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Meat Science 98 (2014) 505519

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Meat Science
journal homepage: www.elsevier.com/locate/meatsci

Halal and kosher slaughter methods and meat quality: A review


M.M. Farouk a,, H.M. Al-Mazeedi b, A.B. Sabow c,g, A.E.D. Bekhit d, K.D. Adeyemi e,g, A.Q. Sazili f,g, A. Ghani a
a

AgResearch Limited, Ruakura Research Centre, East Street, Private Bag 3123, Hamilton, New Zealand
Kuwait Institute for Scientic Research (KISR), PO Box 24885, Safat 13109, Kuwait
c
Department of Animal Resource, University of Salah al-Din, Erbil, Iraq
d
Department of Food Science, Division of Sciences, University of Otago, PO Box 56, Dunedin, New Zealand
e
Department of Animal Production, University of Ilorin, PMB 1515, Ilorin, Nigeria
f
Halal Products Research Institute, Putra Infoport, Universti Putra Malaysia, 43400 UPM Serdang, Selangor, Malaysia
g
Department of Animal Science, Faculty of Agriculture, Universti Putra Malaysia, 43400 UPM Serdang, Selangor, Malaysia
b

a r t i c l e

i n f o

Article history:
Received 14 April 2014
Received in revised form 27 May 2014
Accepted 29 May 2014
Available online 5 June 2014
Keywords:
Ritual slaughter
Nutrition
Stunning
Safety
Meat spiritual quality

a b s t r a c t
There are many slaughter procedures that religions and cultures use around the world. The two that are commercially relevant are the halal and kosher methods practiced by Muslims and Jews respectively. The global trade in
red meat and poultry produced using these two methods is substantial, thus the importance of the quality of the
meat produced using the methods. Halal and kosher slaughter per se should not affect meat quality more than
their industrial equivalents, however, some of their associated pre- and post-slaughter processes do. For instance,
the slow decline in blood pressure following a halal pre-slaughter head-only stun and neck cut causes blood
splash (ecchymosis) in a range of muscles and organs of slaughtered livestock. Other quality concerns include
bruising, hemorrhages, skin discoloration and broken bones particularly in poultry. In addition to these conventional quality issues, the spiritual quality of the meat can also be affected when the halal and kosher religious
requirements are not fully met during the slaughter process. The nature, causes, importance and mitigations of
these and other quality issues related to halal and kosher slaughtering and meat production using these methods
are the subjects of this review.
2014 Elsevier Ltd. All rights reserved.

1. Introduction

2. Denitions and importance of meat quality

Ancient traditions have long guided the production, slaughter


and preparation of meat for human consumption. Two of these, halal
(lawful) and kosher (ritually pure), are still widely practiced by
Muslims and Jews, respectively. The global volume and value of meat
commercially produced using halal and kosher methods are huge
(Table 1). Producers and consumers demand that the quality of this
meat is on par or even better than their equivalents produced using
conventional methods.
Meat quality is generally described in terms of aesthetic, tactile, masticatory, functional, nutritional, health, convenience and environmentalimpact attributes. These can be affected by halal and kosher customs
associated with pre-slaughter, slaughter and post-slaughter (Farouk,
2013).
In this review the impact of the halal and kosher religious slaughter
practices on meat quality are discussed.

2.1. Conventional perspective

Corresponding author. Tel.: +64 7 838 5260.


E-mail address: mustafa.farouk@agresearch.co.nz (M.M. Farouk).

http://dx.doi.org/10.1016/j.meatsci.2014.05.021
0309-1740/ 2014 Elsevier Ltd. All rights reserved.

Producers must follow narrow denitions when grading carcasses


and cuts for quality, but consumers' perception of meat quality is wide
and subjective. It reects regional and national differences, ethnicity
and culture, political and economic considerations, individual beliefs
and ideologies, and package labeling information and context (Fayemi
& Muchenje, 2012; Grunert, 1997; Korzen & Lassen, 2010; Krystallis,
Chryssochoidis, & Scholderer, 2007; Ndu, Muchenje, & Chimonyo,
2011; Polkinghome, Nishimura, Neath, & Watson, 2011; Thompson
et al., 2008; Zepeda, Sirieix, Pizarro, Corderre, & Rodie, 2013). Meat quality is also judged in terms of intrinsic/extrinsic, table/eating, visual/appearance, manufacturing/technological, nutritional/health, safety/
reliance, expected/experienced, functional/chemical, physical/sensory
and credence factors (Farouk, Beggan, Hafejee, Freke, & Bekhit, 2007;
Grunert, 1997; Joo & Kim, 2011; Troy & Kerry, 2010).
Aesthetics such as color and marbling, and eating qualities like
tenderness and juiciness, are intrinsic to meat, whereas reliance quality
traits such as safety, price, presentation, packaging, origin and brand
are extrinsic (Grunert, Bredahl, & Bruns, 2004; Joo & Kim, 2011; Troy
& Kerry, 2010). Tenderness, juiciness and avor are important considerations at the dining table, in contrast to meat protein solubility and the

506

M.M. Farouk et al. / Meat Science 98 (2014) 505519

Table 1
Value (USD x 1000) of imported halal and kosher red meat, poultry and co-products of some selected countries/regions in 2012.
Importing country/region and products

Red meat category

Poultry meat/offal

Chilled beef

Frozen beef

Lamb and chevon

Edible offal

Halal red meat, poultry and co-products


Indonesia
Maghreb
Malaysia
Middle East
- Saudi Arabia
- United Arab Emirates

11,499
57,276
16,972
598,504
75,043
160,105

127,715
305,497
410,097
2,942,249
362,267
195,407

8,083
36,842
95,742
897,159
225,707
223,470

16,792
3,940
48,336
278,916
36,540
12,516

1,209
175,520
108,341
4,078,447
1,513,312
644,587

Kosher red meat. Poultry and co-products


Israel
World total red meat import

264
19,803,464

418,421
17,797,649

9,033
5,642,451

10,854
6,786,811

10,605
25,041,855

Source: Market Analysis Research, International Trade Centre (ITC) Geneva Switzerland (http://www.trademap.org/tradestat/Country_SelProductCountry_TS.aspx). Accessed 23 March
2014.
Maghreb = Algeria, Libya, Mauritania, Morocco and Tunisia.
Middle East = Bahrain, Egypt, Iran, Iraq, Jordan, Kuwait, Lebanon, Oman, Palestine, Qatar, Saudi Arabia, Syria, Turkey, UAE and Yemen.

ability of the solubilized proteins to bind water and fat, which are key parameters during manufacturing. Some characteristics, such as high water
holding capacity (WHC), inuence perceived quality for both the diner
and the manufacturer, particularly for meat intended for frying, grilling
or roasting. However, the same WHC quality is not desirable for a jerky
manufacturer wanting to dry the meat quickly and cheaply.
These conventional denitions of quality are based on inherent or
perceived physical characteristics of meat. For most consumers they
determine the meat's appeal, acceptability, utility and, ultimately, its
value.
2.2. Spiritual perspective
Spirituality and ideology inuence people's attitude toward the
killing of animals and the consumption of meat. Consideration of the
source, life and death of the animal adds another dimension to meat
qualityone that cannot be evaluated by science or measured by instruments. Nevertheless, down-grades on those attributes can have a
marked effect on meat value.
Religions are rich with traditions around eating. For example Islam
teaches that all animals are created by God (Quran 24:45), with some
created specically for man's benet (Quran 36:71) to domesticate
and use for transportation and food (Quran 23:21; 40:79). God provided
these animals for their edible parts as well as their useful by-products
(Quran 16:5, 80). They are to be sacriced for His own sake and the
meat distributed to the poor (Quran 22:34, 36) who cannot on their
own afford to buy and slaughter an animal for meat.
A key condition of the permission given to man to slaughter and eat
the esh of animals is to mention the name of God during the
slaughtering (Quran 6:121; 22:36). According to Al-Qaradawi (1960),
acknowledging God during the slaughter is tantamount to the slaughterer rst obtaining consent from his and the animal's Creator to take
the life of another creature; and it is a declaration on the part of the
slaughterer that his act is not an act of aggression against the universe
nor of oppression of the creature about to be slaughtered, but simply
an act necessitated by a need fullled in the name of God. Conversely,
under some condition consumption is prohibited, such as animals that
were dead prior to exsanguination, or that were slaughtered without
mentioning God, or in which other deities or names other than that of
God were professed during the slaughter, will corrupt the heart and result in loss of piety and acceptance of prayer (Sahih Al-Bukhari 1/49;
Sahih Muslim 2/703).
Thus, in addition to all the conventional terms used to convey the
qualities of meat, spiritual quality is of foundational importance for
Muslims as well as some other faith groups (Fig. 1). Indeed it is the
chief consideration for a large population of consumers and supersedes
physical properties of meat such as color, tenderness, juiciness, protein

