Energy supply patterns for finishing steers: Feed conversion efficiency, components of bodyweight gain and meat quality

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MEAT SCIENCE Meat Science 79 (2008) 86–97 www.elsevier.com/locate/meatsci

Energy supply patterns for finishing steers: Feed conversion efficiency, components of bodyweight gain and meat quality A.P. Moloney

a,b,*

, M.G. Keane a, M.T. Mooney b, K. Rezek F.J.M. Smulders c, D.J. Troy b

c,1

,

a

Teagasc, Grange Beef Research Centre, Dunsany, Co. Meath, Ireland Teagasc, Ashtown Food Research Centre, Ashtown, Dublin 15, Ireland Institute of Meat Hygiene, Meat Technology and Food Science, University of Veterinary Medicine, Vienna, Austria b

c

Received 18 April 2007; received in revised form 15 August 2007; accepted 19 August 2007

Abstract The objective was to determine the effect of pre-slaughter growth rate on feed efficiency, components of body growth and on the tenderness of longissimus muscle from steers reared to a common age and carcass weight. Sixty Friesian steers were group-housed and offered grass silage ad libitum and 3.5 kg concentrates per animal daily for 5 months and then 5 kg concentrates and 1 kg grass hay for 1 month before the experiment began. The animals were then weighed and in a randomised block were assigned to one of 5 groups, for slaughter at the beginning of the experiment or to be offered concentrates and hay (900 and 100 g/kg total diet, respectively) to achieve target growths of: 0.72 kg/day continuously for 17 weeks, 0.36 kg/day for the first 8 weeks and 1.08 kg/day for the final 8 weeks (low–high), 1.08 kg/day for the first 8 weeks and 0.36 for the final 8 weeks (high–low) or 0.36 kg/day for the first 2 weeks, 0.72 kg/day during weeks 4 and 14 and 1.08 kg/day for the final 2 weeks (pulse). One week was allowed for transition to the different dietary allowances within each energy supply pattern. The mean age at the beginning and end of the study was 18 and 22.5 months, respectively. After slaughter, the weight of the carcass and kidney + channel fat depot were recorded, the pistola hind quarter was dissected into fat, lean and bone and the tenderness of the m. longissimus thoracis et lumborum (LTM) muscle was measured instrumentally and using a trained taste panel after 2, 7 or 14 days ageing. The pattern of energy supply did not affect carcass weight, fat score or kidney + channel fat weight. The pistola hind quarter from animals offered the low–high energy pattern had a similar composition to the continuously-fed animals but contained more muscle than that from animals offered high–low or pulse energy patterns. After 14 days ageing, LTM from the continuously-fed animals was more tender than that from animals offered the other energy supply patterns but shear force did not differ between supply patterns. The data do not support the hypothesis that pre-slaughter growth rate increases tenderness but suggest that energy supply pattern can influence body composition of finishing cattle.  2007 Elsevier Ltd. All rights reserved. Keywords: Beef; Energy; Muscle growth; Tenderness; Calpains; Sensory analysis

1. Introduction The sensory perception of tenderness is generally considered to be a major influence on consumer decisions to (re)* Corresponding author. Address: Teagasc, Grange Beef Research Centre, Dunsany, Co. Meath, Ireland. Tel.: +353 46 9061100; fax: +353 46 9026154. E-mail address: [email protected] (A.P. Moloney). 1 Present address: Baxter Bioscience, Lange Allee 24, 1220 Vienna, Austria.

0309-1740/$ - see front matter  2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.meatsci.2007.08.004

purchase beef (Grunert, Bredahl, & Bunsae, 2004). Much research effort has been directed at identifying influences on tenderness within beef production systems and the consensus is that post-slaughter management has a greater influence on tenderness, as experienced by the consumer, than pre-slaughter or ‘‘on-farm’’ factors (Owens & Gardiner, 1999; Thompson, 2002). Pre-slaughter growth rate is one ‘‘on-farm’’ factor that has been reported to influence beef tenderness (e.g. Aberle, Reeves, Judge, Hunsley, & Perry, 1981; May, Dolezal, Gill, Ray, & Buchanan,

A.P. Moloney et al. / Meat Science 79 (2008) 86–97

2. Materials and methods 2.1. Experimental design and animal management Sixty Friesian steers (12 months of age) were grouphoused and offered grass silage ad libitum and 3.5 kg proprietary concentrates per animal daily for 5 months. They were then offered 5 kg concentrates and 1 kg grass hay for one month before the experiment began. The concentrate consisted of (g/kg): sugar beet pulp 802, soyabean meal 135, fat 45 and a proprietary mineral and vitamin mix 18. The chemical composition of the concentrate was: dry matter (DM) (883, SD 7.14 g/kg), crude protein (163, SD 7.6 g/kg DM), ash (70, SD 1.0 g/kg DM), acidhydrolysed ether extract (64, SD 1.2 g/kg DM), neutral detergent fibre (386, SD 18.0 g/kg DM) and metabolisable energy (14, SD 0.1 MJ/kg DM). The hay contained 852 (SD 30.8) g DM/kg and 109 (SD 13.79) g crude protein/ kg DM and had a DM digestibility of 688 (SD 19.2)

