SCIENTIFIC OPINION
ADOPTED: 5 April 2017
doi: 10.2903/j.efsa.2017.4782

Animal welfare aspects in respect of the slaughter or killing
of pregnant livestock animals (cattle, pigs, sheep, goats,
horses)
EFSA Panel on Animal Health and Welfare (AHAW),
Simon More, Dominique Bicout, Anette Botner, Andrew Butterworth, Paolo Calistri,
Klaus Depner, Sandra Edwards, Bruno Garin-Bastuji, Margaret Good,
Christian Gortazar Schmidt, Virginie Michel, Miguel Angel Miranda, Søren Saxmose Nielsen,
Antonio Velarde, Hans-Hermann Thulke, Liisa Sihvonen, Hans Spoolder, Jan Arend Stegeman,
Mohan Raj, Preben Willeberg, Denise Candiani and Christoph Winckler

Abstract
This scientiﬁc opinion addresses animal welfare aspects of slaughtering of livestock pregnant animals.
Term of Reference (ToR) 1 requested assessment of the prevalence of animals slaughtered in a critical
developmental stage of gestation when the livestock fetuses might experience negative affect. Limited
data on European prevalence and related uncertainties necessitated a structured expert knowledge
elicitation (EKE) exercise. Estimated median percentages of animals slaughtered in the last third of
gestation are 3%, 1.5%, 0.5%, 0.8% and 0.2% (dairy cows, beef cattle, pigs, sheep and goats,
respectively). Pregnant animals may be sent for slaughter for health, welfare, management and
economic reasons (ToR2); there are also reasons for farmers not knowing that animals sent for
slaughter are pregnant. Measures to reduce the incidence are listed. ToR3 asked whether livestock
fetuses can experience pain and other negative affect. The available literature was reviewed and, at a
second multidisciplinary EKE meeting, judgements and uncertainty were elicited. It is concluded that
livestock fetuses in the last third of gestation have the anatomical and neurophysiological structures
required to experience negative affect (with 90–100% likelihood). However, there are two different
possibilities whether they perceive negative affect. It is more probable that the neurophysiological
situation does not allow for conscious perception (with 66–99% likelihood) because of brain inhibitory
mechanisms. There is also a less probable situation that livestock fetuses can experience negative
affect (with 1–33% likelihood) arising from differences in the interpretation of the fetal
electroencephalogram, observed responses to external stimuli and the possibility of fetal learning.
Regarding methods to stun and kill livestock fetuses at slaughter (ToR4), sets of scenarios and
respective actions take account of both the probable and less probable situation regarding fetal ability
for conscious perception. Finally, information was collated on methods to establish the dam’s
gestational stage based on physical features of livestock fetuses (ToR5).
© 2017 European Food Safety Authority. EFSA Journal published by John Wiley and Sons Ltd on behalf
of European Food Safety Authority.

Keywords: Slaughter, pregnant animals, livestock species, animal welfare, conscious perception,
pain, fetus

Requestor: Denmark, Germany, the Netherlands and Sweden
Question number: EFSA-Q-2015-00477
Correspondence: alpha@efsa.europa.eu

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Slaughter of pregnant animals

Panel members: Dominique Bicout, Anette Botner, Andrew Butterworth, Paolo Calistri, Klaus Depner,
Sandra Edwards, Bruno Garin-Bastuji, Margaret Good, Christian Gortazar Schmidt, Virginie Michel,
Miguel Angel Miranda, Simon More, Søren Saxmose Nielsen, Antonio Velarde, Hans-Hermann Thulke,
Liisa Sihvonen, Hans Spoolder, Jan Arend Stegeman, Mohan Raj, Preben Willeberg and Christoph Winckler.
Acknowledgements: The Panel wishes to thank the members of the Working group on animal
welfare aspects in respect of the slaughter or killing of pregnant livestock animals (cattle, pigs, sheep,
goats, horses): Sandra Edwards, Mohan Raj, Hans Spooler, Antonio Velarde, Andy Hart and Christoph
Winckler for the preparatory work on this scientiﬁc opinion, the following hearing experts: Ioana
cile Bourguet, Laura Boyle, Ve
ronique Debarge, Richard
Andronie, Carlo Valerio Bellieni, Lotta Berg, Ce
Donker, Bernadette Doyle, Else Enemark, Nicholas Fisk, Lucy Green, Peter Hepper, Pierre Le Neindre,
Michael Marahrens, David Mellor, Bjorn Merker, Joaquim Pallisera, Katharina Riehn, Sara Rota Nodari,
o
sarz, Evangelia Sossidou, Miguel Stevens, Claudia Terlouw, Anne von
Matthias Schwab, Piotr Sl
Thaden, Noelia Yusta and EFSA staff Francesca Porta and Olaf Mosbach-Schulz for the support
provided to this scientiﬁc opinion.
Suggested citation: EFSA AHAW Panel (EFSA Panel on Animal Health and Animal Welfare), More S,
Bicout D, Botner A, Butterworth A, Calistri P, Depner K, Edwards S, Garin-Bastuji B, Good M, Gortazar
Schmidt C, Michel V, Miranda MA, Saxmose Nielsen S, Velarde A, Thulke H-H, Sihvonen L, Spoolder H,
Stegeman JA, Raj M, Willeberg P, Candiani D and Winckler C, 2017. Scientiﬁc Opinion on the animal
welfare aspects in respect of the slaughter or killing of pregnant livestock animals (cattle, pigs, sheep,
goats, horses). EFSA Journal 2017;15(5):4782, 96 pp. https://doi.org/10.2903/j.efsa.2017.4782
ISSN: 1831-4732
© 2017 European Food Safety Authority. EFSA Journal published by John Wiley and Sons Ltd on behalf
of European Food Safety Authority.
This is an open access article under the terms of the Creative Commons Attribution-NoDerivs License,
which permits use and distribution in any medium, provided the original work is properly cited and no
modiﬁcations or adaptations are made.
The EFSA Journal is a publication of the European Food
Safety Authority, an agency of the European Union.

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Slaughter of pregnant animals

Summary
Observations have indicated that slaughtering of pregnant animals is not an isolated phenomenon
and Regulation (EC) No 1099/2009 on the protection of animals at the time of killing does not contain
any provisions with regard to the protection of fetuses of livestock species when a pregnant dam is
slaughtered. Four European Member States (Germany, the Netherlands, Sweden and Denmark)
requested the EFSA Panel on Animal Health and Animal Welfare (AHAW) to deliver a Scientiﬁc Opinion
concerning the animal welfare aspects in respect of the slaughter or killing of pregnant livestock
species (cattle, pigs, sheep, goats, horses). In particular, the European Food Safety Authority (EFSA)
was requested to address the following ﬁve Terms of Reference (ToRs): (1) to assess the prevalence of
pregnant livestock animals slaughtered in a critical developmental stage at which livestock fetuses
might experience suffering; (2) to assess the reasons why pregnant animals are slaughtered in the
critical phase of gestation and propose recommendations to reduce the number of animals slaughtered
while pregnant in this stage; (3) to assess the available scientiﬁc evidence on the capacity of livestock
fetuses to experience pain; (4) to provide scientiﬁc advice on methods suitable for stunning and killing
of fetuses or neonates of the main livestock species when a pregnant dam has been delivered to the
slaughterhouse at a critical phase of gestation, and (5) to provide scientiﬁc advice on methods suitable
for estimating the age of fetuses of the main livestock species at the slaughterhouse after the dam has
been slaughtered.
This mandate has been chosen as a case study for testing the approaches proposed in the draft
Guidance on Uncertainty in EFSA scientiﬁc assessment. Following provisions of the uncertainty
guidance, uncertainty as regards ToR1 and ToR3 was quantiﬁed using expert knowledge elicitation
guided by literature evaluation. The uncertainty assessment was addressed differently for ToR1 and
ToR3. For ToR1, the prevalence of slaughtered pregnant animals was elicited by an Expert Knowledge
Elicitation meeting (referred to as EKE 1). This resulted in ‘median estimates’ for the prevalence (e.g.
3% dairy cows in the last term of gestation) accompanied by a probability distribution range (e.g. from
9% to 27%) that gives the level of uncertainty. For ToR3, expert knowledge was elicited on
statements, e.g. that livestock fetuses have the anatomical structures required (and further statements
derived from the logical model; see below). The answers were formulated as likelihoods of the
statement being true with the distribution of the answers providing the certainty distribution (e.g. from
5% to 40% likelihood that a certain statement is true). From the range of likelihood values and further
interpretation of the literature, a qualitative translation of the uncertainty was derived (e.g. very likely).
The remaining ToRs were addressed by the Panel through appraisal of the scientiﬁc literature.
For ToR1, several possible sources of information including literature review and reports from the
Member States were investigated but the information retrieved was limited. Therefore, a survey in 10
Member States was carried out, addressed to slaughterhouse operators, asking for estimates of the
proportion of total pregnancies in slaughtered animals and the proportion of pregnant animals found in
the different terms of gestation in 2015. The experts who performed the survey were then invited to
an Expert Knowledge Elicitation (referred to as EKE 1) meeting with the aim to generate probability
judgements around the prevalence estimates per livestock species in Europe. Outcomes of the EKE 1
meeting are estimates for the median prevalence of pregnant animals slaughtered for each species as
well as the 50% and 98% uncertainty range. Estimated median percentages of all mature female
animals slaughtered while pregnant in Europe were 16%, 11%, 6%, 10% and 4% (dairy cows, beef
cattle, pigs, sheep and goats, respectively). The respective estimated median percentages of all
mature female animals slaughtered in the last third of gestation were 3%, 1.5%, 0.5%, 0.8% and
0.2% (dairy cows, beef cattle, pigs, sheep and goats, respectively). Estimates for horses are not given
in the opinion due to lack of information.
For ToR2, literature was investigated and a discussion was held at the EKE 1 meeting. It was
concluded that the reasons for unknowingly sending pregnant animals for slaughter include (i) lack of
supervision of breeding, especially in extensive systems, (ii) absence or failure of pregnancy diagnosis,
and (iii) poor record keeping or loss of information in the trading chain. The reasons for knowingly
sending pregnant animals for slaughter can be categorised into (i) health and welfare beneﬁts, (ii)
management advantages and (iii) economic necessity or beneﬁt. To reduce unplanned slaughtering, it
is recommended to improve the health status of animals on farm and to reduce unplanned
pregnancies by single sex housing and supervised breeding. In addition, the pregnancy status of all
animals should be established before they are sent for slaughter; for this purpose, a decision tree to
support farmers has been developed. Information about insemination and pregnancy diagnosis should
be required in documentation accompanying animals at the time of sale. Finally, further research

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should be undertaken to improve pregnancy diagnostic test accuracy and feasibility, especially for the
diagnosis of later stages of pregnancy.
For ToR3, the scope was not exclusively on pain, but also on other types of negative affect. The
topic was subdivided into (i) anatomical structures required, (ii) the neurophysiological situation (e.g.
inhibitory and excitatory systems) and (iii) the response of the livestock fetuses to speciﬁed stunning
and slaughter conditions. Based on literature review, a logical model was created showing how the
above-mentioned subquestions link together to address the overall question on the capacity of
livestock fetuses to experience pain and other negative affect. Due to divergent views in the literature,
in a second EKE (referred to as EKE 2) meeting (i) probability distributions for the propositions in the
subquestions to be true were elicited, and (ii) the level of uncertainty around each subquestion was
expressed through a standardised methodology. The outcomes of the EKE 2 meeting were evaluated
by the AHAW Panel in the context of additional ﬁndings from the literature and further discussion with
some of the EKE 2 experts to generate ﬁnal conclusions for this opinion. These following conclusions,
expressed using an approximate probability scale, are obtained:
1) It is very likely to extremely likely (i.e. with 90–100% likelihood) that livestock fetuses in the
last third of gestation have the anatomical and neurophysiological structures/correlates for
experiencing pain and/or other forms of discomfort.
2) Based on the available scientiﬁc evidence and expert opinion, it cannot be determined with
certainty whether livestock fetuses are capable of cortically based conscious perception, and
therefore, there exist two different situations. It is more probable that ‘the neuro-physiological
situation of the livestock fetuses in the last third of gestation (i.e. inhibitory and excitatory
systems) does not allow for cortically based conscious perception’ (this statement is likely to
very likely correct, i.e. with 66–99% likelihood). This view is supported by the presence of
adenosine-mediated brain inhibitory (neuroprotective) mechanisms operating in utero,
demonstrated by electroencephalogram (EEG) records, the low level of fetal brain oxygen,
the predominance of sleep like states in the fetal EEG and the lack of any direct evidence of
cortically based conscious perception. There is also a less probable situation that ‘the
neuro-physiological situation of the livestock fetuses in the last third of gestation does allow
for cortically based conscious perception’ (this statement is unlikely to very unlikely to be
correct, i.e. with 1–33% likelihood). The reasons on which this less probable situation is
based relate to the lack of any direct evidence proving that livestock fetuses are incapable
of cortically based conscious perception and to differences in the interpretation of indirect
evidence relating to fetal EEG (e.g. signiﬁcance of transitional EEG), observed fetal
behavioural and physiological responses to external stimuli and the possibility of fetal
learning (conscious learning versus conditioned responses).
3) There is no direct evidence demonstrating the existence of subcortical awareness in
livestock fetuses and the existence of a hypothesised raw basic affect. However, even if this
were to exist, it is unlikely to very unlikely (i.e. with 1–33% likelihood) that the
neurophysiological situation of the livestock fetuses in the last third of gestation (i.e.
inhibitory and excitatory systems) would allow for subcortically based conscious perception.
4) It is very likely to extremely likely (i.e. with 90–100% likelihood) that livestock fetuses show
measurable responses to extreme hypercapnic hypoxia, mechanical stimulation and electrical
current. Probabilities are given in the opinion that livestock fetuses are subjected to each of
these stimuli during slaughtering of the dam.
5) However, since all slaughtering procedures involve a maternal circulatory collapse and rapid
fetal hypoxia increasing adenosine mediated brain inhibitory mechanisms, it is unlikely to
very unlikely (i.e. with 1–33% likelihood) that changes/responses occurring during stunning
and bleeding of the dam are associated with pain or other negative affect in the livestock
fetuses.
For ToR4, a set of scenarios and respective actions has been developed for both the assumptions
that livestock fetuses might or might not perceive pain or other negative affect: (1) if it is accepted
that livestock fetuses are not able to experience pain or other negative affect (i.e. the above indicated
66–99% likelihood), the fetus should be left undisturbed in utero for 30 min after the death of the
dam by which time it will be dead. If the livestock fetus is exteriorised before this time, it should be
stunned and killed using approved methods for neonates in accordance with Reg 1099/2009); (2) if it
is accepted that livestock fetuses might experience pain or other negative affect (i.e. the above
indicated 1–33% likelihood), the fetus should be killed in situ together with the dam by an overdose of
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anaesthetic drug if pregnancy is detected at arrival in the slaughterhouse. If the dam is already dead
at the time of detection, the fetus should immediately be exteriorised, stunned and killed using
approved methods.
Regarding ToR5, the determination of gestational stage after post-mortem detection can be based
on physical/morphological characteristics of the livestock fetuses as suggested in the opinion. Due to
variation between breeds, preference should be given to external features such as hair cover over
linear morphological measures. For the allocation to a given term, criteria towards the midstage are
more reliable indicators than those suggested for the exact boundaries between gestational stages,
due to the limitations of available data.

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Table of contents
Abstract.................................................................................................................................................. 1
Summary................................................................................................................................................ 3
1.
Introduction................................................................................................................................ 8
1.1.
Background and Terms of Reference as provided by the requestor.................................................. 8
1.2.
Interpretation of the Terms of Reference....................................................................................... 9
2.
Data and methodologies .............................................................................................................. 10
2.1.
Data........................................................................................................................................... 10
2.1.1. Data for ToR1 (prevalence of pregnant animals at slaughter in EU) ................................................. 10
2.2.
Uncertainty ................................................................................................................................. 11
2.3.
Methodologies............................................................................................................................. 11
2.3.1. Methodology for ToR1 (prevalence of pregnant animals at slaughter) .............................................. 11
2.3.2. Methodology for ToR2 (reasons for slaughtering pregnant animals and recommendations to reduce
the number of pregnant animals slaughtered) ............................................................................... 12
2.3.3. Methodology for ToR3 (assessment of the scientiﬁc evidence available on the capacity of fetuses to
experience pain) ......................................................................................................................... 13
2.3.4. Methodology for ToR4 (methods for stunning and killing of fetuses or neonates of the main livestock
species) ...................................................................................................................................... 14
2.3.5. Methodology for ToR5 (methods for estimating the age of fetuses of the main livestock species at
the slaughterhouse after the dam has been slaughtered) ............................................................... 14
3.
Assessment................................................................................................................................. 14
3.1.
Assessment for ToR1(prevalence of pregnant animals slaughtered in EU) ........................................ 14
3.1.1. Information on prevalence from Member States ............................................................................ 14
3.1.2. Information on prevalence from literature ..................................................................................... 14
3.1.3. Information and weighing of uncertainty on prevalence resulting from Expert Knowledge Elicitation .. 15
3.1.3.1. Country differences in prevalence of slaughtered pregnant cattle .................................................... 16
3.1.3.2. Country differences in prevalence of slaughtered ewes................................................................... 17
3.2.
Assessment for ToR2 (reasons why pregnant animals are slaughtered and recommendations to
reduce the number of animals slaughtered while pregnant)............................................................ 17
3.2.1. Summary of known reasons for the slaughter of pregnant animals.................................................. 17
3.2.2. Results of expert opinion on the reasons for slaughtering of pregnant animals................................. 19
3.2.2.1. Measures to reduce the number of animals slaughtered while pregnant at a critical stage of gestation..
3.2.2.2. Decision-tree to support farmers to reduce the likelihood of pregnant animals sent to slaughter ....... 23
3.2.2.3. Methods for pregnancy diagnosis.................................................................................................. 25
3.3.
Assessment for ToR3 (assessment of the scientiﬁc evidence available on the capacity of fetuses to
experience pain and other negative affect).................................................................................... 26
3.3.1. Working deﬁnitions...................................................................................................................... 26
3.3.1.1. Deﬁnition of fetus........................................................................................................................ 26
3.3.1.2. Deﬁnitions of nociception (sensory perception) and pain (emotional experience).............................. 27
3.3.1.3. Deﬁnition of consciousness .......................................................................................................... 27
3.3.2. Logical model.............................................................................................................................. 27
3.3.3. Summary of available scientiﬁc evidence for ToR3 (capacity of fetuses to experience pain and other
negative affect)........................................................................................................................... 29
3.3.3.1. Summary of scientiﬁc evidence on C1. Anatomical and neurophysiological correlates/structures
necessary for perception of pain and other negative affect (at cortical and/or subcortical level) ........ 29
3.3.3.2. Summary of scientiﬁc evidence on C2. Neurophysiological situation (e.g. inhibitory and excitatory
systems) and possibility of cortically based perception ................................................................... 32
3.3.3.3. Summary of scientiﬁc evidence on the possibility of ‘subcortical’ awareness ..................................... 37
3.3.3.4. Summary of scientiﬁc evidence on C3. Changes occurring during slaughter of the dam and effect on
the fetus (e.g. electric current, hypoxia through ceased maternal blood ﬂow, elevated stress
hormone levels) .......................................................................................................................... 38
3.3.4. Expert judgements on ToR3 (capacity of fetuses to experience pain and other negative affect)......... 40
3.3.4.1. Expert judgement for C1. Anatomical and neurophysiological correlates/structures necessary for
perception of pain and other negative affect ................................................................................. 41
3.3.4.2. Expert judgement for C2. Neurophysiological situation and possibility of cortically based conscious
perception .................................................................................................................................. 41
3.3.4.3. Expert judgement for C3. Changes occurring during slaughter of the dam and effect on the fetus .... 41
3.3.4.4. Expert judgement for C4. Possibility that fetuses experience negative affective state following
speciﬁed stunning and slaughter conditions................................................................................... 42

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3.3.4.5. Expert judgement for C5. Level of negative affective state experienced by fetuses during slaughter
of the dam ................................................................................................................................. 42
3.3.4.6. Logical model for subcortically based conscious perception............................................................. 42
3.4.
Assessment for ToR4 (methods suitable for stunning and killing of fetuses or neonates of the main
livestock species when a pregnant dam has been delivered to the slaughterhouse at a critical phase
of gestation) ............................................................................................................................... 42
3.4.1. Scenarios operating under the assumption that the neurophysiological situation of the fetus does
not allow for consciousness.......................................................................................................... 42
3.4.2. Scenarios operating under the assumption that the neurophysiological situation of the fetus does
allow for consciousness................................................................................................................ 47
3.5.
Assessment for ToR5 (methods to determine the gestational phase under practical conditions by
examining the fetus after the dam has been killed)........................................................................ 48
3.5.1. Results from literature review....................................................................................................... 48
4.
Conclusions................................................................................................................................. 55
5.
Recommendations ....................................................................................................................... 56
References.............................................................................................................................................. 57
Glossary and Abbreviations ...................................................................................................................... 64
Glossary related to the uncertainty ........................................................................................................... 66
Abbreviations .......................................................................................................................................... 66
Appendix A – Literature search on the prevalence of slaughtered pregnant animals in Europe....................... 68
Appendix B – Literature search on the reasons for slaughtering pregnant animals in Europe ......................... 69
Appendix C – Elicitation Report................................................................................................................. 70
Appendix D – Elicitation Report ................................................................................................................ 84

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1.

Introduction

1.1.

Background and Terms of Reference as provided by the requestor

Request for a Scientiﬁc Opinion concerning the animal welfare aspects in respect of the slaughter
or killing of pregnant livestock species (cattle, pigs, sheep, goats, horses).
Recent scientiﬁc studies indicate that the slaughter of pregnant animals in the European Union (EU)
€cker et al., 2003; Di Nicolo, 2006; Riehn et al., 2010; Braunmiller,
is not an isolated phenomenon (Lu
2015). These results contradict the statements of the Scientiﬁc Committee on Veterinary Measures
relating to Public Health (SCVPH) that assumed in its opinion on the potential risks of hormonal
residues in beef to human health (1999) that heifers are only slaughtered in exceptional cases.
Scientiﬁc studies on the sensation of pain in fetuses come to controversial results: Some of these
studies say that, not being in an awake state and lacking appropriate cortex participation, fetuses have
no faculty of sensation and perception as long as they have not started breathing following their
development from the uterus (Mellor and Gregory, 2003; Mellor and Stafford, 2004; Mellor et al.,
2005; Mellor and Diesch, 2006; Mellor, 2010). The Terrestrial Animal Health Code of the OIE (2008)
also recommends, among other things, that from an animal welfare point of view, fetuses should
remain in the unopened uterus until death. This concept of ‘fetal unconsciousness’ with regard to the
sensation and perception of, e.g. pain is rejected by other scientists, however. According to Merker
(2007), a conscious perception of sensory stimuli also takes place in the brain stem. Bellieni and
Buonocore (2012) indicate that a fetal sensation of pain is present during the last third of the
pregnancy at the latest.
Directive 2010/63/EC1 also covers fetal forms of mammals, as there is evidence that they are at an
increased risk of experiencing pain, suffering and distress in the last third of the period of their
development (cf. recital no 9).
In contrast to this, Regulation (EC) No 1099/20092 does not contain any provisions with regard to
the protection of unborn animals. At the same time, Regulation (EC) No 1099/2009 does not provide
the Member States with a possibility to adopt stricter national regulations for the killing of animals
(here: the fetuses) in slaughterhouses either.
If it can be assumed from an animal welfare point of view that fetuses are able to experience pain
and suffering from a certain developmental stage onwards, provisions for the protection of unborn
animals should not only regard laboratory animals. Appropriate regulations should rather also be
included in the EU legislation on the protection of animals at the time of killing.
It should be clariﬁed at EU level how the slaughter of pregnant animals from a critical phase of
gestation onwards (after which the fetus is considered to be able to perceive pain) can be avoided. As
it can be assumed that even in the case of a potential ban on the slaughter of pregnant animals a
certain part of slaughter animals will be falsely declared as not pregnant it should be clariﬁed how the
fetuses should be killed after the killing of the dam. Furthermore, comparable animal welfare problems
with regard to dealing with fetuses also exist in the case of emergency slaughters or killings of the
dam for animal health reasons.
Above all, we consider it necessary to review the current practice in slaughterhouses to leave
developed fetuses in the uterus until death and to determine appropriate stunning and killing methods
for fetuses of dams slaughtered in the critical phase of gestation. As it can be assumed from an animal
welfare point of view that fetuses in general are able to experience pain and suffering from a critical
phase of gestation onwards, the scientiﬁc opinion should cover the main livestock species (cattle, pigs,
sheep, goats, horses).
Therefore, in view of the above, and in accordance with Article 29 of Regulation (EC) No 178/20023,
Denmark, Germany, the Netherlands and Sweden ask the European Food Safety Authority (EFSA) for a
scientiﬁc opinion on the following aspects:
1) Assess the prevalence of pregnant livestock animals slaughtered in the critical
developmental stage after which the fetus is considered to be able to perceive pain in
EU Member States and at EU level; the study should include cattle, pigs, sheep, goats,
1

Directive 2010/63/EU of the European parliament and of the council of 22 September 2010 on the protection of animals used
for scientiﬁc purposes.
2
Council Regulation (EC) No 1099/2009 of 24 September 2009 on the protection of animals at the time of killing.
3
Regulation (EC) No 178/2002 of the European Parliament and of the Council of 28 January 2002 laying down the general
principles and requirements of food law, establishing the European Food Safety Authority and laying down procedures in
matters of food safety.
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2)

3)
4)

5)

1.2.

horses; cattle could be feasible due to data being collected under the Livestock
Database;
Assess the reasons why pregnant animals are slaughtered in the critical phase of gestation
and propose recommendations to reduce the number of animals slaughtered while pregnant
in this stage;
Assess the scientiﬁc evidence available on the capacity of fetuses to experience pain;
Provide scientiﬁc advice on methods suitable for stunning and killing of fetuses or neonates
of the main livestock species when a pregnant dam has been delivered to the slaughterhouse
at a critical phase of gestation;
Provide scientiﬁc advice on methods suitable for estimating the age of fetuses of the main
livestock species at the slaughterhouse after the dam has been slaughtered, in order to
identify if the fetus has reached the critical developmental stage after which it is considered
to be able to perceive pain.

Interpretation of the Terms of Reference

ToR1 asks to ‘Assess the prevalence of pregnant livestock animals slaughtered in the critical
developmental stage after which the fetus is considered to be able to perceive pain’ within the
EU.
Prior to the discussions in ToR3 relating to the existence and timing of the critical period, it was
decided for the purpose of ToR1 to use the deﬁnition previously presented by Directive 2010/63/EC
which states that this critical period is represented by the last third of pregnancy.
ToR2 asks to ‘Assess the reasons why pregnant animals are slaughtered in the critical phase of
gestation and propose recommendations to reduce the number of animals slaughtered while
pregnant in this stage’. This ToR will be addressed taking into consideration three main reasons for
slaughtering pregnant animals, namely related to health and welfare, economic or management
reasons, as well as lack of knowledge of pregnancy state. The opinion will relate the above three
reasons as much as possible to the actual (or estimated) stage of pregnancy. Based on this
analysis, approaches to reduce the number of animals slaughtered in late pregnancy can then be
proposed.
ToR3 asks to ‘Assess the scientiﬁc evidence available on the capacity of fetuses to experience pain’.
For a comprehensive assessment, fetal/neonatal physiology, developmental physiology, embryology
including expertise from human medicine/life sciences need to be considered, to assess the
developmental stage at which the fetus has the anatomical features required to experience pain and
the time at which the fetus is aware of painful stimuli. Regarding the assessment of potential pain in
fetuses, the scope will be extended also to other negative affect (such as distress and discomfort),
which might be experienced following the stunning and slaughter of the dam.
ToR4 asks to ‘provide methods suitable for stunning and killing of fetuses or neonates of the main
livestock species when a pregnant dam has been delivered to the slaughterhouse at a critical phase of
gestation’. If the evidence assessed for ToR3 conclusively demonstrates that the fetus has no ability to
experience pain or other negative welfare consequences prior to birth, then the fetus can be left in the
uterus as suggested in a past EFSA Opinion (EFSA, 2004). If the evidence indicates the certainty or
possibility that the fetus can experience pain or other negative welfare consequences in utero, the
scientiﬁc literature about methods for stunning and killing of fetuses at the deﬁned developmental
stage will be reviewed.
ToR5 asks to ‘provide scientiﬁc advice on methods suitable for estimating the age of fetuses of the
main livestock species at the slaughterhouse after the dam has been slaughtered, in order to identify if
the fetus has reached the critical developmental stage after which it is considered to be able to
perceive pain’. If the evidence conclusively demonstrates that the fetus has no ability to experience
pain or other negative welfare consequences prior to birth, then no further action is required for this
ToR. If the evidence indicates the certainty or possibility that the fetus can experience pain or other
negative welfare consequences in utero, the scientiﬁc literature about practical methods to assess the
age of the fetus will be reviewed.
Emergency killing for disease control remains out of the remit of this work, because this
scientiﬁc opinion is focussed on the slaughterhouse situation. However, such emergency killing is a
situation in which many pregnant animals might be slaughtered and the most humane methods for
dealing with the unborn fetus in such a situation could be extrapolated from the ﬁndings of this
Opinion.
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2.

Data and methodologies

2.1.

Data

2.1.1.

Data for ToR1 (prevalence of pregnant animals at slaughter in EU)

In the ﬁrst instance, data were collected from the Eurostat Livestock Database on the numbers of
cattle, pigs, sheep, goats slaughtered within the EU and associated countries. This database does not
record data on slaughtered horses. While it is possible to collect the denominator data on the total
number of livestock animals slaughtered in the EU from ofﬁcial data, there is no database which
records state of pregnancy. For cattle and horses, it is possible to know the age at slaughter from the
Livestock Database but this is not the case for pigs, sheep and goats.
Following a discussion with governmental representatives of Member States and associated
countries at the AHAW Network meeting, on 10–11 November 2015, EFSA requested Member States
to indicate whether they have any collected data on:

•
•
•

the number of female adult/post-puberty animals slaughtered;
the number of pregnant animals killed;
the gestational age at which these animals are slaughtered.

Responses were received from 10 countries (Belgium, Estonia, Latvia, Lithuania, the Netherlands,
Norway, Portugal, Spain, Sweden and Switzerland).
Furthermore, as a proxy for the number of pregnant animals killed in late pregnancy, EFSA asked
Member States for access to records submitted annually to the Commission under Council Regulation
(EC) No 1/20054, since the number of animals unﬁt for transport should be indicated in such reports
and pregnancy beyond 90% of gestation is a condition for animals being unﬁt for transport. A
standard format for these reports has been prescribed either in the Council Regulation (EC) No 1/2005
or in the Commission Implementing Decision 2013/188/EU5. These reports include information on total
number of animals checked during any type of transport and whether they were checked during
transport, in resting areas or at arrival at slaughter. The regulation requires that no animal shall be
transported unless it is ﬁt for the intended journey. Among the various health related issues, an animal
is not to be considered ﬁt for transport if it is a pregnant female for whom 90% or more of the
expected gestation period has already passed, or females who have given birth in the previous week.
However, the reports submitted to the EU Commission include information on total number of noncompliances out of total number of inspections only, without specifying the reason for non-compliance
but in broad categories (e.g. truck features, missing transport journal, unﬁt animals).
Due to the fact that reliable information was not retrieved from the above-mentioned sources (see
Section 3.1.1), the feasibility of an ex-novo data collection was also considered. However, after careful
evaluation and discussion, this option was excluded for the lack of representativeness, i.e. to be
relevant, a data collection should last at least 1 year, to reﬂect the variations between different periods
(e.g. due to the seasonality of breeding in the sheep sector).
Therefore, it was decided to design a survey, which was outsourced to 10 national scientiﬁc contact
points, set up by the Regulation 1099/2009, or to research institutions in the following EU countries:
Sweden, Italy, France, Spain, Romania, Poland, Greece, Ireland, the UK and Belgium. In each country,
the contractor convenience sampled 10 slaughterhouses – four for cattle, three for pigs, two for sheep,
one for goats and one for horses, when possible.
The surveys were carried out using a questionnaire based on the on-going German project S!GN6
investigating the proportion of pregnancies in slaughtered animals and the reasons for sending pregnant
animals for slaughter. The questionnaire consisted of six questions for which the slaughterhouse
operators were asked to provide either information relating to 2015 from slaughterhouse records or
personal judgements according to their experience:

4

Council Regulation (EC) No 1/2005 of 22 December 2004 on the protection of animals during transport and related options and
amending Directives 64/432/EEC and 93/119/EC and Regulation (EC) No 1255/97.
5
Commission Implementing Decision of 18 April 2013 on annual report on non-discriminatory inspections carried out pursuant to
Council regulation (EC) No 1/2005 on the protection of animals during transport and related operations and amending
Directives 64/432/EEC and 93/119/EC and Regulation (EC) No 1255/97.
6
http://www.ls.haw-hamburg.de/~SiGN/
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Slaughter of pregnant animals

•
•
•
•

the estimated number of adult/post-puberty female animals (cattle, pigs, sheep, goats, horses)
that were slaughtered in 2015 in their facilities.
the estimated number of female animals (cattle, pigs, sheep, goats, horses) that were found
pregnant when they were slaughtered in their facilities in 2015.
any particular action foreseen in the surveyed facility when a pregnant animal has been
slaughtered or if there is any particular action applied for managing the fetuses.
the estimated proportion of fetuses per gestational age category after killing of the dam and, if
present, the protocol used for establishing the gestational age. To facilitate the respondents’
answer to the ﬁrst part of this question, the categorisation tool used in the German project S!
GN was reproduced in the questionnaire.

