Progress in reducing the pale, soft and exudative (PSE) problem in pork and poultry meat

Available online at www.sciencedirect.com

MEAT SCIENCE Meat Science 79 (2008) 46–63 www.elsevier.com/locate/meatsci

Progress in reducing the pale, soft and exudative (PSE) problem in pork and poultry meat S. Barbut

a,*

, A.A. Sosnicki b, S.M. Lonergan c, T. Knapp d, D.C. Ciobanu b, L.J. Gatcliffe e, E. Huff-Lonergan c, E.W. Wilson b a

e

Food Science, University of Guelph, Guelph, Ont., Canada N1G 2W1 b Genus/PIC, Franklin, KY 42135, USA c Animal Science, Iowa State University, Ames, IA 50011, USA d Nicholas Turkeys, P.O. Box 964, US Route 60 West, Lewisburg, WV 24901, USA British United Turkeys, Chowley Five, Chowley Oak Business Park, Tattenhall, Cheshire CH3 9GA, UK Received 1 March 2007; received in revised form 25 July 2007; accepted 27 July 2007

Abstract Research in the area of the pale, soft and exudative (PSE) pork and poultry meat is reviewed in this article with an emphasis on genetic, biochemical and metabolic factors contributing to the problem. Over the past five decades, there has been much more work in the pork meat area where a few genetic markers have been identified, and are currently used to remove susceptible animals from the herd. Some of the markers are linked to aberrant calcium regulation in the early postmortem muscle. The poultry industry is still not at the point of using genetic marker(s); however, some recent work has revealed several potential markers. The review also discusses environmental factors such as antemortem stress and early postmortem processing practices (e.g. chilling rate) that can influence the development and severity of the PSE phenomenon. Some of these factors are known to cause protein denaturation at the early stage of postmortem and directly contribute to poor water-holding capacity and inferior texture in fresh meat and later in processed products. A newer hypothesis suggesting that variation in protein oxidation, in response to antemortem stress and early postmortem tissue environment, can contribute to development of PSE pork is also discussed. Finally, a few recommendations for future work are proposed.  2007 Elsevier Ltd. All rights reserved. Keywords: Chicken; Genetic; Halothane; Meat; Pig; Pork; Poultry; PSE; PSS; Review; Ryanodine

1. Introduction Methods to add value to meat animal products such as selection, feeding, animal husbandry and product processing have been employed for many years. For the most part, selection of animals (e.g. pigs, poultry, cattle) within lines and between lines (crossbreeding) has been a very common procedure for genetically improving traits of economic importance to the meat industry. For producers, production traits such as growth rate, feed conversion, and carcass leanness are of great economic importance. Traits of eco*

Corresponding author. Tel.: +1 519 824 4120. E-mail address: [email protected] (S. Barbut).

0309-1740/$ - see front matter  2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.meatsci.2007.07.031

nomic importance for processors include carcass weight, carcass leanness, proportion of certain primal/sub-primal cuts and processing yields. In recent years, as processors have moved from offering ‘‘commodity pork/poultry’’ to branded products, meat quality has become more economically important. Thus, as a response to the growing meat quality demands of the consumer, the entire meat industry – from live animal genetics to consumer research – has taken several steps to further improve meat tenderness, juiciness, flavor and reduce and/or eliminate pale, soft, exudative (PSE) meat conditions. The latter is especially true in the pig industry where a few genetic markers have been identified and routinely used to remove animals susceptible to the PSE condition. An example is a recent survey of the

S. Barbut et al. / Meat Science 79 (2008) 46–63

US pork industry presented at the 2006 Mid-West meeting of the Animal Society of Animal Science indicated that only: ‘‘3.34% of loins exhibit all three conditions of classic PSE, reporting a range from 0.1% to 10%’’ (Meisinger & Berg, 2006). The poultry industry has not yet identified genetic marker(s) that can be used on a commercial scale for such a selection program; however, progress in this direction is starting to become evident. 2. Factors that contribute to PSE pork Investigation of the factors underlying the development of pale, soft and exudative (PSE) pork date back many years (Briskey, 1959; Briskey & Wismer-Pedersen, 1961a, 1961b, 1961c; Kastenschmidt, Hoekstra, & Briskey, 1966) This is testimony to the persistence of the problem and to the elusiveness of a sustainable solution to the problem. It is generally accepted that the rate of postmortem metabolism is the major contributor to the variation in fresh pork quality and processing functionality of meat proteins. This loss of product and protein quality is attributed to protein denaturation caused by a combination of acidic conditions along with high muscle temperature in very early postmortem muscle. A major contributor to the development of extreme cases of PSE in pork is the syndrome once characterized as ‘‘Porcine Stress Syndrome’’. Pigs with porcine stress syndrome were recognized to be at significant risk to produce PSE pork (Topel, Bicknell, Preston, Christian, & Matsushima, 1969). The well-established PSS condition is known to be linked to a single autosomal recessive gene. This gene is commonly referred to as the halothane gene because diagnosis of the mutation can be made by exposure to halothane anesthesia (Rasmusen & Christian, 1976). A point mutation in the 615 amino acid (Arg615Cys) of the sarcoplasmic reticulum Ca2+ release channel is responsible for the aberrant calcium metabolism observed in postmortem muscle. In pigs with this mutation, Ca2+ is released from the sarcoplasmic reticulum at a rate that is equivalent to twice that of normal muscle (Cheah & Cheah, 1976; Mickelson & Louis, 1996). Ku¨chenmeister, Kuhn, Wegner, Nu¨rnberg, and Ender (1999) demonstrated that Ca2+ uptake is also diminished in postmortem muscle in pigs with this stress susceptibility. This increase in sarcoplasmic Ca2+ is responsible for activating muscle metabolism and accelerating lactate production and subsequent accumulation in postmortem muscle. With the advent of technologies to identify and eliminate this major cause of extreme cases of PSE, a great reduction in the incidence and severity of PSE has been realized by the industry. However, product with poor water-holding capacity and color is still observed, as previously mentioned. Much of the variation in protein functionality and fresh pork quality can still be linked to variation in early postmortem metabolism. The contributions of pH and temperature to protein denaturation and PSE development are well documented and indisputable

47

(Briskey, 1964). An important observation is that quality features like water-holding capacity can vary so much at intermediate and low pH. This observation suggests that additional factors contribute to variation in pork quality. The primary focus of the remainder of this discussion will be other factors that influence water-holding capacity in fresh pork. With the possible exception of rigor formation, denaturation of myosin is one of the most dramatic early postmortem events in muscle. Penny (1967) demonstrated that myosin ATPase activity is among the first to be altered under pH and temperature conditions that mimic postmortem muscle. Presumably this loss in activity is due to denaturation. Stabursvik, Fretheim, and Frøystein (1984) used differential scanning calorimetry of PSE and normal pork to determine that the HMM portion of myosin, specifically HMM S-1 is denatured in PSE pork. The consequence of denaturation of S-1 portion of myosin is likely an alteration of the rigor bonds and the spacing between filaments within the sarcomere. Indeed, Diesbourg, Swatland, and Millman (1988) used low-angle X-ray diffraction to demonstrate that low pH results in shrinkage of the myofibril and less space between myofilaments. The consequence of myofibrillar shrinkage is an increase in extramyofibrillar space within post-rigor meat and a decrease in the barrier for water to traverse out of the meat during storage. Swatland, Irving, and Millman (1989) used differential interference contrast microscopy to follow the time delays as fluid moved from the myofilament lattice to the intermyofibrillar space and finally to the extracellular space. Myofibrillar shrinkage can also be translated into shrinkage of myofibers (cells) if the intermediate filaments and costameric connections between myofibrils and the sarcolemma are intact. Swatland (1985) showed how lateral cytoskeletal connections between myofibrils were changed during the development of rigor mortis. Having followed myofibrillar shrinkage in pork by electron microscopy, Swatland and Belfry (1985) outlined how shrinkage would be affected by desmin. A current hypothesis proposes that proteolysis of key muscle proteins (including desmin, vinculin and talin) minimizes the loss of water-holding capacity (Huff-Lonergan & Lonergan, 2005; Melody et al., 2004; Morrison, Mielche, & Purslow, 1998;) caused by lateral shrinkage of myofibrils in postmortem muscle. In a sense, early postmortem disruption of linkages between the myofibril and the sarcolemma minimizes the impact of myofibrillar shrinkage on myofiber volume. Because l-calpain is known to degrade intermediate filament proteins and costameric proteins (including desmin, vinculin and talin) in postmortem muscle, it is suggested that factors that regulate calpain activity – calpastatin, pH, and oxidation – can influence water-holding capacity. The calpain system includes two well characterized, ubiquitous proteinases (l- and m-calpain), and an endogenous inhibitor of the calpains, calpastatin. (Goll, Thompson, Li, Wei, & Cong, 2003). Both l- and m-calpain are heterodimers composed of an 80 kDa and a 28 kDa sub-

48

S. Barbut et al. / Meat Science 79 (2008) 46–63

unit (Suzuki, 1990). l-Calpain requires between 5 and 65 lM Ca2+ for half-maximal activity, while m-calpain requires between 300 and 1000 lM Ca2+ for half-maximal activity (Goll, Thompson, Taylor, & Christianson, 1992). These two enzymes cleave the same myofibrillar proteins that are degraded during postmortem aging (Huff-Lonergan et al., 1996; Kendall, Koohmaraie, Arbona, Williams, & Young, 1993) without degrading actin and myosin (Dayton, Goll, Stromer, Robson, & Reville, 1975). Autolysis of l-calpain is considered to be a hallmark for activation of l-calpain in postmortem muscle. It is therefore suggested that a greater proportion of the l-calpain catalytic subunit present as the 76 kDa autolysis product indicates that a greater proportion of l-calpain has been active. A higher proportion of l-calpain catalytic subunit present as the unautolyzed 80 kDa subunit can be interpreted as less calpain has been active. Melody et al. (2004) demonstrated that when limited autolysis had occurred in the first 24 h postmortem, limited degradation of desmin was observed at 24 h postmortem. These same samples exhibited poorer water-holding capacity compared to samples with more evident l-calpain autolysis and degradation of desmin. Zhang, Lonergan, Gardner, and HuffLonergan (2006) reported that l-calpain autolysis, as determined by a decrease in the percent 80 kDa (intact) large subunit and an increase in the percent 76 kDa autolysis product, appears to be hindered by lower pH early postmortem (but not low enough to promote formation of PSE product). Because calpain autolysis is considered to be an indicator of calpain activation in postmortem muscle, the data suggest that lower pH early postmortem will delay activation of l-calpain. In fact, Maddock, Huff-Lonergan, Rowe, and Lonergan (2005) reported a slower rate of activation of l-calpain at pH 6.0 compared to pH 6.5. Gardner, Huff-Lonergan, and Lonergan (2005) used pH decline, temperature decline, desmin degradation and lcalpain autolysis to predict water-holding capacity and determined that pH at 6 h postmortem predicts approximately 34% of the variation in drip loss. Inclusion of 24 h pH and percent of l-calpain large subunit present as the 76 kDa autolysis product (76%) improves the model R2 to 0.483. A negative coefficient for 76% indicates that less autolysis within the first 24 h postmortem tends to predict greater drip loss, even after considering pH at two distinct time points. The first variable to enter the model to predict purge loss was the ratio of intact desmin present at 1 day postmortem. A high proportion of intact desmin predicts greater purge loss. Inclusion of calpain autolysis and desmin degradation measurements in models designed to predict water-holding capacity suggests that proteolysis is more than a response that is dependent on pH decline, but may have a direct influence on meat water-holding capacity and tenderness. Conditions that promote production of PSE pork are known to have specific negative effects on proteolysis of specific muscle proteins. Boles, Parrish, Huiatt, and Rob-

son (1992) reported a slower rate of postmortem proteolysis of titin in PSE pork. This likely contributes to the inferior tenderness that is often observed in PSE pork (Boles, Parrish, Skaggs, & Christian, 1991). The explanation for this limited degradation is rapid autolysis and inactivation of l-calpain. Fig. 1 makes a comparison between normal and PSE pork. The normal pork loin had higher pH at 45 min and 6 h postmortem. Not surprisingly, the normal pork loin had lower shear force and lower drip loss. The striking difference in the protein profile of the product demonstrates the possible role of proteolysis in formation of PSE pork. Fig. 1 illustrates that at 45 min postmortem, there is very little difference in l-calpain activity measured on a casein zymogram (Raser, Posner, & Wang, 1995). It follows that no difference in titin degradation is observed at 45 min postmortem. However, by 6 h postmortem, lcalpain activity was not detected in the low PSE product. It is also clear that once the l-calpain is inactivated, little proteolysis occurs as at 120 h postmortem intact titin (T1) was degraded in the normal sample, but remained undegraded in the product with the rapid pH decline. Calpastatin, the endogenous inhibitor of the calpain enzymes, has been found in all the tissues that contain calpains. Interestingly, calpastatin requires calcium to bind calpain. The amount of calcium required to allow halfmaximal binding of calpastatin to calpains is generally lower than that required for half-maximal activity of the unautolyzed and autolyzed forms of m-calpain and l-calpain (Kapprell & Goll, 1989). High calpastatin activity has been associated with limited degradation of muscle proteins in beef (Lonergan, Huff-Lonergan, Wiegand, & Kriese-Anderson, 2001a), pork (Lonergan, Huff-Lonergan, Rowe, Kuhlers, & Jungst, 2001b) and lamb (Koohmaraie, Shackelford, Wheeler, Lonergan, & Doumit, 1995). The nature of calpastatin inhibition of calpains is not yet well characterized. A broad range of molecular weight in calpastatin has been attributed both to proteolysis and alternative splicing. Furthermore, phosphorylation of calpastatin (Adachi et al., 1991) changes specificity of inhibition of calpains (Pontremoli et al., 1991) and solubility of calpastatin (Averna et al., 2001). The molecular diversity of calpastatin may hold important information regarding how it regulates calpain-mediated events. Recent research demonstrates that mutations within the coding region of the calpastatin gene influence meat quality (Ciobanu et al., 2004). A relatively new observation is that oxidation can inhibit postmortem proteolysis of meat proteins. Oxidation of proteins is a normal physiological response within living tissues. It is also clear that proteins are susceptible to oxidation in postmortem muscle. This is often documented by a decrease in free sulfhydryl concentration or an increase in carbonyl content of proteins (Rowe, Maddock, Lonergan, & Huff-Lonergan, 2004a). Oxidation of l-calpain in solution with hydrogen peroxide inhibits activation and cleavage of desmin (Carlin, Huff-Lonergan, Rowe, & Lonergan, 2006). Conditions that stimulate oxidation in

