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Lafuente & López

Meat Science 98 (2014) 247–254
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Effect of electrical and mechanical stunning on bleeding, instrumental
properties and sensory meat quality in rabbits
R. Lafuente a, M. López b,⁎
Gobierno de Aragón, Departamento de Sanidad, Bienestar Social y Familia, Vía Universitas 36, 50071 Zaragoza, Spain
Universidad de Zaragoza, Departamento de Producción Animal y Ciencia de los Alimentos, Facultad de Veterinaria, Miguel Servet 177, 50013 Zaragoza, Spain
a r t i c l e
i n f o
Article history:
Received 15 November 2013
Received in revised form 25 April 2014
Accepted 30 May 2014
Available online 8 June 2014
Neck dislocation
a b s t r a c t
Different voltage and frequency (T-1 = 49 V, 250 Hz; T-2 = 130 V, 172 Hz; T-3 = 22 V, 833 Hz) combinations of
electrical stunning and cervical dislocation (T-4) were studied in 101 commercial rabbits in an industrial abattoir.
Electrical stunning accelerated the early muscular acidification, providing lower pH-45 and pH-2 h values on
Longissimus dorsi and Biceps femoris and higher pH-24 h on Biceps femoris than cervical dislocation (P b 0.02).
Furthermore, meat from rabbits stunned with electrical methods showed more redness (a* with mean values
1.17–1.30 vs. 0.66, P b 0.02), although this cannot be associated to low exsanguination levels because electrical
methods tend to produce even higher bleeding percentage than mechanical stunning (P = 0.063). Haematin
content in muscle, water-holding capacity and cooking losses were similar in all treatments. Shear force did
not change because of the stunning methods, but the members of experienced panel found the meat coming
from electrical stunning T-1 (with intermediate voltages and frequencies) tougher and less juicy than the meat
obtained with other electrical applications or with cervical dislocation (P b 0.05).
© 2014 Elsevier Ltd. All rights reserved.
1. Introduction
The implementation of the European legislation on Animal Protection at the moment of slaughter has led the EU rabbit sector to replace
pre-slaughter mechanical stunning methods (such as the commonly
used cervical dislocation), with procedures that guarantee in commercial
facilities a sufficient degree of unconsciousness and lack of sensitivity to
avoid or minimize the reactions of fear, anxiety, pain and stress until the
death of the animal. In most cases, both in the EU and in other countries,
electrical methods have been chosen for rabbits, with very few abattoirs
using gas, others using pneumatically powered stunning guns (OMAFRA,
2011) and some experiments with captive bolt apparatus (SchüttAbraham, Knauer-Kraetzl, & Wormuth, 1992) which have had little practical repercussion.
The introduction of electrical stunners, with good results from the
point of view of the welfare of the animal (Anil, Raj, & McKinstry, 1996,
1998, 2000; María, López, Lafuente, & Mocé, 2001) and improving the
work in the abattoir in terms of comfort and risk, gave rise to initial
suspicions from the part of specialized workers, who reported that the
carcasses obtained after electric stunning showed more pinkness than
those obtained by traditional procedures, which were very pale. This
made the sector regard post-electrical stunning bleeding as deficient
and, also, question the conservation time of the carcasses and the quality
of the meat. These ideas were not new, since previous references on
⁎ Corresponding author. Tel.: +34 976 762324; fax: +34 976 761612.
E-mail address: [email protected] (M. López).
0309-1740/© 2014 Elsevier Ltd. All rights reserved.
electrical stunning used on pigs discouraged its use on fattened pigs
due to the damage caused to the carcasses and the reduction of the period
of conservation of the meat because of its high blood-holding level
(Ducksbury & Anthony, 1929). There are also some old results on preslaughter electro-narcosis used in rabbits, as it was studied by Croft
(1952), although the methodology was limited and not enough to provoke insensibility periods which were acceptable for the species. Today
the electrical possibilities to stun rabbits in commercial practice are varied and they use indiscriminate combinations of high and low voltages,
together with high and low frequencies and, in turn, with different intensities and application times. This situation, as well as the negative opinion
previously mentioned, led us to develop a work protocol designed to
provide information about some electrical combination which would
successfully induce an adequate degree of insensibility during the
required time and also which would not affect the parameters of
the carcass or the quality of the meat. Results on the degree and pattern
of desensitization and recovery of rabbits in the conditions of this study
were previously published (López, Lafuente and María, 1998; María
et al., 2001). Few studies have been carried out on pre-slaughter stunning in rabbits since then (López et al., 2008; Rota Nodari, Lavazza, &
Candotti, 2009; Xiong, Zhu, Zhao, Shi, & Tang, 2006) or the results are
hardly applicable in commercial practice (Apata, Eniolorunda, Amao,
& Okubanjo, 2012). The present study shows the results on rabbit
meat quality obtained by applying three electrical combinations of
pre-slaughter stunning with a commercial abattoir machine, and compares them with that achieved with the use of cervical dislocation, an
unauthorized practice in EU slaughterhouses, which is nevertheless
R. Lafuente, M. López / Meat Science 98 (2014) 247–254
widely applied in smaller processing in many countries (McNitt &
Swanson, 2005).