The surveys were performed in the period February–April 2016.
The questionnaire was also shared with the other Member States who requested the mandate, so
that they could use it for their ongoing national projects on this topic.

2.2.

Uncertainty

The EFSA’s Scientiﬁc Committee is developing a guidance document (EFSA, under development) to
offer a toolbox of methodologies – both quantitative and qualitative – for analysing scientiﬁc
uncertainties in all its scientiﬁc assessments. Through the application of these tools EFSA aims to give
decision-makers a clearer picture of the scientiﬁc uncertainties affecting each assessment.
This mandate has been chosen as a case study for testing the applicability of the approach
proposed in the draft Guidance on Uncertainty in the EFSA scientiﬁc assessment. The experience
gained with this speciﬁc risk assessment and the other case-studies identiﬁed in each Unit in EFSA will
be used to ﬁne-tune the Guidance document.
In this mandate, it was decided to apply approaches from the uncertainty guidance to ToR1 and
ToR3. In both cases, an Expert Knowledge Elicitation was performed and uncertainty was quantiﬁed by
appropriate statistical methodology (see below). The other ToRs were addressed by the Panel through
appraisal of the scientiﬁc literature.

2.3.

Methodologies

2.3.1.

Methodology for ToR1 (prevalence of pregnant animals at slaughter)

Several methods have been used to gather scientiﬁc publications, reports and ofﬁcial documents
relevant for this opinion. A literature search was conducted on Web of Science. Detailed information on
the literature search performed is provided in Appendix A. Literature from outside Europe was not
considered relevant. The number of papers with information related to the prevalence of pregnant
animals slaughtered was very limited. Additional papers and speciﬁc reports from Member States were
found on the web (Google search) or provided by the experts of the Working Group (WG).
As described under the section on data for ToR1 (see Section 2.1.1), estimates about the prevalence
of pregnant livestock animals slaughtered and the developmental stage were collected in 10 EU
countries through surveys requesting slaughterhouse operators to give a personal estimate of
prevalence of slaughtered pregnant animals and their distribution across terms of gestation. The
experts who performed the surveys were then invited to an Expert Knowledge Elicitation (EKE) meeting
that was held on 16–17 June 2016 at EFSA premises. In EKE 1,7 following the EFSA guidance on EKE
(EFSA, 2014), the experts were asked, based on the estimates collected through the surveys, to give
probability judgements per species about the overall prevalence of pregnant animals slaughtered at
European level and respective proportions for terms of gestation. Finally, a collective view on the
prevalence and phases of gestation of slaughtered pregnant animals per each livestock species in
Europe was agreed upon (see Appendix C for EKE 1 report). At the EKE 1 meeting, the prevalence
estimates for pregnancies distributed along the three terms of gestation were obtained as prevalence in
each term of gestation out of the total number of female animals slaughtered. After the meeting, the
probability distribution of animals in the third term of gestation was recalculated, using the original raw
data from individual responses, to provide the percentage of animals in the third term of gestation out
of the total number of pregnant female animals. In the opinion, only the latter is reported.
7

Since two EKE meetings were performed for the development of this opinion, from here onwards this ﬁrst meeting will be
referred to as EKE 1, and the second as EKE 2 (see Section 2.3.3).

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Uncertainty involved in estimating the prevalence is represented using a probability distribution
which expresses the likelihood of possible estimates. These distributions were obtained from a
structured expert knowledge elicitation considering both available evidence (e.g. existing survey
results) and judgements on the remaining uncertainties. Judgements on the prevalence of gestation
and conditional prevalence on the gestation stage were combined by stochastic simulation to obtain
the unconditional prevalence of the gestation stage, whereby values were drawn randomly from the
distribution speciﬁed for each input parameter. For these calculations, smooth distributions were ﬁtted
to the speciﬁed percentiles. The stochastic simulations were repeated at least 10,000 times to
generate a probability distribution of outcomes. The distributions of the uncertainty components are
characterised by different values and ranges. The median is a central value with equal probability of
over- or underestimating the actual value. The interquartile range which is bounded by the 1st and 3rd
quartile (the 25th and 75th percentile) of the distribution is an interval around the median, where it is
as likely that the actual value is inside as it is likely that the actual value is outside that range. This
range expresses the precision of the estimation of interest. The wider the interquartile range, the
greater is the uncertainty on the estimate. In this opinion, we refer to the interquartile range by using
the term ‘50% uncertainty range’.
Following the meeting, a summary report of the proceedings was produced and circulated
electronically to all participants to check for accuracy. Corrections were incorporated in a ﬁnal report
provided as an Appendix to the opinion.

2.3.2.

Methodology for ToR2 (reasons for slaughtering pregnant animals and
recommendations to reduce the number of pregnant animals slaughtered)

This opinion suggests reasons for knowingly and unknowingly slaughtering pregnant animals. A
literature search was conducted on Web of Science. Detailed information on the literature search
performed is provided in Appendix B. However, the number of papers with information related to
the reasons for slaughtering of pregnant animals was very limited. Additional papers and speciﬁc
reports from Member States were found on the web (Google search) or provided by the experts of
the WG.
For all species, the results of the assessment reﬂect the opinion of the experts of the WG,
considering the results from literature reviews and the outcomes from the discussion held at the EKE 1
meeting on factors increasing the prevalence.
A list of potential measures to reduce the number of animals which are pregnant when slaughtered
is also proposed. This is based on the knowledge of the experts of the WG and the outcomes from the
discussion held at the EKE 1 meeting on factors decreasing the prevalence.

2.3.3.

Methodology for ToR3 (assessment of the scientiﬁc evidence available on
the capacity of fetuses to experience pain)

Regarding the assessment of potential suffering in fetuses, the scope was not exclusively on
pain, but also on other types of negative affect (e.g. possible discomfort experienced by the fetus
during asphyxia in utero). Anatomical/morphological/physiological structures to experience pain/
negative affect as well as evidence for capacity to experience pain/negative affect were investigated
separately for each species. These were addressed by focussing on new evidence available since
the past EFSA opinions of 2004 (EFSA, 2004, 2005). Furthermore, the evidence used in the EU
Directive on the protection of animals used for scientiﬁc purposes (DIR. 2010/63/EU) was
considered.
To answer this ToR of the mandate, the WG agreed to use a step-wise approach. The topic was
subdivided into (i) anatomical structures required for perception of pain and other types of negative
affect including discomfort and suffering, (ii) the neurophysiological situation (e.g. inhibitory and
excitatory systems) and (iii) the response of the fetus to speciﬁed stunning and slaughter conditions.
For answering these questions the WG reviewed the available literature. The WG also created a logical
model showing how those subquestions relate to each other to address the overall question on the
capacity of fetuses to experience pain and other negative affect. In addition, an EKE meeting was
performed (c.f. EKE 2) to collect expert judgements related to this ToR through a standardised
methodology (EFSA, 2014). The EKE 2 meeting was held on 6–8 July 2016 and nine external hearing
experts were selected based on the additional expertise needed for the exercise. Expertise needed
related to fetal anaesthesia, fetal consciousness, fetal and neonatal physiology, pain treatment of the
prematurely born child from the human ﬁeld; animal consciousness, animal welfare, fetal
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Slaughter of pregnant animals

consciousness, effect of hypoxia on fetuses and effect of various stunning interventions on fetuses
from the veterinary ﬁeld. Relating to the logical model, the experts were asked to (i) elicit probability
distributions for the propositions in the subquestions to be true and (ii) express the level of uncertainty
associated to each subquestion.
Following EKE 2, a summary report of the proceedings was produced and circulated electronically
to all participants to check for accuracy. Corrections were incorporated in a ﬁnal report provided as an
Appendix to this opinion (Appendix D).
The outcomes of the EKE 2 meeting were evaluated by the AHAW Panel in the context of additional
ﬁndings from the literature and further discussion with some of the EKE 2 experts to generate ﬁnal
conclusions for this opinion. These conclusions were developed by expert discussion and expressed
using the approximate probability scale proposed in the draft Guidance on Uncertainty produced by
EFSA (EFSA, 2016 in progress pp. 58 and pp. 96).
Uncertainty judgements on the substatements and ﬁnal conclusion of the logical model (ToR3) are
expressed as the certainty of the correctness of the statement versus its incorrectness. It is referred to
as percentage certainty with the interpretation of the strength of belief that the statement is correct.
It is to be noted that the uncertainty assessment is addressed differently in ToR1 and ToR3,
particularly. A schematic representation is given in Figure 1. Brieﬂy, for ToR1, the prevalence of
slaughtered pregnant animals was elicited by an Expert Knowledge Elicitation meeting (referred to as
EKE 1). This resulted in ‘median estimates’ for the prevalence (e.g. 3% dairy cows in the last term of
gestation) accompanied by a probability distribution range (e.g. from 9% to 27%) that gives the level
of uncertainty. For ToR3, expert knowledge was elicited on statements e.g. that fetuses have the
anatomical structures required (and further statements derived from the logical model; see below).
The answers were formulated as likelihoods of the statement being true with the distribution of the
answers providing the certainty distribution (e.g. from 5% to 40% likelihood that a certain statement
is true). From the range of likelihood values and further interpretation of the literature, a qualitative
translation of the uncertainty was derived (e.g. very likely).
TOR1

TOR3

Question: What is the prevalence of
slaughtered pregnant animals?

Question: Is a statement e.g. ‘fetuses show
responses to stimuli during slaughter’ correct?

Possible answers: 0–100 %

Possible answers: Likelihood of correctness of
statement

Median estimate: Median prevalence
(with equal probability of over/under
estimation)

vs

Median estimate: Not used
Uncertainty: Range of likelihood values - derived
from the individual judgements of the expert
elicitation group

Uncertainty: P25 – P75 (Range of possible
prevalence values around the median
covering 50% of the probability
distribution)

Qualitative translation of the uncertainty: Based
on the range of likelihood values and further
interpretation of the literature
Qualitative translation

values

Extremely likely

99–100%

Very likely

90–99%

Likely

66–90%

As likely as not

33–66%

Unlikely

10–33%

Very unlikely

1–10%

Extremely unlikely

0–1%

Figure 1: Schematic comparison of the uncertainty assessment of ToR1 and ToR3

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Slaughter of pregnant animals

2.3.4.

Methodology for ToR4 (methods for stunning and killing of fetuses or
neonates of the main livestock species)

Literature review was used as a basis to develop scenarios and related actions relevant to this
question. The past EFSA opinions (EFSA, 2004, 2005) were also consulted as well as the methods
prescribed under Regulation 1099/2009.

2.3.5.

Methodology for ToR5 (methods for estimating the age of fetuses of the
main livestock species at the slaughterhouse after the dam has been
slaughtered)

Literature review was carried out to extract information on potential indicators of fetal age and
whether reliable information on sensitivity and speciﬁcity of indicators exists or could be generated.

3.

Assessment

3.1.

Assessment for ToR1(prevalence of pregnant animals slaughtered
in EU)

3.1.1.

Information on prevalence from Member States

Discussion with Member State representatives of the AHAW network revealed that no ofﬁcial
records of the pregnancy state of slaughtered animals were available. Few countries provided some
information: in Latvia, the number of animals reported in 2014 to the national authorities as having
been killed pregnant was four dairy cattle (between 5 and 8 months of pregnancy) and one sow. In
Lithuania, the ofﬁcial inspectors in slaughterhouses estimated that the percentage of pregnant animals
slaughtered annually is less than 5%. As explained in Section 2.1.1, further information was collected
about possible infringements of regulation 1/2005; however, most of the Member States do not specify
the cause of the non-compliances due to animals unﬁt for transport. The number of non-compliances
due to animals slaughtered in the last 10% of pregnancy was only reported by Belgium (15 bovines in
2015) and Catalonia (15 bovines, 6 horses and 1 ovine in 2015, and 21 bovines, 11 horses and 4
sheep in 2014).

3.1.2.

Information on prevalence from literature

The literature search resulted in 16 papers that were further assessed. The results of the search
are reported in Table 1 below divided by species and country. When available, the proportion or
number of pregnant animals at slaughter and the stage of pregnancy are reported.
Table 1:

Results of the literature search on the prevalence of pregnant animals slaughtered in the EU and Switzerland
divided by species and country (n.a.: data not available)

Species Country

Percentage/number of
animals found pregnant
at slaughter

Percentage per term of gestation
Of pregnant animals

6.3% 3rd term

26.8%

Singleton and
Dobson (1995)

LU: 25% 3rd term
DE: 46% 3rd term
IT: 15% 3rd term

Di Nicolo (2006)

n.a.

€cker et al.
Lu
(2003)

Cattle

United
Kingdom

23.5% (out of 6,670 cows;
1 slaughterhouse)

Cattle

Luxemburg
Germany
Belgium
Italy

Cattle

Germany

LU: 5.3% (out of 3,619 cows, LU: 1.3% 3rd term
DE: 2.3% 3rd term
range
1.3–5.4%; 3 slaughterhouses) IT: 0.7% 3rd term
DE: 4.9% (out of 1,012 cows;
1 slaughterhouse)
BE: 10.1% (out of 965 cows;
1 slaughterhouse)
IT: 4.5% (out of 3,071 cows;
1 slaughterhouse)
4.4% pregnant (median
n.a.
2.9%; range
0–10.8%; 10 slaughterhouses)

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Reference

Of total number
slaughtered

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Slaughter of pregnant animals

Species Country

Percentage/number of
animals found pregnant
at slaughter

Cattle

Germany

7.1% (median; 53
slaughterhouses,
questionnaire study)
2.6% (out of 115 tracts
examined)

Pig

Sweden

Pig

Finland

Pig

Denmark

Pig

United
Kingdom

13% (out of 142 tracts of
sows and gilts from Scottish
herds culled for infertility)

Pig

Belgium

3%/14% (sows/gilts; out of
502 sows from 7 Belgian
commercial pig herds)

Sheep

Ireland

10% (out of 870 ewes)

Sheep

Spain

n.a.

Goat

Spain

n.a.

Percentage per term of gestation
Reference

Of total number
slaughtered

Of pregnant animals

6.4% 2nd and 3rd term

90% 2nd and 3rd term

Riehn et al.
(2011)

n.a.

n.a.

Dalin et al.
(1997)

1.5% (out of 1,708 sows from No information on stage, but n.a.
one Finnish abattoir over
tracts weighed 2.2 kg with
1 year period)
large SD
4.2% pregnant sows
n.a.
n.a.
involuntarily culled

Heinonen et al.
(1998)
Jensen et al.
(2010)

7.7% early pregnancy (up to 59.2% early pregnancy (up
to 6 weeks gestation),
6 weeks gestation), 2.8%
mid-pregnancy (7–13 weeks) 21.4% mid-pregnancy
(7–13 weeks)
2.8% late pregnancy
21.4% late pregnancy
(14 weeks or more)
(14 weeks or more)
n.a.
n.a.

85.1% early stage of
8.5% early stage of
gestation
gestation
13.8% midgestation
1.4% midgestation
1.1% late gestation
0.1% late gestation
Number of pregnant females Data from Catalan
government
registered over 90%
gestation: 1 sheep (2014)
4 sheep (2015)

Ward et al.
(2010)

de Jong et al.
(2014)
Alosta et al.
(1998)

Number of pregnant females Data from Catalan
government
registered over 90%
gestation: 6 goats (2014)
11 goats (2015)

The literature search revealed a very scattered picture of prevalence of pregnant animals at
slaughter with the limited evidence focussing on German speaking countries in the case of cattle and
North-Western European countries for pigs. Regarding small ruminants and horses, only very little or
no information was available. Since reliable conclusions on the European situation could not be drawn
from the available evidence, it was decided to perform a survey in 10 EU countries to obtain estimates
from slaughterhouse operators of the total prevalence of pregnant animals at slaughter and the
distribution across different phases of gestation. This information served as the starting point for an
EKE meeting to judge the overall European situation.

3.1.3.

Information and weighing of uncertainty on prevalence resulting from
Expert Knowledge Elicitation

Tables 2 and 3 summarise the results of the EKE exercise held in June 16, 2016 (see report in the
Appendix). In Table 2, the median estimate for the prevalence of pregnant animals slaughtered for
each species is indicated. The percentiles (P) which deﬁne the 50% uncertainty range (P25–P75) as
well as the 98% uncertainty range (P1–P99) are also given. As an indication of the uncertainty, there is
a 1 in 2 chance that the actual prevalence lies between the P25 and P75 value, and there is a 98 in
100 chance that the actual prevalence lies between the P1 and P99 value.
Table 3 provides the same information in relation to the percentage of all female animals which are
in their last third of gestation when sent to slaughter.
For bovines, the Elicitation group agreed to differentiate between dairy and beef cattle, due to the
importance of differences in management systems of the two groups. For pigs, the data were
restricted to cull breeding animals and did not include female fattening pigs. The slaughtering of
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Slaughter of pregnant animals

pregnant female fattening pigs can be an issue in farming systems where males for fattening are not
routinely castrated, which is the normal situation in the UK and likely to increase across the EU
because of concerns about the welfare implications of castration. Anecdotally, the proportion of gilts
pregnant at slaughter in the UK is signiﬁcant. Reports from vets working in abattoirs indicated
pregnancy prevalence of at least 10% and up to 40% in extreme cases. These gilts are likely to be in
early pregnancy in most cases because age at puberty will typically be 170–180 days and with current
UK slaughter weights most gilts will be 160–180 days at slaughter. If entire males are kept in countries
where slaughter weight and age is higher, this prevalence could increase, but would be easily avoided
by split-sex rearing.
Due to a limited number of representatives at the EKE meeting from countries where horses are
slaughtered, it was not possible to elicit expert judgements about the prevalence of mares which are
sent to slaughter when pregnant and the respective proportions across the various terms of gestation.
However, the survey data from countries, where slaughtering of horses is practised (Belgium, Ireland,
Italy, Poland, Romania, Spain) indicate a rather low prevalence of pregnant mares arriving at the
slaughterhouse with a maximum of 6% stated for one slaughterhouse, but the majority indicating a
0% prevalence.
Table 2:

Estimated prevalence (median) of mature female animals that are pregnant at the time of
slaughter in Europe, including the uncertainties expressed as probability distribution. The
latter is described by the percentiles (P) which deﬁne the 50% uncertainty range (P25–P75),
as well as the 98% uncertainty range (P1–P99)

All pregnancies

P1

P25

Median

P75

P99

Dairy cows

2%

9%

16%

27%

60%

Beef cattle
Pigs

1%
0%

7%
3%

11%
6%

18%
9%

40%
20%

Sheep

0%

5%

10%

14%

40%

Goats

0%

2%

4%

6%

10%

Table 3:

Estimated prevalence (median) of all mature female animals which are in the last third
of gestation at the time of slaughter in Europe, including the uncertainties expressed as
probability distribution. The latter is described by the percentiles (P) which deﬁne the 50%
uncertainty range (P25–P75), as well as the 98% uncertainty range (P1–P99)

Last 3rd

P1

P25

Median

P75

P99

Dairy cows

0.2%

1.6%

3%

5.2%

14.4%

Beef cattle
Pigs

0.1%
0.0%

0.8%
0.2%

1.5%
0.5%

2.5%
1.0%

7.2%
3.6%

Sheep

0.0%

0.4%

0.8%

1.6%

5.3%

Goats

0.0%

0.1%

0.2%

0.4%

1.5%

Estimates for the percentage of pregnant animals which are in the ﬁrst and second term of
gestation were also obtained from the EKE, but the AHAW Panel considers these estimates unreliable
because of difﬁculties in detection of early stages of gestation in the course of the slaughter process.
3.1.3.1. Country differences in prevalence of slaughtered pregnant cattle
Major differences in the overall prevalence of slaughtered pregnant dairy cows in the EU are due to
the production intensity, i.e. the incidence of production diseases such as lameness resulting in the
involuntary culling of pregnant animals (EFSA, 2009), and to the prevalence of on-farm euthanasia.
Major differences regarding proportions of dairy cows in different terms of gestation at EU level are
linked to the production system (intensiveness of farming and ability to keep records), and to
economic considerations relating to pregnancy anabolism of the dam or the value of the new-born calf.
The EKE participants agreed that the comparatively high prevalence of slaughtered pregnant beef
cattle in some countries may be explained by the type of breed slaughtered by the surveyed abattoirs.

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3.1.3.2. Country differences in prevalence of slaughtered ewes
In most cases, sheep are raised for dual (e.g. meat and wool or milk and meat) or multiple
purposes. Breeding ewes (for reproductive, milk and wool production purposes) and lambs (as
breeding replacements or for meat production) are the dominant sheep types present on farm (EFSA
AHAW Panel, 2014). In intensive and semi-intensive systems, ewes are highly selected for milk yield or
meat traits and the rate of replacement is high. The EKE participants agreed that in those countries
with intensive and semi-intensive systems, pregnant breeding ewes are sent to the abattoir because of
production or health reasons. In extensive and very extensive production systems, where the
stockperson does not have frequent and close contact with the sheep, ewes might be transported to
the slaughterhouse without prior pregnancy diagnosis.

3.2.

Assessment for ToR2 (reasons why pregnant animals are
slaughtered and recommendations to reduce the number of animals
slaughtered while pregnant)

3.2.1.

Summary of known reasons for the slaughter of pregnant animals

The review of the available literature showed that there were very few published articles on
reasons for slaughtering pregnant animals. The results are therefore primarily based on a synthesis of
expert opinion obtained at the EKE 1 and from the knowledge and discussions of working group
members.
In the ﬁrst part of this section, an overview of known reasons for the slaughter of pregnant animals
is reported, while the second part summarises the few publications found for each species.
Pregnant animals may be slaughtered because of lack of awareness of their condition, because of
mistaken belief that the animal might be barren combined with lack of pregnancy testing or
determination of an incorrect test result. Where females are kept together with mature male animals,
particularly in more extensive systems where breeding activity is difﬁcult to monitor, animals may
unknowingly become pregnant. It is also possible that breeding by stray or feral males can
unknowingly occur. Unobserved breeding may also occur in more intensive systems if large herd size
and limited staff time for animal observation pertain. Many farms do not have equipment for
pregnancy testing, or staff may be poorly trained in its use, and animals believed not to be pregnant
and showing no obvious external signs are consequently sent for slaughter. Where animals are traded
through markets or between different farms, information on pregnancy status can be lost during the
transaction process. The ﬁnal owner, knowing the animals could not have become pregnant while in
their premises, therefore unknowingly can send to slaughter an animal which became pregnant during
a previous ownership.
However, in addition to this accidental slaughtering of pregnant animals, various reasons for
knowingly slaughtering pregnant animals were also identiﬁed. These can be divided into three main
categories: health and welfare reasons, management reasons and economic reasons.
Health and welfare reasons may include the slaughter or killing of animals identiﬁed as infected by
a disease whose spread is to be controlled by their immediate removal as a source of further spread.
In extreme cases, this may require on-farm killing as part of an EU or national eradication policy (a
topic outside the scope of this opinion). In other cases, speciﬁc animals identiﬁed as carriers of a
pathogen, which may spread to susceptible animals, may be slaughtered through an abattoir in the
normal way. If a farm is identiﬁed as having infected animals, a management decision may be made to
depopulate the whole farm as a precursor to establishment of a new disease-free population. In this
circumstance, animals at all stages of pregnancy may be affected by the decision, as such
depopulation is usually done in the fastest possible time so as to minimise the risk of possible exposure
of other susceptible animals as well as infection of humans in the case of a zoonosis or for cash-ﬂow
reasons. If disease or injury is causing acute or chronic pain to an individual animal, slaughter or killing
may be required on welfare grounds. This may take place on farm if the animal is deemed unﬁt for
transport or if the disease or injury makes the meat unﬁt for human consumption. However, in other
circumstances including chronic disease states, loss of condition or old age, in which animals fail to
thrive or produce efﬁciently but have meat ﬁt for human consumption, animals may be sent to an
abattoir.
There are also situations in which animals are deliberately made pregnant for management
reasons, despite knowing that they will subsequently be slaughtered. This can occur when an excess
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Slaughter of pregnant animals

number of animals in a batch production system are inseminated to ensure that, allowing for possible
conception failures, the correct batch size will be achieved to maximise subsequent utilisation of
facilities. Once the pregnancy outcome of each animal is known, a selection is made of the best
individuals to retain and the surplus are sent for slaughter, usually in early pregnancy. Such an
approach is commonly recommended in the case of batch farrowing systems for sows, where it is
widely recommended to serve all available sows (see WattAgNet8), and then to cull the excess animals
after pregnancy diagnosis has conﬁrmed which ones have successfully conceived. With this practice,
slaughter is likely to be in early/mid-pregnancy as the batch would normally receive a pregnancy
diagnosis at 4 weeks after service.
Animals may also be made pregnant, despite the intention for subsequent slaughter, to modify their
behavioural characteristics in ways desirable for the duration of their period on the farm. This is most
commonly seen in the case of dairy cattle, where non-pregnant animals show periodic disruptive riding
behaviours associated with oestrus.
Economic reasons giving rise to the slaughter of pregnant animals may relate to a conscious
decision at the time of insemination to exploit pregnancy anabolism in meat animals (Robinson, 1986),
or to improve carcass quality by reducing consequences of preslaughter stress on meat quality
(Ferguson and Warner, 2008). These practices were identiﬁed as applying particularly to cattle.
In contrast to these planned strategies, unplanned slaughter of pregnant animals may also be
dictated by economic circumstances because their unexpectedly poor performance, such as low milk
yield in dairy cattle or sheep, makes it uneconomic to retain them until their next parturition. Changes
in the market opportunities may also result in pregnant animals being sold. For example, seasonal
marketing opportunities give higher values to sheep or goat sales at particular times, such as around
Easter or end of Ramadan, and animals may be held back to older ages to exploit these markets or a
decision taken that their value for slaughter in these market conditions outweighs the value of keeping
them until the offspring are delivered. If the current market value of the offspring is low, as may be
the case for progeny of dairy cattle and sheep, the incentive to retain less productive animals until
parturition is reduced. Pregnant animals may also be sent for slaughter because of unexpected
extreme economic necessity, as in the case of bankruptcy of a business or an urgent cash-ﬂow
requirement.
Table 4 presents a summary of data found in literature on the reasons for slaughter of pregnant
animals for the different livestock species. Only data on cattle and pigs could be retrieved. Lack of
awareness of pregnancy state was commonly reported, either in association with unplanned matings
or an incorrect pregnancy diagnosis.
Table 4:

Summary of the papers found in literature on the reasons for slaughter of pregnant
animals for the different livestock species (cattle, pigs)

Species

Country

Reason why

Reference

Cattle

United
Kingdom

Lack of awareness of pregnancy (50% of farmers), natural
mating (66% of cows)

Singleton and
Dobson (1995)

Cattle

False negative pregnancy check

Di Nicolo (2006)

Cattle

Luxemburg,
Germany,
Belgium, Italy
Switzerland

Lack of awareness of pregnancy (70% of farmers), high rate of
false negative pregnancy check

BLV (2014)

Pig

Denmark

Pig

United
Kingdom

Among the observed sows, 4.2% were involuntarily culled for
lameness
Infertility incorrectly diagnosed

Jensen et al.
(2010)
Ward et al.
(2010)

Pig

Belgium

4% of the sows culled because they were assumed to be not
pregnant were pregnant and sows culled due to leg weakness
demonstrated 10% pregnancy

de Jong et al.
(2014)

Pig

Norway

Out of the 491 gilts selected for mating, 39 died/were culled
before farrowing their ﬁrst litter because of reproductive
disorders, lameness and injuries

Thingnes et al.
(2015)

8

http://www.wattagnet.com/articles/6652-the-benefits-of-more-informed-sow-culling

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Slaughter of pregnant animals

3.2.2.

Results of expert opinion on the reasons for slaughtering of pregnant
animals

Based on the results from literature review (see Table 4) and the outcomes of the discussion held
at the EKE 1 meeting, the reasons for sending pregnant animals to slaughter are as summarised in the
following Table 5. The relative importance of these causes cannot be established from the available
information.
For bovines, results for dairy and beef cattle are presented separately because of differences in the
management systems of the two cattle categories resulting in differences in the respective inﬂuencing
factors.

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1) Economic crises and
low milk prices
2) Low productivity
during lactation
3) Anabolic effect of
pregnancy (more
muscles)
4) Low calf price

Dairy cows

1) Economic crises
2) Anabolic effect of
pregnancy (more
muscles)
3) Reducing risk of poor
meat quality due to
oestrus (dark cutting
beef)

Beef Cattle

20

1) Economic crises
2) Anabolic effect of
pregnancy (more
muscles)

Pigs

1) Economic crises
2) Low productivity
during lactation
(dairy sheep)
3) Low lamb price
(dairy sheep)
4) Seasonal marketing
opportunities giving
higher values to
ewe sales (e.g.
around Easter, end
of Ramadan)

Sheep

Summary of reasons divided by species and based on expert opinion, for sending pregnant animals to slaughter

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Economic
reasons

Table 5:

Slaughter of pregnant animals

Horses

EFSA Journal 2017;15(5):4782

1) Economic crises
1) Economic crises
2) Declaration for
2) Low productivity
meat
during lactation
consumption or
(dairy goats)
3) Low kid price (dairy
illegal
goats)
slaughtering to
4) Seasonal marketing
reduce killing
opportunities giving
costs of leisure
higher values to
horses
doe sales (e.g.
around Easter, end
of Ramadan)

Goat

1) Pregnancy not
recognised
2) Non-awareness of
pregnancy: (i)
keeping cows with
bulls, especially in
pasture based
farming systems with
less observation, (ii)
lack or failure of
pregnancy tests, (iii)
poor record keeping
on insemination and
pregnancy checks
3) Lack of information
on insemination and
pregnancy checks or
loss of respective
information during
trading
4) Calmer and more
easily manageable
cows, reduced
mounting and risk of
injury

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Management
reasons

Dairy cows

Slaughter of pregnant animals

1) Pregnancy not
recognised
2) Non-awareness of
pregnancy: (i)
keeping cows with
bulls, especially in
pasture based
farming systems with
less observation, (ii)
lack or failure of
pregnancy tests, (iii)
poor record keeping
on insemination and
pregnancy checks
3) Lack of information
on insemination and
pregnancy checks or
loss of respective
information during
trading
4) Calmer and more
easily manageable
cows, reduced
mounting and risk of
injury

Beef Cattle

Sheep

21

1) Pregnancy not
1) Pregnancy not
recognised
recognised
2) Non-awareness of
(pregnancy
pregnancy: (i)
diagnosis in sheep
keeping sows with
is less practiced)
2) Non-awareness of
boars, especially in
pregnancy: (i)
outdoor systems with
keeping ewes with
less observation, (ii)
rams, especially in
contact with wild
pasture based
boars in extensive
farming systems
systems (iii) lack or
with less
failure of pregnancy
observation, (ii)
tests, (iv) poor
lack or failure of
record keeping on
pregnancy tests,
insemination and
(iii) poor record
pregnancy checks
3) Lack of information
keeping on
on insemination and
insemination and
pregnancy checks or
pregnancy checks
3) Lack of information
loss of respective
on insemination
information during
and pregnancy
trading
4) Insemination of a
checks or loss of
higher number to
respective
ensure batch sizes
information during
are maintained,
trading
giving rise to surplus
pregnant animals
5) Fattening pigs in
mixed sex groups
with entire males

Pigs

Horses

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1) Pregnancy not
1) Pregnancy not
recognised
recognised
2) Non-awareness
(pregnancy
of pregnancy:
diagnosis in goats is
(i) keeping
less practiced)
mares with
2) Non-awareness of
stallions,
pregnancy:
especially in
(i) keeping does
free-roaming/
with bucks,
feral systems,
especially in pasture
(ii) lack or
based farming
failure of
systems with less
pregnancy
observation,
tests, (iii) poor
(ii) lack or failure of
record keeping
pregnancy tests,
on insemination
(iii) poor record
and pregnancy
keeping on
checks
insemination and
3) Lack of
pregnancy checks
information on
3) Lack of information
insemination
on insemination
and pregnancy
and pregnancy
checks or loss
checks or loss of
of respective
respective
information
information during
during trading
trading

Goat

Beef Cattle

1) Problems
1) Problems
necessitating
necessitating
slaughter for welfare
slaughter for welfare
reasons or leading to
reasons or leading to
increased costs for
increased costs for
keeping the cows
keeping the cows
(e.g. lameness,
(e.g. lameness,
mastitis or claw
mastitis or claw
problems)
problems)
2) Culling of reactors in 2) Culling of reactors in
disease eradication
disease eradication
control programmes,
control programmes,
e.g. TB, brucellosis
e.g. TB, brucellosis

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Health and
welfare
reasons

Dairy cows

Slaughter of pregnant animals

Sheep

Goat

Horses

22

EFSA Journal 2017;15(5):4782

1) Problems
1) Problems
1) Problems
1) Problems
necessitating
necessitating
necessitating
necessitating
slaughter for
slaughter for
slaughter for
slaughter for welfare
welfare reasons
welfare reasons or
welfare reasons or
reasons or leading to
or leading to
leading to increased
leading to increased
increased costs for
increased costs
costs for keeping
costs for keeping
keeping the sows
for keeping the
the does (e.g.
the ewes (e.g.
(e.g. lameness,
horses (e.g.
lameness, mastitis
lameness, mastitis
mastitis or claw
injuries from
or claw problems)
or claw problems)
problems)
2) Culling of reactors
2) Culling of reactors
2) Depopulation of
accidents)
in disease
in disease
herds for disease
eradication control
eradication control
eradication control
programmes, e.g.
programmes, e.g.
programmes, e.g.
blue-tongue
blue-tongue
PRRS

Pigs

Slaughter of pregnant animals

3.2.2.1. Measures to reduce the number of animals slaughtered while pregnant at a
critical stage of gestation
If risk managers consider that the likelihood of welfare problems in fetuses as indicated by ToR3, together
with other risk management relevant considerations, warrants action then there are several possible options
which might reduce the prevalence of slaughter of pregnant females in the last third of gestation. It is ﬁrst
necessary to ensure that farmers are aware of the reasons why animals pregnant in the last third of
gestation should not be sent to slaughter. This information and education process may then need to be
supported by incentives or penalties. Options may include actions at the level of market price intervention
(e.g. incentives as regards an increase in the value of the new-born animal relative to other products such as
milk or meat) or at the level of risk management (such as a penalty at slaughter for animals presented in the
last third of pregnancy except with veterinary derogation) but these would require a detailed macroeconomic analysis which is outside the remit of the scientiﬁc assessment included in this scientiﬁc opinion.
Therefore, measures that could reduce the number of animals slaughtered when they are in the
last third of pregnancy can be categorised as those designed to increase awareness of the nature and
extent of the problem (1 and 2) or to improve pregnancy testing (3 and 4):
1) Avoid unplanned slaughter (reduce prevalence of production disease). A general
improvement in health status of the herd or ﬂock will make it less likely that animals will
become chronically ill or low producing in later pregnancy, and thus remove the motivation
to slaughter these animals prematurely. Measures to improve health will include correct
biosecurity, an appropriate vaccination strategy and good maintenance of facilities to
minimise the risk of injury and lameness.
2) Avoid unplanned pregnancies. The separate housing of male and female animals throughout
the production period, or the castration of all male animals in mixed sex groups, would
preclude unplanned pregnancies by only allowing supervised breeding. Proper maintenance
of stock-proof fencing between groups is necessary to avoid accidental contact. This
approach is likely to be unfeasible in extensive production systems where stray or feral
males may roam in uncontrolled conditions.
3) Ensure the pregnancy status of all animals is conﬁrmed before sending to slaughter (see
Figure 2 below). Where it is not possible to be certain that unobserved breeding has not
occurred, a conﬁrmed negative pregnancy diagnosis is the only method to ensure pregnant
animals are not unknowingly sent for slaughter. Methods are available for on-farm use by
farm staff or the veterinarian, but false negative results have been reported and it is
essential that staff is trained in correct use and interpretation of these methods.
4) Ensure that information about insemination and pregnancy diagnosis are required in
documentation accompanying animals at the time of sale, so that this information is reliably
transmitted along the trading chain. This could be done by requiring all insemination events,
co-housing with males and pregnancy diagnosis results to be recorded on animal passports.
Effectiveness of these measures in reducing the possibility that farmers send animals in the last
third of gestation to slaughter will be impaired by failure of education and communication strategies
and a pregnancy test efﬁcacy of less than 100%.
3.2.2.2. Decision-tree to support farmers to reduce the likelihood of pregnant animals
sent to slaughter
A decision tree to support farmers to reduce the likelihood of pregnant animals sent to slaughter
during the last third of gestation is presented below in Figure 2. The ﬁrst action, when the planned
date for slaughter is known, is to retrospectively calculate the window of time where the pregnancy
could have been established. A series of questions is then suggested leading to yes or no answers and
thus to the possibility to proceed to slaughter or the need to carry out pregnancy diagnosis
beforehand. Information is required on the puberty age of the animals. Indicative period ranges for
the timing of puberty and length of pregnancy in females of different livestock species are reported in
Table 6 below the ﬁgure (taken from the Merck Veterinary Manual9). However, puberty onset may be
modiﬁed within species by genetic, nutritional and environmental inﬂuences, particularly contact with
males, and more speciﬁc benchmarks for each farm circumstance should be sought. For multiparous
9

http://www.merckvetmanual.com/reproductive-system/reproductive-system-introduction/overview-of-the-reproductive-system
#v4663856

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Slaughter of pregnant animals

animals where the date of previous parturition is known, this can also be used in determination of the
possibility that an animal could be in the last third of a subsequent pregnancy. In the case of cattle, it
is legally required that this information is recorded in the Livestock Database (Maher et al., 2008).
Pregnancy diagnosis is suggested at different points in time. Various methods exist to diagnose
pregnancy in farmed animals; they are discussed after Figure 1.
KNOWING THE DATE OF SLAUGHTER, DETERMINE THE CRITICAL TIME WINDOW
DURING WHICH PREGNANCY WOULD NEED TO BE ESTABLISHED TO CAUSE A
PROBLEM FOR SLAUGHTER

DURING THAT PERIOD COULD THE ANIMAL HAVE BEEN IN A FERTILE STATE, I.E.
HAD IT PASSED THE STAGE OF PUBERTY OR PUERPERIUM?

