halal and khoser slauhgter methods and meat quality_a review

15
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 b 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 abstract article info 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 There are many slaughter procedures that religions and cultures use around the world. The two that are commer- cially 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 conven- tional quality issues, the spiritual qualityof 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 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, mas- ticatory, functional, nutritional, health, convenience and environmental- impact 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. Denitions and importance of meat quality 2.1. Conventional perspective 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 qual- ity is also judged in terms of intrinsic/extrinsic, table/eating, visual/ap- pearance, 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 avor are important consider- ations at the dining table, in contrast to meat protein solubility and the Meat Science 98 (2014) 505519 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. Contents lists available at ScienceDirect Meat Science journal homepage: www.elsevier.com/locate/meatsci

Upload: ekosaputrobbppbatu

Post on 29-Sep-2015

236 views

Category:

Documents


4 download

DESCRIPTION

Halal and Khoser Slauhgter Methods and Meat Quality_a Review

TRANSCRIPT

  • eD.Zeal

    ew Z

    ng, SSerd

    Keywords:

    cednd ked u

    ded th

    tional/health, safety/ical, physical/sensory

    Meat Science 98 (2014) 505519

    Contents lists available at ScienceDirect

    Meat Sc

    j ourna l homepage: www.e lspractices on meat quality are discussed. 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 like2013).In this review the impact of the halal and kosher religious slaughter

    pearance, manufacturing/technological, nutrireliance, expected/experienced, functional/chemMuslims and Jews, respectively. The global volume and value of meatcommercially produced using halal and kosher methods are huge(Table 1). Producers and consumers demand that the quality of thismeat is on par or even better than their equivalents produced usingconventional methods.

    Meat quality is generally described in terms of aesthetic, tactile, mas-ticatory, functional, nutritional, health, convenience and environmental-impact attributes. These can be affected by halal and kosher customsassociated with pre-slaughter, slaughter and post-slaughter (Farouk,

    and cuts for quality, but consumers' perception of meat quality is wideand subjective. It reects regional and national differences, ethnicityand culture, political and economic considerations, individual beliefsand 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; Thompsonet al., 2008; Zepeda, Sirieix, Pizarro, Corderre, & Rodie, 2013). Meat qual-ity is also judged in terms of intrinsic/extrinsic, table/eating, visual/ap- Corresponding author. Tel.: +64 7 838 5260.E-mail address:[email protected] (M.M

    http://dx.doi.org/10.1016/j.meatsci.2014.05.0210309-1740/ 2014 Elsevier Ltd. All rights reserved.e production, slaughtertion. Two of these, halalstill widely practiced by

    2.1. Conventional perspective

    Producers must follow narrow denitions when grading carcasses

    and preparation of meat for human consump(lawful) and kosher (ritually pure), areRitual slaughterNutritionStunningSafetyMeat spiritual quality

    1. Introduction

    Ancient traditions have long guitheir 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 bloodsplash (ecchymosis) in a range of muscles and organs of slaughtered livestock. Other quality concerns includebruising, hemorrhages, skin discoloration and broken bones particularly in poultry. In addition to these conven-tional quality issues, the spiritual quality of the meat can also be affected when the halal and kosher religiousrequirements are not fully met during the slaughter process. The nature, causes, importance and mitigations ofthese and other quality issues related to halal and kosher slaughtering andmeat production using thesemethodsare the subjects of this review.

    2014 Elsevier Ltd. All rights reserved.

    2. Denitions and importance of meat qualityAvailable online 5 June 2014meat produced using the methods. Halal and kosher slaughter per se should not affect meat quality more thanAccepted 29 May 2014red meat and poultry producHalal and kosher slaughter methods and m

    M.M. Farouk a,, H.M. Al-Mazeedi b, A.B. Sabow c,g, A.E.a AgResearch Limited, Ruakura Research Centre, East Street, Private Bag 3123, Hamilton, Newb Kuwait Institute for Scientic Research (KISR), PO Box 24885, Safat 13109, Kuwaitc Department of Animal Resource, University of Salah al-Din, Erbil, Iraqd Department of Food Science, Division of Sciences, University of Otago, PO Box 56, Dunedin, Ne Department of Animal Production, University of Ilorin, PMB 1515, Ilorin, Nigeriaf Halal Products Research Institute, Putra Infoport, Universti Putra Malaysia, 43400 UPM Serdag Department of Animal Science, Faculty of Agriculture, Universti Putra Malaysia, 43400 UPM

    a b s t r a c ta r t i c l e i n f o

    Article history:Received 14 April 2014Received in revised form 27 May 2014

    There aremany slaughter procially relevant are the halal a. Farouk).at quality: A review

    Bekhit d, K.D. Adeyemi e,g, A.Q. Sazili f,g, A. Ghani a

    and

    ealand

    elangor, Malaysiaang, Selangor, Malaysia

    ures that religions and cultures use around theworld. The two that are commer-osher methods practiced by Muslims and Jews respectively. The global trade insing these twomethods is substantial, thus the importance of the quality of the

    ience

    ev ie r .com/ locate /meatsc itenderness and juiciness, are intrinsic to meat, whereas reliance qualitytraits such as safety, price, presentation, packaging, origin and brandare extrinsic (Grunert, Bredahl, & Bruns, 2004; Joo & Kim, 2011; Troy& Kerry, 2010). Tenderness, juiciness and avor are important consider-ations at the dining table, in contrast to meat protein solubility and the

  • solubility, andWHC. For halal and kosher adherents,meat that has grad-ed well, yet failed tomeet theminimum requirements of religious com-mandments during its production, would be considered spirituallyworthless.

    2.2.1. Harmonizing spiritual and temporal viewsIndustrial production of high-quality meatmust juggle the disparate

    e selected countries/regions in 2012.

    Poultry meat/offal

    ef Lamb and chevon Edible offal

    8,083 16,792 1,20936,842 3,940 175,52095,742 48,336 108,341

    897,159 278,916 4,078,447225,707 36,540 1,513,312223,470 12,516 644,587

    9,033 10,854 10,6059 5,642,451 6,786,811 25,041,855

    ttp://www.trademap.org/tradestat/Country_SelProductCountry_TS.aspx). Accessed 23 March

    Saudi Arabia, Syria, Turkey, UAE and Yemen.

    506 M.M. Farouk et al. / Meat Science 98 (2014) 505519ability of the solubilized proteins to bindwater and fat, which are key pa-rameters duringmanufacturing. Some characteristics, such as highwaterholding capacity (WHC), inuence perceived quality for both the dinerand the manufacturer, particularly for meat intended for frying, grillingor roasting. However, the same WHC quality is not desirable for a jerkymanufacturer wanting to dry the meat quickly and cheaply.

    These conventional denitions of quality are based on inherent orperceived physical characteristics of meat. For most consumers theydetermine the meat's appeal, acceptability, utility and, ultimately, itsvalue.

    2.2. Spiritual perspective

    Spirituality and ideology inuence people's attitude toward thekilling of animals and the consumption of meat. Consideration of thesource, life and death of the animal adds another dimension to meatqualityone that cannot be evaluated by science ormeasured by instru-ments. Nevertheless, down-grades on those attributes can have amarked effect on meat value.

    Religions are rich with traditions around eating. For example Islamteaches that all animals are created by God (Quran 24:45), with somecreated specically for man's benet (Quran 36:71) to domesticateand use for transportation and food (Quran23:21; 40:79). Godprovidedthese 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 themeat distributed to the poor (Quran 22:34, 36) who cannot on theirown afford to buy and slaughter an animal for meat.

    A key condition of the permission given to man to slaughter and eat

    Table 1Value (USD x 1000) of imported halal and kosher red meat, poultry and co-products of som

    Importing country/region and products Red meat category

    Chilled beef Frozen be

    Halal red meat, poultry and co-productsIndonesia 11,499 127,715Maghreb 57,276 305,497Malaysia 16,972 410,097Middle East 598,504 2,942,249- Saudi Arabia 75,043 362,267- United Arab Emirates 160,105 195,407

    Kosher red meat. Poultry and co-productsIsrael 264 418,421World total red meat import 19,803,464 17,797,64

    Source: Market Analysis Research, International Trade Centre (ITC) Geneva Switzerland (h2014.Maghreb = Algeria, Libya, Mauritania, Morocco and Tunisia.Middle East = Bahrain, Egypt, Iran, Iraq, Jordan, Kuwait, Lebanon, Oman, Palestine, Qatar,the esh of animals is to mention the name of God during theslaughtering (Quran 6:121; 22:36). According to Al-Qaradawi (1960),acknowledging God during the slaughter is tantamount to the slaugh-terer rst obtaining consent from his and the animal's Creator to takethe life of another creature; and it is a declaration on the part of theslaughterer that his act is not an act of aggression against the universenor of oppression of the creature about to be slaughtered, but simplyan act necessitated by a need fullled in the name of God. Conversely,under some condition consumption is prohibited, such as animals thatwere dead prior to exsanguination, or that were slaughtered withoutmentioning God, or in which other deities or names other than that ofGod were professed during the slaughter, will corrupt the heart and re-sult 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 thequalities of meat, spiritual quality is of foundational importance forMuslims as well as some other faith groups (Fig. 1). Indeed it is thechief consideration for a large population of consumers and supersedesphysical properties of meat such as color, tenderness, juiciness, proteindemands of consumer groups and food safety regulators. There is urgentneed to harmonize devout spiritual views with those that are temporalor corporeal and which are based on scientic evaluation. A major areaof contention is the slaughter of animals without stunning prior tothroat slit and exsanguination. This practice is allowed in many coun-tries, but it is extremely controversial with regard to animal welfare.Areas of concern include the stress of restraining the animal, whetherthe cut is painful, and whether the animal experiences undue distresswhile 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 themindful 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 attributesPackaging

    Halal livestock

    Legally owned & ethically farmed

    Slaughtered the prophetic way, faithfully & sincerely

    Fed and watered prior to slaughter

    Spiritual quality

    Marbling

    Colour

    Juiciness Water & fat binding capacity

    Tenderness Protein solubility

    Safe

    Healthy/ nutritious

    Appearance Texture/Firmness

    Aroma

    Flavour

    Country of origin

    Emulsion activity index

    OrganicPrice

    BSE freeGelling capacity

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

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

  • slaughter, using a sharp knife to quickly severe the four vessels in theneck, mentioning the name of God during the slaughtering with sincer-ity and conviction, such that the animal will be dispatched as painlesslyas possible.