solubility, and WHC. For halal and kosher adherents, meat that has graded well, yet failed to meet the minimum requirements of religious commandments during its production, would be considered spiritually
worthless.
2.2.1. Harmonizing spiritual and temporal views
Industrial production of high-quality meat must juggle the disparate
demands of consumer groups and food safety regulators. There is urgent
need to harmonize devout spiritual views with those that are temporal
or corporeal and which are based on scientic evaluation. A major area
of contention is the slaughter of animals without stunning prior to
throat slit and exsanguination. This practice is allowed in many countries, but it is extremely controversial with regard to animal welfare.
Areas of concern include the stress of restraining the animal, whether
the cut is painful, and whether the animal experiences undue distress
while bleeding out, such as the aspiration of blood into the lungs
(Grandin, 2010; Gregory, 2005).
Islam teaches that animals are to be slaughtered according to the
mindful and attentive way taught by the prophet (prophetic method).
This includes giving the animal full access to feed and water before

Halal consumer
Desired meat attributes
Marbling

Juiciness

Appearance

Texture/Firmness

Water & fat


binding capacity

Safe
Country of origin

Gelling capacity
Price

Flavour

Packaging

Aroma

Emulsion activity
index

Colour

Tenderness

Protein solubility

BSE free
Organic
Healthy/
nutritious

Spiritual quality
This is the foundation of quality on which all other quality considerations rest

Halal livestock
Legally owned &
ethically farmed

Slaughtered the prophetic


way, faithfully & sincerely

Fed and watered


prior to slaughter

Fig. 1. Spiritual perspective of meat quality showing the importance of spiritual considerations over temporal in determining the quality of meat.

M.M. Farouk et al. / Meat Science 98 (2014) 505519

slaughter, using a sharp knife to quickly severe the four vessels in the
neck, mentioning the name of God during the slaughtering with sincerity and conviction, such that the animal will be dispatched as painlessly
as possible.
For Muslims, meat produced this way would be considered of the
highest spiritual quality. On the other hand, this method of slaughter is
considered cruel and contrary to scientic wisdom by those who think
that the animal must rst be stunned in order to avoid compromising
its welfare. These groups advocate for food labeling that identies meat
from animals slaughtered without stunning and they consider such
meat to be ideologically of the lowest quality. The importance of harmonizing these opposing views and the issues involved for commercial
production of meat could be understood in light of reviews by Ahmed
(2008), Regenstein (2012), Silver (2011) and Zoethout (2013).
The combative posturing of the rival sides is partly a result of outdated thinking that pitches science against religion and encourages
dogmatic arguments that create stumbling blocks toward progress
(Nelson, 2006). In fact, there is an essential starting point for nding
consonance in the pre-slaughter stunning debate; both sides agree
that animal welfare is important in the production of meat. Thus resolution seems possible. In similar spiritually charged arguments, a critical
and rational examination of the issues often reveals little basis for conict between practitioners and their world views (Bainbridge, 2004;
Bakar, 2005; Smedes, 2005). As Harper (2001) puts it, both science
and religion have practical reasons for exploring constructive dialogue
to avoid the conict-perpetuating tendencies of both religious fundamentalism and its scientic counterpart, reductionist scientism. Such
tendencies are unhealthy for both science and religion.
For this debate to become a dialogue, some signicant differences in
cognitive orientation and epistemology must be overcome. Proponents
of conventional pre-slaughter stunning need to consider whether:
true knowledge includes not only scientic or empirical knowledge,
but also metaphysical and theological knowledge, which are useful
and should not be discounted (Nelson, 2006);
people's deepest cultural values, often nourished and embodied in
religious contexts, should be appreciated as more than outmoded
nonsense, with a certain humility and respectfulness by science
toward this accumulated reservoir of moral wisdom (Harper, 2001);
science should not try to use its methods to explain what is spiritual
or use inciting vocabulary or attempt to superimpose empiricist
meanings on religious terms in its discourse with religious groups
(Henriksen, 2008; Regenstein, 2012);
it is possible that when religious slaughter is done faithfully and

507

properly, the welfare of the slaughtered animal is not compromised,


even if this cannot be veried scientically using currently available
instruments.
On the other hand, supporters of non-stunning methods need to
acknowledge that:
some commercial production facilities have poorly trained
slaughtermen and unacceptable animal restraint systems that cause
unnecessary animal suffering;
in some unscrupulous processing plants and backyard abattoirs,
religious invocations are merely whitewash over horric slaughter
practices (Gregory, Schuster et al., 2012; Gregory, von Wenlawowicz
et al., 2012);
scientic methods that have been proven to harmonize the religious
and spiritual requirements must be adopted to improve animal welfare
and to produce meat of both high spiritual and conventional qualities.

3. Halal and kosher meat production practices


The pre- and post-slaughter practices involved in halal and kosher
production of red meat have been recently reviewed (Farouk, 2013)
and are compared (Table 2) and pictorially represented together with
poultry slaughter practices in Figs. 2, 3 and 4.
The impact of these practices on meat quality can be discussed under
three broad categories:
1. Pre-slaughter practices include (a) the use of restraints to hold livestock in place for ease of slaughter and the welfare of the slaughtered
livestock and the safety of workers; (b) pre- and post-slaughter
stunning particularly the use of head-only electrical stunning in
halal meat production; and (c) how closely the halal and kosher
requirements have been adhered to pre-slaughter.
2. Slaughter and post-slaughter practices include the slaughtering
activity and the subsequent use of immobilization and thoracic sticking in halal and schechita (kosher ritual) practices, plus the removal
of residual blood in kosher meat production.
3. Combination of pre- and post-slaughter practicesThe use of electrical currents in pre-slaughter stunning and post-slaughter immobilization increases the electrical inputs in carcasses that could lead to
the rapid fall in pH in muscles post-mortem compared to the use of
mechanical stunning without immobilization or no stunning at all.