2. Materials and methods
2.1. Animals, experimental design and slaughter traits
Terminal rabbits from a three way crossbreeding scheme, from the
same commercial farm and similar conditions on the farm and during
transport to the slaughterhouse were used. The transport was carried
out in a truck. Animals were housed in 8 floors of cages towers (12
rabbits/cage), with a duration of 3.5–4 h of transport and resting for
about 2 h pre-slaughter. The choice of each rabbit was at random, but
they were within the commercial range of 1.8–2.0 kg. Sex was not
considered due to its little effect on meat quality in rabbits (Carrilho,
Campo, Olleta, Beltrán, & López, 2009; Cavani et al., 2000; Trocino,
Xiccato, Queaque, & Sartori, 2003), nor age (62–65 days), but position
on the tower cage was considered (Liste et al., 2009), selecting rabbits
from all cages in the tower for each treatment. The experiment was
conducted following the Spanish and European animal welfare regulations for animal husbandry, transport and slaughter.
A total of 101 rabbits were used. Rabbits were divided into 4 groups
and stunned using one of the following methods: T-1, voltage and
power frequency usually used at this slaughterhouse (49 V and 250 Hz)
(n = 24); T-2, high voltage (130 V) and low frequency (172 Hz) (n =
24); T-3, low voltage (22 V) and high frequency (833 Hz) (n = 27);
T-4, traditional cervical dislocation (CD) (n = 26). Rabbits received the
electric shock in the frontal sinus (Fossa temporalis) through a V-shape
jagged electrode, which provided a good grip. The slaughterer was the
worker usually responsible for the operation in the abattoir. The contact
time of the electrodes was always under 2 s. The combination of extreme
electric values (high voltage + high frequency, low voltage + low
frequency) was ignored because its effects on the degree of insensibility
and the pattern of recovery in rabbits were similar to some of the
electric combinations mentioned (López et al., 1998; María et al., 2001)
and, also, because these combinations are not often used in commercial
Every rabbit was weighed before stunning and slaughtered 10 s after
stunning by exsanguination from the main blood vessels on both sides
of the neck, oesophagus and trachea. Ninety seconds after slaughter,
the rabbit was weighed again: the difference in weight accounted for
the blood loss. For the calculations, we used the absolute values of
blood weight as well as the percentage in relation to the weight of the
live animal.
Immediately after the completion of dressing, which happened 10–
13 min after stunning and 2–3 min after evisceration, the carcasses
were aired for 6 min (normal time in this slaughterhouse) and then
placed in standard storing crates and protected by polyethylene sheets;
they were later kept in cold storage rooms at a temperature of 0–4 °C.
The pH of the Longissimus dorsi (LD) and Biceps femoris (BF) from the
left side was determined in the storage room firstly 45 min after and
then 2 h after the dressing process (CRISON, pHmeter model 507; Crison
Instruments, Alella, Barcelona, Spain). The measurements were taken
with a penetration electrode in the LD at the level of the 5th–6th lumbar
vertebra and in the middle of the BF muscle, the sites recommended by
the World Rabbit Scientific Association (Blasco, Ouhayoun, & Masoero,
2.2. Instrumental and sensory determinations
After 24 h of cooling, the carcasses were evaluated in the laboratory
of the University of Zaragoza, where the pH-24 (pHu; according to Hulot
& Ouhayoun, 1999) was obtained and then the muscles of the dorsalproximal region of the hind limbs (Biceps femoris, Semitendinosus,
Semimembranosus, Abductor cruris, Gluteus and Tensor fasciae latae)
(HL muscles) were dissected, wrapped in aluminium foil and kept at a
temperature of 4 °C for a later chemical colour analysis and to determine
the water-holding capacity (WHC). The Longissimus dorsi muscle from
both sides was also dissected dividing it into two portions, cranial and
caudal. The cranial ones were used to determine the colour on the
area of the cut, as detailed below. They were later vacuum-packaged
in a polyethylene bag and used to study the cooking losses (CL) and
the muscle texture. The caudal sides were vacuum-packaged in a polyethylene bag and reserved for the sensory analysis.
A Minolta CM 2002 (Minolta Inc., Osaka, Japan) spectrophotometer
was used for measuring physical colour in the LD muscle within the
CIELAB system (CIE, 1976) with a D65 illuminant and a 10º observer,
with an aperture size of 2.54 cm, following the methodology of reference given by Honikel (1998) for meat products. A chemical analysis
of the total haem pigments from a minced sample of the HL muscles
was carried out to determine the parts per million of haematin per
gram of muscle using the method described by Hornsey (1956), with
spectrophotometer readings (HITACHI U-1100; Hitachi Ltd., Chiyoda,
Tokio, Japan) of optical density at wavelengths 640λ and 512λ (Alberti
et al., 2005). All measurements were carried out in duplicate.
Water holding capacity was measured using the modified Grau and
Hamm (1953) technique as described by Carrilho et al. (2009), to determine the percentage of expelled juice in a 5 g minced sample of the HL
muscles under a weight of 2250 g for 5 min. Water holding capacity was
calculated as the difference between the initial and final weights of the
samples over the initial weight (percentage of expelled juice). Two samples were used from each rabbit. Both cranial portions of the LD were
kept in polyethylene bags and water-bathed (FLANGE, GFL Series
D3006; GFL Gesellschaft für Labortechnik mbH, Burgwedel, Germany)
at 75–80 °C for 20–25 min to assess the loss of weight after cooking.