    For Muslims, meat produced this way would be considered of thehighest spiritual quality. On the other hand, this method of slaughter isconsidered cruel and contrary to scientic wisdom by those who thinkthat the animal must rst be stunned in order to avoid compromisingits welfare. These groups advocate for food labeling that identies meatfrom animals slaughtered without stunning and they consider suchmeat to be ideologically of the lowest quality. The importance of har-monizing these opposing views and the issues involved for commercialproduction 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 outdat-ed thinking that pitches science against religion and encouragesdogmatic arguments that create stumbling blocks toward progress(Nelson, 2006). In fact, there is an essential starting point for ndingconsonance in the pre-slaughter stunning debate; both sides agreethat animal welfare is important in the production of meat. Thus resolu-tion seems possible. In similar spiritually charged arguments, a critical

    properly, the welfare of the slaughtered animal is not compromised,even if this cannot be veried scientically using currently availableinstruments.

    On the other hand, supporters of non-stunning methods need toacknowledge that:

    some commercial production facilities have poorly trainedslaughtermen and unacceptable animal restraint systems that causeunnecessary animal suffering;

    in some unscrupulous processing plants and backyard abattoirs,religious invocations are merely whitewash over horric slaughterpractices (Gregory, Schuster et al., 2012; Gregory, von Wenlawowiczet al., 2012);

    scientic methods that have been proven to harmonize the religiousand spiritual requirementsmust be adopted to improve animalwelfareand to produce meat of both high spiritual and conventional qualities.

    3. Halal and kosher meat production practices

    3; Regenstein et al., 2003).

    uirede-slinsee cu

    es

    each

    our vroke

    rgamixe

    507M.M. Farouk et al. / Meat Science 98 (2014) 505519and rational examination of the issues often reveals little basis for con-ict between practitioners and their world views (Bainbridge, 2004;Bakar, 2005; Smedes, 2005). As Harper (2001) puts it, both scienceand religion have practical reasons for exploring constructive dialogueto avoid the conict-perpetuating tendencies of both religious funda-mentalism and its scientic counterpart, reductionist scientism. Suchtendencies are unhealthy for both science and religion.

    For this debate to become a dialogue, some signicant differences incognitive orientation and epistemology must be overcome. Proponentsof 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 usefuland should not be discounted (Nelson, 2006);

    people's deepest cultural values, often nourished and embodied inreligious contexts, should be appreciated as more than outmodednonsense, with a certain humility and respectfulness by sciencetoward this accumulated reservoir of moral wisdom (Harper, 2001);

    science should not try to use its methods to explain what is spiritualor use inciting vocabulary or attempt to superimpose empiricistmeanings on religious terms in its discourse with religious groups(Henriksen, 2008; Regenstein, 2012);

    it is possible that when religious slaughter is done faithfully and

    Table 2Comparison of halal and kosher meat production and consumption practices (Farouk, 201

    Practice/attribute Kosher

    Pre-slaughter handling Humane and deliberate treatment reqPre-slaughter state of consciousness Animal must be alive and conscious prPre-slaughter stunning Any stunning that renders the animal

    slaughter is not acceptable. None of thacceptable

    Post-slaughter stunning Accepted by very few kosher authoritiSlaughterer Must be a Jewish shochetSlaughter knife A special knife (chalef) is required forBlessing on animals at time of slaughter Not required on each animalSlaughtering Must be a single stroke to severe the f

    without severing the head. Multiple stnon-kosher

    Post-slaughter further processing On the complete death of the animalPorging and koshering Required practicesMeat spiritual quality Foundationally importantResidual blood in meat following slaughter Not acceptable. Must be kosheredEdible portions Certain parts of the carcass and some oMeat spiritual status Kosher status could be affected when

    kosher foodsAcceptability Kosher meat is halal for MuslimsHalal

    Humane and deliberate treatment requiredaughter Animal need only be alive pre-slaughternsible prior torrent methods are

    Although non-stunning is most preferred, reversible forms ofstunning is widely accepted and practiced

    Next-best to no-stun for the proponents of this methodA Muslim or a practicing Jew (follower of Judaism) or Christian

    specie No special knife is required. Knife can be used across speciesRequired on each animal

    essels in the necks renders meat

    Single stroke is preferred. Multiple strokes do not render the meatnon-halal. The head should not be deliberately severed duringslaughterOn the complete death of the animalNot requiredFoundationally importantWhat naturally remains in meat is acceptable

    ns are not eaten All edible parts are halald with certain Halal status remain regardless of what other halal food it is mixed

    withHalal meat is not kosher for JewsThe pre- and post-slaughter practices involved in halal and kosherproduction of red meat have been recently reviewed (Farouk, 2013)and are compared (Table 2) and pictorially represented together withpoultry slaughter practices in Figs. 2, 3 and 4.

    The impact of these practices onmeat quality can bediscussed underthree broad categories:

    1. Pre-slaughter practices include (a) the use of restraints to hold live-stock in place for ease of slaughter and thewelfare of the slaughteredlivestock and the safety of workers; (b) pre- and post-slaughterstunning particularly the use of head-only electrical stunning inhalal meat production; and (c) how closely the halal and kosherrequirements have been adhered to pre-slaughter.

    2. Slaughter and post-slaughter practices include the slaughteringactivity and the subsequent use of immobilization and thoracic stick-ing in halal and schechita (kosher ritual) practices, plus the removalof residual blood in kosher meat production.

    3. Combination of pre- and post-slaughter practicesThe use of electri-cal currents in pre-slaughter stunning and post-slaughter immobili-zation increases the electrical inputs in carcasses that could lead tothe rapid fall in pH in muscles post-mortem compared to the use ofmechanical stunning without immobilization or no stunning at all.

  • nni

    508 M.M. Farouk et al. / Meat Science 98 (2014) 5055193.1. Pre-slaughter practices

    3.1.1. Pre-slaughter restraintsAnimals to be slaughtered must be properly restrained. This is

    Fig. 2. Steps in the industrial production of halal red meat including stuparticularly important in halal and kosher methods where theanimal's neck needs to be presented to the knife and held relativelystill until the slaughtering is complete (Agbeniga, 2012). Securerestraint spares the animal from distress, pain, bruises and injury

    Fig. 3. Halal slaughtering of lambs showing animals at lairage, being s(Lambooij, van der Werf, Reimert, & Hindle, 2012; Velarde et al.,2014). Common methods of restraining red meat animals prior tostunning and/or slaughter include hoisting by hind-leg, castingwith a rope and/or chain, restraint in a V-shaped or straddled

    ng, slaughter and further processing using modern slaughter methods.conveyor, full or half inversion in a rotary pen and upright restraintsystem (Gregory, 2005) while the use of cones and shacklingare common methods of restraining birds (Lambooij, Pieterse,Hillebrand, & Dijksterhuis, 1999).

    tunned, slaughtered and bled using modern slaughter methods.

  • Problems and risks associated with old fashioned restraint systemswere addressed in the design of upright restraints (also known asASPCA pens), as demonstrated by Koorts (1991) who observed thatthe severity and prevalence of struggling were higher in animalsinverted in casting pen than those positioned uprightly followingkosher and conventional slaughter. Similarly, Dunn (1990) observedlower hematocrit, cortisol and ultimate pH in cattle slaughtered inASPCA pens compared to those slaughtered in Weinberg casting pens.Head restraint before inversion in cattle produced less vigorous strug-gling than head restraint after inversion (Van Oers, 1987). Cattlerestrained in a poorly designed head holder (i.e., where the timerequired to drive the animal into the holder exceeded 30 s) had higherlevels of the stress hormone cortisol than those stunned with theirheads free (Ewbank, Parker, & Mason, 1992). For religious slaughter,the likely changes occurring during inversion were not severe enoughto cause substantial respiratory problems as indicated by blood gastensions (Wagner, Muir, & Grospitch, 1990). Despite the merits ofupright restraining pens, Gregory (2005) identied two signicantshortcomings. Firstly, the throat cut is somewhat difcult since it hasto bemade upward instead of downward. Secondly, due to the positionof the slaughterer relative to the cut, he ismore likely to be coveredwithblood. In addition, poorly constructedASPCApens could apply excessivepressure to the neck and thoracic regions of cattle (Grandin &Regenstein, 1994). Also, the effectiveness of the restraining systemsdepends to a large extent on the calmness and experience of the opera-tor (Grandin & Regenstein, 1994).

    controls to avoid excessive pressure; (3) no protrusions or sharpedges to avoid injuries; (4) smooth and steady movement of restraintdevices; (5) noise control to avoid scaring the animals; and (6) lightingand shields that guides the animal into the restrainer. All these mea-sures are relevant in terms of meat quality in addition to preservingthe welfare of the animal during slaughter.