NO

YES

DURING THAT PERIOD, WAS THE ANIMAL ARTIFICIALLY INSEMINATED OR DID
IT HAVE ANY POSSIBILITY TO BE IN CONTACT WITH AN ENTIRE MALE?

NO

MAYBE / YES

HAS THE ANIMAL HAD A PREGNANCY TEST?

YES

HAS THE TEST BEEN
CONFIRMED
NEGATIVE?

NO

YES

DO A PREGNANCY
TEST

WAS THE RESULT POSITIVE?

NO

YES

IS PREGNANCY IN THE LAST THIRD?

PROCEED TO
SLAUGHTER

NO

DO NOT SEND
FOR
SLAUGHTER

YES

Figure 2: Decision tree to support farmers to reduce the likelihood of pregnant animals sent to
slaughter during the last third of gestation
Table 6:

Indicative period ranges for the timing of puberty and length of pregnancy in females of
different livestock species
Species
Cattle

Sheep

Goats

Pigs

Horses

Age at puberty (months)

10–12

6–9

5–7

6–7

10–24

Length of pregnancy

9 months

5 months

5 months

3 months
3 weeks
3 days

11 months

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Slaughter of pregnant animals

3.2.2.3. Methods for pregnancy diagnosis
Methods for pregnancy diagnosis fall into four broad categories, which have different degrees of
reliability and on-farm practicality (Ishwar, 1995; Purohit, 2010). In general, the emphasis in scientiﬁc
study has been on the reliability of early detection of pregnancy as soon as possible after insemination,
as this has important economic effects. The reliability of diagnosis of later stages of pregnancy, as
more relevant for this Opinion, has received less study.
External observation
This relies on visual observation of morphological changes in animal size, shape or other features
associated with pregnancy. These include growth of the abdomen as uterine volume expands, increase
in size of the mammary glands (e.g. from 4 months onwards in dairy heifers), vaginal discharge (e.g.
from 4 to 5 months onward in dairy cows) and fetal movements seen by movement of the abdominal
wall (6 months onwards in cattle). These changes usually only become apparent in late pregnancy as
fetal size becomes signiﬁcant and as the endocrine changes associated with preparation for parturition
and lactation are initiated. They are generally very unreliable for the purposes of pregnancy diagnosis
as they may be inﬂuenced by the body condition of the dam, the presence of a thick coat or ﬂeece
and number or size of fetuses present. The absence of any signs of oestrus behaviour, such as intense
activity, mounting or being mounted, is also sometimes taken as a sign of pregnancy, but is again very
unreliable because of the sporadic nature and large individual differences in expression.
Physical examination
These methods rely on external palpation of the abdomen or rectal palpation of the uterus.
Abdominal palpation can detect the fetal presence in cows from ~ 7 months onwards and in small
ruminants from ~ 4 months. However, the method is unreliable and can be inﬂuenced by maternal
body condition.
Transrectal palpation is the most widely used method in large animals (cattle, horses), but requires
facilities for restraint of the animal. It is considered accurate for a trained person from ~ 35 days in
cattle and ~ 20 days in horses, by detection of uterine changes, but becomes more reliable as
pregnancy progresses and direct palpation of the fetus is possible. In pigs and small ruminants, the
method is limited by the size of the pelvis and rectum/anus and therefore less practical.
Ultrasonic methods
This method relies on reﬂection of high frequency sound waves which occurs differentially according
to tissue acoustic impedance. A simple on-farm equipment uses either A-mode ultrasonography or
Doppler detection. A-mode detectors generally operate based on detecting the presence of anechoic
ﬂuid within the uterine lumen. This has been shown to be reliable from 50–120 days of gestation in
small ruminants, with commercial devices showing accuracy (combining both sensitivity and speciﬁcity)
of positive pregnancy diagnosis exceeding 95% after 50 days (Watt et al., 1984). False negatives may
occur in late gestation because of the decrease in ratio of uterine ﬂuid to fetal tissue.
Doppler-based detection is based on detection of movements associated with increased blood ﬂow
in the uterine artery, or later the fetal heartbeat. Accuracy has been reported as 100% in sheep
between 66 and 122 days of gestation (Shone and Fricker, 1969). In sows, the test has been reported
to have 86% accuracy at 31–35 days, with a similar accuracy for A-mode ultrasound (Almond and Dial,
1986).
More sophisticated equipment uses B-mode ultrasonography, which generates a 2-D picture of
tissue structure for diagnostic imaging. In early pregnancy, the presence of anechoic ﬂuid within the
uterine lumen is used diagnostically, but later the fetal heart beat and fetal skeleton can be seen (e.g.
fetal bone by day 60 in cattle and day 70 in sheep). This technique also allows the possibility of
estimating fetal age by morphological characteristics, but the equipment is likely to be too expensive
and lacking in robustness for widespread routine on-farm use.
Ultrasonography can be carried out transabdominally in pigs and small ruminants (after coat
clipping), and is often used transrectally in cattle and horses. Transrectal scanning is possible in small
ruminants with a specialised probe, and more accurate in the early stage of pregnancy (before
50 days). In goats, 98% sensitivity and 100% speciﬁcity have been reported after 26 days (Gonzalez
et al., 2004). However, good restraint facilities are necessary to minimise the possibility of injury during
the process, making it less suitable for ﬁeld conditions. To ensure reliable results from ultrasonographic
pregnancy diagnosis, staff should have appropriate training to operate equipment and interpret results.
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Slaughter of pregnant animals

Biochemical markers in body ﬂuids
The most commonly used endocrine marker is progesterone, which shows sustained elevation in
pregnant animals. This can be measured in serum or in milk of lactating animals. Measurement by
radioimmunoassay requires specialised laboratory facilities but enzyme-linked immunosorbant assay
(ELISA) tests have now been developed as commercial kits which can be used on farm for immediate
results. Sensitivity of the test (i.e. correct detection of animals which are pregnant) is generally good,
but speciﬁcity (i.e. ability to correctly detect animals which are not pregnant) can be low because of
false positives occurring during the luteal phase of the oestrus cycle of non-pregnant animals, ovarian
cysts or cases of embryonic death. In small ruminants, different studies have reported accuracy of
detecting non-pregnancy by milk samples or blood samples as 100%, or of correct pregnancy
conﬁrmation as 80–90% (Holdsworth and Davies, 1979; Gonzalez et al., 2004). In sows, a serum
progesterone test has been reported to have 92% accuracy at 31–35 days (Almond and Dial, 1986).
Other diagnostic markers include the presence of estrone sulfate (ES) in urine, milk, faeces or
blood, and commercial kits based on this have been developed for use in horses after 120 days. It is
detectable in serum of sheep from ~ 70 days, and goats from ~ 50 days. In goats, a milk ES ELISA
had a reported accuracy of 82% for pregnancy conﬁrmation (Murray and Newstead, 1988). In sows,
the test on blood samples has been reported to have 98% accuracy at 31–35 days (Almond and Dial,
1986), while a faecal test gave a sensitivity of 96% and speciﬁcity of 94% at this stage (Vos et al.,
1999). The ﬁeld measurement of urinary oestrone conjugates in horses by ELISA was reported to give
100% accuracy (Kirkpatrick et al., 1993). Furthermore, the same authors reported a 83% accuracy for
a simple urinary dipstick ELISA for detection of equine chorionic gonadotrophin, although this was
effective only between ~ 35 and 140 days and not in later pregnancy.
Another widely used diagnostic marker for cattle and small ruminants is the presence of pregnancyassociated glycoproteins (PAG). These can be used from ~ 30 days post-breeding. In goats, a PAG
plasma test by radioimmunoassay (RIA) has been shown to have sensitivity and speciﬁcity of 100% by
26 days (Gonzalez et al., 2004). In cows of > 60 days, a milk PAG ELISA test for conﬁrmation of
pregnancy gave 98–99% sensitivity and 92–100% speciﬁcity (LeBlanc, 2013; Lawson et al., 2014).
At the present time, reliable and feasible on-farm detection of animals in the last third of gestation
should be achievable by:
Pigs: transabdominal Doppler ultrasound
Dairy cattle (lactating): milk progesterone, PAG or rectal palpation
Beef cattle: rectal palpation
Dairy sheep/goats: milk progesterone, PAG or transabdominal ultrasound
Meat sheep/goats: transabdominal ultrasound
Horses: rectal palpation

3.3.

Assessment for ToR3 (assessment of the scientiﬁc evidence
available on the capacity of fetuses to experience pain and other
negative affect)

The topic was subdivided into (i) anatomical structures required for the perception of pain and
other negative affect, (ii) the neurophysiological situation (e.g. inhibitory and excitatory systems) and
(iii) the response of the fetus to speciﬁed stunning and slaughter conditions. The WG created a logical
model showing ﬁve subquestions that link together to address the overall question on the capacity of
fetuses to experience pain and other negative affect. As explained in Section 2.3.3, to answer the
subquestions, a literature review was completed and an EKE 2 exercise was held. Finally, the experts
of the Panel expressed, based on the outcomes of literature and EKE 2, probabilities for each
subquestion by expert discussion. The following chapters present the logical model, a summary of the
scientiﬁc evidence available for each subquestion of the logical model and the outcomes of the expert
discussion.

3.3.1.

Working deﬁnitions

3.3.1.1. Deﬁnition of fetus
In this opinion, the term fetus is used for a developing organism from the time of implantation until
the moment it takes its ﬁrst breath ex utero.

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Slaughter of pregnant animals

3.3.1.2. Deﬁnitions of nociception (sensory perception) and pain (emotional experience)
Nociception can be deﬁned as the physical activation of neuronal pathways by potentially harmful
stimuli, with or without the subjective emotional experience of pain. For example, somatic reﬂex arcs
occur at the level of spinal cord or even at the brain stem level in response to a stimulus without
involving higher centres in the brain. Knee-jerk response is a typical example of a spinal reﬂex.
This opinion uses the deﬁnition of pain from the International Association for the Study of Pain
(IASP): ‘Pain can be deﬁned as an unpleasant sensory and emotional experience associated with actual
or potential tissue damage, or described in terms of such damage’. It therefore requires the presence
of consciousness as prerequisite to evaluate a stimulus as unpleasant. In this regard, the sensory and
emotional experiences may also include other forms of suffering, i.e. negative affect or mental states.
3.3.1.3. Deﬁnition of consciousness
For this scientiﬁc opinion, the words ‘consciousness’ and ‘awareness’ are considered synonymous.
Awareness is often referred to as one of two aspects or dimensions of consciousness, namely the
‘content’ of consciousness, while the other aspect reﬂects the ‘level’ of consciousness, which addresses
the level of arousal or wakefulness (Laureys et al., 2009). Both aspects are usually positively
associated thus not requiring a distinction. Awareness may also be addressed as the ‘raw material’
from which animals develop consciousness, i.e. the knowledge about the internal state or the external
environment by way of sensory perception and processing presumably at the brain stem level
(‘knowing what is going on’ as opposed to nociception), and therefore regarded a prerequisite for
consciousness, but this distinction is again not consistently made. This is also reﬂected in very similar
deﬁnitions for both terms in dictionaries (see Le Neindre et al., 2017), who provide an extensive
review of the concepts of consciousness in humans and animals) or in the synonymous use of the
terms in scientiﬁc literature (e.g. Duncan, 2006).
Consciousness of an animal is essentially its ability to cognitively process and subjectively evaluate
internal and external sensory inputs and to feel emotions. It also implies decision-making and
voluntary motor responses as opposed to mere reﬂexes. Sentience, i.e. the (functional) capacity to
perceive sensations originating from sensory inputs, which is present from a certain developmental
stage onwards (see Table 7 below), is considered fundamental (Mellor and Diesch, 2006).
Furthermore, consciousness requires being awake, while nociception can occur during sleep and may
induce arousal and awakening.

3.3.2.

Logical model

The logical model is shown in Figure 3 as a ﬂow chart. It shows a series of subquestions in boxes
and how they link together to address the overall question. The subquestions (indicated in the
Figure as C.1–C.5) are then addressed separately in the following sections considering the available
scientiﬁc evidence and the expert judgements. For each subquestion, the box reports the paragraphs
including the relevant scientiﬁc literature and/or the paragraph including the outcomes from the expert
judgements.
While most the scientiﬁc evidence addresses the question of cortically based consciousness, more
recently subcortically based consciousness has been hypothesised (Merker, 2007; Campbell et al.,
2014). In this context, the logical model can be considered in both the context of cortical and
subcortical awareness (see EKE 2 report in Appendix D).

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C3. SPECIFIED STUNNING &
SLAUGHTER CONDITIONS:
•
Electrical stunning
•
Mechanical stunning
•
Gas stunning
•
S cking
See SecƟon 3.3.3.4.(literature) and
SecƟon 3.3.4.3. (expert judgement)

C1. Do livestock fetuses, at any gesta onal
age, have the anatomical and
neurophysiological correlates/structures
necessary for percep on of pain and
nega ve aﬀect?
See SecƟon 3.3.3.1. (literature) and
SecƟon 3.3.4.1. (expert judgement)

C3 a. Do livestock fetuses at any
gesta onal age show a response to
hypoxia (i.e. hypoxia reaching the
foetus following the stunning
and/or s cking of the dam)?

Probability

C2. If so, does the neuro-physiological
situa on (e.g. inhibitory and excitatory
systems) allow for percep on?
See SecƟon 3.3.3.2. (literature) and
SecƟon 3.3.4.2. (expert judgement)

C3 b. Do livestock fetuses at any
gesta onal age show a response to
hypercapnia/hypoxia?

Probability
a
b
c
d
Probability

C3 c. Do livestock fetuses at any
gesta onal age show a response to
physical s mula on (e.g. seizures
of the dam, movements)?

C4. Will the livestock fetus EXPERIENCE a
NEGATIVE AFFECTIVE STATE arising from the
SPECIFIED CONDITION?
See SecƟon 3.3.4.4. (expert judgement)

a b c d

Probability

C3 d. Do livestock fetuses at any
gesta onal age show a response to
electrical s mula on?

C5. If the livestock fetus experiences a
NEGATIVE STATE, what would be the level
(minor, moderate, severe)?
See SecƟon 3.3.4.5. (expert judgement)

*in any of the species under consideraƟon

Figure 3: Logical model for assessment of ToR3 (capacity of fetuses to experience pain and other
negative affect)
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3.3.3.

Summary of available scientiﬁc evidence for ToR3 (capacity of fetuses to
experience pain and other negative affect)

3.3.3.1. Summary of scientiﬁc evidence on C1. Anatomical and neurophysiological
correlates/structures necessary for perception of pain and other negative affect
(at cortical and/or subcortical level)
Fetal brain development
The mandate on killing of pregnant animals involves cattle, sheep, goats, pigs and horses and
these species are termed precocial, i.e. their fetal brains are neurologically matured at the time of birth
(McIntosh et al., 1979; Morell et al., 1993). It is worth noting that the maturation of fetal pig brain, as
in humans, continues until the perinatal period (Conrad and Johnson, 2015). Therefore, fetal brain
development data, expressed as a fraction of gestational age, corresponding to sheep, goats, cattle,
and horses may be comparable, and these may be different from pigs. In pigs, the most rapid neural
development occurs between 50 days prenatal and 40 days postnatal (Dickerson and Dobbing, 1967).
Most rodents and carnivores are altricial, i.e. their neonates are born neurologically immature (Dobbing
and Sands, 1979; Clancy et al., 2001), so extrapolation from these species is not appropriate.
Campbell et al. (2014) identiﬁed three phases of neurological developments to be critical for
acquiring capacity for consciousness: (1) development of connectivity of sensory nerves to the spinal
cord and the early development of lower brain centres; (2) the connection of peripheral nerves to
lower brain centres; and (3) integrated neural processing of sensory inputs involving interactivity
between the thalamus and the cerebral cortex via thalamocortical connections.
Fetal brain development involves four key stages: neuronal differentiation, proliferation, migration
and synaptogenesis. For example, in domestic pigs by 20–22 days, the brain has divided into ﬁve
primitive regions: telencephalon, diencephalon, mesencephalon, metencephalon and myelencephalon.
Early cortical development begins at this time with the formation of the preplate and subsequent
increases in neurogenesis and neuronal migration. A graphical representation of corticogenesis in mice
is provided in Figure 4.
It is known that the subplate zone is a transient cytoarchitectonic compartment of the fetal
telencephalic wall and contains a population of subplate neurons (SPns), which play a key role in
normal development of cerebral cortical structure and connectivity. SPns receive thalamic and
neuromodulatory inputs and project into the developing cortical plate. Thus, SPns form one of the ﬁrst
functional cortical circuits and are required to relay early oscillatory activity into the developing cortical
plate. In mammals, SPns are well developed by the mid-pregnancy stage.

Figure 4: Visualisation of corticogenesis (i.e. migration of neurons formed in the ventricular zones) in
mice during neurodevelopment; by Wikipedia, CopperKettle https://commons.wikimedia.
org/w/index.php?curid=37111233

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Formation of thalamocortical projections
It was suggested that SPns transmit activity patterns to the cortical plate before the thalamic ﬁbres
invade the cortex. However, optical recording and current source density analytical studies did not
demonstrate any activation of the cortical plate before the substantial invasion of the thalamic ﬁbres
(Higashi et al., 2002). Mellor and Diesch (2006) suggested based on these stages of neurological
development in mammalian farm animal fetuses that the capacity for conscious perception develops
during the second half of pregnancy. Timelines for fetal brain developments in the different species are
presented in Table 7.
Onset of somatosensory evoked potentials (SEPs)
According to Tawia (1992), the capacity to consciously perceive somatosensory stimuli is a central
event at the level of the cerebral cortex, not the periphery. In this regard, peripheral somatosensory
receptors transmit information to second order neurons located in the spinal cord and medulla, and
these neurons transmit sensory information to third-order neurons located in the thalamus which, in
turn, relay the sensory input to sensory regions of the cerebral cortex. Sensory information received by
the cerebral cortex is transmitted to the motor cortex where stimulus speciﬁc voluntary movements are
generated, which are then conveyed via efferent neurons to different motor neurons, via the brain
stem or spinal cord, resulting in speciﬁc muscular movements. In this regard, it is worth nothing that
the brain stem neurons, which project axons to the spinal cord in the fetal sheep, are the same as in
other mammalian species. More importantly, these neurons responsible for fetal motor/physical
behaviour reach the spinal cord by 55 days of gestation (0.4 G) in sheep, an age well before the
change in motor behaviour occurs, suggesting that the projections do not become fully functional until
later (Stockx et al., 2007).
Tawia (1992) argues that although the basic neuronal substrate for sensory perception in the fetus
may be developed by midgestation, the functional capacity of the neuronal circuitry is limited because
of its immaturity. In a mature, fully functional nervous system a peripheral somatosensory stimulus is
transmitted to, and perceived at the cerebral cortex where an appropriate response is generated.
Transmission of information requires appropriate neurotransmitters in adequate concentrations and
their receptor systems. Low levels of neurotransmitters within the fetal sensory and motor neurons,
and the spinal cord can be seen as evidence of an immature system. On this basis, elicitation and
measurement of a somatosensory evoked potential (SEPs) in the brain can be considered as evidence
for the existence of a matured nervous system, and hence the capacity for conscious perception. It is
worth mentioning that a mature SEP has several primary components: the presence of a ﬁrst negative
(N1) component is indicative of arrival of the somatosensory stimulus at the cortical level and the
presence of positive components, especially the second positive component (P2) is indicative of the
arrival of the stimulus at the primary somatosensory cortex and information processing (see Tawia,
1992). It is therefore inferred that the elicitation of a mature SEP, especially the late latency potential,
can be seen as an indication of the capacity for somatosensory perception, including pain. Cook et al.
(1987) successfully recorded SEPs from 97 to 148 days old (0.66–0.99 G) in a chronically instrumented
fetal lamb by stimulating the upper lip or upper limb. Stimulation of the upper lip produced SEPs with
a pattern including mean peak latencies of 9, 13.2, 17.8, 21.3, 33.8 and 206 ms at a gestation age of
125 days (0.85 G). Similar peaks, but of slightly later mean latencies, were seen following the upper
limb stimulation.
Onset of cyclical ECoG activity
Electroencephalograms (EEGs) and electrocorticograms (ECoGs) have been used to record
spontaneous and evoked electrical activity in the brain. The ECoGs recorded in fetuses show that it
remains predominantly isoelectric during early stages, develops random activity at about 0.6 of
gestational age and ﬁnally cyclical electrical activity in the brain starts after 0.75 of gestational age (in
sheep), i.e. alternating between a high-voltage, low-frequency (3–12 Hz) ECoG state known as nonrapid eye movement sleep (NREM) and a low-voltage, high-frequency (10–20 Hz) ECoG state known
as rapid eye movement sleep (REM). A so-called ‘awake state’ (AW), occurs brieﬂy in between the two
sleep states and is often referred to as a transition stage (Mellor et al., 2005).
REM sleep becomes established in fetal lambs at 110–125 days of gestational age (0.75–0.85 G)
(Berger et al., 1986), and in late gestation fetal sheep (125–140 days, 0.9 G) the percentage of time
spent in each state was: NREM sleep 53%, REM sleep 41.4% and AW state 5.6% (Ioffe et al., 1980).
Quantitative analysis of the ECoG signals to calculate spectral edge frequency, as a measure of the
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maturation of electrocortical activity in the fetal lamb with advancing gestation, has been used to
determine the frequency below which 90–95% of the power in the spectrum resides (Szeto and
Hinman, 1985; Szeto, 1990). The results showed that at gestational ages below 122–125 days
(0.85 G), only one spectral edge peak was present representing quiet sleep, whereas above this range
of gestational age, two peaks were present representing two sleep states.
Timelines for fetal brain developments in the different species have been estimated by
extrapolating the proportion of gestational age from published sheep fetus data and are presented in
Table 7. Data are not given for pigs because of the uncertainty of extrapolation from sheep indicated
previously.
Table 7:

Species

Estimated timelines for fetal brain developments in the different species

Gestation
period
(days)

Formation of
thalamocortical
projections (Mellor
and Diesch, 2006)

Onset of somatosensory
evoked potentials
(SEPs) (Cook et al.,
1987)

Days

Proportion of
gestation

Days

Proportion of
gestation

Onset of cyclical ECoG
activity (Szeto and
Hinman, 1985;
Szeto, 1990)
Days

Proportion of
gestation

Cattle

280–291

> 140

0.5

244

0.85

224

0.8

Sheep
Goat

144–150
148–156

> 72
> 74

0.5
0.5

125
129

0.85
0.85

> 115
118

0.8
0.8

Horse

330–345

> 165

0.5

287

0.85

264

0.8

Pig

112–120

> 56

0.5

n.a.

n.a.

n.a.

n.a.

Development of fetal reﬂexes and capacity for independent existence
As with brain development, most information on this subject comes from studies on sheep fetuses,
although extrapolation to the other precocial species again seems reasonable.
Fetal body movements
Ruckebusch et al. (1977) deﬁned three types of fetal movements in sheep fetuses: (1) simple fetal
movements involving activities such as extension of the head and forelimb, without associated changes
in fetal heart rate; (2) complex fetal movements involving 2–3 large deﬂections of the limb, trunk and
neck, with associated changes in fetal heart rate; (3) gross fetal movements which occur as bouts of
complex movements lasting for 3–10 min, about 15 bouts per day, and which are restricted to the AW
state. It is inferred that fetal body movements also occur in both sleep states, but vigorous body
movements occur as breathing and swallowing mainly during brief periods of AW state. However, this
state is unlikely to represent wakefulness, and these fetal body movements are vital for the
development of lungs and musculoskeletal systems (Rurak, 2016).
Rurak and Wittman (2013) measured fetal lamb motility and abdominal diameter at weekly
intervals for 30 min from 55 days of gestation (0.37 G) to term. The body movements observed in this
study were movements of the limbs and body of the fetus sufﬁcient to cause displacement of the fetal
trunk. The results showed that fetal movement counts/min were relatively constant between 55 and
about 90 days (0.6 G), and declined progressively thereafter, the breakpoints in the regression curves
ranged from 65 to 110 days of gestation and averaged 91.9 + 5.2 days. Fraser and colleagues have
studied fetal movements in sheep, cattle and horses (Fraser et al., 1975; Fraser, 1976, 1989; Husa
et al., 1988). The types of movements observed include rapid opening and closing of the mouth in the
late gestation sheep. In the fetal horse, simple movements were ﬁrst detected at 90 days of gestation
(0.27 G) and the incidence increased until about 180 days (0.53 G), remained at a plateau until
250 days (0.74 G), then decreased until 280 days (0.83 G), and remained at that level until term.
There was an increase in the duration of quiescent periods with advancing gestation. In cattle, simple
fetal movements increased between 4 and 6.5 months (0.68 G) and then decreased, although the
magnitude of the decrease is less than that in fetal cattle and horse. In all the three species, speciﬁc
‘righting reﬂexes’ were observed in late gestation, which are postural and positional changes (foreleg
extension and head elevation) manifested by the fetuses of these quadruped species in the prepartum
period in preparation for birth. They occurred over the last 2 days of gestation in sheep, 1 day
prepartum in the cattle, and in early labour in the horse. These fetal movements in utero appear to be
purposeful in preparation for the passage through the birth canal.
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Fetal breathing movements
The pattern of breathing seems to change with the gestation age of the fetal lamb, depending upon
the method used to record breathing movements. When diaphragmatic activity, recorded using
electromyogram (EMG), was used there was continuous breathing prior to 110 days of gestation
(0.75 G), breathing becomes episodic after 110 days, and at 120 days (0.82 G), the episodic breathing
is largely restricted to REM sleep (Dawes et al., 1972; Clewlow et al., 1983). Between 134 days (0.92 G)
and term, the incidence of breathing decreases (Berger et al., 1986). In contrast, when fetal breathing
was measured using real time ultrasound, the incidence of breathing has been reported to increase from
6% at 55–64 days (0.4 G) to about 45% between 95 and 134 days of gestation (0.78 G) (Rurak and
Wittman, 2013). More importantly, at no stage of fetal development is the breathing continuous.
Nevertheless, two types of breathing movements can be recognised in fetal lamb: (1) single, large
amplitude inspiratory effort, and (2) rapid irregular breathing movements (Dawes et al., 1972). Rapid
irregular breathing activity occurs mainly during REM sleep. The single inspiratory efforts, often
referred to as gasping, occurred 4% of the time. Occasional gasps were not related to any sleep or
AW state (Ioffe et al., 1980). Measurement of ﬂuid movement in the sheep fetal airways associated
with breathing indicated that the ﬂuid volume rarely exceeded 0.5 mL (Dawes et al., 1972). Further
studies revealed that the glottis remained closed when these gasps occurred, leading to the conclusion
that these inspiratory efforts mainly occurred during quiet sleep and closely resembled regurgitation
associated with rumination after birth (Harding et al., 1980). When observed in fetal pigs, the
inspiratory efforts have been termed hiccups (Harding et al., 1991).
Fetal lung development
There are ﬁve stages of lung development in sheep (Alcorn et al., 1981; Gnanalingham et al.,
2005):

•
•
•
•
•

Embryonic – 0 to 40 days
Pseudoglandular – 40 to 80 days
Canalicular – 80 to 120 days
Saccular – 120 to 148 days
Alveolar – 140 days to early postnatal