Cooking loss was expressed as a percentage and was calculated as the
difference between the initial and final weights over initial weight of
both portions (CL %). Texture was later analysed on these samples
after cutting them as prisms (2 cm length × 1 cm2 base) using a scalpel
and with the muscle fibres parallel to longitudinal axis. On these samples we studied the maximum shear force required to break the sample
perpendicularly to the muscle fibres. A 4301 series INSTRON (Instron
Corp. Barcelona, Spain) machine equipped with a Warner–Bratzler
(WB) device was used.
The sensory analysis was carried out 72 h after sacrifice. A trained
11-member taste panel (ISO 8586) evaluated the samples in red-lit
cabins. Four sessions with 12 samples in each session were required to
obtain the data. In every session, a comparative multi-sample test
with three samples each time in a balanced incomplete-block design
was used to detect differences in sensory features among the four treatments. The order of presentation was changed between panellists and
sessions to avoid first order and carry-over effects (Macfie, Bratchell,
Greenhoff, & Vallis, 1989). Both caudal parts of Longissimus dorsi were
used. They were cooked unseasoned on a SAMMIC P8D-2 (Sammic,
Azkoitia, Gipuzkoa, Spain) double plate grill at 200 °C, inside aluminium
paper, until the internal temperature reached 65 °C (probe JENWAY
2000; Jenway, Staffordshire, United Kingdom). Each sample was cut in
11 pieces, which were served at random to the taste panel on a hot
dish. Bottled water and bread were given to the panel at the beginning
of the session and in between dishes. All the panellists tasted pieces
from all treatments, and giving a total of 132 assessments per treatment.
The parameters were tenderness, juiciness, flavour intensity and overall
appraisal in a non-structured scale of 100 points (where 0 stood for very
tough, no juiciness, no flavour intensity and low overall appraisal, and
100 stood for maximum tenderness, very juicy, high flavour intensity
and high overall appraisal).
2.3. Statistical analysis
Data were processed using the analysis of variance option of the
GLM procedure of the SPSS Statistics (19.0) with the stunning treatment
as a fixed effect. For the sensory test, session was also included in the
R. Lafuente, M. López / Meat Science 98 (2014) 247–254
Table 1
Body weight pre-stunning (LW), body weight post-bleeding and blood loss in the four stunning treatments (mean ± SD).
Stunning treatment
Body weight pre-stunning, g
Body weight post-bleeding, g
Blood loss, g
Blood loss, LW %
T-1 (49 V–250 Hz)
T-2 (130 V–172 Hz)
T-3 (22 V–833 Hz)
T-4 (CD)
1998.89 ± 13.63
1932.59 ± 13.19
66.30 ± 11.49
3.32 ± 0.53
2001.85 ± 17.35
1932.96 ± 16.98
68.89 ± 8.92
3.45 ± 0.42
1994.00 ± 13.73
1926.40 ± 13.45
67.60 ± 13.00
3.39 ± 0.63
2043.85 ± 14.21
1979.62 ± 13.90
64.23 ± 13.02
3.14 ± 0.58
model after analysing the consensus of the panellists for each descriptor. Because the pH was determined in both LD and BF muscles, the
effect of stunning treatment, the effect of the muscle and their interaction on pH values were studied. When F-tests were significant, means
were compared by Duncan's multiple range test with signification
level of P ≤ 0.05. The probability value less than 0.10 was discussed as
a trend. Likewise, a Pearson correlation analysis was performed to evaluate the relationship between some physicochemical (bleeding with
colour variables; pHu and L* with colour variables, WHC, CL, WB shear
force) or sensory variables (tenderness, juiciness, flavour intensity and
overall appraisal). When r was significant, for predictive purposes the
residual coefficient of variation (RCV) (Berg & Butterfield, 1976) was
calculated by simple linear regression analysis.
3. Results
The results on bleeding are shown in Table 1. Although there were
no significant differences between the stunning methods (P N 0.05),
cervical dislocation would tend to cause lower bleeding percentage
because Duncan (P = 0.063) separated means of T1 (3.32ab ± 0.53),
T2 (3.45a ± 0.42), T3 (3.39ab ± 0.63) and T4 (3.14b ± 0.58).
Regarding pH, there was no significant interaction S × M (P N 0.636)
but the effect of muscle factor was significant (P b 0.001) in pH-45, pH-2
and pHu. In consequence, pH values 45 min, 2 h and 24 h post mortem
are shown in Table 2 separately for LD and BF. pH-45 values for any electrical combination were lower than those obtained through mechanical
stunning both in LD and BF (P b 0,01). pH-2 h was also significant
lower after electrical stunning in both muscles. Twenty-four hours
after slaughter the effect of the treatment on the pH was only significant
in the Biceps femoris but with the opposite result, that is to say, the final
pH levels after electrical stunning were higher than those obtained
through mechanical stunning (P b 0,05). Only pHu of T-2 was not significantly different from T-4.
