purpose of animal use. Of
course, the raison d’être of the context would need further reflection, but this is beyond the scope of
this paper. Because of this raison d’être, it may appear, to some extent and to some people, that it is
justified to apply different euthanasia methods in different contexts since the methods need to follow
industry requirements (e.g. no meat contamination). However, to sum up, our opinion remains that
using different euthanasia methods for rabbits in different contexts is not justified from a biological
approach to animal welfare.
3. Conclusion on Ethical basis
The present review discussed the importance granted to animal welfare aspect in the choice of the
euthanasia method, within each context. It also attempted to infer the moral standing attributed to
animals in each context. It results from this review is that rabbits do not seem to receive equal moral
standing across contexts. Consequently, no equal consideration is attributed to their welfare at
euthanasia neither.
The question that remains to be tackled in the scope of the present review is whether it is ethically
justified to use different methods in different contexts for rabbit euthanasia. Although the raison
d’être of the context can give a semblance of justification, to many people, it appears intuitively
obvious that identical euthanasia standards should apply when killing one animal species in different
contexts [18]. This intuition demonstrates a need for an ethical reflection.
60 Master Thesis, Utrecht University
O. Szczodry
2013
Although the ethical reflection about the raison d’être of a context of animal use seems to adopt a
utilitarian-like approach, i.e. animals have moral standing but our interests outweigh theirs so we use
them, the approach in the issue of rabbits euthanasia methods across contexts seems to be closer to the
relational view. This is corroborated by the notion put forward by DeGrazia (2008) that the moral
status does not have to be an “all-or-nothing” concept but that degrees of moral status can be
attributed. However, even from this perspective, it is still morally arguable to define the moral status
of a single species exclusively by looking at its relationship with humans.
The particularity in the present topic is that the moral standing is not defined at a species level but at
the level of the individual. Indeed, moral standing does not appear to be granted following the
relationship that the species has with humans, but according to the relationship that the individual
animal has with humans. Hence, the idea suggested by this approach is that the moral standing does
not have to be equal for the whole species but can be individual. To us, this does not appear to be
logically consistent.
Therefore, in our opinion, the relationship that an animal has with humans is not a valid criterion to
define the moral status of the animal, which will, as an indirect consequence, determine the amount of
suffering inflicted in the process of euthanasia. On the whole, it appears to us, that using different
euthanasia methods between contexts of rabbit use in not ethically justified.
4. Final statements
We are aware of the fact that the conclusions stated above may present limitations. The unique clearcut conclusion that can be drawn is that there is a strong need for refinement of the currently used
euthanasia methods for rabbits. The methods shall be put into practice in a way that is as close as
possible to what is foreseen in theory. Indeed, in the present review, some methods were shown to be
theoretically
acceptable
but
practically
unacceptable
(e.g.
electronarcosis
followed
by
exsanguination). Additionally, it has been seen that distress can significantly be decreased when
minor refinements are integrated (e.g. euthanizing in the home cage, Hackbarth, Küppers, & Bohnet,
2000).
Another notable statement is that the problem does not consist only of different euthanasia methods
used in different contexts but is more general and lies in the manner the animals are used nowadays.
The issue goes, at least to some extent, beyond welfare and a serious questioning about the current
system of animal use in general needs to take place.
To sum up, the welfare implications of different euthanasia methods of rabbits were developed in the
present review, and for each context, the most commonly used methods were outlined. We saw that in
each context, the moral standing of the animal appears different. As a consequence, the importance of
61 Master Thesis, Utrecht University
O. Szczodry
2013
welfare in euthanasia seemed to differ between contexts as well, with what is labelled as the most
animal-friendly method, i.e. sodium pentobarbital, applied for pet rabbits, and the least welfare
preserving methods used for pest rabbits (e.g. kill traps, poisoning, or viruses).
From our findings we can conclude that, in terms of biological aspects of animal welfare, it is not
justified to use different euthanasia methods for rabbits according to the context of the rabbit’s use.
Based on our ethical reflection, we think that it is not ethically justifiable either.
As emphasised earlier, this review attempted to take a first step in the debate whether it is justified to
apply different euthanasia methods in rabbits due to context differences. After having analysed
thoroughly the biological aspect of the debate, we have briefly explored the ethical aspect of the issue
and we conclude that there is a need for a more profound ethical reflection on the topic, as a secondstep in the debate.
Of note, results from this review can be helpful in the reflection on other practices in which the same
species is used in several contexts.
62 Master Thesis, Utrecht University
O. Szczodry
2013
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O. Szczodry
69 Master Thesis, Utrecht University
2013
I would like to express my gratitude to my
supervisors S.S. Arndt and F.L.B Meijboom for
their expertise, time and support throughout the
whole writing process. I highly appreciate the
valuable
advice,
comments
and
suggestions
received during all stages of the review drafting i.e.
from definition of the topic to the final comments on
the outline of the paper, as it considerably added to
my graduate experience. Moreover, I thank them
for the valued understanding provided at all times.
I also would like to thank my family and friends for
their
encouragements
and
positive
attitude
expressed from the very beginning. Appreciation
goes especially to my mother and my boyfriend that
looked thoroughly at the finest details of the
manuscript. Finally, I thank F. Ohl and the
department of Animals in Science and Society
(DWM), Veterinary Faculty, Utrecht University, for
the opportunity they gave me to write my master
thesis within the department.
Literature Master Thesis
Environmental Biology –
Behavioural Biology
Utrecht University
Supervisors: S.S. Arndt &
F.L.B. Meijboom
70 Master Thesis, Utrecht University
September 2013