Table 2
Comparison of halal and kosher meat production and consumption practices (Farouk, 2013; Regenstein et al., 2003).
Practice/attribute

Kosher

Halal

Pre-slaughter handling
Pre-slaughter state of consciousness
Pre-slaughter stunning

Humane and deliberate treatment required


Animal must be alive and conscious pre-slaughter
Any stunning that renders the animal insensible prior to
slaughter is not acceptable. None of the current methods are
acceptable
Accepted by very few kosher authorities
Must be a Jewish shochet
A special knife (chalef) is required for each specie
Not required on each animal
Must be a single stroke to severe the four vessels in the neck
without severing the head. Multiple strokes renders meat
non-kosher
On the complete death of the animal
Required practices
Foundationally important
Not acceptable. Must be koshered
Certain parts of the carcass and some organs are not eaten
Kosher status could be affected when mixed with certain
kosher foods
Kosher meat is halal for Muslims

Humane and deliberate treatment required


Animal need only be alive pre-slaughter
Although non-stunning is most preferred, reversible forms of
stunning is widely accepted and practiced

Post-slaughter stunning
Slaughterer
Slaughter knife
Blessing on animals at time of slaughter
Slaughtering

Post-slaughter further processing


Porging and koshering
Meat spiritual quality
Residual blood in meat following slaughter
Edible portions
Meat spiritual status
Acceptability

Next-best to no-stun for the proponents of this method


A Muslim or a practicing Jew (follower of Judaism) or Christian
No special knife is required. Knife can be used across species
Required on each animal
Single stroke is preferred. Multiple strokes do not render the meat
non-halal. The head should not be deliberately severed during
slaughter
On the complete death of the animal
Not required
Foundationally important
What naturally remains in meat is acceptable
All edible parts are halal
Halal status remain regardless of what other halal food it is mixed
with
Halal meat is not kosher for Jews

508

M.M. Farouk et al. / Meat Science 98 (2014) 505519

Fig. 2. Steps in the industrial production of halal red meat including stunning, slaughter and further processing using modern slaughter methods.

3.1. Pre-slaughter practices


3.1.1. Pre-slaughter restraints
Animals to be slaughtered must be properly restrained. This is
particularly important in halal and kosher methods where the
animal's neck needs to be presented to the knife and held relatively
still until the slaughtering is complete (Agbeniga, 2012). Secure
restraint spares the animal from distress, pain, bruises and injury

(Lambooij, van der Werf, Reimert, & Hindle, 2012; Velarde et al.,
2014). Common methods of restraining red meat animals prior to
stunning and/or slaughter include hoisting by hind-leg, casting
with a rope and/or chain, restraint in a V-shaped or straddled
conveyor, full or half inversion in a rotary pen and upright restraint
system (Gregory, 2005) while the use of cones and shackling
are common methods of restraining birds (Lambooij, Pieterse,
Hillebrand, & Dijksterhuis, 1999).

Fig. 3. Halal slaughtering of lambs showing animals at lairage, being stunned, slaughtered and bled using modern slaughter methods.

M.M. Farouk et al. / Meat Science 98 (2014) 505519

Problems and risks associated with old fashioned restraint systems


were addressed in the design of upright restraints (also known as
ASPCA pens), as demonstrated by Koorts (1991) who observed that
the severity and prevalence of struggling were higher in animals
inverted in casting pen than those positioned uprightly following
kosher and conventional slaughter. Similarly, Dunn (1990) observed
lower hematocrit, cortisol and ultimate pH in cattle slaughtered in
ASPCA pens compared to those slaughtered in Weinberg casting pens.
Head restraint before inversion in cattle produced less vigorous struggling than head restraint after inversion (Van Oers, 1987). Cattle
restrained in a poorly designed head holder (i.e., where the time
required to drive the animal into the holder exceeded 30 s) had higher
levels of the stress hormone cortisol than those stunned with their
heads free (Ewbank, Parker, & Mason, 1992). For religious slaughter,
the likely changes occurring during inversion were not severe enough
to cause substantial respiratory problems as indicated by blood gas
tensions (Wagner, Muir, & Grospitch, 1990). Despite the merits of
upright restraining pens, Gregory (2005) identied two signicant
shortcomings. Firstly, the throat cut is somewhat difcult since it has
to be made upward instead of downward. Secondly, due to the position
of the slaughterer relative to the cut, he is more likely to be covered with
blood. In addition, poorly constructed ASPCA pens could apply excessive
pressure to the neck and thoracic regions of cattle (Grandin &
Regenstein, 1994). Also, the effectiveness of the restraining systems
depends to a large extent on the calmness and experience of the operator (Grandin & Regenstein, 1994).
In poultry, Lambooij et al. (1999) compared cone restraining and
shackling methods on carcass quality of broiler chickens. The authors
found that the incidence of thigh muscle hemorrhaging was higher in
shackled birds than those restrained in cones. Nonetheless, shackled
birds had slightly greater blood loss and their meat was judged to be
more tender than those from cone-restrained birds, probably due to
the high pH value observed in the meat of cone-restrained birds.
Kannan, Heath, Wabeck, and Mench (1997) also observed that longer
shackling duration elevated corticosterone levels and impaired color
of breast muscle in broiler chickens subjected to ritual slaughter.
To reduce stress in red meat animals, Grandin (2013) and OIE
(2007) recommended that all restraint devices should have the following features: (1) non-slip ooring in the restraint device; (2) pressure

509

controls to avoid excessive pressure; (3) no protrusions or sharp


edges to avoid injuries; (4) smooth and steady movement of restraint
devices; (5) noise control to avoid scaring the animals; and (6) lighting
and shields that guides the animal into the restrainer. All these measures are relevant in terms of meat quality in addition to preserving
the welfare of the animal during slaughter.
3.1.2. Pre-slaughter/post-slaughter stunning
The effects of pre-slaughter stunning on meat quality of large
animals and poultry are summarized in Table 3 and discussed below.
3.1.2.1. Hemorrhages due to pre-slaughter stunning. A number of
problems with meat and carcass quality can be directly attributed to
pre-slaughter stunning (Daly, 2005). Ecchymosis (blood splash) and
speckles are forms of hemorrhages that occur in livestock (Fig. 5). Studies in the 1970s and 1980s involving hundreds of lambs established the
causes of blood splash and the factors affecting the phenomenon.
Hemorrhages can manifest as blood splash or speckles (Gilbert &
Devine, 1982; Leet, Devine, & Gavey, 1997). The former is spots of
blood in muscles and the latter is petechial hemorrhages in fat or connective tissue overlying the muscle. Both may be a consequence of
shearing and rupture of blood vessels resulting from severe muscle
spasm or supercontracture (Gilbert & Devine, 1982; Leet et al.,
1997). Hemorrhages are found in muscle, connective tissue and organs (hearts, lungs, gall bladder, and duodenum) (Kirton, Bishop,
Mullord, & Frazerhurst, 1978). They range in size from microscopic
to several centimeters, which can affect the appearance and acceptability of the meat (Leet et al., 1997).
The effect of stunning methods on the severity of blood splash is in the
order: no stun b percussion b captive bolt b head-to-back electrical
b head-only electrical (Kirton, Frazerhurst, Bishop, & Winn, 1980-81;
Kirton, Frazerhurst, Woods, & Chrystall, 1980-81). Incidence of blood
splash and speckle in electrically stunned lambs increases with stun
duration and current (Devine, Gilbert, & Ellery, 1983).
Incidence of blood splash is reduced with shorter stun-to-stick time,
meaning that the faster the stunned animal was slaughtered the less
the severity of blood splash (Kirton et al., 1978).

Fig. 4. Steps in the modern processing of ducks showing transport, shackling, stunning, slaughtering and bleeding. These steps are similar for most poultry, including chickens.

510

M.M. Farouk et al. / Meat Science 98 (2014) 505519

Table 3
Effect of pre-slaughter stunning used in halal meat production on the defects and quality of meat from halal livestock.
Type of stunning

Species

No pre-slaughter stunning
(NS) compared to electrical
stunning (ES)

Cattle and sheep including


calves and lambs

Head-only ES

Defects/quality issues or improvement

No petechiae, ecchymosis/blood splash, hematomas and


bone fractures in NS carcass and organs compared to ES,
higher heart petechiae in ES than NS; lower pH,
cookloss, drip loss in NS lambs than ES.
Poultry, including broilers, hens, No physical defects associated with NS in poultry. ES
turkeys, ducks
may improve tenderness due to faster rigor attainment
compared to NS.
Rabbits
NS meat had lower pH and was lighter than ES.
Cattle, sheep, deer, goats
Ecchymosis/petechial hemorrhaging/blood splash;
including calves, lambs and goat hematomas; occasional broken bones and attendant
kids
consequences on meat quality.
Ostriches and poultry, including Red wing tips; wing, shoulder, strawberry and breast
broilers, hens, turkeys, ducks
muscle hemorrhages/blood splash, engorged/smearing
of wing and pectoral veins; red feather tract; broken
bones, coracoid, furculum, scapula, and pectoral.