Results of chemical and physical determination of meat colour are
shown in Table 3. The effect of stunning method on colour chemical
parameters was not significant. In turn, the correlation between haematin
content and bleeding level in absolute or relative values was not significant in either treatment. Considering all data together as those of a single
group (T1–4), the amount of haematin (λ = 640) was associated to
bleeding expressed in absolute values, and this correlation was positive
(r = 0.250, P b 0.05). The correlation was not significant when bleeding
was considered in percentage vs. haematin λ640, or in haematin λ512
vs. absolute or relative bleeding. On the other hand, the level of bleeding
was not related to colour parameters CIE L*a*b* (Table 3), which
showed mean values 48.03 ± 2.86 in L* (lightness) and 2.16 ± 1.25 in
b* (yellowness). There was no effect of stunning method on these
values. The a* (redness) values ranged from 1.24 in meat obtained by
electrical stunning to 0.66 in meat obtained by mechanical stunning
(P b 0.05).
The percentage of expelled juice per minced sample from HL muscles was 16.25 ± 3.43%, with no statistical effect of stunning method
(Table 3). In turn, the percentage of cooking loss in the LD portion
water-bathed was 14.73 ± 3.17% on average. The shear force values
did not change with the stunning method.
Sensory analysis showed difference on tenderness (P ≤ 0.05), but
the highest and lowest levels of tenderness were obtained within the
electrical methods, while T-4 meat was not significantly different from
the other groups. Thus, T-1 provided the least tender meat, and this
meat was also the least juicy (P ≤ 0.05) (Table 4). The effect of stunning
method on flavour intensity and overall appraisal (panel mean marks
55.30 ± 15.73 and 48.17 ± 15.72 respectively) was not significant. As
we can see in Table 5, sensory tenderness and juiciness presented a significant positive correlation (r = 0.400, P b 0.01). There was no correlation between flavour and tenderness or juiciness, but the overall
appraisal was linked to each of the sensory characteristics that were
assessed: it increased with higher levels of tenderness, juiciness and
flavour (P b 0.01).
In relation to the physico-chemical traits, within each electric stunning groups the pHu of LD or BF muscles showed a significant and negative correlation with L*, WHC and CL, and not significant or with high
residual coefficients of variation with most of the other features
(Table 6). Within mechanical group there was no relation between
pHu and cooking losses, but was significant and positive with haematin
content (λ = 640). After the combination of the four groups (T1–4) we
observed the usual relations between pH values and the instrumental
properties of meat: an increase of pH-24 is accompanied by a higher
WHC and lower cooking losses, higher redness and lower lightness
and yellowness, as well as a greater shear force and less haematin,
except in group T-4, as just indicated, what is less frequent. In general
BF showed a slightly lower RCV than LD; therefore, it could be a best
Table 2
Effect of stunning on pH 45 min, pH 2 h and pHu values in Longissimus dorsi and Biceps femoris muscles (mean ± SD).
Stunning treatment
T-1 (49 V–250 Hz)
T-2 (130 V–172 Hz)
T-3 (22 V–833 Hz)
T-4 (CD)
Longissimus dorsi
pH 45 min
pH 2 h
pH 24 h
6.79b ± 0.26
6.56b ± 0.23
6.00 ± 0.17
6.84b ± 0.24
6.56b ± 0.22
5.99 ± 0.20
6.84b ± 0.31
6.61b ± 0.26
5.98 ± 0.26
7.06a ± 0.22
6.74a ± 0.18
5.91 ± 0.12
Biceps femoris
pH 45 min
pH 2 h
pH 24 h
6.54b ± 0.29
6.47b ± 0.23
6.18b ± 0.18
6.62b ± 0.31
6.40b ± 0.19
6.12ab ± 0.21
6.57b ± 0.29
6.46b ± 0.24
6.16b ± 0.25
6.82a ± 0.25
6.68a ± 0.24
6.01a ± 0.17
a, b: different letters within row mean differences among treatments, P b 0.05.
R. Lafuente, M. López / Meat Science 98 (2014) 247–254
Table 3
Effect of stunning on instrumental characteristics of rabbit meat: chemical (haematin content) and physical (L*a*b*) colour, water holding capacity (WHC), cooking losses and texture
(shear force) (mean ± SD).
Haematin (ppm/g)
WHC (%)
Cooking losses (%)
Shear force (kg/cm2)
Stunning treatment
T-1 (49 V–250 Hz)
T-2 (130 V–172 Hz)
T-3 (22 V–833 Hz)
T-4 (CD)
27.11 ± 10.58
28.66 ± 22.94
47.54 ± 2.87
1.25a ± 0.65
1.87 ± 1.39
15.27 ± 3.99
14.41 ± 3.18
2.59 ± 0.67
28.72 ± 11.46
26.76 ± 17.48
47.67 ± 3.41
1.30a ± 0.69
2.35 ± 1.15
16.67 ± 3.09
14.55 ± 3.16
2.48 ± 0.62
28.67 ± 13.64
27.75 ± 16.06
47.90 ± 2.81
1.17a ± 0.91
2.04 ± 1.20
16.53 ± 3.76
14.61 ± 3.43
2.46 ± 0.59
31.29 ± 15.57
37.42 ± 24.93
48.95 ± 2.22
0.66b ± 0.70
2.37 ± 1.25
16.50 ± 2.79
15.26 ± 3.04
2.46 ± 0.74
a, b: different letters within row mean differences among treatments, P b 0.05.
predictor of physicochemical properties. Also L* was significantly correlated with some instrumental features, improving estimation of some
variables with respect to BF.
