The effect of nutrition on muscle ph decline and ultimate ph post mortem in sheep and cattle
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1 33 The effect of nutrition on muscle ph decline and ultimate ph post mortem in sheep and cattle G.E. Gardner 1,2, B.L. Daly 1, J.M. Thompson 1 and D.W. Pethick 2 1 School of Rural Science and Agriculture, The University of New England, Armidale NSW 2351, g.gardner@murdoch.edu.au 2 School of Veterinary and Biomedical Sciences, Murdoch University, Murdoch WA 150 Summary This paper reviews the effect of nutrition on rate of post mortem ph decline, ph change after electrical stimulation (delta ph) and ultimate ph in skeletal muscle of sheep and cattle. The importance of muscle glycogen concentration as a determinant of ultimate ph, delta ph and rate of ph decline post mortem is illustrated. As delta ph and rate of ph decline are increased by high muscle glycogen concentration, nutrition may affect the rate of ph decline through its effect on glycogen concentration. Muscle type also has an effect on the rate of ph decline: white muscles comprised of fast glycolytic fibres have greater rates of ph decline and delta ph than red, oxidative muscles. The effect of nutritional restriction on muscle fibre type and rate of ph decline through its effect on physiological maturity and metabolic enzyme expression is discussed. Keywords: fibre type, glycogen, electrical stimulation Introduction After slaughter, muscle glycogen induces the gradual acidification of muscle via glycolytic production of lactic acid, decreasing ph from about 7.2 to an ultimate ph (phu) of Poor nutrition and stress can reduce muscle glycogen content at slaughter, resulting in elevated phu, which, when greater than ph , can result in dark, firm and dry meat (DFD). Glycolysis and the associated ph decline are of primary importance for meat quality during processing. The rate of ph decline in a carcass relative to the chilling rate affects meat tenderness, water binding capacity, colour and colour stability. Electrical stimulation is used to control the rate of glycolysis and has been optimised for specific slaughter operations in recent years. Despite these efforts, there is evidence suggesting that considerable variation in the rate of glycolysis still exists (Daly, 2005). Post slaughter glycolytic rate is influenced by a number of factors. Many of these are associated with temperature, including variations in thermal inertia due to carcass size and fat depth, and chilling practices (Jolley et al. 1981). However, the metabolic characteristics of muscle may also play a role. Skeletal muscle consists of several fibre types, the two main groups being type I (slow), and type II (fast) fibres. Type II fibres are classified as type IIA, fast oxidative fibres, and type IIB, fast glycolytic fibres (Conlee et al. 1978). Because glycolytic rates are greater in type IIB fibres than in type I or IIA fibres, muscles with greater proportions of type IIB fibres display greater glycolytic rates in living tissue (Lawrie 1992). Factors that affect the prevalence of these fibre types within muscles, such as genotype and nutrition, may result in variation in glycolytic rate between animals. Furthermore, the substrate for glycolysis may also be a rate limiting factor. The aim of this paper is to review recent experiments focusing on the impact of nutrition on the rate of ph decline in skeletal muscles of cattle and sheep. The effect of muscle glycogen The importance of muscle glycogen is well known within the meat industry, particularly its role in determining ultimate ph and the incidence of dark cutting. Numerous studies have shown that as muscle glycogen increases, ultimate ph decreases until it reaches levels of (depending on species and muscle), usually correlating with muscle glycogen concentrations of about mmol/kg wet tissue. This relationship is demonstrated in Figure 1, which shows data for m. semimembranosus (SM), m. semitendinosus (ST) and m. longissimus dorsi (LD) of two year old Merino wethers. Muscle glycogen concentration is also implicated in control of the rate of ph decline. Daly et al. (2005) demonstrated that an increased muscle glycogen concentration increases the delta ph response to electrical stimulation (i.e., the decrease in ph during stimulation), particularly in muscle tissue that has a pre stimulation ph of. or less (Figure 2). This is particularly Recent Advances in Animal Nutrition in Australia, Volume 15 (2005)