    3.1.2. Pre-slaughter/post-slaughter stunningThe 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 ofproblems with meat and carcass quality can be directly attributed topre-slaughter stunning (Daly, 2005). Ecchymosis (blood splash) andspeckles are forms of hemorrhages that occur in livestock (Fig. 5). Stud-ies in the 1970s and 1980s involving hundreds of lambs established thecauses 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 ofblood inmuscles and the latter is petechial hemorrhages in fat or con-nective tissue overlying the muscle. Both may be a consequence ofshearing and rupture of blood vessels resulting from severe musclespasm or supercontracture (Gilbert & Devine, 1982; Leet et al.,1997). Hemorrhages are found in muscle, connective tissue and or-

    509M.M. Farouk et al. / Meat Science 98 (2014) 505519In poultry, Lambooij et al. (1999) compared cone restraining andshackling methods on carcass quality of broiler chickens. The authorsfound that the incidence of thigh muscle hemorrhaging was higher inshackled birds than those restrained in cones. Nonetheless, shackledbirds had slightly greater blood loss and their meat was judged to bemore tender than those from cone-restrained birds, probably due tothe high pH value observed in the meat of cone-restrained birds.Kannan, Heath, Wabeck, and Mench (1997) also observed that longershackling duration elevated corticosterone levels and impaired colorof 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 follow-ing features: (1) non-slip ooring in the restraint device; (2) pressure

    1

    2

    5Fig. 4. Steps in the modern processing of ducks showing transport, shackling, stunning, slagans (hearts, lungs, gall bladder, and duodenum) (Kirton, Bishop,Mullord, & Frazerhurst, 1978). They range in size from microscopicto several centimeters, which can affect the appearance and accept-ability of the meat (Leet et al., 1997).

    The effect of stunningmethods on the severity of blood splash is in theorder: no stun b percussion b captive bolt b head-to-back electricalb head-only electrical (Kirton, Frazerhurst, Bishop, & Winn, 1980-81;Kirton, Frazerhurst, Woods, & Chrystall, 1980-81). Incidence of bloodsplash and speckle in electrically stunned lambs increases with stunduration 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 lessthe severity of blood splash (Kirton et al., 1978).

    3

    4

    6

    4ughtering and bleeding. These steps are similar for most poultry, including chickens.

  • f m

    or im

    sis/rcasin ES lasociass d

    andheml brqu

    houlooeinsum,

    oodciat

    orrthe

    510 M.M. Farouk et al. / Meat Science 98 (2014) 505519In an unpublished report Ahmad (2007) questioned whetherviolently counteracting muscle contractions during electrical stunningactually cause localized tearing of the capillary bed that leads to bloodsplash. He cited a number of authors and summarized their ndings asfollows:

    Hemorrhages can be induced electrically in tissues that have noskeletal muscle, such as the brain (Hassin, 1933). If this appliesmore broadly, it is unlikely that localized striated muscle contractionis 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, inrats, propranolol reduced and phentolamine increased the extent ofblood splash. The effects of these drugs would not necessarily be lim-ited to the arterial side of the circulation, as venous dilatation couldalso play a role (Vanhoutte, Verbeuren, & Webb, 1981). Presumably,it is the engorgement of the capillary bed which encourages rupture

    Table 3Effect of pre-slaughter stunning used in halal meat production on the defects and quality o

    Type of stunning Species Defects/quality issues

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

    Cattle and sheep includingcalves and lambs

    No petechiae, ecchymobone fractures in NS cahigher heart petechiaecookloss, drip loss in N

    Poultry, including broilers, hens,turkeys, ducks

    No physical defects asmay improve tendernecompared to NS.

    Rabbits NS meat had lower pHHead-only ES Cattle, sheep, deer, goats

    including calves, lambs and goatkids

    Ecchymosis/petechialhematomas; occasionaconsequences on meat

    Ostriches and poultry, includingbroilers, hens, turkeys, ducks

    Red wing tips; wing, smuscle hemorrhages/bof wing and pectoral vbones, coracoid, furcul

    Low (5060 HZ) vs. high(N600 HZ) frequency ES

    Livestock Lower incidences of bldefects in poultry assocompared to low.

    Percussive stunning (PS)compared to ES or NS

    Cattle, sheep Incidence of brain hemor NS; blood splash inof vessels when placed under pressure. The blood vessels may be unduly fragile. Histological examination ofblood splash in meat has shown that the vessels that burst are onthe venous side of the capillary bed, which has less elastic walls thanthe arterial side, and so are weaker and more prone to damage.Blood splash is common in animals that have died from anticoagulantpoisoning and these animals have increased capillary fragility (Fulton& Berman, 1964; Littin, 2004). Lambs in a ock that had a high preva-lence of blood splash had poor blood coagulation in terms ofprothrombin time (Restall, 1981), and it was suggested that the com-mon link might be ingestion of excessive amounts of coumarins frompasture. The raised susceptibility to blood splash in unweaned lambsmight be a low vitamin K status because of their milk-based diet.

    During intense generalized muscle body contractions, the venous andarterial systems experience severe external pressure. Squeezing ofthe veins results in large rises in venous pressure, which is transmittedto the capillary system at sites that can be some distance from thecontractions. The venules in the capillary bed probably burst wherethey are weakest, or where venous pressure is particularly high. Thisreferral of pressure, causing distant petechial hemorrhage, has beenseen in other contexts when sudden intense pressures have beenapplied to veins (French & Callender, 1962). Engorgement of thevenous circulation would presumably exaggerate this effect.

    Electrical stimulation of tissues, even at low currents, will promoteextravasations of blood cells from the capillary bed, but this is aninammatory response and is slower than the time available underslaughtering conditions (Nanmark, Buch, & Albrektsson, 1985).

    Ahmad (2007) concluded by suggesting the need for concertedscientic effort to understand the real causes of blood splash.

    Gilbert (1993) described practical techniques for managingproblems associated with electrical stunning. Blood splash and specklebruising can be reduced by using minimum stunning currents, mini-mum stun-to-stick times and very good stunning techniques, whichprincipally ensure good electrode contact. Ecchymosis was reported tobe reduced in fallow deer by thoracic stick exsanguination executedless than 10 s after stunning (Mulley, Felapau, Flesch, &Wiklund, 2010).

    3.1.2.2. Red meat animals. Anil, Love, Helps, and Harbour (2002) com-pared penetrating captive bolt, non-penetrating captive bolt and electri-cal stunning of cattle and sheep and found that there was a risk ofhematogenous dissemination of central nervous system tissue with

    eat from halal livestock.

    provement References

    blood splash, hematomas ands and organs compared to ES,S than NS; lower pH,mbs than ES.

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

    ted with NS in poultry. ESue to faster rigor attainment

    Kettlewell and Hallworth (1990); Papinaho and Fletcher(1996); Mast and Macneil (1983); Fernandez et al.(2003).

    was lighter than ES. Lpez et al. (2008); Nakyinsige et al. (2014)orrhaging/blood splash;oken bones and attendantality.

    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).

    lder, strawberry and breastd splash, engorged/smearing; red feather tract; brokenscapula, and pectoral.

    Gregory and Wilkins (1989); Raj et al. (1998); Wilkinset al. (1999); Wilkins andWotton (2002); Turcsn et al.(2003); Ali et al. (2007); Fernandez et al. (2010); Hindleet al. (2010); Lines et al. (2011); Lambooij et al. (1999,2014).

    splash in larger animals anded with high-frequency ES

    Gregory et al. (1991); Mouchoniere et al. (1999);Fernandez et al. (2003).

    hage with PS compared to ESorder NS b PS b ES.

    Kirton, Frazerhurst, Woods et al. (1980-81); nenc &Kaya (2004); Sazili et al. (2013).the use of pneumatically or cartridge-operated penetrating captivebolt but nonewith electrical stunning. The dissemination of central ner-vous system tissue poses a threat to public health in relation to possibleslaughter of animals with preclinical bovine spongiform encephalopa-thy (Anil et al., 2002).

    The use of electrical stunning in ruminants can cause bruising, bloodsplash, 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 electri-cally 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 heartsof head-only electrically stunned lambs compared to non-stunnedlambs. Grandin (2003) is of the opinion that electrical stunning is lessproblematic when used on grass-fed cattle compared to feedlot cattle;she gave an example of the success of electrical stunning in NewZealand and the problem of blood splash and meat damage whenused in Australia on feedlot cattle.

    Electrically stunned lambs have been reported to have approximate-ly 20 times the noradrenaline and 14 times the adrenaline level of non-stunned lambs (Pearson, Kilgour, de Langen, & Payne, 1977). This wasrecently conrmed for other pre-slaughter stunning methods but notin penetrative percussive stunning after slaughter (Zulkii et al.,2014). These stress markers are evidence that stunning, whether elec-trical or mechanical, affects the animal. Sazili et al. (2013) compared

  • ryin

    511M.M. Farouk et al. / Meat Science 98 (2014) 505519the effects of four slaughtering methods on the quality of bovine m.longissimus and m. semitendinosus. The methods were high powernon-penetrative percussive stunning prior to slaughter (HPNP); lowpower non-penetrative percussive stunning prior to slaughter (LPNP);penetrative percussive stunning prior to slaughter and penetrative per-cussive stunning after slaughter. The authors found HPNP stunning hadnegative effect on WHC and color values and resulted in higher lipidoxidation and shear force values compared with the rest of treatmentsin m. semitendinosus but not m. longissimus. nenc and Kaya (2004)found no difference in WHC in beef from stunned and non-stunnedanimals, but the cooking loss was higher in beef from electricallystunned animals. The authors reported the non-stunned beef tobe more tender but beef from stunned animals had better color.Agbeniga, Webb, and O'Neil (2013) compared the meat quality of

    Fig. 5. Examples of blood splashes in different bovine muscles of vapost-cut captive bolt stunned and kosher slaughtered feedlot cattle tothat of pre-slaughtered captive bolt conventionally slaughtered equiva-lent animals and found that the meat from the shechita slaughteredanimals was more tender and had less cook loss compared to its con-ventionally slaughtered equivalents.

    3.1.2.3. Poultry. The two major types of stunning used in birds are gasand electrical stunning. However, electrical stunning is themost univer-sally acceptable (McKeegan et al., 2007) and the most commonly prac-ticed stunning method in halal poultry slaughtering requiring highthroughput rates (Che Man & Sazili, 2010). The ability of the electricalstunning to rapidly immobilize birds, lessen slaughter-related struggleand enhance bleeding efciency substantiate its use in the poultry in-dustry. Electrical stunning is also relatively cheap, convenient and safe(Farouk, 2013; Fletcher, 1993). Nonetheless, in spite of its improvedmethodology and widespread use, electrical stunning has been impli-cated in poor meat quality due to low bleeding efciency, occurrenceof blood blisters, and tougher meat if the time is insufcient for rigormortis to develop prior to lleting (Summers, 2006).