S. Barbut et al. / Meat Science 79 (2008) 46–63

µ-calpain activity on casein zymogram 45 min post-exsanguination. normal rapid 45 min pH

6.63

c 45 min normal rapid

5.76

µ-calpain activity

49

120 hr normal rapid

Titin (T 1) T2

µ-calpain activity on casein zymogram 6 hr postexsanguination. normal rapid

6 hour pH

6.03

5.37

µ-calpain activity 48 hr shear force (kg)

2.9

Drip loss

1.1%

4.3

6.8%

Fig. 1. Rapid pH decline in PSE pork longissimus muscle inactivates calpain and arrests protein degradation. Two samples represent a normal and a rapid pH decline in pork longissimus dorsi muscle. The rapid pH decline sample had a 1 day drip loss of 6.8% and a shear force value of 4.3 kg after 2 days of postmortem aging. The normal pH decline sample had 1.1% drip loss after storage of 1 day and a shear force value of 2.9 kg. (a) Casein zymogram of lcalpain extracted from each muscle at 45 min postmortem. Similar clear zones indicate that l-calpain activity remains in the muscle in both samples. (b) Casein zymogram of l-calpain extracted from each muscle at 6 h postmortem. Absence of a clear zone in the rapid pH decline sample indicates that lcalpain is completely inactivated. (c) A 5% SDS–PAGE of extracts from normal and rapid pH decline samples at 45 min and 120 h postmortem. A large amount of intact titin (T1) remains in the sample with rapid pH decline, rapid inactivation of l-calpain, high drip loss, and high shear force value.

meat early postmortem can effectively arrest activation of l-calpain (determined by measuring extent of autolysis) and degradation of muscle proteins during postmortem storage (Rowe, Maddock, Lonergan, & Huff-Lonergan, 2004b). The lack of degradation manifests itself in a less tender product, even after aging 14 days (Rowe et al., 2004b). Specific antemortem events result in oxidation of muscle proteins. Leeuwenburgh, Hansen, Holloszy, and Heinecke (1999) demonstrated elevated oxidation of mitochondrial proteins in response to acute stress in rats. More recently Ku¨chenmeister, Kuhn, and Ender (2005) reported that acute stress immediately prior to slaughter decreased sarcoplasmic reticulum Ca2+ transport. The reason for decreased function was not determined, however, it is known that oxidation of the sarcoplasmic reticulum stimulates Ca2+ release (Favero, Zable, & Abramson, 1995, 2003). Oxidation of thiol groups in the ryanodine receptor can modify the calcium sensitivity of this calcium channel (Zissimopoulos & Lai, 2006). It is becoming evident that free radical accumulation does occur in muscle following acute exercise (Bailey et al., 2007) and that this change in redox potential can result in a change in control of intracellular Ca2+ levels (Hool & Corry, 2007). Clearly loss of Ca2+ regulation is a common theme in development of PSE meat. Acute stress prior to exsanguination may result in production of reactive oxygen species in muscle and oxidation of calcium channels and premature loss of calcium regulation in early postmortem muscle. This arguably could initiate the cascade events that lead to rapid pH decline and protein denaturation.

3. Advances in genetic research in pigs It is generally recognized by the pork industry and academia that a ‘‘status quo’’ has been reached between production of pork quantity (carcass leanness) and quality (meat eating and processing attributes), and that the new directions for the industry are being clearly defined by consumer trends (Hoen, 1996; Miller, 2003). As a consequence, the focus of the pork supply chain is dramatically shifting towards economically balanced ‘‘best cost production of consumer quality products’’, and the new production systems are merging the economic and marketing value of ‘‘Quality Lean’’ (Huff-Lonergan, Melody, Klont, & Sosnicki, 2003; Sosnicki, Pommier, Klont, Newman, & Plastow, 2003; Sosnicki, Wilson, Sheiss, & de Vries, 1998; Wood, Holder, & Main, 1998). As meat processors have moved from offering ‘‘commodity pork’’ to branded pork products, meat quality has become more economically important within the entire US pork industry. The industry – from pig biology and genetics to consumer research – has taken several steps to reduce and/or eliminate PSE meat conditions and to further improve meat tenderness, juiciness and flavor (Fig. 2). As mentioned in the introduction, the results of 2006 survey of the US pork industry indicated that only, ‘‘3.34% of loins exhibit all three conditions of classic PSE, reporting a range from 0.1% to 10%’’ (Meisinger & Berg, 2006). The environment that swine genetic companies work in has seen increasing competition, significant consolidation, the involvement of multi-national companies and increasingly multi-species interest (Knap, 1998; McLaren, 2007).

50

S. Barbut et al. / Meat Science 79 (2008) 46–63 Pig

Prod

s

uctio

n Pig

Muscle Welfare/ DifferenStress tiation Physiology & Growth

Developmental (Muscle) Biology

Proc

g

odu k Pr

Por

“Ready -to- “Readyto cook” (Global) eat” Consumer Retail Retail & (trends)

Raw/Fresh Retail, Food Service & Export

Muscle Development

Valu

e-Ad

ded

Conversion of Muscle to Meat & Meat Quality

Sale

b

istri

cts D

essin

n& utio

& Food Food Service, Service, Export Export

Prod

ucts

Data = Information=Progress Fig. 2. Graphic illustration of the pork industry system designed to deliver high quality, value-added products to the consumer. The biological (developmental muscle biology, stress/welfare physiology and postmortem conversion of muscle to meat) inputs knowledge along with the understanding of environmental conditions enabling to optimize meat quality traits (left part of the chart) are required for the processing industry to efficiently produce a large variety of fresh and pre-cooked products to the market place (right part of the chart).

The response has been an increase in the level of professionalism in the breeding industry and a concomitant increase in the use of genetic and computational technology. Genomic information is increasingly becoming integrated into quantitative genetic practice. Numerous DNA markers are used in pig improvement programs today. These programs integrate molecular genetics discoveries with quantitative genetic methodologies to increase the accuracy of selection for complex breeding objectives in commercial environments, including pre-harvest, post-harvest and meat processing sectors of the industry (Beuzen, Stear, & Chang, 2000; Bidanel & Rothschild, 2002; Bendixen, Hedegaard, & Horn, 2005; Kinghorn & van der Werf, 2005; Maltin & Plastow, 2004; Plastow, 2002; Rothschild & Plastow, 1999; Montaldo & Mezera-Herrera, 1998). Customer needs have led pig breeding organizations to develop technical offerings beyond the core disciplines of genetic improvement and health. Technical services have expanded into areas of meat science, animal (pig) nutrition and reproduction, as the necessity to not only create healthy breeding stock with increased genetic potential, but to help insure that the companies within the supply chain achieve their product goals quickly, i.e. eliminating PSE meat (Knap, 1998). Implementation of statistical process control principles at every stage of production, processing and distribution has also been dramatically helping to optimize the genetic and environmental factors, which influence cost of production, meat quantity and quality (Wood et al., 1998). 3.1. Breeding for pork quality, importance of ultimate pH In the last 10–15 years, pig breeders have focused on elimination of PSE pork via including meat quality traits in their selection programs. A major improvement in pork quality has been achieved through elimination of the HAL1843 and RN genes. Additionally, breed differences in

meat quality traits are large and commercially relevant (SanCristobal et al., 2002). However, without the ability to directly measure meat quality in live animals, only progeny testing or measuring meat quality in full- or half-siblings has been available to calculate estimated breeding values (EBVs) for meat quality traits. Some researchers demonstrated that glycolytic potential or muscle fiber-type composition measured in vivo are viable options to predict meat quality, but recent guidelines and standards for animal welfare discourage live animal biopsies (Karlsson et al., 1993; Lengerken, Von Maak, Wicke, Fiedler, & Ender, 1994; Chang & Fernandes, 1997; Chang et al., 2003; Ender, Fiedler, & Dietl, 2006; Fiedler et al., 1999; Gill, Gospert, Klont, Sosnicki, & Plastow, 2006; Gill et al., 2003; Greaser, Okochi, & Sosnicki, 2001; Karlsson, Klont, & Fernandez, 1999; Klont, Brocks, & Eikelenboom, 1998; Larzul et al., 1999; Larzul et al., 1997; Le Roy, 1998; Schiaffino & Reggiani, 1996; Tanabe, Murroya, Chikuni, & Nakai, 1997; Mormede et al., 2004; Toniolo et al., 2004). Modern breeding practices of including data of progeny, full-sibs and half-sibs of nucleus pedigree animals allows for traits such as ultimate pH, or pHu; i.e. measured 24 h postmortem; to now be more readily incorporated into genetic improvement programs (Cameron, 1990; de Vries, Sosnicki, Garnier, & Plastow, 1998; de Vries, van der Wal, Eikelenboom, & Merks, 1994a; de Vries, van der Wal, Long, Eikelenboom, & Merks, 1994b; de Vries & van der Wal, 1992; Knap, Sosnicki, Klont, & Lacoste, 2002; Knap, van der Steen, & Plastow, 2001; McLaren & Schultz, 1992). The wide-ranging effects of pHu on pork quality and the relative ease of collecting the phenotypic data make this an ideal trait for selection purposes. Ultimate pH has been shown to be genetically and phenotypically correlated with many economically important criteria such as meat color, meat tenderness, water-holding capacity (WHC), and sensory qualities; i.e. achieving pork pHu > 5.70 effectively eliminates PSE pork (Bidner et al., 2004; Cameron, 1990;

S. Barbut et al. / Meat Science 79 (2008) 46–63

Lonergan et al., 2007). More specifically, a higher pHu is associated with better WHC, translating into lower drip or purge losses during storage, and a higher yield when processing (Eikelenboom, Hoving-Bolink, & van der Wal, 1996; Eikelenboom, Van der Wal, & De Vries, 1995; Greaser, 1986; Huff-Lonergan et al., 2002). Although continuing to increase meat pHu may have a positive effect on waterholding capacity and processing characteristics, flavor of fresh pork and shelf life may be compromised when pHu exceeds 6.1 (Klont et al., 2002). Therefore, pig breeding companies focusing on improving meat quality must keep the pH level within an upper threshold to both maximize the benefits of darker color and improved WHC while minimizing effects of potential off-flavor and decreased shelf life. Focusing selection strictly on one area of performance, such as meat quality, while disregarding potential negative effects on growth or carcass quality could actually create a negative trend for the overall economic performance of the animal. For instance, it was shown that the converse of this to be true when selection emphasis placed strictly on lean growth efficiency while ignoring meat quality traits resulted in lower pHu and higher drip loss than in the randomly selected control line (Huff-Lonergan, Kuhlers, Lonergan, & Jungst, 1998; Lonergan et al., 2001b). 3.2. Breeding for pork quality, importance of commercial progeny testing A specific difference in an environment (climate, nutrition, health, management, pre-slaughter handling, etc.) does not necessarily have the same effect on different pig genetic populations, or on the progeny of different individuals (i.e. Nucleus boars) within these populations, due to varying degrees of sensitivity. Genotype by environment interactions (often referred to as G · E) are particularly relevant to swine improvement programs, including genetics of meat quality, as the progeny of individuals raised, tested and slaughtered under ‘‘ideal’’ genetic nucleus or ‘‘meat lab’’ conditions have to perform under a range of varying commercial production and plant environments (Bijma & Van Arendonk, 1998; Brandt & Ta¨ubert, 1998; Lutaaya et al., 2001, 2002; Van der Werf, Van der Wei, & Brascamp, 1994). Genetic correlations between purebred and crossbred performance for economically important traits in the pig can deviate significantly from unity, indicating not all the improvement predicted (based on measures in a GN and meat lab environment) will be realized when crossbred progeny are evaluated in a commercial environment. Perez, Casey, and McLaren (2006), estimated the effects of using a crossbred vs. purebred trait objective function, and including crossbred half-sib to GN tested purebred pigs performance test data vs. use of purebred (GN) data only. Among many traits of economic importance included in the selection objectives (i.e. age at 90 kg carcass weight, average daily feed intake, back fat thickness, loin muscle