g/kg. The animals were then weighed on consecutive days, and based on mean bodyweight and age assigned to one of 5 groups in a randomised block design. The 5 groups were then randomly assigned to one of 4 treatment groups or for slaughter at the beginning of the experiment. The animals were penned individually and offered the above concentrates and hay (900 g and 100 g/kg total diet, respectively). At the commencement of the experiment (mean age 18 months), one group of animals was slaughtered (details below) and the remaining groups were assigned to one of four energy supply patterns based on individual bodyweight (Fig. 1) to achieve target growth rates (AFRC (1993)) of: (i) 0.72 kg/day throughout the study (continuous), (ii) 0.36 kg/day for the first 8 weeks, transition to higher dietary allowance in week 9 and 1.08 kg/day for the final 8 weeks (low–high), (iii) 1.08 kg/day for the first 8 weeks, transition to lower dietary allowance in week 9 and 0.36 for the final 8 weeks (high–low) or (iv) 0.36 kg/ day for the first 2 weeks transition to higher dietary allowance in week 3, 0.72 kg/day during weeks 4 and 14 transition to higher dietary allowance in week 15 and 1.08 kg/ day for the final 2 weeks (pulse). To facilitate pre- and post-slaughter management, animals were assigned to 4 groups, balanced for treatment and on a descending block basis. The groups started the experiment in sequence with an interval of 1 week between each start date. Animals were offered their daily concentrate allowances individually, in 2 equal feeds (hay in one feed daily) and were weighed at 2 week intervals. Feed allowances were adjusted on a 4-week basis, or as appropriate to each pattern. On the day before slaughter urine was collected from each animal in the low–high and high–low groups for 4 h. Urine was acidified with 500 ml of 0.5 M hydrochloric acid/l, filtered and samples were stored at 20 C for analysis of creatinine and methylhistidine concentrations. On each day of slaughter, (mean age 22.5 months) animals were weighed, transported 120 km to a commercial slaughter facility and slaughtered at random within 4 h of removal from their accommodation. After slaughter, cold carcass weight (hot carcass weight · 0.98) was recorded. The carcasses were classified for fat score (1 = leanest and 5 = fattest) and conformation score (P = 1 to E = 5) using the EU Beef

12 10

Kg/day

1992). The underlying basis for hypothesising a positive influence of pre-slaughter growth rate on tenderness is the relationship between nutrient consumption/growth rate and protein turnover. Thus, Jones, Starkey, Calkins, and Crouse (1990) observed that myofibrillar protein degradation and synthesis decreased in cattle during nutrient restriction but increased following nutrient repletion. It is assumed that the proteolytic systems involved in muscle accretion also operate post-mortem such that an increase in protein degradation during rapid growth will be reflected in an increase in post-mortem proteolysis and ultimately tenderness (Wood et al., 1996). However, the data are equivocal and in many studies the apparently positive effects of growth rate on tenderness are confounded by differences in age at slaughter, carcass weight/fatness and intramuscular fat concentration, all of which may independently influence tenderness (Shorthose & Harris, 1990; May et al., 1992; Owens & Gardiner, 1999, respectively). Moreover, muscle protein degradation was not measured in the majority of the above studies. Following a statistical evaluation of data from 3370 temperate-breed cattle, Perry and Thompson (2005) concluded that when adjusted for market weight (220, 280 or 340 kg carcass), growth rate had a small quadratic effect on sensory tenderness (an increase of 2 U on a 100 unit scale for an increase in growth rate from 0.5 to 1.0 kg/day) and no effect on shear force, an objective measurement of toughness. In contrast, Warkup and Kempster (1991) statistically removed the effects of fatness per se and concluded that pre-slaughter growth impetus increases meat tenderness in pigs independent of an increase in fat deposition. Since consumer preference is for lean meat, it is important to confirm if tenderness can be improved without an effect on fatness in beef cattle. We hypothesised therefore, that at a common age and carcass weight/fatness within a commercially relevant specification, an increase in growth rate prior to slaughter would not increase tenderness of beef.

87

8 6 4 2 0 0

5

10

15

20

Week Fig. 1. Concentrate consumption patterns by Friesian steers (h = continuous; j = low–high; m = high–low; n = pulse).

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Carcass Classification Scheme (Anon, 1981). The weight of kidney and channel fat (KCF) on each carcass was also recorded. 2.2. Post-slaughter measurements and sampling For the 4 treatment groups that completed the experiment the pH of the M. longissimus thoracis et lumborum (LTM) was measured at hourly intervals for 8 h and at 24 h post-mortem by making a scalpel incision at the 10th/11th rib and inserting a glass electrode (Model EC2010-11, Amagruss Electrodes Ltd., Castlebar, Co. Mayo, Ireland) attached to a portable pH meter (Model no. 250A, Orion Research Inc., Boston, USA) approximately 2.5 cm into the muscle. During the second and subsequent slaughter times, the temperature of the LTM muscle was measured. A probe was inserted approximately 6 cm into the LTM muscle immediately anterior to the 9th rib and temperature was recorded every 15 min for the first 24 h using a Squirrel temperature logger (1200 series, Grand Instruments Ltd., Barrington, Cambridge, UK). Ambient temperature was also recorded by suspending temperature probes in the chill. For measurement of calpain and calpastatin activity, samples of LTM were taken at the 10th rib at 3 h and 24 h post-mortem, frozen in liquid nitrogen ( 196 C) and stored at 80 C. The sides were cold-boned at 24 h post-mortem. Samples of the right side LTM anterior to the 9th rib were vacuum packed (SuperVac GK-166T) and aged at 4 C for 2, 7 or 14 days post-mortem. Steaks, 2.5 cm thick, were cut after 2 days for compositional analysis and after 2, 7 and 14 days post-mortem, for sensory analysis, colour and Warner– Bratzler shear force (WBSF) measurements. These were vacuum packed and frozen at 30 C for subsequent analysis. Samples for measurement of protein degradation were also taken at 2, 7 and 14 days post-mortem, frozen in liquid nitrogen ( 196 C) and stored at 80 C. The left side pistola hind quarter was removed from all 5 groups as described by Keane and Allen (2002), transported in a refrigerated truck to Ashtown Food Research Centre and dissected into fat, individual muscles, and bone. The subcutaneous fat depth and the cross-sectional area of LTM was measured at the 10th rib. 2.3. Meat quality assessments Colour measurement was done according to the procedure of Strange, Benedict, Gugger, Metzger, and Swift (1974). Freshly cut samples were wrapped in an oxygen permeable PVC wrap and left to bloom at 4 C for 3 h. The redness (Hunter ‘a’ values), the yellowness (Hunter ‘b’ values) and the lightness (Hunter ‘L’ values) of each sample were then measured using a Hunter lab Ultra Scan XE colorimeter with Universal Software Version 2.2.2 (Hunter Associates Laboratory, Inc., Reston, VA, USA). Drip loss and sarcomere length was measured in steaks