Low (5060 HZ) vs. high


(N600 HZ) frequency ES

Livestock

Percussive stunning (PS)


compared to ES or NS

Cattle, sheep

Lower incidences of blood splash in larger animals and


defects in poultry associated with high-frequency ES
compared to low.
Incidence of brain hemorrhage with PS compared to ES
or NS; blood splash in the order NS b PS b ES.

In an unpublished report Ahmad (2007) questioned whether


violently counteracting muscle contractions during electrical stunning
actually cause localized tearing of the capillary bed that leads to blood
splash. He cited a number of authors and summarized their ndings as
follows:
Hemorrhages can be induced electrically in tissues that have no
skeletal muscle, such as the brain (Hassin, 1933). If this applies
more broadly, it is unlikely that localized striated muscle contraction
is the only cause of vessel rupture.
One of the contributing factors may be arteriolar dilatation (Shaw,
Weidemann, & Baxter, 1971). This was based on the nding that, in
rats, propranolol reduced and phentolamine increased the extent of
blood splash. The effects of these drugs would not necessarily be limited to the arterial side of the circulation, as venous dilatation could
also play a role (Vanhoutte, Verbeuren, & Webb, 1981). Presumably,
it is the engorgement of the capillary bed which encourages rupture
of vessels when placed under pressure.
The blood vessels may be unduly fragile. Histological examination of
blood splash in meat has shown that the vessels that burst are on
the venous side of the capillary bed, which has less elastic walls than
the arterial side, and so are weaker and more prone to damage.
Blood splash is common in animals that have died from anticoagulant
poisoning and these animals have increased capillary fragility (Fulton
& Berman, 1964; Littin, 2004). Lambs in a ock that had a high prevalence of blood splash had poor blood coagulation in terms of
prothrombin time (Restall, 1981), and it was suggested that the common link might be ingestion of excessive amounts of coumarins from
pasture. The raised susceptibility to blood splash in unweaned lambs
might be a low vitamin K status because of their milk-based diet.
During intense generalized muscle body contractions, the venous and
arterial systems experience severe external pressure. Squeezing of
the veins results in large rises in venous pressure, which is transmitted
to the capillary system at sites that can be some distance from the
contractions. The venules in the capillary bed probably burst where
they are weakest, or where venous pressure is particularly high. This
referral of pressure, causing distant petechial hemorrhage, has been
seen in other contexts when sudden intense pressures have been
applied to veins (French & Callender, 1962). Engorgement of the
venous circulation would presumably exaggerate this effect.
Electrical stimulation of tissues, even at low currents, will promote
extravasations of blood cells from the capillary bed, but this is an

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inammatory response and is slower than the time available under


slaughtering conditions (Nanmark, Buch, & Albrektsson, 1985).
Ahmad (2007) concluded by suggesting the need for concerted
scientic effort to understand the real causes of blood splash.
Gilbert (1993) described practical techniques for managing
problems associated with electrical stunning. Blood splash and speckle
bruising can be reduced by using minimum stunning currents, minimum stun-to-stick times and very good stunning techniques, which
principally ensure good electrode contact. Ecchymosis was reported to
be reduced in fallow deer by thoracic stick exsanguination executed
less than 10 s after stunning (Mulley, Felapau, Flesch, & Wiklund, 2010).
3.1.2.2. Red meat animals. Anil, Love, Helps, and Harbour (2002) compared penetrating captive bolt, non-penetrating captive bolt and electrical stunning of cattle and sheep and found that there was a risk of
hematogenous dissemination of central nervous system tissue with
the use of pneumatically or cartridge-operated penetrating captive
bolt but none with electrical stunning. The dissemination of central nervous system tissue poses a threat to public health in relation to possible
slaughter of animals with preclinical bovine spongiform encephalopathy (Anil et al., 2002).
The use of electrical stunning in ruminants can cause bruising, blood
splash, blood speckle, broken bones and pelt damage (Daly, 2005;
Gilbert, 1993; Gregory, 1998). Velarde, Gispert, Diestre, and Manteca
(2003) reported no incidence of hemorrhages, petechiae, ecchymosis,
hematomas and bone fracture in lambs that had been head-only electrically stunned for 3 s at a constant voltage of 250 V. However, the authors
(Velarde et al., 2003) found higher incidence of petechiae in the hearts
of head-only electrically stunned lambs compared to non-stunned
lambs. Grandin (2003) is of the opinion that electrical stunning is less
problematic when used on grass-fed cattle compared to feedlot cattle;
she gave an example of the success of electrical stunning in New
Zealand and the problem of blood splash and meat damage when
used in Australia on feedlot cattle.
Electrically stunned lambs have been reported to have approximately 20 times the noradrenaline and 14 times the adrenaline level of nonstunned lambs (Pearson, Kilgour, de Langen, & Payne, 1977). This was
recently conrmed for other pre-slaughter stunning methods but not
in penetrative percussive stunning after slaughter (Zulkii et al.,
2014). These stress markers are evidence that stunning, whether electrical or mechanical, affects the animal. Sazili et al. (2013) compared

M.M. Farouk et al. / Meat Science 98 (2014) 505519

511

Fig. 5. Examples of blood splashes in different bovine muscles of varying levels of severity. Blood splash represents poor aesthetic quality.

the effects of four slaughtering methods on the quality of bovine m.


longissimus and m. semitendinosus. The methods were high power
non-penetrative percussive stunning prior to slaughter (HPNP); low
power non-penetrative percussive stunning prior to slaughter (LPNP);
penetrative percussive stunning prior to slaughter and penetrative percussive stunning after slaughter. The authors found HPNP stunning had
negative effect on WHC and color values and resulted in higher lipid
oxidation and shear force values compared with the rest of treatments
in m. semitendinosus but not m. longissimus. nenc and Kaya (2004)
found no difference in WHC in beef from stunned and non-stunned
animals, but the cooking loss was higher in beef from electrically
stunned animals. The authors reported the non-stunned beef to
be more tender but beef from stunned animals had better color.
Agbeniga, Webb, and O'Neil (2013) compared the meat quality of
post-cut captive bolt stunned and kosher slaughtered feedlot cattle to
that of pre-slaughtered captive bolt conventionally slaughtered equivalent animals and found that the meat from the shechita slaughtered
animals was more tender and had less cook loss compared to its conventionally slaughtered equivalents.
3.1.2.3. Poultry. The two major types of stunning used in birds are gas
and electrical stunning. However, electrical stunning is the most universally acceptable (McKeegan et al., 2007) and the most commonly practiced stunning method in halal poultry slaughtering requiring high
throughput rates (Che Man & Sazili, 2010). The ability of the electrical
stunning to rapidly immobilize birds, lessen slaughter-related struggle
and enhance bleeding efciency substantiate its use in the poultry industry. Electrical stunning is also relatively cheap, convenient and safe
(Farouk, 2013; Fletcher, 1993). Nonetheless, in spite of its improved
methodology and widespread use, electrical stunning has been implicated in poor meat quality due to low bleeding efciency, occurrence
of blood blisters, and tougher meat if the time is insufcient for rigor
mortis to develop prior to lleting (Summers, 2006).
Electrical stunning of birds is typically carried out in an electrically
charged water bath by moving the head of the birds across water containing a submerged electrode. Conscious birds are hung upside down
on a moving metal shackle line and passed through the electried
water bath in such a way that the current ows through the entire
body toward the shackle (Che Man & Sazili, 2010). However, shackling
of conscious birds to overhead line has been implicated in considerable

