Effects of dietary lipid type on muscle fatty acid

0 downloads 0 Views 280KB Size Report
as described by Atkins and Thompson (1979). Carcass halves were ..... and meat toughness of lambs fed a low-quality basal dieta. Item. BASb. LUPb. FMb.
Effects of dietary lipid type on muscle fatty acid composition, carcass leanness, and meat toughness in lambs E. N. Ponnampalam, A. J. Sinclair, B. J. Hosking and A. R. Egan J ANIM SCI 2002, 80:628-636.

The online version of this article, along with updated information and services, is located on the World Wide Web at: http://jas.fass.org/content/80/3/628

www.asas.org

Downloaded from jas.fass.org by guest on May 24, 2011

Effects of dietary lipid type on muscle fatty acid composition, carcass leanness, and meat toughness in lambs1,2 E. N. Ponnampalam*3, A. J. Sinclair†, B. J. Hosking*, and A. R. Egan* *Department of Animal Production, University of Melbourne, Victoria 3010, Australia and †Department of Food Science, Royal Melbourne Institute of Technology, Melbourne, 3001, Australia

lumborum (LL) muscles were taken from chilled (4°C) carcasses for the assessment of FA composition and meat tenderness, respectively. Lambs fed lupin or fish meal with or without barley had heavier slaughter weights (P < 0.004) and HCW (P < 0.001) than lambs fed basal or barley when initial BW was included as a covariate. The lupin diet also resulted in heavier carcasses (P < 0.05) than the fish meal or barley/fish meal diets. With GR as an indicator, fish meal and barley/ fish meal diets produced leaner carcasses (P < 0.01) than lupin and barley/lupin lambs. Long-chain n-3 FA content [20:5n-3 (P < 0.001), 22:5n-3 (P < 0.003), and 22:6n-3 (P < 0.001)] in the LT muscle were substantially higher with the fish meal and barley/fish meal diets, whereas muscle total n-6 FA was increased (P < 0.003) by lupin and barley/lupin compared with all other diets. Thus, increased muscle long-chain n-3 FA content occurred without an increase in fatness measured as GR, whereas increased muscle n-6 FA content was associated with an increase in carcass fatness. Under these circumstances, a reduction in carcass fatness had no effect on meat tenderness measured as Warner-Bratzler shear force.

ABSTRACT: Isonitrogenous amounts of two protein sources differing in rumen degradation rate and in lipid composition were fed to sheep with or without a rapidly fermentable cereal grain. The effects on intake, carcass leanness, and muscle fatty acid (FA) composition were examined. Thirty-eight crossbred wether lambs (9 mo, 35 to 48 kg) were allocated by stratified randomization to six treatment groups: 1) basal diet of alfalfa hay:oat hay (20:80) ad libitum = basal; 2) basal + lupin (358 g DM/d) = lupin; 3) basal + fish meal (168 g DM/d) = fish meal; 4) basal + barley (358 g DM/d) = barley; 5) basal + barley + lupin (179 + 179 g DM/d) = barley/lupin; or 6) basal + barley + fish meal (179 + 84 g DM/d) = barley/ fish meal. Lambs were fed individually. Dietary treatments were imposed for 8 wk, and the supplements were offered at 2-d intervals. Daily feed intake and weekly BW of lambs were recorded. At the end of the feeding period lambs were slaughtered after an overnight fast. Hot carcass weight (HCW) and fat depth (GR; total fat and muscle tissue depth at 12th rib, 110 mm from midline) were recorded. At 24 h postmortem samples of longissimus thoracis (LT) and longissimus

Key Words: Carcass Composition, Diet, Fatty Acids, Lambs, Meat Quality, Muscle Tissue 2002 American Society of Animal Science. All rights reserved.

Introduction

J. Anim. Sci. 2002. 80:628–636

markedly in the chemical nature of absorbed substrates in the ME fraction, particularly in fatty acid (FA) content and composition. Such differences may affect not only the nature but also the anatomical distribution of the lipids deposited (Rule et al., 1995; Smith, 1995). Any effects, where they occur, may be significant in relation to eating quality (Wood, 1990). In the mid-1990s, the role of dietary fat type in the maintenance of healthy life in humans focused on the importance of long-chain n-3 FA in the diet (Newton, 1998; Simopoulos, 1998). We have shown that the longchain n-3 FA, such as eicosapentaenoic acid and docosahexaenoic acid, in tissues of lambs can be significantly increased by feeding natural supplements ostensibly as protein supplements but differing in FA content (Ponnampalam et al., 2001a). It was found that diets supporting modified n-3 FA content of muscle membrane

Energy and protein supplements fed to improve growth rate of pasture-based lambs affect energy intake and partitioning of energy retained (Margan, 1994; Beauchemin et al., 1995). Supplements used can vary

1

This project was supported in partnership by Meat and Livestock Ltd. (Australia) and the University of Melbourne. 2 The Authors wish to thank D. Whitfield, A. Thalen, and Leeann Johnson for technical assistance. 3 Correspondence and current address: Department of Food Science, RMIT University, GPO Box 2476V, Melbourne, Victoria 3001, Australia (phone: 03 9925 3967; fax: 03 9925 5241; E-mail: [email protected]). Received March 19, 2001. Accepted October 30, 2001.

628 Downloaded from jas.fass.org by guest on May 24, 2011

Diet and meat fatty acid composition

structural phospholipid also significantly altered plasma insulin concentrations, lipid metabolite concentrations in plasma, and i.m. fat content in the carcass (Ponnampalam et al., 2001b). The nutritional variables encountered in feeding supplements can be very complex and supplements provided for one reason (e.g., protein provision) may also provide other nutrients and have physiological effects that, for example, influence energy partitioning, carcass composition, and muscle lipid composition. The objective of this study was to examine the effects of two dietary supplements, lupin and fish meal, used because of their high content and differential degradability of protein but that also differ in FA composition. Each was fed with or without a rapidly fermentable dietary energy source. Effects on intake, carcass weight, fat depth, muscle FA composition, and meat tenderness were evaluated.