(2.5 cm in thickness) cut at 2 days post-mortem according to Honikel (1987) and Cross, West, and Dutson (1980), respectively. Frozen vacuum-packed steaks were thawed in a circulating water bath at 10–15 C and allowed to equilibrate at ambient temperature. Sensory analysis was performed by an eight member, trained panel on steaks grilled to an internal temperature of 70 C, according to the American Meat Science Association Guidelines (AMSA, 1978). Panellists were asked to assess the samples for the following attributes: Tenderness (scale 1–8, 1 = extremely tough, 8 = extremely tender). Moisture/juiciness (scale 1–8; 1 = extremely dry, 8 = extremely juicy). Overall flavour (scale 1–6; 1 = very poor, 6 = very good). Overall firmness (scale 1–8; 1 = extremely mushy, 8 = extremely firm). Residual chewiness (scale 1–6; 1 = not chewy, 6 = extremely chewy). Overall texture (scale 1–6; 1 = very poor, 6 = very good). Overall acceptability (scale 1–6; 1 = not acceptable, 6 = extremely acceptable). Warner–Bratzler shear force was measured according to the procedure of Shackelford, Koohmaraie, and Savell (1994). Steaks were cooked in retortable vacuum pack bags to an internal temperature of 70 C, by immersing in a water bath (Model Y 38, Grant Instruments Ltd.) at 80 C. The internal temperature of the steaks was measured using a Hanna Foodcare digital thermometer (HI 9041). Five cores (1.25 cm diameter) were cut from the steaks parallel to the direction of the muscle fibres and sheared using an Instron Universal testing machine equipped with a Warner–Bratzler shearing device. The cross-head speed was 5 cm/min. Instron Series IX Automated Materials Testing System software for windows (Instron Corporation, High Wycombe, Bucks, UK) was employed in the analysis. Calpain I, II and calpastatin were extracted and separated using ion exchange chromatography on a fast protein liquid chromatography system (FPLC, System C, Pharmacia LKB Biotech.) as described by O’Halloran, Troy, Buckley, and Reville (1997). Activities of calpain I, II and calpastatin were assayed as described by Iversen, Ertbjerg, Larsen, Monllao, and Moller (1993). Results were corrected for non-calcium dependent proteolytic activity by the use of EDTA. One unit of calpain I and calpain II activity was defined as that amount producing an increase in absorbance at 278 nm of 1.0 per hour at 25 C. Calpastatin activity was determined using a casein assay containing a specific amount of calpain II extracted and fractionated. One unit of calpastatin was defined as that amount of inhibitor activity which inhibited one unit of calpain II activity. Due to a freezer failure, not all samples

A.P. Moloney et al. / Meat Science 79 (2008) 86–97

were analysed for calpain and calpastatin activity. Myofibrils were extracted and separated using 15% SDS–PAGE gels as described by O’Halloran et al. (1997). 2.4. Chemical analyses Intramuscular fat and moisture concentrations of thawed minced LTM samples were determined using an automated, integrated microwave moisture and methylene chloride fat extraction method (Bostian, Fish, Webb, & Arey, 1985) on a CEM moisture/solids analyser (Model AVC 80, CEM Corp., Matthews, NC, USA). Protein was determined by the method of Sweeney and Rexroad (1987) using a LECO protein analyser (LECO FP428, LECO Corp., St. Joseph, MI, USA). Analysis of feeds and urinary creatinine were carried out as described by Moloney and O’Kiely (1995) and Moloney, Beermann, Gerrard, Robinson, and Finnerty (1998), respectively. For methylhistidine analysis, urine was mixed with 10% sulphosalicylic acid (4 vol/vol) and allowed to stand at 4 C for 30 min. Following centrifugation one part supernatant was mixed with 4 parts lithium citrate buffer pH 2.2 and 50 ll applied to a Biotronic LC5000 Amino Acid Analyser operated according to the protocol of the manufacturer. The assay was linear up to 1000 lmol/l, had a sensitivity of 5 lmol/l and a between assay coefficient of variation of 5% CV. 2.5. Statistical analyses Variables measured at a single time point were subjected to analysis of variance using a model that had terms for block and treatment. Daily tissue growth was calculated by reference to the mean tissue weight of the animals

89

slaughtered at the beginning of the study. The LTM temperature data at various times post-mortem were logarithmically transformed and linear regression was used to derive a cooling constant for each carcass. These values were then analysed using a model that had terms for slaughter day and treatment. Where a significant effect of treatment was detected, means were separated using the least significant difference procedure. Due to non-homogeniety of variance, calspastatin data were logarithmically transformed prior to statistical analysis. Due to non-normality, the methylhistidine: creatinine ratio was similarly transformed prior to analysis. pH data and data for variables measured 2, 7 and 14 days post-slaughter were subjected to analysis of variance using a model appropriate for a split (day)-plot design. 3. Results Unless stated otherwise, all differences mentioned were significant (P 6 0.05). Growth rate and feed conversion efficiency data are summarised in Table 1. In the first 8 weeks, growth rate was lowest for the low–high group and highest for the high–low group, and this pattern was reversed in the final 8 weeks. For the pulse group, growth rate was similar to the continuous group in the first 8 weeks but not different for the low–high group in the final 8 weeks. Overall growth rate did not differ between the continuous, high–low or pulse groups but was higher for the low–high group than the continuous or high–low group. The efficiency of conversion of feed to bodyweight gain was highest in the first 8 weeks and lowest in the final 8 weeks for the high–low group compared with the other treatments. Overall, the efficiency of conversion of feed to bodyweight gain and pistola muscle gain was highest for

Table 1 Feed intake and conversion efficiency in steers with different energy supply patterns prior to slaughter PatternA Cont.

SED LH

HL

Pulse

Feed dry matter intake (DMI) (kg/d) 0–8 week 6.75c 10–17 week 7.28b Overall 6.93

5.06a 9.52d 7.11

8.73d 5.64a 7.08

6.16b 8.06c 6.95

Growth (g/d) 0–8 week 10–17 week 15–17 week Overall

372a 1148c 1123b 942b

1282c 497a 653a 743a

716b 1011c 719a 843a,b

0.073a 0.121b 0.135b 66.3 9.7c

0.149c 0.091a 0.106a 57.9 7.4a,b

0.117b 0.124b 0.122a,b 58.6 6.6a

822b 787b 646a 775a

Feed efficiency (g liveweight gain/g DMI) 0–8 week 0.122b 10–17 week 0.109a,b Overall 0.112a g carcass/kg DMI 65.1 g pistola lean/kg DMI 8.7b,c A

0.106 0.092 0.076 95.5 88.5 165.7 73.5 0.0140 0.0110 0.0103 5.00 1.11

SignificanceB

*** ***

0.06 *** *** * *

*** * *

NS *

Cont., LH, HL and pulse are continuous, low followed by high, high followed by low, and low for 2 weeks, followed by continuous and then high for 3 weeks before slaughter, respectively. B NS, * and *** not significant, P < 0.05 and P < 0.001, respectively. Means in rows with a common superscript do not differ significantly (P < 0.05).