product damage, arduous working conditions and poor animal welfare


(Abeyesinghe et al., 2007).
In order to correct these anomalies, improvements are being made
in mechanical design and the electrical parameters of voltage, amperage
and frequency (Fernndez-Lpez, Sendra-Nadal, & Sayas-Barber,
2010). For an effective stun, the parameters must cause loss of sensibility and consciousness but not carcass damage or death of the birds in
compliance with halal requirements (Che Man & Sazili, 2010;
Nakyinsige, Che Man et al., 2013). For instance, the use of high voltage
and current in the water bath has been criticized for producing muscular contraction that negatively imparts meat quality (Mouchoniere,
Pottier & Fernandez, 1999; Wilkins, Gregory, Wotton, & Parkman,
1998). These contractions may cause red wing tips which result in
losses in yield and saleable product since they are often trimmed during
nal inspection of carcasses (McNeal, Fletcher, & Buhr, 2003). High
voltage may also induce heart brillation, causing inefcient bleeding,
increased hemorrhaging, and even death before exsanguination
(Fernndez-Lpez et al., 2010; Gregory & Wilkins, 1989). High current
increased the incidence of dislocation, broken bones, red wing tips
and hemorrhaging of wing veins and of deep breast muscle in broilers
(Ali, Lawson, Tauson, Jensen, & Chwalibog, 2007; Mota-Rojas et al.,
2008). Similarly, Fernandez, Leprettre, Dubois, Auvergne, and Babile
(2003) appraised the inuence of different currents (30, 50 or 70 mA)
on quality defects of carcass in geese. The authors observed increased
incidence of carcass downgrading with increasing amperage. This
corroborates the ndings of Hindle, Lambooij, Reimert, Workel, and
Gerritzen (2010) which showed that increased amperage and voltage
decreased carcass quality in duck, hen and broilers. Contrarily,
Papinaho and Fletcher (1995) observed that low-voltage electrical stunning does not affect total blood loss after the 90 to 120 s exsanguination
period despite lower early blood loss.
Frequency (hertz) of the alternating current also affects stunning effectiveness and meat quality in birds. Details of this are described in
Section 4.2.
3.2. Slaughter of red meat animals and poultry
The aim of efcient and humane slaughtering is to remove the blood
as quickly as possible and stop the delivery of oxygen to the brain
(Gregory, 2007). From the Judeo-Islamic perspective, in addition to

512

M.M. Farouk et al. / Meat Science 98 (2014) 505519

killing the animal through the loss of blood, the removal of owing
blood is necessary because it is considered an impurity that should not
be consumed.
The halal and kosher requirements for slaughtering in red meat production have been discussed earlier (Farouk, 2013). In poultry, the act of
slaughtering begins with the incision on the neck at a point just below
the glottis (Che Man & Sazili, 2010). Throat cutting in halal and kosher
is done to severe the trachea, esophagus and the two carotid arteries
and jugular veins without head decapitation during the process (Che
Man & Sazili, 2010; Farouk, 2013; Lpez et al., 2008).
Ritual slaughtering has been reported to produce meat with high pH
after extended storage time (D'Agata, Russo, & Preziuso, 2009;
Zuckerman & Mannheim, 2001). In contrast, Holzer, Berry, Campbell,
Spanier, and Solomon (2004) reported lower pH in kosher meat compared to non-kosher.
Although the halal and kosher status of meat is usually sufcient to
determine the purchasing decision of observant Muslims and Jews
(Ahmed, 2008; Chowdhury, Helman & Greenhalgh, 2000), halal and kosher meats are increasingly perceived as wholesome and healthy
(Cohen, Schwartz, Antonovski, & Saguy, 2002; Hanzaee & Ramezani,
2011; Nakyinsige, Che Man, & Sazili, 2012). The main reason for this
perception appears to be linked to the perceived greater blood loss
during halal slaughtering and the koshering process post-slaughter
(described in Section 3.3.2). This general perception of higher blood
loss during halal and kosher slaughtering have been challenged by the
studies that found no difference in total blood loss in sheep and cattle
slaughtered with or without (halal/kosher) stunning (Agbeniga &
Webb, 2012; Anil et al., 2004, 2006; Chrystall, Devine, & Newton,
1981). Some studies even found higher blood loss due to stunning in
lambs (Hopkins, Shaw, Baud, & Walker, 2006; Velarde et al., 2003). On
the other hand, Nakyinsige et al. (2014) found higher blood loss in
New Zealand white rabbits halal-slaughtered without stunning
compared to gas stun-killed animals. This higher blood loss in nonstunned animals was conrmed by lower hemoglobin content in m.
longissimus lumborum from this treatment group. These conicting
results may suggest species-effect for the slaughtering methods.
Heme iron, rather than inorganic iron, was shown to be the responsible compound causing the formation of the carcinogenic N-nitroso
compounds (Cross, Pollock, & Bingham, 2003). A study by Pierre,
Freeman, Tach, Van der Meer, and Corpet (2004) used several diets
containing inorganic iron (control), chicken (low heme content), beef
(medium concentration heme content), blood sausage (high heme
content) and hemoglobin (equivalent to beef diet) to examine the
formation of aberrant crypt foci and mucin-depleted foci, markers for
colon carcinogenesis, in rats with low calcium diet. All diets containing
heme promoted mucin-depleted foci and the highest putative precancerous lesions per rat colon was the highest in blood sausage.
Alvarado, Richards, O'Keefe, and Wang (2007) examined the following
ve slaughter techniques to determine their effects on pH, color, lipid
oxidation and residual hemoglobin concentration in broiler breast llets: 1) CO2 slaughter and not bled, 2) no stunning and bled, 3) electrical
stunning (ES) and bled, 4) CO2 stunning and bled, and 5) ES and decapitation. The authors (Alvarado et al., 2007) found that the llets from the
CO2 slaughter and not bled birds were redder and had higher residual
amount of hemoglobin compared to the other treatments; and that
lipid oxidation was signicantly lower in ES and bled birds compared
to others.
3.2.1. Red meat animals
Although it is recommended that the two jugular veins, carotid arteries, trachea and esophagus be severed during halal slaughtering,
opinions among Islamic scholars differ as to the minimum parts to be
cut for the animal to be Halal (Al-Qaradawi, 1960). However all agree
that the neck is where the cutting should take place, and that the
blood has to gush forth. Properly severing all the arteries and veins hastens the death of the animal. Prolonged death does not necessarily

render the meat non-Halal, but prolonged suffering is not acceptable.