Materials and Methods Animals and Diets. Thirty-eight crossbred (Dorset Horn × Merino, 9 mo of age) wether lambs (initial weight 35 to 48 kg) were allocated to six treatment groups by stratified randomization. The basis of allocation was six per treatment, but for reasons of anticipated animal variability in acceptance or adverse response to the supplement two extra lambs were included in one treatment (fish meal), defined below. After 7 d of adaptation to a basal diet of alfalfa hay:oat hay (20:80), five treatment groups were fed energy and protein supplements throughout an 8-wk period. The treatments allocated were 1) basal diet (basal), alfalfa:oat (20:80) provided for ad libitum consumption; 2) basal + lupin (358 g DM/d) = lupin; 3) basal + fish meal (168 g DM/d) = fish meal; 4) basal + barley (358 g DM/d) = barley; 5) basal + barley (179 g DM/d) + lupin (179 g DM/d) = barley/lupin; or 6) basal + barley (179 g DM/d) + fish meal (84 g DM/d) = barley/fish meal. The lambs were allowed ad libitum access to hay, which allowed for ME intakes similar to those of lambs fed a poor-quality, mature pasture diet (6.88 MJME/kg DM) during the summer/autumn seasons in southern Australia. Lambs were individually penned and fed and measurements were made on each lamb; the experimental unit was the individual lamb. Eight lambs were allocated to the fish meal diet to allow exclusion of lambs that rejected fish meal. Variation among lambs in their acceptance of fish meal had been observed in a previous experiment, but in this experiment all lambs consumed the supplement completely in the 1st wk and were retained in the experiment. Data from all eight lambs in the fish meal treatment group were included for the statistical analysis of intakes and carcass traits. However, muscle samples from only six randomly chosen lambs from the fish meal group were submitted for FA analysis, as for all other dietary treatments, due to the

629

high cost of FA analysis. This number was sufficient for statistical comparisons. All supplements were offered at 2-d intervals (i.e., 2d allowance) at 0900 along with the basal roughage new each day in a separate container; all supplements were consumed. Fish meal in the fish meal treatment was fed with 100 g of alfalfa hay and was accepted by all lambs. No additional mineral and vitamin mixture was included in the diets, to provide a condition, similar to feeding in the field, where under grazing conditions these additions are often not made by farmers. Drinking water was available at all times. All animal procedures were reviewed and approved by the Animal Experimentation Ethics Committee, University of Melbourne, Parkville, Australia. The CP content was reduced by 50% in treatments 5 and 6 by introducing a carbohydrate source (barley grain) in an equal amount in those treatments, thus reducing the amount of lupin or fish meal by 50%. This was planned to provide initial evidence on whether the fat partition in the carcass was influenced either by energy limitation or protein limitation in the diet or was more closely related to the dietary effects through alteration of muscle membrane FA. The supplements provided in treatments lupin vs fish meal and barley/ lupin vs barley/fish meal were isonitrogenous in order to examine the effects of amount and type of dietary protein, lupin being relatively rapidly degraded and fish meal relatively slowly degraded (Hussein and Jordan, 1991; Margan, 1994; Beauchemin et al., 1995) on carcass fat partitioning. A further variable in the dietary measurements relates to the nature and type of FA in the lipid fraction of the protein supplements. Measurements and Slaughter Procedure. Over the 8wk experimental period, roughage and supplement intakes were recorded daily and BW once a week at 0900 before lambs were offered fresh feed. Samples of basal diet and supplements were collected twice each week, bulked, and mixed well, and representative samples were taken for chemical analysis (Table 1). The ME values of roughage and supplements were provided by FEEDTEST (Agriculture Victoria, Hamilton, Australia) based on the Near Infrared Reflectance (NIR) technique calibrated for a similar range of feed ingredients. At the end of an 8-wk experimental period, lambs were slaughtered at a commercial abattoir as reported previously (Ponnampalam et al., 2001a). Carcass Traits and Muscle Sample Collection. Hot carcass weight (HCW) was recorded at 45 min postmortem. At 24 h postmortem, chilled carcasses were cut into halves along the midline and the right sides were taken to Meat Research Laboratory, Mt Derrimut Field Station, The University of Melbourne, Australia. Carcass length was measured between the anterior edge of the first rib and the anterior end of the pubic symphysis as described by Atkins and Thompson (1979). Carcass halves were stored at 1°C in a cold room, consistent with commercial practice, until dissection and muscle sampling was completed within the next 5 h. Half sides

Downloaded from jas.fass.org by guest on May 24, 2011

630

Ponnampalam et al.

Table 1. Chemical composition of basal diets and supplements fed to lambsa Item Alfalfa hay Oat hay Barley grain Lupin grain Fish mealc

DM, %

CP, %

Lipid, %

Ash, %

ME, MJ/kgb

88 88 89 89 91

17 8 11 31 67

3 2 2.5 6.2 11.9

9.5 5.4 3.1 3.0 18.7

8.2 6.8 12 13 12

a

All values expressed on dry matter basis and means were calculated from two observations. Reported values, others were determined values. Fish meal was imported from Peru.