    Electrical stunning of birds is typically carried out in an electricallycharged water bath by moving the head of the birds across water con-taining a submerged electrode. Conscious birds are hung upside downon a moving metal shackle line and passed through the electriedwater bath in such a way that the current ows through the entirebody toward the shackle (Che Man & Sazili, 2010). However, shacklingof conscious birds to overhead line has been implicated in considerableproduct damage, arduous working conditions and poor animal welfare(Abeyesinghe et al., 2007).

    In order to correct these anomalies, improvements are being madeinmechanical design and the electrical parameters of voltage, amperageand frequency (Fernndez-Lpez, Sendra-Nadal, & Sayas-Barber,2010). For an effective stun, the parameters must cause loss of sensibil-ity and consciousness but not carcass damage or death of the birds incompliance with halal requirements (Che Man & Sazili, 2010;Nakyinsige, Che Man et al., 2013). For instance, the use of high voltageand current in the water bath has been criticized for producing muscu-lar contraction that negatively imparts meat quality (Mouchoniere,Pottier & Fernandez, 1999; Wilkins, Gregory, Wotton, & Parkman,1998). These contractions may cause red wing tips which result inlosses in yield and saleable product since they are often trimmed during

    g levels of severity. Blood splash represents poor aesthetic quality.nal inspection of carcasses (McNeal, Fletcher, & Buhr, 2003). Highvoltage may also induce heart brillation, causing inefcient bleeding,increased hemorrhaging, and even death before exsanguination(Fernndez-Lpez et al., 2010; Gregory & Wilkins, 1989). High currentincreased the incidence of dislocation, broken bones, red wing tipsand 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 increasedincidence of carcass downgrading with increasing amperage. Thiscorroborates the ndings of Hindle, Lambooij, Reimert, Workel, andGerritzen (2010) which showed that increased amperage and voltagedecreased carcass quality in duck, hen and broilers. Contrarily,Papinaho and Fletcher (1995) observed that low-voltage electrical stun-ning does not affect total blood loss after the 90 to 120 s exsanguinationperiod despite lower early blood loss.

    Frequency (hertz) of the alternating current also affects stunning ef-fectiveness and meat quality in birds. Details of this are described inSection 4.2.

    3.2. Slaughter of red meat animals and poultry

    The aim of efcient and humane slaughtering is to remove the bloodas 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) 505519killing the animal through the loss of blood, the removal of owingblood is necessary because it is considered an impurity that should notbe consumed.

    The halal and kosher requirements for slaughtering in redmeat pro-duction have been discussed earlier (Farouk, 2013). In poultry, the act ofslaughtering begins with the incision on the neck at a point just belowthe glottis (Che Man & Sazili, 2010). Throat cutting in halal and kosheris done to severe the trachea, esophagus and the two carotid arteriesand jugular veins without head decapitation during the process (CheMan & Sazili, 2010; Farouk, 2013; Lpez et al., 2008).

    Ritual slaughtering has been reported to producemeatwith high pHafter 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 com-pared to non-kosher.

    Although the halal and kosher status of meat is usually sufcient todetermine the purchasing decision of observant Muslims and Jews(Ahmed, 2008; Chowdhury, Helman & Greenhalgh, 2000), halal and ko-sher 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 thisperception appears to be linked to the perceived greater blood lossduring halal slaughtering and the koshering process post-slaughter(described in Section 3.3.2). This general perception of higher bloodloss during halal and kosher slaughtering have been challenged by thestudies that found no difference in total blood loss in sheep and cattleslaughtered 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 inlambs (Hopkins, Shaw, Baud, & Walker, 2006; Velarde et al., 2003). Onthe other hand, Nakyinsige et al. (2014) found higher blood loss inNew Zealand white rabbits halal-slaughtered without stunningcompared to gas stun-killed animals. This higher blood loss in non-stunned animals was conrmed by lower hemoglobin content in m.longissimus lumborum from this treatment group. These conictingresults may suggest species-effect for the slaughtering methods.

    Heme iron, rather than inorganic iron, was shown to be the respon-sible compound causing the formation of the carcinogenic N-nitrosocompounds (Cross, Pollock, & Bingham, 2003). A study by Pierre,Freeman, Tach, Van der Meer, and Corpet (2004) used several dietscontaining inorganic iron (control), chicken (low heme content), beef(medium concentration heme content), blood sausage (high hemecontent) and hemoglobin (equivalent to beef diet) to examine theformation of aberrant crypt foci and mucin-depleted foci, markers forcolon carcinogenesis, in rats with low calcium diet. All diets containingheme promoted mucin-depleted foci and the highest putative precan-cerous lesions per rat colon was the highest in blood sausage.Alvarado, Richards, O'Keefe, and Wang (2007) examined the followingve slaughter techniques to determine their effects on pH, color, lipidoxidation and residual hemoglobin concentration in broiler breast l-lets: 1) CO2 slaughter and not bled, 2) no stunning and bled, 3) electricalstunning (ES) and bled, 4) CO2 stunning and bled, and 5) ES and decap-itation. The authors (Alvarado et al., 2007) found that thellets from theCO2 slaughter and not bled birds were redder and had higher residualamount of hemoglobin compared to the other treatments; and thatlipid oxidation was signicantly lower in ES and bled birds comparedto others.

    3.2.1. Red meat animalsAlthough it is recommended that the two jugular veins, carotid ar-

    teries, trachea and esophagus be severed during halal slaughtering,opinions among Islamic scholars differ as to the minimum parts to becut for the animal to be Halal (Al-Qaradawi, 1960). However all agreethat the neck is where the cutting should take place, and that theblood has to gush forth. Properly severing all the arteries and veins has-

    tens the death of the animal. Prolonged death does not necessarilyrender the meat non-Halal, but prolonged suffering is not acceptable.Devine, Tavener, Gilbert, and Day (1986) reported a case in which astunned calf bled poorly because only a single carotid artery was sev-ered, with this animal the electroencephalogram remained at a highlevel and fell only slowly indicating a possibility of prolonged suffering.Gregory and Wotton (1984) found that severing both carotid arteriesplus jugular veins in sheep induced a loss of brain responsiveness(ash-evoked responsiveness in the electrocorticogram) in 14 s, where-as severing only one carotid artery plus one jugular vein took 70 s.When only the jugular veinswere cut, the time to loss of evoked respon-siveness was approximately 5 min. Newhook and Blackmore (1982)found that in one sheep thatwas slaughtered by severance of the carotidartery and jugular vein on one side of the neck only, the onset of insen-sibility, as determined from the study of electroencephalograms, wasdelayed for 29 s.

    3.2.2. PoultryIndustrial halal poultry slaughtering can be achieved via manual

    (hand) slaughter or a mechanical device, depending on available facili-ties and size of operation (Che Man & Sazili, 2010). Manual slaughter ispreferable and ismostly used in slaughter plants controlled byMuslims.In large-scale production where halal is not the focus, productionefciency dictates mechanical slaughtering. These machines aredesigned to cut the throat and esophagus and sever the jugular veinsand carotid arteries (Gregory & Wilkins, 1989). However birds can bemis-slaughtered (other parts of the body are cut instead) or missed(not slaughtered) by the machine. The requirements for halal poultryslaughtering using manual or mechanical method have been summa-rized by Che Man and Sazili (2010).

    In birds, Davis (1996) reported that head decapitation increasestime of death as it disrupts the nervous system causing asphyxia andsuffocation while separation of the jugular vein and carotid arterieswithout head decapitation shortens the time of death. Zaman, Nassir,Abdurrazq, Salleh, and Rahman (2012) investigated variation of totalprotein prole in chicken skeletal muscle as inuenced by twomethodsof slaughtering using a sharp knife. In the rst treatment, the neck waspartially cut leaving the spinal cord intact and bodywas released imme-diately after slaughtering while in the second treatment, the neck wascompletely cut off and body was tied until the animal died. Using 2-Dgel electrophoresis the authors found a protein near pH 5.0 and MW116 kDa that was present in skeletal muscle from the second treatmentonly.

    Mast and Macneil (1983) compared the quality attributes and meatyield of broiler chickens processed in commercial plants using eitherconventional or kosher procedures. Conventionally processed chickenhad higher water uptake during immersion chilling and lost moreweight during storage. Breast meat from kosher chicken was more ten-der than conventional breast meat as evaluated by sensory techniquesand shear test. Albeit the differences were not statistically signicant,kosher samples consistently had lower microbial counts and slightlyhigher thiobarbituric acid (perioxide) values than its conventionalcounterpart. Lpez et al. (2008) assessed the welfare, bleeding efcien-cy and meat quality in rabbits subjected to either halal slaughter with-out stunning or electrically stunned prior to slaughtering; the authorsfound that halal slaughtered rabbits had higher blood loss and lowerpH values in longissimus dorsi and biceps femoris muscles. Similarly,Nakyinsige, Sazili et al. (2013) did not observe signicant difference inmeat quality of rabbits slaughtered through the halal procedure or gasstunning before slaughtering.

    3.3. Post-slaughter processes

    3.3.1. Electro-immobilization and thoracic stickElectro-immobilization and thoracic sticking are common post-

    slaughter processes associated with the electrical head-only pre-

    slaughter stunning of livestock. The procedures have been described

  • thoroughly by Farouk (2013). The post-mortem fall in pH is faster inmuscles from electro-immobilized carcasses (Daly, 2005). The benetsof this effect are discussed in Section 3.4. Thoracic stick aids thecomplete bleeding of slaughtered cattle and consequently reduces thenegative effects of residual blood in meat (refer to Section 3.3).