51

depth) loin pH at 24 h postmortem was used to estimate its value for breeding for meat quality (Perez et al., 2006). In conclusion, the combination of crossbred records and emphasis on crossbred/commercial performance increased the accuracy of breeding for pH by 0.04 units (i.e. approximately one fourth of a genetic and phenotypic standard deviation) above the base breeding program including only purebred records and purebred index. Furthermore, the predicted economic improvement per pig to slaughter based on the commonly accepted economic values of the traits was 26% higher in the program using crossbred information where the (only) objective was the improvement of crossbred performance (Perez et al., 2006). Overall, this can be used as an example of a procedure to improve meat quality. 3.3. Breeding for pork quality, importance of ‘‘desired gains’’ program It is generally accepted that a primary consideration in the development of a genetic improvement program is the definition of a breeding objective. Geneticists usually define these breeding objectives as an aggregate of breeding values for all traits influencing income and/or expenses, with each breeding value weighted by an appropriately derived economic value (Woolliams, Bijma, & Villanueva, 1999). Objectives defined in this way are ideally suited to examine the flow of benefits between segments of a breeding pyramid. Product prices and production costs have to be assumed for the definition of the breeding objective. While conventional wisdom indicates that selection indexes are ‘‘robust’’ against price and cost deviations certain conditions might indicate using an economic value much different than current values. Therefore, a target production level approach, sometimes called desired gains can be used in the development of breeding objectives (Kinghorn & van der Werf, 2005; Hanenberg & Merks, 2000). Desired gains is useful when the response of specified traits in the breeding objective may be required to equal pre-determined values, while the rate of genetic change in other traits is maximized. The weightings are determined from the desired gains and economic values in the breeding objective (Kinghorn, Meszaros, & Vagg, 2002). Examples of the use of desired gains might be to differentially balance meat quality; i.e. a dramatic improvement of meat quality and, thus elimination of PSE meat, by increasing meat ultimate pH by 0.05 units and decrease meat lightness L* by 1.5 units (darker meat), while maintaining growth rate and carcass back fat thickness at current levels. Niche markets, i.e. pork with various characteristics desired by certain consumers, have been the first beneficiaries of such genetic approach. Examples include certain so-called heritage breeds (e.g. Gloucestershire Old Spot, Large Black, Tamworth, Berkshire, (http://www.berkridge.com; http://www.heritagefoodsusa. com) and other combinations of genetics and production systems (i.e. Premium Standard Farms USDA Process

52

S. Barbut et al. / Meat Science 79 (2008) 46–63

Verified antibiotic free pork http://www.psfarms.com/ process_verified_pork.html; Leidy’s Nature’s Tradition, ‘‘100% All-Natural pork with no antibiotics’’ http:// www.leidys.com/about.php).

Longissimus muscle glycogen content in RN homozygous and heterozygous pigs and concomitant lower muscle at pH 24 h postmortem, reduced WHC, and much lower cooked ham yields (Andersson, 2003; Milan et al., 2000).

3.4. Breeding for pork quality, importance of major genes, HAL-1843 and RN

3.5. Breeding for pork quality, importance of marker assisted selection (MAS)

Application of molecular genetics technology to the pig improvement industry began with discovery of the point mutation responsible for porcine stress syndrome (Fujii et al., 1991), and subsequent commercial availability of a DNA test (HAL-1843; the HAL-1843 trademark is licensed by The Innovations Foundation, Toronto, Canada, owner of the trademark). The halothane or stress gene is the most studied major gene affecting meat quality, and it is the first practical manipulation of a major gene in pig breeding using molecular biology tools (Fujii et al., 1991; Lister, 1987; MacLennan & Phillips, 1992; Otsu, Khanna, Archibald, & MacLennan, 1991;). Briefly, a single point mutation in the calcium release channel ryanodine receptor gene (ryrl) in recessive condition is responsible for porcine stress syndrome (PSS, malignant hyperthermia; pigs homozygous for this mutation are likely to develop the PSE condition postmortem). This gene also results in, or is closely linked to, a gene(s) involved in determining muscling and leanness (for reviews see Greaser, 1986; Lister, 1987; Vogeli, 1992; Vogeli, Schworer, Kuhne, & Wysshaar, 1985). The detection of this mutation using the HAL-1843 test has provided pig breeders with the means to precisely control the distribution of the mutation and enabled exploitation of the intermediate position of the heterozygote (Nn) animals between the two homozygous (NN and nn) for most of the carcass leanness and meat quality traits including pH-45 min postmortem and PSE incidence; i.e. the n allele is not completely recessive (Fujii et al., 1991; McLaren & Schultz, 1992; Otsu et al., 1991; Sellier, 1998). However, the results of many studies demonstrated that the HAL1843 gene accounts only for about 25–35% of the PSE meat observed in commercial abattoirs (Allison, Johnson, & Doumitt, 2005; Allison et al., 2006; de Vries et al., 1994b). Another major gene affecting meat quality that has been widely implemented in breeding programs is the RN (Redement Napole) gene (Monin & Sellier, 1985; Sellier, 1998). Le Roy, Naveau, Elsen, & Sellier (1990) reported that the RN is a dominant gene that primarily acts by increasing the glycogen content of the ‘‘white’’ (fast-glycolytic) fiber and muscle types. Also, there is a relationship between the sarcoplasmic accumulation of glycogen in the ‘‘white’’ fibers and a high muscle glycolytic potential resulting in low ultimate pH, partial protein denaturation, and consequently a low Napole yield (Le Roy, 1998). Milan et al. (2000) discovered a non-conserved R200Q substitution in the Protein Kinase, AMP-activated, Gamma-3subunit (PRKAG3 gene); that explained the dominant mutation (denoted RN ) that caused a 70% increase in

The development of the field of genomics has stimulated interest in ‘molecular breeding for meat quality’ as this ‘trait’ constitutes the classic case where DNA marker-based selection is at its most efficient, where the trait cannot be measured on the selection candidate and can only be measured at high costs on its relatives postmortem; i.e. meat ultimate pH (Plastow, 2002; Rothschild & Plastow, 1999). Once a DNA marker (a polymorphism) has been shown to be associated with variation in the target trait, then it can be used to genetically DNA-type young animals for pre-selection before performance testing. To date DNA markers are being identified using two basic approaches, Quantitative Trait Loci (QTL) mapping and the ‘‘candidate gene approach’’. Quantitative Trait Loci (QTL) mapping, this approach utilizes specific genetic designs (for example, three generation families based on divergent breed crosses such as Chinese Meishan or Wild Boar and Large White) to find the location of QTL on the genetic map. Several QTL studies have addressed pork quality traits and they provide the starting point for the identification of individual genes (or markers) influencing these traits (the positional candidate gene approach). Indeed, the RN mutation, identified initially by a mapping approach was then elucidated using positional cloning and a ‘‘BAC contig’’ constructed for that region of the genome, a physical representation of the DNA sequence from the QTL region (Jeon, Amarger, Rogel-Gaillard, Robic, & Bonggam-Rudloff, 2001; Milan et al., 2000). In recent years the linkage and physical maps of the pig genome have developed considerably (for review, see Rothschild & Plastow, 1999). These maps have been exploited to search for genes influencing variation in commercially important traits. Several QTL scans and candidate gene analyses have identified important chromosomal regions and major genes associated with traits of economic interest in the pig (reviewed in Bidanel & Rothschild (2002)). These include QTL for meat quality traits (chromosomes 2, 3, 4, 6, 7, 12, 15), growth and back fat thickness (chromosomes 1, 2, 3, 4, 5, 6, 7, 8, 13, 14), and reproduction (chromosome 4, 6, 7, 8). Much statistical genetics work has been conducted on methods for linkage mapping of QTL in livestock (Bidanel, Milan, Renard, Gruand, & Mourot, 2002; Desaites et al., 2002; Edwards, 2006; Gerbens et al., 2000; Malek et al., 2001; Ovolo et al., 2002; Rohrer et al., 2005; Rohrer, Thallman, Shackelford, Wheeler, & Koohmaraie, 2005; Rothschild, Bidanel, & Ciobanu, 2004; Van Wijk et al., 2006; Wimmers et al., 2006). QTL regions discovered, however, are often

S. Barbut et al. / Meat Science 79 (2008) 46–63

very large (20–40 centiMorgan (cM) long; 20–40 mega base pairs (Mb) of DNA), and could contain 200–400 positional candidate genes (McLaren, 2007). Development of ‘‘gene chip’’ (microarrays capable of measuring gene expression) technology and decreasing cost per marker genotype have made use of high-density marker genotyping to detect QTLfeasible (Bidanel & Rothschild, 2002). The objective of high density genotyping is that, by having markers spaced at approximately 1 cM intervals throughout the genome, there will be markers in linkage disequilibrium (LD) with all the QTL which will be practical to implement for improvement using population-wide LD–MAS. A number of research centers around the world established ‘‘reference families’’ using genetically diverse breeds to study gene segregation in F2 populations and determine the probability of chromosomal locations of QTLs, i.e. genes (loci) affecting various meat quality-associated quantitative traits (Bidanel & Rothschild, 2002). Examples of genetical genomics (expression QTL) research that resulted in useful marker discovery can be found in the area of pork quality (http://www.qualityporkgenes.com) and disease resistance (http://www.pathochipproject.com). However, it was postulated that in the near future livestock microarrays are unlikely to prove important outside of research because they are too expensive to use in routine breeding program evaluations (McLaren, 2007). Candidate genes, this approach is to search for markers associated with candidate genes (Rothschild & Plastow, 1999). By focusing on markers for genes thought likely to be causative for variation in traits of interest, based often on comparisons with other mapped mammalian genomes, a number of useful causative mutations and linked marker polymorphisms for meat quality (e.g. HAL-1843; RN , PRKAG3, Calpastatin (CAST), Fatty Acid Binding Protein (FABP) as well as for other economically important traits (i.e. reproduction: Estrogen Receptor-ESR; Prolactin Receptor-PRLR; Retinol Binding Protein 4-RBP4; Follicle Stimulating Hormone Beta-FSHB; feed intake and growth: Melanocortin Receptor 4-MC4R; carcass composition: Insulin-like Growth factor 2-IGF2; coat color: Mast/stem cell growth factor receptor-KIT; Melanocortin receptorMC1R); were discovered and became applied in pig breeding (Ciobanu et al., 2004; Ciobanu et al., 2002; Ciobanu et al., 2001; Fields et al., 2002; Huszar, Lynch, FairchildHuntress, Dunmore, & Fang, 1997; Jeon, Carlborg, Tornstein, Giuffra, & Amarger, 1999; Kim, Larsen, Short, Plastow, & Rothschild, 2000; Nezer, Moreau, Karim, Brouwers, & Coppieters, 1999; Plastow, 2002; Rothschild et al., 2004; Short et al., 1997). Identification of candidate genes for meat quality characteristics in combination with MAS programs is positioned to greatly enhance genetic improvement of meat quality whilst not compromising lean percentage. The pig industry is already actively using MAS strategies to improve swine production (Ciobanu et al., 2002; Fields et al., 2002; Rothschild & Plastow, 1999). It is anticipated that the developments in genomic and proteomic technolo-

53

gies will increase the number of markers that can be used in MAS, so that selection for meat quality, and thus selection to eliminate PSE pork, can be carried out on live animals (Bendixen, 2005; McLaren, 2007; Morzel et al., 2004). 3.6. Breeding for pork quality, general conclusions MAS in general, and focus on improving pork quality in particular, provides a distinct advantage over sib and commercial pedigreed-progeny slaughter programs which are increasingly difficult and expensive to implement. The database builds up over time to provide a very useful resource for this purpose, for further validation of DNA markers identified in experimental populations or to test candidate markers. However, sibling and progeny slaughter schemes designed to improve carcass and meat quality will continue to play a large role in immediate and distant future, both for the identification of new markers and for monitoring breeding lines in order to optimize the breeding direction (the advantage of incorporating markers into selection programs can be sustained when new markers are identified to replace older markers that begin to reach fixation). Thus, the fundamental base of genetic improvement will continue to be quantitative genetics, high volume testing and selection, measuring traits of economic interest for individual boars and gilts and their commercial progeny. Subsequently, by using selection indexes focused on ‘‘producing best quality pork at least cost’’, unfavorable genetic correlations between carcass and meat quality traits and production costs can be overcome. Sequencing of the porcine genome is an important milestone in the development of enabling technology focused on the biology of the pig, including skeletal muscle biology, postmortem conversion of muscle to meat and meat quality. The premise of ‘‘genomic selection’’ is that with the availability of dense marker maps (genome could be considered as many thousand small segments the phenotypic effects of which could be estimated), trait breeding values could potentially be predicted solely based on ‘‘marker’’ genotype and pedigree. The International Swine Genome Sequencing Consortium, formed in September 2003, (http://piggenome.org/; http://www.animalgenome.org/ pigs/genomesequence/) expects to have a draft sequence released in late 2007/2008. Further advancement in genomics and proteomics will enable for development of more complex and accurate genetic improvement programs leading to reduce genetic susceptibility to PSE (or maybe even 1 day to total elimination of PSE pork), and hence overall improvement in pork quality. 4. Factors that contribute to PSE poultry Over the past five decades, the poultry industry has seen tremendous changes, which were part of a significant increase in meat consumption (i.e. doubling or tripling per-capita consumption in different parts of the world).