Studies involving artiﬁcial ventilation of lungs of fetal lambs of different gestational ages showed
that, inﬂation of lungs is difﬁcult in fetuses of less than 110 days of gestational age and, consequently,
they are unable to oxygenate their blood adequately, and hence have reduced viability (Born et al.,
1955). Additionally, functional maturity of lungs is attained over the last few days of gestation after
140 days in fetal sheep (Kitterman et al., 1981).
Based on the available data, it is therefore inferred that only fetuses in the last third of gestation
will have the anatomical and functional brain structures associated with the perception of pain or other
negative affect. In addition, fetal body and respiratory movements do not represent evidence for
capacity to perceive pain or other negative affect. It is also evident that fetuses will require the
anatomical development necessary to inﬂate lungs and the capacity to breathe and oxygenate the
brain in order to survive independently.
3.3.3.2. Summary of scientiﬁc evidence on C2. Neurophysiological situation (e.g.
inhibitory and excitatory systems) and possibility of cortically based perception
Even if a fetus has full development of the peripheral and cortical anatomical features required to feel pain,
or other noxious stimulation of sensory mechanisms, this does not mean that it necessarily experiences an
unpleasant affective state when nociceptive pathways are stimulated, even if a motor response is observed.
To perceive negative affect, it is generally accepted that the fetus must be in a conscious state. Thus, a
functional cortex is deemed necessary for pain experience but not sufﬁcient (RCOG, 2010).
To emotionally experience pain or negative affect, the animal has to be cognitively aware of the
stimulus (a cortical process), which most scientists believe requires that it is awake. Wakefulness is a
state of brainstem and thalamic activity, described by Mellor et al. (2005) as a state of non-sleeparousal, whereas consciousness additionally requires cortical processing. However, they state that it is
not possible to be asleep and conscious. Being asleep or awake is not as easy to distinguish in the
fetus as it is in adults, but the broad categories can be classiﬁed based on EEG recordings.
Most information on cortical states in the fetus comes from studies in the sheep, which is widely
used as a model for investigation of pregnancy issues in human medicine. There are good reasons to
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believe that these ﬁndings will extrapolate to the other farm livestock species of interest in this
Opinion, since they are all ungulate species.
In late gestation fetal sheep (125–140 days, 0.9 G), NREM sleep accounts for 53% and REM sleep
for 41% of time (Ioffe et al., 1980). Therefore, it is inferred that mammalian farm animal fetuses are
asleep most of the time during gestation. In the other 6% of time, there is greater cortical activity,
with a low-voltage, irregular, mixed pattern of ECoG and simultaneous appearance of vigorous somatic
muscle activity, breathing movements, and the presence of eye activity (Ruckebusch and Gaujoux,
1976; Bissonnette et al., 1995), which some authors refer to as the ‘awake state’ (AW). This gives rise
to the question of whether the fetus is truly awake and conscious during these periods, which typically
occur as the fetus is transitioning into, or sometimes out of, NREM sleep. Mellor et al. (2005) propose
that this AW state represents a transition phase between sleep states, a state which in the newborn is
called indeterminate sleep (Mirmiran et al., 2003), and is not indicative of true consciousness. They
cite as evidence for this view the study of Rigatto et al. (1986), who directly observed an
unanaesthetised sheep fetus, in utero, through a Plexiglas window, for 5,000 h without observing signs
of wakefulness such as eyes opening or coordinated movement of the head.
Dawes et al. (1972) observed fetal sheep at 115–147 days (0.9 G) of gestation that were delivered
into a warm saline bath (39–40°C) adjacent to the ewes under epidural anaesthesia and with intact
umbilical circulation. The authors reported that in sheep fetuses less than 128 days of gestation, it was
difﬁcult to identify the two sleep states as the ECoG signal amplitude was consistently low. In addition,
the periods of apparent AW state were accompanied with movement of limbs, raising of heads,
opening of eyes and the fetuses also responded to tactile and auditory stimuli during this AW period.
However, this behavioural state was not accompanied by breathing. In subsequent experiments on
mature fetal lambs by Dawes and colleagues (unpublished data, cited on pp 93 by Rurak, 2016),
wakefulness was observed when the bath temperature was reduced. In this study, when fetal core
temperature reached about 37°C (compared to normal temperature of 39.5°C), wakefulness was
observed, which included fetuses raising their heads out of the bath and onset of continuous
pulmonary ventilation. More importantly, when the bath and fetal core temperature was raised back to
normal, the pulmonary ventilation ceased and the head of fetus sunk back into the bath. These results
suggest that surface and core cooling of the fetus following birth could be important for the initiation
of arousal, wakefulness and continuous breathing. It is therefore inferred that mammalian farm animal
fetuses are asleep most of the time during gestation and any fetal movements observed during studies
involving exteriorisation of the uterus from the dam (i.e. the pregnant animal) are probably due to the
cooling effect. It has been demonstrated ‘in utero’ that warmth has an inhibitory effect on fetal arousal
(Gluckman et al., 1983).
The lack of consciousness in the fetus is attributed to a range of causal factors. As an evolutionary
mechanism assumed to protect the comfort of the dam and help maintain pregnancy to full term, it is
desirable that the activity of the fetus while in utero should be markedly inhibited. The mechanisms by
which consciousness is suppressed in utero have been reviewed by Lyche et al. (2005) and Mellor
et al. (2005). This involves control over a number of endogenous factors related to fetal oxygenation
(Mellor et al., 2005), supported by physical elements of the uterine environment, which are warmth,
buoyancy and cushioning.
There are several chemical suppressors in utero which act to inhibit neural activity in the fetus to a
far greater degree than is seen postnatally. This has been attributed to the combined neuroinhibitory
actions of adenosine, a powerful EEG suppressor and sleep inducing agent, allopregnanolone and
pregnanolone, two neurosteroids which have anaesthetic, sedative and analgesic actions, and
prostaglandin D2, a potent sleep-inducing hormone. There may be additional neuroinhibitory factors
produced by the placenta which further support these effects.
Adenosine is a purinergic messenger, with a very short half-life of under 10 s, which is produced in
all tissues but primarily in the placenta and, to a lesser extent, the fetal liver (Slegel et al., 1988; Sawa
et al., 1991; Ball et al., 1996). It regulates many physiological processes in excitable tissues by
inhibiting metabolic activity and/or by modulating the supply of metabolic substrates via vasodilatation
(Dunwiddie and Masino, 2001; Porkka-Heiskanen et al., 2002), with high circulating and tissue
concentrations of adenosine promoting sleep and increasing NREM-related EEG activity. In the sheep
and human, the circulating concentrations of adenosine are two- to fourfold higher in the fetus than
the dam (Sawa et al., 1991; Yoneyama et al., 1994). Concentrations increase during hypoxaemia
(Hunter et al., 2003) and it has been suggested that this is an evolutionary mechanism to reduce
metabolic requirement and minimise cerebral neuronal damage when uterine oxygen supply is
compromised (Newby et al., 1990). It has been suggested that the ﬁrst appearance of consciousness
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after birth occurs only when breathing oxygenates the neonate sufﬁciently to remove the dominant
adenosine inhibition of brain function (Mellor and Diesch, 2006). Allopregnanolone and pregnanolone
are metabolites of progesterone which have potent sedative/hypnotic and anaesthetic effects
(Majewska, 1992; Paul and Purdy, 1992). They are primarily synthesised within the central nervous
system (CNS) where they increase the activity of gamma-amino-butyric acid (GABA) inhibitory
pathways modulating EEG activity and behavioural state. During later pregnancy, the sheep placenta
produces large quantities of progesterone (Bassett et al., 1969) and plasma concentrations and brain
concentrations of progesterone and the pregnanes fall markedly after birth (Seamark et al., 1970;
Nguyen et al., 2003). Again, in stress situations such as hypoxia, allopregnanolone levels are increased
in circulating plasma (Nguyen et al., 2003). Prostaglandin D2 is a sleep-inducing hormone synthesised
in the adult CNS. The required enzyme, prostaglandin D synthase, is present in the fetal sheep at 125
and 135 days of gestation (0.85–0.92 G) but not at 90 days (0.61 G), suggesting a role in inducing
sleep in fetal sheep from at least 125 days of gestation (0.85 G), when discrete REM and NREM sleep
states are established. There is some evidence for an additional placental inhibitory peptide, since
infusion of a placental extract suppresses fetal activity and respiration within 2 min (Alvaro et al.,
1993, 1997). A range of other inhibitory factors, including neuropeptide Y (NPY), corticotropin
releasing hormone (CRH) and growth hormone (GH) may also contribute to suppression of fetal
activity in utero (Mellor et al., 2005).
Extrapolation across species may be problematic. Bellieni and Buonocore (2012) have argued that
in the late term human the putative neuroinhibitory substances, adenosine and progesterone, show
fetal levels which are similar to those in the mother, who does not experience analgesia. However, the
scientiﬁc literature is not consistent in this respect. As mentioned previously, in the sheep and human,
the circulating concentrations of adenosine have been reported to be two- to fourfold higher in the
fetus than the dam (Sawa et al., 1991; Yoneyama et al., 1994).
There is a dynamic interaction between oxygen tensions and the concentrations of adenosine and
other neuroinhibitory agents. The fetal lamb’s arterial oxygen partial pressure (PaO2) is usually < 25%
and its arterial carbon dioxide partial pressure (PaCO2) is usually > 135% of the respective values in
the conscious ewe because of the concentration gradients required for these gases to diffuse across
the placenta. In mature animals, this degree of hypoxaemia causes unconsciousness, and it was
suggested that fetal arousal and awareness may be suppressed by low oxygen (O2) status (Mellor and
Gregory, 2003). The suggestion that, because of this fetal hypoxia, it is improbable that the fetus
could experience consciousness before birth was supported by the observation that artiﬁcially
increased fetal O2 tensions stimulate continuous breathing and behavioural arousal in fetal lambs
(Baier et al., 1990; Hasan and Rigaux, 1991), whereas acute reductions in fetal PaO2 decrease the
incidence of behavioural arousal (Bocking and Harding, 1986). It is normally only after birth that a
series of changes induce wakefulness: exposure to cold, physical stimulation of delivery and (in some
species) maternal licking and nosing, and the reduction in umbilical blood supply act to initiate
breathing and increased oxygenation of the blood. It is this change in oxygenation which removes an
over-riding inhibitory effect of adenosine, which when combined with birth-related neuroactivators
allows the neonate to be conscious.
It has been reported that, in mammals born neurologically mature, the withdrawal of
neurosuppression, along with concurrent neuroactivation, leads to the onset of consciousness shortly
after birth (Mellor et al., 2005; Mellor and Diesch, 2006). However, there are indications that
persistence of the neurosuppressive agents after birth may modulate pain responses in the early
neonate. For example, in sheep plasma concentrations of the neurosuppressive agents pregnanolone
and allopregnanolone were found to be signiﬁcant up to 3 days after birth (Nguyen et al., 2003),
leading to the suggestion that these chemicals may continue to exert some cerebral effects after birth,
albeit insufﬁcient to suppress consciousness and concurrent EEG activation (Mellor and Diesch, 2006).
A study investigating the effects of postnatal age on EEG responses to castration in lambs over the
ﬁrst 6 weeks of life identiﬁed an increase in cerebral responsiveness to noxious stimulation over the
period 7–10 days (Johnson et al., 2009), and the authors concluded that the lingering effects of fetal
neurosuppressive mechanisms might have been responsible for the lesser responsiveness in younger
lambs. Quantitative EEG analysis showed that 1-day-old neonatal piglets did not respond to noxious
stimulation caused by tail docking, whereas piglets aged between 5 and 15 days showed a
characteristic nociceptive response (Kells et al., 2013). It is not known whether signiﬁcant
concentrations of these agents are present in the plasma of premature ungulate fetuses of different
gestational ages, and whether they might inﬂuence the capacity to attain full consciousness or
experience pain when exteriorised and exposed to air.
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Despite all the considerations presented above, there is no direct evidence which proves that
fetuses remain unaware and unable to experience pain or negative affect throughout pregnancy, and
some observations have led to suggestions that this may not be the case. While in utero, the sheep
fetus at 0.8 G has been shown to respond to pressure and auditory stimuli/ noise by somatic
movements, tachycardia and changes in ECoG (Ruckebusch, 1972). Fetal lambs also show a
respiratory response to somatic stimulation which varies according to their sleep state; response was
greatest during REM sleep, lowest during NREM sleep, and intermediate during the AW state (Ioffe
et al., 1980). Surgery in unaesthesised lambs (ewes given epidural anaesthesia) provokes strong
movements, especially after 120 days of gestation (0.82 G); no such reactions are seen in the
anaesthesised fetus. Similarly, human fetuses respond to invasive intrahepatic vein transfusion with
vigorous body and breathing movements and a rise in cortisol and b-endorphin levels, which are not
seen following non-invasive umbilical vein transfusion (Giannakoulopoulos et al., 1994). However, such
behavioural reactions can be mediated at the subcortical and brainstem level and are not, therefore,
conclusive evidence for experience of pain or other negative affect (Mellor et al., 2005). It is known
that stimulus processing can be independent of conscious perception, as is demonstrated during
surgery in adult animals under general anaesthesia, where nociceptive stimuli can still elicit
subcortically mediated physiological stress responses despite unconsciousness (Desborough, 2000;
Marana et al., 2000). Electrical activity in the somatosensory cortex can be elicited by sensory input
from the forelimb from about 125 days of gestation (0.85 G) in lambs (Cook et al., 1987). However, it
is suggested that the ‘exaggerated’ responses to nociceptive stimuli seen in the fetus are a feature of
immaturity of the central nervous system rather than enhanced pain perception (Mellor and Gregory,
2003). Despite this view, Mellor and Gregory, 2003 still recommend the use of general anaesthesia of
both mother and fetus to minimise fetal movements during surgery and to ensure the fetus remains
unaroused and unconscious throughout. Even while it is completely anaesthetised, the fetus will exhibit
physiological stress responses due to direct surgical stimulation, to cooling and to increased
hypoxaemia/hypercapnia through compromised placental gas exchange (Jones, 1977; Jones and Fox,
1977; Gunn and Bennet, 2009). In human infants and developing mammals, there is an arousal
sequence including both subcortical or autonomic and cortical changes that occurs both spontaneously
and in response to external stimuli (Lijowska et al., 1997; Dauger et al., 2001; Darnall et al., 2010).
Mellor et al. (2005) discuss further evidence that fetal arousal in response to noxious stimuli is
suppressed, from studies of the intense and potentially painful or distressing stimuli used in
vibroacoustic stimulation (VAS). This is accompanied by variable changes in EEG activity, depending on
the fetal sleep state during stimulation. However, they propose that detailed analysis of the EEG
indicates similar dynamics to those seen during spontaneous sleep state transitions rather than arousal
to an AW state (Schwab et al., 2000).
It is difﬁcult to interpret whether EEG activity is indicative of conscious awareness in the fetus. One
indirect line of evidence would be to identify characteristics of the EEG which are associated with
conscious experience in the only species able to self-report – the human. In human literature,
conscious awareness has been speciﬁcally associated with the presence of late latency potentials
following a somatosensory stimulus (Schubert et al., 2006). They demonstrated that the EEG
associated with conscious stimulus processing differs signiﬁcantly from unconscious processing with
potentials starting around 100 ms after stimulus presentation when the signal is processed in parietal
and frontal cortices, brain regions crucial for stimulus access into conscious perception. In the fetal
EEG, such late latency potentials do exist (Cook et al., 1987), but it is uncertain if the same
interpretation can be made.
Selective responsiveness of the fetus to external stimuli has been shown in several examples. In
human fetuses, an advanced functional magnetic resonance imaging (fMRI) procedure was used to
demonstrate selective cortical processing for the maternal voice at 34 weeks of gestational age
(0.88 G). At 33 weeks, the left temporal cortex was signiﬁcantly more activated during exposure to
voices than to pure tones, while at 34 weeks a differential response to the maternal voice and an
unfamiliar voice was recorded, suggesting the existence of in utero associative learning (Jardri et al.,
2010). Furthermore, a single case study suggests the possibility of operant conditioning of a human
fetus with an increased frequency of kicking induced in response to a reinforcer of paternal
verbalisation (Cautilli and Dziewolska, 2005).
There is also evidence that interventions applied during pregnancy can have long-term effects on
development and behaviour postnatally (Schneider and Suomi, 1992; Janczak et al., 2006). The fetus
of various species has been shown to be capable of ‘associative learning’; stimuli with which the
human fetus has become familiar in utero are differentiated from novel stimuli postnatally. Human
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fetuses, and subsequently neonates, have shown differential response to familiar music (Hepper, 1991)
and to the maternal voice (Hepper et al., 1993). Using the sucking response, neonates have been
shown to differentiate their mother’s voices from other female voices, and the maternal voice is a
more effective reinforcer when compared to other female voices. Furthermore, neonates were shown
to prefer a familiar passage of reading performed during pregnancy over a novel passage of reading,
regardless of whether the passage was recited by the infant’s mother or an unfamiliar woman
(DeCasper and Spence, 1986). There has also been demonstration of postnatal aversion in rodents
when presented with stimuli that were associated with an artiﬁcially induced episode of hypoxia in
utero, or following conditioned taste aversion at the fetal stage (Gruest et al., 2004), and of postnatal
attraction to chemical odours and ﬂavours experienced in the uterine environment in a range of
species (Hepper, 1988; Schaal et al., 2000). This evidence of memory for classical conditioning,
habituation and exposure learning paradigms (James, 2010) is the basis for some to believe in fetal
consciousness, but these could occur by passive learning in the absence of any conscious state. Such
‘fetal learning’ responses do not necessarily require a cortex in a state of wakefulness and can be
induced in simple circuits in lower organisms (Hawkins and Byrne, 2015). A better test of fetal
consciousness could be devised if there were forms of learning that absolutely require a conscious
state for successful performance. It has been suggested that the ‘trace conditioning’ paradigm bears
on consciousness in a very focused way. It is claimed that trace conditioning does not take place
without the learner being focally aware of the conditioning contingency (Clark and Squire, 1998), but
testing of such paradigms has not yet been reported for the fetus.
The possibility that the fetus may experience pain or other negative affective states has been
considered by previous scientiﬁc working groups focussed on both animals used in experiments and on
humans. At ﬁrst sight, their conclusion that legal protection should be given to the fetus and that
anaesthesia should be provided during any procedures might be taken to support a view that the fetus
is capable of feeling pain or negative affect. However, reading of the justiﬁcation for their
recommendation does not indicate that this is the case. Based on the available evidence, the Scientiﬁc
Opinion on ‘Aspects of the biology and welfare of animals used for experimental and other scientiﬁc
purposes’ (EFSA, 2005) concluded that, even though the mammalian fetus can show physical responses
to external stimuli, the weight of evidence suggested that consciousness does not occur in the fetus
until it is delivered and starts to breathe air. However, since experimental procedures that involve
oxygenating a fetus might induce consciousness, and since events in utero can inﬂuence the behaviour
of the individual once it is born, and some of those effects could be important to its subsequent welfare,
they concluded that fetuses in the second half of pregnancy should be given legal protection when used
for experimental purposes. This decision that protection is necessary does not have implications for the
welfare of the fetus at slaughter of the dam, since such fetuses are not subject to prior experimental
intervention and will not survive to experience any possible detrimental effects in later life.
Consideration of the issue of fetal pain by the Royal College of Obstetricians and Gynaecologists
(RCOG, 2010), which includes experimental evidence gathered from sheep fetuses, led to similar
conclusions regarding the human fetus. While the evidence suggested that the autonomic and
endocrine pathways are in place for the fetus to mount a stress response as early as 18 weeks of
gestation (0.47 G), with increases in cerebral blood ﬂow, catecholamines and cortisol following invasive
procedures, and attenuation of these responses by administration of fetal analgesia at the start of the
procedure, the RCOG concluded that these responses cannot be interpreted as evidence that the fetus
is feeling pain. This interpretation is disputed by Bellieni and Buonocore (2012), who argue that a
dramatic increase in stress hormones during fetal procedures, and its abolition by anaesthesia should
be viewed as providing evidence of fetal pain perception. The RCOG report gives credence to the
evidence that the fetus never experiences a state of true wakefulness in utero and is kept, by the
presence of its chemical environment, in a continuous sleep-like unconsciousness or sedation which
can suppress higher cortical activation in the presence of intrusive external stimuli. However, since fetal
exposure to ‘stress’ in utero can modulate the later function of the hypothalamic–pituitary axis,
reducing the magnitude of the initial stress response, for example by using fetal analgesia, may have
beneﬁcial effects. The degree to which these effects can be observed following fetal exposure to a
painful stimulus remains uncertain, as most studies to date are postnatal and refer to intense,
repetitive stimuli that are not normally experienced in utero. They concluded that the uncertain beneﬁt
of attenuating the fetal stress response to a noxious stimulus in utero by administering analgesia
needs to be balanced against the practical difﬁculties to the administration of effective fetal analgesia,
as well as the possibility of adverse effects. While the evidence that analgesia confers any beneﬁt on

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the fetus at any stage of gestation is lacking, in practice, maternal infusion of opiates has been used
to sedate the human fetus, to achieve immobilisation, rather than analgesia.
The balance of evidence therefore indicates that the fetus is subject to overriding brain inhibitory
mechanisms which will preclude experience of pain or other negative affect. These inhibitory
mechanisms persist until overridden by mechanical and thermal stimuli associated with birth and the
increase in oxygenation of the brain when breathing is initiated. However, some lines of evidence give
rise to the possibility that the fetus might have periods of conscious experience while in uterus.
3.3.3.3. Summary of scientiﬁc evidence on the possibility of ‘sub-cortical’ awareness
While most research into consciousness assumes (almost without questioning it) that cognitive
processes are exclusively performed in the upper cortex of the brain, recent discussions hypothesise that
lower regions may also be involved. Merker (2005) triggered this debate by redeﬁning what
consciousness means, and describing it as the processes which are inbetween the establishment of a
‘world space’ based on highly complex sensory input, and the intentional and detailed execution of
musculoskeletal activities within this space. He argues that with increasing complexity of the organism
higher up the phylogenetic ladder, the processes required to link the sensory preliminaries and the motor
sequels become equally increasingly complex. He hypothesises that a major category of information for
decision-making is included, and relates to a ‘vast array of emotional/motivational biasing variables
experienced as feelings, affects, moods, and sentiments’ (Merker, 2005). To determine the actual location
in the brain where these activities take place is not an easy task, but Merker proposes that essential
aspects of consciousness are functionally linked to cellular territories which extend from the colliculus to
the hypothalamus. Together with the midbrain reticular formation, they provide pivotal structures which
determine behavioural states through several endocrine mechanisms including serotonergic, adrenergic
and cholinergic systems. They regulate sleep cycles, wakefulness, activity levels, and vigilance, and ‘set
the ‘boundary conditions’ for consciousness’ (Merker, 2005). The regions Merker refers to are in direct
contact with the upper cortex, but reside in the upper brainstem. In a later paper, Merker (2007) argues
that this structure is central in establishing conscious perception, even when cortical input is absent. It
may therefore not be necessary to have cortical processing for an organism to be conscious.
Empirical evidence to support this hypothesis comes from work by Whishaw (1990) on decorticated
rats, which show no gross abnormalities in behaviour to the casual observer (although some impaired
behavioural indicators would be noted by an experienced observer). Furthermore, Merker (2007)
presents a medical condition called hydranencephaly (Friede, 1989). It is acquired, for example, by
wholesale resorption of the forebrain tissue due to an intrauterine vascular accident (stroke) of the
fetal brain. The tissue is replaced by cerebrospinal ﬂuid, ﬁlling otherwise empty meninges. The
condition is often not diagnosed until several months postnatally when the children start developing a
variety of complications that always include motoric ones (e.g. cerebral palsy), and often include
seizures. However, this situation can be stabilised and children live for many years or even decades.
These fragile patients have no cerebral cortex, but show evidence of not only being awake, but also
respond to environmental stimuli in a conscious way (Shewmon et al., 1999). These two examples
support the so far unproven theory that some degree of consciousness, including the possibility of
suffering, may be present because of these subcortically based structures.
The fetal thalamus develops much earlier than the cortex (Anand, 2007). The brainstem reﬂexes
like breathing are already present before the EEG appears. Therefore, the proposed subcortically
based consciousness may even occur before the developmental stage at which the capacity for
cortically based consciousness is established. Campbell et al. (2014) therefore postulate that, prior to
the stage at which the cortex is sufﬁciently developed, there may be manifestations of subcortical
consciousness that include relatively undifferentiated negative experiences of discomfort. They refer to
this as the presence of ‘raw basic affects’, and suggest that ‘although such proposed experiences
would be unpleasant, it is not known if their character, intensity and duration would be sufﬁcient to
constitute suffering. Thus, the possibility that suffering may occur during this stage of neurological
development can, at this point in time, neither be ruled in, nor ruled out’ (Campbell et al., 2014). Data
on the exact stage of pregnancy, at which these hypothesised experiences may start, is not available.
There are at least three objections to the notion of subcortically based consciousness according to
Campbell et al. (2014). First, Merker made the argument that upper brainstem functions of lower
phyla species may be conserved in earlier developmental stages of higher phyla species, but the
assumption that neurological development and sequencing of connectivity are uniform across species
is not supported in scientiﬁc literature. Secondly, the evidence based on decorticated animals or
hydranencephalic infants may be misleading due to residual functional cortical tissue. Finally, even if
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subcortically based consciousness may be present in certain pathologies, it is still uncertain if
subcortically based consciousness precedes functional cortically based consciousness in healthy and
intact animals or operates if cortical activity is suppressed.
Of course, it is unsure if these awareness ‘states’ (in particular in relation to the hydranencephalic
child) are comparable to that of an unborn fetus. It can be argued that, unlike the fetal brain, the
brain of the hydranencephalic child is not under inhibitory substance control. This would mean that
even if ‘raw basic affects’ in fetuses are anatomically possible, they would not be perceived consciously
by the fetus. The subcortical system also requires a sufﬁcient level of oxygen to be active, similar to
any other system in the body. It appears the brainstem reﬂexes are mediated in the same way as
cortical reﬂexes or responses. Although adenosine concentrations are lower in these regions (Bocking,
2003), hypoxia mediated increase will lead to cessation of breathing and fetal movements in utero,
which are regulated by brain stem structures.
The hypothesised subcortical consciousness theory is not yet proven. However, in utero raw basic
affects are unlikely to cause negative experiences in fetuses in the last third of gestation because the
previously described brain inhibitory mechanisms would also suppress subcortical structures.
3.3.3.4. Summary of scientiﬁc evidence on C3. Changes occurring during slaughter of the
dam and effect on the fetus (e.g. electric current, hypoxia through ceased
maternal blood ﬂow, elevated stress hormone levels)
Effect of acute maternal stress through handling in the abattoir on the fetus
In abattoirs, animals are unloaded, held in pens, moved to the stunning area, restrained, stunned and
slaughtered. During this period, the dam is exposed simultaneously to a variety of stressors that may result
in high levels of fearfulness and pain, inducing psychological and physical stress that might have an indirect
effect to the fetus through the maternal hypothalamus–pituitary–adrenal (HPA) axis. In sheep, prenatal
maternal stress, during early or late gestation increases fetal cortisol responses (Rakers et al., 2013).
Effect of stunning methods
Captive bolt stunning
During captive bolt stunning, the impact of the bolt on the skull results in brain concussion and
immediate loss of consciousness and sensibility. The penetration of the bolt into the brain produces
substantial damage of the vital centres in the brain stem rapidly rendering the animal unconscious until
death caused by severing the major arteries supplying the brain. Successful induction of brain
concussion manifests as immediate collapse of the animal and onset of apnoea (absence of breathing),
followed by the onset of a tonic seizure, which can be recognised from the occurrence of arched back
and legs ﬂexed under the body, and ﬁxed eyes (EFSA AHAW Panel, 2013). The duration of the tonic
seizure is inﬂuenced by several factors (e.g. animal category, type of captive bolt gun and
ammunition), but usually lasts for seconds and is followed by loss of muscle tone.
Electrical stunning
Electrical stunning is based on passing an electrical current through the head that causes a
generalised epileptiform activity in the brain and the immediate loss of consciousness (EFSA, 2004).
Successful induction of epileptiform activity is manifested as immediate collapse owing to the onset of
tonic seizure. During the tonic phase, the blood pressure increases and the animal shows tetanus (rigidly
extended legs), breathing is absent and the eyeballs may be ﬁxed or obscured (cornea not visible due to
eyeball rotation into the socket). Tonic seizure is followed by clonic seizures lasting for seconds and
terminating in loss of muscle tone (EFSA AHAW Panel, 2013). The seizures are not conducive to prompt
and accurate sticking of animals to prevent return of consciousness following stunning.
In head-to-body electrical stunning, the current ﬂows from the electrode located on the head to a
second one placed on the chest or on the spinal cord, caudal to the position of the heart, thereby
causing the current to pass through the heart and the spinal nerves. The inhibition of the spinal nerve
function produces a reduction in clonic convulsions. This reduces the intensity of muscle contractions
and limits the increase in blood pressure. The current ﬂows through the heart inducing cardiac
ventricular ﬁbrillation in the dam, cardiac arrest and death of the animal.
During head-to-body electrical stunning, the current might pass through the uterus stimulating
muscle convulsions and inducing birth in late pregnant animals. On the other hand, the current
passing through the amniotic ﬂuid might cause fetus’ ventricular ﬁbrillation and death.

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Peisker et al. (2008) studied the fetal responses in sows killed by electrical current during the second
and last third of pregnancy. Treatments implied the application of electrical current either to the head
and heart, to the head, heart and the uterus or from the upper body to the vagina. Fetuses were then
delivered through caesarean section at intervals of 3–4 min but remained attached to the umbilical cord
while the rest of the fetuses remained in the uterus until delivery. No method was found to kill the fetal
pigs immediately. However, in the last third of gestation, fetuses from sows that received a current from
the upper body to the vagina showed a signiﬁcantly faster decrease in heart rate and blood pressure as
well as a shorter period of time for the absence of fetal body movements and reﬂexes. Body
movements were observed/palpated in both fetuses which had been delivered as well as in fetuses
which remained in the uterus. Cardiovascular decompensation occurred after on average 13 and 16 min
(second and last third of gestation, respectively) after killing of the sow via head-to-heart electrical
current and after 15 and 6 min when electrical current was applied from the upper body to the vagina.
Gas stunning
Under the EU legislation, stunning of mammals by exposure to gas mixtures is only permitted in
pigs. An atmosphere with high concentrations of carbon dioxide (CO2) (> 80% by volume in air) induces
hypercapnic hypoxia in the dam and inhibits neurones through acidosis. During CO2 inhalation, partial
pressure of oxygen (pO2) and oxygen saturation (SatO2) in the blood decrease progressively (Rodriguez
et al., 2008), and induces respiratory and metabolic acidosis, reduces the pH of cerebrospinal ﬂuid
(CSF), which bathes the brain and spinal cord and neurons, thereby exerting its neuronal inhibitory and
anaesthetic effects (Woodbury and Karler, 1960). Consequently, the animal loses consciousness
(Gregory, 1986). In this regard, normal pH of CSF is 7.4 and unconsciousness begins when the CSF pH
falls below 7.1 and reaches a maximum at pH 6.8. The presence of CO2 in the blood is sensed by
speciﬁc CO2-sensitive chemoreceptors that stimulate respiration (hyperventilation), heart rate and blood
pressure, and sense of breathlessness prior to loss of consciousness.
Piglets exposed to CO2 as an anaesthetic for surgical castration, showed also signs of
breathlessness and behavioural excitation (Kohler et al., 1998) as well as an initial stimulation and later
depression of breathing and heart rate (Gerritzen et al., 2008).
Hypoxia or anoxia occurring because of the inhalation of argon or nitrogen (< 2% by volume of
oxygen) induces unconsciousness by depriving the brain of oxygen. It has been established that
cerebral dysfunction occurs in mammals when the partial pressure of oxygen in cerebral venous blood
falls below 19 mm Hg. The depletion of O2 causes neuronal depolarisation and intracellular metabolic
crisis leading to cellular death in neurons (Rosen and Morris, 1991; Huang et al., 1994). In contrast to
hypercapnia, anoxia does not cause aversion prior to loss of consciousness.
The partial pressure of oxygen (pO2) and partial pressure of carbon dioxide (pCO2) in the blood of
sheep fetus are 20–27 mm Hg and 40–50 mm Hg that represent 25% and 135% in relation to the
maternal pO2 and pCO2, respectively (Mellor and Gregory, 2003). This fetal hypoxaemia contributes to
the elevated level of adenosine, being between two- and fourfold higher than in the dam.
When exposing the dam to high concentration of CO2, the maternal blood with high pCO2 will ﬂow
also to the placenta exhibiting a rapid rise of pCO2 and decrease in pO2 in the fetal circulation. The
fetal anoxia accompanying the gas mixture inhalation of the dam triggers adenosine release (Koos and
Doany, 1991) that suppresses cerebral metabolism, helping to limit cortical damage during transient
hypoxic/anoxic episodes (Hunter et al., 2003). The developing fetal cerebral anoxia, through the
agency of adenosine, will shut down the electrocortical activity, reducing cortical oxygen demands, i.e.
the EEG becomes isoelectric (Mallard et al., 1992). If the oxygen supply is reinstated within 5–6 min,
the EEG and cortical oxygen consumption usually return to normal (Campbell et al., 2014).
Effect of post-maternal death (by bleeding or killing)
The neck cut of the dam will rapidly stop blood ﬂow to the uterus within about 10 s, preventing
oxygen delivery to fetal tissues, including the brain. This severe fetal hypoxaemia and hypercapnia
would be equivalent to occluding the umbilical cord in utero and will lead to ﬂattening of the fetal
brain electrical activity within 1 min (Mallard et al., 1992). Cortical activity cannot continue in anoxic
conditions whether or not adenosine is acting, eliminating any possible behavioural arousal and
awareness (Mellor and Gregory, 2003). Once oxygen supply to the fetus has ceased, the isoelectric
EEG will continue until death apart from some seizure activity that, according to Mellor and Gregory
(2003), indicates disrupted function that precedes neuronal death. If the fetus remains in the uterus,
the high PaCO2 will prevent behavioural arousal or awareness.