Devine, Tavener, Gilbert, and Day (1986) reported a case in which a
stunned calf bled poorly because only a single carotid artery was severed, with this animal the electroencephalogram remained at a high
level and fell only slowly indicating a possibility of prolonged suffering.
Gregory and Wotton (1984) found that severing both carotid arteries
plus jugular veins in sheep induced a loss of brain responsiveness
(ash-evoked responsiveness in the electrocorticogram) in 14 s, whereas severing only one carotid artery plus one jugular vein took 70 s.
When only the jugular veins were cut, the time to loss of evoked responsiveness was approximately 5 min. Newhook and Blackmore (1982)
found that in one sheep that was slaughtered by severance of the carotid
artery and jugular vein on one side of the neck only, the onset of insensibility, as determined from the study of electroencephalograms, was
delayed for 29 s.
3.2.2. Poultry
Industrial halal poultry slaughtering can be achieved via manual
(hand) slaughter or a mechanical device, depending on available facilities and size of operation (Che Man & Sazili, 2010). Manual slaughter is
preferable and is mostly used in slaughter plants controlled by Muslims.
In large-scale production where halal is not the focus, production
efciency dictates mechanical slaughtering. These machines are
designed to cut the throat and esophagus and sever the jugular veins
and carotid arteries (Gregory & Wilkins, 1989). However birds can be
mis-slaughtered (other parts of the body are cut instead) or missed
(not slaughtered) by the machine. The requirements for halal poultry
slaughtering using manual or mechanical method have been summarized by Che Man and Sazili (2010).
In birds, Davis (1996) reported that head decapitation increases
time of death as it disrupts the nervous system causing asphyxia and
suffocation while separation of the jugular vein and carotid arteries
without head decapitation shortens the time of death. Zaman, Nassir,
Abdurrazq, Salleh, and Rahman (2012) investigated variation of total
protein prole in chicken skeletal muscle as inuenced by two methods
of slaughtering using a sharp knife. In the rst treatment, the neck was
partially cut leaving the spinal cord intact and body was released immediately after slaughtering while in the second treatment, the neck was
completely cut off and body was tied until the animal died. Using 2-D
gel electrophoresis the authors found a protein near pH 5.0 and MW
116 kDa that was present in skeletal muscle from the second treatment
only.
Mast and Macneil (1983) compared the quality attributes and meat
yield of broiler chickens processed in commercial plants using either
conventional or kosher procedures. Conventionally processed chicken
had higher water uptake during immersion chilling and lost more
weight during storage. Breast meat from kosher chicken was more tender than conventional breast meat as evaluated by sensory techniques
and shear test. Albeit the differences were not statistically signicant,
kosher samples consistently had lower microbial counts and slightly
higher thiobarbituric acid (perioxide) values than its conventional
counterpart. Lpez et al. (2008) assessed the welfare, bleeding efciency and meat quality in rabbits subjected to either halal slaughter without stunning or electrically stunned prior to slaughtering; the authors
found that halal slaughtered rabbits had higher blood loss and lower
pH values in longissimus dorsi and biceps femoris muscles. Similarly,
Nakyinsige, Sazili et al. (2013) did not observe signicant difference in
meat quality of rabbits slaughtered through the halal procedure or gas
stunning before slaughtering.
3.3. Post-slaughter processes
3.3.1. Electro-immobilization and thoracic stick
Electro-immobilization and thoracic sticking are common postslaughter processes associated with the electrical head-only preslaughter stunning of livestock. The procedures have been described

M.M. Farouk et al. / Meat Science 98 (2014) 505519

thoroughly by Farouk (2013). The post-mortem fall in pH is faster in


muscles from electro-immobilized carcasses (Daly, 2005). The benets
of this effect are discussed in Section 3.4. Thoracic stick aids the
complete bleeding of slaughtered cattle and consequently reduces the
negative effects of residual blood in meat (refer to Section 3.3).
3.3.2. Koshering
Koshering is an important post-shechita procedure in the production of kosher meat. It is undertaken to purge meat of all remaining
blood following slaughter. This is because blood, including all the
removable residual blood in the meat is not permitted to those who
consume kosher meat for religious reasons (Regenstein, Chaudry, &
Regenstein, 2003). This process has tremendous effects on the meat
quality (Table 4). Koshering also removes some myoglobin and other
sarcoplasmic proteins (Asghar, Torres, Gray, & Pearson, 1990) due to
the use of water for Shriah (soaking in cold water for 30 min) and extensive use of salt for Hadacha (salting the surface using kosher coarse salt
for approximately 1 h) (Regenstein & Regenstein, 1988). The removal of
myoglobin will have several consequences on the color, avor and the
overall product quality, but the most important effect from health
point view is its impact on the oxidative processes. Hemoglobin and
myoglobin contain iron atoms in their porphyrin rings and this iron
can change in oxidation state during reactions with other molecules.
The lowest iron oxidation state is the ferrous form (Fe2+) with water
bound to the iron nucleus in the case of deoxymoglobin or oxygen
bound to the iron in the case of oxymyoglobin. There is also
metmyoglobin (Fe3 +), ferrylmyoglobin (Fe4 +), and the short-lived
perferryl radical that can exist at different stages of oxidation. Myoglobin contains iron in variable valances and may act as either an antioxidant (Alayash, Patel, & Cashon, 2001; Lapidot, Granit, & Kanner, 2005)
or pro-oxidant (Baron, Skibsted, & Andersen, 1997; Lapidot et al.,
2005) depending on the presence of reducing compounds at certain
concentrations. Lipid hydroperoxides are generated during lipid peroxidation and the presence of myoglobin catalyzes the breakdown of lipid
hydroperoxides (Baron et al., 1997; McClements & Decker, 2008).
Several mechanisms have been proposed for myoglobin-induced
lipid oxidation (for more information see Bekhit, Hopkins, Fahri, &
Ponnampalam, 2013; Carlsen, Moller, & Skibsted, 2005).
Myobrillar proteins are also soluble in water (Ito, Tatsumi,
Wakamatsu, Nishimura, & Akihito Hattori, 2003) and in salt solutions
(Stanley, Stone, & Hultin, 1994) and therefore some myobrillar proteins are expected to be solubilized but there are no published reports
to document this assertion. The protein loss from sarcoplasmic and
myobrillar fraction maybe signicant from nutritional point of view
but it may be balanced by changes in moisture (Hajmmer, Marsden,
Crozier-Dodson, Basheer, & Higgins, 1999). The extent of protein losses
due to koshering is unknown and is worthy to be included in future
investigations.

513

The reduction in heme proteins affects the color of the nal product.
Kosher meats have been reported to have low color intensity (Holzer
et al., 2004; Torres, Pearson, Gray, Booren, & Shimokomaki, 1988;
Zuckerman & Mannheim, 2001). The use of large amounts of salt causes
low color stability and accelerates the discoloration of meat (Torres
et al., 1988; Zuckerman & Mannheim, 2001) which can be alleviated
by the use of antioxidants such as erythorbate or sodium ascorbate
(Zuckerman & Mannheim, 2001) or the use of hydrodynamic pressure
(Holzer et al., 2004).
An important nutritional quality factor in kosher meat compared to
conventionally slaughtered meat is the high salt content. Mast and
Macneil (1983) found the sodium content in meat and skin of kosher
chicken to be 4- to 6-fold greater than non-kosher chicken (Mast &
Macneil, 1983; Powers & Mast, 1980) and beef (Zuckerman &
Mannheim, 2001). This high salt content was found to persist in the
meat and was not affected by rinsing and cooking (Angel, Weinberg, &
Jaffe, 1989). Salt is a catalyst for lipid oxidation (Kanner, Harel, & Jaffe,
1991), and kosher meat may develop objectionable odor during postmortem refrigeration (Holzer et al., 2004).
The koshering process was reported to reduce the levels of
Escherichia coli and Salmonella spp. due to its preservative actions such
as altering the water activity and ionic strength of meat (Hajmmer
et al., 1999) and reducing attachment of Salmonella to chicken surface
(Oscar, 2008).
3.4. Accelerated post-mortem pH fall due to combined electrical inputs from
stunning and immobilization
Daly (2005) observed that among some of the carcass quality problems associated with electrical stunning and immobilization is that of
accelerated pH decline due to the violent forces produced by muscle
contraction caused by the stun. The meat quality effects of high temperature and low pH have been thoroughly reviewed (Jacob & Hopkins,
2014; Kim, Warner, & Rosenvold, 2014).
According to Simmons et al. (2008), the combined electrical input
from stunning and immobilization can drive muscle glycolysis faster
resulting in the muscles attaining rigor at higher temperature leading
to a denaturing condition and a number of meat quality problems
summarised in Table 5. Simmons et al. (2008) electrically stunned and
immobilized 40 steers using low or high frequency and found that the
use of low-frequency immobilization drove the pH down faster resulting
in higher drip loss and shear force compared to high-frequency immobilization. Warner, Dunshea, Gutzke, Lau, and Kearney (2014) determined
the incidence of high rigor temperature in 1512 beef carcasses across
Australia and found very high occurrence of the phenomenon (up to
94%) from meat plants that apply various electrical inputs during processing including post-slaughter electrical immobilization of carcasses.
The electrical stunning of poultry reduced initial pH values (Papinaho