b c

were cut across the 12th rib and the carcass fat depth (the total tissue depth of adipose and muscle at 12th rib, 110 mm from the midline; GR) was recorded according to the AUSMEAT procedure for lambs. The longissimus thoracis (LT) and longissimus lumborum (LL) muscles were then dissected out and samples were taken for measurement of FA composition (∼2-cm-thick chops) and meat tenderness (toughness) as described below. The LL muscle was cut into two portions (about 100 g) and packed in oxygen-impermeable polythene bags. All samples were immediately frozen at −20°C until further analysis. Fatty Acid Analysis. Total lipid content and total FA composition of LT muscle and of feed samples were determined as described by Ponnampalam et al. (2001a). In the present study, FA composition of muscle phospholipid and triglyceride were not determined as separate fractions, due to cost and time involved with the analysis. One milliliter of extracted lipid sample was added with 1 mL of internal standard (heptadeconoic acid, 4 mg/mL; NU-CHEK PREP, Elysian, MN) and the solvent was evaporated under nitrogen gas. After evaporation to dryness, the FA were saponified using KOH (0.68 M in methanol) followed by transesterification with 20% boron trifluoride in methanol. The FA composition of LT muscle and diets was determined by gas chromatography using a 50-m × 0.32-mm BPX70 fused silica capillary column (SGE, Melbourne, Australia) as described by Sinclair and O’Dea (1987). Measurement of Meat (Muscle LL) Toughness. Within 2 mo of slaughter, LL muscle samples taken for evaluation of tenderness were thawed at 4°C for 12 h and external fat (s.c. adipose tissue) was removed from the surface of the muscle. Each muscle sample was placed in a polyethylene bag with holes, in order to immerse the sample under water for completeness of cooking, and cooked in a thermostatically controlled water bath for 1 h at 80°C. Cooked samples (still in bag) were cooled in running water for 30 min (Bouton et al., 1978). The cooked samples were taken from the bag, dried with paper towel to remove excess surface moisture, and held overnight at 4°C. Samples were cut from the cooked loin as rectangular cross sections (1 × 1 × 5 cm) with the fibers lying parallel to the long axis (Moller, 1980) using a fitted double scalpel with a 1-cm gap difference. Each sample was then sheared at right angles to the fiber axis (perpendicular to muscle fibers), using a Warner-

Bratzler (WB) shear blade with the triangular slot cutting edge. An Instron Material Testing Machine was used to determine the peak force (kg) to shear the samples and an average of five measurements were taken for each LL muscle sample. The cooking procedure and the measurement of shear force values were conducted at the Food Science Laboratory, Food Research Institute, Werribee, Australia. Statistical Analysis. Data were analyzed using the Minitab Statistical Package (Minitab Inc., 1995, State College, PA). Results for DM intakes, muscle FA composition, and carcass traits were analyzed by ANOVA using the GLM procedure. The treatments were individual, and not in a factorial design, because lupin and fish meal supplements were reduced when barley grain was added to the barley/fish meal and barley/lupin treatments. Therefore, a one-way ANOVA was used to analyze the data. The main effect tested was dietary treatment. Initial BW was included as a covariate for the calculation of final BW, carcass length, and HCW, whereas HCW was included as a covariate for GR fat and meat toughness determination. Results are reported as least squares means and pooled SEM values. When significant treatment effects were detected by ANOVA, means were separated using LSD, with P < 0.05 considered statistically significant (Steel and Torrie, 1982).

Results Intakes of total daily CP, ME, and lipid were calculated from the mean values obtained in Table 3 and chemical composition of the feed ingredients as reported in Table 1. Statistical analysis was not carried out on those derived data. However, the calculated daily intakes of CP, lipid, and ME were similar for the lupin and fish meal, barley/lupin and barley/fish meal, and basal and barley diets. The daily ME intakes between the basal and barley diets differed. Lambs supplemented with lupin (lupin, barley/lupin) received relatively high levels of total n-6 FA in their diets, between 94% (lupin) and 65% (barley/lupin) greater than those received by lambs on the basal diet. Lambs fed fish meal (fish meal and barley/fish meal) had a substantially higher total n-3 FA intake than the lambs on the basal diet. Lambs fed barley had intakes of total n-3 FA similar to those consumed by lambs on

Downloaded from jas.fass.org by guest on May 24, 2011

631

Diet and meat fatty acid composition

Table 2. Mean daily intake of n-3, n-6, and long-chain (LC) n-3 fatty acids of roughage and supplements for basal and supplemented lambsa Item

BASb

LUPb

FMb

BARb

B+LUb

B+FMb

Hay n-3 FA intakec Supplement n-3 FA intake Hay n-6 FA intakec Supplement n-6 FA intake Total n-3 FA intake Total n-6 FA intake Total LC n-3 FA intake

918 0 6,258 0 918 6,258 0

705 832 4,809 7,375 1,537 12,184 0

943 4,112 6,431 448 5,055 6,879 4,045

621 304 4,232 3,361 925 7,593 0

729 568 4,971 5,368 1,297 10,339 0

796 2,207 5,428 1,905 3,003 7,333 2,022

Intakes were expressed in mgⴢlamb−1ⴢd−1. Diet abbreviations: BAS = basal diet, LUP = lupin diet, FM = fish meal diet, BAR = barley diet, B+LU = barley with lupin, B+FM = barley with fish meal. c n-3 FA = omega-3 fatty acid, n-6 FA = omega-6 fatty acid. a b

basal diet. Among the supplemented lambs, lambs on fish meal and barley/fish meal treatments had threefold and twofold higher total n-3 FA intakes, respectively, than lambs receiving lupin, barley, or barley/lupin treatments (Table 2). Intakes of dietary long-chain n3 FA for the basal, lupin, barley, and barley/lupin treatments (Table 2) were negligible. Roughage intake was reduced (P < 0.001) with lupin, barley, and the combination of both compared with the basal diet. Feeding fish meal did not reduce the roughage intake, but with barley added to fish meal roughage intake was reduced compared to that of lambs fed the basal diet (P < 0.01; Table 3). Compared with the basal diet, total intake of DM was increased by all dietary supplements (P < 0.001) except barley (Table 3). Compared with the basal diet, final BW (P < 0.004) and HCW (P < 0.001) were significantly greater in both lupin- and fish meal-fed lambs and in lambs fed barley/ lupin or barley/fish meal (Table 4). Lambs fed lupin alone or barley/lupin had greater (P < 0.01) fat depth (measured as GR) than lambs on all other treatments. Barley-fed lambs had a lesser carcass length (P < 0.03) than other supplementary feed groups but were similar to lambs fed the basal diet. Tenderness of meat was not significantly different among treatment groups ex-