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Acute hypoxia in the sheep fetus induced by reduced uterine blood ﬂow or umbilical cord occlusion
decreases fetal breathing movements and this effect is attributed to hypoxia induced elevated levels of
adenosine in the brain (Koos et al., 1994, 1997; Watson et al., 2002). When acute fetal hypoxia is
associated with hypercapnia, the amplitude of the fetal breathing movement increases (Watson et al.,
2002) and is attributed to the effects of hypercapnia and central acidosis (Dawes et al., 1982; Hohimer
et al., 1983). Research involving sheep fetal brain sectioning has demonstrated that the fetal midbrain
is responsible for the episodic breathing pattern and hypoxic inhibition of breathing (Dawes et al.,
1983). The parafascicular complex, located in the rostral part of the reticular activating system, has
been identiﬁed as responsible for inhibition of fetal breathing during acute hypoxaemia (Koos et al.,
1998). The responses to hypoxia and hypercapnia are maintained in the decorticate sheep fetuses
(Ioffe et al., 1980), suggesting that the cerebral cortex is not involved. Both central and peripheral
chemoreceptors are responsible for these effects.
Both hypoxia and hypercapnia produce bradycardia. However, when the fetal hypoxaemia is
maintained in pregnant sheep, there is a gradual return in the fetal heart rate to normal followed by
tachycardia which is associated with elevations in fetal catecholamine levels.
Fetal breathing movements (FBMs) are rhythmic contractions of the diaphragm, intercostals and
laryngeal muscles presented approximately 30% of the time in the late gestation in human and ovine
fetuses (Dawes et al., 1972). In fetal sheep, a reduction to 33% of fetal arterial oxygen saturation
from its baseline value did not change frequency and amplitude of breathing movements (Sameshima
and Koos, 1986). More acute hypoxia resulted in decline of breathing movements and muscle atonia
(Breen et al., 1997), due to the increase of the adenosine levels in the areas of the brain regulating
FBMs (Bocking, 2003). Bissonnette (2000) concluded that there is considerable evidence that central
mechanisms overcome the excitatory input from peripheral chemoreceptors, resulting in respiratory
depression. However, Bocking (2003) suggested that severe hypoxia increases the number and
amplitude of deep inspiratory efforts, equivalent to gasps prior to death (Bocking, 2003). When the
acute fetal hypoxia is associated with increased PaCO2, the metabolic acidosis increases the amplitude
of the remaining FBMs (Bocking, 2003; Darnall, 2010).
In neonates and adult animals, the exposure to high concentration of CO2 induces breathlessness.
At least three different qualities of breathlessness are currently recognised: respiratory effort, air
hunger and chest tightness (Beausoleil and Mellor, 2015). The form of breathlessness most likely to be
experienced by the fetus, if it has any conscious experience, is ‘air hunger’ and is linked to the
CO2-sensitive chemoreceptors activation.
When a pig fetus, still in the amniotic sac, is removed from the uterus of a sow which has been
killed by cardiac arrest but not exsanguinated, there is an increased physical activity e.g. gasping and
convulsions (Peisker et al., 2008). These movements (convulsions) were not observed in fetuses with a
gestational age of 0.3 G but observed in fetuses about 0.6 G (so after midterm) (Peisker et al., 2008).
Since the fetus is not in contact with air, it would be interesting to know if, e.g. hypothermia induced
by this process acted as an environmental stimulus for these manifestations. These convulsions also
occurred when the pig fetuses were left in the uterus, but observed/palpated. Peisker et al. (2008)
interpret these movements as ‘hypoxic distress’. These manifestations could be interpreted as a
struggle by the fetus to escape a perceived negative situation due to brainstem stimulation associated
with raw basic affects. However, there is no evidence for any relation to sub-cortical structures. To be
certain about the interpretation it would be necessary to differentiate between brain stem reﬂexes and
spinal reﬂexes by abolishing brainstem control.
Therefore, during the last third of gestation, the tonic-clonic seizures induced by mechanical and
electrical stunning of the dam might lead to physical stimulation of the fetus immediately after stunning.
However, due to the presence of brain inhibitory mechanisms fetuses may not experience associated
pain or other negative affect. The hypercapnic hypoxia occurring in the dam during gas stunning would
lead to adenosine mediated inhibitory inﬂuences on the fetal brain as previously explained.

3.3.4.

Expert judgements on ToR3 (capacity of fetuses to experience pain and
other negative affect)

The outcomes from EKE 2 are shown in Appendix D. These outcomes were evaluated in the
context of additional ﬁndings from the literature and further expert discussion to generate ﬁnal
conclusions for this opinion.

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3.3.4.1. Expert judgement for C1. Anatomical and neurophysiological correlates/
structures necessary for perception of pain and other negative affect
There was broad agreement among EKE 2 participants that livestock fetuses by the last term of
gestation have all structures required to feel pain and other negative affect. The AHAW
Panel concludes that it is very likely to extremely likely (i.e. with 90–100% likelihood) that ‘livestock
fetuses in the last third of gestation have the anatomical and neurophysiological structures/correlates
for experiencing pain and/or other negative affect’. This is based on the expert judgement related to
the critical stage of gestation as reported in Appendix D.
3.3.4.2. Expert judgement for C2. Neurophysiological situation and possibility of cortically
based conscious perception
There was broad agreement among EKE 2 participants that livestock fetuses by the end of
gestation do respond to external stimuli including those that have the possibility to cause pain or
negative affect. However, when assessing the possibility of actually experiencing negative states while
showing such responses, there was no consensus among EKE 2 participants and no certainty at either
end, with two group views: one group (12 experts) with a 5–40% likelihood that such negative
experience occurs and another group (2 experts) with a 70–85% likelihood that it does.
Based on the available evidence and expert judgement, the Panel concluded that it is likely to very likely
that ‘the neuro-physiological situation of the livestock fetuses in the last third of gestation (e.g. inhibitory
and excitatory systems) does not allow for cortically based conscious perception’ (i.e. with 66–99%
likelihood of correctness for this statement according to the qualitative likelihood scale; see Figure 1).
Evidence suggesting lack of conscious perception arises from:
i) the presence of adenosine mediated brain inhibitory (neuroprotective) mechanisms
operating in utero, demonstrated by EEG records;
ii) low level of fetal brain oxygen;
iii) predominance of sleep like states in the fetal EEG;
iv) lack of direct evidence of cortically based conscious perception.
It is therefore possible, but unlikely to very unlikely that ‘livestock fetuses in the last third of
gestation can consciously perceive pain and negative affect’ (i.e. with 1–33% likelihood of correctness
for this statement). This possibility arises from:
ithe lack of direct evidence proving that fetuses are incapable of cortically based conscious perception;
iidifferences in the interpretation of indirect evidence relating to:

•
•
•

fetal EEG (e.g. signiﬁcance of transitional EEG);
observed fetal behavioural and physiological responses to external stimuli;
fetal learning (conscious learning versus conditioned responses).

3.3.4.3. Expert judgement for C3. Changes occurring during slaughter of the dam and
effect on the fetus
There was broad agreement at EKE 2 that livestock fetuses show responses to speciﬁed stunning
and slaughter conditions. The Panel concluded that:
• It is very likely to extremely likely (i.e. with 90–100% likelihood) that a livestock fetus shows
measurable responses to extreme hypercapnic hypoxia, mechanical stimulation and electrical
current.
• The likelihood that ‘the fetus will be subjected to these stimuli during stunning of the dam’ is:
–
–
–
–
–

extremely likely (i.e. with 99–100% likelihood) in the case of CO2 stunning (hypercapnic
hypoxia).
unlikely (i.e. with 10–33% likelihood) in the case of movements or seizures of the dam
during handling, stunning and shackling (mechanical stimulation).
very unlikely (i.e. with 1–10% likelihood) in the case of head-only electrical stunning
(electrical current).
as likely as not (i.e. with 33–66% likelihood) in the case of head-to-body electrical stunning
(electrical current).
it is very likely to extremely likely (i.e. with 90–100% likelihood) that fetuses show
measurable responses to hypercapnic hypoxia as induced by maternal circulatory
collapse/sticking of the dam.

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Slaughter of pregnant animals

3.3.4.4. Expert judgement for C4. Possibility that fetuses experience negative affective
state following speciﬁed stunning and slaughter conditions
No direct evidence is available on the possibility that livestock fetuses experience negative affective
states following the applications of stunning and slaughter conditions to the pregnant animals. This
was discussed at the EKE 2 meeting and probability estimates were elicited. The Panel concluded that,
since all slaughtering procedures involve a maternal circulatory collapse, it is unlikely to very unlikely
(i.e. with 1–33% likelihood) that changes/responses occurring during stunning and bleeding of the
dam are associated with pain or other negative affective states in the fetus. This is because of the
combination of the probability of exposure to the stimulus and the considerations detailed here below
in the conclusions on cortical and subcortical awareness (see Section 3.3.4.6).
3.3.4.5. Expert judgement for C5. Level of negative affective state experienced by fetuses
during slaughter of the dam
It was not possible to provide a meaningful answer to this question during the EKE 2 meeting
because of the difﬁculty of objectively categorising intensity of affective state. The AHAW
Panel concluded that on the basis of present scientiﬁc evidence it is not possible to reach an objective
conclusion on the intensity of affective states which would be present if livestock fetuses did have
conscious experience.
3.3.4.6. Logical model for subcortically based conscious perception
Discussion at the EKE 2 meeting led to agreement that the presence of a sleep-like state in
livestock fetuses (due to neuroinhibitors in utero) would make the distinction between cortex and
subcortex irrelevant. There is no direct evidence demonstrating the existence of subcortical awareness
in livestock fetuses and the existence of the hypothesised raw basic affect. However, even if this were
to exist it is unlikely to very unlikely (i.e. with 1–33% likelihood of correctness) that ‘the neurophysiological situation of the livestock fetuses in the last third of gestation (e.g. inhibitory and
excitatory systems) allows for sub-cortically based conscious perception’. This probability estimate
arises from the same considerations as for the cortical situation because the same inhibitory
mechanisms will pertain. The combination of the low likelihood of the existence of raw basic affect and
the high likelihood of an inhibitory uterine environment makes it very unlikely (i.e. with 1–10%
likelihood of correctness) that the livestock fetuses will experience negative affect as a result of
subcortical awareness.

3.4.

Assessment for ToR4 (methods suitable for stunning and killing of
fetuses or neonates of the main livestock species when a pregnant
dam has been delivered to the slaughterhouse at a critical phase of
gestation)

According to the outcomes of the assessment of ToR3 (see above), it seems appropriate to restrict
actions as regards stunning and killing of fetuses to the third term of gestation, since there is no
indication of capacity to experience pain and other negative affect at earlier stages. Focusing on the
third term, however, two perspectives may be taken when approaching this term of reference. A ﬁrst
set of scenarios and respective actions to be taken was developed under the assumption that it is
likely to very likely (i.e. with 66–99% likelihood) that the neurophysiological situation of the fetus in
the third term of gestation does not allow for conscious perception (see Section 3.4.1).
Since, however, uncertainty exists regarding the ability of fetuses to experience negative affective
states (i.e. with 1–33% likelihood that the neurophysiological situation does allow for consciousness), a
set of scenarios which would be applicable to this less likely situation was also developed (see
Section 3.4.2).

3.4.1.

Scenarios operating under the assumption that the neurophysiological
situation of the fetus does not allow for consciousness

Four scenarios are described taking into consideration when the pregnancy is detected and if the
fetus has been exposed to air (Figure 5). For each scenario a course of action is proposed. These
actions operate under the assumption that the neurophysiological situation of the fetus does not allow
for consciousness.

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Slaughter of pregnant animals

Assump on 1 (66–99% likelihood that fetuses do not perceive pain and
nega ve aﬀect)
If pregnancy is detected….
Scenario 1
...in lairage,
when dam is
sƟll alive

Scenario 2
...during
evisceraƟon,
before uterus is
opened

Scenario 3
...during
evisceraƟon, aŌer
uterus is accidentally
opened within 30’ of
killing the dam

Scenario 4
...in lairage,
when dam gives
birth there

The course of acƟon should be to...

Ac on A
...leave carcass
uneviscerated
for 30’ aŌer
killing the dam

Ac on B
...leave uterus
unopened for 30’
aŌer killing the
dam

Ac on C
...stun & kill the neonate
immediately (according to EU Reg
1099)

Figure 5: Scenarios and respective courses of action as regards handling of the fetus/neonate under
the assumption that the neurophysiological situation of the fetus does not allow for
consciousness and taking into consideration when the pregnancy is detected and if the
fetus has been exposed to air.
Scenario 1: The pregnancy is detected during unloading or in lairage when the dam is still alive.
Action A: Pregnant animals in the last third of gestation should be stunned and slaughtered without
any delay. If the dam is ﬁt, move it to the slaughter area for stunning and sticking. If not, perform the
emergency killing on the spot according to the standard operating procedure of the slaughterhouse. In
both cases, leaving the fetus in the uterus inside the dam (uneviscerated) for 30 min after slaughter of
the dam eliminates the possibility of occurrence of hypothermia and physical stimulation due to
evisceration before the death of the fetus from hypoxia and hypercapnia. After that time, the survival
risk of the fetus is low. However, if afterwards the uterus is opened and the neonate has a heartbeat
or starts to show any breathing movements, it should be stunned and killed immediately, following
Action C (see scenario 3 below).
In the slaughter situation, cessation of maternal circulation and its physiological consequences for
the fetus, analogous to experimental cord occlusion, would occur rapidly. Independent of the stunning
method, cutting of the major blood vessels in the neck of the dam results in a time to loss of 50 and
90% of the total blood volume, respectively, of 38 and 94 s in cattle and 14 and 56 s in sheep (Anil

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Slaughter of pregnant animals

et al., 2004, 2006). There are no published corresponding data for horses, goats and pigs.
Nevertheless, cutting both carotid arteries or the vessels from which they arise is mandatory in all
animal species slaughtered for human consumption under the EC Slaughter Regulation 1099/2009 and
therefore most of the circulating blood volume is expected to be lost within the ﬁrst minute after
slaughter of the dam. It is also worth noting that, according to Regulation 1099/2009, carcass dressing
must not begin until the absence of signs of life of the animal has been veriﬁed and bleeding rails are
normally used as buffer to hold and maintain steady supply of carcasses to the evisceration line,
especially in high-throughput slaughterhouses. Owing to this, the time interval between maternal
slaughter and carcass evisceration may exceed 20 min in modern high throughput slaughterhouses.
Physiologically, systemic blood pressure in the dam would be reduced signiﬁcantly when 50% of the
total blood volume is lost during slaughter and uterine blood ﬂow would also be expected to cease
(Mellor and Gregory, 2003). As a consequence, placental gas exchange would be expected to stop,
leading to rapid onset of fetal hypoxia and hypercapnia (referred to as asphyxia in literature), and
marked reduction in oxygen supply to the fetal brain (Jensen et al., 1987; Gunn and Bennet, 2009).
Under this situation, fetal brain activity (recorded using electrocorticogram, ECoG) will be severely
depressed within 60–90 s, as demonstrated by complete umbilical cord occlusion in utero in sheep
(Mallard et al., 1992; Hunter et al., 2003). Although brainstem functions controlling respiration and
cardiac activity are preserved in these fetuses under severe hypoxia and hypercapnia (Jensen et al.,
1987), in the absence of maternal circulation required to oxygenate the brain and remove metabolic
waste, they are unlikely to become aware or conscious. More importantly, these fetuses left in the
uterus would exhibit gasping and heartbeat for different durations (Boddy et al., 1974; Jensen et al.,
1982; Rigatto et al., 1986), which means that, especially those in the last third of gestation, they have
the capacity to attain consciousness if removed from the uterus and allowed to breath air.
The World Organisation for Animal Health (OIE) has proposed some guidelines in its Terrestrial
Animal Health Code (Article 7.5.5. Management of fetuses during slaughter of pregnant animals) to
deal with fetuses under different scenarios.
According to this Code, ﬁrst, ‘fetuses should not be removed from the uterus sooner than 5 min
after the maternal neck or chest cut to ensure absence of consciousness’. It also states that ‘if a live
mature fetus is removed from the uterus, it should be prevented from inﬂating its lungs and breathing
air (e.g. by clamping the trachea)’. These statements may be relevant only to scenarios where access
to live, but unconscious, fetuses is warranted. Secondly, the Code states that ‘when uterine, placental
or fetal tissues are to be collected, where practical, fetuses should not be removed from the uterus
until at least 15–20 min after the maternal neck or chest cut’. Thirdly, the Code states that ‘when
uterine, placental or fetal tissues, including blood, are not to be collected as part of the post-slaughter
processing of pregnant animals, all the fetuses should be left inside the unopened uterus until they are
dead’, which is considered to be most relevant to this Mandate. The time period of 30 min after the
slaughter of the dam suggested by the AHAW Panel experts is based on the consideration that this
period would be sufﬁcient to cause death in fetuses, although the time to onset of brain death in
fetuses left in utero after slaughter of dams has not been studied in any of the species addressed in
this opinion (i.e. all gestational ages of cattle, sheep, goat, pig and horse). Nevertheless, the impact of
acute, near-terminal umbilical cord occlusion (UCO) in sheep fetuses has been studied to some extent
to elucidate the neurological consequences of asphyxia (hypoxia plus hypercapnia with metabolic
acidosis), which is the expected physiological outcome during slaughter of dams in all these species of
animals. The majority of data comes from sheep fetuses and examples are listed in Table 8; it is to be
noted that the experimental protocol used in these studies involved re-establishment of fetal circulation
(i.e. removal of UCO), which does not apply to the slaughter situation.
Table 8:

Examples of umbilical cord occlusion (UCO) studies carried out in sheep fetuses and outcomes

Author(s)
Keunen et al. (1997)

Mallard et al. (1992)

Gestational
age – GA
(in days)
0.6 (85–90)

0.8 (120–127)

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Number of Duration of
animals
UCO (min)

Outcome

EEG

Brain histology

Not recorded

No neuronal damage

Suppressed EEG
during UCO

Neuronal loss in
hippocampus

11

10

Survived

8
4

15
20

Survived
Survived

6

10

Survived

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Slaughter of pregnant animals

Author(s)

Gestational
age – GA
(in days)

Number of Duration of
animals
UCO (min)

Outcome

EEG

Brain histology

Bennet et al. (1999)

0.6 (89–93)

10

30

Survived

Not recorded

Not recorded, but
cerebral vascular
responses studied
indicated cerebral
injury

George et al. (2004)

0.6 (90–92)

7
10

20
30

Survived
Survived

Suppressed EEG
during UCO in both
In 30 min group,
epileptic activity
superimposed on
suppressed EEG
during reperfusion

Severe brain stem
injury in 30 min
group but not in
20 min group

Drury et al. (2014)

0.85 (125–129)

29

Wassink et al. (2007)

0.6 (90–92)

12

0.7 (103–105)

12

0.85 (124–126)

7

Neuronal loss in
3 died during UCO Suppressed EEG
Until mean
cortical and
during UCO and
8 died during
arterial
subcortical regions
recovery for 3 h
pressure (MAP) recovery
Neuronal loss was
13 fetuses
dropped to 8 5 ewes entered
more severe in
developed status
mm Hg (on labour, hence
fetuses showing
epilepticus
average 16 min euthanised
status epilepticus
13 survived until
of UCO)
euthanised for
post-mortem
Not recorded
30
Survived
Remained
suppressed during
25
Survived
occlusion. Magnitude
15
6 out of 9
of suppression was
survived
greater in 0.85 GA
group

In addition, Dawes et al. (1972) investigated UCO in fetal lambs of 40–146 days of gestation age
(5 g–6 kg body weight) delivered under maternal epidural or spinal anaesthesia into a warm saline bath
(39–40°C). The results showed that the time to the last gasp after tying the umbilical cord, when body
temperature was maintained constant, varied with gestational age in fetal lambs. At 80–100 days, it was
7.1  0.38 (mean  S.E.) min, which is statistically signiﬁcantly longer than at term (5.1  0.17 min)
and at 40–55 days of gestation (2.0  0.13 min). Prolonged survival time in midgestation fetuses is
attributed to relatively higher glycogen store, greater anaerobic capacity in vital tissues and lower basal
metabolic activity (Dawes et al., 1959). The only other species on which data are found is the pig
(Peisker et al., 2008), indicating that at 102 days of gestation all piglets were dead within 20 min after
killing of the sow. However, further research on in utero survival time is needed in all species.
It is also reassuring from the welfare point of view to note that Karlsson and Kjellmer (1974)
investigated changes occurring in the somatosensory evoked responses (SERs), as a measure of the
extent of neuronal disruption, in 25 lamb fetuses of 0.7–1.0 gestational ages (105–145 days) that were
removed from their uterus with intact umbilical cords but maintained on a heated table during
exposure of artiﬁcially ventilated dams (through open circuit) to hypoxic-normocapnic and hypoxichypercapnic gas mixtures. The results showed that the SERs were abolished in the latter group,
typically within 15 min of administration of hypoxic-hypercapnic gas mixture to the dam. At the
moment of abolition of SERs, the fetal arterial partial pressure of oxygen level (PaO2) fell to
15 mm Hg, partial pressure of carbon dioxide (PaCO2) increased to 76 mm Hg, blood pH fell to 6.92
and oxygen saturation was 34% of baseline value indicating a rapid onset of profound brain
dysfunction. Peripartum asphyxia has been known to result in epileptic seizures and neuronal loss in
foals (Vaala, 1999) and increased perinatal mortality in piglets (Alonso-Spilsbury et al.,2005).
It is therefore inferred that leaving fetuses in utero for 30 min after the slaughter of the dam would
be sufﬁcient to cause death. As a matter of precaution, the uterus should only be opened when fetal
movements (including seizures) have ceased. These movements are not to be interpreted as signs of
experiencing pain or negative affect but are triggered by reﬂexes (see Section 3.3.3.1).

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Slaughter of pregnant animals

Scenario 2: The pregnancy is detected during evisceration, but before the uterus is opened.
Action B: If the fetus has not been exposed to air, it is recommended to leave the uterus unopened
and the fetus kept in the uterus for at least 30 min after killing the dam. It has to be ensured that the
uterus is intact during this time and the fetus is not exposed to air allowing it to inﬂate the lungs.
Leaving the fetus in the uterus outside the dam (after evisceration) carries the risk of stimulation of
the fetus due to hypothermia and physical stimulation due to evisceration. However, the fetus is not
expected to survive 30 min after the collapse of maternal circulation, but to die from hypoxia and
hypercapnia as discussed in scenario 1. However, if afterwards the uterus is opened and the neonate
has a heartbeat or starts to show any breathing movements, it should be stunned and killed
immediately, following Action C (see scenario 3 below).
Scenario 3: The pregnancy is detected during evisceration, but after the uterus has been accidentally
opened within 30 min of killing the dam.
Action C: In this case, there is a risk of breathing leading to arousal and perhaps to a conscious
state of the fetus. If this occurs, intervention must be applied to stun and kill it humanely.
There are no legal requirements concerning the methods of killing fetuses, and there are no
available data in literature. However, as soon as the uterus is opened the fetus effectively becomes a
neonate and Regulation 1099/2009 applies. The options available under Regulation 1099/2009 include
penetrative captive bolt for all species and weights, percussive blow to the head of neonates up to
5 kg, and non-penetrative captive bolt stunning of ruminant neonates intended for human
consumption and weighing up to 10 kg, followed by bleeding.
Data regarding the efﬁcacy of using penetrating captive bolt on exteriorised fetuses of any species
is scarce. This raises the welfare concern about whether ﬁring a penetrative captive bolt on the soft
(unossiﬁed) skull with pliable bone sutures of a fetus or neonate will lead to brain concussion inducing
unconsciousness. However, it has been reported that ﬁring on the forehead of Jersey calves (n = 8) a
captive bolt gun (Blitz PTB-No3-69; Jopp) with a bolt diameter of 12 mm and extrusion length of
75 mm using a blue cattle cartridge resulted in immediate, extensive trauma, with disintegration of
large parts of the cerebrum and vital centres in the brainstem (recorded by macroscopic examination
and CT scans), leading to immediate and lasting unconsciousness (Svendsen et al., 2008). Therefore, it
is inferred that penetrative captive bolts used for stunning adult animals in slaughterhouses may also
be used to stun exteriorised fetuses and neonates before slaughter by severing two carotid arteries.
In the case of non-penetrative captive bolt and percussive blow, the force and location of the blow
are two key parameters that determine the outcome. Regulation 1099/2009 states that, when using
non-penetrative captive bolts, fracture of the skull should be avoided. This consideration may not be
applicable to neonates because application of a non-penetrative captive bolt would cause extensive
damage to the skull and the brain, leading to immediate death. However, food business operators
should ensure that the size of the non-penetrative captive bolt is appropriate for size of the skulls of
exteriorised fetuses. Non-penetrative captive bolts have been used effectively to kill neonatal goats up
to 48 h of age (Sutherland et al., 2016), 3-day-old piglets (Casey-Trott et al., 2013), 5- to 49-day-old
(3–9 kg) piglets (Casey-Trott et al., 2014) and neonatal piglets weighing up to 10.9 kg (Grist et al.,
2017). Based on the EEG evidence in goat kids and computed tomography scan results in piglets, it is
suggested that, when maintained and used correctly according to the manufacturers’ instructions, the
magnitude of traumatic brain injury caused by commercially available non-penetrating captive bolts,
would be sufﬁcient to kill ungulate neonates.
Regulation 1099/2009 also allows head-only electrical stunning followed by bleeding or head-tobody electrical stunning for neonates. However, the large size of the electrodes designed for stunning
large animals may not be appropriate for neonates. Even in the event of using specially designed and
constructed stunning electrodes, application of an electric current to neonates that have been freshly
removed from the uterus may lead to shunting of current over the surface of their wet skin (least
resistant pathway to current ﬂow), rather than ﬂowing through the skull or body required to achieving
desired welfare outcome.
Lethal injection is not permitted for slaughter under Regulation 1099/2009. It could be used for
killing of the neonate, which is excluded from the human food chain, but has limitations including
availability of suitable drugs (e.g. barbiturates) and requirement for administration by a licensed
veterinarian. There are also considerations of food safety – in the event of fetuses entering the food
chain e.g. pet food – and environmental impact associated with carcass disposal. It is worth noting

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Slaughter of pregnant animals

that a publication from the USA showed sodium pentobarbital was detectable for 367 days in equine
mortality compost piles, which would have environmental consequences (Payne et al., 2015).
Scenario 4: The dam gives birth in the lairage.
Since it is illegal to transport a newly born animal in which the navel is not completely healed (see
EC Regulation 1/2005), Action C as described for scenario 3 applies and the neonate should be
stunned and killed immediately.

3.4.2.

Scenarios operating under the assumption that the neurophysiological
situation of the fetus does allow for consciousness

Figure 6 here below summarises four scenarios, taking into consideration when the pregnancy is
detected and if the fetus has been exposed to air, and the related courses of action. These actions
operate under the assumption that the neurophysiological situation of the fetus does allow for
consciousness.

Assumpon 2 (1–33% likelihood that fetuses do perceive pain and
negave aﬀect)
If pregnancy is detected….
Scenario 1
...in lairage,
when dam is
sll alive

Scenario 2
...during
evisceraon,
before uterus is
opened

Scenario 3
...during evisceraon,
aer uterus is
accidentally opened

Scenario 4
...in lairage, when
dam gives birth
there

The course of acon should be to...

Acon D
...kill the dam
and the fetus
with an
overdose of
anaesthec
drug

Acon E
...open the uterus
immediately and
stun and kill the
neonate
according to Reg
1099

Acon F
...stun & kill the neonate
immediately (according to EU Reg
1099)

Figure 6: Scenarios and respective courses of action as regards handling of the fetus/neonate under
the assumption that the neurophysiological situation of the fetus does allow for
consciousness and taking into consideration when the pregnancy is detected and if the
fetus has been exposed to air

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Slaughter of pregnant animals

Scenario 1: The pregnancy is detected during unloading or in lairage when the dam is still alive.
Action D: The dam and the fetus should be euthanised with an overdose of anaesthetic agents. For
killing of the fetus, the drug should be able to cross the placental barrier. Barbiturates, when
administered as overdose, depress the central nervous system and the respiratory centre, causing
apnoea, cardiac arrest and death. These also cross the placental barrier, thus killing the fetus.
Intravenous administration is preferred because it is the most rapid and reliable method. Prior sedation
should therefore be considered as a means to reduce the stress associated with the administration of
the anaesthetic drug. After the injection, the animals should be left without any disturbance until
death supervenes. Handling and use of anaesthetic agents is restricted to trained, competent and
authorised personnel. Furthermore, this intervention will render the meat of the dam and the fetus
unsuitable for consumption and gives rise to other safety risks associated with the presence of
hazardous agents in a food plant.
Scenario 2: The pregnancy is detected during evisceration, but before the uterus is opened.
Action E: After killing of the dam, the uterus should be immediately opened and the neonate
stunned and killed according to the description given previously for Action C (see Figure 5).
Scenarios 3 and 4: The pregnancy is detected during evisceration, but after the uterus has been
accidentally opened within 30 min of killing the dam or the dam gives birth in lairage.
Action F: In both cases, the neonate should be stunned and killed according to the description
given previously for Action C (see Figure 5).

3.5.

Assessment for ToR5 (methods to determine the gestational phase
under practical conditions by examining the fetus after the dam has
been killed)

3.5.1.

Results from literature review

The available literature was assessed for compiling the following tables (Tables 9–12) presented
separately for each species (one common table has been produced for sheep and goats). The tables
include criteria, based on physical features of the uterus and the fetus, for estimating the gestational
age after the dam has been slaughtered. In order to allow for a ﬁrst assessment of the gestational age
when the reproductive tract has been eviscerated, physical features of the uterus such as width/
diameter of the uterus or largest circumference of the uterus are provided. Once a critical gestational
age is assumed and the decision taken to examine the fetus (for timelines since killing of the dam see
Sections 3.4.1 and 3.4.2), external features of the fetus (such as the presence of hair, teeth) or linear
measures such as crown-rump length, nose-to-tail length or length of large bones may be applied.
As indicated by Tables 9–12, for some species there are relatively few studies on the
characterisation of fetal age. Where these data exist, they seldom give a satisfactory basis for
conclusion. In terms of reliability of the measures suggested, the following needs to be considered: (i)
most data were collected years/decades ago on older genotypes which makes it difﬁcult to establish
reliable benchmarks for modern breeds or selection lines; (ii) there is a lack of sensitivity/speciﬁcity
studies on the determination of gestational age from the physical features; (iii) criteria for the exact
boundaries between gestational stages are therefore less reliable indicators for the allocation to a
given term than those towards midstage; (iv) given the differences between breeds in mature body
weight and size, and the individual variation within breeds, external morphological features should be
better indicators of gestational stage than linear dimensions such as fetus size or bone length.

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€sse and
Ru
Grunert
(1993)

€sse and
Ru
Grunert
(1993)

Roberts
(1986)

Largest
circumference
of the uterus
(in cm)

Width/diameter
of the uterus
in cm

12.4

10.0–13.0

51.4

n.a.

22.2

Day 150

Day 180

n.a.

18.0–23.0

12.5–18.0

110.8

n.a.

74.0

n.a.

n.a.

Day 210

Day 240

n.a.

n.a.

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n.a.

n.a.

Last third of gestation (day 181 – day 285)

15.0

Day 120

Second third of gestation (day 91–day 180)

Day 90

Fine short hair all
over body, incisor
teeth not erupted

Hair on metatarsal,
metacarpal, and
phalangeal region
of extremities and
beginning on back,
long hair on tip of
tail

Hair on eyebrows
and lips, testes
in the scrotum,
teats developing
Hair on inside
of ear and around
horn pits, tip of
tail and muzzle

Fine hair on
eyebrows,
claws developed
and yellowcoloured

Hair on lips, chin
and eyelids,
scrotum present

Roberts (1986)

Body fully covered
with hair (day 230)

49

n.a.

n.a.

78.0

62.0

50.0

n.a.

Horn bud covered
with hair, tail tip
hairs present

n.a.

36.0

n.a.

n.a.

24.0

15.0

Evans and
Sack (1973)

n.a.

n.a.

Nielsen and
Andersen
(2016)

60.0–85.0

55.0–75.0

40.0–60.0

30.0–45.0

22.0–32.0

13.0–17.0

Roberts
(1986)

Crown-rump- length in cm

n.a.

Scrotum present
Hoofs becoming
ﬁrm and opaque
(day 100)

Evans and
Sack (1973)

External features

Gestational stages of cattle based on physical features of the fetuses (n.a.: data not available)

First third of gestation (day 1–day 90)

Reference

Cattle

Table 9:

Slaughter of pregnant animals

83.9

66.2

52.7

40.0

28.2

17.5

121.0

90.0

59.0

37.0

22.0

10.0

Habermehl
(1975; based
on Regli, 1963)

57.0

47.0

38.0

29.0

20.0

10.0

€ngerBu
Marek
(1972)

Length of metatarsus
in mm

EFSA Journal 2017;15(5):4782

Thomsen
(1975)

Nose-to-tail
length in
cm

31.5

Day 255

Day 280

No source
provided

96.0

n.a.

Largest
circumference
of the uterus
(in cm)

Wu et al. (1987)

Reference

Evans and Sack (1973)

External features

Palate fused, facial
clefts closed, eyelids
begin to cover eyes

Day 44

245

www.efsa.europa.eu/efsajournal

Prepuce, scrotum,
labia and clitoris present

Second third of gestation (day 39–day 76)

270

First third of gestation (day 1–day 38)

Length of the
uterine horn in cm

Day 38

Multiple
sources

Hair coat
complete
and long

n.a.

~ 75

~ 45

Evans and
Sack (1973)

n.a.

46 (d40)

Njaa
(2012)

Crown-rump-length in mm

50

28 (d49)

17 (d35)

Odlaug
(1955)

98 (d51)

25 (d30)

Ullrey et al.
(1965)

Multiple
68 embryos
sources
from the
Cornell Collection
(+ data from multiple
references)
Numbers extrapolated
from graph

18 calves
(7 Jersey,
8 Holstein,
3 crossbreeds),
convenience
sample

68 embryos from
the Cornell
Collection (+ data
from multiple
references)

15

n.a.