    3.3.2. KosheringKoshering is an important post-shechita procedure in the produc-

    tion of kosher meat. It is undertaken to purge meat of all remainingblood following slaughter. This is because blood, including all theremovable residual blood in the meat is not permitted to those whoconsume kosher meat for religious reasons (Regenstein, Chaudry, &Regenstein, 2003). This process has tremendous effects on the meatquality (Table 4). Koshering also removes some myoglobin and othersarcoplasmic proteins (Asghar, Torres, Gray, & Pearson, 1990) due tothe use ofwater for Shriah (soaking in coldwater for 30min) and exten-sive use of salt for Hadacha (salting the surface using kosher coarse salt

    The reduction in heme proteins affects the color of the nal product.Kosher meats have been reported to have low color intensity (Holzeret al., 2004; Torres, Pearson, Gray, Booren, & Shimokomaki, 1988;Zuckerman &Mannheim, 2001). The use of large amounts of salt causeslow color stability and accelerates the discoloration of meat (Torreset al., 1988; Zuckerman & Mannheim, 2001) which can be alleviatedby 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 toconventionally slaughtered meat is the high salt content. Mast andMacneil (1983) found the sodium content in meat and skin of kosherchicken 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 themeat and was not affected by rinsing and cooking (Angel, Weinberg, &Jaffe, 1989). Salt is a catalyst for lipid oxidation (Kanner, Harel, & Jaffe,

    on m

    lor p

    canr ox

    ongiiffer

    513M.M. Farouk et al. / Meat Science 98 (2014) 505519for approximately 1 h) (Regenstein & Regenstein, 1988). The removal ofmyoglobin will have several consequences on the color, avor and theoverall product quality, but the most important effect from healthpoint view is its impact on the oxidative processes. Hemoglobin andmyoglobin contain iron atoms in their porphyrin rings and this ironcan change in oxidation state during reactions with other molecules.The lowest iron oxidation state is the ferrous form (Fe2+) with waterbound to the iron nucleus in the case of deoxymoglobin or oxygenbound to the iron in the case of oxymyoglobin. There is alsometmyoglobin (Fe3+), ferrylmyoglobin (Fe4+), and the short-livedperferryl radical that can exist at different stages of oxidation. Myoglo-bin contains iron in variable valances and may act as either an antioxi-dant (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 certainconcentrations. Lipid hydroperoxides are generated during lipid perox-idation and the presence of myoglobin catalyzes the breakdown of lipidhydroperoxides (Baron et al., 1997; McClements & Decker, 2008).Several mechanisms have been proposed for myoglobin-inducedlipid 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 pro-teins are expected to be solubilized but there are no published reportsto document this assertion. The protein loss from sarcoplasmic andmyobrillar fraction maybe signicant from nutritional point of viewbut it may be balanced by changes in moisture (Hajmmer, Marsden,Crozier-Dodson, Basheer, & Higgins, 1999). The extent of protein lossesdue to koshering is unknown and is worthy to be included in futureinvestigations.

    Table 4Some positive (+) and negative () aspects of halal and kosher post-slaughter processes

    Process Nutritional and quality aspects

    Koshering Removal of haem/blood (+); higher discoloration (); lower covalues) ()Removal of proteins ()High salt content ()

    High lipid oxidation ()Low microbial count (+)

    Halal slaughtering No effect on removal of haem/blood in sheep and cattle but signiLower drip loss (+); no effect on color parameters (L*, a* and b*) odisplay60% higher dye uptake by ultrasound in halal chickenLower lipid oxidation in beef semitendinosus and NZwhite rabbit LPseudomonas aeruginosa and Escherichia coli but total count not d1991), and kosher meat may develop objectionable odor during post-mortem refrigeration (Holzer et al., 2004).

    The koshering process was reported to reduce the levels ofEscherichia coli and Salmonella spp. due to its preservative actions suchas altering the water activity and ionic strength of meat (Hajmmeret al., 1999) and reducing attachment of Salmonella to chicken surface(Oscar, 2008).

    3.4. Accelerated post-mortempH fall due to combined electrical inputs fromstunning and immobilization

    Daly (2005) observed that among some of the carcass quality prob-lems associated with electrical stunning and immobilization is that ofaccelerated pH decline due to the violent forces produced by musclecontraction caused by the stun. Themeat quality effects of high temper-ature and low pH have been thoroughly reviewed (Jacob & Hopkins,2014; Kim, Warner, & Rosenvold, 2014).

    According to Simmons et al. (2008), the combined electrical inputfrom stunning and immobilization can drive muscle glycolysis fasterresulting in the muscles attaining rigor at higher temperature leadingto a denaturing condition and a number of meat quality problemssummarised in Table 5. Simmons et al. (2008) electrically stunned andimmobilized 40 steers using low or high frequency and found that theuse of low-frequency immobilization drove the pH down faster resultingin higher drip loss and shear force compared to high-frequency immobi-lization. Warner, Dunshea, Gutzke, Lau, and Kearney (2014) determinedthe incidence of high rigor temperature in 1512 beef carcasses acrossAustralia and found very high occurrence of the phenomenon (up to94%) from meat plants that apply various electrical inputs during pro-cessing including post-slaughter electrical immobilization of carcasses.The electrical stunning of poultry reduced initial pH values (Papinaho

    eat quality.

    Reference

    arameters (L*, a* and b* 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)Powers and Mast (1980); Torres et al. (1988)Powers and Mast (1980); Hajmmer et al. (1999);Zuckerman and Mannheim (2001); Holzer et al. (2004)

    t effect in rabbits Anil et al. (2004, 2006); Nakyinsige et al. (2014)ymyoglobin % over 6 days of D'Agata et al. (2009)

    Leal-Ramos et al. (2011)ssimus lumborum (+); lowerent in rabbit (+)

    Sazili et al. (2013); Nakyinsige et al. (2014)

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

    Livestock Stunning method Outcome Reference

    General for all livestock Increased electrical inputs into carcases due toelectrical stunning and immobilization

    Accelerated post-mortem glycolysis and pH decline while muscle temperature re-mains high. Effects include color shelf-life; water holding and fat binding capacities, protein solubility/extractability, meat toughness, ageing potential.

    Offer (1991); Farouk and Swan (1998); Farouk and Lovatt (2000); Daly(2005); Bekhit, Farouk, Cassidy, and Gilbert (2007); Lombart et al.(2008); Simmons et al. (2008); Kim, Kerr et al. (2014); Kim, Warneret al. (2014); Warner et al. (2014).

    Poultry Whole-body electricalstunning (10 s, 110 mA, 300 Hz) in a water bathcompared to air pressure stunning (0.5 s, 2 atm)

    Air pressure stunning resulted in rate of pH decline and hemorrhage scores inbreast (48.5%) and thigh meat (43.8%).

    Redder meat was found with air pressure stunning.

    Lambooij et al. (1999).

    Electrical whole-body and head-only stunning withdifferent voltages (25 vs. 100 V) and frequencies (50vs. 200 Hz), and mechanical captive bolt stunning

    No differences in ultimate pH were found. Head-only stunning resulted in darker and redder breast muscles compared withwhole-body stunning.

    Head-only and captive bolt stunning resulted in less hemorrhages in breastcompared with whole-body stunning.

    Hillebrand et al. (1996).

    Whole body, head only, captive bolt, and gas stunning(CO2 and argon)

    14%, 44.9%, 56.1% and 53.4% reduction in hemorrhage score due to the use of headonly (100 V, 50 Hz, 4 s), captive bolt, CO2 and argon, respectively compared to bathelectrical stunning (100 V, 50Hz, 4 s).

    Higherwater 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.

    Savenije et al. 2002).

    Lamb Head only electrical stunning (125 V for 10 s). Stunning did not affect pH, color L*, a*, b* values, water holding capacity (WHC) andshear force (SF).

    Vergara and Gallego (2000).

    Industrial stunning Authors' concluded Even low electrical input during immobilization can ade-quately stimulate carcasses and avoid cold shortening.

    Geesink et al. (2001).

    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 at45 min and 24 h were not signicantly different between treatments.

    The amount of blood lost relative to live body weight and the killing-out weresignicantly higher in electrically stunned lambs compared with non-stunnedlambs.

    Velarde et al. (2003).

    Head electrical stunning (ESL; 110 V, 50 Hz for 5 s),CO2 gas stunning (GSL), no stunning (USL)

    The highest pH was found in the USL group whereas the lowest pH decline wasfound in GSL group.

    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.

    Vergara et al. (2005).

    514M.M

    .Farouketal./M

    eatScience98

    (2014)505

    519

  • 515M.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 amper-age on early rigor development and breast meat quality of broilers. Thebirds were assigned to three stunning treatments; 0 (no stun), 50, and125 mA. Results showed that stunning at 50 or 125 mA caused a signif-icantly higher pH values up to 6 h post-mortem; cooking loss wasnot inuenced by stunning treatment but stunning at 125mAproducedsignicantly tougher meat up to 10 h post-mortem thanmeat from un-stunned birds or birds stunned at 50mA. However, the effects of electri-cal stunning on early rigor development disappeared at by 46 h post-mortem.

    4. Pre- and post-slaughter processes and technologies to improvehalal and kosher meat quality

    4.1. Slaughter cut position

    Gregory, Schuster et al. (2012) assessed the time to onset of arrestedblood ow and the size of false aneurysms in the severed carotid arter-ies of 126 cattle during halal slaughter without stunning and found that29% showed early arrest of blood ow and in 6%, both the left and rightcarotid arteries in the same animal were affected. Making the cut in theneck at the rst cervical vertebra instead of the second to fourth cervicalvertebrae reduced the frequency of the false aneurysm formation andthe early arrested blood ow improving bleeding efciency.