cept for those fed lupin, for which the rating was greater (tougher, P < 0.05) as determined by WB shear force (Table 4). Muscle lipid FA compositions for FA of chain length less than C18 are not reported here, because long-chain FA were considered most important in this study. Linoleic acid (18:2n-6) content was greater with lupin feeding (P < 0.003) and intermediate with barley/lupin feeding (P < 0.05) than with other treatments (Table 5). Fish meal and barley/fish meal diets produced lower (P < 0.001) arachidonic acid (20:4) concentrations in meat than did basal, lupin, barley, or barley/lupin diets. The concentrations of the long-chain FA 20:5n-3 (P < 0.001), 22:5n-3 (P < 0.003), and 22:6n-3 (P < 0.001) in the muscle lipids were dramatically increased in lambs fed fish meal alone or fish meal combined with barley compared with the concentrations in lambs fed basal, barley, lupin, or barley/lupin diets (Table 5). Lambs fed the fish meal and barley/fish meal had muscle lipids with similar total n-3 FA and total long-chain n-3 FA contents, these being substantially higher (P < 0.001) than those from other dietary treatments (Table 6). Total n6 FA content was increased (P < 0.003) by both lupin and barley/lupin compared with basal, fish meal and barley/fish meal. The ratio of n-6:n-3 FA in LT muscle

Table 3. Daily intakes of roughage, supplements, dietary crude protein, lipid, and metabolizable energy of control and supplemented lambsa Item Roughage intake Supplement intake Total intake Supplement CP intake Total CP intake Total lipid intake Total ME intake

BASb

LUPb

FMb

BARb

B+LUb

B+FMb

SEMc

1,192h 0 1,192e 0 124 26.2 8.2

916f 358 1,274f 114 209 42.4 10.6

1,225h 168 1,393g 113 240 46.9 10.5

806e 358 1,164e 40.3 125 29.9 9.8

947f 358 1,305f 79 177 36.4 10.8

1,034g 263 1,297f 79 185 37.2 10.3

34.2 — 33.7 NDd NDd NDd NDd

All values are calculated on DM basis and expressed in gⴢlamb−1ⴢd−1. Diet abbreviations: BAS = basal diet, LUP = lupin diet, FM = fish meal diet, BAR = barley diet, B+LU = barley with lupin, B+FM = barley with fish meal. c Values for pooled SEM are shown. d ND = not determined: values were calculated from the means of treatment intakes and chemical composition reported in Table 1. e,f,g,h Within a row, means without a common superscript letter differ (P < 0.05). a b

Downloaded from jas.fass.org by guest on May 24, 2011

632

Ponnampalam et al.

Table 4. Effect of dietary supplementation on final body weight (FBW), carcass quality, and meat toughness of lambs fed a low-quality basal dieta Item

BASb

LUPb

FMb

BARb

B+LUb

B+FMb

SEMc

Final body weight, kg Hot carcass weight, kg GR fat depth, mmd Carcass length, cm Intramuscular fat, % Warner-Bratzler shear, kg S cost/kg HC gain, $e

48.9f 20.9f 10.3f 64.4fg 3.3 3.9f 0

53.9g 25.8h 15.7g 65.7g 4.2 5.7g 1.15

54.3g 23.5g 10.0f 65.8g 3.6 3.9f 2.30

49.4f 21.1f 10.4f 63.2f 3.6 4.8fg 9.30

53.1g 24.9gh 13.6g 65.8g 4.1 4.7fg 1.05

53.9g 23.6g 10.2f 64.9g 3.9 4.1f 1.65

1.55 0.89 1.61 0.80 0.80 0.75 —

a Final live weight, carcass length, and hot carcass weight (HCW) were adjusted to a common initial BW; GR fat depth and meat toughness were adjusted to a common HCW using covariates. b Diet abbreviations: BAS = basal diet, LUP = lupin diet, FM = fish meal diet, BAR = barley diet, B+LU = barley with lupin, B+FM = barley with fish meal. c Values for pooled SEM are shown. d GR fat depth = total tissue depth (fat + muscle) at the 12th rib, 110 mm from the midline. e S cost/kg HC gain = supplement cost/kg of hot carcass gain. f,g,h Within a row, means without a common superscript letter differ (P < 0.05).

was greater (P < 0.001) with lupin and barley/lupin diets and lower with fish meal and barley/fish meal diets (P < 0.001) than that in LT muscle from lambs fed basal or barley diets (Table 6).

Discussion The results are consistent with the hypothesis that the type of FA in the diet influences the FA composition of the structural lipids in muscle (Ponnampalam et al., 2001a,b), and further that this in turn is an important factor in determining the deposition of adipose and lean tissue in the carcass. The provision of other nutrients such as carbohydrate (energy) or protein in the diet may influence but not be major factors that determine the level of adipose tissue deposition and the composition of the total FA deposited in adipose and lean tissues in the carcass of lambs. Also, within the levels achieved in this experiment, the reduction in the carcass fatness, demonstrated by GR values, and the changes in FA composition did not significantly affect meat tenderness

evaluated as WB shear force, as might occur if the properties of meat were substantially altered. In Australia, during drought or seasonal pasture shortage, barley (Rowe et al., 1989) and lupin (Margan, 1994) grains are commonly used as “energy” and “protein” supplements, respectively, to improve the growth rate of lambs on low-quality roughage diets. The economic benefit depends on costs of supplements and prices received for the product. In the present study, supplements were offered every 2nd d because under commercial grazing systems sheep are mostly supplemented either on alternate days or twice weekly. When cereal grains are fed as supplements to ruminants (sheep or cattle), the glucose production rate may be increased through the increased yields of gluconeogenic (propionate) precursor and(or) through increased intestinal digestion of ruminally undegraded starch (Rowe and Pethick, 1994; Beever and Thorp, 1997). Rapidly degradable and ruminally undegraded protein supplements can also increase glucose production, depending on both intraruminal effects on VFA proportions and