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the low–high group but not different from the pulse group. The efficiency of conversion of feed to carcass gain was unaffected by energy supply pattern. The conversion of feed to pistola muscle gain was highest for the low–high group (but not different from the continuous group). The log of the ratio of methylhistidine to creatinine did not differ between the low–high and high–low groups and averaged 1.39 and 1.62 (SED 0.178), respectively. The characteristics of the animals slaughtered at the beginning and end of the experiment are summarised in Tables 2 and 3, respectively. Energy supply pattern did not affect carcass weight and classification, weight of kidney + channel fat or fat depth. The pistola weight, as a proportion of the weight of the carcass side, was unaffected by energy supply pattern but the muscle proportion of the pistola was higher for the low–high group than the high– low or pulse groups but similar to the continuous group. A smaller proportion of the muscle component of the pistola was represented in the gluteus muscle group in the low– high group than in the high–low or pulse groups or in the continuous group (P < 0.1). The growth of components of bodyweight are summarised in Table 4. Energy supply pattern did not affect the Table 2 Characteristics of steers (n = 12) slaughtered at the beginning of the study Variable

Mean

SD

Liveweight (kg) Carcass weight (kg) Fatness score Conformation score Kidney and channel fat (kg) (g/kg carcass) Mean fat depth (mm) Longissimus area (cm2) Pistola weight (g/kg side)

460 246 3.06 1.44 6.8 27.1 5.22 54.4 465.3

34.0 16.5 0.217 0.339 2.89 10.24 1.984 2.57 12.41

Composition (g/kg) Subcutaneous fat Intermuscular fat Total fat Muscle Bone

51 81 132 658 210

8.6 10.2 14.9 12.5 9.4

Individual muscles (g/kg total muscle in the pistola) Gastrocnemius 46.5 Biceps femoris 133.8 Semimembranosus 99.9 Semitendinosus 46.2 Gluteus group 87.2 Quadriceps 121.4 Adductor 36.7 Psoas major 48.2 Psoas minor 6.0 Longissimus lumborum 90.6 Longissimus thoracis 34.4 Longissimus thoracis et lumborum 125.0

3.50 5.38 4.79 3.16 4.60 7.27 4.11 3.01 1.26 7.20 3.24 8.27

Muscle trim Distal pelvic Proximal pelvic Lumbar Ribs

3.97 4.11 5.42 5.77

52.6 92.2 28.9 75.4

growth of the carcass, kidney + channel fat depot or the intact pistola. The growth of muscle within the pistola was higher for the low–high group than the high–low or pulse groups, but did not differ from the continuous group. Within the pistola muscles, the growth of the biceps femoris and longissimus muscle group were higher for the low– high compared to all other groups. Energy supply pattern did not influence fat or bone growth rate. There was no difference between energy supply patterns in the pattern of decline of LTM pH post-mortem (Fig. 2). Similarly, energy supply pattern did not affect the ultimate pH, rate of cooling, drip loss or sarcomere length of the LTM muscle (Table 5). The lipid concentration of LTM from the high–low group was lower than that of the continuous and pulse groups, which did not differ but protein and moisture concentrations were not affected by energy supply pattern. Quality characteristics of the LTM muscle are summarised in Table 6. Muscle L, a and b values were higher and WBSF values lower, on day 7 compared to day 2, but not different from day 14. There was no effect of energy supply pattern on colour or WBSF values and no interaction between energy supply pattern and time post-mortem. There was an interaction between energy supply pattern and day post-mortem with respect to sensory tenderness, flavour, firmness, chewiness (P < 0.1) and acceptability (P < 0.1). Thus, tenderness was higher for the high–low compared to the low–high group at 2 days post-mortem, there was no effect of energy supply pattern on tenderness at 7 days post-mortem, and after 14 days post-mortem, tenderness was higher for the continuous group than the low–high group and tended to be higher (P < 0.1) than the high–low and pulse groups. Firmness was inversely related to tenderness. Flavour was similar for all groups at day 2 and day 7 post-mortem. At day 14 post-mortem, flavour was greater for the pulse group compared to the high–low and low–high group which did not differ from the continuous group. Samples from the high–low group were more acceptable (P < 0.1) than samples from the pulse group at day 2 postmortem, all groups were similar at day 7 post-mortem, whereas at day 14 post-mortem, samples from the continuous group were more acceptable than those from the low– high and high–low groups which did not differ. The 30 kDa protein band in SDS–PAGE was similar for the low–high and high–low groups at 2 days post-mortem but greater for the high–low group at 7 and 14 days post-mortem. Calpain and calpastatin activities are summarised in Table 7. At 3 h post-mortem, calpain 1 activity was higher in the continuous group than the other groups which did not differ. There was no effect of energy supply pattern on calpain 1 activity at 24 h post-mortem or on calpain 2 or calpastatin activity at 3 h or 24 h post-mortem. 4. Discussion Of the production factors that potentially influence beef quality and in particular tenderness, growth rate is of

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Table 3 Carcass characteristics and individual muscle weights of steers with different energy supply patterns prior to slaughter PatternA Cont. Final liveweight (kg) Carcass weight (kg) Fatness score Conformation score Kidney and channel fat (kg) (g/kg carcass) Mean fat depth (mm) Longissimus area (cm2) Pistola weight (g/kg side) Composition (g/kg) Subcutaneous fat Intermuscular fat Total fat Muscle Bone