S. Barbut et al. / Meat Science 79 (2008) 46–63

These changes have resulted in pressure on breeders, nutritionists and growers to increase the growth rate of birds (chickens, turkeys), feed efficiency, size of breast muscle, etc. Today, birds are marketed at about half the time and at about twice the body weight compared to 50 years ago. This kind of selection has obviously put more stress on the growing bird and some believe it has resulted in an increase of the PSE problem. However, research focusing on the PSE problem in poultry has only started to emerge during the past decade. Prior to that, there were only a few research papers referring to the possibility of ‘a PSE pork-like condition’ in poultry (Aberle, Stadelman, Zachariah, & Haugh, 1971; Vanderstoep & Richards, 1974). Another important point to remember is the change in consumption patterns, where consumers buy today more further-processed products and cut-up parts, meaning that the poultry industry has to deal with more meat quality issues (drip loss, color, texture) that did not matter much when most poultry was sold as whole birds. This is especially true when expensive portions, such as deboned breast fillets, are sold with or without marination. Table 1 shows data from 1974 concerning two distinct groups of turkeys which show fast and slow glycolyzing rates. It was suggested that the postmortem muscle behavior of the fast glycolyzing group was fairly similar to the phenomenon seen in PSE pork muscle, where the fast pH drop could result in reducing protein functionality. However, no further studies were done to investigate the problem over the next 15–20 years. Only later, researchers started to re-examine the problem. Sante, Bilicki, Renerre, & Lacourt (1991) reported on the differences between fastand slow-growing breeds of turkeys, and highlighted some of the differences. Later, estimates on the occurrence of the so called ‘pale meat problem’ were published: 0–28% for broilers (L* > 49) in Ontario, Canada (Barbut, 1997), 5– 30% of turkeys (L* > 50.5) in Ontario in a study examining 4000 turkeys (McCurdy, Barbut, & Quinton, 1996), and 40% in a study examining 3000 turkeys (L* > 53) in Texas (Owens, Hirschler, McKee, Martinez-Dawson, & Sams, 2000a). The lighter meat from these studies was also evaluated for its water-holding capacity, pH, color and texture, and it was demonstrated that correlations among these parameters could be established. Seasonal differences in the rate of the ‘light meat problem’ were also demonstrated (Fig. 3), suggesting that excess heat stress during the summer months results in higher incidences of the PSE problem; a similar trend was reported in pork meat. It should also be mentioned that Swatland (1990) demonstrated the basic mechanism of muscle (bovine) paleness to be a

% Birds > truncation value

54

1 Summer Spring Autumn Winter

0.8 0.6 0.4 0.2 0 45

46

47

48

49 50 51 Truncation level

52

53

54

55

Fig. 3. Truncation values of L* measurements obtained for young turkey tom breast meat showing seasonal effects. Data from McCurdy et al. (1996).

decrease in pH, which causes an increase in myofibrillar refraction. Swatland (1995) later showed that this refraction effect is separate from denaturation of sarcoplasmic proteins (i.e. can be caused by fast pH drop while the muscle is still warm, as mentioned earlier in this review). Whereas the refractive effect was reversible in pork muscle taken from pH 7 to 5 and back to 7, the sarcoplasmic protein denaturation was not. For additional information on the progress in understanding meat paleness, see review by Swatland (2004). Later, Pietrzak, Greaser, & Sosnicki (1997) investigated the differences between normal and low postmortem pH groups of turkeys (Table 2). By using SDS PAGE, Western blotting and immuno-fluorescence microscopy, they revealed that phosphorylase became tightly associated with the myofibrils in muscles from the PSE group. Their conclusion was that the ability to classify fast and slow postmortem glycolysis rates may suggest a genetic basis for the differences. This was followed by Wang, Brem, Zarosley, Booren, & Strasburg (1999) reporting on the muscle Ca++ channel ryanodine (RYR) binding in poultry. They indicated that RYR binding of the sarcoplasmic reticulum (SR) vesicles from a commercial turkey line showed higher (p > 0.05) affinity for RYR compared to an unimproved/ non-selected turkey line (Kd = 12.2 vs. 20.5 nM, respectively). This corresponded to Mickelson et al. (1988) who reported that purified SR from genetically defined stresssusceptible pigs bound RYR at three times the affinity seen in normal pigs. The cause of the porcine stress syndrome (PSS) was identified as an Arg615 to Cys615 substitution (Fujii et al., 1991). This mutation gives rise to hyper-metabolism and can cause malignant hyperthermia in stressed, PSS-susceptible pigs. Wang et al. (1999) also showed higher abundance of a 75 kDa protein (unidentified) in the com-

Table 1 Characteristics of ‘‘Fast’’ and ‘‘Slow-Glycolyzing’’ White Cannon turkey muscle Group

ATP-0 (lM/100 g)

ATP 60/0 min (% conc.)

pH (15 min)

Lactate (15 min, lM/100 g)

‘‘Slow’’ ‘‘Fast’’

5.07 + 1.0 2.24 + 0.7

60 + 5.5 16 + 4.0

6.07 + 0.1 5.85 + 0.1

265 410

Data from Vanderstoep and Richards (1974).

S. Barbut et al. / Meat Science 79 (2008) 46–63 Table 2 Differences between high pH (normal) and low pH turkey breast muscle groups Parameter pH at

20 min PM 180 min

ATP at

20 min 180 min (lM/g)

Lactate at 20 min WHC (%) Cook yield (%) Minolta L* (24 h PM)

High pH(n = 8)

Low pH (n = 8)

6.44 ± 0.3 5.88 ± 0.1

5.80 ± 0.1 5.69 ± 0.1

3.3 ± 1.1 1.6 ± 1.8

1.4 ± 0.4 0.4 ± 0.2

58 ± 16 112 ± 6 126 ± 8 44 ± 1.8

94 ± 19 85 ± 12 107 ± 8 49 ± 1.0

Data from Pietrzak et al. (1997).

mercial turkey line, and isolated two iso-forms (a, b) of the Ca++ channel proteins from both populations. The later was in agreement with previous results of avian, amphibians, piscine and reptilian species (Sutko & Airey, 1996). It should be mentioned that in contrast, mammalian species posses only one skeletal muscle iso form (Ogawa, 1994). It should also be indicated that in humans, about 30 mutations in the primary structure of RYR-I have been described to cause malignant hyperthermia; the mutations concentrate in three main reigns called Hot Spots I, II and III (amino acid residue 35–614, 2162–2458, and 4550–4940, respectively). Another point to remember is that the overall postmortem glycolsis process in poultry is about three times faster compared to pork muscle. Wang et al. (1999), concluded that the functional differences between the commercial and unimproved turkey lines might be in one or both channel isoforms, and that the significant difference in the amount of the 75 kDa protein (corresponding to the SR vesicles) could have resulted from genetic selection over the years. Overall, the research mentioned above suggests genetic mutations similar to the ones in pigs. However, a study on halothane sensitive turkeys (i.e. about 3.5% of the birds exposed to 3% halothane gas for 5 min at 4 week of age and showed signs of muscle rigidity in the leg) revealed that these birds did not show higher incidences of PSE meat (slaughtered at 20 week of age) compared to a group of non-sensitive birds (Owens, Matthews, & Sams, 2000b). In 2004, Chiang, Allison, Linz, and Strasburg identified two a-RYR alleles in turkey skeletal muscle and characterized them. They started with the hypothesis that a mutation in the RYR receptor underlines turkey meat quality problems that are strikingly similar to PSE in pork meat, and used real time PCR for their investigation. They reported at least three transcript variants in the 376–615 region of the amino acid sequence. The transcripts included: W – homologous to the mammalian skeletal RYR-I, AS 81 – absence of 81 bases at the beginning of exon 13, and AS 193 – a deletion of 193 bases or the entire exon 13. They found that most birds in the study (n = 76) expressed all three-transcript variants, but some W only, W with AS 193 but no AS 81, or AS 81 and AS 193, but no W. No bird

55

expressing only AS 81 or AS 193 or W with AS 81 was found, suggesting that birds with only AS 193 could not survive because of no functional a channel protein. They also identified two a-RYR genomic DNA alleles (I, II). The homozygous a-RYR I was the most frequent in the non-selected group (56%). In the commercial turkey line (i.e. selected for fast growth), a-RYR I and II were about equal: 47 vs. 41%. Heterozygous birds were about 12% in both populations. In addition, they showed that turkeys homozygous for a-RYR II tended to have superior meat quality indicators (higher pH 15 min: 6.01 vs. 5.80 (p < 0.001), and lower water-holding at 24 h postmortem: 5.03 vs. 0.79% (p < 0.05), respectively), but no differences in percent exudate were detected. At the moment, unlike the pork industry, the poultry industry does not have a reliable genetic marker(s) for commercial selection. Yet the question presented by the industry is: what can be done to minimize production losses due to the PSE problem? The answer can be divided into shortand long-term solutions. In the short-term, our practical knowledge indicates that reducing stress prior to slaughter (e.g. during loading, transport, unloading and stunning) can help. Procedures such as providing a rest period after transportation (i.e. in a cool area under blue light), switching to lower stress unloading methods (e.g. automatic unloading to eliminate manually pulling birds from transport containers), and switching to lower stress stunning methods (e.g. two stage gas stunning) can be useful. Another area is the post-stunning treatment (Offer, 1991), which can include better chilling regimes; various researchers, in both the pork and poultry areas, have discussed this aspect. In the poultry area, Pietrzak et al. (1997) mentioned ‘‘the results indicate that the irreversible myosin insolubility, due to low pH and high temperature conditions, is decisive in the development of PSE turkey breast muscle.’’ Later, Sams & Alvarado (2004) mentioned that ‘‘to varying degrees, slower chilling rates resulted in lower pH, greater degree of lightness, greater cook loss and reduced gel strength (in turkey breast muscle). However, chilling rate had no effect on total protein solubility . . . Chilling rate seems to contribute to PSE turkey meat characteristics by mechanism independent of total protein solubility’’. In the area of marketing fresh poultry meat, color variations among breast meat fillets can be perceived as a problem by consumers. Fletcher (1999) evaluated packages from different brands sold at supermarkets across the state of Georgia, USA, and reported that several companies have been sorting out the meat. He examined the percentage of color defects (i.e. one or more breast fillet showing a noticeable color difference within a package), and reported 0–25% incidences among the different brands. When meat is used for making products at the plant, it is also possible to sort out the meat (e.g. currently done by some pork processors during the selection of large hams for injection). In the case of chicken/turkey breast meat used for further processing, different color and pH cut-off values have been suggested (Barbut, 1998; McCurdy