    Therefore, in order to bettermeet the halal and kosher requirementsfor proper and complete bleeding of slaughtered animals for the highestmeat spiritual quality, the slaughter position on the neck recommend-ed by Gregory, Schuster et al. (2012); Gregory, von Wenlawowicz et al.(2012) should be considered for adoption in the halal and kosher indus-trial meat production, once it is conrmed that the suggested position isnot 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 wasdescribed by Simons et al. (2006). The HFST uses similar voltage andamperes settings as the Jarvis traditional head-only electrical stunningbut uses higher frequencies (10002000 Hz) with a square ratherthan sinusoidal waveform. The settings used in the traditional systemwhen applied to full animal body will stop the heart but the modiedsystemat higher frequency does not and thus can be applied fromeitherhead to leg, head to belly or head-to-back instead of head-only in use inthe traditional system (Farouk, 2013).

    The ability of high-frequency electrical stunning not to cause cardiacarrest makes it acceptable in halal slaughter by some adherents ofIslamic faith (Farouk, 2013). In addition, high-frequency stunning hasbeen shown to enhance bleeding efciency andmeat quality and reducecarcass damage (Gregory, 2005; Simons et al., 2006).

    The physiological basis for stunning using high-frequency wave-forms was discussed by Daly (2005). High-frequency currents owclose to the surface of a conductor hence may produce a less severemuscular spasm at the beginning of the current ow (Gregory,Wilkins, &Wotton, 1991). Passing a high-frequency waveform throughthe body of an animal can create the spinal inhibition of the seizuremovement without ventricular brillation. Animals subjected to high-frequency stunning are less likely to suffer muscle contraction, musclehemorrhages and broken bones (Hillebrand, Lambooy, & Veerkamp,1996; McNeal et al., 2003; Simons et al., 2006). In bids the major com-mercial importance of high-frequency electrical stunning is reductionin the incidence of carcass hemorrhages and blood spots (Gregory,2005) and lower blood retention in the visceral which could increasethe yield of trimmed livers for foie gras production (Turcsn et al.,

    2003). Frequencies N600Hz fail to create ventricularbrillation keepinghead-to-leg pathway normal but minimized seizures (Gregory et al.,1991). It was observed that a frequency of 300 Hz caused cardiac arrestin 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 re-duced engorged wing and pectoral veins, and wing hemorrhages whenbirds were subjected to high-frequency (1400 Hz) stunning. Prinz(2009) reviewed a number of studies relating to carcass characteristicsand meat quality assessment of poultry subjected to electrical water-bath stunning at high frequencies and concluded that a signicantlylower occurrence of broken bones and breast meat hemorrhages wasobserved in broilers stunned with a sine wave AC of 1500 Hz comparedto 50 Hz. The ndings of Fernandez et al. (2003) showed that petechialhemorrhages in the breast muscle were absent in non-stunned geeseand those stunned at high frequency (1200 Hz) compared to low fre-quency (50 Hz) where 55% of geese showed the defect.

    Bleeding efciency was higher and the incidence of cardiac arrestwas lower with high-frequency stunning (Mouchoniere et al., 1999).Similarly, Contreras and Beraquet (2001) reported higher blood losswhen birds were subjected to frequency of 1000 Hz compared tothose subjected to lower frequencies.

    Xu et al. (2011) reported a signicantly lower shear force andcooking loss in broiler chickens subjected to high-frequency (400 and1000 Hz) electrical stunning compared to low frequency (160 Hz).The authors attributed the lower tenderness of birds subjected to160 Hz to higher concentration of glycogen observed in the birds. Sim-ilarly, Choe et al. (2008) indicated a reduced glycogen concentration fol-lowing a stun with high frequencies (400 and 1000 Hz) which resultedin reduced drip loss and meat paleness.

    4.3. Controlled/modied and low atmosphere pressure stunning

    In modied atmosphere stunning (MAS) livestock are exposed tocarbon dioxide (CO2) in pits, tunnels, containers or sealed buildings,sometimes in two phases where livestock are successively exposed toa gas mixture containing up to 40% CO2 by volume in air, followed bya higher concentration of CO2 after the animals have lost consciousness.Alternatively the CO2 is mixed with inert gases such as argon, nitrogenor helium to promote anoxia, or inert gases are used exclusively (EFSAAHAW, 2013). Low atmospheric pressure stunning is a method ofstunning that renders livestock unconscious by gradually reducing theoxygen tension in the atmosphere to achieve progressive hypoxia(EFSA AHAW, 2013). The exposure of livestock to gas mixtures or lowatmospheric pressure causes loss of consciousness and sensibility dueto the inhibition of brain function. MAS methods are widely used forstunning pigs and poultry.

    The issues associated with the use of MAS in poultry were recentlyreviewed (Joseph et al., 2013; Raj, 2006). There is not enough workdone on the use of MAS in the reversible stunning of livestock forhalal and kosher meat production to enable the full assessment of thepotential of the methods as alternative to the reversible electrical andmechanical 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 throughthe vascular system of cattle and sheep carcasses during slaughter. Itreduces the amount of residual blood in meat (Farouk, Price, Salih, &Burnett, 1992; Feirtag & Pullen, 2003). This may aid the process ofkoshering and potentially could reduce the amount of surface saltingrequired during the koshering process and the attendant consequencesof the salt on meat quality.

    The removal of residual blood from carcasses resulted in lighter col-ored 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) 505519technology has also been shown to signicantly reduce the number ofmicroorganisms, particularly coliforms and generic E. coli on cattle car-casses. The efcacy of the system in improving the microbial contami-nation of cattle carcasses was investigated and it was found that thesystem reduced aerobicmicroorganisms on rinsed carcasses by 40%; co-liforms 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-slaughterstunning technologies for livestock with the potential to minimizemeat quality problems. For example microwave energy may reduce themuscle spasm associated with mechanical and electrical methods(Small, McLean, Keates, Owen, & Ralph, 2013). Robins, Pleiter, Latter,and Phillips (2014) developed a new systemof reversible electrical stun-ning using a single pulse of ultra-high current (5000 V, 70 A, 50 msec)that eliminated post-stun grand mal seizures and its associated negativeconsequences on meat quality such as ecchymosis. However, thesetechnologies need to be validated and optimized before they can beimplemented for industrial meat production.

    5. Conclusions

    A substantial quantity of meat is produced around the world usinghalal and kosher slaughter methods and associated processes. There-fore, it is important that the quality of that meat is given due attention.The conventionally dened attributes of meat quality are demanded byhalal, kosher and conventional consumers alike. However, an additionalattribute of spiritual quality is paramount for those who consumehalal and kosher for religious reasons. A number of meat quality prob-lems including different forms of hemorrhages in the muscles and or-gans of livestock; carcass damage; broken bones; poor color stability;reduced ageing potential; increased drip loss, etcetera are associatedwith the use of pre-slaughter stunning and accompanying practices.These issues are rarely encountered in carcasses of non-stunnedanimals. Although slaughter without pre-stunning is used in halal andkoshermeat production and the practiceminimizesmeat quality issues,nonetheless, it has the potential to compromise animal welfare atslaughter if not carefully and conscientiously applied. The practice haspitched the proponents and opponents of stunning into a dogmaticargument that is surreptitiously turning into a human versus animalrights and/or religion versus science public debate. This detracts fromthe main issue of the ethical, sustainable and humane production ofwholesome meat for its tumultuous lovers around the globe. This re-view called on both sides of the stunning debate to resort to dialogue,if meat of high spiritual and conventional quality is to be producedand the welfare of the animal at slaughter is to be consistentlyprotected.

    Acknowledgments

    The principal author acknowledges the support provided throughAgResearch MBIE core funding contract no. A19113 that enabled thisreview to be realized, and Drs Scott O. Knowles and Cameron Craigieof 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. BritishPoultry Science, 48, 406423.

    Agbeniga, B. (2012). Inuence of conventional and Kosher slaughter techniques in cattle on car-cass andmeat quality. (M.Sc. Thesis). Pretoria, SouthAfrica: University of Pretoria (http://www.repository.up.ac.za/bitstream/handle/2263/26243/dissertation.pdf?sequence=1Accessed 16 February 2014).Agbeniga, B., &Webb, E. C. (2012). Effect of slaughter technique on bleed-out, blood in thetrachea and blood splash in the lungs of cattle. South African Journal of Animal Science,42, 524529.

    Agbeniga, B., Webb, E. C., & O'Neil, H. A. (2013). Inuence of kosher (shechita) andconventional slaughter techniques on shear force, drip and cooking loss of beef.South African Journal of Animal Science, 43, S98S102.

    Ahmad, H. (2007). Investigations on Halal slaughter in the light of religion and science.Unpublished Report. Meat Research Laboratory, Pakistan Council of Scientic &Industrial Research (PCSIR) Laboratories Complex, Lahore, Pakistan.

    Ahmed, A. (2008). Marketing of halal meat in the United Kingdom supermarkets versuslocal shops. British Food Journal, 110, 655670.

    Alayash, A. I., Patel, R. P., & Cashon, R. E. (2001). Review: Redox reactions of haemoglobinand myoglobin: Biological and toxicological implications. Antioxidants and RedoxSignaling, 3, 313327.

    Ali, A., Lawson, M.A., Tauson, A. -H., Jensen, J. F., & Chwalibog, A. (2007). Inuence ofelectrical stunning voltages on bleed out and carcass quality in slaughtered broilerchickens. Archiv fuer Geuegelkunde, 71, 3540.

    Al-Qaradawi, Y. (1960). The lawful and the prohibited in Islam (Al-Halal Wal Haram FilIslam). Indianapolis, IN. USA: American Trust Publications.

    Alvarado, C. Z., Richards, M. P., O'Keefe, S. F., & Wang, H. (2007). The effect of bloodremoval on oxidation and shelf life of broiler breast meat. Poultry Science, 86(1),156161.

    Angel, S., Weinberg, Z. G., & Jaffe, R. (1989). Salt content of kosher chicken parts studiesunder controlled conditions. Journal of Food Quality, 11, 365373.

    Anil, M. H., Love, S., Helps, C. R., & Harbour, D. A. (2002). Potential for carcass contamina-tion with brain tissue following stunning and slaughter in cattle and sheep. FoodControl, 13, 431436.