4. Discussion
In the process of slaughter, the stunning method should ideally lead
to the highest bleeding efficiency after throat cutting to obtain better
quality meat. In the production chain, badly bled carcasses are related
to a more intense colour and a less attractive aspect, and vice versa. To
the best of our knowledge, only one experiment has been performed
to study the effect of stunning on blood loss in rabbits (López et al.,
2008). Newly weaned rabbits that weighed 1 kg were slaughtered
after electrical stunning and compared to others slaughtered by the
halal rite without previous stunning. The group electrically stunned
tended to show lower bleeding levels than the halal group. Moreover,
the percentage of blood expelled was higher than the present experiment (4.06% electrical stunning, 4.64% halal, P = 0.075) may be due
to different calculation procedure, to different bleeding times or to different maturity of the animals (Kotula & Helbacka, 1966a; Swatland,
2006), whereby a comparison is quite difficult. In general, our results
for the levels of blood expelled are near the 3.6% referred to by
Ouhayoun (1986) for 10–11 week old commercial rabbits with a weight
of 2.3 kg. According to Gregory (1998), the weight of blood in an animal
is usually about 8% of its live weight and, normally, only about half that
blood is voided during slaughter. When bleeding is delayed after stunning, the volume of blood could decrease (Omojola, 2007). In relation
to the effect of stunning procedure on bleeding and comparing to
other species of similar size, Kotula and Helbacka (1966a, 1966b) studied the kosher method in chickens, which was efficient for a bleeding
period of 300 s when compared to other methods such as brain perforation, electricity, CO2 or pneumatically powered captive bolt stunner.
According to the authors, it leads to high blood retention in the offal,
something that happens when animals are not stunned before slaughter. Kuenzel and Ingling (1977) also studied chicken that had not previously been stunned: when jugular veins and carotid arteries are cut on
one side with partial damage to the backbone, they show spasmodic
muscle movements which result in lower bleeding levels. Even if the
captive bolt stunner only produces brain disruption, with no brain
penetration, the bleeding levels during 120 s are lower than in the
case of electrical stunning (Göskoy et al., 1999).
As refers to electrical methods, Kuenzel and Ingling (1977) note that
cardiac fibrillation occurs when applying voltages of 95 V and AC (alternating current) in chicken, which could be the reason for poor bleeding.
The same authors found wounds in heart tissues in chickens after 130
V AC had been applied and pointed out that, if heartbeat is kept active
during bleeding, bleeding efficiency is higher. Göskoy et al. (1999)
reach the same conclusion when, after 120 s of bleeding, the efficiency
was significantly higher in chickens that did not fibrillate after electrical
stunning. On the other hand, Schütt-Abraham, Wormouth, and Fessel
(1983) compared the bleeding level in chickens that survived electrical
stunning with those that were electrocuted and only found significant
differences during the first 90 s (2.48% vs. 2.08% in live weight, respectively). Ninety seconds later the differences were no longer significant
(2.98% vs. 2.78%). According to the authors, this could mean that the
effect produced by the stunning method disappears if time is given
when bleeding poultry. In this context and according to the results of
Papinaho and Fletcher (1995), a bleeding period of 150 s would be
enough to eliminate the effect of the stunning method on chicken bleeding. The authors did not obtain significant differences when they compared unstunned chickens (0 mA) to chickens stunned at different
currents (50, 100, 150 and 200 mA). However, Contreras and Beraquet
(2001) showed that 360 s is not enough to eliminate the effect of stunning. These authors found that, when compared to chickens stunned by
applying 20 and 40 V, unstunned chickens showed lower blood losses.
Therefore, two factors should be taken into account in after-slaughter
bleeding: the stunning method used and the bleeding time. According to
Kotula and Helbacka (1966a) and Schütt-Abraham et al. (1983), for the
same bleeding times, the stunning method affects the blood expelled in
the initial post mortem moments. Our study suggests that mechanical
methods might produce poorer bleeding efficiency than electrical
stunning, something similar to what happened when animals were
slaughtered without stunning (Contreras & Beraquet, 2001; Kuenzel &
Ingling, 1977). Or maybe it could be that the stunning method causes
some differences in the speed of blood loss after slaughter, faster bleeding with electrical stunning and slower bleeding in the case of mechanical stunning. In our experiment the 90 s bleeding time accounts for the
time needed for the animals to go along the chain, from the initial
Table 4
Effect of stunning on sensory traits of the rabbit meat (mean ± SD).
Flavour intensity
Overall appraisal
Stunning treatment
T-1 (49 V–250 Hz)
T-2 (130 V–172 Hz)
T-3 (22 V–833 Hz)
T-4 (CD)
45.96a ± 23.12
43.18a ± 19.44
55.45 ± 17.81
48.60 ± 15.59
53.72b ± 20.82
48.15b ± 20.31
55.05 ± 16.02
49.63 ± 14.60
51.91b ± 23.79
48.53b ± 18.07
53.65 ± 14.24
46.69 ± 16.83
51.13ab ± 20.60
49.14b ± 19.90
57.05 ± 14.62
47.80 ± 15.79
a, b: different letters within row mean differences among treatments, P b 0.05.
R. Lafuente, M. López / Meat Science 98 (2014) 247–254
Table 5
Pearson's correlation coefficients (r) between traits of the sensory analysis.