56

S. Barbut et al. / Meat Science 79 (2008) 46–63

et al., 1996). This might be more important for turkey breast meat where large portions are commonly used to produce a whole muscle roast. The idea is not to try and inject added moisture (usually 20–30%) to a PSE portion, since it could not be held during cooking. In a case of a cook-in-the-bag product, it would also require opening and draining the liquid, which will substantially shorten the shelf life. It is also important to note that up to now, the poultry grading system has been based on aesthetics criteria (e.g. tears in the skin, bruises, missing parts), which gives the processor no indication of meat quality attributes (e.g. water-holding capacity, texture, color). In any case, when processors decide about using a color cutoff system, they should take into account the inherent differences in meat color among breeds, age groups, etc. Another approach to minimize the effect of the PSE problem in further processed products is the addition of non-meat ingredients such as starch, carrageenan, and soy proteins to enhance moisture binding capacity and texture building. Zhang & Barbut (2005) compared the use of different starches (regular and modified potato and tapioca) in PSE, normal and DFD meat. They showed that cook loss in PSE meat was the highest (28%), and that with some starches, it could be reduced to about 5%. Long-term solutions should include genetic selection and breeding for specific meat quality attributes. As discussed above, most selection so far has been done to improve growth rate, size of certain muscles, and feed conversion. An example of the downside result of selecting for growth rate is a poor deposition of connective tissue in turkeys. Swatland (1990) reported an increase of about 35-folds in cross-sectional area of muscle fibres during growing from 1 to 15 weeks. At the same period, the endomysium connective tissue layer only increased two times in thickness, and the perimysium five times in width. This can later translate into poor slicing and fragmentation seen in cooked deli products. Another trigger for poor sliceability might also be the formation of large intercellular spaces, as the unbound fluid in PSE meat is released from myofibrils during the postmortem process. 5. Genetic/breeding research in poultry As discussed above PSE-type meat has been described in various species as poor quality meat. The two genetic mutations in pigs that have been linked to the development of PSE include: the Ryanodine receptor (Ryr) or Halothane (Hal) gene mutation (causing Porcine Stress Syndrome (PSS) or Malignant Hyperthermia (MH) resulting in rapid drop to low pH at high muscle temperatures), and the Rendement Napole (RN) gene mutation which results in pigs exhibiting normal rate of pH decline but the PSE condition is caused by very low ultimate pH. The description of PSE has been applied to any meat that has a paler appearance and high drip loss in chickens and turkeys (e.g. Barbut, 1998, 1996) but as yet a role for the Ryr or RN gene mutations has not been demonstrated

in poultry. In susceptible pigs MH or PSS can be triggered by volatile anaesthesia (e.g. halothane) and depolarising muscle relaxants (e.g. succinylcholine) and these have been successfully employed to distinguish reactors (nn) from non-reactors (NN and Nn). Studies in turkeys using halothane (Owens, McKee, Matthews, & Sams, 2000c) and succinylcholine (McKee, Hargis, & Sams, 1998) were inconclusive, as there were no clear reactors/non-reactors as seen in pigs and a ‘positive’ response, defined as leg muscle rigidity, was generally a poor predictor of the subsequent development of PSE meat. In addition, MH has not been described in turkeys. It is possible that these differences in observations between pigs and poultry are due to differences in the Ryanodine receptor isoforms in the two species, or that a different mechanism or genetic mutation underlies PSE meat in the two species. For example, there are several gene mutations responsible for malignant hyperthermia in humans and a defect affecting any process involved in calcium homeostasis could easily manifest itself in development of PSE-type meat (Mitchell, 1999). The Ryanodine receptor controls release of calcium from the sarcoplasmic reticulum (SR). A rise in intramuscular calcium causes muscle contraction and energy is required to remove calcium and enable muscle relaxation. PSS/MH susceptible pigs have a faulty Ryanodine receptor that is highly sensitive and can be easily triggered to release excessive calcium, causing hypercontraction of the muscle and massive heat production, which can lead to death or PSE meat. There are four subunits that make up the Ryanodine receptor and in mammals these four subunits are composed of the same isoform (RYR1). A gene mutation of RYR1 has been identified and if more than one subunit has this mutation the function of the Ryanodine receptor is altered. However, it is a recessive condition and only homozygous (nn) individuals, with mutations of all four subunits, will exhibit full-blown PSS/MH. In avian species, there are two Ryanodine receptor isoforms: a-Ryr (equivalent to RYR1) and b-Ryr. These mix in equal quantities to form the Ryanodine receptor. If only a-Ryr expresses the gene mutation identified in pigs then it is more likely that turkeys will be heterozygous (Nn) and only exhibit altered function of the Ryanodine receptor rather than full-blown MH. So far a single point mutation has been considered as the candidate for causing PSE meat in poultry. However, there are other hypotheses that should be considered as having the potential to cause PSE meat: (a) the nature and metabolism of the breast muscles, (b) the size of the muscle and the size of muscle fibres (Dransfield & Sosnicki, 1999), and (c) perimortem environmental conditions (Berri et al., 2005; Debut et al., 2005; McKee & Sams, 1997). Many factors influence the final characteristics of turkey meat, for example, the structure of the muscle and muscle metabolism at slaughter have impact on toughness, texture, water-holding capacity (WHC) and appearance of the meat. Environmental factors play an important role in influencing meat quality and it is important to try to

S. Barbut et al. / Meat Science 79 (2008) 46–63

understand the environmental vs. genotype interaction. Understanding postmortem muscle metabolism could help key decision makers to modify bird handling and processing procedures to help minimize the incidence of PSE meat. The flight (breast) muscles of chickens and turkeys are entirely Type-IIb fibres (glycolytic), capable of short bursts of activity for the ‘Fight or flight’ response. Energy is produced anaerobically via glycoslysis, whereby glycogen is broken down to lactic acid, which is normally then removed by the blood. The metabolism of the breast muscle and conditions at slaughter could contribute to PSEtype meat because there are large glycogen stores within the breast muscle with a high propensity to produce lactic acid (entirely glycolytic) and therefore the potential for a rapid drop in pH and/or low ultimate pH postmortem exists. In addition there is the potential for high muscle temperatures due to flapping, struggle, stress, and high metabolic rate in the lead-up to slaughter and the large breast muscle mass (particularly in turkeys) being difficult to chill postmortem. From a breeders perspective it is important to understand how the selection process has affected the structure of the muscle, particularly in terms of the number and size of muscle fibres. Could the PSE-condition be linked to the size of the muscle fibres? Could large fibres be more susceptible to stress-induced muscle damage? Descriptions of ‘focal myopathy’ in commercial turkeys are very similar to ‘capture myopathy’ described in wild turkeys. Could loading and transportation to slaughter have a similar affect to capture in wild birds? When the birds are then slaughtered the muscle does not have time to recover and regenerate, could this influence meat quality? Internal research at British United Turkeys has looked at variation in muscle histology and meat quality within and between lines. Initial trials found that when comparing traditional strains with one commercial strain the expected correlation of increasing fibre size with increasing liveweight was observed. However, comparing several modern strains under different selection pressures gave no clear correlation between fibre size and liveweight. This suggests other factors were also involved such as variability in the number of muscle fibres contributing to growth (set in the embryo). A PhD study comparing growth, muscle structure and muscle damage in a commercial and traditional strain of turkey indicated that at similar breast weights the traditional strain actually had larger fibres than the commercial, suggesting that the commercial birds possibly have more muscle fibres contributing to growth (Mills, 2000). The same commercial birds were feed restricted to determine the effect of growth rate on muscle damage. Creatine kinase (CK) is a muscle enzyme, which leaks from the muscle when there is a loss of membrane integrity or fibre damage and its presence in the blood is a marker for muscle damage. Muscle damage appeared to correlate with body weight irrespective of growth rate. The relationship with fibre size suggests there may be a maximum limit to fibre size above which there is either a

57

loss of membrane integrity (fibres become ‘leaky’) or fibres become more susceptible to exercise-induced muscle damage (stress). These conclusions suggest there may be a benefit in promoting fibre number so that similar yields and weights can be achieved without fibres getting so large. However, a very recent study of muscle structure, metabolism and meat quality in broiler chickens suggests that increased fibre size (cross-sectional area) was associated with higher pH, darker meat and reduced drip loss. The authors suggest the meat from birds with larger fibres would therefore be better adapted to further processing compared to birds with smaller fibres (Berri et al., 2007). Clearly this is an area that requires further study to define the role of muscle fibre size in meat processing ability and to clarify potential differences between broilers and turkeys, given the wide differences in market weight and final muscle size. A second study looking at weight, number of nuclei within muscle fibres and number of muscle fibres within the semi-tendinosus muscle suggested that the relationship between weight, nuclei and fibre number is not straightforward and that there is variability between strains which could be exploited in the selection process. Further research was carried out with the Royal Veterinary College, London to investigate the possibility of controlling muscle fibre number in the embryo through incubation temperature. It was found that through manipulation of incubation temperature it was possible to increase the number of myonuclei, and the number of muscle fibres in the embryo and investigations looking at myogenin expression suggested the mechanism was via a delay in the process of differentiation in the muscle (Maltby, Somaiya, French, & Stickland, 2004). A fully pedigreed line of turkeys was used in a project with Roslin Institute, Edinburgh to identify quantitative trait loci (QTL). Meat Quality traits (L*, pHi, pHu, drip loss) were measured along with histology traits (fibre size, muscle damage score) in a group of 400+ birds. Blood samples were also taken and the aims of the project are to progress towards identifying microsatellite markers for traits of interest and use these markers for genotyping (B.U.T. personal communication). A study with INRA, France also used a fully pedigreed line of turkeys to investigate heritabilities (genetic and phenotypic correlations) of meat quality traits (Le BihanDuval et al., 2003). It was found that meaningful correlations could only be picked up when the birds were processed under commercial slaughter conditions (compared to controlled experimental conditions) highlighting that variability in meat quality traits is only expressed when the birds are exposed to environmental stressors. Correlations between traits were weaker on the phenotypic than genetic level. Under commercial conditions there was evidence of a genetic control over the rate of fall in pH. The rate of pH fall strongly correlated to ultimate pH (0.59) and this relationship was stronger than that reported in pigs and chickens. The rate of fall in pH was also strongly

58

S. Barbut et al. / Meat Science 79 (2008) 46–63

genetically correlated to paleness of the meat (L*) ( 0.80). The genetic correlation between ultimate pH and L* was weaker ( 0.53) and this was in contrast to that reported for chickens ( 0.91) (Le Bihan-Duval, Millet, & Re´mignon, 1999). The results suggest that in turkey the rate fall in pH may have greater impact on meat quality than ultimate pH. Should further research determine a single point mutation, this would provide rapid response to selection once a marker was identified, whereas the hypothesis involving muscle fibre size and stress-induced muscle damage suggests polygenic effects which would be more difficult to identify. The environment chosen to record meat quality traits may strongly affect the results of genetic analysis. Further work is required into muscle structure, metabolism and fibre growth and the influence on meat quality. Elucidation of the role of the Ryanodine receptor in turkeys is also required as previous studies have suggested differences in the binding affinity of ryanodine in different turkey genotypes (Wang et al., 1999) and a mutation in the turkey aRyr gene has been reported but is yet to be linked to meat quality. Selection to improve meat quality in the future needs to focus on fibre number/fibre size, the rate of pH fall and ultimate pH, colour (L*a*b*), and the possibility for direct selection on meat characteristics (e.g. texture, WHC). The investigation of many of these factors unfortunately requires the slaughter of selection candidates, which is a very expensive method unless genetic markers or QTL can be identified for these traits. 6. Conclusions Advancement of efforts to improve meat quality and value is uniquely dependent on discovery of heretofore unexplained sources of variation in meat quality. It is likely that employing the same approaches will result in failure to make these critical discoveries. Future success for the pig industry will require the production of consistent and predictable high pork product quality to ensure consumer satisfaction. The target should be to combine efficient growth with the best possible meat quality or alternatively the aim can be described as optimizing meat quality at the lowest cost of production. Implementation of statistical process control principles at every stage of pork production system has already helped to control and optimize the genetic and environmental factors, which influence the incidence of PSE meat and meat quality overall. The feedback-based supply chain approach – from system-specific genetics/live animal production systems, to fresh and processed pork products fulfilling consumer demands and back to customized genetics – will further insure elimination of undesirable PSE meat and sustainability of the pork industry. For the poultry industry, establishing best antemortem and post slaughter handling practises may be the best available short term strategies when quite a few processors are concerned with PSE meat. However, one of the most important long-term approaches should be the identifica-

tion of a reliable genetic marker(s) that can be used for commercial selection purposes of poultry. As discussed in this review, using genetic markers to remove stress susceptible pigs, has been successful in reducing the incidences of PSE. At the moment, the genetic basis of PSE in poultry is still not fully understood, but it is likely that one or more mutations predispose the birds to exhibit PSE conditions. The work by Chiang, Allison, Linz, & Strasburg (2004), can serve as an example of searching for genetic mutation(s) to find reliable markers for the poultry industry. References Aberle, E. D., Stadelman, W. J., Zachariah, G. L., & Haugh, C. G. (1971). Impedance of turkey muscle: relation to post mortem metabolites and tenderness. Poultry Science, 50, 746–749. Adachi, Y., Ishida-Takahashi, A., Takahashi, C., Takano, E., Murachi, T., & Hatanaka, M. (1991). Phosphorylation and sub-cellular distribution of calpastatin in human hemopoietic cells. Journal of Biological Chemistry, 266, 3968–3972. Allison, C. P., Johnson, R. C., & Doumitt, M. E. (2005). The effects of halothane sensitivity on carcass composition and meat quality in Hal1843-normal pigs. Journal of Animal Science, 83, 671–678. Allison, C. P., Marr, A. L., Berry, N. L., Anderson, D. B., Ivers, D. J., Richardson, L. F., et al. (2006). Effects of halothane sensitivity on mobility status and blood metabolites of Hal-1843-normal pigs after rigorous handling. Journal of Animal Science, 84, 1–14. Andersson, L. (2003). Identification and characterization of AMPK-y3 mutations in the pig. Biochemical Society Transactions, 31(1), 232–235. Averna, M., De Tulio, R., Passalacqua, M., Salamino, F., Pontremoli, S., & Melloni, E. (2001). Changes in intracellular calpastatin localization are mediated by reversible phosphorylation. Biochemical Journal, 354, 25–30. Bailey, D. M., Lawrenson, L., McEneny, J., Young, I. S., James, P. E., Jackson, S. K., et al. (2007). Electron paramagnetic spectroscopic evidence of exercise-induced free radical accumulation in human skeletal muscle. Free Radical Research, 41, 182–190. Barbut, S. (1996). Estimates and detection of the PSE problem in young turkey breast meat. Canadian Journal of Animal Science, 76, 455–457. Barbut, S. (1997). Problem of pale soft exudative meat in broiler chickens. British Poultry Science, 38, 355–358. Barbut, S. (1998). Estimates of the magnitude of the PSE problem in poultry-a review. Journal of Muscle Food, 9, 35–49. Bendixen, B. (2005). The use of proteomics in meat science. Meat Science, 71, 138–149. Bendixen, C., Hedegaard, J., & Horn, P. (2005). Functional genomics in farm animals – Microarray analysis. Meat Science, 71, 128–137. Berri, C., Debut, M., Sante-Lhoutellier, V., Arnould, C., Boutten, B., Sellier, N., et al. (2005). Variations in chicken breast meat quality: implications of struggle and muscle glycogen content at death. British Poultry Science, 46(5), 572–579. Berri, C., Le Bihan-Duval, E., Debut, M., Sante´-Lhoutellier, V., Bae´za, E., Gigaud, V., et al. (2007). Consequence of muscle hypertrophy on Pectoralis major characterictics and breast meat quality of broiler chickens. Journal of Animal Science, 85, 2005–2011. Beuzen, N. D., Stear, M. J., & Chang, K. C. (2000). Molecular markers and their use in animal breeding. The Veterinary Journal, 160, 42–52. Bidanel, J. P., Milan, D., Renard, C., Gruand, J., & Mourot, J. (2002). Detection of quantitative trait loci for intramuscular fat content and lipogenic activities in Meishan · Large White f2 pigs. Paper 03–13, In Proceedings of the 7th world congress of genetics applied to livestock production. INRA. Castanet-Tolosan, France. Bidanel, J. P., & Rothschild, M. (2002). Current status of quantitative trait locus mapping in pigs. Pig News and Information, 23(2), 39N–53N.