Table 5. Effect of dietary supplementation on total fatty acid composition of longissimus thoracis muscle in lambs fed a low-quality basal dieta Item

BASb

LUPb

FMb

BARb

B+LUb

B+FMb

SEMc

18:0 18:1 18:2n-6d 18:3n-3d 20:4n-6 20:5n-3 22:4n-6 22:5n-3 22:6n-3

421 866 123ghi 30 36h 14.2g 1.2h 15.2h 6.1g

563 1,297 159 i 34 41h 12.1g 2.4g 15.6h 7.1g

495 969 107g 30 26g 33.4h 0.7h 23.4g 17.0h

448 984 129ghi 30 38h 16.4g 2.0g 17.7h 6.8g

549 1,264 149hi 35 38h 12.1g 2.2g 15.8h 5.0g

510 1,037 128ghi 32 28g 32.5h 0.3h 22.8g 17.1h

108 259 15.0 7.4 2.7 2.5 0.4 1.5 1.9

a Values are expressed in mg/100 g of meat sample and fatty acid contents of C16 and below are not reported here. b Diet abbreviations: BAS = basal diet, LUP = lupin diet, FM = fish meal diet, BAR = barley diet, B+LU = barley with lupin, B+FM = barley with fish meal. c Values for pooled SEM are shown. d n-3 = omega-3 fatty acid, n-6 = omega-6 fatty acid. g,h,i Within a row, means without a common superscript letter differ (P < 0.05).

Downloaded from jas.fass.org by guest on May 24, 2011

633

Diet and meat fatty acid composition

Table 6. Effect of dietary supplementation on major fatty acid classes and essential fatty acids of longissimus thoracis muscle in lambs fed a low-quality basal dieta Item Total MUFAd Total SFAd Total PUFAd Total n-6 FAe Total n-3 FAe Total LC n-3 FAf Ratio of n-6:n-3

BASb

LUPb

FMb

BARb

B+LUb

B+FMb

SEMc

919 1,019 234 165gh 69g 35g 2.5h

1,370 1,425 277 209 j 68g 35g 3.1i

1,031 1,270 245 141g 104h 74h 1.4g

1,045 1,153 246 174hi 71g 41g 2.5h

1,330 1,371 262 194 ij 69g 33g 2.8i

1,103 1,336 267 162gh 105h 72h 1.5g

298 310 24 16.4 10.1 4.9 0.14

a

Values are expressed in mg/100 g of meat sample. Diet abbreviations: BAS = basal diet, LUP = lupin diet, FM = fish meal diet, BAR = barley diet, B+LU = barley with lupin, B+FM = barley with fish meal. c Values for pooled SEM are shown. d MUFA = monounsaturated fatty acid (C16:1 + C18:1), SFA = saturated fatty acid (C14:0 + C16:0 + C18:0), PUFA = polyunsaturated fatty acid (C18:2n-6 + C18:3n-3 + C20:4n-6 + C20:5n-3 + C22:4n-6 + C22:5n-3 + C22:6n-3). e n-3 = omega-3 fatty acid, n-6 = omega-6 fatty acid. f Total LC n-3 FA = total long-chain n-3 fatty acids (C20:5n-3, C22:5n-3, and C22:6n-3). g,h,i,j Within a row, means without a common superscript letter differ (P < 0.05). b

the increase in absorption of amino acid in the intestine (MacRae and Egan, 1980; Leng, 1985; Lee et al., 1987; Margan, 1994). Consequently, from these and our previous experiments (Ponnampalam et al., 2001a,b), it was accepted that the types of FA deposited in the muscle and the energy partition in the carcass could not be attributed only to protein effects. Dry Matter Intake. The reduction in roughage intake (substitution rate) was greater with barley as an energy supplement than with lupin chosen as also providing a source of ruminally degradable protein. The lower relative substitution rate for lupin compared with cereal grain has also been reported by others (Margan, 1994). The extent of substitution is primarily influenced by the availability of forage, type of supplement, and the amount of supplement offered (Beever and Thorp, 1997). Barley contains a high level of starch that is rapidly fermentable and may produce fermentation conditions (e.g., low pH in the rumen) that contribute to lower roughage intake. The decreased roughage intake with the barley/fish meal diet indicates that the substitution rate is more influenced by barley as a rapidly fermentable energy source than by the mass of the supplement. Lupins have high protein and energy content and relatively high degradability in the rumen (Yu et al., 2000), but have little or no true starch (Margan, 1994; Rowe and Pethic, 1994) and are less likely than barley to produce very low pH in the rumen digesta (Valentine and Bartsch, 1987). The calculated intake of CP, lipid, and ME achieved by each dietary treatment group was similar for lupin and fish meal and for barley/lupin and barley/fish meal; only basal and barley diets differed in estimated ME intake. Only fish meal alone did not depress roughage intake. Furthermore, fish meal supported a higher intake of roughage in lambs also receiving barley than lupin, suggesting a beneficial interaction of the more slowly degraded high biological value protein (Hussein and Jordan, 1991). We have observed such effects with