559 300 3.36 1.81 9.1 30.2 9.82 65.6 454.2 64 88 152 653a,b 195

Individual muscles (g/kg total muscle in the pistola) Gastrocnemius 45.8 Biceps femoris 136.6 Semimembranosus 99.4 Semitendinosus 48.4 Gluteus group 82.5a,b Quadriceps 124.9 Adductor 34.7 Psoas major 46.9 Psoas minor 6.5 Longissimus lumborum 85.4 Longissimus thoracis 34.3 Longissimus thoracis et lumborum 119.7 Muscle trim Distal pelvic Proximal pelvic Lumbar Ribs

45.4 98.4 34.5 76.3

LH 575 303 3.31 1.62 9.0 29.8 8.76 68.6 459.3 61 85 146 662a 192

HL 554 296 3.39 1.69 8.0 26.9 8.08 65.0 457.1 65 89 154 648b 198

SED

SignificanceB

9.9 4.5 0.218 0.113 1.86 0.62 0.920 2.72 3.88

NS NS NS NS NS NS NS NS NS

4.3 5.6 8.8 7.2 5.0

NS NS NS

Pulse 564 296 3.60 1.53 9.0 30.4 9.08 64.6 454.7 67 91 159 640b 201

*

NS

47.1 141.3 99.5 46.1 78.6b 120.9 34.7 46.6 6.0 91.3 34.5 125.8

49.0 139.6 100.2 46.5 83.8a 121.1 34.1 45.8 7.3 86.2 34.3 120.5

46.5 140.5 100.4 46.7 83.4a 124.7 33.0 47.1 6.3 86.5 33.8 120.1

1.46 2.09 2.02 1.04 1.99 2.59 1.36 1.68 0.67 3.56 1.60 3.82

NS NS NS NS

45.0 99.7 35.2 73.4

46.9 97.0 34.8 73.3

45.8 95.5 34.3 75.6

1.71 3.64 2.39 3.40

NS NS NS NS

*

NS NS NS NS NS NS NS

A Cont., LH, HL and Pulse are continuous, low followed by high, high followed by low, and low for 2 weeks, followed by continuous and then high for 3 weeks before slaughter, respectively. B NS, * and *** not significant, P < 0.05 and P < 0.001, respectively. Means in rows with a common superscript do not differ significantly (P < 0.05).

particular interest both from an applied and mechanistic perspective. The basis for hypothesising a positive influence of pre-slaughter growth rate on tenderness is the relationship between growth rate and protein turnover. It is assumed that the proteolytic systems involved in muscle accretion also operate post-mortem such that an increase in protein synthesis and in particular protein degradation, during rapid growth will be reflected in an increase in post-mortem proteolysis and ultimately tenderness (Koohmaraie, Kent, Shackelford, Veiseth, & Wheeler, 2002; Wood et al., 1996). The data from studies addressing the ‘‘growth rate hypothesis’’ are equivocal. Thus, while several studies report a positive relationship between pre-slaughter growth rate (e.g. Aberle et al., 1981; Fishell, Aberle, Judge, & Perry, 1985), several others did not find this relationship to be statistically significant (e.g. Calkins, Seideman, & Crouse, 1987; Sinclair et al., 2001). Because of the confounding effects of age at slaughter, carcass weight/fatness

and intramuscular fat concentration that exist in many studies, our intention was to manipulate pre-slaughter growth while controlling ration composition, carcass weight and age at slaughter. The cattle chosen were typical of one beef production system used in Ireland, i.e. steers from the dairy herd, reared for slaughter at 24 months of age, to yield a carcass of approximately 300 kg (Keane & Allen, 2002). The pulse treatment was chosen to test the effect of duration of high energy supply since the data of Aberle et al. (1981) indicated that no positive effect of an increase in growth rate was observed beyond 70 days, the shortest period examined in that study. The animal production data indicate that the animals on the low–high energy supply pattern exhibited compensatory growth. This was a novel finding since compensatory growth has usually been observed when previouslyrestricted animals were offered an ad libitum allowance of feed, rather than a higher amount of a restricted allowance, as in the present study. A consequence of the compensatory

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Table 4 Growth (g/day) of tissues in steers with different energy supply patterns prior to slaughter PatternA

SED

SignificanceB

Cont.

LH

HL

Pulse

456 19.6 95.5 12.0 11.3 23.3 60.5a,c 11.7

478 19.3 102.6 11.3 10.7 21.9 69.7a 11.0

416 10.0 88.0 12.1 11.2 23.2 52.8b,c 12.0

414 18.6 84.8 13.2 12.5 25.7 46.6b 12.6

37.4 15.60 9.75 2.39 3.04 4.77 7.92 3.10

NS NS NS NS NS NS

Individual muscles Gastrocnemius Biceps femoris Semimembranosus Semitendinosus Gluteus group Quadriceps Adductor Psoas major Psoas minor Longissimus lumborum Longissimus thoracis Total longissimus

2.6 9.1b 5.9 3.6 3.6 8.6 1.5 2.5 0.5 3.6 2.0 5.6b

3.3 12.2a 6.9 3.2 2.9 8.3 1.8 2.8 0.4 6.6 2.5 9.1a

3.3 9.1b 5.5 2.5 3.4 6.3 1.0 1.7 0.8 3.3 1.8 5.1b

2.1 8.6b 4.9 2.4 2.8 6.8 0.4 1.9 0.4 2.9 1.4 4.3b

0.59 1.27 1.17 0.58 0.93 1.39 0.60 0.65 0.26 1.45 0.58 1.57

NS

Muscle trim Distal pelvic Proximal pelvic Lumbar Ribs

0.6 7.9 3.7 4.9

0.9 9.1 4.4 4.5

0.7 6.6 3.6 3.1

0.1 5.4 3.1 3.5

0.78 1.81 0.89 1.14

Carcass Kidney + channel fat Pistola Subcutaneous fat Intermuscular fat Total fat Muscle Bone

*

NS

*

NS NS NS NS NS NS NS 0.065 NS *

NS NS NS NS

A Cont., LH, HL and pulse are continuous, low followed by high, high followed by low, and low for 2 weeks, followed by continuous and then high for 3 weeks before slaughter, respectively. B NS, * and *** not significant, P < 0.05 and P < 0.001, respectively. Means in rows with a common superscript do not differ significantly (P < 0.05).