S. Barbut et al. / Meat Science 79 (2008) 46–63 Bidner, B., Ellis, M., Brewer, M. S., Campion, D., Wilson, E. R., & McKeith, F. K. (2004). Effect of ultimate pH on the quality characteristics of pork. Journal of Muscle Foods, 15, 139–154. Bijma, P., & Van Arendonk, J. A. M. (1998). Maximizing genetic gain for the sire line of a crossbreeding scheme utilizing both purebred and crossbred information. Animal Science, 66, 529–542. Boles, J. A., Parrish, F. C., Jr., Huiatt, T. W., & Robson, R. M. (1992). Effect of porcine stress syndrome on the solubility and degradation of myofibrillar/cytoskeletal proteins. Journal of Animal Science, 70, 454–464. Boles, J. A., Parrish, F. C., Jr., Skaggs, C. L., & Christian, L. L. (1991). Effect of porcine somatotropin, stress susceptibility, and final end point of cooking on the sensory, physical, and chemical properties of pork loin chops. Journal of Animal Science, 69, 2865–2870. Brandt, H., & Ta¨ubert, H. (1998). Parameter estimates for purebred and crossbred performances in pigs. Journal of Animal Breeding and Genetics, 115, 97–104. Briskey, E. J. (1959). Changes occurring during rigor mortis and subsequent ripening of muscle tissues. In Proceedings of the 12thannual reciprocal meat conference (pp. 108–124). The National Livestock and Meat Board. Briskey, E. J. (1964). Etiological status and associated studies of pale, soft, exudative porcine musculature. Advances in Food Research, 13, 89–178. Briskey, E. J., & Wismer-Pedersen, J. (1961a). Biochemistry of pork muscle structure. 1. Rate of anaerobic glycolysis and temperature change versus the apparent structure of muscle tissue. Journal of Food Science, 26, 297–305. Briskey, E. J., & Wismer-Pedersen, J. (1961b). Biochemistry of pork muscle structure. 2. Preliminary observations of biopsy samples versus ultimate muscle structure. Journal of Food Science, 26, 306–313. Briskey, E. J., & Wismer-Pedersen, J. (1961c). Rate of anaerobic glycolysis versus structure in pork muscle. Nature, 189, 318–320. Cameron, N. D. (1990). Genetic and phenotypic parameters for carcass traits, meat and eating quality traits in pigs. Meat Science, 27, 227–247. Carlin, K. R. M., Huff-Lonergan, E., Rowe, L. J., & Lonergan, S. M. (2006). Effect of oxidation, pH and ionic strength on calpastatin inhibition of l- and m-calpain. Journal of Animal Science, 84, 925–937. Chang, K. C., da Costa, N., Blackley, R., Southwood, O., Evans, G., Plastow, G. S., et al. (2003). Relationship of myosin heavy chain fibre types to quality traits in traditional and modern pigs. Meat Science, 64, 93–103. Chang, K. C., & Fernandes, K. (1997). Developmental expression and 5’end cDNA cloning of the porcine 2x and 2b myosin heavy chain genes. DNA Cell Biology, 16, 1429–1437. Cheah, K. S., & Cheah, A. M. (1976). The trigger for PSE condition in stress-susceptible pigs. Journal of the Science of Food and Agriculture, 27, 1137–1144. Chiang, W., Allison, C. P., Linz, J. E., & Strasburg, G. M. (2004). Identification of two aRYR alleles and characterization of aRYR transcript variants in turkey skeletal muscle. Gene, 330, 177–184. Ciobanu, D. C., Bastiaansen, J. W. M., Lonergan, S. M., Thomsen, H., Dekkers, J. C. M., Plastow, G. S., et al. (2004). New alleles in calpastatin gene are associated with meat quality traits in pigs. Journal of Animal Science, 82, 2829–2839. Ciobanu, D. C., Bastiaansen, J., Malek, M., Helm, J., Woollard, J., Plastow, G., et al. (2001). Evidence for new alleles in the protein kinase adenosine monophosphate-activated c3-subunit gene associated with low glycogen content in pig skeletal muscle and improved meat quality. Genetics, 159, 1151–1162. Ciobanu, D. C., Klont, R. E., Lonergan, S. M., Bastiaansen, J. W. M., Woollard, J. R., Malek, M., Huff-Lonergan, E. J., Plastow, G. S., Sosnicki, A. A. & Rothschild, M. F. (2002). Associations of new calpastatin gene alleles with meat quality traits in pigs. In Proceedings of the international conference of meat science and technology (pp. 614– 615). Rome, Italy. Dayton, W. R., Goll, D. E., Stromer, M. H., Robson, R. M., & Reville, W. J. (1975). Some properties of the Ca2+-activated protease that may be involved in myofibrillar protein turnover. In E. Reich, D. B. Rifkin,

59

& E. Shaw (Eds.), Proteases and Biological Control (pp. 551). Cold Spring Harbor, NY: Cold Spring Harbor Laboratory. Debut, M., Berri, C., Arnould, C., Guemene, D., Sante-Lhoutellier, V., Sellier, N., et al. (2005). Behavioural and physiological responses of three chicken breeds to pre-slaughter shackling and acute heat stress. British Poultry Science, 46(5), 527–535. Desaites, C., Bidanel, J. P., Milan, D., Iannucelli, N., Amigues, Y., Bourgeois, F., et al. (2002). Genetic linkage mapping of quantitative trait loci for behavioral and neuroendocrine stress response traits in pigs. Journal of Animal Science, 80, 2276–2285. de Vries, A., Sosnicki, A. A., Garnier, J. P., & Plastow, G. S. (1998). The role of major genes and DNA technology in selection for meat quality. In Proceedings of the international conference of meat science and technology, August 31–September 5, 1998, Session 3, II, Barcelona, Spain. de Vries, A. G., & van der Wal, P. G. (1992). Breeding for pork quality. In E. Puolanne & D. I. Demeyer (Eds.). Pork quality, genetic and metabolic factors (pp. 58–75). CAB International. de Vries, A. G., van der Wal, P. G., Eikelenboom, G., & Merks, J. W. M. (1994a). Pork quality, only 20% genetic influence? PIGS-Misset(August), 14–15. de Vries, A. G., van der Wal, P. G., Long, T., Eikelenboom, G., & Merks, J. W. M. (1994b). Genetic parameters and production traits in Yorkshire populations. Livestock Production Science, 40, 277–289. Diesbourg, L., Swatland, H. J., & Millman, B. M. (1988). X-Ray diffraction measurements of postmortem changes in the myofilament lattice of pork. Journal of Animal Science, 66, 1048–1054. Dransfield, E., & Sosnicki, A. A. (1999). Relationship between muscle growth and poultry meat quality. Poultry Science, 78, 743–746. Edwards, E. (2006). QTL mapping in an F2 Duroc · Pietrain resource population, II. Carcass and meat quality traits. Mid-West Meeting of ASAS,Des Moines. Eikelenboom, G., Van der Wal, P. G., & De Vries, A. G. (1995). The significance of ultimate pH for pork quality. In Proceedings of the International Congress of Meat Science and Technology (pp. 654–655). 20–25 August 1995, San Antonio, Texas, USA. Eikelenboom, G., Hoving-Bolink, A. H., & van der Wal, P. G. (1996). The eating quality of pork. Fleischwirtschaft International, 3, 20–21. Ender, K., Fiedler, G., & Dietl, G. (2006). The use of muscle structure traits for pig breeding. Research Institute for the Biology of Farm Animals, Dummerstorf, Germany (personal communication). Favero, T. G., Webb, J., Papiez, M., Fisher, E., Trippichio, R. J., Broide, M., et al. (2003). Hypochlorous acid modifies calcium release channel function from skeletal muscle sarcoplasmic reticulum. Journal of Applied Physiology, 94, 1387–1394. Favero, T. G., Zable, A. C., & Abramson, J. J. (1995). Hydrogen peroxide stimulates the Ca release channel from skeletal muscle sarcoplasmic reticulum. Journal of Biological Chemistry, 270, 25557–25563. Fiedler, I., Ender, K., Wicke, M., Maak, S., Lengerken, G. V., & Meyer, W. (1999). Stuctural and functional characteristics of muscle fibres in pigs with different malignant hyperthermia susceptibility (MHS) and different meat quality. Meat Science, 53, 9–15. Fields, B., Klont, R. E., Jungst, S. B., Wilson, E. R., Plastow, G. S., & Sosnicki, A. A. (2002). New DNA marker affecting muscle glycogen content, practical implications for pork quality. In Proceedings of the International Congress of Meat Science and Technology (pp. 620–62). 25–30 August 2002, Rome, Italy. Fletcher, D. L. (1999). Color variations in commercially packed broiler breast fillets. Journal of Applied Poultry Research, 8, 67–69. Fujii, J., Otsu, K., Zorzato, F., de Leon, S., Khanna, V. K., Weiler, J. E., et al. (1991). Identification of mutation in porcine ryanodine receptor associated with malignant hyperthermia. Science, 253, 448–451. Gardner, M., Huff-Lonergan, E., & Lonergan, S. M. (2005). Prediction of fresh pork quality using indicators of protein degradation and calpain activation. In Proceedings, international congress of meat science and technology (pp. 1428–1434). 6–13 August, Baltimore, Maryland. Gerbens, F., de Konig, D. J., Harders, F. L., Meuwissen, T. H., Janss, L. L., Groenen, M. A., et al. (2000). The effect of adipose and heart fatty