Flavour intensity
Overall appraisal
Flavour intensity
Overall appraisal
⁎⁎ = P ≤ 0.01.
slaughter to the cutting machine of the distal part of the front limbs. So,
unfortunately, we could not determine if rabbits bled after this
moment, as the experiment took place in a normalised abattoir. We
cannot, therefore, make any other inferences since, if weighed again,
the amount of blood expelled might have been the same for both
methods, or different.
However, three factors suggest correct bleeding of the rabbits with
any of the stunning methods: no effect of stunning on the haematin
content in the hind limb muscles, few correlations between colour
parameters and bleeding, and the amount of blood eliminated. This
discards the misconception that electrical stunning is connected to
poor bleeding. In fact, very little blood is retained in the meat during
slaughter, and most of the remaining blood is in the offal and major
blood vessels (Gregory, 1998). Warris (1977) and Warris and Rhodes
(1977) indicated that fresh meat contains very little residual blood
and that haemoglobin increases redness in meat only in cases of poor
bleeding. The only significant correlation in absolute measurements
between haematin (λ = 640) and bleeding was positive (r = 0,250,
P b 0.05), which would indicate that rabbits with higher levels of
pigments in their meat show higher blood losses, which is difficult
to explain. When colour is determined in the CIE L* a* b* space, a* values
could indicate that the common belief might have a scientific base after
all, since mechanical stunning goes along with low redness. However, in
the literature we find contradictory results. In the experiment by Dal
Bosco, Castellini, and Bernardini (1997) electrical and mechanical stunning had no effect on the level of redness in the muscle Longissimus
dorsi of rabbit. The same happened in chicken breast after electrical
stunning vs. captive bolt stunning (Hillebrand, Lambooy, & Veerkamp,
1996), although electrical stunning vs. beheading shows different a*
values in this species (McNeal, Fletcher, & Buhr, 2003). In this last
case, values for electrical stunning are lower than values for beheading.
Finally, the effect of electrical stunning and halal was not significant on
the values of redness in rabbit meat, but, subjectively, the colour of the
carcass immediately after dressing was redder with electrical stunning
and paler in halal sacrifice (López et al., 2008). It is important to take
into account the high variability in most colour variables, both in our
case and in the above mentioned studies, which might have made it impossible to find significant effect of the stunning methods in these
It is possible to establish the differences in the post-mortem acidification process: faster with electrical stunning and initially slow but constant and more intense after 24 h with mechanical stunning (at least on
muscle Biceps femoris). The differences in initial acidification have been
reported in rabbits (Civera, Julini, Quaglino, & Ferrero, 1989; Dal Bosco
et al., 1997; Ouhayoun, 1988). Hulot and Ouhayoun (1999), in an extensive review, reported that the stress of electro anaesthesia accelerates
muscular acidification, although it does not modify ultimate pH in
meat. López et al. (2008) found that ultimate pH was, in fact, modified
because of stunning, both in the Longissimus dorsi and in the Biceps
femoris, and in the present study the effect stays in the pH-24 of the
Bicep femoris. These differences between electrical and mechanical
methods can be due to the increase in lactate in the blood produced by
the strong muscle contractions caused by electrical stunning (Sybesma
& Groen, 1970). Nevertheless, Lee, Hargus, Webb, Rickansrud, and
Hagberg (1979) and Papinaho and Fletcher (1995, 1996) in their studies
on chicken breast, obtained initial pH values and also values during the
first 4 h which were higher in electrically stunned animals than in
unstunned animals. The first authors also reported slower glycolysis
(measured as an increase of the levels of lactate in the muscle) and,
consequently, higher pH levels in stunned chickens. On the other
hand, Overstreet, Marple, Huffman, and Nachreiner (1975) obtained
lower pH values in electrically stunned pigs than in unstunned pigs, corresponding to low lactate levels in carcasses that came from unstunned
animals. Later, Velarde, Gispert, Faucitano, Manteca, and Diestre (2000)
confirmed that electrical stimulation of the nervous system in pigs
accelerates the degradation of muscular glycogen into lactate, which
results in a rapid pH fall in some muscles. The present study obtained
the same results in rabbits, and the data suggest that the ATP activity
which determines the changes in pH fall (Monin, 1988) could be more
intense in electrically stunned rabbits and, consequently, the glycogen
reserves in the muscles were used up more quickly in these groups.
As a result, after electrical stunning the pH-24 was higher than after
mechanical stunning, at least in the muscle Biceps femoris.
Taking into account the nature of the muscles, the contractile and
metabolic features affect acidification regardless of the stunning
method used. The muscles studied here have been classified as oxy
glycolitic metabolism by Ouhayoun and Delmas (1983), as the muscle LD has a high amount of type IIB fibres of glycolitic activity and
variable proportions of type I and type IIA fibres, whereas the muscle
BF only has these last types of fibres and consequently shows a higher
oxidative trend. In such a way, the BF showed more acid pH levels during the first 2 h of cooling (Ouhayoun & Delmas, 1988), as well as a
Table 6
Pearson's correlation coefficients (r) and residual coefficient of variation (%, in brackets) between pHu Longissimus dorsi, pHu Biceps femoris and L* with physicochemical parameters.