2 34 Gardner et al. important in fast glycolytic muscles such as the ST, which generally have a lower pre stimulation ph than others. Increasing muscle glycogen concentration reduced ph at 1.5 hours post mortem in beef and veal carcases (Figure 5)...4 LD SM ST LD SM ST Ultimate ph Muscle Glycogen (mmol/kg wet muscle tissue) Delta ph Muscle Glycogen Glycogen Concentration (mmol/kg wet muscle tissue) tissue) Figure 1 Effect of muscle glycogen concentration on ultimate ph in m. semimembranosus (SM), m. semitendinosus (ST) and m. longissimus dorsi (LD) of sheep (Daly et al. 2005). Values are least square means ± S.E. Figure 3 Delta ph at various muscle glycogen concentrations in the m. semimembranosus (SM), m. semitendinosus (ST) and m. longissimus dorsi (LD) of sheep (Daly et al. 2005). Values are least square means ± S.E. Delta ph ph at 3 Hours h..4 Non Stimulated Stimulated Pre-Stimulation ph =.8 Pre-Stimulation ph =. Pre-Stimulation ph = Glycogen Concentration (mmol/kg wet muscle tissue) Glycogen Concentration (mmol/kg wet muscle tissue) Figure 2 Effect of pre stimulation ph on delta ph at various muscle glycogen concentrations in sheep (Daly et al. 2005). Values are least square means ± S.E Muscle Glycogen (mmol/kg wet wet muscle tissue) tissue) Figure 4 Effect of electrical stimulation on ph at 3 hours post mortem in three muscles (LD, SM, ST) at various muscle glycogen concentrations in sheep (Daly et al. 2005). Values are least square means ± S.E. The importance of muscle glycogen concentration for delta ph differs between muscles, irrespective of pre stimulation ph (Daly et al. 2005); the locomotive ST and SM muscles are more strongly influenced than the LD (Figure 3). Taken together, the results shown in Figures 2 and 3 highlight the importance of substrate (i.e., glycogen) for delta ph in fast glycolytic muscle tissue under more intense contractile states. Irrespective of stimulation responses, the overall rate of ph decrease post mortem is also influenced by muscle glycogen concentration. Daly et al. (2005) demonstrated that increased muscle glycogen increased the rate of ph decline in 2 year old Merino wethers; this response was greater in post electrically stimulated muscle tissue (Figure 4). The effect of muscle glycogen concentration has also been demonstrated in cattle (Daly et al. 2002). ph at 1.5 hrs h PM Non LVES LVES - Veal Muscle Glycogen (mmol/kg wet muscle tissue) Muscle Glycogen (mmol/kg wet muscle tissue) Figure 5 Effect of muscle glycogen concentration (mmol/ kg wet muscle tissue) on ph at 1.5 hours post mortem (PM) in beef that was not subject to low voltage electrical stimulation (LVES) and veal that was subjected to LVES (Daly et al. 2002). Values are least square means ± S.E.
3 The effect of nutrition on muscle ph decline and ultimate ph post mortem in sheep and cattle 35 Nutrition is a major determinant of muscle glycogen concentration in sheep (Pethick and Rowe 199) and cattle (Gardner et al. 2001). Responses to nutrition are greater in red aerobic muscles than in other types (Figure ). Martin et al. (2004) increased metabolizable energy (ME) intakes of four month old Merino and Poll Dorset lambs two weeks prior to sampling and observed increased basal glycogen concentrations in muscles; this effect was more pronounced in the red SM. Thus, high ME diets that increase muscle glycogen concentration will reduce the incidence of dark cutting and increase the response to electrical stimulation, but this effect will differ between muscles. Effects of muscle fibre type Muscle type affects delta ph and the amount of stored glycogen. These differences are evident from rates of ph decline in the study of Daly et al. (2005): at 3 h post mortem, the fast glycolytic ST had a lower ph than the LD or SM, irrespective of muscle glycogen concentration (Figure 7). Muscle Glycogen Glygocen Concentration Concentratin (mm) Figure The effect of metabolizable energy intake on basal muscle glycogen concentration in m. semimembranosus (SM) and m. semitendinosus (ST) of sheep (Martin et al. 2004). Values are least square means ± S.E. ph ph at 3 at Hours 3 h 100 SM 90 ST ME ME intake Intake 22 w pre exercise pre-exercise (MJ/day) (MJ/day) LD SM ST Muscle Muscle Glycogen (mmol/kg wet wet muscle muscle tissue) tissue) Figure 7 Effect of muscle glycogen concentration (mmol/ kg wet muscle tissue) on ph at 3 h post mortem in the m. semimembranosus (SM), m. semitendinosus (ST) and m. longissimus dorsi (LD) of sheep (Daly et al. 2005). Values are least square means ± S.E. The mechanism of this effect of fibre type is poorly understood. Gardner et al. (2002) compared nine month old Piedmontese calves (characterised by double muscling) with Angus and Wagyu cross breed calves. Because selection for muscling increases the expression and size of fast glycolytic type IIB fibres (Wegner et al. 2000), muscle of Piedmontese calves is likely to have a high glycolytic capacity. The more glycolytic muscle types are likely to express higher myofibrillar and sarcoplasmic reticulum Ca 2+ dependent ATPases. SM and ST muscles of Piedmontese and Angus cattle had higher (P<0.05) Ca 2+ dependent myofibrillar ATPase activities (0.1 ± 0.00) than those of Wagyu cattle (0.14 ± 0.003). Piedmontese cattle had higher (P<0.05) sarcoplasmic reticulum Ca 2+ dependent ATPase activities of SM and ST (0.034 ± 0.003) than either Angus or Wagyu (0.028 ± 0.003). These results highlight the fast glycolytic nature of the muscles of the Piedmontese. Delta ph of SM and ST decreased to a greater extent (P<0.01) in the Piedmontese (0.2 ±.07) than in the Angus or Wagyu (0.05 ± 0.07). Considering that ATPase activities were interchangeable with breed in a linear model describing delta ph, the breed effect may have been mediated by ATPase activity. ATPase activities also differed between muscles. Higher Ca 2+ dependent myofibrillar ATPase activity and lower total Mg 2+ dependent ATPase activity were observed in the faster, anaerobic ST (0.17 ± 0.00 and 0.17 ± 0.010, respectively) than in the more aerobic SM (0.13 ± 0.00 and 0.22 ± 0.010, respectively). Thus, these ATPases may also determine differences in the rate of ph decline between muscles. The rate of ph decline may be more dependent on expression of glycolytic pathway enzymes. Gardner et al. (2005) demonstrated that nutrition and muscle fibre type (based on myosin heavy chain isoform staining) affected expression of key glycolytic and tricarboxylic acid cycle enzymes. Lambs fed at a low level of nutrition had a higher ratio of glycolytic:oxidative fibre types (3.13 ± 0.122) than those fed at a high level of nutrition (2.2 ± 0.117; Greenwood et al. 2005). As carcasses of lambs fed at the low level of nutrition weighed less (low nutrition, 1.7 ± 0.5 kg; high nutrition, 27.0 ± 0.5 kg), had reduced fatness (GR tissue depth: low nutrition, 8.2 ± 3.77 mm; high nutrition, 23.7 ± 3.78 mm) and had reduced skeletal maturity (Cake et al. 2005), it is likely that they were physiologically less mature. The fibre type differences are consistent with results of Brandstetter et al. (1998a), who demonstrated that young, growing bulls express proportionately more slow type 1 muscle fibres as they mature. However, other work by Brandstetter et al. (1998b) demonstrated that nutritional restriction in growing bulls resulted in increased oxidative enzyme activity, a metabolically more efficient system for energy production. This finding is also consistent with that of Gardner et al. (2005), who observed increased activity of the oxidative enzyme, citrate synthase (Figure 8), and decreased expression
4 3 Gardner et al. of the glycolytic enzymes, phosphofructokinase and lactate dehydrogenase (Figure 9), in all muscles tested in lambs fed a low plane of nutrition. However, evidence of decreased expression of the oxidative enzyme, isocitrate dehydrogenase, and the oxygen binding protein, myoglobin, (Figure 8) is contrary to the general trend. It is suggested that, although nutrition has a strong influence on the metabolic characteristics of muscle in so far as expression of glycolytic enzymes is concerned, it does not override the effect that maturity has on the differentiation of muscle into various fibre types. Furthermore, it appears that the nutritional environment may, to some extent, uncouple the link between fibre type and metabolic enzyme expression. In the study of Gardner et al. (2005), correlations were determined between metabolic enzyme expression and post mortem rate of ph decline. Lactate dehydrogenase had the greatest correlation coefficient (0.50), and a linear model for estimating the rate of ph decline (ph slope in Figure 10) predicted an interaction between lactate dehydrogenase activity and concentration of lactate 10 minutes post slaughter. This suggests that lactate dehydrogenase activity is important for ph slope only when lactate concentrations are low, a state that coincides with the early stage of the ph decline. Thus, given its effect on muscle fibre type, nutrition is likely to have a considerable effect on the rate of ph decrease. Figure 10 The effect of lactate dehydrogenase activity and muscle lactate concentration (mm) in the m. longissimus thoracis et lumborum on ph slope in sheep (Gardner et al. 2005). Values are least square means ± S.E. Figure 8 The effect of nutrition and muscle on the activities of isocitrate dehydrogenase (µmol/min/g tissue), citrate synthase (µmol/min/g tissue) and concentration of myoglobin (mg/g tissue) in sheep (Gardner et al. 2005). Values are least square means ± S.E. SM, m. semimembranosus; ST, m. semitendinosus; LT, m. longissimus thoracis et lumborum. Figure 9 The effect of nutrition and muscle on the activities of fructose 1, bisphosphatase (µmol/min/g tissue) 10 1 ), phosphofructokinase (µmol/min/g tissue) 0.5) and lactate dehydrogenase (µmol/ min/g tissue) 10 2 ) in sheep (Gardner et al. 2005). Values are least square means ± S.E. SM, m. semimembranosus; ST, m. semitendinosus; LT, m. longissimus thoracis et lumborum.