60

S. Barbut et al. / Meat Science 79 (2008) 46–63

acid-binding protein genes on intramuscular fat and backfat content in Meishan crossbred pigs. Journal of Animal Science, 78, 552–559. Gill, M., Gospert, M., Klont, R., Sosnicki, A. A., & Plastow, G. S. (2006). Metabolic and contractile characteristics of muscle Longissimus Thoracis and Semimembranosus from two porcine lines. Archives Tierzucht Dummerstorf, 49, 26–30. Gill, M., Oliver, M. A., Gisper, M., Diestre, A., Sosnicki, A. A., Lacoste, A., et al. (2003). The relationship between pig genetics, myosin heavy chain I, biochemical traits and meat quality of M. longissimus thoracis. Meat Science, 65(3), 1063–1070. Goll, D. E., Thompson, V. F., Li, H., Wei, W., & Cong, J. (2003). The calpain system. Physiological Reviews, 83, 731–801. Goll, D. E., Thompson, V. F., Taylor, R. G., & Christianson, J. A. (1992). Role of the calpain system in muscle growth. Biochimie, 74, 225–237. Greaser, M. L. (1986). Muscle as food. In Conversion of muscle to meat (pp. 37–95). Academic Press. Greaser, M. L., Okochi, H., & Sosnicki, A. A. (2001). Role of fiber types in meat quality. In Proceedings of the international conference of meat science and technology (pp. 34–37). Krakow, Poland. Hanenberg, E. H. A. T., & Merks, J. W. M. (2000). Optimization of pig breeding programs by implementing the Optimal Genetic Contribution theory. Journal of Animal Science, 78(S1), 68. Hoen, O. (1996). Purchasing criteria for pork raw materials in Europe and Japan, the Danish experience. In Proceedings of the Allen D. Leman Swine conference, pp. 45–50. Hool, L. C., & Corry, B. (2007). Redox control of calcium channels: From mechanisms to therapeutic opportunities. Antioxidants & Redox Signaling, 9, 409–435. Huff-Lonergan, E., Baas, T. J., Malek, M., Dekkers, J. C. M., Prusa, K., & Rothschild, M. F. (2002). Correlations among selected pork quality traits. Journal of Animal Science, 80, 2–10. Huff-Lonergan, E., Kuhlers, D. L., Lonergan, S. M., & Jungst, S. B. (1998). Characterization of pork quality in response to five generations of selection for lean growth efficiency. Journal of Animal Science, 76(1), 151–162. Huff-Lonergan, E., & Lonergan, S. M. (2005). Mechanisms of water holding capacity in meat: The role of postmortem biochemical and structural changes. Meat Science, 71, 194–204. Huff-Lonergan, E., Melody, J., Klont, R., & Sosnicki, A. A. (2003). Pork quality, current and future needs of industry and academia. In Proceedings of the 56th annual reciprocal meat conference (pp. 23–29). University of Missouri. Huff-Lonergan, E., Mitsuhashi, T., Beekman, D. D., Parrish, F. C., Jr., Olson, D. G., & Robson, R. M. (1996). Proteolysis of specific muscle structural proteins by l-calpain at low pH and temperature is similar to degradation in postmortem bovine muscle. Journal of Animal Science, 74, 993–1008. Huszar, D., Lynch, C. A., Fairchild-Huntress, V., Dunmore, J. H., & Fang, Q. (1997). Targeted disruption of the melanocortin-4 receptor results in obesity in mice. Cell, 88, 131–141. Jeon, J. T., Amarger, V., Rogel-Gaillard, C., Robic, A., & BonggamRudloff, B. (2001). Comparative analysis of a BAC contig of the porcine RN region and the human transcript map, implications for cloning trait loci. Genomics, 72, 297–303. Jeon, J. T., Carlborg, O., Tornstein, A., Giuffra, E., & Amarger, V. (1999). A paternally expressed QTL affecting skeletal and cardiac muscle mass in pigs maps to the IGF2 locus. Nature Genetics, 21, 157–158. Kapprell, H. P., & Goll, D. E. (1989). Effect of Ca2+ on binding of calpains to calpastatin. Journal of Biological Chemistry, 264, 17888–17896. Karlsson, A., Enfa¨lt, A. C., Esse´n-Gustavson, B., Lundstro¨m, K., Rydhmer, L., & Stern, S. (1993). Muscle histochemical and biochemical properties in relation to meat quality during selection for increased lean tissue growth rate in pigs. Journal of Animal Science, 71, 930–938. Karlsson, A. H., Klont, R. E., & Fernandez, X. (1999). Skeletal muscle fibers as factors for meat quality. Livestock Production Science, 60, 255–269.

Kastenschmidt, L. L., Hoekstra, W. G., & Briskey, E. J. (1966). Metabolic intermediates in skeletal muscles with fast and slow rates of postmortem glycolysis. Nature, 212, 288–289. Kendall, T. L., Koohmaraie, M., Arbona, J. R., Williams, S. E., & Young, L. L. (1993). Effect of pH and ionic strength on bovine m-calpain and calpastatin activity. Journal of Animal Science, 71, 96–104. Kim, K. S., Larsen, N., Short, T., Plastow, G., & Rothschild, M. F. (2000). A missense variation of the porcine melanocortin-4 receptor (MC4R) gene is associated with fatness, growth and feed intake traits. Genome, 11, 13–135. Kinghorn, B., & van der Werf, J. (2005). Identifying and incorporating genetic markers and major genes in animal breeding programs. International Course, Belo Horizonte,May 31–June 5, Brazil. http:// www.personal.une.edu.au/~jvanderw/brazilcourse.html. Kinghorn, B., Meszaros, S. A., & Vagg, R. D. (2002). Dynamic tactical decision systems for animal breeding. In Seventh world congress on genetics applied to livestock production. Montpellier, France. Klont, R. E., Brocks, L., & Eikelenboom, G. (1998). Muscle fibre type and meat quality. Meat Science, 49, S219–S229. Klont, R. E., Davidson, P. M., Fields, B., Knox, B. L., Van Laack, R. L. J. M., & Sosnicki, A. A. (2002). Relationship between ultimate pH and shelf life of pork loins. In Proceedings of the international congress of meat science and technology (pp. 25–30). August 2002, Rome, Italy. Knap, P. W. (1998). Internationalisation of pig breeding companies. In Proceedings of the 6thWorld congress on genetics applied to livestock production (Vol. 26, pp. 143–146). Armidale. Knap, P. W., Sosnicki, A. A., Klont, R. E., & Lacoste, A. (2002). Simultaneous Improvement of Meat Quality and Growth and Carcass Traits in Pigs. Proceedings of the 7th World Congress on Genetics Applied to Livestock Production (Vol. 31, pp. 339–346). CastanetTolosan, France: INRA. Knap, P. W., van der Steen, H. A. M., & Plastow, G. S. (2001). Developments in pig breeding and the role of research. Livestock Production Science, 72, 43–48. Koohmaraie, M., Shackelford, S. D., Wheeler, T. L., Lonergan, S. M., & Doumit, M. E. (1995). A muscle hypertrophy condition in lamb (callipyge): Characterization of effects on muscle growth and meat quality traits. Journal of Animal Science, 73, 3596–3607. Ku¨chenmeister, U., Kuhn, G., & Ender, K. (2005). Pre-slaughter handling of pigs and the effect of heart rate, meat quality, including tenderness, and sarcoplasmic reticulum Ca2+ transport. Meat Science, 71, 690–695. Ku¨chenmeister, U., Kuhn, G., Wegner, J., Nu¨rnberg, G., & Ender, K. (1999). Postmortem changes in Ca2+ transporting proteins of sarcoplasmic reticulum in dependence on malignant hyporthermia status in pigs. Molecular and Cellular Biochemistry, 195, 37–46. Larzul, C., Lefaucheur, L., Ecolan, P., Gogue, J., Talmant, A., Sellier, P., et al. (1997). Phenotypic and genetic parameters for Longissimus muscle fiber characteristics in relation to growth, carcass, and meat quality traits in Large White pigs. Journal of Animal Science, 75, 3126–3137. Larzul, C., Le Roy, P., Gogue, J., Talmant, A., Jacquet, B., Lefaucheur, L., et al. (1999). Selection for reduced muscle glycolytic potential in Large White pigs. II. Correlated responses in meat quality and muscle compositional traits. Genetics Selection Evolution, 31, 61–76. Le Bihan-Duval, E., Berri, C., Baeza, E., Sante, V., Astruc, T., Re´mignon, H., et al. (2003). Genetic parameters of meat technological quality traits in a grand-parental commercial line of turkey. Genetic Selection and Evolution, 35(6), 623–635. Le Bihan-Duval, E., Millet, N., & Re´mignon, H. (1999). Broiler meat quality: Effect of selection for increased carcass quality and estimates of genetic parameters. Poultry Science, 78, 822–826. Leeuwenburgh, C., Hansen, P. A., Holloszy, J. O., & Heinecke, J. W. (1999). Hydroxyl radical generation during exercise increases mitochondrial protein oxidation and levels of urinary dityrosine. Free Radical Biology and Medicine, 27, 186–192. Lengerken, G., Von Maak, S., Wicke, M., Fiedler, I., & Ender, K. (1994). Suitability of structural and functional traits of skeletal muscles for the

S. Barbut et al. / Meat Science 79 (2008) 46–63 improvement of meat quality in pigs. Archives of Animal Breeding (Achiv fur Tierzucht, Dummerstorf), 37, 133–143. Le Roy, P. (1998). Selection for reduced muscle glycolytic potential in Large White Pigs. I. Direct responses. Genetic Selection and Evolution, 30. Le Roy, P., Naveau, J., Elsen, M., & Sellier, P. (1990). Evidence for a new major gene influencing meat quality in pigs. Genetic Research, 55, 33–40. Lister, D. (1987). The physiology and biochemistry of the Porcine Stress Syndrome. In Tarrant, Eikeleneboom, & Monin (Eds.), Evaluation and control of meat quality in pigs, pp. 3–16. Lonergan, S. M., Huff-Lonergan, E., Rowe, L. J., Kuhlers, D. L., & Jungst, S. B. (2001b). Selection for lean growth efficiency in Duroc pigs: Influence on pork quality. Journal of Animal Science, 79, 2075–2085. Lonergan, S. M., Huff-Lonergan, E., Wiegand, B. R., & Kriese-Anderson, L. A. (2001a). Postmortem proteolysis and tenderization of top loin steaks from Brangus cattle. Journal of Muscle Foods, 12, 121–136. Lonergan, S. M., Stalder, K. J., Huff-Lonergan, E., Knight, T. J., Goodwin, R. N., Prusa, K. J., et al. (2007). Influence of lipid content on pork sensory quality within pH classification. Journal of Animal Science, 85, 1074–1079. Lutaaya, E., Misztal, I., Mabry, J. W., Short, T., Timm, H. H., & Holzbauer, R. (2001). Genetic parameter estimates from joint evaluation of purebreds and crossbreds in swine using the crossbred model. Journal of Animal Science, 79, 3002–3007. Lutaaya, E., Misztal, I., Mabry, J. W., Short, T., Timm, H. H., & Holzbauer, R. (2002). Joint evaluation of purebreds and crossbreds in swine. Journal of Animal Science, 80, 2263–2266. MacLennan, D. H., & Phillips, M. S. (1992). Malignant hyperthermia. Science, 256, 789–794. Maddock, K. R., Huff-Lonergan, E., Rowe, L. J., & Lonergan, S. M. (2005). Effect of pH and ionic strength on of l- and m-calpain inhibition by calpastatin. Journal of Animal Science, 83, 1370–1376. Malek, M. J., Dekkers, C. M., Lee, H. K., Baas, T. J., Prusa, K., HuffLonergan, E. J., et al. (2001). A molecular genome scan analysis to identify chromosomal regions influencing economic traits in the pig. II. Meat and muscle composition. Mammalian Genome, 12, 637–645. Maltby, V., Somaiya, A., French, N. A., & Stickland, N. C. (2004). In ovo temperature manipulation influences post-hatch, muscle growth in the turkey. British Poultry Science, 45(4), 491–498. Maltin, C., & Plastow, G. S. (2004). Functional genomics and proteomics in relation to muscle tissue. In M. F. W. Te Pas, M. E. Everts, & H. P. Haagsman (Eds.), Muscle Development in Livestock (pp. 267–296). Wallingford, UK: CAB International. McCurdy, R. D., Barbut, S., & Quinton, M. (1996). Seasonal effect on pale soft excudative (PSE) occurrence in young turkey breast meat. Food Research International, 29, 363–366. McKee, S. R., Hargis, B. M., & Sams, A. R. (1998). Pale, soft, and exudative meat in turkeys treated with succinylcholine. Poultry Science, 77, 356–360. McKee, S. R., & Sams, A. R. (1997). The effect of seasonal heat stress on rigor development and the incidence of pale, exudative turkey meat. Poultry Science, 76, 1616–1620. McLaren, D. (2007). Recent development in genetic improvement in pigs. Manitoba Swine Seminar, February 1, 2007 (in press). McLaren, D. G., & Schultz, C. M. (1992). Genetic selection to improve the quality and composition of pigs. In Proceedings of reciprocal meat conference (Vol. 45, pp. 15121). Meisinger, J., & Berg, E. (2006). United States pork industry pork quality survey. In Proceedings of Mid-West section of animal society of animal science, Abstract 245, March 2006, Des Moines. Melody, J. L., Lonergan, S. M., Rowe, L. J., Huiatt, T. W., Mayes, M. S., & Huff-Lonergan, E. (2004). Early postmortem biochemical factors influence tenderness and water-holding capacity of three porcine muscles. Journal of Animal Science, 82, 1195–1205. Mickelson, J. R., Gallant, E. M., Litterer, L. A., Johnson, K. M., Rempel, W. E., & Louis, C. F. (1988). Abnormal sarcoplasmic reticulum