Ullrey et al.
(1965)

Humerus length mm

n.a.

92.0

n.a.

n.a.

n.a.

Six incisors
erupted: 97%
probability to
be > 90% of
gestation

n.a.

Crown-rump- length in cm

n.a.

External features

Gestational stages of pigs based on physical features of the fetuses (n.a.: data not available)

Multiple
sources

n.a.

Pigs

Table 10:

Information No source
on source provided
reliability

n.a.

Cattle

n.a.

Width/diameter
of the uterus
in cm

Slaughter of pregnant animals

3

2

German
Black and
White
Lowland
fetuses
Gjesdal (1969)
High correlations
of length of long
bones diaphysis
with fetal age
(but not for width
and diameter)
Simmental and
Fribourg cattle
fetuses

n.a.

n.a.

Gjesdal
(1972)

69.0

n.a.

148.0

n.a.

Length of metatarsus
in mm

EFSA Journal 2017;15(5):4782

Wenham et al.
(1973)

82 Red
Danish
and Holstein
fetuses +
reexamination
of older data

106.5

n.a.

Nose-to-tail
length in
cm

264

Day 76

Eyelids fused (d50)

External features

278
273

Eyelids separated
n.a.

Njaa (2012)

Reference

Testes have descended into
scrotum (80)
Colour markings appear (104)

84

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Hair begins to cover body (67)

67

Second third of gestation (day 50–day 100)

100

207 (d85)
270 (d110)

Not given
Data from
range of sources 1897
–1968
Numbers extrapolated
from graph

~ 250
~ 300

Evans and Sack
(1973)

Large tactile hairs appear
on lips and upper eyelids (91)
n.a.

No hair; rumen development
near the end of this gestational
period (63)

n.a.
Philtrum present; eyelids
fused; pinna covers acoustic
meatus; external genitals
differentiated; teats present (43)

First third of gestation (day 1–day 50)

External features

50

163 (d72)

n.a.

220 (d100)
300

360 (108)

230 (80)

125 (60)

95 (55)

Alcorn et al.
(1981)

51

n.a.

350 (91)

155 (63)

90 (42)

Njaa
(2012)

Crown-rump-length (mm)

41
53

n.a.

230 (91)

115 (63)

50 (42)

Evans and Sack
(1973)

1.26 (108)

0.26 (80)

0.09 (60)

0.05 (55)

Alcorn et al.
(1981)

Total body
weight (kg)

254 Yorkshire fetuses
254 Yorkshire
fetuses (30, 51, (30, 51, 72, 93 days)
plus 35 full term
72, 93 days)
plus 35 full term
Tuberosity to condyle

228 (d93)
294

26

n.a.

~ 200
170 (d70)

Humerus length mm

Crown-rump-length in mm

Gestational stages of sheep and goats based on physical features of the fetuses (n.a.: data not available)

Sheep and
goats(a)

Table 11:

Information 320 pregnant pigs at Data from range of
on source 3, 5, 7, 9, 11, 13 and sources 1897–1968
15 weeks of gestation
reliability
Uterine size affected
by number of fetuses
but not pregnancy
stage

Day 90
Day 115

Last third of gestation (day 77–day 115)

Length of the
uterine horn in cm

Pigs

Slaughter of pregnant animals

4.804

3.108

1.608

0.622

EFSA Journal 2017;15(5):4782

3.745

2.351

1.167

0.431

Femur McDonald
et al. (1977)

Tibia McDonald
et al. (1977)

519 Norwegian
Landrace fetuses
Diaphyseal
length
34 large white fetuses
Diaphyseal length from
radiograph

Length of major
bones (mm)(b)

28
43

19

29
42

20

External features

Birth (144)

No source mentioned

147

Information
on source
reliability

Based on a large
number of data
sets from between
1936 and 1966,(c)
as well as 26
embryos
in the ‘Cornell
Collection’

470 (144)

480 (144)

No source
mentioned

400 (126)

n.a.

400 (126)

n.a.

Based on a data
set of 14 fetuses
from MerinoCorriedale or
Border Leicester
cross ewes

3.75 (141)

3.9 (133)

1.85 (117)

Total body
weight (kg)

Based on radiography
of 215 fetuses,
obtained from
80 Finish landrace
x Dorset horn ewes

7.877

6.685

5.253

Length of major
bones (mm)(b)

Based on
radiography
of 215 fetuses,
obtained from
80 Finish
landrace
x Dorset horn
ewes

9.446

8.150

6.545

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52

EFSA Journal 2017;15(5):4782

(a): Data on goats were only found in one case (Singh et al., 2004), but the observations were before day 50 of gestation and therefore not included. The data in this table relate to sheep embryos, in all but one case: Njaa (2012)
refers to ‘sheep and goats’ in his Appendix A, without further indication of the source. It is worth noting that Prummel (1988) who uses the bone length data of McDonald et al. (1977) suggests that ‘the identiﬁcation of foetal bones
of sheep and goat will be even more difﬁcult than that of postnatal bones from these’. This would imply that the developmental stages of both species are comparable.
(b): Data based on an equation developed by McDonald et al., 1977: ln (y/P) = (Q/100R) 9 (1 eR(144 t)) to relate foetal age of sheep in days after conception (t) and the diaphyseal length (y in cm). The underlying constant values
are presented in the paper: P is an estimate of length at birth; Q is an estimate of the speciﬁc growth rate (%) at birth; R is the rate of exponential decay of the speciﬁc growth rate; s is the residual standard deviation of diaphyseal
length.
(c): Barcroft (1946), 186 specimens; Batten (1960), 120 specimens; Bogolyubsksiy (1959); Cloete (1939), 49 specimens; Eaton (1952), 18 specimens; Evans et al. (1966); Galpin (1935), 18 specimens; Green and Winters (1945); Harris
(1937), 25 specimens; Joubert (1956), 17 specimens; Malon and Curson (1936), 56 specimens; Romanes (1947), 11 specimens; Stephensons (1959), 100 specimens; Winters and Feuffel (1936), 73 specimens; and 26 embryos in
the Cornell Collection.

Based on a data
set of 14 fetuses
from MerinoCorriedale or
Border
Leicester cross
ewes

Based on a large number of
data sets from between 1936
and 1966,(c) as well as 26
embryos in the ‘Cornell
Collection’

Eyelids separated (126)

355 (117)

Eyelashes are well developed,
460 (133)
some hair on tail and head (126)
480 (141)
Fetus becomes fully developed
with the body covered with hair;
hoofs complete but soft (144)

Hair covering complete (116)

132

n.a.

Crown-rump-length (mm)

116

Last third of gestation (day 100 – day 150)

Sheep and
goats(a)

Slaughter of pregnant animals

Width/
diameter
of the uterus
in cm

€sse and Roberts
Ru
(1986)
Grunert
(1993)

Volume
of the
uterus in
L

Njaa (2012)

15–3.5
(d90)

12.5–15
(d90)

Mammary nipples
and hooves
visible (d90)

10–15
(d180)

Day 210

n.a.

n.a.

Hair on lips, nose
eyebrow, eyelids,
edge of ear, tip of
tail, back and
mane

External genitalia
formed, scrotum
empty, ergots and
orbital areas
prominent

n.a.

60–90

Day 270

330

n.a.

n.a.

n.a.

Complete hair
coat, testes
descended

Short ﬁne hair
over entire body

Hair on mane
and tail, back and
distal portion
of extremities

www.efsa.europa.eu/efsajournal

n.a.

Day 240

Last third of gestation (day 227–day 340)

n.a.

Day 120

Second third of gestation (day 113–day 226)

Day 112

n.a.

53

118

99

~ 100

n.a.

83

~ 80

70

~ 65

Eyelashes emerged,
mane and tail hair
present, mane hair
~ 2.5 mm long

Hair appears on
poll, pinnae, throat
chin and muzzle;
mane hair 5 mm
long; hair covers
distal half of tail
Body covered
with ﬁne hair;
mane hair 1.5 cm
long; short switch
on tail.

n.a.

n.a.

Platt
(1978)

~ 25

~ 20

Evans and
Sack (1973)

Crown-rumplength in cm

Fine hair on muzzle,
chin and around
eyes; orbital area
prominent; ergot
prominent

Tactile hairs on
lips; teats well
formed.

Evans and Sack
(1973)

External features

Gestational stages of horses based on physical features of the fetuses

First third of gestation (day 1–day 112)

Reference

Horse

Table 12:

Slaughter of pregnant animals

n.a.

80–90

60–80

55–70

15–20

10–14
(d90)

Njaa
(2012)

212
(44 weeks)

140
(37 weeks)

n.a.

89
(29 weeks)

41
(20 weeks)

23
(15 weeks)

Habermehl
(1975)

Femur
length

n.a.

n.a.

236
(44 weeks)

n.a.

n.a.

n.a.

n.a.

30 (30)

37
(d320)
(35)

~ 34

30 (28)

29 (25)

16 (15)

14 for
horse
(for pony)

Turner
et al.
(2006)

~ 31

~ 28

~ 28

~ 17

~ 16

Murase et al.
(2014)

Eye length mm
(Ultrasonography)

EFSA Journal 2017;15(5):4782

Guffy et al.
(1970)

154
(37 weeks)

n.a.

80
(29 weeks)

32
(20 weeks)

17
(15 weeks)

Habermehl
(1975)

Length of metatarsus
in mm

Width/
diameter
of the uterus
in cm
Data from Bergin
et al., (1967;
93 specimens)
Ewart, 1897,
review of
Zietzschmann
and Krolling
(1955)

External features

Data from Bergin
et al., (1967; 93
specimens);
Roberts, (1971)

www.efsa.europa.eu/efsajournal

Information No source Multiple
resources
on source provided
which can
reliability
mostly not
be retrieved

Horse

Volume
of the
uterus in
L

Slaughter of pregnant animals

Bergin et al.,
(1967; 93
specimens)
Ewart, 1897,
review of
Zietzschmann
and Krolling,
1955)
Numbers
extrapolated
from graph

54

179 aborted
thoroughbred
foals

Crown-rumplength in cm
n.a.

Data from
Habermehl
(1975) on
22 horse
fetuses

Femur
length
Data from
Habermehl
(1975) on
22 horse
fetuses

10 thoroughbred
mares
Numbers
extrapolated
from graph

23 ponies
(36
pregnancies)
Back calc
from
parturition
assuming
340 days and
data from
Kahn
and Leidl
(1987 –
n = 77) and
Turner et al.
(2006 –
n = 66) on
light horses
Concluded
houses and
ponies
had diff
equations

Eye length mm
(Ultrasonography)

EFSA Journal 2017;15(5):4782

101
American
fetuses

Length of metatarsus
in mm

Slaughter of pregnant animals

4.

Conclusions

•
•

•
•

While most evidence used in this opinion regarding anatomical and neurophysiological
correlates of consciousness has been obtained from sheep fetuses, it is considered rather
similar for precocial ungulate and equid species (ToR3).
Since there are no conclusive objective measures of the capacity of livestock fetuses to
experience pain and other negative affect (ToR3), the assessment of this question is based on
the available scientiﬁc evidence and on expert opinion. Each conclusion is expressed as a
statement accompanied by the likelihood – that the statement is correct – in the form of a
percentage.
It is very likely to extremely likely (i.e. with 90–100% likelihood) that livestock fetuses in the
last third of gestation have the anatomical and neurophysiological correlates for experiencing
pain and/or other forms of discomfort (ToR3).
It is likely to very likely (i.e. with 66–99% likelihood) that the neurophysiological situation of
the livestock fetuses in the last third of gestation (e.g. inhibitory and excitatory systems) does
not allow for perception of pain or other negative affect (ToR3). This arises from:
the presence of brain inhibitory (neuroprotective) mechanisms operating in the fetus,
low levels of fetal brain oxygen,
predominance of sleep like states in the fetal EEG,
lack of any direct evidence of perception of pain and other negative affect.

•

It is therefore possible, but unlikely to very unlikely (i.e. with 1–33% likelihood) that livestock
fetuses in the last third of gestation can perceive pain and other negative affect (ToR3). This
possibility arises from:
the lack of any direct evidence proving that fetuses are incapable of perceiving pain and
other negative affect.
differences in the interpretation of indirect evidence relating to:
fetal EEG (e.g. signiﬁcance of transitional EEG);
fetal behavioural and physiological responses to external stimuli;
fetal learning (conscious learning versus conditioned responses);

•

•

•

There is no direct evidence demonstrating the existence of subcortical awareness in livestock
fetuses and the existence of the hypothesised raw basic affect. However, even if this were to
exist it is unlikely to very unlikely (i.e. with 1–33% likelihood) that the neurophysiological
situation of the livestock fetuses in the last third of gestation (e.g. inhibitory and excitatory
systems) allows for sub-cortically based conscious perception because the same inhibitory
mechanisms will pertain. The combination of the low likelihood of the existence of raw basic
effect and the high likelihood of an inhibitory uterine environment makes it very unlikely (i.e.
with 1–10% likelihood) that the livestock fetuses will experience pain or other negative affect
because of subcortically based conscious perception (ToR3).
It is very likely to extremely likely (i.e. with 90–100% likelihood) that livestock fetuses show
measurable responses to extreme hypercapnic hypoxia, mechanical stimulation and electrical
current. However, since all slaughtering procedures involve a maternal circulatory collapse, it is
unlikely to very unlikely (i.e. with 1–33% likelihood) that these responses observed in the fetus
during stunning and bleeding of the dam are associated with pain or other negative affect
(ToR3).
The most appropriate management of livestock fetuses at slaughter (ToR4) depends on the
point in the slaughter chain at which it is detected that the dam is in the last third of
gestation. Once detected, the recommended course of action depends on the risk
management decision regarding the probability that fetuses might experience pain and other
negative affect.

•
•

Under the more likely assumption (i.e. with 66–99% likelihood) that the neurophysiological
situation of the livestock fetus in the last third of gestation does not allow for perception of
pain or other negative affect, actions should be taken to prevent onset of breathing by the
fetus (ToR4, Section 3.4.1).
However, if the risk management decision is based on the less likely assumption (i.e. with
1–33% likelihood) that the livestock fetus in the last third of gestation can experience pain

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55

EFSA Journal 2017;15(5):4782

Slaughter of pregnant animals

or other negative affect, alternative actions for immediate stunning and killing of the fetus
are required (ToR4, Section 3.4.2).

•

•

Determination of fetal age after post-mortem detection (ToR5) should be possible from
morphological characteristics including measures of fetal size. Due to breed differences and
variations within breed, external features, e.g. hair growth, are likely to be better indicators of
gestational age of the fetus than linear measures. However, the available data do not currently
allow reliable benchmarks to be derived.
The prevalence of slaughtered pregnant animals (ToR1) is not available in the literature or in
existing data sets. The median estimate for the overall percentage of female animals that are
in the third term of gestation when sent to slaughter in Europe was obtained by a structured
expert knowledge elicitation (EKE exercise) summarising the limited evidence in form of a
probability distribution and resulted to be:
3% for dairy cows (with a 50% uncertainty range from 1.6% to 5.2%)
1.5% for beef cows (with a 50% uncertainty range from 0.8% to 2.5%)
0.5% for pigs (sows) (with a 50% uncertainty range from 0.2% to 1%)
0.8% for sheep (with a 50% uncertainty range from 0.4% to 1.6%)
0.2% for goats (with a 50% uncertainty range from 0.1% to 0.4%)

•
•
•
•
•

5.

The experts expressed the opinion that the prevalence of pregnant mares slaughtered is lower
compared to the other farm animal species.
Estimates from the EKE for the percentage of pregnant animals which are in the ﬁrst and
second term of gestation were considered unreliable because of difﬁculties in detection of early
stages of gestation in the course of the slaughter process.
There is paucity of information on the reasons why pregnant animals are sent to slaughter
(ToR2), but they include (i) health and welfare, (ii) management and (iii) economic reasons.
The relative importance of these reasons is unknown.
The reasons for farmers not knowing that animals sent for slaughter are pregnant in the last
third of gestation include (i) lack of supervision of breeding, especially in extensive systems, (ii)
the absence or failure of pregnancy diagnosis, (iii) poor record keeping or loss of information
in the trading chain.
Measures to reduce the prevalence of pregnant animals slaughtered in the last third of
gestation (ToR2) can be linked to each of these reasons. The effectiveness of the proposed
measures in reducing the possibility that farmers send pregnant animals to slaughter will be
impaired by (i) failure of education and communication strategies on the welfare implications
and preventive measures and (ii) a pregnancy test efﬁcacy of less than 100%.

Recommendations

•
•
•

Further research is needed using multidisciplinary approaches to establish the ability of fetuses
of different developmental stages to perceive pain or other negative affect (ToR3).
Food business operators should include in their standard operation procedures actions with
regard to management of female animals detected to be in the last third of gestation (ToR4).
If the more likely conclusion that the livestock fetus is not capable of perceiving pain or other
negative affect is accepted, the fetus should be left undisturbed in utero for 30 min after the
death of the dam by which time it should be dead. If the fetus is exteriorised before this time
or subsequently shows signs of life, it should be stunned and killed using approved methods
for neonates in accordance with Regulation 1099/2009 (ToR4).
If the less likely conclusion that the livestock fetuses can experience pain and other
negative affect is accepted, the fetus should be killed in situ together with the dam by an
overdose of anaesthetic drug if pregnancy is detected at arrival in the slaughterhouse. If
the dam is already dead at the time of detection, the fetus should immediately be
exteriorised, stunned and killed using approved methods for neonates in accordance with
Regulation 1099/2009 (ToR4). The food safety risks associated with each course of action
should be considered.

•

Research should be carried out to develop and evaluate appropriate methods of stunning and
killing exteriorised fetuses (ToR4).

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Slaughter of pregnant animals

Further research should be carried out to determine the survival time in utero of fetuses
of different livestock species and gestational stages following slaughtering of the dam
(ToR4).

•
•
•
•

Further research should be carried out to assess the sensitivity and speciﬁcity of animal based
measures in livestock fetuses to conﬁrm death (ToR4).
Sensitivity and speciﬁcity of indicators for establishing gestational age in different species and
breeds/selection lines should be determined and models to estimate the gestational age should
be developed (ToR5).
Systematic data collection for prevalence estimation is needed on the present situation
regarding the slaughter of animals during the last third of gestation (ToR1).
To reduce the prevalence of animals slaughtered in the last third of pregnancy (ToR2), it is
recommended to:
implement measures to improve the health status of animals on farm and thus to reduce
unplanned slaughtering.
implement management practices such as single sex housing and supervised breeding
and thus to reduce unplanned pregnancies.
establish the pregnancy status of all animals to ensure that they are not sent for
slaughter in the last third of gestation.
ensure information on insemination and pregnancy diagnosis is present in documentation
accompanying animals at the time of sale.
implement education and communication strategies for farmers.
undertake further research to improve rapid on-farm pregnancy diagnostic test accuracy
and feasibility, especially for the diagnosis of later stages of pregnancy in small ruminants
and pigs.

•

Each of these measures can be addressed at different levels by the appropriate stakeholder
including farmers, veterinarians and other advisors, supply chain managers, competent
authorities and researchers.

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plasma of the pregnant ewe. Journal of Endocrinology, 45, 449–457.
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Glossary and Abbreviations
Analgesia
Anoxia
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The absence of pain in response to stimulation which would
normally be painful.
The absence of oxygen in the blood.
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Arousal
Aspiration reﬂex

Aversion
Awareness
Consciousness

Death
Electroencephalogram (EEG)
Electrocorticogram (ECoG)
Fetus
Gagging or gasping
Hazard
Humane killing
Hypercapnia
Hypoxaemia
Killing
Nociception

Pain

Seizure
Sensibility
Sentience
Slaughter

Somatosensory evoked
potentials (SEPs) or
responses
(SERs)
Sticking or bleeding
Stun or stunning
Suffering
Vibroacoustic stimulation
(VAS)

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The state or condition of being alert or stimulated
Stimulation (chemical, electrical or mechanical) of the pharyngeal
branch of glossopharyngeal nerve or trigeminal afferents that
evokes a short-duration spasmodic inspiratory sniff- or gasp-like
aspiration.
A tendency to show behaviour to avoid or to withdraw from a
situation which is associated with a noxious stimulus.
is linked with wakefulness and implies that responses to stimuli
involve higher brain centres and are not merely reﬂexes.
is the state in which an animal is able to cognitively process and
subjectively evaluate internal and external sensory inputs and to
feel emotions
is the state of an animal where all vital functions have
permanently ceased.
Electrical activity of the brain usually recorded from the surface of
the skull using non-invasive techniques.
Electrical activity of the brain usually recorded on the surface of
the brain or dura (a membrane covering the brain).
is an unborn animal from the stage of its development when its
main adult features can be recognised
Rudimentary respiratory activity occurring through mouth (oral
breathing).
Any factor with the potential to cause poor welfare.
A method of killing that causes no avoidable pain, distress or
other suffering to the animal(s) concerned.
An increased blood carbon dioxide levels in the blood or
atmosphere.
A decrease in oxygen levels in the blood.
Any intentionally induced process which causes the death of an
animal
The neural process of encoding noxious stimuli. Consequences of
encoding may be autonomic (e.g. elevated blood pressure) or
behavioural (motor withdrawal reﬂex or more complex nocifensive
behaviour). Pain sensation is not necessarily implied.
An unpleasant sensory and emotional experience associated with
actual or potential tissue damage, or described in terms of such
damage.
Convulsions that may occur with or without loss of consciousness
or pathological electroencephalogram.
Ability to perceive external stimuli and internal stimuli (e.g. pain).
(Functional) capacity to perceive sensations originating from
sensory inputs
Slaughter means the killing of animals intended for human
consumption by the process of bleeding to induce death, usually
by severing major blood vessels supplying oxygenated blood to
the brain.
Electrical activity in the brain evoked by somatosensory (painful)
stimuli.

Act of severing major blood vessels (also see neck cutting).
Any intentionally induced process which causes loss of
consciousness and sensibility without pain, prior to killing.
One or more unpleasant feelings (mental state) such as pain,
distress and other welfare consequences.
Application of a vibratory sound stimulus to the abdomen of a
pregnant woman to induce response in a fetuses

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Wakefulness

Wakefulness is a state of brainstem and thalamic activity and of
non-sleep-arousal, not requiring cortical processing

Glossary related to the uncertainty
Elicitation Group

Median estimate
Expert knowledge
elicitation (EKE)
Likelihood
Probability
Probability distribution

Subquestion

Uncertainty
Uncertainty analysis
50% Uncertainty range
98% Uncertainty range

The elicitation group performs the elicitation protocol and elicits
the information from the expert panel. The elicitation group is
responsible for all contacts with the expert panel, the
documentation of the elicitation phase, the result report, and the
feedback to the experts.
Median prevalence (with equal probability of over/under
estimation).
A systematic, documented and reviewable process to retrieve
expert judgements from a group of experts, often in the form of a
probability distribution.
The chance or probability of something.
Quantiﬁcation of uncertainty as degree of belief regarding the
likelihood of a particular range or category.
A probability distribution is a thorough description of uncertainty
regarding a quantity. It is built up from a series of expert
judgements about ranges of the uncertain quantity containing the
true value with a particular probability.
A question whose answer is useful to address a subsequent
question. Assessment of a complex question may be facilitated by
dividing it into a series of subquestions.
In this document, uncertainty is used as a general term referring
to all types of limitations in knowledge.
A collective term for the processes used to identify, characterise,
explain and account for uncertainties.
Range of possible prevalence values around the median covering
50% of the probability distribution (P25–P75).
Range of possible prevalence values around the median covering
98% of the probability distribution (P1–P99).

Abbreviations
AHAW
AW
CNS
CRH
CSF
ECoG
EEG
ELISA
EKE
EMG
ES
FBM
fMRI
GABA
GH
HPA
IASP
MAP
MS
NPY
NREM
OIE

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EFSA Panel on Animal Health and Animal Welfare
awake
central nervous system
corticotropin releasing hormone
cerebrospinal ﬂuid
electrocorticogram
electroencephalogram
enzyme-linked immunosorbant assay
Expert Knowledge Elicitation
electromyogram
estrone sulfate
fetal breathing movement
functional magnetic resonance imaging
gamma-amino-butyric acid
growth hormone
hypothalamus–pituitary–adrenal
International Association for the Study of Pain
mean arterial pressure
Member State
neuropeptide Y
non-rapid eye movement sleep
World Organisation for Animal Health

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Slaughter of pregnant animals

PAG
RIA
RCOG
REM
SCVPH
SEP
SER
SPn
ToR
UCO
VAS
WG

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pregnancy-associated glycoproteins
radioimmunoassay
Royal College of Obstetricians and Gynaecologists
rapid eye movement sleep
Scientiﬁc Committee on Veterinary Measures relating to Public Health
somatosensory evoked potential
somatosensory evoked response
subplate neuron
Term of Reference
umbilical cord occlusion
vibroacoustic stimulation
Working Group

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Slaughter of pregnant animals

Appendix A – Literature search on the prevalence of slaughtered pregnant
animals in Europe
As indicated in Sections 2.3.1 (Methodology) and 3.1.2 (Assessment), a literature search was
conducted to identify available evidence concerning the prevalence of slaughtered pregnant animals in
Europe.
The searches were conducted using combinations of terms covering four main question
components: 1) livestock animals, 2) gestation, 3) slaughter and 4) prevalence. The search string used
is reported in Table A.1. The search was conducted in the following database: Web of Science. The
search was conducted for years 1975–2017 and on the following indexes: SCI-EXPANDED, SSCI,
A&HCI, CPCI-S, CPCI-SSH, BKCI-S, BKCI-SSH, ESCI, CCR-EXPANDED, IC.
Table A.1:

Search string used for a literature search on the prevalence of slaughtered pregnant
animals in Europe

Search terms

Field
searched

(((Cull* OR kill* OR slaughter* OR abattoir*) NEAR (pregnan* OR gestat*)))

Title

AND
Title
((Livestock* OR ((Farm OR farms OR farmed OR farming) NEAR/3 animal*) OR ruminant* OR
cattle OR bovin* OR cow OR cows OR calf OR calves OR heifer* OR “Bos Taurus” OR (dairy
NEAR/1 (herd* OR breed*)) OR weaner* OR yearling* OR stirk OR stirks OR springer* OR
feeder* OR beef* OR swine OR (sus NEAR/1 (scrofa OR domestica OR domesticus)) OR pork
OR porks OR porcine OR suidae OR pig OR pigs OR piglet* OR “sow” OR “sows” OR gilt OR
gilts OR equidae* OR equus OR horse OR horses OR equine* OR yearling* OR mare OR mares
OR pony OR ponies OR ﬁlly OR ﬁllies OR ass OR asses OR mule OR mules OR donkey* OR ovis
OR ovine* OR ewe OR ewes OR lamb OR lambs OR sheep* OR mouﬂon* OR hogget* OR ram
OR rams OR tup OR tups OR Goat OR goats OR capra OR capras OR caprin* OR dam OR
dams))
AND
((prevalence OR number) OR (per cent* OR percent*))

Topic

Titles and abstracts of the references were screened to identify relevant papers to be reviewed in
detail. When screening the references, papers were considered relevant if:

•
•
•

they were about pregnant animals during the slaughter situation (and not, e.g. examining
gestation on-farm prior to slaughter);
they were based in Europe;
the paper language was English.

Sixteen references (9 February 2017) were retrieved and screened for studies of interest. After the
screening, four papers were evaluated (Singleton and Dobson, 1995; Jensen et al., 2010; Riehn et al.,
2011; Maurer et al., 2016)

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Appendix B – Literature search on the reasons for slaughtering pregnant
animals in Europe
As indicated in Sections 2.3.2 (Methodology) and 3.2.1 (Assessment), a literature search was
conducted to identify available evidence concerning the reasons for slaughtering pregnant animals in
Europe.
The searches were conducted using combinations of terms covering four main question
components: (1) livestock animals, (2) gestation, (3) slaughter and (4) prevalence. The search string
used is reported in Table B.1. The search was conducted in the following database: Web of Science.
The search was conducted for years 1975–2017 and on the following indexes: SCI-EXPANDED, SSCI,
A&HCI, CPCI-S, CPCI-SSH, BKCI-S, BKCI-SSH, ESCI, CCR-EXPANDED, IC.
Table B.1:

Search string used for a literature search on the reasons for slaughtering pregnant
animals in Europe

Search terms

Field
searched

(((Cull* OR kill* OR slaughter* OR abattoir*) NEAR (pregnan* OR gestat*)))

Title

AND
Title
((Livestock* OR ((Farm OR farms OR farmed OR farming) NEAR/3 animal*) OR ruminant* OR
cattle OR bovin* OR cow OR cows OR calf OR calves OR heifer* OR “Bos Taurus” OR (dairy
NEAR/1 (herd* OR breed*)) OR weaner* OR yearling* OR stirk OR stirks OR springer* OR
feeder* OR beef* OR swine OR (sus NEAR/1 (scrofa OR domestica OR domesticus)) OR pork
OR porks OR porcine OR suidae OR pig OR pigs OR piglet* OR “sow” OR “sows” OR gilt OR
gilts OR equidae* OR equus OR horse OR horses OR equine* OR yearling* OR mare OR mares
OR pony OR ponies OR ﬁlly OR ﬁllies OR ass OR asses OR mule OR mules OR donkey* OR ovis
OR ovine* OR ewe OR ewes OR lamb OR lambs OR sheep* OR mouﬂon* OR hogget* OR ram
OR rams OR tup OR tups OR Goat OR goats OR capra OR capras OR caprin* OR dam OR
dams))
AND
(reason* OR choice* OR decision* OR attitude* OR judgment* OR ethic* OR survey OR
surveys OR questionnaire* OR Respondent*)

Topic

Titles and abstracts of the references were screened to identify relevant papers to be reviewed in
detail. When screening the references, papers were considered relevant if:

•
•
•

they were about pregnant animals during the normal slaughter situation (and not, e.g. on-farm
emergency killing);
they were based in Europe;
the paper language was English.

Thirteen references (9 February 2017) were retrieved and screened for studies of interest. After the
screening, three papers were evaluated (Singleton and Dobson, 1995; Jensen et al., 2010; Thingnes
et al., 2015).