fish meal on roughage intake previously (Ponnampalam et al., 2001a) and also have been reported by others in dairy (Doreau and Chilliard, 1996) and beef (Comerford et al., 1992; Mandell et al., 1997) cattle. Body Weight and Carcass Weight Gain. The substantial increase in final BW and HCW in lambs fed lupin, fish meal, and their combination with barley compared to performance with barley grain alone indicated a beneficial effect of additional protein along with additional ME. The superior performance in terms of BW gain and HCW with lupin compared with fish meal at similar intakes of supplementary protein suggests that rapidly degradable protein and energy from lupin was more efficiently utilized for carcass gain than was that from fish meal. Similar performance of lambs was observed by Beauchemin et al. (1995), who concluded that there was no response to increasing protein content in the diet beyond 15% CP, and that supplementing with ruminally undegradable protein is not required when diets are formulated using primarily barley or canola meal. In the present study adding barley ($90/t) to lupin ($265/t) or fish meal ($600/t) produced large, lean lambs with 30 and 32% lower supplementary feed cost, respectively, than feeding lupin or fish meal alone. Barley alone was not effective in increasing BW or HCW above values for basal-fed lambs, which is consistent with the results observed in a previous study (Ponnampalam, 1994). The poor performance with barley even though the ME intake was increased above that with the basal diet (Table 3) was reflected in lower carcass length compared with other treatments (Table 4).

Source of Diet, Type of Fatty Acid in Diet, and Carcass Quality. Subcutaneous fat depth (GR) is considered a good predictor of leanness for intact carcasses (Kempster et al., 1976; Beauchemin et al., 1995). Using GR and i.m. fat content as criteria, our results indicated that the increased HCW with lupin and barley/lupin diets was mainly associated with increased fat deposi-

Downloaded from jas.fass.org by guest on May 24, 2011

634

Ponnampalam et al.

tion in the carcass rather than with an improvement in carcass leanness, as was found with the fish meal and barley/fish meal diets. Margan et al. (1988) reported a lower protein deposition, measured as N retention in a N balance study, with lupin alone or as a supplement to roughage compared to performance with a legume forage diet. Compared with values for the basal treatment, the high (27%) and modest (16%) increases in the muscle total n-6 FA (mainly linoleic acid) with lupin and barley/ lupin, respectively (Table 6), were associated with a greatly increased and a moderately increased intake of dietary n-6 FA (Table 2). Similarly, the dramatic increase in total muscle long-chain n-3 FA content with fish meal (52%) and barley/fish meal (52%) treatments (Table 6) reflected relatively greater intakes of dietary long-chain n-3 FA (Table 2) compared with lambs on basal and other supplements. The large reduction in relatively rapidly degradable dietary protein (114 vs 79 g/d) between lupin and barley/lupin or in more slowly degradable but digestible dietary protein (113 vs 79 g/ d) between fish meal and barley/fish meal, by substituting the respective protein sources with barley, did not significantly change the carcass adipose tissue or lean deposition shown by HCW, GR fat, and i.m. lipid content (Table 4). Barley/fish meal provided a 50% lower intake of dietary long-chain n-3 FA than fish meal alone, but similar levels of long-chain n-3 FA were deposited in the muscle (Table 6). This suggests that in the lambs there may have been an upper limit for deposition of these FA in muscle and once this was reached the n-3 FA were utilized elsewhere. In a previous study (Ponnampalam et al., 2001b), lambs fed fish oil or fish oil/sunflower meal protein received (5,120 to 5,760 mg/d) more long-chain n-3 FA than did the lambs fed fish meal or barley/fish meal (2,022 to 4,045 mg/d) in the present study. Even though they consumed more n-3 FA, the maximum levels of long-chain n-3 FA found in the muscle (78 and 74 mg/100 g of muscle for fish oil and fish oil/sunflower meal, respectively) were similar to those observed in the present study. Studies conducted in both rats and humans have shown that n-3 FA are more likely to be oxidized for energy than the equivalent n6 FA, which are more likely to be stored in the body (Storlien et al., 1995). This is consistent with our findings that fatter carcasses were produced when increased levels of n-6 FA were deposited in lambs fed the lupin and barley/lupin diets.

Muscle Fatty Acid Deposition and Fat Partition in the Carcass. Altering the n-3 FA composition in muscle membrane structural components can lead to changes in biochemical composition of cellular lipids, which in turn affects the physiological and pathological behavior of the cell membrane (Cave, 1991; Clandinin et al., 1991; Baur et al., 1998). For example, the responsiveness of the cell membrane to growth factors, hormones, and antibodies may be affected (Goldspink, 1991), and processes such as eicosanoid synthesis in

disease control (McDonald, 1995) or insulin-stimulated glucose utilization/oxidation in skeletal muscle (Storlien et al., 1995) may be altered. Changes in membrane function, in the activity of membrane-associated protein (Baur et al., 1998), and in blood plasma lipoprotein metabolism (Paik and Blair, 1996; Ponnampalam et al., 2001) have been reported. The significant increase in the muscle n-6 FA content (Table 6) with the lupin and barley/lupin diets was associated with larger carcasses with increased amount of s.c. fat depth (GR) and i.m. lipid. There is some indirect evidence that n-6 FA may have an influence on partitioning of use of energy substrates. In rats, for example, diets high in n-6 FA have been shown to lead to hepatic and peripheral insulin resistance (Storlien et al., 1991). From human studies it has also been reported that a higher n-6:n-3 ratio in skeletal muscle can lead to a lower insulin action (insulin binding capacity), which in turn can increase the accumulation of storage adipose tissue in the body (Storlien et al., 1995). A significant difference in plasma insulin concentration was also observed in lambs that had increased muscle n-3 FA compared with those that had more n-6 FA or a higher n-6:n-3 FA ratio, which has been discussed in a previous study (Ponnampalam et al., 2001b). Insulin concentration was not measured in the present study, but the substantial increase in muscle n-6 FA and in the ratio of n-6:n-3 FA content (shown in LT muscle) was similar to that in a previous experiment (Ponnampalam et al., 2001b). Lower insulin action in skeletal muscle tissues of lambs fed lupin and barley/ lupin diets due to the higher muscle n-6:n-3 FA ratio may thus underlie the increased gain in adipose tissue in the carcass. This may be one point of nutritional and metabolic interaction with increased glucose entry or increased amino acid entry rates and requires more attention.