Group and
Haematin (ppm/g)
−.641*** (4.64)
−.709*** (4.26)
−.625*** (5.58)
−.842*** (3.86)
−.810*** (3.43)
−.891*** (2.66)
−.503** (3.93)
−.816*** (2.62)
−.676*** (4.39)
−.816*** (3.44)
−.357* (48.71)
−.509* (45.51)
.445** (69.76)
.453** (69.48)
−.443** (69.86)
−.399* (97.81)
.294*** (68.75)
.343*** (67.57)
−.457*** (63.98)
−.431* (44.19)
.440* (43.97)
−.335* (55.34)
−.344* (55.17)
.363* (54.73)
.514** (45.13)
−.255** (55.92)
−.343*** (54.33)
.398*** (53.06)
−.353* (36.49)
−.363* (44.35)
−.375* (44.12)
−.249** (43.18)
−.379* (53.57)
.423* (60.37)
−.218* (67.00)
pHu LD
pHu BF
pHu LD
pHu BF
pHu LD
pHu BF
pHu LD
pHu BF
pHu LD
pHu BF
* = P ≤ 0.05; ** = P ≤ 0.01; *** = P ≤ 0.001.
WHC (%)
CL (%)
Shear force (kg/cm2)
−.561** (21.63)
−.511** (22.46)
−.666*** (13.82)
−.663*** (13.88)
.814*** (10.76)
−.604*** (18.15)
−.681*** (16.67)
.450** (20.33)
−.464** (14.98)
−.473** (14.90)
.467** (14.96)
−.569*** (17.38)
−.578*** (17.24)
.495*** (18.37)
−.648*** (16.83)
−.572** (18.12)
.428* (19.97)
−.490* (18.96)
−.619** (17.09)
.679*** (15.98)
−.633*** (18.17)
−.755*** (15.39)
.569** (19.30)
−.519*** (18.41)
−.556*** (17.89)
.501*** (18.63)
.497* (21.59)
−.546** (20.85)
−.531** (20.30)
.455* (26.85)
.296** (24.80)
−.327*** (24.54)
R. Lafuente, M. López / Meat Science 98 (2014) 247–254
quicker acidification and a higher pH 24 h. In relation to Hudson's
(2012) observations about pH decline rate related to mitochondrial
content and meat quality, the red BF showed lower overall changes
between initial and final values than the white LD. The high glycolitic
potential of the LD accounts for the low ultimate pH (Delmas &
Ouhayoun, 1990; Ouhayoun & Dalle Zotte, 1993; Ouhayoun & Delmas,
1988). Our pHu values of BF and LD confirm those obtained by other
authors for rabbits raised in the standard conditions of commercial
farms (Carrilho et al., 2009; Pla, Hernández, & Blasco, 1996; Trocino
et al., 2003) or in other housing conditions (Combes, Moussa, Gondret,
Doutreloux, & Remignon, 2005; Dalle Zotte et al., 2009; Xiccato et al.,
2013). Some experiences in alternative housing with very high availability to perform movements by a low density (Volek et al., 2012) or
physical stimuli induced by endurance training (Gondret, Hernández,
Rémignon, & Combes, 2009) showed a decreased frequency of type IIB
and increased type I and type IIA in BF muscle of trained rabbits compared with sedentary rabbits. Trained rabbits had a similar pHu to the
sedentary rabbits but, according to Gondret et al. (2009), the former
ones improved their oxidative energy metabolism and had a greater
proportion of succinate dehydrogenase-positive myofibers rich in mitochondria and myoglobine, and, accordingly, a greater redness in BF.
Also regardless of the stunning method, the pHu obtained is relatively high in this experiment, with mean values of 5.97 for the LD
and 6.01–6.18 for BF. These pH values close to 6 are not infrequent
in rabbit meat but they are high if compared to the results obtained
in other studies (Dalle Zotte, Rizzi, & Riovanto, 2008; Hernández,
Ariño, Grimal, & Blasco, 2006; Pla, Zomeño, & Hernández, 2008).
These values could be caused firstly by long distance transportation,
as the rabbits used in the experiment were carried in a lorry for at
least 3 h and had to wait over 2 h in the abattoir, which could cause
stress in animals and high ultimate pH in meat (Dal Bosco et al., 1997;
Ouhayoun, 1988). Secondly, the rabbits had to rest before slaughter
(this has not been properly estimated but, in any case, it was over
2 h) which, according to a study on chicken by Khan and Nakamura
(1970), might reduce the rate of glycolysis after sacrifice and result in
high pH 24 h. Finally, in our study the time between the end of the
dressing process and cooling was about 15 min, during which the carcasses were at a temperature of 21 °C; they were later placed in a cold
storage room at 0–4 °C (65% humidity), so the carcass cooling started
soon after slaughter. This could bring about a halt in the consumption
of the energy reserves of the muscle (Ouhayoun, Daudin, & Raynal,
1990) as low temperatures act on myosin ATPasa and actomyosin
ATPasa activity (Ouhayoun, Delmas, Monin, & Roubiscoul, 1990) and
post mortem changes in the muscle are slower with low temperatures
(−1 °C) (Honikel, Roncalés, & Hamm, 1983).