7.5

7

pH

6.5

6

5.5

5 0

5

10

15

20

25

30

Time (h) Fig. 2. Muscle pH post-mortem in steers with different energy supply patterns prior to slaughter (h = continuous; j = low–high; m = high– low; n = pulse).

growth in the low–high group was an increase in growth in the total musculature of the pistola joint relative to the high–low and pulse groups, and differential growth of muscles within the pistola relative to the continuous, high–low and pulse groups. This difference was not accompanied by a difference in fat cover and consequently there was no dif-

ference between treatments in the rate of carcass cooling or sarcomere length which is often used as an index of ‘‘coldshortening’’ and consequently tougher meat (Shackelford, Koohmaraie, Miller, Crouse, & Reagan, 1991). Keane (2002) and Moloney, Keane, Dunne, Mooney, and Troy (2001) have previously shown that manipulating the pattern of concentrate supply in a forage and concentrate nutritional regime can decrease indices of fatness in beef cattle. This study indicates that such an effect could be mediated via an effect on muscle growth. The differential effects of the low–high energy supply seemed to reflect growth impetus of the muscles since muscle growth coefficients (Keane & Allen, 2002) were positively correlated with the difference in muscle growth between continuous and low–high concentrate supply patterns. That the growth pattern differentially affects the more valuable LTM suggests that manipulation of energy supply could be a readily applied management tool for increasing muscle accretion and hence carcass value in finishing cattle. It is recognised that the absolute differences were small and likely not to be of commercial importance. However, the impact of rapid pre-slaughter growth for longer than 8 weeks merits study in this regard. Methyl-histidine excretion has been used to estimate protein degradation in vivo (Harris & Milne, 1981).

A.P. Moloney et al. / Meat Science 79 (2008) 86–97

93

Table 5 Composition (g/kg) and selected characteristics of longissimus thoracis et lumborum from steers with different energy supply patterns prior to slaughter PatternA

Protein Lipid Moisture pH (48 h) Cooling rate (h 1) Drip loss (g/kg) Sarcomere (lm)

Cont.

LH

HL

Pulse

219 34b,c 735 5.51 0.090 31.0 1.71

223 29a,b 737 5.50 0.095 31.1 1.73

217 24a 741 5.43 0.091 32.2 1.74

209 39c 732 5.48 0.092 31.0 1.71

SED

SignificanceB

4.2 5.0 4.4 0.053 0.0030 3.24 0.042

NS *

NS NS NS NS NS

A Cont., LH, HL and pulse are continuous, low followed by high, high followed by low, and low for 2 weeks, followed by continuous and then high for 3 weeks before slaughter, respectively. B NS, * and *** not significant, P < 0.05 and P < 0.001, respectively. Means in rows with a common superscript do not differ significantly (P < 0.05).

Estimation of absolute protein degradation using this measurement requires collection of total urine produced over several days, which was not possible in the present study. Accordingly, the methyl-histidine concentration in urine samples collected for 4 h from the extreme growth rate groups (low–high and high–low) was expressed as a ratio to creatinine to adjust for possible differences in muscle mass, so that changes would reflect muscle metabolism (Gibson, 1990). The trend for this ratio to be higher in the low–high compared to the high–low (0.041 vs 0.024) groups may indicate increased muscle protein degradation in the animals growing faster prior to slaughter. Using the total methyl-histidine excretion procedure, Lobley et al. (2000) and Therkildsen (2005) observed an increase in the protein fractional breakdown rate when the dietary allowance of cattle was increased. The differences between those studies and the present study may reflect less precision when using the ratio rather than the total urine collection approaches. With respect to assessment of protein degradation postmortem, components of the calpain/calpastatin proteolytic system were measured, since this system is considered to be a major regulator of muscle protein degradation, both in vivo and post-mortem (Koohmaraie et al., 2002; Therkildsen, 2005). That neither form of calpain nor calpastatin activity differed between the low–high and high–low groups supports the observations of Therkildsen, Larsen, Bang, and Vestergaard (2002) who found no difference in LTM from calves that grew at 770 or 1204 g/d before slaughter. Data on the effects of pre-slaughter growth rate on the calpain/calpastatin system are however equivocal and it appears that the response to different growth rates depends on the genotype of the animal, the age/maturity at slaughter and the degree of nutrient restriction imposed preslaughter. The higher activity of calpain 1 in the continuous group compared to the low–high and high–low groups may reflect the temporal pattern of change in activity in response to dietary perturbation, i.e. the increase in activity in the low–high group subsequent to the increase in energy consumption had not attained the ‘‘baseline’’ value of the continuous group whereas the decrease in activity subsequent to a decrease in energy consumption in the high–

low value had exceeded the ‘‘baseline’’. While Therkildsen (2005) provided some information on the temporal pattern of change in the calpain/calpastatin system in young bull calves such a pattern remains to be elucidated in the older steers used in the present study. Why calpain 1 activity was lower in the pulse compared to the continuous group is not clear at this time. However, that calpain 1 activity at 3 h post-mortem was highest in the LTM that were most tender at 14 days hours post-mortem (continuous energy supply pattern) supports the role of calpain 1 rather than calpain 2 in post-mortem ageing (O’Halloran et al., 1997). In contrast to the above, the greater amount of the 30 kDa band in muscle from the high–low group compared to the low–high group suggests greater proteolysis due to lower nutrient consumption which was not reflected in increased tenderness. The apparent increase in calpastatin activity from 3 h to 24 h post-mortem was unexpected based on the data of O’Halloran et al. (1997). However, an increase in calpastatin activity in the first 24 h post-mortem was also observed by Therkildsen et al. (2002) and Thomson, Dobbie, Cox, and Simmons (1999). The latter stated that ‘‘the reasons for this apparent increase are presently unknown but may be related to the efficiency of extraction pre and post-rigor and need to be investigated further’’. The similar fall in, and ultimate, pH of LTM indicates that pre-slaughter glycogen stores were adequate even in the high–low animals to ensure normal values. Consequently, there was no difference in colour or drip loss. The apparent effects of pre-slaughter growth rate on muscle colour (e.g Vestergaard, Oksbjerg, & Henckel, 2000) are frequently confounded with age, carcass weight, ration composition and/or exercise. In general, there is little evidence of an effect of growth rate per se or ration composition on muscle colour when animals are not subjected to pre-slaughter stress (French et al., 2000, 2001). It is recognised that animals offered a low plane of nutrition prior to slaughter are likely to be at greater risk of having high ultimate pH/dark muscle if they experience even mild preslaughter stress due to lower muscle glycogen storage than animals offered a high plane of nutrition. Since the above early post-mortem influences on tenderness (O’Halloran, Troy, & Buckley, 1997) were not affected