Energy Partition in the Carcass and Tenderness of Meat. Meat quality was assessed as tenderness of cooked LL muscle. We sought to investigate whether diets leading to increased carcass weight but different degrees of leanness and composition of FA in muscle would cause a detrimental effect on meat tenderness. The increased carcass weight without increased fat depth achieved with fish meal and barley/fish meal was not associated with altered tenderness compared to lambs fed the basal diet. In contrast, meat from the lupin-fed group, with greater fat depth, was significantly tougher than meat from other dietary groups. Berge et al. (1993) provided evidence consistent with the concept that long-chain n-3 FA modification in longissimus muscle may influence the tenderness of meat. At a similar level of muscle deposition, tenderness of meat from steers fed high soybean-rapeseed meal was lower than tenderness of meat from steers fed linseed meal. One possible explanation is that the linseed diet may have resulted in deposition of more n-3 FA in the muscle, which in turn has influenced the tenderness of meat; linseed oil has 60% n-3 FA, compared to 8 to 10%

Downloaded from jas.fass.org by guest on May 24, 2011

635

Diet and meat fatty acid composition

n-3 FA in soybean-rapeseed oil. It was suggested by Berge et al. (1993) that linseed meal has a specific effect on nitrogen metabolizm and lean tissue accretion that affects beef carcass composition and meat quality as often reported by producers. However, FA content of longissimus muscle was not reported in that study (Berge et al., 1993). Vatansever et al. (1998) and Scollan et al. (2001) reported that feeding linseed as a dietary supplement increased longissimus muscle long-chain n-3 FA content in steers. We have shown previously that dietary long-chain n3 FA were preferentially deposited in muscle membrane structural phospholipid rather than in storage triglyceride (Ponnampalam et al., 2001a,b). The differences in long-chain n-3 FA content were not, however, shown to be associated with significant differences in meat tenderness under our testing conditions. It is possible that there exist other relationships of the long-chain n3 polyunsaturated FA that affect meat characteristics. For example, the metabolism of phospholipid, particularly the phosphoinositides (PI), appears to be important in muscle protein turnover and contractile function (Campion, 1987). In the present study, PI was not measured, nor did we investigate any aspect of muscle function, including the role of other substances such as prostaglandins also derived from precursor long-chain n-3 FA. In conclusion, compared to the basal diet, fish meal and barley/fish meal diets produced larger, lean carcasses with increased concentrations of long-chain n-3 FA and decreased ratios of n-6:n-3 FA in meat. In contrast, the lupin and barley/lupin diets produced large, fatter carcasses with increased concentrations of n-6 FA and a higher n-6:n-3 FA ratio in the meat. This indicates that the type of FA in the diet contributed to energy partition in the carcass of lambs and may have overridden or added to any effects of intestinally digested protein or carbohydrate (energy). We note also that with 2-d supplementary feeding, the potential for non-steady state in energy substrates and metabolic conditions may contribute to the partitioning outcomes for energy deposition.

Implications In lambs fed roughage and a range of supplements at similar levels of daily intakes of protein, metabolizable energy, and fat content, inclusion of fish meal in the diet either alone or in combination with barley produced meat with 111% more long-chain n-3 fatty acid and 25% less n-6 fatty acid than did the inclusion of lupin alone or in combination with barley grain in the diet. Adding barley to either lupin or fish meal in combination can produce a large carcass with 30 and 32% lower daily supplementary feed cost compared to lupin or fish meal fed alone, without changing the n-3 and n-6 fatty acid concentrations in meat. The reduction in carcass fatness with fish meal alone or in combination with barley grain did not affect the tenderness of cooked meat. The

relationships between enrichment of long-chain n-3 fatty acids and tenderness of meat in lambs needs further examination, particularly in relation to energy partition into protein synthesis or muscle deposition.