5 The effect of nutrition on muscle ph decline and ultimate ph post mortem in sheep and cattle 37 Conclusion Nutrition and muscle glycogen concentration are important determinants of ultimate ph, delta ph and rate of ph decrease post mortem. Muscle fibre type also influences the rate of ph decrease, but the exact mechanisms responsible are unclear. The effect of pasture based nutrition on fibre type suggests that potential exists to affect the rate of ph decrease. References Brandstetter, A.M., Picard, B. and Geay, Y. (1998a). Muscle fibre characteristics in four muscles of growing bulls. I. Postnatal differentiation. Livestock Production Science 53, Brandstetter, A.M., Picard, B. and Geay, Y. (1998b). Muscle fibre characteristics in four muscles of growing male cattle. II. Effect of castration and feeding level. Livestock Production Science 53, Cake, M.A., Gardner, G.E., Hegarty, R.S., Boyce, M.D. and Pethick, D.W. (2005). Effect of Nutritional Restriction and Sire Genotype on Forelimb Bone Growth and Carcase Composition in Crossbred lambs. Australian Journal of Agricultural Research, (submitted). Conlee, R.K., Hickson, R.C., Winder, W.W., Hagberg, J.M. and Holloszy, J.O. (1978). Regulation of glycogen resynthesis in muscles of rats following exercise. American Journal of Physiology 235, R Daly, B.L. (2005). Factors Affecting Rate of ph Decline in Bovine Muscle Post Mortem, PhD thesis. School of Rural Science and Agriculture, University of New England, Armidale, Australia. Daly, B.L., Gardner, G.E., Ferguson, D.M. and Thompson, J.M. (2005). The effect of time off feed prior to slaughter on muscle glycogen metabolism and rate of ph decline. Australian Journal of Agricultural Research, (submitted). Daly, B.L., Richards, I., Gibson, P.G., Gardner, G.E. and Thompson, J.M. (2002). Rate of ph decline in bovine muscle post mortem a benchmarking study. International Congress of Meat Science and Technology 2, Gardner, G.E., Kuypers, R., Thompson, J.M., Daly, B.L., Hearnshaw, H., Greenwood, P. and Pethick, D.W. (2002). Effect of breed, electrical stimulation, and muscle on rate of ph decline and ultimate ph in cattle post mortem. International Congress of Meat Science and Technology 2, 5 7. Gardner, G.E., McIntyre, B.L., Tudor, G. and Pethick, D.W. (2001). The impact of nutrition on bovine muscle glycogen metabolism following exercise. Australian Journal of Agricultural Research 52, Gardner, G.E., Pethick, D.W., Greenwood, P.L. and Hegarty, R.S. (2005). The effect of genotype and plane of nutrition on rate of ph decline post mortem and the expression of enzymatic markers of metabolism in lamb carcases. Australian Journal of Agricultural Research, (submitted). Greenwood, P.L., Gardner, G.E., Hegarty, R.S. (2005). Myofibre characteristics are influenced by sire estimated breeding values and nutrition of lambs from birth to slaughter at 8 months of age. Australian Journal of Agricultural Research, (submitted). Jolley, P.D., Honikel, K.O. and Hamm, R. (1981). Influence of temperature on the rate of post mortem metabolism and water holding capacity of bovine neck muscles. Meat Science 5, Lawrie, R.A. (1992). Conversion of muscle into meat: biochemistry. Royal Society of Chemistry, special publication No. 10. Martin, K.M., Gardner, G.E., Thompson, J.M. and Hopkins, D.L. (2004). Nutritional impact on muscle glycogen metabolism in lambs selected for muscling. Journal of Animal and Feed Sciences 13 (Suppl. 1). Pethick, D.W. and Rowe, J.B. (199). The effect of nutrition and exercise on carcass parameters and the level of glycogen in skeletal muscle of Merino sheep. Australian Journal of Agricultural Research 47, Wegner, J., Albrecht, E., Fiedler, I., Teuscher, F., Papstein, H.J. and Ender, K. (2000). Growth and breed related changes of muscle fibre characteristics in cattle. Journal of Animal Science 78,
6 38 Gardner et al.
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