94

Table 6 Quality characteristics of longissimus thoracis et lumborum from steers with different energy supply pattern prior to slaughter Pattern (P)A LH

HL

Pulse

Day

Day

Day

Day

2

7

14

2

7

14

2

7

14

2

7

14

SED

P

Day

P · day

34.3 12.1 7.5 6.02 280

36.0 15.9 9.2 4.10 283

36.8 15.7 9.2 3.85 281

35.2 12.9 8.0 7.35 289

36.7 15.4 9.2 5.56 292

37.5 15.4 9.2 4.69 284

34.5 12.5 7.8 6.19 291

36.2 15.5 9.1 4.50 287

37.2 15.5 9.3 4.29 286

34.4 12.7 7.5 7.00 284

36.1 15.7 9.2 4.65 284

36.3 15.9 9.1 3.83 266

0.73 0.58 0.37 0.672 11.2

NS NS NS NS NS

***

NS

NS NS NS NS NS

0.425 0.334 0.161 0.249 0.183 0.252 0.228 1.163

NS NS NS NS NS NS NS

***

*

*

***

Sensory characteristics Tenderness 3.68a Juiciness 5.21 Flavour 3.78a Firmness 6.15a Texture 3.15 Chewiness 4.17 Acceptability 3.01a 30 kDa protein – A B C

SignificanceB

5.57c 4.81 3.96a,b 5.05c 3.71 2.97 3.72b –

6.09c 5.27 3.81a 4.73c 3.70 2.62 3.98b,c –

3.59a 4.66 3.72a 6.09a 2.91 4.30 2.87a 2.26a

5.04c 5.15 4.09b 5.43c 3.44 3.42 3.55b 9.81b

4.84c,d 5.02 3.72a 5.20c,d 3.52 3.34 3.39b 12.06c

4.48b 5.18 3.77a 5.69b 3.34 3.78 3.23a 4.06a

5.34c 4.80 3.80a 5.24c 3.65 3.09 3.55a,b 13.17d

5.27c 4.99 3.53a 5.13c 3.49 3.08 3.44b 18.35e

3.94a 5.10 3.62a 5.85a 2.98 4.09 2.81a –

5.09c 4.42 4.06b 5.42c 3.52 3.28 3.51b –

5.28c 4.82 4.08b 5.24c,d 3.54 3.18 3.65b –

*** *** ***

**

NS

**

*

***

*

***

NS 0.08 0.07

*** ***

*

Cont., LH, HL and Pulse are continuous, low followed by high, high followed by low, and low for 2 weeks, followed by continuous and then high for 3 weeks before slaughter, respectively. NS, * and *** not significant, P < 0.05 and P < 0.001, respectively. Means in rows with a common superscript do not differ significantly (P < 0.05). Warner–Bratzler shear force.

A.P. Moloney et al. / Meat Science 79 (2008) 86–97

Colour L a b WBS (kg)C Cook loss (g/kg)

Cont.

A.P. Moloney et al. / Meat Science 79 (2008) 86–97

95

Table 7 Calpain and calpastatin activity (U/kg muscle) in longissimus thoracis et lumborum from steers with different energy supply patterns prior to slaughter PatternA

Calpain, 1–3 h Calpain, 1–24 h Calpain, 2–3 h Calpain, 2–24 h Calpastatin, 3 hC Calpastatin, 24 hC

Cont.

LH

HL

Pulse

353b 162 1057 239 8710 13,183

210a 97 961 301 2399 10,000

195a 193 939 346 7244 11,749

171a 157 908 193 6166 7763

SED

SignificanceB

53.7 71.3 137.4 111.0 0.304 0.163

NS NS NS NS NS

*

A

Cont., LH, HL and pulse are continuous, low followed by high, high followed by low, and low for 2 weeks, followed by continuous and then high for 3 weeks before slaughter, respectively. B NS, * and *** not significant, P < 0.05 and P < 0.001, respectively. Means in rows with a common superscript do not differ significantly (P < 0.05). C Data log-transformed prior to analysis. Back-transformed means are presented in the table.

by energy supply pattern, these do not confound the treatment effects on tenderness. Similarly, the absolute difference in intramuscular lipid concentration is unlikely to have an important effect on tenderness (Purchas & Lloyd Davies, 1974). Despite the effects on muscle growth, the effects on tenderness were inconsistent (no effect on shear force and no effect on sensory tenderness after 7 days ageing post-mortem). The lack of an effect of increased growth rate, relative to the continuous energy supply pattern on LTM tenderness is consistent with the measured indices of protein degradation and supports our initial hypothesis. Therefore, for 14-day-aged beef, a continuous growth path is more appropriate for ensuring tender beef, rather than high growth rate for either 2 or 8 weeks pre-slaughter. Our observations contrast with those of other studies (e.g. Aberle et al., 1981; Fishell et al., 1985; Hornick, Van Eenaeme, Clinquart, Diez, & Istasse, 1998; Therkildsen et al., 2002), where positive relationships between growth rate prior to slaughter and beef tenderness were observed. Many other studies agree with the present study and observed no enhancement in beef tenderness due to an increase in pre-slaughter growth (e.g. Bruce, Ball, & Mowat, 1991; Hornick, Van Eenaeme, Clinquart, Gerard, & Istasse, 1998; French et al., 2001; Sami, Augustini, & Schwarz, 2004; Sazili et al., 2004; Sinclair et al., 2001). In the studies of Aberle et al. (1981) and Fishell et al. (1985) a greater range in growth rates and a higher ‘‘high’’ growth 1.4 kg/day were achieved than in the present study. It should be noted also, that carcass weights were up to 100 kg lighter for steers on the low planes of nutrition in the studies of Aberle et al. (1981) and Fishell et al. (1985) with associated differences in carcass fatness. The failure to detect effects of energy supply pattern on beef tenderness in the present study may be due, in part, to magnitude of the difference in growth rate between the experimental treatments in the final weeks before slaughter. Thus, in the study of Sinclair et al. (2001), the difference in preslaughter growth was 0.97 vs 1.20 kg/day and no effect was seen. Similarly, steers achieving a similar range in growth rate (Bruce et al., 1991) to those in the present study, also showed no relationship between tenderness and growth rate.