    Anil, M. H., Yesildere, T., Aksu, H., Matur, E., McKinstry, J. L., Erdogan, O., Hughes, S., &Mason, C. (2004). Comparison of religious slaughter of sheep with methods that in-clude pre-slaughter stunning, and the lack of differences in exsanguination, packedcell volume and meat quality parameters. Animal Welfare, 13, 387392.

    Anil, M. H., Yesildere, T., Aksu, H., Matur, E., McKinstry, J. L., Erdogan, O., Hughes, S., &Mason, C. (2006). Comparison of halal slaughter with captive bolt stunning andneck cutting in cattle: Exsanguination and quality parameters. Animal Welfare, 15,325330.

    Asghar, A., Torres, E., Gray, J. I., & Pearson, A.M. (1990). The effect of salt onmyoglobin de-rivatives in the sarcoplasmic extract from pre-and post-rigor beef in the presence orabsence of mitochondria and microcosms. Meat Science, 27, 197209.

    Bainbridge, W. S. (2004). Religion and science. Futures, 36, 10091023.Bakar, O. (2005). Glen on religion and science: A theological perspective. The Muslim

    World, 95, 359372.Baron, C. P., Skibsted, L. H., & Andersen, H. J. (1997). Pro-oxidative activity of myoglobin

    species in linoleic acid emulsions. Journal of Agricultural and Food Chemistry, 45,17041710.

    Bekhit, A. E. D., Farouk, M. M., Cassidy, L., & Gilbert, K. V. (2007). Effects of rigor temper-ature and electrical stimulation on venison quality. Meat Science, 75, 564574.

    Bekhit, A. E. D., Hopkins, D. L., Fahri, F. T., & Ponnampalam, E. N. (2013). Oxidative process-es in muscle systems and fresh meat: Sources, markers and remedies. ComprehensiveReviews in Food Science and Food Safety, 12, 565597.

    Berg, C., Nordensten, C., Hultgren, J., & Algers, B. (2012). The effect of stun duration andlevel of applied current on stun and meat quality of electrically stunned lambsunder commercial conditions. Animal Welfare, 21, 131138.

    Carlsen, C. U., Moller, J. K. S., & Skibsted, L. H. (2005). Haem iron in lipid oxidation.Coordination Chemistry Reviews, 249, 485498.

    Che Man, Y. B., & Sazili, A. Q. (2010). Food production from the halal perspective. InIsabel-Guerrero-Legarreta (Ed.), Handbook of Poultry Science and Technology:Primary Processing, Vol. 1. (pp. 183215)New Jersey, USA: John Wiley & Sons, Inc.

    Choe, J. H., Choi, Y. M., Lee, S. H., Shin, H. G., Ryu, Y. C., Hong, K. C., & Kim, B. C. (2008). Therelation between glycogen, lactate content and muscle ber type composition, andtheir inuence on postmortem glycolytic rate and pork quality. Meat Science, 80,355362.

    Chowdhury, A.M., Helman, C., & Greenhalgh, T. (2000). Food beliefs and practices amongBritish Bangladeshis with diabetes: Implications for health education. Anthropologyand Medicine, 7, 209226.

    Chrystall, B. B., Devine, C. E., & Newton, K. G. (1981). Residual blood in lambmuscles.MeatScience, 5, 339345.

    Cohen, E., Schwartz, Z., Antonovski, R., & Saguy, S. (2002). Consumer perceptions ofkosher products. Journal of Foodservice Business Research, 5, 6988.

    Contreras, C. C., & Beraquet, N. J. (2001). Electrical stunning, hot boning, and quality ofchicken breast meat. Poultry Science, 80, 501507.

    Cross, A. J., Pollock, J. R. A., & Bingham, S. A. (2003). Haem, not protein or inorganic iron, isresponsible for endogenous intestinal N-nitrosation arising from red meat. CancerResearch, 63, 23582360.

    D'Agata, M., Russo, C., & Preziuso, G. (2009). Effect of Islamic ritual slaughter on beefquality. Italian Journal of Animal Science, 8, 489491.

    Daly, C. C. (2005). The use of alternative electrical frequencies for stunning of livestockbefore religious slaughter. Animal Welfare at Ritual Slaughter. InternationaleFachtagung des Instituts fr Tieschutz und Tierverhalten/FU Berlin (pp. 7784).

    Davis, K. (1996). Prisoned chickens, poisoned eggs: An inside look at the modern poultryindustry. Summertown, Tennessee, USA: Book Publishing Company, 105124.

    Devine, C. E., Gilbert, K. V., & Ellery, S. (1983). Electrical stunning of lambs: The effect ofstunning parameters and drugs affecting blood ow and behaviour on petechialhaemorrhage incidence. Meat Science, 9, 247256.

    Devine, C. E., Tavener, A., Gilbert, K. V., & Day, A.M. (1986). Electroencephalographic stud-ies of adult cattle associated with electrical stunning, throat cutting and carcasselectro-immobilisation. New Zealand Veterinary Journal, 34, 210213.

  • 517M.M. Farouk et al. / Meat Science 98 (2014) 505519Dunn, C. (1990). Stress reactions of cattle undergoing ritual slaughter using two methodsof restraint. Veterinary Record, 126, 522525.

    EFSA AHAW Panel (EFSA Panel on Animal health and Welfare (2013). Guidance on theassessment criteria for studies evaluating the effectiveness of stunning methodsregarding animal protection at the time of killing. EFSA Journal, 11(12), 3486.

    Ewbank, R., Parker, M. J., & Mason, C. W. (1992). Reactions of cattle to head restraint atstunning: A practical dilemma. Animal Welfare, 1, 5563.

    Farouk, M.M. (2013). Advances in the industrial production of halal and kosher red meat.Meat Science, 95, 805820.

    Farouk, M. M., Beggan, M., Hafejee, I. I., Freke, C., & Bekhit, A. E. D. (2007). Manufacturingfunctionality of chilled venison and beef. Journal of Food Quality, 30, 764782.

    Farouk, M. M., & Lovatt, S. J. (2000). Initial chilling rate of pre-rigor beef muscles as anindicator of colour of thawed meat. Meat Science, 56, 139144.

    Farouk, M. M., & Price, J. F. (1994). The effect of post-exsanguination infusion on the com-position, exudation, color and post-mortemmetabolic changes in lamb.Meat Science,38, 477496.

    Farouk, M. M., Price, J. F., Salih, A.M., & Burnett, R. J. (1992). The effect of post-exsanguination infusion of beef on composition, tenderness and functional proper-ties. Journal of Animal Science, 70, 27732778.

    Farouk, M. M., & Swan, J. E. (1998). Effects of rigor temperature and frozen storageon functional properties of hot-boned manufacturing beef. Meat Science, 49(2),233247.

    Feirtag, J. M., & Pullen, M. M. (2003). A novel intervention for the reduction of bacteria onbeef carcasses. Food Protection Trends, 23(7), 558562.

    Fernandez, X., Leprettre, S., Dubois, J. -P., Auvergne, A., & Babile, R. (2003). The inu-ence of current parameters during the water-bath stunning of overfed geese(Anser anser) on blood loss and on fatty liver and meat downgrading. AnimalResearch, 52, 383397.

    Fernandez, X., Lahirigoyen, E., Auvergne, A., Molette, C., & Bouillier-Oudot, M. (2010). Theeffects of stunningmethods on product qualities in force-fed ducks and geese. 1. Car-cass downgrading and meat quality. Animal, 4(1), 128138.

    Fernndez-Lpez, J., Sendra-Nadal, E., & Sayas-Barber, E. (2010). Slaughtering equipmentand operation. In Isabel-Guerrero-Legarreta (Ed.), Handbook of Poultry Science andTechnology: Primary Processing, Vol. 1. (pp. 79100)New Jersey, USA: John Wiley &Sons, Inc.

    Fletcher, D. L. (1993). Stunning of broilers. Broiler Industry, 56, 4046.French, R.W., & Callender, G. R. (1962). Ballistic characteristics of wounding agents. In J. B.

    Coates, & J. C. Beyer (Eds.), Wound ballistics. Medical Department US Army. O.ce of theSurgeon General (pp. 91141). Washington, USA: Department of the Army.

    Fulton, G. P., & Berman, H. J. (1964). The defective vascular wall as a factor in bleeding.Annals of the New York Academy of Sciences, 115, 5666.

    Geesink, G. H., Mareko, M. H. D., Morton, J. D., & Bickerstaffe, R. (2001). Electrical stimu-lation-when more is less. Meat Science, 57, 145151.

    Gilbert, K. V. (1993). Electrical stunning and slaughter in New Zealand. MIRINZ TechnicalReport 908. Hamilton, New Zealand: AgResearch Ltd.

    Gilbert, K. V., & Devine, C. E. (1982). Effect of electrical stunning methods on petechialhaemorrhages and on the blood pressure of lambs. Meat Science, 7, 197207.

    Grandin, T. (2003). Stunning options. Meat & Poultry(October), 118.Grandin, T. (2010). Auditing animal welfare at slaughter plants. Meat Science, 86, 5665.Grandin, T. (2013). Evaluation of methods of restraint for holding (xation) of cattle,

    calves, and sheep for Kosher and Halal slaughter. http://www.grandin.com/ritual/evaluation.restraint.methods.kosher.halal.html (Accessed 6 March 2014)

    Grandin, T., & Regenstein, J. M. (1994). Religious slaughter and animal welfare: A discus-sion for meat scientists. Meat Focus International, 3, 115123.

    Gregory, N. G. (1998). Animal Welfare and Meat Science. Oxon, UK: CABI Publishing,223253.

    Gregory, N. G. (2005). Recent concerns about stunning and slaughter. Meat Science, 70,481491.

    Gregory, N. G. (2007). Animal welfare and meat production (2nd ed.) Wallingford, UK:CABI Publishing, 213226.

    Gregory, N. G., Schuster, P., Mirabito, L., Kolesar, R., & McManus, T. (2012). Arrested bloodow during false aneurysm formation in the carotid arteries of cattle slaughteredwith and without stunning. Meat Science, 90, 368372.