61

ryanodine receptor in malignant hyperthermia. Journal of Biological Chemistry, 263, 9310–9315. Mickelson, J. R., & Louis, C. F. (1996). Malignant hypothermia: Excitation-contraction coupling, Ca2+ release channel and cell Ca2+ regulation defects. Physiological Reviews, 76, 537–592. Milan, D., Jeon, J. T., Looft, C., Amager, V., Thelander, M., Robic, A., et al. (2000). A mutation in PRKAG3 associated with excess glycogen in pig skeletal muscle. Science, 288, 1248–1251. Miller, R. K., (2003). Assessing consumer attitudes toward meat and meat products. In Proceedings of the international congress of meat science and technology (pp. 67–73). Campinas, Brazil. Mills, L. J. (2000). Skeletal muscle characteristics of commercial and traditional strains of turkey. PhD thesis, University of Manchester. Mitchell, M. (1999). Muscle abnormalities: Pathophysiological mechanisms. In Poultry Meat Science. In R. I. Richardson & G. C. Mead (Eds.). Poultry Science Symposium Series (Vol. 25, pp. 65–98). CABI publishing, Chapt. 3. Monin, G., & Sellier, P. (1985). Pork of low technological quality with a normal rate of muscle pH falls in the immediate postmortem period, the case of hempshire breed. Meat Science, 3, 49–63. Montaldo, H. H., & Mezera-Herrera, C. (1998). Use of molecular markers and major genes in the genetic improvement of livestock. Electronic Journal of Biotechnology, 1(2). Mormede, P., Foury, A., Geverink, N. A., Gispert, M., Hortos, M., Font, I., et al. (2004). Reponses neuroendocriniennesde stress et caracteristiques de carcasse, comparaison de cinq races de porcs. Donnees preliminares obtenues dans le project Europeen QualityPorkgenes. Journees de la Recherche Porcine en France, 36, 259–264. Morrison, E. H., Mielche, M. M., & Purslow, P. P. (1998). Immunolocalisation of intermediate filament proteins in porcine meat. Fiber type and muscle-specific variations during conditioning. Meat Science, 50, 91–104. Morzel, M., Chambon, C., Hamelin, M., Sante-Lhoutellier, V., Sayd, T., & Monin, G. (2004). Proteome changes during pork meat aging following use of two different pre-slaughter handling procedures. Meat Science, 67, 689–696. Nezer, C., Moreau, I., Karim, L., Brouwers, B., & Coppieters, W. (1999). An imprinted QTL with major effects on muscle mass and fat deposition maps to the IGF2 locus in pigs. Nature Genetics, 21, 155–156. Offer, G. (1991). Modelling of the formation of pale, soft, and exudative meat: Effects of chilling regime and rate and extent of glycolysis. Meat Science, 30, 157–184. Ogawa, Y. (1994). Role of ryanodine receptors. Critical Reviews in Biochemistry and Molecular Biology, 29, 229–274. Otsu, K., Khanna, V. K., Archibald, A. L., & MacLennan, D. H. (1991). Cosegregation of porcine malignant hyperthermia and a probable causal mutation in the skeletal muscle ryanodine receptor gene in backcross families. Genomics, 11, 744–750. Ovolo, C., Clop, A., Noguera, J. L., Olivers, M. A., Barragan, C., Rodriquez, C., et al. (2002). Quantitative trait locus mapping of meat quality traits in an Iberian · Landrace F2 pig population. Journal of Animal Science, 80, 2801–2808. Owens, C. M., Hirschler, E. M., McKee, S. R., Martinez-Dawson, R., & Sams, A. R. (2000a). The characterization and incidence of pale, soft, exudative turkey meat in a commercial plant. Poultry Science, 79, 553–559. Owens, C. M., Matthews, N. S., & Sams, A. R. (2000b). The use of halothane gas to identify turkeys prone to developing pale, exudative meat when transported before slaughter. Poultry Science, 79, 789–795. Owens, C. M., McKee, S. R., Matthews, N. S., & Sams, A. R. (2000c). The development of pale, exudative meat in two genetic lines of turkeys subjected to heat stress and its prediction by halothane screening. Poultry Science, 79, 30–435. Penny, I. F. (1967). The influence of pH and temperature on the properties of myosin. Biochemical Journal, 104, 609–615. Perez, M., Casey, D., & McLaren, D. (2006). Crossbred breeding values, Selecting for commercial performance. In The proceedings of the 37th

62

S. Barbut et al. / Meat Science 79 (2008) 46–63

annual meeting of the american association of swine veterinarians, pp. 83–84. Pietrzak, M., Greaser, M. L., & Sosnicki, A. A. (1997). Effect of rapid rigor mortis processes on protein functionally in pectoralis major muscle of domestic turkeys. Journal of Animal Science, 75, 2106–2116. Plastow, G. S. (2002). Needs for Biotechnology in Animal Production. In K. Schellander, N. Li, A. M. Neeteson, & K. Wimmers (Eds.), Genomics and Biotechnology in Livestock Breeding (pp. 11–18). Aachen: Shaker Verlag. Pontremoli, S., Melloni, E., Viotti, P. L., Michetti, M., Salamino, F., & Horecker, B. L. (1991). Identification of two calpastatin forms in rat skeletal muscle and their susceptibility to digestion by homologous calpains. Archives of Biochemistry and Biophysics, 288, 646–652. Raser, K. D., Posner, A., & Wang, K. W. (1995). Casein Zymography: A method to study l-calpain, m-calpain and their inhibitory agents. Archives of Biochemistry and Biophysics, 319, 211–216. Rasmusen, B. A., & Christian, L. L. (1976). H blood types in pigs as predictors of stress susceptibility. Science, 191, 947–948. Rohrer, G.A., Beever, A.D., Rothschild, M.F., Schook, L. Gibbs, A., & Weinstock, A. USDA-ARS, U of IL, ISU, Baylor College of Medicine.(2005). Porcine Sequencing White Paper, Porcine Genomic Sequencing Initiative. http://www.csrees.usda.gov/nea/animals/pdfs/ porcine_genome.pdf. Rohrer, G. A., Thallman, R. M., Shackelford, S., Wheeler, T., & Koohmaraie, M. (2005). A genome scan for loci affecting pork quality in a Duroc-Landrace F2 population. Animal Genetics, 37, 17–27. Rothschild, M. F., Bidanel, J. P., & Ciobanu, D. (2004). Genome analysis of QTL for muscle tissue development and meat quality. Muscle Development of Livestock Animals. CAB International, pp. 247–262. Rothschild, M. F., & Plastow, G. S. (1999). Advances in pig genomics and industry applications. Agricultural Biotechnology Network, 10, 1–8. Rowe, L. J., Maddock, K. R., Lonergan, S. M., & Huff-Lonergan, E. (2004a). Influence of early postmortem protein oxidation on beef quality. Journal of Animal Science, 82, 785–793. Rowe, L. J., Maddock, K. R., Lonergan, S. M., & Huff-Lonergan, E. (2004b). Oxidative environments decrease tenderization of beef steaks through inactivation of l-calpain. Journal of Animal Science, 82, 3254–3266. Sams, A. R., & Alvarado, C. Z. (2004). Turkey carcass chilling and protein denaturation in the development of pale, soft, and exudative meat. Poultry Science, 83, 1039–1048. SanCristobal, M., Chevalet, C., Haley, C. S., Russell, G., Plastow, G., Siggens, K., et al. (2002). Genetic diversity in pigs – preliminary results on 58 European breeds and lines. Proceedings of the 7thWorld congress on genetics applied to livestock production (Vol. 33, pp. 525–528). Castanet-Tolosan, France: INRA. Sante, V., Bilicki, G., Renerre, M., & Lacourt, A. (1991). Post mortem evaluation in the pectoralis superficialis muscle from two turkey breeds: A relationship between pH and color. In Proceedings of the 37th international congress on meat science (pp. 465–468). Germany. Schiaffino, S., & Reggiani, C. (1996). Molecular diversity of myofibrillar proteins, Gene regulation and functional significance. Physiological Reviews, 76, 371–423. Sellier, P. (1998). Genetics of meat and carcass traits. In M. F. Rothschild & A. Ruvinsky (Eds.), The genetics of the PIG (pp. 463–510). Wallingfors, United Kingdom: CABI. Short, T. H., Rothschild, M. F., Southwood, O. I., McLaren, D. G., de Vries, A., van der Steen, H., et al. (1997). Effect of the estrogen receptor locus on reproduction and production traits in four commercial pig lines. Journal of Animal Science, 75, 3138–3142. Sosnicki, A. A., Pommier, S., Klont, R., Newman, S., & Plastow, G. S. (2003). Best-cost production of high quality pork, bridging the gap between pig genetics, muscle biology/meat science and consumer trends. In Proceedings of manitoba pork seminar. Sosnicki, A. A., Wilson, E. R., Sheiss, E. B., & de Vries, A. (1998). Is there a cost effective way to produce high-quality pork? Reciprocal Meat Conference Proceedings, 51, 19–27.

Stabursvik, E., Fretheim, K., & Frøystein, T. (1984). Myosin denaturation in pale, soft, and Exudative (PSE) porcine muscle tissue as studied by differential scanning calorimetry. Journal of the Science of Food and Agriculture, 35, 240–244. Sutko, J. L., & Airey, J. A. (1996). Ryanodine receptor Ca++ release channel: does diversity in form equal diversity in function? Physiological Reviews, 76, 1027–1071. Suzuki, K. (1990). The structure of calpains and the calpain gene. In R. L. Mellgren & T. Murachi (Eds.), Intracellular calcium-dependent proteolysis (pp. 25–35). Boca Raton, FL: CRC Press. Swatland, H. J. (1985). A computer-operated rigorometer for studying the development of rigor mortis in excised samples of pork and beef. Canadian Institute of Food Science and Technology, 18(3), 207–212. Swatland, H. J. (1990a). Effect on pH on the birefringence of skeletal muscle fibers measured with a polarizing microscope. Trans American Microscopy Society, 109(4), 361–367. Swatland, H. J. (1990b). A note on the growth of connective tissues binding turkey muscle fibers together. Canadian Institute of Food Science and Technology Journal, 23, 239–241. Swatland, H. J. (1995). Reversible pH effect on pork paleness in a model system. Journal of Food Science, 60(5), 988–991, & 995. Swatland, H. J. (2004). Progress in understanding the paleness of meat with a low pH. South African Journal of Animal Science, 34, 1–7. Swatland, H. J., & Belfry, S. (1985). Post mortem changes in the shape and size of myofibrils from skeletal muscle of pigs. Mikroskopie (Wien), 42, 26–34. Swatland, H. J., Irving, T. C., & Millman, B. M. (1989). Fluid distribution in pork, measured by x-ray diffraction, interference microscopy and centrifugation compared to paleness measured by fiber optics. Animal Science, 67(6), 1465–1470. Tanabe, R., Murroya, S., Chikuni, K., & Nakai, H. (1997). The difference in the ratio of each myosin heavy chain isoform content among porcine skeletal muscles. International Congress of Meat Science and Technology, 696–697. Toniolo, L., Patruno, M., Maccatrozzo, L., Pellegrino, M. A., Canepari, M., Rossi, R., et al. (2004). Fast fibres in a large animal, fiber types, contractile properties and myosin expression in pig skeletal muscles. Journal of Experimental Biology, 207, 1875–1886. Topel, D. G., Bicknell, E. J., Preston, K. S., Christian, L. L., & Matsushima, L. Y. (1969). Porcine stress syndrome. Modern Veterinary Practice, 49, 40–60. Vanderstoep, J., & Richards, J. F. (1974). Post mortem, glycolytic and physical changes in turkey breast muscle. Canadian Institute of Food Science and Technology Journal, 7, 120–125. Van der Werf, J. H. J., Van der Wei, M., & Brascamp, E. W. (1994). Combined crossbred and purebred selection to maximize genetic response in crossbreds. In Proceedings 5th World congress on genetics applied to livestock production (Vol. 18, pp. 266–269). Van Wijk, H. J., Dibbits, B., Baron, E. E., Brings, D. D., Harlizius, B., Groenen, M. A., et al. (2006). Identification of quantitative trait loci for carcass composition and pork quality traits in a commercial finishing cross. Journal of Animal Science, 84, 789–799. Vogeli, P. (1992). Genetics and Porcine Stress Syndrome and association with oedema disease. In E. Puolanne & D. I. Demeyer (Eds.). Pork quality, genetic and metabolic factors (pp. 22–36). CAB International, 58-75. Vogeli, P., Schworer, D., Kuhne, R., & Wysshaar, M. (1985). Trends in economic traits, halothane sensitivity, blood groups and enzyme systems of Swiss Landrace and Large White pigs. Animal Blood Groups Biochemistry and Genetics, 16, 285–296. Wang, L., Brem, T. M., Zarosley, J., Booren, A. M., & Strasburg, G. M. (1999). Skeletal muscle calcium channel ryanodine binding activity in genetically unimproved and commercial turkey populations. Poultry Science, 78, 792–797. Wimmers, K., Fiedler, I., Hardge, T., Murani, E., Schellander, K., & Ponsuksilli, S. (2006). QTL for micostructural and biophysical

S. Barbut et al. / Meat Science 79 (2008) 46–63 muscle properties and body composition in pigs. BMC Genetics, 7, 15. Wood, J. D., Holder, J. S., & Main, D. C. J. (1998). Quality Assurance Schemes. In Proceedings of the 44th international congress of meat science and technology (Vol. 1, pp. 206–215). Barcelona, Spain. Woolliams, J. A., Bijma, P., & Villanueva, B. (1999). Expected genetic contributions and their impact on gene flow and genetic gain. Genetics, 153, 1009–1020.

63

Zhang, L., & Barbut, S. (2005). Effect of regular and modified starches on cooked PSE, normal and DFD chicken breast meat batters. Poultry Science, 84, 789–796. Zhang, W. G., Lonergan, S. M., Gardner, M. A., & Huff-Lonergan, E. (2006). Contribution of postmortem changes of integrin, desmin and l-calpain to variation in water holding capacity of pork. Meat Science, 74, 578–585. Zissimopoulos, S., & Lai, F. A. (2006). Redox regulation of the ryanodine receptor/calcium release channel. Biochemical Society Transactions, 34, 919–921.