In the study of Therkildsen et al. (2002), the calves were very immature (194–271 days of age). As well as a higher rate of protein turnover, faster growth rate has also been suggested to result in a lower proportion of mature crosslinked collagen in muscle (Aberle et al., 1981; Jones et al., 1990; Millward, Garlick, Steward, Nnanyelugo, & Waterlow, 1975). The relative contribution of protein degradation and connective tissue concentration and cross-linking to post-mortem tenderisation is a function of animal maturity (Fishell et al., 1985). Thus, young animals with less (insoluble) collagen per se may be more responsive to the changes in the proteolytic component of pre-slaughter growth rate. The trend in the literature is for positive effects to be seen with younger animals (<18 mo of age at the beginning of the study e.g. Aberle et al., 1981; Therkildsen et al., 2002) except in the 60-d-old calves used by Sazili et al. (2004). In support of this trend, Perry and Thompson (2005) found that in an analysis of groups of cattle, adjusting for mean age between groups of animals reduced any relationship between group growth rate and meat eating quality traits. 5. Conclusion The increases in pre-slaughter growth rate achieved through dietary manipulation during a 17 week finishing period in the present study failed to improve tenderness and overall palatability of beef from Friesian steers. These growth rates were typical of those observed for such animals reared in commercial practice and suggest that there is little opportunity to enhance beef quality by increasing growth rate by dietary means within the final finishing period provided continuous, moderate growth rates are maintained. Manipulation of the pattern of consumption of a fixed quantity of concentrates during the finishing period can enhance total pistola muscle growth but also preferential growth of commercially important muscles. The commercial relevance of the latter requires evaluation. Acknowledgements This research was partially funded under the Food SubProgramme of the Operational Programme for Industrial

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Development, which was administered by the Irish Department of Agriculture and Food and supported by national and EU funds. Ms. Rezek was partially funded through the EU-CRAFT programme (Contract No. FAIR-CT 989591). The skilled technical assistance of V. McHugh and T. Darby and the co-operation of the management and staff at Meadow Meats, Rathdowney, Co. Laois, Ireland are gratefully acknowledged as is the assistance of P. Reilly with the care of the animals. References Aberle, E. D., Reeves, E. S., Judge, M. D., Hunsley, R. E., & Perry, T. W. (1981). Palatability and muscle characteristics of cattle with controlled weight gain: Time on a high energy diet. Journal of Animal Science, 52, 757–763. AFRC (1993). Energy and protein requirement of ruminants. Wallingford, UK: CAB International. AMSA (1978). Guidelines for cookery and sensory evaluation of meat. Chicago: American Meat Science Association, National Livestock and Meat Board. Anon. (1981). Community scale for the classification of the carcasses of adult bovine animals. E.C. No. 1208/81 and 2930/81. Luxembourg: Office for the Official Publications of the European Communities. Bruce, H. L., Ball, R. O., & Mowat, D. N. (1991). Effects of compensatory growth on protein metabolism and meat tenderness of beef steers. Canadian Journal of Animal Science, 71, 659–668. Bostian, M. L., Fish, D. L., Webb, N. B., & Arey, J. J. (1985). Automated methods for determination of fat and moisture in meat and poultry products: Collaborative study. Journal of Association of Official Analytical Chemists, 68, 876–882. Calkins, C. R., Seideman, S. C., & Crouse, J. D. (1987). Relationship between rate of growth, catheptic enzymes and meat palatability in young bulls. Journal of Animal Science, 64, 1448–1457. Cross, H. R., West, R. L., & Dutson, T. R. (1980). Comparison of methods for measuring sarcomere length in beef semitendinosus muscle. Meat Science, 5, 261–266. Fishell, V. K., Aberle, E. D., Judge, M. D., & Perry, T. W. (1985). Palatability and muscle properties of beef as influenced by preslaughter growth rate. Journal of Animal Science, 61, 151–157. French, P., O’Riordan, E. G., Caffrey, F. J., Monahan, P. J., Vidal, M., Mooney, M. T., et al. (2000). Meat quality of steers finished on autumn grass, grass silage concentrate-based diets. Meat Science, 56, 173–180. French, P., O’Riordan, E. G., Caffrey, F. J., Monahan, P. J., Mooney, M. T., Troy, D. J., et al. (2001). The eating quality of meat of steers fed grass and/or concentrates. Meat Science, 57, 379–386. Gibson, R. S. (1990). Principles of nutritional assessment. New York, NY: Oxford University Press, pp. 308, 312, 324. Grunert, K. G., Bredahl, L., & Bunsae, K. (2004). Consumer perception of meat quality and implications for product development in the meat sector – A review. Meat Science, 66, 259–272. Harris, C. I., & Milne, G. (1981). The urinary excretion of N-methylhistidine by cattle: Validation as an index of muscle protein breakdown. British Journal of Nutrition, 45, 411–422. Honikel, K. O. (1987). The water binding of meat. Fleischwirtschaft, 67, 1098–1103. Hornick, J. L., Van Eenaeme, C., Clinquart, A., Diez, M., & Istasse, L. (1998). Different periods of feed restriction before compensatory growth in Belgian Blue bulls: 1. Animal performance, nitrogen balance, meat characteristics and fat composition. Journal of Animal Science, 76, 249–259. Hornick, J. L., Van Eenaeme, C., Clinquart, A., Gerard, O., & Istasse, L. (1998). Different modes of food restriction and compensatory growth in double-muscled Belgian Blue bulls: Animal performance, carcass and meat characteristics. Animal Science, 69, 563–572.

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