Table 4
Some positive (+) and negative () aspects of halal and kosher post-slaughter processes on meat quality.
Process

Nutritional and quality aspects

Koshering

Removal of haem/blood (+); higher discoloration (); lower color parameters (L*, a* and b*
values) ()
Removal of proteins ()
High salt content ()

Halal slaughtering

Reference

Torres et al. (1988); Zuckerman and Mannheim (2001);


Holzer et al. (2004)
Asghar et al. (1990)
Powers and Mast (1980); Zuckerman and Mannheim
(2001); Mast and Macneil (1983); Angel et al. (1989)
High lipid oxidation ()
Powers and Mast (1980); Torres et al. (1988)
Low microbial count (+)
Powers and Mast (1980); Hajmmer et al. (1999);
Zuckerman and Mannheim (2001); Holzer et al. (2004)
No effect on removal of haem/blood in sheep and cattle but signicant effect in rabbits
Anil et al. (2004, 2006); Nakyinsige et al. (2014)
Lower drip loss (+); no effect on color parameters (L*, a* and b*) or oxymyoglobin % over 6 days of D'Agata et al. (2009)
display
60% higher dye uptake by ultrasound in halal chicken
Leal-Ramos et al. (2011)
Lower lipid oxidation in beef semitendinosus and NZ white rabbit Longissimus lumborum (+); lower Sazili et al. (2013); Nakyinsige et al. (2014)
Pseudomonas aeruginosa and Escherichia coli but total count not different in rabbit (+)

514

Table 5
Effect of combined electrical inputs during stunning and immobilization on meat pH and the associated consequences on meat quality.
Livestock

Stunning method

General for all livestock

Increased electrical inputs into carcases due to


electrical stunning and immobilization

Poultry

Reference

Accelerated post-mortem glycolysis and pH decline while muscle temperature reOffer (1991); Farouk and Swan (1998); Farouk and Lovatt (2000); Daly
mains high. Effects include color shelf-life; water holding and fat binding capacities, (2005); Bekhit, Farouk, Cassidy, and Gilbert (2007); Lombart et al.
protein solubility/extractability, meat toughness, ageing potential.
(2008); Simmons et al. (2008); Kim, Kerr et al. (2014); Kim, Warner
et al. (2014); Warner et al. (2014).
Whole-body electrical
Air pressure stunning resulted in rate of pH decline and hemorrhage scores in Lambooij et al. (1999).
stunning (10 s, 110 mA, 300 Hz) in a water bath
breast (48.5%) and thigh meat (43.8%).
compared to air pressure stunning (0.5 s, 2 atm)
Redder meat was found with air pressure stunning.
Electrical whole-body and head-only stunning with
No differences in ultimate pH were found.
Hillebrand et al. (1996).
different voltages (25 vs. 100 V) and frequencies (50 Head-only stunning resulted in darker and redder breast muscles compared with
vs. 200 Hz), and mechanical captive bolt stunning
whole-body stunning.
Head-only and captive bolt stunning resulted in less hemorrhages in breast
compared with whole-body stunning.
Whole body, head only, captive bolt, and gas stunning 14%, 44.9%, 56.1% and 53.4% reduction in hemorrhage score due to the use of head Savenije et al. 2002).
only (100 V, 50 Hz, 4 s), captive bolt, CO2 and argon, respectively compared to bath
(CO2 and argon)
electrical stunning (100 V, 50Hz, 4 s).
Higher water holding capacity in head only stunning compared to other treatments.
Gas stunning decreased the redness and increased the lightness of the meat.
Stunning method did not have an effect on tenderness.
Head only electrical stunning (125 V for 10 s).
Stunning did not affect pH, color L*, a*, b* values, water holding capacity (WHC) and Vergara and Gallego (2000).
shear force (SF).
Industrial stunning
Authors' concluded Even low electrical input during immobilization can adeGeesink et al. (2001).
quately stimulate carcasses and avoid cold shortening.
Head stunning (250 V, 50 Hz sinusoidal A.C., for 3 s) Color (L, a, b), muscle ultimate pH (pHu), chilling losses and carcass weight at
Velarde et al. (2003).
45 min and 24 h were not signicantly different between treatments.
The amount of blood lost relative to live body weight and the killing-out were
signicantly higher in electrically stunned lambs compared with non-stunned
lambs.
Vergara et al. (2005).
Head electrical stunning (ESL; 110 V, 50 Hz for 5 s), The highest pH was found in the USL group whereas the lowest pH decline was
found in GSL group.
CO2 gas stunning (GSL), no stunning (USL)
No effect on water holding capacity; cooking loss and color parameters.
After 7 days meat from stunned animals had lower drip loss.
GSL had more tender meat (lower SF value) than ESL and USL
(P b 0.05).
No blood splash in any of the carcasses of the GSL group.

M.M. Farouk et al. / Meat Science 98 (2014) 505519

Lamb

Outcome

M.M. Farouk et al. / Meat Science 98 (2014) 505519

& Fletcher, 1995) and improved tenderness (Kettlewell & Hallworth,


1990) when compared to un-stunned control.
Papinaho and Fletcher (1996) studied the effects of stunning amperage on early rigor development and breast meat quality of broilers. The
birds were assigned to three stunning treatments; 0 (no stun), 50, and
125 mA. Results showed that stunning at 50 or 125 mA caused a significantly higher pH values up to 6 h post-mortem; cooking loss was
not inuenced by stunning treatment but stunning at 125 mA produced
signicantly tougher meat up to 10 h post-mortem than meat from unstunned birds or birds stunned at 50 mA. However, the effects of electrical stunning on early rigor development disappeared at by 46 h postmortem.
4. Pre- and post-slaughter processes and technologies to improve
halal and kosher meat quality
4.1. Slaughter cut position
Gregory, Schuster et al. (2012) assessed the time to onset of arrested
blood ow and the size of false aneurysms in the severed carotid arteries of 126 cattle during halal slaughter without stunning and found that
29% showed early arrest of blood ow and in 6%, both the left and right
carotid arteries in the same animal were affected. Making the cut in the
neck at the rst cervical vertebra instead of the second to fourth cervical
vertebrae reduced the frequency of the false aneurysm formation and
the early arrested blood ow improving bleeding efciency.
Therefore, in order to better meet the halal and kosher requirements
for proper and complete bleeding of slaughtered animals for the highest
meat spiritual quality, the slaughter position on the neck recommended by Gregory, Schuster et al. (2012); Gregory, von Wenlawowicz et al.
(2012) should be considered for adoption in the halal and kosher industrial meat production, once it is conrmed that the suggested position is
not in contravention of the halal and kosher religious requirements.
4.2. High-frequency stunning
A development in the use of high-frequency electrical currents
(HSFT) to stun and immobilize red meat animals pre-slaughter was
described by Simons et al. (2006). The HFST uses similar voltage and
amperes settings as the Jarvis traditional head-only electrical stunning
but uses higher frequencies (10002000 Hz) with a square rather
than sinusoidal waveform. The settings used in the traditional system
when applied to full animal body will stop the heart but the modied
system at higher frequency does not and thus can be applied from either
head to leg, head to belly or head-to-back instead of head-only in use in
the traditional system (Farouk, 2013).
The ability of high-frequency electrical stunning not to cause cardiac
arrest makes it acceptable in halal slaughter by some adherents of
Islamic faith (Farouk, 2013). In addition, high-frequency stunning has
been shown to enhance bleeding efciency and meat quality and reduce
carcass damage (Gregory, 2005; Simons et al., 2006).
The physiological basis for stunning using high-frequency waveforms was discussed by Daly (2005). High-frequency currents ow
close to the surface of a conductor hence may produce a less severe
muscular spasm at the beginning of the current ow (Gregory,
Wilkins, & Wotton, 1991). Passing a high-frequency waveform through
the body of an animal can create the spinal inhibition of the seizure
movement without ventricular brillation. Animals subjected to highfrequency stunning are less likely to suffer muscle contraction, muscle
hemorrhages and broken bones (Hillebrand, Lambooy, & Veerkamp,
1996; McNeal et al., 2003; Simons et al., 2006). In bids the major commercial importance of high-frequency electrical stunning is reduction
in the incidence of carcass hemorrhages and blood spots (Gregory,
2005) and lower blood retention in the visceral which could increase
the yield of trimmed livers for foie gras production (Turcsn et al.,
2003). Frequencies N600 Hz fail to create ventricular brillation keeping