The WHC was low according to previous studies in which slaughter
was carried out after electrical stunning (13–14%, Carrilho et al., 2009),
or electrical and halal (13.7 and 12.8%; López et al., 2008) and unlike
after cervical dislocation, when it was higher (18–19%; Lite, 1989). Evidently, even when using the same technique in the lab, the differences
cannot be attributed only to the stunning method, as, for instance,
the muscles were also different: Biceps femoris in the first two studies, Longissimus dorsi in Lite (1989) and in the group Biceps femoris,
Semitendinosus, Semimembranosus, Abductor cruris, Gluteus and Tensor
fasciae latae in our experiment. Ouhayoun (1988) reports that WHC in
the muscle Abductor cruris (an oxidative muscle) in rabbits improves
if electrical stunning is applied instead of mechanical stunning, whereas
in the Longissimus dorsi the effect is not relevant. In the present study,
the effect of stunning was not significant in the WHC of the HL muscles,
nor in the cooking losses in the LD nor in the shear force texture parameter on the LD, which confirms Dal Bosco et al. (1997) when they
studied the effect of electrical and mechanical stunning on these
quality parameters of rabbit meat. In chickens, Papinaho and Fletcher
(1995) obtain less cooking losses when they were electrically stunned,
if compared with no stunning, but the differences are small according to
the authors. Texture results in chickens are contradictory. In a first
experiment on poultry with an Allo-Kramer blade, Papinaho and
Fletcher (1995) reported higher toughness with high pre-slaughter
electric intensities than with low intensities or no stunning. Nevertheless, the same authors in 1996 and McNeal and Fletcher (2003) could
not find differences between the several electrical systems and no
stunning. The Allo-Kramer cutting values in turkey breast were not
affected by the stunning methods studied by Goodwin, Mickelberry,
and Stadelman (1961), based on Nembutal, brain removing, electrical
blade, CO2, reserpine or no treatment. Also with Allo-Kramer, Lee et al.
(1979) obtained tougher meat in broilers after pre-cooling tank when
chickens were electrically stunned rather than when they were
sacrificed unstunned. After being stored at 2 °C for 24 h, the former
were tenderer. Contreras and Beraquet (2001) obtained similar results
using Warner–Bratzler shears in broilers. According to the first authors,
this would mean that electrical stunning causes tenderness in chicken
meat after some storing time (4 h), which we could not observe in
our experiment. Our WB shear force values support those found in
other studies (Carrilho et al., 2009; Hernández & Dalle Zotte, 2010)
As sensory analysis is concerned, and considering that the panellists
did not find the effect of electrical vs. mechanical stunning significant, in
our study we observed that sensory tenderness and juiciness were positively correlated, as it is often observed in young rabbits (Hernández,
Pla, Oliver, & Blasco, 2000; Jehl & Juin, 1999), although this relation is
not so clear in older rabbits (Gondret, Juin, Mourot, & Bonneau, 1998).
Both variables were scored differently between treatments, being T-1
the least valued for both qualities. There is no reason to think of any
meat deterioration in this group that could account for the lower
score: the pre-slaughter treatment was similar to that in other groups
and this group did not stand out when considering their desensitization
pattern compared to other combinations of frequency and intensity
(María et al., 2001). We should point out that, although there was no
effect of the stunning procedure on WHC or on shear force values, this
T-1 group showed high pHu, which was significantly correlated to
these traits in the total T1–4. Therefore, we can infer that some differences which were not detected in the instrumental evaluation might
appear when compared sample to sample in the sensory analysis.
These results of our study are especially important, as treatment T-1 is
the one applied in this commercial abattoir on a regular basis. According
to the above said, this electric combination must be changed if we want
to offer better meat quality to consumers.
Also our results indicate that as the meat from electric stunning has a
high pHu level, it is prone to have more conservation problems,
although, as a positive thing, the rabbit meat is quickly commercialized
and it is consumed before 24–48 h post mortem. Moreover, low values
in tenderness and juiciness do not affect the panellists' global appraisal,
but, if both sensory features improved, the overall appraisal would also
be better due to the positive correlation between them. Finally, working
procedures in abattoirs should be revised to correct anything necessary
in order to obtain the best possible sensory qualities of the product for
the market. In our case both T-2 and T-3 treatments were similar from
a welfare point of view (María et al., 2001), but pHu in T-2 is near to
the lower pH values of this experiment; therefore, it could be a more
adequate treatment. More studies would be necessary to take decisions
about the best electrical combinations in the abattoirs and, even, to
know which stunning method is the best to obtain a high meat quality.
Simple protocols designed to compare the routine procedure with
respect to some alternative methods, taking into account a taste panel
and using pHu of LD or, better, of BF or L* as moderate predictors of
the physicochemical traits, could be useful to improve meat quality.
5. Conclusions
This study has shown that electrical stunning accelerates the early
muscular acidification, can provide high pHu values on some muscles
of rabbits and can be linked to higher redness, but not to low exsanguination levels. Extreme voltage and frequency could be preferable to
R. Lafuente, M. López / Meat Science 98 (2014) 247–254
medium voltage and frequency levels with the aim of improving sensory qualities, such as tenderness and juiciness. Nevertheless, this study
suggests a revision of the current working procedures in abattoirs, gathering the opinion of sensory panels in order to recommend the optimal
level to stun rabbits. pHu of BF or L* of LD, as moderate predictors of the
physicochemical traits, could contribute to improve the working conditions and the rabbit meat quality.
The authors are to grateful Mr. Félix Cativiela for allowing us to use
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