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Appendix C – Elicitation Report
‘PREVALENCE OF PREGNANT ANIMALS SLAUGHTERED IN EU’
EFSA PREMISES, PARMA (ITALY), 16–17 JUNE 2016
This is a summary of the Expert Knowledge Elicitation (EKE) 1 exercise. Country speciﬁc
information has been removed for conﬁdentiality reasons.
PART 1 – EXPERT KNOWLEDGE ELICITATION EXERCISE DESCRIPTION
Purpose of the elicitation
The purpose of this exercise was to estimate probabilities around the prevalence of pregnant
animals slaughtered in the European Union (EU). The exercise follows up from a set of surveys carried
out in 10 EU countries about estimates perceived of such prevalence in 2015 and information from
three data collections currently on-going in the Netherlands (NL), Denmark (DK) and Germany (DE).
Attendants, roles and expertise
The elicitation group included an Elicitor and analyst – from the EFSA Assessment and Methodology
Unit – experienced in the elicitation of expert knowledge using the Shefﬁeld method, a recorder – from
the EFSA scientiﬁc secretariat staff – and a member of the Working Group (WG) on ‘Slaughter of
pregnant animals’ (EFSA-Q-2015-00477).
The Elicitation experts were 6 experts out of the 10 who conducted the surveys in the EU countries
(experts were from Italy, France, Spain, Ireland, the UK and Belgium; experts from Romania, Poland,
Sweden and Greece were not available to participate to the workshop); these were mainly researchers on
animal welfare at slaughter, ofﬁcial veterinarians and auditors in their national slaughterhouses. The
Elicitation group also included representatives of the two EU countries (DE, DK) that are currently working
on national projects to collect data about slaughtering of pregnant animals in their countries and two
observers from the Dutch and German Governments where similar projects are also being performed.
The participants introduced themselves and explained their background and relation to the
elicitation topic. They were invited to indicate possible conﬂicts of interests.
Participants were made aware that judgements made in the elicitation, and the reasoning used,
were going to be recorded, but that they were not going to be attributed to the experts by name
(applying the ‘Chatham House rule’).
Introduction
At the start of the workshop, the Elicitor gave a short introduction into the Expert Knowledge
Elicitation process. He explained the purpose of the elicitation workshop and the tasks that Elicitation
experts would be asked to perform.
Evidence
Under commercial circumstances, the uterus is not opened to speciﬁcally look for pregnancies and
especially ﬁrst term of gestation pregnancies are usually undetected at slaughter. Therefore, the
starting point for the elicitation were a set of surveys carried out in 10 EU countries about estimates of
pregnancy prevalence in 2015 for all species and three data collections currently ongoing in the
Netherlands (NL), Denmark (DK) and Germany (DE). The representatives of NL, DE and DK presented
the preliminary outcomes of their national projects collecting data on the prevalence of slaughtered
pregnant animals.
The project carried out in the Netherlands is a study run in 14 slaughterhouses (5 for cattle, 2 for
pigs, 1 for horses, and 6 for sheep and goats) through a questionnaire similar to that outsourced by
EFSA in the surveys. The overall prevalence of slaughtered animals detected as pregnant was found to
be 1% for cattle, 0.5% for pigs, 1% for horses and 15% for sheep and goats. It was highlighted that
no special attention was given to detect pregnancies in the slaughterhouses, one slaughterhouse
reported very high (50%) incidence of pregnant sheep; also sheep giving birth in the waiting room
was reported. Slaughterhouses usually have no special protocol for managing uterus and fetus: the
uterus is not opened, and will be discarded as usual. One slaughterhouse always reports pregnant
bovines to veterinary authorities.
The project in Germany has been running from the beginning of 2015 and is collecting data on
prevalence, reasons for slaughtering pregnant animals, stage of gestation at slaughter, cost-beneﬁt
calculation and indications on the fate of fetuses after slaughter of the dam. For cattle, a prevalence of
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1.05% was found (but the German meat industry and slaughter associations think it is higher) with
most pregnancies around the second and third terms. For pigs and small ruminants, a prevalence of
0.06% and 2.03% was found with most pregnancies at the second term. Overall, the project leaders
advise that prevalence cannot be averaged because it depends on supply structure, animal species and
category and cooperation of stakeholders.
The project in DK has collected data – for bovines and pigs – about the total numbers of
slaughtered female animals (227,636 bovines and 306,548 sows) and the number of adult female
animals (150,521 for bovines and 298,819 for pigs). The prevalence of those found pregnant at
slaughter was investigated and ranged from 25–75% (best estimate), 20% as estimate for reasonable
low number and 35–75% for reasonable high number. It was also highlighted that pregnancy is usually
not detected until after slaughtering, that the distribution between the pregnancy stages is quite even,
that no differences in stunning of pregnant animals are applied and that the uterus is only opened if
the gestation period is suspected to be in the last 10th. Regarding the latter, if six teeth (three in each
side) have erupted, it is evaluated that the gestation is in the last 10th and a ﬁne will be issued to the
farmer (2004 act on prohibition of slaughtering and killing of pregnant production animals and horses
in the last 10% of the gestation period; for 2015, in bovines 32 non-compliances were found out of
440,000 adult females slaughtered).
Prior to the meeting, the Elicitation experts received a background document summarising i) the
Eurostat statistics about slaughtering and ii) the outcomes of the 10 surveys performed in Sweden,
Italy, France, Spain, Romania, Poland, Greece, Ireland, the UK and Belgium. In each country, 10
slaughterhouses – 4 for cattle, 3 for pigs, 2 for sheep, 1 for goats and 1 for horses, when possible –
were visited. During the meeting, a summary overview from all conducted surveys was given by the
WG member and the main outcomes were discussed.
Training on Expert Knowledge Elicitation process
At the start of the workshop, the Elicitor gave a short training about the EKE process. Afterwards,
the Elicitation experts carried out a practice elicitation in which each expert gave a probability for an
example question. The Elicitor explained that for the questions that followed, the group would also be
asked to arrive at a consensus probability or range of probabilities expressing their collective
judgement.
The elicitation protocol
The same procedure was adopted for questions for each of the slaughtered species of interest, in
this order:
1A) Slaughtering of dairy cows
1B) Slaughtering of female beef cattle
2) Slaughtering of breeding sows
3) Slaughtering of female sheep
4) Slaughtering of female goats
5) Slaughtering of female horses.
The protocol comprised a sequence of individual and group elicitations as follows:
a) The question was reviewed and any queries were clariﬁed.
b) The evidence was reviewed: the relevant section of the background document was examined
i.e. for the species under discussion, the Elicitor presented the ﬁgures from Eurostat about
national and total EU slaughtering and the results from the 10 slaughterhouses visited in each
of the 10 EU countries. Any points of clariﬁcation or differences were discussed; participants
were asked to summarise any additional evidence they considered relevant.
c) Discussion on factors increasing or decreasing the prevalence of pregnant animals
slaughtered: experts were asked to consider their country survey results and any additional
information related to inﬂuencing factors they might have collected during the surveys. An
overall consensus list of factors increasing and decreasing the prevalence at EU level was then
drafted for deﬁning factors.
d) Elicitation about prevalence of pregnant animals slaughtered at national level and EU level:
The Elicitor ﬁrst presented the ﬁgures from Eurostat about slaughtered animals per each EU
country and total EU together with the ﬁgures resulting from each survey performed at
national level. Any points of clariﬁcation and important country differences were discussed.
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Elicitation of judgements about the prevalence of pregnant dairy cows slaughtered was then done
in three steps: ﬁrst the experts were individually asked to judge about national prevalence, then about
the EU overall prevalence and ﬁnally consensus judgements were derived for the EU overall
prevalence.
1st step: The group of experts were asked to write down their initial judgements on the
prevalence at their national level individually, expressed as lower and upper limit,
followed by the best estimate for the prevalence (median), and ﬁnally as interquartile
range (1st and 3rd quartile) to express their uncertainty about the prevalence. The
experts were invited to reﬂect on the evidence provided in their national surveys,
representativeness of the surveys for their whole country, and important factors
increasing or decreasing the prevalence of pregnant animals slaughtered to be
considered in their country.
The initial probability judgements were collected and immediately visualised as
probability densities (using EXCEL) to feedback the individual judgements to the group.
A weighted average for the European prevalence was calculated taking into account the
different production ﬁgures of the countries involved (EUROSTAT). The Elicitor
facilitated a discussion of the judgements made, and the reasons for major changes
compared to their national survey outcomes, or differences between European regions.
In the following step, the experts were asked to consider individually whether to retain
their initial judgement or amend it.
2nd step: The group of experts were then asked to give their judgements on the same question
for the European level. The experts were invited to reﬂect on European differences and
importance for the elicitation question.
Again, the initial probability judgements were collected and immediately visualised as
feedback to the group. An unweighted average was calculated as proposal for a group
result. The Elicitor facilitated a discussion of the judgements made, and the reasons for
major differences in the group.
3rd step: The Elicitor facilitated a discussion working towards a consensus judgement expressing
the collective view of the group. The Elicitor checked for agreement on the result of this
discussion before moving on to the next question.
e) Elicitation about terms of gestation of pregnant animals slaughtered at EU level: The Elicitor
ﬁrst presented the ﬁgures resulting from each survey performed at national level. Any
additional points of clariﬁcation and important country differences were discussed.
Elicitation of judgements about three terms (1st, 2nd or 3rd term) of gestation of slaughtered
animals was then done in three steps, similarly to the elicitation about the prevalence (see point d
above): ﬁrst, the experts were individually asked to judge about national ﬁgures divided by term of
gestation, then about the EU ﬁgures and ﬁnally consensus judgements were derived for the EU
ﬁgures. To simplify the procedure for the proportion of pregnant animals in the ﬁrst and second term
of gestation, only best estimates were asked. Full uncertainty assessment was done for the third
term.10
Strengths and weaknesses
Three experts from the surveys conducted in Romania, Poland and Greece were not available to
participate to the workshop. The participating experts were asked to take into account these three
national survey results when judging probabilities at EU level and when considering factors increasing
or decreasing the prevalence. The experts from Romania, Poland and Greece were given the
opportunity to comment on this report before publication.
PART 2 – ELICITATION QUESTIONS
It was agreed that beef and dairy cows should be dealt with separately due to the differences in
management.

10

After the meeting, the probability distribution of animals in the third term of gestation was recalculated based on animals in
the third term of gestation out of the total number of pregnant female animals. In the opinion only the latter is reported.

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Expert knowledge elicitation on dairy cattle

•

Discussion on main factors inﬂuencing increase and decrease of prevalence in dairy cattle

The experts discussed about the main factors increasing the prevalence of slaughtered pregnant
dairy cows and agreed that they are as follows:
1) Market reasons (end of production period)
2) Health reasons (lameness, mastitis, claw problems) leading to increased costs for keeping
the cows
3) Lack of information during trading
4) At regional level (i.e. depending on the EU region): non-awareness as an effect of natural
mating in pasture farming during the summer period. However, in general the issue of
non-awareness of dairy cow pregnancy is limited due to the use of artiﬁcial insemination
5) Economic crises and low milk prices
6) Lactation period/different breeds/intensity of milk production/exchange time
7) Pregnancy not recognised at early stage (1st third of gestation)
8) Avoiding unwanted behaviour and accidents on slippery ﬂoor because of cows in heat
9) False negative pregnancy test
10) Anabolic effect of pregnancy (more muscle growth)
There was a general agreed view that all reasons could be summarised into economic reasons.
Afterwards, the experts discussed about the main factors decreasing the prevalence in dairy cows
and agreed the following:
1) Good farming practice
2) Increased prices for calves and milk (when milk price gets lower, the prevalence gets higher
– but this is a theoretical factor because dairy calf prices are very low in most EU countries)
3) Surveillance by authorities or slaughterhouses
4) Complete awareness along the production chain.

•

Judgements about prevalence of pregnant dairy cows slaughtered at EU level

Question 1: Please give your judgement on the average occurrence of pregnancy per
100 slaughtered adult dairy cows in Europe in 2015 [in %]
Discussion on the differences between the countries:
Based on the discussion on the Eurostat ﬁgures and national survey outcomes, the participants
agreed that a high prevalence of slaughtered pregnant dairy cows found in some countries is due to the
high prevalence in those regions where cows have 2.5 lactations (meaning that their life is 5 years). This
depends on the intensity of farms because the more intensive they are the more likely the dairy cows
develop metabolic disorders and other health and welfare deﬁciencies and are sent to slaughter. In other
countries, replacement and peak lactation are (heavy) factors leading to selling dairy cows at the ﬁrst
term of gestation. There are other countries with a high prevalence of slaughtered pregnant dairy cows
due again to the intensive production – it is then common to inseminate the dairy cows and then send
them to slaughter when most convenient. On the other hand, there are countries where the production
is less intensive and allows for better surveillance and more care to the whole production cycle.
Collective view on question 1:
Figure C.1 here below represents the density of probabilities, obtained by consensus judgement,
expressing the collective view of the group regarding the overall prevalence of pregnant cattle (dairy
cows) slaughtered.

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Slaughter of pregnant animals

Europe

0.00%

20.00%

40.00%

60.00%

80.00%

Figure C.1: Probability density regarding the overall prevalence of pregnant cattle (dairy cows)
slaughtered
Table C.1 represents the estimated proportion of all dairy cows which are pregnant at the time of
slaughter in Europe.
Table C.1:

Estimated proportion of all dairy cows which are pregnant at the time of slaughter in
Europe. Given are the best estimate (median) and the quartiles (Q) which deﬁne the 50%
uncertainty range (1st Q–3rd Q) as well as the 98% uncertainty range (lower–upper)

Lower

1st Q

Median

3rd Q

Upper

2%

9%

16%

27%

60%

Overall, in the EU, it is possible to observe high and low prevalence of slaughtered pregnant dairy
cows depending on the production intensity.

•

Judgements about terms of gestation of slaughtered pregnant dairy cows at EU level

Question 2: Please give your judgement on the EU average distribution of the stages of
pregnancy for 100 slaughtered pregnant dairy cows [in %]
Discussion on the differences between the countries:
Participants were asked to discuss particularly low and high ﬁgures from the surveys, especially
related to the third term of gestation. In some countries, ﬁgures for the third term of gestation are low
because farmers usually do not sell pregnant animals to slaughter (and there is no intermediate
salesman). In case of health reasons, they cull on farm. High prevalence at third term of gestation was
given in some countries but it was clariﬁed that this was due to the fact that judgement was given
without differentiating beef and dairy cattle. High prevalence in second term can be explained by an
underrating of third term due to incapability of distinction. High prevalence in ﬁrst term is linked to the
fact that high performance dairy herds depend on milk yield and not on gestation phase, so the farmer
can decide to sell the cow at an early stage. It would not be convenient to sell it at the third term
because the feed used to feed that cow is almost already converted into a calf.
Collective view on question 2:
Mostly the differences at EU level are linked to the production system and in general dairy cows are
sold to slaughter only at a very early stage of gestation. Table C.2 here below represents the
estimated proportion of all dairy cows which are pregnant at any stage of gestation at the time of
slaughter in Europe.
Table C.2:

Estimated proportion of all dairy cows which are pregnant at any stage of gestation at
the time of slaughter in Europe

1st term of gestation
46%

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2nd term of gestation

3rd term of gestation

35%

19%

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Slaughter of pregnant animals

Full uncertainty assessment was done for the third term of gestation only and is reported here
below: Figure C.2 represents the density of probabilities, obtained by consensus judgement,
expressing the collective view of the group regarding the overall prevalence of pregnant cattle (dairy
cows) slaughtered at the third term of gestation.

Europe (3rd trimester)

0.00%

10.00% 20.00% 30.00% 40.00% 50.00% 60.00%

Figure C.2: Probability density regarding the overall prevalence of pregnant cattle (dairy cows)
slaughtered at the third term of gestation
Table C.3 represents the estimated proportion of all dairy cows which are pregnant at the third
term of gestation at the time of slaughter in Europe.
Table C.3:

Estimated proportion of all dairy cows which are pregnant at third term of gestation at
the time of slaughter in Europe. Given are the best estimate (median) and the quartiles
(Q) which deﬁne the 50% uncertainty range (1st Q–3rd Q) as well as the 98%
uncertainty range (lower–upper)

Lower

1st Q

Median

3rd Q

Upper

5%

15%

19%

25%

45%

Expert knowledge elicitation on beef cattle

•

Discussion on main factors inﬂuencing increase and decrease of prevalence in beef cattle

The experts discussed about the main factors increasing the prevalence of slaughtered pregnant
beef cattle and agreed that they are as follows:
1) Natural breeding in extensive outdoor farms (note: in beef cattle there is more extensive
production than in dairy) due to unexpected mating plus lack of surveillance in outdoor conditions
2) Longer trading chain leading to reduced/non-awareness of pregnancy
3) Anabolic effect of pregnancy (more muscle growth).
Afterword, the experts discussed about the main factors decreasing the prevalence in beef cattle
and agreed the following:
1)
2)
3)
4)
5)

•

Better pregnancy detection diagnosis due to higher prices of calves
Intensive indoor production (less pregnancy, fewer females)
Better human-animal management, care/accessibility
Retailers and consumer pressure on animal welfare
Penalty at slaughter for pregnant animals.

Judgements about prevalence of pregnant beef cattle slaughtered at EU level

Question 3: Please give your judgement on the average occurrence of pregnancy per
100 slaughtered adult female beef cattle in Europe in 2015 [in %]
Discussion on the differences between the countries:
Based on the discussion on the Eurostat ﬁgures and national survey outcomes, for some countries,
the average was increased based on the assumption that the ﬁrst term of gestation was not detected
in the surveys and also because the survey revealed that sometimes the percentage is very high

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because of the anabolic effect. It was clariﬁed that in Italy beef cattle are not grown but the largest
amount is bought from France.
Collective view on question 3:
The participants agreed that a high prevalence of slaughtered pregnant beef cattle in some countries
is explained by the breed slaughtered by the surveyed abattoirs in which very expensive breeds for meat
are kept extensively outdoors so the bull is there and natural mating occurs (but calves are not
expensive so the dam may get slaughtered). On the other hand, there are countries where the
production is less intensive with more care to the whole chain and it is convenient to keep the calves.
Figure C.3 represents the density of probabilities, obtained by consensus judgement, expressing
the collective view of the group regarding the overall prevalence of pregnant beef cattle slaughtered.

Europe

0.00%

10.00% 20.00% 30.00% 40.00% 50.00% 60.00%

Figure C.3: Probability density regarding the overall prevalence of pregnant beef cattle slaughtered
Table C.4 represents the estimated proportion of all beef cattle which are pregnant at the time of
slaughter in Europe.
Table C.4:

Estimated proportion of all beef cattle which are pregnant at the time of slaughter in
Europe. Given are the best estimate (median) and the quartiles (Q) which deﬁne the 50%
uncertainty range (1st Q–3rd Q) as well as the 98% uncertainty range (lower–upper)

Lower

1st Q

Median

3rd Q

Upper

1%

7%

11%

18%%

40%

•

Judgements about stages of gestation of slaughtered pregnant beef cattle at EU level

Question 4: Please give your judgement on the EU average distribution of the stages of
pregnancy for 100 slaughtered pregnant female beef cattle [in %]
Discussion on the differences between the countries:
Based on the discussion on national survey outcomes, participants were asked to discuss
particularly low and high ﬁgures, especially related to the third term of gestation of gestation.
For some countries, the prevalence of beef cattle found at their third term of gestation is low
because it is an infringement to the transport regulation since cows should not be transported in the
last 10% of gestation. It was, however, noted that the last 10% of gestation can be recognised but
not the whole last third of gestation. Some countries have low percentages representing the accidents
to the transport regulation.
In some other countries, higher prevalence ﬁgures were given and it was explained that often the
ﬁrst is not recognised before cattle are sold to an intermediate salesman. The salesmen buy the live
weight but might keep the cow for some time before selling it to slaughter. Therefore, it can occur that
the salesmen do not know about the cow pregnancy when they buy it (still they know it when they
sell it to slaughter). In other countries, there is also a long trading but the payment is different so the
prevalence of pregnancies is lower: the salesmen pay for the live weight and then they sell the carcass
on the carcass weight (they do not keep the cow for some time but they sell it almost immediately
after buying). In this case, they will not buy and sell a pregnant cow.
Table C.5 represents the estimated proportion of all beef cattle which are pregnant at third term of
gestation at the time of slaughter in Europe.
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Table C.5:

Estimated proportion of all dairy cows which are pregnant at the third term of gestation
at the time of slaughter in Europe. Given are the best estimate (median) and the
quartiles (Q) which deﬁne the 50% uncertainty range (1st Q–3rd Q) as well as the 98%
uncertainty range (lower–upper)

1st trimester
47%

2nd trimester

3rd trimester

38%

15%

Full uncertainty assessment was done for the third term of gestation only and is reported here
below: Figure C.4 represents the density of probabilities, obtained by consensus judgement,
expressing the collective view of the group regarding the overall prevalence of pregnant beef cattle
slaughtered. Overall, the prevalence of beef cattle found at their third term of gestation is quite low
explained by lower prevalence of pregnancy in general. Country differences exist especially in terms of
the trading chain.

Europe (3rd trimester)

0.00%

10.00% 20.00% 30.00% 40.00% 50.00% 60.00%

Figure C.4: Probability density regarding the overall prevalence of pregnant beef cattle slaughtered at
the third term of gestation
Table C.6 represents the estimated proportion of all beef cattle which are pregnant at the third
term of gestation at the time of slaughter in Europe.
Table C.6:

Estimated proportion of all beef cattle which are pregnant at the third term of gestation
at the time of slaughter in Europe. Given are the best estimate (median) and the
quartiles (Q) which deﬁne the 50% uncertainty range (1st Q–3rd Q) as well as the 98%
uncertainty range (lower–upper)

Lower

1st Q

Median

3rd Q

Upper

1%

10%

14%

18%

40%

Expert knowledge elicitation on pigs (sows)

•

Discussion on main factors inﬂuencing increase and decrease of prevalence in pigs (sows)

The experts agreed the main factors increasing the prevalence of slaughtered pregnant sows are as
follows:
1) Economic situation of breeders (bankruptcy, etc)
2) Health status of breeding sows (e.g. lameness)
3) Farm management of pregnant sows (over production): mostly health reasons (weaker
sows, unwanted behaviour)
4) Insemination and high pregnancy rate. In some farms, there is not enough space in the
farrowing crates. If pregnant sows are sent to slaughter in a late stage of gestation, it is
because the farmer waited to send the sows with lower health status
5) Difﬁculty to recognise pregnancy (3 week time before conﬁrmation)
6) Slaughter pigs (early gestation)
7) No control for slaughter pigs (mixed groups with non-castrated males)
8) Country differences of age for slaughtering (up to 9 months in Italy)
9) Production system: outdoor farming has less control of mounting in entire animals.
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Slaughter of pregnant animals

Among the main factors decreasing the prevalence in sows, the experts agreed:
1) Better prices for piglets
2) Good farm management (big farms).

•

Judgements about prevalence of pregnant pigs slaughtered at EU level

Question 5: Please give your judgement on the average occurrence of pregnancy per
100 slaughtered adult breeding sows in Europe in 2015 [in %]
Discussion on the differences between the countries:
In some countries, a high prevalence of pregnancies (all stages) is due to the overproduction
leading to a high rate of animals sent to slaughter. Another factor is the over-insemination: calculation
of loss rate due to health problems leads to more insemination. Then, farrowing crates are the limiting
factor resulting in more sows sent to slaughter. Other countries instead do not commonly have such
overproduction and production of piglets is an added value to the sow production. In other countries,
replacement strategy plays an important role: sows that are not needed are not inseminated leading
to a low prevalence of pregnant sows. The feed cost of a pregnant animal also represents an
inﬂuencing factor: if feed cost is low it is not a problem to feed a sow otherwise they try to avoid
empty days. Some other countries gave low ﬁgures and clariﬁed that, although they have a high level
of uncertainty, they think the prevalence is low because farmer does not send sows to slaughter for
not losing money.
It was agreed that related to the prevalence of pregnant slaughtered sows there is a quite big
variation, associated to high uncertainty, as reﬂected in the discussion.
Collective view on question 5:
Figure C.5 represents the density of probabilities, obtained by consensus judgement, expressing
the collective view of the group regarding the overall prevalence of pregnant sows slaughtered.

Europe

0.00%

5.00%

10.00% 15.00% 20.00% 25.00% 30.00%

Figure C.5: Probability density regarding the overall prevalence of pregnant sows slaughtered
Table C.7 represents the estimated proportion of all sows which are pregnant at the time of
slaughter in Europe.
Table C.7:

Estimated proportion of all sows which are pregnant at the time of slaughter in Europe.
Given are the best estimate (median) and the quartiles (Q) which deﬁne the 50%
uncertainty range (1st Q–3rd Q) as well as the 98% uncertainty range (lower–upper)

Lower

1st Q

Median

3rd Q

Upper

0%

3%

6%

9%

20%

•

Judgements about stages of gestation of slaughtered pregnant sows at EU level

Question 6: Please give your judgement on the EU average distribution of the stages of
pregnancy for 100 slaughtered pregnant breeding sows [in %]

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Discussion on the differences between the countries:
Participants were asked to discuss particularly low and high ﬁgures, especially related to the third
term of gestation. One country explained that a high average (30%) of sows was found at their third
term of gestation. The reason was unknown but it might be due to bankruptcy of two farms.
Table C.8 represents the estimated proportion of all sows which are pregnant at any term of
gestation at the time of slaughter in Europe.
Table C.8:

Estimated proportion of all sows which are pregnant at any term of gestation at the
time of slaughter in Europe

1st term of gestation

2nd term of gestation

3rd term of gestation

30%

10%

60%

Full uncertainty assessment was done for the third term of gestation only and is reported here
below: Figure C.6 represents the density of probabilities, obtained by consensus judgement,
expressing the collective view of the group regarding the overall prevalence of pregnant sows
slaughtered at the third term of gestation.

Europe (3rd trimester)

0.00%

10.00% 20.00% 30.00% 40.00% 50.00% 60.00%

Figure C.6: Probability density regarding the overall prevalence of sows slaughtered at the third term
of gestation
Table C.9 represents the estimated proportion of all sows which are pregnant at the third term of
gestation at the time of slaughter in Europe.
Table C.9:

Estimated proportion of all sows which are pregnant at third term of gestation at the
time of slaughter in Europe. Given are the best estimate (median) and the quartiles (Q)
which deﬁne the 50% uncertainty range (1st Q–3rd Q) as well as the 98% uncertainty
range (lower–upper)

Lower

1st Q

Median

3rd Q

Upper

1%

6%

10%

14%

40%

Expert knowledge elicitation on sheep

•

Discussion on main factors inﬂuencing increase and decrease of prevalence in sheep (ewes)

The experts agreed that the main factors increasing the prevalence of slaughtered pregnant ewes are:
1) High seasonality (holidays): Muslim community concentrates the slaughtering normally
around the end of Ramadan period but the period changes every year – the ewes that are
not good in lambing are discharged and slaughtered but they might be pregnant. The same
issue occurs over the Christmas and Easter period in EU
2) Mainly outdoor/pasture farming, seasonal life cycle, trade in autumn
3) Use of sheep for environmental purpose
4) Less pregnancy diagnosis for outdoor farming (small farms)
5) Health reasons
6) Farming during winter.

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Among factors decreasing the prevalence:
1) More attention paid to year periods of heavy lamb consumption
2) Good price for sheep milk/cheese.
Judgements about prevalence of pregnant sheep slaughtered at EU level
Question 7: Please give your judgement on the average occurrence of pregnancy per
100 slaughtered adult female sheep in your country in 2015 [in %]
Discussion on the differences between the countries:
The participants tackled that in sheep management systems do not inﬂuence much the slaughter
practices because animals are moved all around the EU. Main differences between Eurostat data and
data from the surveys were explained. It was clariﬁed that in the ﬁgures from Eurostat, data related to
northern countries is based on the total population slaughtered (ewes for milk, meat or wool
consumption and also females in extensive condition that might arrive to the adult age but not for
breeding purposes) while in southern countries it only relates to adult ewes.
Collective view on question 7:
Figure C.7 represents the density of probabilities, obtained by consensus judgement, expressing the
collective view of the group regarding the overall prevalence of pregnant ewes slaughtered.

Europe

0.00%

10.00%

20.00%

30.00%

40.00%

50.00%

Figure C.7: Probability density regarding the overall prevalence of pregnant ewes slaughtered
Table C.10 represents the estimated proportion of all ewes which are pregnant at the time of
slaughter in Europe.
Table C.10:

Estimated proportion of all ewes which are pregnant at the time of slaughter in Europe.
Given are the best estimate (median) and the quartiles (Q) which deﬁne the 50%
uncertainty range (1st Q–3rd Q) as well as the 98% uncertainty range (lower–upper)

Lower

1st Q

Median

3rd Q

Upper

0%

5%

10%

14%

40%

Overall, the main difference related to judgements was for some southern EU countries. Breeding
pregnant ewes are sent to the abattoir because of the end of production or for health reason (culling)
and they are likely to be pregnant. It was noted that in some countries, e.g. Italy and Spain, only
lambs are consumed.
• Judgements about stages of gestation of slaughtered pregnant ewes at EU level
Question 8: Please give your judgement on the EU average distribution of the stages of
pregnancy for 100 slaughtered pregnant female sheep [in %]
Discussion on the differences between the countries:
From the national surveys, it resulted that 10% of slaughtered pregnant ewes fall into the third
period of pregnancy. Third stage of pregnancy was found to be high in some countries and was
explained as seasonality of the slaughtering. Instead, reasons for slaughtering at the second stage of
gestation are linked to health or other reasons for which it may not be worth to wait for birth, or

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associated to the fact that in the period between 1st and second stage it is difﬁcult to detect
pregnancy. In some countries, slaughtering for Muslim consumption occurs during the whole year and
most of slaughtered pregnant ewes are found at the ﬁrst stage of gestation.
Table C.11 represents the estimated proportion of all ewes which are pregnant at third term of
gestation at the time of slaughter in Europe.
Table C.11:

Estimated proportion of all ewes which are pregnant at third term of gestation at the
time of slaughter in Europe. Given are the best estimate (median) and the quartiles
(Q) which deﬁne the 50% uncertainty range (1st Q–3rd Q) as well as the 98%
uncertainty range (lower–upper)

1st term of gestation

2nd term of gestation

3rd term of gestation

35%

10%

55%

Full uncertainty assessment was done for the third term of gestation only and is reported here
below: Figure C.8 represents the density of probabilities, obtained by consensus judgement,
expressing the collective view of the group regarding the overall prevalence of pregnant ewes
slaughtered at the third term of gestation.

Europe (3rd trimester)

0.00%

10.00% 20.00% 30.00% 40.00% 50.00% 60.00%

Figure C.8: Probability density regarding the overall prevalence of ewes slaughtered at the third term
of gestation
Table C.12 represents the estimated proportion of all ewes which are pregnant at the third term of
gestation at the time of slaughter in Europe.
Table C.12:

Estimated proportion of all ewes which are pregnant at third term of gestation at the
time of slaughter in Europe. Given are the best estimate (median) and the quartiles
(Q) which deﬁne the 50% uncertainty range (1st Q–3rd Q) as well as the 98%
uncertainty range (lower–upper)

Lower

1st Q

Median

3rd Q

Upper

0%

6%

10%

14%

40%

Expert knowledge elicitation on goats

•

Discussion on main factors inﬂuencing increase and decrease of prevalence in goats

The experts discussed about the main factors increasing the prevalence of slaughtered pregnant
goats and agreed that they are as follows:
1) In southern Europe, meat/milk production from goats is similar to sheep production:
outdoor farming and poor pregnancy diagnosis
2) Goat milk production is a growing sector
3) Seasonality: goat kids are eaten at Christmas time and Eastern in Italy and Spain
4) Milk production is intensive while meat production is in outdoor farms.

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Factors decreasing the prevalence:
1) Goats kept as pets
2) Higher level of artiﬁcial insemination
3) Higher prices for kids of goats

•

Judgements about prevalence of pregnant goats slaughtered at EU level

Question 9: Please give your judgement on the average occurrence of pregnancy per
100 slaughtered adult female goats in Europe in 2015 [in %]
Discussion on the differences between the countries:
From the ﬁgures from Eurostat, it was noted that Spain counts for 75% of the total EU goat
slaughtering. Differences between Germany, Belgium, Italy (where goat is only produced for milk) and
Spain (where it is for meat and milk) are not reﬂected in the European ﬁgures. The UK and Ireland
clariﬁed they have no experience with goats. France and Denmark representatives have left the
meeting prior to this elicitation.
Collective view on question 9:
Figure C.9 represents the density of probabilities, obtained by consensus judgement, expressing
the collective view of the group regarding the overall prevalence of pregnant goats slaughtered.

Europe

0.00%

5.00%

10.00%

15.00%

20.00%

25.00%

Figure C.9: Density of probabilities expressing the collective view of the group regarding the overall
prevalence of pregnant goats slaughtered
Table C.13 represents the estimated proportion of all goats which are pregnant at the time of
slaughter in Europe.
Table C.13:

Estimated proportion of all goats which are pregnant at the time of slaughter in
Europe. Given are the best estimate (median) and the quartiles (Q) which deﬁne the
50% uncertainty range (1st Q–3rd Q) as well as the 98% uncertainty range (lower–
upper)

Lower

1st Q

Median

3rd Q

Upper

0%

2%

4%

6%

10%

•

Judgements about stages of gestation of slaughtered pregnant goats at EU level

Question 10: Please give your judgement on the EU average distribution of the stages
of pregnancy for 100 slaughtered pregnant female goats [in %]
Discussion on the differences between the countries:
Most ﬁgures from the national surveys indicated that most slaughtered pregnant goats fall into the
ﬁrst period. When pregnancy is recognised, the goat is not sent to slaughter for the value of the kids.
In Italy, a high percentage was found in the ﬁrst stage of gestation but the reason is not clear.
Table C.14 represents the estimated proportion of all ewes which are pregnant at any stage of
gestation at the time of slaughter in Europe.

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Table C.14:

Estimated proportion of all dairy cows which are pregnant at any stage of gestation at
the time of slaughter in Europe

1st term of gestation

2nd term of gestation

3rd term of gestation

27%

6%

67%

Full uncertainty assessment was done for the third term of gestation only and is reported here
below: Figure C.10 represents the density of probabilities, obtained by consensus judgement,
expressing the collective view of the group regarding the overall prevalence of pregnant goats
slaughtered at the third term of gestation.

Europe (3rd trimester)

0.00%

10.00%

20.00%

30.00%

40.00%

Figure C.10: Probability density regarding the overall prevalence of sows slaughtered at the third
term of gestation
Table C.15 represents the estimated proportion of all goats which are pregnant at the third term of
gestation at the time of slaughter in Europe.
Table C.15:

Estimated proportion of all goats which are pregnant at third term of gestation at the
time of slaughter in Europe. Given are the best estimate (median) and the quartiles
(Q) which deﬁne the 50% uncertainty range (1st Q–3rd Q) as well as the 98%
uncertainty range (lower–upper)

Lower

1st Q

Median

3rd Q

Upper

0%

3%

6%

8%

30%

Expert knowledge elicitation on horses

•

Discussion on main factors inﬂuencing increase and decrease of prevalence in horses

Due to lack of time, it was only possible to discuss about the factors increasing the prevalence of
slaughtered pregnant horses (mares). The production, from Eurostat ﬁgures, resulted to be quite
important in Italy (more than 70% of total European horse slaughtering). A large number of horses
are imported from Romania to Italy. The prevalence of pregnant mares that are slaughtered is quite
low (max 6%). Health or economic problems are the factors leading to slaughtering horses.
Among the factors increasing the prevalence:
1)
2)
3)
4)

Declaration for meat consumption to reduce killing costs
Mixing of male and female
Horse traders without knowledge of animal pregnancy, less control
Injuries, accidents.