515

head-to-leg pathway normal but minimized seizures (Gregory et al.,


1991). It was observed that a frequency of 300 Hz caused cardiac arrest
in 57% of turkeys while none of the birds had cardiac arrest at 600 Hz
(Mouchoniere, Pottier, & Fernandez, 1999). Also, Wilkins and Wotton
(2002) observed increased carcass quality in turkeys manifested by reduced engorged wing and pectoral veins, and wing hemorrhages when
birds were subjected to high-frequency (1400 Hz) stunning. Prinz
(2009) reviewed a number of studies relating to carcass characteristics
and meat quality assessment of poultry subjected to electrical waterbath stunning at high frequencies and concluded that a signicantly
lower occurrence of broken bones and breast meat hemorrhages was
observed in broilers stunned with a sine wave AC of 1500 Hz compared
to 50 Hz. The ndings of Fernandez et al. (2003) showed that petechial
hemorrhages in the breast muscle were absent in non-stunned geese
and those stunned at high frequency (1200 Hz) compared to low frequency (50 Hz) where 55% of geese showed the defect.
Bleeding efciency was higher and the incidence of cardiac arrest
was lower with high-frequency stunning (Mouchoniere et al., 1999).
Similarly, Contreras and Beraquet (2001) reported higher blood loss
when birds were subjected to frequency of 1000 Hz compared to
those subjected to lower frequencies.
Xu et al. (2011) reported a signicantly lower shear force and
cooking loss in broiler chickens subjected to high-frequency (400 and
1000 Hz) electrical stunning compared to low frequency (160 Hz).
The authors attributed the lower tenderness of birds subjected to
160 Hz to higher concentration of glycogen observed in the birds. Similarly, Choe et al. (2008) indicated a reduced glycogen concentration following a stun with high frequencies (400 and 1000 Hz) which resulted
in reduced drip loss and meat paleness.
4.3. Controlled/modied and low atmosphere pressure stunning
In modied atmosphere stunning (MAS) livestock are exposed to
carbon dioxide (CO2) in pits, tunnels, containers or sealed buildings,
sometimes in two phases where livestock are successively exposed to
a gas mixture containing up to 40% CO2 by volume in air, followed by
a higher concentration of CO2 after the animals have lost consciousness.
Alternatively the CO2 is mixed with inert gases such as argon, nitrogen
or helium to promote anoxia, or inert gases are used exclusively (EFSA
AHAW, 2013). Low atmospheric pressure stunning is a method of
stunning that renders livestock unconscious by gradually reducing the
oxygen tension in the atmosphere to achieve progressive hypoxia
(EFSA AHAW, 2013). The exposure of livestock to gas mixtures or low
atmospheric pressure causes loss of consciousness and sensibility due
to the inhibition of brain function. MAS methods are widely used for
stunning pigs and poultry.
The issues associated with the use of MAS in poultry were recently
reviewed (Joseph et al., 2013; Raj, 2006). There is not enough work
done on the use of MAS in the reversible stunning of livestock for
halal and kosher meat production to enable the full assessment of the
potential of the methods as alternative to the reversible electrical and
mechanical methods currently in use.
4.4. Whole carcass blood rinsing technology
A Rinse & Chill technology (MPSC Inc., St. Paul, Minnesota, USA)
involves the infusion of a chilled solution of sugars and salts through
the vascular system of cattle and sheep carcasses during slaughter. It
reduces the amount of residual blood in meat (Farouk, Price, Salih, &
Burnett, 1992; Feirtag & Pullen, 2003). This may aid the process of
koshering and potentially could reduce the amount of surface salting
required during the koshering process and the attendant consequences
of the salt on meat quality.
The removal of residual blood from carcasses resulted in lighter colored meat compared to controls (Farouk & Price, 1994; Hunt et al.,
2003; Yancey, Hunt, Dikeman, Addis, & Katsanidis, 2001). The

516

M.M. Farouk et al. / Meat Science 98 (2014) 505519

technology has also been shown to signicantly reduce the number of


microorganisms, particularly coliforms and generic E. coli on cattle carcasses. The efcacy of the system in improving the microbial contamination of cattle carcasses was investigated and it was found that the
system reduced aerobic microorganisms on rinsed carcasses by 40%; coliforms by 68% to 99%, and generic E. coli by 84% compared to controls
(Feirtag & Pullen, 2003).
4.5. Other technologies
Farouk (2013) described alternative non-invasive pre-slaughter
stunning technologies for livestock with the potential to minimize
meat quality problems. For example microwave energy may reduce the
muscle spasm associated with mechanical and electrical methods
(Small, McLean, Keates, Owen, & Ralph, 2013). Robins, Pleiter, Latter,
and Phillips (2014) developed a new system of reversible electrical stunning using a single pulse of ultra-high current (5000 V, 70 A, 50 msec)
that eliminated post-stun grand mal seizures and its associated negative
consequences on meat quality such as ecchymosis. However, these
technologies need to be validated and optimized before they can be
implemented for industrial meat production.
5. Conclusions
A substantial quantity of meat is produced around the world using
halal and kosher slaughter methods and associated processes. Therefore, it is important that the quality of that meat is given due attention.
The conventionally dened attributes of meat quality are demanded by
halal, kosher and conventional consumers alike. However, an additional
attribute of spiritual quality is paramount for those who consume
halal and kosher for religious reasons. A number of meat quality problems including different forms of hemorrhages in the muscles and organs of livestock; carcass damage; broken bones; poor color stability;
reduced ageing potential; increased drip loss, etcetera are associated
with the use of pre-slaughter stunning and accompanying practices.
These issues are rarely encountered in carcasses of non-stunned
animals. Although slaughter without pre-stunning is used in halal and
kosher meat production and the practice minimizes meat quality issues,
nonetheless, it has the potential to compromise animal welfare at
slaughter if not carefully and conscientiously applied. The practice has
pitched the proponents and opponents of stunning into a dogmatic
argument that is surreptitiously turning into a human versus animal
rights and/or religion versus science public debate. This detracts from
the main issue of the ethical, sustainable and humane production of
wholesome meat for its tumultuous lovers around the globe. This review called on both sides of the stunning debate to resort to dialogue,
if meat of high spiritual and conventional quality is to be produced
and the welfare of the animal at slaughter is to be consistently
protected.
Acknowledgments
The principal author acknowledges the support provided through
AgResearch MBIE core funding contract no. A19113 that enabled this
review to be realized, and Drs Scott O. Knowles and Cameron Craigie
of AgResearch for reviewing the manuscript.
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