Halal and Khoser Slauhgter Methods and Meat Quality_a Review

Meat Science 98 (2014) 505–519

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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 Scientific 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

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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. Definitions 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: [email protected] (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 definitions when grading carcasses and cuts for quality, but consumers' perception of meat quality is wide and subjective. It reflects 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, & Brunsø, 2004; Joo & Kim, 2011; Troy & Kerry, 2010). Tenderness, juiciness and flavor are important considerations at the dining table, in contrast to meat protein solubility and the

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M.M. Farouk et al. / Meat Science 98 (2014) 505–519

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), influence 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 definitions 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 influence 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 quality—one 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 specifically for man's benefit (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 sacrificed 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 flesh 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 first 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 fulfilled 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 scientific 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.


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 scientific wisdom by those who think that the animal must first be stunned in order to avoid compromising its welfare. These groups advocate for food labeling that identifies 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 finding 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 conflict 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 conflict-perpetuating tendencies of both religious fundamentalism and its scientific counterpart, reductionist ‘scientism’. Such tendencies are unhealthy for both science and religion.” For this debate to become a dialogue, some significant differences in cognitive orientation and epistemology must be overcome. Proponents of conventional pre-slaughter stunning need to consider whether: • true knowledge includes not only scientific 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

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properly, the welfare of the slaughtered animal is not compromised, even if this cannot be verified scientifically 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 horrific slaughter practices (Gregory, Schuster et al., 2012; Gregory, von Wenlawowicz et al., 2012); • scientific 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 practices—The 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

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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.


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) identified two significant shortcomings. Firstly, the throat cut is somewhat difficult 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 flooring in the restraint device; (2) pressure

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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).

2

1

3

6

5

4

4

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.

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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 (50–60 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 findings 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 finding 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 flock 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

References Kirton, Frazerhurst, Bishop et al. (1980-81); Velarde et al. (2003); Linares et al. (2007);

Kettlewell and Hallworth (1990); Papinaho and Fletcher (1996); Mast and Macneil (1983); Fernandez et al. (2003). López et al. (2008); Nakyinsige et al. (2014) Kirton, Frazerhurst, Bishop et al. (1980-81); Kirton, Frazerhurst, Woods et al. (1980-81); Gilbert and Devine (1982); Gregory (1998); Mulley et al. (2010); Berg et al. (2012). Gregory and Wilkins (1989); Raj et al. (1998); Wilkins et al. (1999); Wilkins and Wotton (2002); Turcsán et al. (2003); Ali et al. (2007); Fernandez et al. (2010); Hindle et al. (2010); Lines et al. (2011); Lambooij et al. (1999, 2014). Gregory et al. (1991); Mouchoniere et al. (1999); Fernandez et al. (2003). Kirton, Frazerhurst, Woods et al. (1980-81); Önenc & Kaya (2004); Sazili et al. (2013).

inflammatory response and is slower than the time available under slaughtering conditions (Nanmark, Buch, & Albrektsson, 1985). Ahmad (2007) concluded by suggesting the need for concerted scientific 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 confirmed for other pre-slaughter stunning methods but not in penetrative percussive stunning after slaughter (Zulkifli et al., 2014). These stress markers are evidence that stunning, whether electrical or mechanical, affects the animal. Sazili et al. (2013) compared


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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. Önenc 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 efficiency 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 efficiency, occurrence of blood blisters, and tougher meat if the time is insufficient for rigor mortis to develop prior to filleting (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 electrified water bath in such a way that the current flows 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 (Fernández-López, Sendra-Nadal, & Sayas-Barberá, 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 final inspection of carcasses (McNeal, Fletcher, & Buhr, 2003). High voltage may also induce heart fibrillation, causing inefficient bleeding, increased hemorrhaging, and even death before exsanguination (Fernández-López 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 influence 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 findings 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 efficient 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

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killing the animal through the loss of blood, the removal of flowing 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; López 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 sufficient 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 confirmed by lower hemoglobin content in m. longissimus lumborum from this treatment group. These conflicting 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, Taché, 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 five slaughter techniques to determine their effects on pH, color, lipid oxidation and residual hemoglobin concentration in broiler breast fillets: 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 fillets 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 significantly 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 (flash-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 efficiency 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 profile in chicken skeletal muscle as influenced by two methods of slaughtering using a sharp knife. In the first 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 significant, kosher samples consistently had lower microbial counts and slightly higher thiobarbituric acid (perioxide) values than its conventional counterpart. López et al. (2008) assessed the welfare, bleeding efficiency 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 significant 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


thoroughly by Farouk (2013). The post-mortem fall in pH is faster in muscles from electro-immobilized carcasses (Daly, 2005). The benefits 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, flavor 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). Myofibrillar proteins are also soluble in water (Ito, Tatsumi, Wakamatsu, Nishimura, & Akihito Hattori, 2003) and in salt solutions (Stanley, Stone, & Hultin, 1994) and therefore some myofibrillar proteins are expected to be solubilized but there are no published reports to document this assertion. The protein loss from sarcoplasmic and myofibrillar fraction maybe significant 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.

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The reduction in heme proteins affects the color of the final 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 significant 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 (+)

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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 significantly different between treatments. • The amount of blood lost relative to live body weight and the killing-out were significantly 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.


Lamb

Outcome


& 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 influenced by stunning treatment but stunning at 125 mA produced significantly 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 4–6 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 flow 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 flow and in 6%, both the left and right carotid arteries in the same animal were affected. Making the cut in the neck at the first cervical vertebra instead of the second to fourth cervical vertebrae reduced the frequency of the false aneurysm formation and the early arrested blood flow improving bleeding efficiency. 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 confirmed 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 (1000–2000 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 modified 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 efficiency 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 flow close to the surface of a conductor hence may produce a less severe muscular spasm at the beginning of the current flow (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 fibrillation. 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 (Turcsán et al., 2003). Frequencies N600 Hz fail to create ventricular fibrillation keeping

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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 significantly 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 findings 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 efficiency 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 significantly 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/modified and low atmosphere pressure stunning In modified 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

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technology has also been shown to significantly reduce the number of microorganisms, particularly coliforms and generic E. coli on cattle carcasses. The efficacy 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 defined 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. References Abeyesinghe, S. M., McKeegan, D. E. F., McLeman, M.A., Lowe, J. C., Demmers, T. G. M., White, R. P., Kranen, R. W., van Bemmel, H., Lankhaar, J. A.C., & Wathes, C. M. (2007). Controlled atmosphere stunning of broiler chickens: I. Effects on behaviour, physiology and meat quality in a pilot scale system at a processing plant. British Poultry Science, 48, 406–423. Agbeniga, B. (2012). Influence of conventional and Kosher slaughter techniques in cattle on carcass and meat quality. (M.Sc. Thesis). Pretoria, South Africa: University of Pretoria (http:// www.repository.up.ac.za/bitstream/handle/2263/26243/dissertation.pdf?sequence=1 Accessed 16 February 2014).

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