Among the factors decreasing the prevalence:
1) Horses are considered pets
2) Individual slaughtering
3) Higher health surveillance.
Closing remarks
The Elicitor and Recorder thanked everyone for their valuable contributions to the workshop.
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Appendix D – Elicitation Report
SLAUGHTER OF PREGNANT ANIMALS ‘CAPACITY OF FETUSES TO FEEL PAIN AND
NEGATIVE AFFECT’
EFSA PREMISES, PARMA (ITALY), 6–8 JULY 2016
PART 1 – EXPERT KNOWLEDGE ELICITATION EXERCISE DESCRIPTION
Purpose of the elicitation
The purpose of this exercise was to judge probabilities11 around the possibility that fetuses feel
pain – and other negative affects – by expert knowledge elicitation.
Attendants, roles and expertise
The elicitation group included an elicitor – experienced in the elicitation of expert knowledge using
the Shefﬁeld method – a recorder – from the EFSA scientiﬁc secretariat staff – and an analyst – from
the EFSA Assessment and Methodology Unit.
The Elicitation experts were members of the Working Group (WG) on ‘Slaughter of pregnant
animals’ (EFSA-Q-2015-00477) together with nine external hearing experts selected based on the
additional expertise needed for the exercise. Expertise needed related to fetal anaesthesia, fetal
consciousness, fetal and neonatal physiology, pain treatment of the prematurely born child from the
human ﬁeld; animal consciousness, animal welfare, fetal consciousness, effect of hypoxia on fetuses
and effect of various stunning interventions on fetuses from the veterinary ﬁeld.
Participants were made aware that judgements made in the elicitation, and the reasoning used,
were going to be recorded, but that they were not going to be attributed to the experts by name.
Training for the elicitation workshop
A week before the workshop, experts were sent a document explaining the purpose of the
elicitation workshop and the tasks that Elicitation experts would be asked to perform. This was
reinforced by a presentation at the start of the workshop. The Elicitation experts then carried out a
practice elicitation in which each expert gave a probability for an example question, using probability
wheels as a visual aid. The Elicitor explained that for the questions that followed, the group would also
be asked to arrive at a consensus probability or range of probabilities expressing their collective
judgement.
Evidence
Prior to the meeting, the Elicitation experts received a background document summarising evidence
reviewed by the WG, subdivided by key questions needed to address the overall question on whether
fetuses feel pain and negative affect. The background document also speciﬁed that the concept of
pain was extended, by agreement of the AHAW WG and Panel, to negative affect. Additionally, the
experts received the logical model developed by the WG.
The background document included a list of important information gaps identiﬁed by the WG.
Experts were asked to send in advance, or bring to the workshop, any additional evidence on these
points and any other additional evidence they considered relevant.
At the meeting, the mandate on the ‘Slaughter of pregnant animals’ was shortly presented; the
logical model was presented in depth, also focusing on the particular slaughter situations.
The logical model is shown as a ﬂow chart in Figure D.1. It shows the series of subquestions
(approximately corresponding to the questions of the background document), and how they link
together to address the overall question. These subquestions are written in bold and each of them is
followed by a question in italics – the latter is a hypothetical experiment expressing the question in a
way that is potentially observable: this is good practice for elicitation (EFSA, 2014) to aid consistent
interpretation of questions and judgements between experts. The logical model was duplicated and
one version of it was made speciﬁc to the brain cortex and another version speciﬁc to the subcortex
(Figures D.1 and D.2). The questions related to the cortex are indicated as C1, C2, etc; the questions
related to the subcortex are indicated as SC1, SC2, etc.
Strengths and weaknesses

11

The term ‘probability’ used in this report equals to the term ‘likelihood’ as used in the body of the scientiﬁc opinion.

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Figure D.1: Flow charts of logical models as circulated prior to workshop. For version revised at
workshop, with questions as elicited, see Figure D.2 (later)
Three aspects of the framing of questions in the logical model were discussed before starting the
Elicitation Exercise:

•

Extrapolation from different species:

The framing of the questions assumed that the answers to the questions of the logical model are
not species-speciﬁc. A discussion was therefore held whether there are any species-speciﬁc
considerations and whether evidence can be meaningfully extrapolated among species. The
participants discussed that the neurophysiological development is the same but the timing might
slightly change (e.g. precocial animals). From the learning experiments, there are no species-speciﬁc
considerations. It was then agreed that the answers are applicable to all species under consideration
(pig, sheep, cow, horses) and that if a deviation would be found along the process then the distinction
would be made.
• Gestational age:
The questions were phrased in such a way that the answer would be positive if the proposition in
the question was true at one or more points in the gestational age of the fetuses. A discussion was
held on whether the elicitation group should consider the answer in relation to any point in gestation
or to a particular stage of fetal development. Clariﬁcation was expressed by a WG member that the
group will be operating under the precautionary principle, i.e. it is necessary to know if the fetus is
conscious at any age. Comments were raised that, since in the slaughterhouse there is usually no way
to know the exact stage of pregnancy, then there is no need for considering the precise point in
gestation. Other experts suggested that the questions should focus on the stage of neurological
development. The Elicitor explained that it would not be possible in the time available to elicit expert
knowledge on all these variations. It was ﬁnally agreed that the questions would better be re worded
as ‘is there any gestational age at which. . .’ and that at the end of the meeting additional questions
referring to different periods of gestational age would be asked.

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•

Any average fetus:

The questions were framed in terms of the average fetus, based on the assumption that the degree
of variation in answers for fetuses of the same age would be too small to be of practical importance.
Comments were raised that there are important physiological variations, for instance, pathological
conditions – e.g. small placenta leading to hypoxia exposure for the fetus – or different levels of
development – e.g. for lambs where there might be more than one fetus from the same pregnant dam
reaching different levels of physiological development. It was ﬁnally agreed that, although there might
be variations, these do not need to be quantiﬁed but need to be taken into account when considering
the average fetus.
Participants additionally requested some clariﬁcations on the process and on the wording of the
questions. The need to agree on operational deﬁnitions and to include them in the glossary was
highlighted. The deﬁnition of a fetus was discussed: the WG has deﬁned it as a fetus till the moment it
is independent, i.e. the moment it takes its ex-utero ﬁrst breath. However, comment was raised that a
preterm child or animal cannot breathe air successfully but it becomes a newborn anyway. Also, during
the second half of pregnancy, there are several breathing attempts in utero and measurable
behavioural changes provoked by external stimuli. The ﬁnal agreement was that, for the purposes of
discussion in this EKE, the fetus is a fetus till removal from the uterus into a non-ﬂuid (air)
environment.
It was clariﬁed that, for questions 3a–3d, all procedures, subsequent to stunning and sticking, that
potentially affect the fetus should be considered to deﬁne the relevant degree of stimulation.
Structuring of the elicitation
The same procedure was adopted for each question:
1) The question was reviewed and any queries were clariﬁed.
2) The evidence was reviewed: the relevant section of the background document was
identiﬁed and any points of clariﬁcation or disagreement were discussed; participants were
asked to summarise any additional evidence they considered relevant.
3) Experts were asked to write down their initial judgements on the question individually,
expressed as probabilities (in the form of percentages).
4) The initial probability judgements were collected verbally and shown together on a ﬂip
chart.
5) The Elicitor facilitated a discussion of the judgements made, and the reasons for major
differences.
6) Experts were asked to consider individually whether to retain their initial judgement or write
down an amended judgement.
7) The revised probability judgements were collected verbally and shown on the ﬂip chart.
8) The Elicitor facilitated a discussion working towards a consensus judgement expressing the
collective view of the group. The Elicitor checked for agreement on the result of this
discussion before moving on to the next question.
At several points, the Elicitor made clear that (a) if experts felt they lacked relevant expertise for a
question or could not give a judgement, they should not give one, and (b) experts could give either a
single probability or a range for each question.
Questions 3a–3d were asked ﬁrst, then questions 1, 2 and 4. Finally, a set of questions referring to
different gestational ages was elicited. Due to shortage of time, the procedure described above was
reduced for the later questions (as speciﬁed below).
PART 2 –ELICITATION QUESTIONS
Elicitation for questions 3a–3d
Q3: Is there any gestational age at which the average fetus shows a response to a.
hypercapnic hypoxia by maternal circulatory collapse; b. more extreme hypercapnia by
artiﬁcially elevating CO2 levels in the blood; c. mechanical event (e.g. seizures of the dam,
movements); d. electrical current? When a full-term fetus is rendered ‘conditions a, b, c, d’ (see
logical model revised) does it show a measurable response e.g. Motor responses, breathing
movements, heart rate?

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Question deﬁnition
It was clariﬁed that questions 3a–3d are related to measurable responses irrespective of whether
the fetus experiences pain. Any degree of hypoxia should be considered, i.e. the answer would be yes
for a high level but also for a low level of hypoxia.
Questions 3a and 3b differentiate a) situations where hypoxia is generated by the fetus itself
following cord occlusion or maternal circulation arrest/collapse from b) situations in which the
concentration of blood CO2 is increased because the gas-stunned dam transfers it to the fetus i.e.
higher level and quicker level reaching the fetus.
It was agreed that, in terms of the strength of stimulus:

•
•
•
•

3a is intended as maternal circulation collapse, and 50% of blood of the dam is removed
within 20–30 s following sticking.
3b is intended as dam being exposed to 80% CO2 (in pigs).
3c is intended as tonic/clonic seizures of the dam and shackling and hoisting due to inversion
of the dam for cutting plus evisceration.
3d is intended as 1.3 Amp head to body current applied to the dam assuming that a high
amount also reaches the fetus.

Evidence added in the meeting
Participants were asked if there were other examples of measurable responses and the following
were added: EEG, ECoG, defecation, hormone responses, brain imaging changes. These were taken
into account for the responses to the question.
Judgements of probability
Probability judgements (%)
First round judgements in black, second round in red text in brackets, if modiﬁed
Q3a

Q3b

Q3c

Q3d

1
2

100 (99)
90

100 (99)
90

90
90

90
50 (90)

3
4

100 (99)
98

99
98

75 (85)
95

99
98

5
6

95
100

95
80 (95)

95 (98)
80 (95)

95
80 (95)

7
8

95
100

60 (95)
100

95
80 (90)

95
80–100 (90)

9
10

100
100

99 (100)
50

99
100

95–99 (99)
90

11
12

99
95

99
95

95
95

99
50 (95)

13

100

100

100

100

14

100

100

100

100

For the ﬁrst round of judgements, most experts judged the questions 3a–3d with very high
probabilities. The Elicitor ﬁrst asked explanation about the 100% answers, and secondly to the
diverging answers. Expert 14 was asked to explain his/her 100% probability answer and explained that
he/she had seen such outcomes in experimental settings. Expert 13 gave 100% probability answer and
explained that for question 3d the assumption is that the current passes through the fetus. For the
same question, expert 2 gave a 50% probability answer and explained that he/she thought that the
electrical application is so brief that there would not be time for any response. Also, expert 12 gave a
50% for the uncertainty related to the positioning of the electrodes, e.g. if electrodes are placed on
the thorax there is lower probability that the fetus responds to the electric current. Expert 10
explained that for question 3b, he/she gave a 50% answer for the probability that fetus may somehow
become sedated and thus not respond. Expert 5 put all at 95% and not 100% for expressing residual
uncertainty reﬂecting the conﬁdence of experimental studies. Expert 3 put 75% at question 3c
because of the scarce evidence about fetal responses to tonic/clonic contractions.
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After the discussion on the ﬁrst round of judgements, the experts made the second round
judgements of the same questions. In the above table, amended probabilities, compared to the ﬁrst
round, are indicated in red.
Collective view for questions 3a–3d
Group judgement reasoning was discussed and consensus was reached that the following ranges
appropriately represent the collective view of the group:
Question 3a: 95–99.9
Question 3b: 95–99.9
Question 3c: 90–99.9
Question 3d: 90–99.9
Elicitation for question 1
Q1: Is there any gestational age at which fetuses have the anatomical and
neurophysiological structures/correlates necessary for cortical perception? When dissecting
the brain of a full-term fetus, is the cortex present with fully developed thalamocortical connections?
Question deﬁnition
The question was thoroughly discussed: ﬁrst, for some experts the question included two
questions, the ﬁrst asking about the presence of the brain ‘equipment’, the second asking whether
such equipment would provide for the necessary background for perception of affect. Although the
question in italics – i.e. the hypothetical experiment - clariﬁes this aspect, the question in italics is not
necessarily correlated to a positive answer to the question in bold. Therefore, the thalamocortical
connections need to be deﬁned as those related to processing stimuli. Related to the cortical (or
subcortical) perception, expert 6 expressed his/her view that sensation of pain and perception of
affects are two different things. A discussion was held to clarify the meaning of cortical perception. It
was agreed to change the word ‘perception’ to ‘experience’ because breathlessness and affect are
experienced, not perceived. Experts 5 and 6 argued that perception is a lower process than
experience. For instance, perception of pain is an affect but nociception might not be, e.g. nociception
can be associated to no pain perception. WG members explained that the concept of pain was
extended to other negative affect and an expert explained that by the word ‘affect’ it is meant, in
order, breathlessness, hunger and pain. It was ﬁnally agreed that the question should be focused on
experience of pain and other discomforts.
Agreed question:
Q1 revised: Is there any gestational age at which fetuses have the anatomical and
neurophysiological structures/correlates for experiencing pain and/or other forms of
discomfort? When dissecting the brain of a full-term fetus*, is the cortex present with sufﬁciently
developed thalamocortical connections necessary for processing stimuli?
Evidence added in the meeting
Expert 2 suggested adding evidence on EEG of prematurely born child (from 26 weeks of
gestation) to the background document.
Judgements of probability
Probability judgements (%)
First round judgements in black, second round in red (in brackets) if modiﬁed
Q1
1
2

99.9
95

3
4

99
100

5
6

98
85 (95)

7

95

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Probability judgements (%)
First round judgements in black, second round in red (in brackets) if modiﬁed
Q1
8

100

9
10

95
99

11
12

95 (98)
98

13

100

14

95

The Elicitor asked for explanation about diverging probability values. Expert 13 gave a 100%
because in literature it is well documented that, at least at the end of gestation, fetuses have all
structures. Expert 6 explained he/she gave 85% as the answer because he/she interpreted processing
stimuli as all types of stimuli. Expert 12 explained these were all stimuli relevant to a fetus, while
experts 5 and 9 interpreted them as all stimuli relevant to the slaughter conditions. Consensus was
achieved in which stimuli were deﬁned as any of those associated with the measurable responses
listed in question 3a–3d.
Collective view for question 1
After the second round of judgements, group judgement reasoning was discussed and consensus
was reached that the probability for the proposition in this question to be true is in the range from
95% to 99.9%.
Elicitation for question 2
Q2: If so, does the neurophysiological situation allow for cortical perception? If so,
when the full term fetus is subject to a somatosensory stimulus, does the evoked potential include late
latency potentials (those that are speciﬁc to awareness/cognitive processes)?
Due to the intrinsic complexity of the question, the group discussed the appropriateness of the
hypothetical experiment used in the second part of this question. Expert 2 suggested that several
papers studied magnetoencephalography evoked potentials not only during labour but also during
pregnancy (e.g. before and after a mother’s meal). Expert 5 suggested continued learning tests, and
also suggested that for a better understanding of the question there is a need to clarify the meaning
of ‘late’. Expert 13 answered that, in human adults, when stimuli are consciously perceived (as
opposed to not perceived) then evoked potentials are observed 100–140 ms after the stimulus
application. He/she then asked if somatosensory evoked potentials are identical in anesthetised and
non-anesthetised patients. Expert 8 explained they are not identical but there is no clear measure. In
clinics, evoked potentials are used to test the velocity of nerve conductance from peripheral signals,
with focus on the early, rather than late signals. The Elicitor asked if the reliable absence of late
evoked potentials would imply that there is no awareness. Expert 8 answered that the absence would
imply there is brain damage which itself means there is no cortical awareness.
Expert 5 commented that a good question would be if it is possible to arouse a fetus. Expert 12
answered that a fetus cannot be aroused to a semiconscious state by a stimulus because the fetus is
maintained in continued unconscious state. Expert 2 did not agree with this view because papers show
that four or ﬁve behavioural states can be observed in fetuses showing that they have active
responses to pain and stimuli, e.g. noises. Expert 8 agreed on the latter, but commented that evoked
potentials following arousal of a fetus do not mean that it is conscious and arousal is not only deﬁned
as capacity to respond to stimuli. Expert 6 argued that habituation experiments demonstrate cortical
involvement in the response not just a spinal reﬂex.
Expert 2 highlighted that by ‘cortical perception’ it is indeed meant ‘consciously experiencing pain
and discomfort’. The elicitation group agreed that common deﬁnitions of ‘perception’ and ‘pain’ were
needed to respond the question.
Perception might mean ‘state of being aware’. It is characterised by the ability to experience a
variety of negative and positive subjective sensations or feelings. However, experts agreed that states
of alert awareness or perception may have various levels. Expert 11 highlighted that from the

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Regulation on Animal Slaughter (EC Reg 1099/2009) awareness is the ability to feel emotions and
control voluntary mobility. For expert 2, awareness is a disturbed response to an external stimulus
which involves the cortex.
One expert suggested the group consider the IASP deﬁnition of pain: An unpleasant sensory and
emotional experience associated with actual or potential tissue damage, or described in terms of such
damage.
Expert 2 felt that the IASP deﬁnition of pain is focused on adult humans, not applicable to fetus
and animals.
Expert 7 suggested that ‘pain for an animal is considered as the physiological response coming
from any stimulation which is perceived as painful and results in a response to protect against that
stimulus’ (Mohony and Kent, 1997).
It was ﬁnally agreed that question 2 would better be reworded and split in two:
Question 2a. Does the full term fetus subjected to a noxious stimulus, which in the
neonate produces a response indicative of pain, respond with changes e.g. in a
combination of parameters such as EEG (including EPs), HR and BP, attempts to breathe,
grimaces, body movements, stress hormones?
Question 2b. If so, do the observed changes represent conscious experience of pain for
the full term fetus?
Evidence
The Elicitor asked if, in light of the discussion reported above, there was a need to amend the
evidence brought in the background document. Main points related to the paragraph on vibroacoustic
stimulation (VAS) and observed changes in responses; the reported paper by Jardri and the suggested
selective responsiveness, needing to highlight that the evidence is not indicative of associative learning
but only of learning. Expert 2 expressed his/her view that the theory of in utero sedation due to
adenosine, allopregnanolone and pregnanolone, does not take into account that the levels of these
messengers are not different from those in the blood of a mother at the end of pregnancy, thus raising
the question why the mother is not also asleep. He/she also pinpointed the difference between
analgesia and sedation (the fetus might be sedated but this does not imply analgesia). Expert 12
argued that pregnanolone has analgesic effects. Expert 2 responded that analgesic effect is only
observed when injected in cerebral ﬂuid not when naturally produced because the level would not be
high enough. Expert 12 said that allopregnanolone and pregnanolone are synthesised in the brain and
the fetus is producing the hormone. He/she clariﬁed that in the paper from Gregory, the inhibitory
effect was considered to be related to O2 level when in fact it was related to changes in adenosine
concentration consequent on this.
Judgements of probability
Probability judgements (%)
First round judgements in black, second round in red (in brackets) if modiﬁed
Q2a. Does the full term fetus subjected to a noxious
stimulus, which in the neonates produces a response
indicative of pain, respond with changes e.g. in a
combination of parameters such as EEG (including EPs),
HR and BP, attempts to breathe, grimaces, body movements,
stress hormones?

Q2b. If so, do the observed
changes represent conscious
experience of pain for the
full term fetus?

1
2

99.9 (95.9)
95

15 (35)
80 (85)

3
4

95
75 (95)

20
20

5
6

33 (85)
80 (60)

14 (20)
10

7
8

95 (80)
50 (90)

50 (10)
20 (10)

9

95

40 (20)

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Probability judgements (%)
First round judgements in black, second round in red (in brackets) if modiﬁed
Q2a. Does the full term fetus subjected to a noxious
stimulus, which in the neonates produces a response
indicative of pain, respond with changes e.g. in a
combination of parameters such as EEG (including EPs),
HR and BP, attempts to breathe, grimaces, body movements,
stress hormones?

Q2b. If so, do the observed
changes represent conscious
experience of pain for the
full term fetus?

10

98

70

11
12

85
98

30

13

90

50 (40)

14

60 (90)

50 (15)

5–15

Discussion on judgements for question 2a
The Elicitor asked explanation about diverging probability values for the ﬁrst round of judgements.
Expert 5 gave 33% because he/she thinks fetuses do not show changes because they are in a very
speciﬁc physiological state. Also, there is confusion in the available data and it is not possible to know
if a set of changes observed in some studies derived from responses in neonates exposed to stimuli.
Expert 2 and 13 responded that, at pp 8 of the background document, more references are reported
of fetuses responding with behavioural changes. Expert 6 rated it 80% because there is evidence of
single responses but not of the full set of responses and still thinks 80% is quite high. Expert 12
highlighted that cardiovascular changes are similar in fetus and neonates but the most reliable
changes are behavioural and physiological (EEG being the most reliable).
Expert 2 gave 99.9% because he/she interpreted ‘a response’ as any one or more of the set, not
requiring the whole set to be present together. The Elicitor conﬁrmed that this interpretation seems
consistent with the ‘e.g.’ and ‘such as’ in the question, and asked other group members to use this
interpretation when making second round judgements. Other experts rated the question low because
they had not observed grimaces. Expert 3 explained grimaces in fetuses have never been observed,
they are purely theoretical although in rats facial expressions are described. The group decision was to
take out grimaces from the set.
Collective view for question 2a
After the second round judgements, a ﬁnal range of 80–95% was agreed for the response to
question 2a.
Discussion on judgements for question 2b
Expert 2 rated question 2b high (80%) and explained again that he/she does not accept the
assumption of ‘sedated’ fetuses, that do not feel pain, because of three main reasons: (a) fetal sleep is
not continuous, (b) sedation differs from anaesthesia (the latter is the absence of pain and any
movements to any stimulus) and (c) the levels of the supposed sedative substances in fetal blood
appear in scientiﬁc literature to be similar to those in their mothers, who are neither sedated or
anaesthetised during pregnancy. Fetuses respond to external stimuli so they are not anesthetised.
Sedation is instead the reduction of responses due to, e.g. benzodiazepine administration and no one
does surgery relying on benzodiazepine-induced sedation. Expert 12 clariﬁed that what he/she refers
to is ‘sleep like unconsciousness’ and the EEG pattern is the key observation. When you stimulate
arousal there are movements but they are not associated to evoked potentials.
A long discussion was then held on whether this ‘sleep like unconsciousness’ is sedation. Expert 8
said that sedation is a live form of anaesthesia. Expert 2 clariﬁed that with deep sedation there is still a
response to external stimuli. Also, all neuroinhibitors can be used as drugs but the difference would be
the amount, surely a big amount of pregnanolone injected into the brain can anesthetise.
Expert 13 explained that the key point is the deﬁnition of awake and sleep states – and associated
interpretation of EEG patterns – but considered that there is not good enough evidence to distinguish
those states in the fetus.

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Expert 5 said that in surgery the primary aim is to prevent pain: if we imagine removal of the pain
system (i.e. receptors) this would be equal to a completely conscious patient without pain. Therefore,
anaesthesia is not so relevant for this discussion because pain is not the matter in the slaughter
situation, but rather distress and discomfort. The Elicitor reminded that the ToR is about pain, to which
Expert 5 responded that there is no pain if you are not conscious.
Expert 12 expressed the view that focusing the discussion on anaesthesia might be incorrect: when
you are sleeping you are unconscious, but you can wake up. The fetus in contrast does not wake up.
Expert 2 expressed again the fact that four behavioural states have been described, and observed
by obstetricians without EEG, by assessing eye movement, heart and muscle tone but Expert 8
responded that these four behavioural states are observed in humans because it is not possible to do
EEG or ECOG. In animals, EEG is possible on fetuses, demonstrating that there are awake states, but
wakefulness in fetuses is not comparable to that in neonates (interpreted as transitional stages
between sleep states rather than wakefulness seen in neonates).
It was agreed that it is not possible to deﬁne a conclusive hypothetical experiment for question 2b.
The Elicitor went around the table inviting every Expert to comment on the probability they had
given. Expert 12 rated the probability at 5–15% because there are speciﬁc and direct data from sheep
– behavioural and EEG states – demonstrating neuroinhibitory evidence, thus indicating that the fetus
is in a continuous sleep state of unconsciousness. The probability was not rated 0 because it’s difﬁcult
to demonstrate conclusively. Similarly, Experts 5 and 6 rating it at 14% and 10%, respectively. Expert
3 also rated it at 20% for the uncertainty and for the ﬁndings of Fitzgerald concluding that when the
baby is born it is not awake; delivery wakes it up.
Expert 4 rated at 20% after following the discussion and wishing to give a balanced view. Similarly,
Expert 9 rated it at 40% to express uncertainty.
Expert 13 rated it 50% because of the uncertainty in the interpretation of changes in EEG observed
in fetuses. For the same reason Expert 10 rated it on 70% because those signs still express a higher
probability than 50/50.
Since Experts 2 and 12 defended divergent positions, the Elicitor invited each of them to summarise
their position in a 1-min statement:
Expert 2: ‘In the ‘80s and ‘90s of the last century, similar discussions took place about baby’s pain
and the conclusion was that newborn babies don’t feel pain because they are assumed to be always in
a sleeping state. Babies then underwent surgery with no anaesthesia and they showed cortisol rises
and other signs of pain were observed. There is equivalence between fetuses and newborns. I agree
that fetuses spend most of time sleeping but I think studies demonstrate they can be awoken, maybe
not in 100% of cases because e.g. sickness or deep sleep. Fetuses can be aroused and birth is an
example: when they are just born they have still a certain amount of fetal blood components but they
will arouse during birth. Finally, no one would undergo surgery if sleeping only’.
Expert 12: ‘Focusing on distinctions between pharmacologically induced anaesthesia, sedation and
analgesia as a refutation of the published evidence, and on circulating concentrations of the different
endogenously produced neuroinhibitors misrepresents both the rationale and the nature of the detailed
experiments, the results of which support the rationale. Three lines of evidence support speciﬁcally the
presence of continuous states of “sleep-like unconsciousness”, not sedation: (i) direct EEG patterns, (ii)
evidence showing that the physiological environment of the fetal brain in utero is uniquely
neuroinhibitory: there exist at least 8 neuroinhibitory mechanisms with demonstrated neuroinhibitory
actions on the fetal cerebral cortex, and (iii) the inability to rouse the fetus to consciousness using
noxious stimuli that awaken the sleeping newborns of the same species to consciousness. The
question of noxious stimuli and impact on EEG has been assessed several times because all invasive
methods in surgery have been followed by EEG: EEG activation is observed as well as cortisol changes.
It is clear there is no evidence of arousal during general anaesthesia, so I am convinced the fetuses do
not respond to pain’.
Summary of the group view for question 2b
The Elicitor offered a verbal summary of the judgements made by the group: there is a wide range
of opinion with one expert going below 10% and the highest at 80% but no one is certain at either
end. Most of the judgements are in the range 10–30%, with two at 70% and 80% and three at 50%.
The Experts agreed that this would be taken as a summary of their views.

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Elicitation for questions 4a–4d
Will the average fetus showing the responses of question 3a EXPERIENCE a NEGATIVE
AFFECTIVE STATE arising from the SPECIFIED CONDITIONS through CORTICAL
perception? Will the full term fetus demonstrate a change in response frequency (indicative of
aversiveness) in an operant conditioning paradigm using the speciﬁed stimulus (with appropriate
controls)?
Question deﬁnition
Expert 13 explained that this qualifying experiment is not a reﬂex conditioning but an operant
paradigm. The Elicitor asked if the hypothetical experiment was possible and Expert 6 conﬁrmed the
suggested experiment is possible. Expert 12 agreed. Expert 5 said that a conditioning test is not
possible with a conditioned stimulus. Trace conditioning would be the best experiment. Expert 6 said
that it would be possible to establish an experiment requiring learning of a contingency between two
events, using either classical or operant conditioning paradigms. Expert 1 expressed a view that
operant conditioning would help in understanding the outcome while associative learning would be
weaker. Experts were asked to consider also the sub-cortical situation as in question SC4 of the logical
model for subcortex: the question is the same but the question in bold asks about sub-cortical
perception and the question in italics asks if the full-term decorticated fetus demonstrates a change in
response frequency.
Calculation based on earlier judgements
The Elicitor explained that the original form of the logical model (Figure D.1) implied that the
probabilities given for questions 1–3 could be combined by calculation to give estimated probabilities
for question 4, assuming question 2 was conditional on question 1 and both 1 and 2 were independent
of question 3, These calculations were carried out by the EFSA analyst during the workshop and
results for each expert were printed together in numerical form and as pie charts. These results were
distributed to the Experts and brieﬂy explained by the Elicitor. The Elicitor noted that the revision of
question 2 had probably removed the conditionality of question 2a on question 1, making the
calculated probabilities somewhat lower than they should be. The Elicitor stated that the calculations
were presented only to raise awareness of the potential relationships between the questions and
encouraged the Experts not to anchor on the calculated results but rather form their own judgements
when answering question 4.
Given the limited remaining time, the Elicitor asked the Experts to make their ﬁrst round
judgements on Questions 4a–4d without a preliminary discussion of evidence.
Judgement of probability
Probability judgements (%)
First round judgements in black, second round in red (in brackets) if modiﬁed
Q4a

Q4b

Q4c

Q4d

1
2

25
90

30
90

20 (5)
80

30 (40)
70

3
4

15–30 (10)
10

15–30 (10)
10

15–30 (5)
10

15–30
10

5
6

5 (20)
50

5 (20)
50

5 (20)
0

5 (20)
100

7
8

80 (60)
10

80 (60)
10

80 (60)
10

80 (60)
10

9
10

0–15
60–70

0–15
20–30 (50)

0–15
50

0–15
50

11
12

5–10
10

15
10

15
10

5–10
10

13

10

20

10

30

14

10

10

10

10

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Discussion on judgements
A big variation was observed from high to low and it was discussed whether the responses were
high or low for different reasons than for the previous questions 3a–3d. There was group agreement
that these responses would not be possible in a decorticated fetus.
Expert 6 rated the ﬁrst two questions Q4a and Q4b at 50% due to the uncertainty whether electric
and gas stunning would create a response. For the uterine contractions, the answer would be 0 while
for the electrical shock it would be 100%.
Expert 10 gave lower probability for the second condition because if the slaughter procedure
causes high CO2 to the dam, then the death of mother occurs too quickly for the fetus to go to deep
sleep unconsciousness from the CO2.
Expert 12 said that 2% O2 means that any response would be subcortical.
Expert 2 gave different responses for the different conditions because of the uncertainty and lack of
familiarity with the slaughter situation.
Summary of the group view for questions 4a–4d
The Elicitor asked whether the Experts would be content for the range of views in the group to be
summarised after the workshop in a similar way to what had been agreed for Question 2b (above).
This was agreed.
Elicitation on Question C2b in relation to gestational age
The Elicitor noted that insufﬁcient time remained to complete all the planned questions. Related to
the questions on the subcortex, there was no time to consider them extensively; yet a relevant aspect
of it had been considered during the elicitation for question 4 and the discussion led to the agreement
that a decorticated fetus would show no responses to changes. A member of the WG proposed to use
the remaining time to consider Question C2b in relation to gestational age, and this was agreed.
Preceding questions had referred either to a fetus of any age or to full-term fetuses. The Experts
were reminded of the wording of Question C2b (‘If so, do the observed changes represent conscious
experience of pain the full term fetus?’). The probability judgements they had made for C2b were
displayed, and the experts’ own written records of their judgements and reasoning were made
available to those who wished to review them.
The question was expressed as:
Given your probability for question C2b what is your probability of conscious
experience of pain for any ante-natals in each of the speciﬁed gestational age ranges?
Probability judgements (%)
First round judgements in black, second round in red (in brackets) if modiﬁed
100–80%
pregnancy

80–60%
pregnancy

60–40%
pregnancy

40–20%
pregnancy

20–0%
pregnancy

1
2

30–35
95

20–30
90

5 (0–2)
50

0
0

0
0

3
4

20
No answer

7–11 (14)
No answer

1
No answer

0
No answer

0
No answer

5
6

20
10

10
2 (8)

0
0

0
0

0
0

7
8

10
10

2
10

0
2

0
0

0
0

9
10

15–20
70

15
50

0–5 (2)
0–2 (1)

0
0

0
0

11
12

30
5–15 (0)

10
5–10 (0)

5
0

0
0

0
0

13

40

40

0

0

0

14

15

10

5

0

0

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Discussion on judgements
Expert 5 had to leave at this point. Before going, the expert said that he/she now considered that
the evidence presented in the workshop for a sleep-like state in fetuses would make the distinction
between cortex and subcortex distinction irrelevant.
It was observed that probabilities drop off in the third column (40–20% of pregnancy). Experts 1
and 11 agreed that they drop because it is demonstrated that it is only at the last third of gestation
that they may feel pain.
Expert 10 put already a drop in probability at 60–40% of pregnancy but he/she raised such
probability value at the second round.
Expert 2 gave high values for the ﬁrst three periods of pregnancy because there is possibility of
subcortical experience and also because from the 26th week of gestation onwards the human doctors
usually give opioids.
Expert 2 asked about the interpretation of those studies demonstrating that fetuses are awake from
26th weeks. Expert 12 explained that transitional sleep states occupy 5% of the last period of
pregnancy (3 s per minute) but they are sleep transitions and are therefore a continuation of
unconsciousness.
Experts were asked to make their second round judgements on the question. These were not
displayed or discussed, due to lack of time. The Experts were asked to leave their written judgements
and notes on reasoning at the end of the workshop.
Closing remarks
It was not possible to address question C5 within the available time because the difﬁculty of
objectively categorising intensity of affective state would require prolonged discussion.
The Elicitor and Recorder thanked everyone for their valuable contributions to the Workshop. The
Recorder conﬁrmed that the draft report would be circulated to all participants for review.
An updated version of the logical model showing the changes agreed during the workshop. The
wording of questions 1 and 2 was changed; question 2 was subdivided into two questions. The second
logical model relating to the subcortex was not used in the elicitations.

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Figure D.2: Revision of the logical model

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