    Gregory, N. G., von Wenlawowicz, M., von Holleben, K., Fielding, H. R., Gibson, T. J.,Mirabito, L., & Kolesar, R. (2012). Complication during shechita and halal slaughterwithout stunning in cattle. Animal Welfare, 21(s2), 8186.

    Gregory, N. G., & Wilkins, L. J. (1989). Effect of stunning current on down grading inturkeys. British Poultry Science, 30, 761764.

    Gregory, N. G., Wilkins, L. J., & Wotton, S. B. (1991). Effect of electrical stunning frequencyon ventricular brillation, downgrading and broken bones in broilers, hens andquails. British Veterinary Journal, 14, 7177.

    Gregory, N. G., & Wotton, S. B. (1984). Sheep slaughtering procedures. II. Time to loss ofbrain responsiveness after exsanguinations or cardiac arrest. British VeterinaryJournal, 140, 354360.

    Grunert, K. G. (1997). What's in a steak? A cross-cultural study on the quality perceptionof beef. Food Quality and Preference, 8(3), 157174.

    Grunert, K. G., Bredahl, L., & Bruns, K. (2004). Consumer perception of meat quality andimplications for product development in the meat sector-a review. Meat Science, 66,259272.

    Hajmmer, M. N., Marsden, J. L., Crozier-Dodson, B.A., Basheer, I. A., & Higgins, J. J. (1999).Reduction of microbial counts at a commercial beef koshering facility. Journal of FoodScience, 64, 719723.

    Hanzaee, K. H., & Ramezani, M. R. (2011). Intention to halal products in the worldmarkets. Interdisciplinary Journal of Research in Business, 1, 17.

    Harper, C. T. (2001). Book reviews. Why science and religion need to talk humanfallenness, freedom and pain are the preserve of both arenas. Nature, 411, 239240.Hassin, G. B. (1933). Changes in the brain in legal electrocution. Archives of Neurology andPsychiatry, 30, 10461060.

    Henriksen, J. (2008). Review of the spiritual dimension. Religion, philosophy and humanvalue, 8. (pp. 113114)Ars Disputandi, 113114 (http://www.ArsDisputandi.org).

    Hillebrand, S. J. W., Lambooy, E., & Veerkamp, C. H. (1996). The effects of alternativeelectrical and mechanical stunning methods on haemorrhaging and meat quality ofbroiler breast and thigh muscles. Poultry Science, 75, 664671.

    Hindle, V., Lambooij, E., Reimert, H., Workel, L., & Gerritzen, M. (2010). Animal welfareconcerns during the use of the water bath for stunning broilers, hens, and ducks.Poultry Science, 89, 401412.

    Holzer, Z., Berry, B. W., Campbell, A.M., Spanier, A.M., & Solomon, M. B. (2004). Effect ofkoshering and hydronynamic pressure on beef colour, odor, and microbial loads.Journal of Muscle Foods, 15, 6982.

    Hopkins, D. L., Shaw, F. D., Baud, S., & Walker, P. J. (2006). Electrical currents applied tolamb carcasses-effects on blood release and meat quality. Australian Journal ofExperimental Agriculture, 2006(46), 885889.

    Hunt, M. C., Schoenbeck, J. J., Yancey, E. J., Dikeman, M. E., Loughin, T. M., & Addis, P. B.(2003). Effect of post-exsanguination vascular infusion of carcasses with calciumchloride or a solution of saccharides, sodium chloride, and phosphates on beefdisplay-color stability. Journal of Animal Science, 81, 669675.

    Ito, Y., Tatsumi, R., Wakamatsu, J. -I., Nishimura, T., & Akihito Hattori, A. (2003). Thesolubilization of myobrillar proteins of vertebrate skeletal muscle in water. AnimalScience Journal, 74, 417425.

    Jacob, R. H., & Hopkins, D. L. (2014). Techniques to reduce the temperature of beefmuscle early in the post-mortem period - a review. Animal Production Science, 54,482493.

    Joo, S., & Kim, G. (2011). Meat quality traits and control technologies. In Seon-Tea Joo(Ed.), Control of Meat Quality (pp. 129). T.C., Kerala, India: Research Signpost.

    Joseph, P., Schilling, M. W., Williams, J. B., Radhakrishnan, V., Battula, V., Christensen, K.,Vizzier-Thaxton, Y., & Schmidt, T. B. (2013). Broiler stunning methods and their ef-fects on welfare, rigor mortis, and meat quality. World's Poultry Science Journal, 69,99112.

    Kannan, G., Heath, J. L., Wabeck, C. J., & Mench, J. A. (1997). Shackling of broilers: Effectson stress responses and breast meat quality. British Poultry Science, 38(4), 323332.

    Kanner, J., Harel, S., & Jaffe, R. (1991). Lipid peroxidation of muscle foods as affected byNaCl. Journal of Agriculture and Food Chemistry, 32, 370376.

    Kettlewell, P. J., & Hallworth, R. N. (1990). Electrical stunning of chickens. Journal ofAgricultural Engineering Research, 47, 139151.

    Kim, Y. H. B., Kerr, M., Geesink, G., &Warner, R. D. (2014). Impacts of hangingmethod andhigh pre-rigor temperature and duration on quality attributes of ovine muscles.Animal Production Science, 54, 414421.

    Kim, Y. H. B., Warner, R. D., & Rosenvold, K. (2014). Inuence of high pre-rigor tempera-ture and fast pH fall on muscle proteins and meat quality: A review. AnimalProduction Science, 54, 375395.

    Kirton, A. H., Bishop, W. H., Mullord, M. M., & Frazerhurst, L. F. (1978). Relationshipsbetween time of stunning and time of throat cutting and their effect on bloodpressure and blood splash in lambs. Meat Science, 2, 199206.

    Kirton, A. H., Frazerhurst, L. F., Bishop, W. H., & Winn, G. W. (1980-81). A comparison ofthe effect s of electrical, captive bolt or percussion stunning on the incidence ofblood splash in lambs. Meat Science, 2, 407411.

    Kirton, A. H., Frazerhurst, L. F., Woods, E. G., & Chrystall, B. B. (1980-81). Effect of electricalstunning method and cardiac arrest on bleeding efciency, residual blood and bloodsplash in lambs. Meat Science, 5, 347353.

    Koorts, R. (1991). The development of a restraining system to accommodate the Jewishmethod of slaughter (shechita). M. Dip. Tech., Technikon Witwatersrand Johannesburg(pp. 7281).

    Korzen, S., & Lassen, J. (2010). Meat in context. On the relation between perception andcontexts. Appetite, 54(2), 274281.

    Krystallis, A., Chryssochoidis, G., & Scholderer, J. (2007). Consumer perceived quality intraditional food chains: The case of the Greek meat supply chain. Appetite, 48(1),5468.

    Lambooij, E., Pieterse, C., Hillebrand, S., & Dijksterhuis, G. (1999). The effects of captivebolt and electrical stunning, and restraining methods on broiler meat quality.Poultry Science, 78, 600607.

    Lambooij, E., van der Werf, J. T. N., Reimert, H. G. M., & Hindle, V. A. (2012). Restrainingand neck cutting or stunning and neck cutting of veal calves.Meat Science, 91, 2228.

    Lapidot, T., Granit, R., & Kanner, J. (2005). Lipid peroxidation by free iron ions and myo-globin as affected by dietary antioxidants in simulated gastric uids. Journal ofAgricultural and Food Chemistry, 53, 33833390.

    Leal-Ramos, M., Alarcon-Rojo, A. D., Mason, T. J., Paniwnyk, L., & Alarjah, M. (2011). Ultra-sound-enhanced mass transfer in Halal compared with non-Halal chicken. Journal ofthe Science of Food and Agriculture, 91, 130133.

    Leet, N. G., Devine, C. E., & Gavey, A.B. (1997). The histology of blood splash in lambs.MeatScience, 1, 229234.

    Linares, M. B., Bornez, R., & Vergara, H. (2007). Effect of different stuning systems onmeatquality of light lamb. Meat Science, 76, 675681.

    Lines, J. A., Wotton, S. B., Barker, R., Spence, J., Wilkins, L., & Knowles, T. G. (2011). Broilercarcass quality using head-only electrical stunning in a waterbath. Bristish PoultryScience, 52(4), 439445.

    Littin, K. E. (2004). The behaviour, pathophysiology and pathology of brushtail possums(Trichosurus vulpecula) poisoned with 1080 or brodifacoum, and the implications forpossum welfare. (PhD thesis). New Zealand: Massey University.

    Lombart, A.C., Johnson, N. V., McGurk, J. M., Cummings, T. L., Daly, C. C., & Simmons, N. J.(2008). The effect of different electrical immobilisation and stimulation procedureson meat quality. 54th International Congress of Meat Science and Technology (ICoMST),10 - 15 August, Cape Town, South Africa (http://www.icomst.helsinki./ICoMST2008).

  • 518 M.M. Farouk et al. / Meat Science 98 (2014) 505519Lpez, M., Carrilho, M., Campo, M., Lafuente, R., Xicato, G., Trocino, A., & Lukefahr, S.(2008). Halal slaughter and electrical stunning in rabbits: Effect on welfare andmuscle characteristics. Proceedings of the 9th World Rabbit Congress, Verona, Italy,10-13 June 2008 (pp. 12011206). World Rabbit Science Association.

    Mast, M., &Macneil, J. (1983). Effect of kosher vs conventional processing on yield quality,and acceptability of broiler chickens. Journal of Food Science, 48, 10131015.

    McClements, J.D., & Decker, E. A. (2008). Chapter 4: Lipids. In S. Damodaran, K. L. Parkin, &O. R. Fennema (Eds.), Fennema's food chemistry (pp. 187195) (4th ed.). Boca Raton,Florida: CRC Press (198-206).

    McKeegan, D. E. F., Abeyesinghe, S. M., McLema