Literature Cited Atkins, K. D., and J. M. Thompson. 1979. Carcass characteristics of heavy weight crossbred lambs. I. Growth and carcass measurements. Aust. J. Agric. Res. 30:1197–1205. Baur, L. A., J. O’Connor, and L. H. Storlien. 1998. Fat, fat subtypes and insulin action. Proc. Nutr. Soc. Aust. Annu. Conf. 22:151– 157. Beauchemin, K. A., L. A. McClelland, S. D. M. Jones, and G. C. Kozub. 1995. Effects of crude protein content, protein degradability and energy concentration of the diet on growth and carcass characteristics of market lambs fed high concentrate diets. Can. J. Anim. Sci. 75:387–395. Beever, D. E., and C. L. Thorp. 1997. Supplementation of forage diets. In: R. A. S. Welch, D. J. W. Burns, S. R. Davis, A. I. Popay, and C. G. Prosser (ed.) Milk Composition, Production and Biotechnology. p 419. Biotechnology in Agriculture Series No. 18, CAB International, Wallingford, U.K. Berge, P., J. Culioli, M. Renerre, C. Touraille, D. Micol, and Y. Geay. 1993. Effect of feed protein on carcass composition and meat quality in steers. Meat Sci. 35:79–92. Bouton, P. E., P. V. Harris, D. Ratcliff, and D. W. Roberts. 1978. A research note: Shear force measurements on cooked meat from sheep of various ages. J. Food Sci. 43:1038–1039. Campion, D. R. 1987. Lipid and muscle function. In: Proc. 40th Annu. Recip. Meat Conf., Am. Meat Sci. Assoc., St. Paul, MN. pp 75–82. Cave, W. T., Jr. 1991. Dietary n-3 polyunsaturated fatty acid effects on animal tumorigenesis. FASEB J. 5:2160–2166. Clandinin, M. T., S. Cheema, C. J. Field, M. L. Garg, J. Venkatraman, and T. R. Clandnin. 1991. Dietary fat: Exogenous determination of membrane structure and cell function. FASEB J. 5:2761–2769. Comerford, J. W., R. B. House, H. W. Harpster, W. R. Henning, and J. B. Cooper. 1992. Effects of forage and protein source on feedlot performance and carcass traits of Holstein and crossbred beef steers. J. Anim. Sci. 70:1022–1031. Doreau, M., and Y. Chilliard. 1996. Digestion and metabolism of dairy fat in farm animals. In: Proc. ADAS Dairy Res. Centre Feed Evaluation and Nutr. Sci. Int. Conf., Birmingham, U.K. pp 1–35. Goldspink, G. 1991. Prospectives for the manipulation of muscle growth. In: A. M. Pearson and T. R. Dutson (ed.) Growth Regulation in Farm Animals. Advances in Meat Research. vol. 7. Elsevier Applied Science, London. Hussein, H. S., and R. M. Jordan. 1991. Fish meal as a protein supplement in finishing lamb diets. J. Anim. Sci. 69:2115–2122. Kempster, A. J., P. R. D. Avis, A. Cuthbertson, and G. Harrington. 1976. Prediction of the lean content of lamb carcasses of different breed types. J. Agric. Sci. 86:23–34. Lee, G. J., D. W. Hennessey, J. V. Nolan, and R. A. Leng. 1987. Responses to nitrogen and maize supplements by young cattle offered a low-quality pasture hay. Aust. J. Agric. Res. 38:195– 207. Leng, R. A. 1985. Efficiency of feed utilization by ruminants. In: R. B. Cumming (ed.) Recent Advances in Animal Nutrition in Australia. Paper No. 32. University of New England, Armidale, N.S.W., Australia. MacRae, J. C., and A. R. Egan. 1980. The measurement of glucose kinetics in sheep—what relevance do such measurements have to the glucose requirements of an animal? EAAP Publ. No. 26. pp 421–426. Pudoc, Wageningen, The Netherlands. Mandell, I. B., J. C. Buchanan-Smith, B. J. Holub, and C. P. Campbell. 1997. Effects of fish meal in beef cattle diets on growth performance, carcass characteristics, and fatty acid composition of longissimus muscle. J. Anim. Sci. 75:910–919.

Downloaded from jas.fass.org by guest on May 24, 2011

636

Ponnampalam et al.

Margan, D. E. 1994. Energy and protein value of lupin seed as a production ration or as a supplement for sheep fed chaffed wheaten hay. Aust. J. Exp. Agric. 34:331–337. Margan, D. E., N. McC. Graham, D. J. Minson, and T. W. Searle. 1988. Energy and protein values of four forages, including a comparison between tropical and temperate species. Aust. J. Exp. Agric. 28:729–736. McDonald, B. E. 1995. Oil properties of importance in human nutrition. In: D. Kimber and D. I. McGregor (ed.) Brassica Oilseed: Production and Utilization. CAB International, Wallingford, U.K. Moller, A. J. 1980. Analysis of warner-bratzler shear pattern with regard to myofibrillar and connective tissue components of tenderness. Meat Sci. 5:247–260. Newton, I. S. 1998. Global food fortification perspectives of long-chain w-3 fatty acids. World Rev. Nutr. Diet. 83:199–209. Paik, I. K., and R. Blair. 1996. Atherosclerosis, cholesterol and egg— review. Asian-Australas. J. Anim. Sci. 9:1–25. Ponnampalam, E. N. 1994. Carcass composition and meat quality characteristics of young sheep fed protein and energy supplements. M.S. thesis. The University of Melbourne, Australia. Ponnampalam, E. N., A. J. Sinclair, A. R. Egan, S. J. Blakeley, and B. J. Leury. 2001a. Effects of diets containing n-3 fatty acids on muscle long-chain n-3 fatty acid content in lambs fed low- and medium-quality roughage diets. J. Anim. Sci. 79:698–706. Ponnampalam, E. N., A. J. Sinclair, A. R. Egan, S. J. Blakeley, D. Li, and B. J. Leury. 2001b. Effect of dietary modification of muscle long-chain n-3 fatty acid on plasma insulin and lipid metabolites, carcass traits, and fat deposition in lambs. J. Anim. Sci. 79:895–903. Rowe, J. B., G. Brown, I. J. Ralph, J. Ferguson, and J. F. Wallace. 1989. Supplementary feeding of young Merino sheep, grazing wheat stubble, with different amounts of lupin, oat or barley grain. Aust. J. Exp. Agric. 29:29–35. Rowe, J. B., and D. W. Pethick. 1994. Starch digestion in ruminants— problems, solutions and opportunities. Proc. Nutr. Soc. Aust. Annu. Conf. 18:40–51. Rule, D. C., S. B. Smith, and J. R. Romans. 1995. Fatty acid composition of muscle and adipose tissue of meat animals. In: S. B. Smith and D. R. Smith (ed.) The Biology of Fat in Meat Animals:

Current Advances. p 144. American Society of Animal Science, Champaign, IL. Scollan, N. D., N. J. Choi, E. Kurt, A. V. Fisher, M. Enser, and J. D. Wood. 2001. Manipulating the fatty acid composition of muscle and adipose tissue in beef cattle. Br. J. Nutr. 85:115–124. Simopoulos, A. P. 1998. Overview of evolutionary aspects of w-3 fatty acids in the diet. World Rev. Nutr. Diet. 83:1–11. Sinclair, A. J., and K. O’Dea. 1987. The lipid levels and fatty acid compositions of the lean portions of Australian beef and lamb. Food Technol. Aust. 39:228–231. Smith, S. B. 1995. Substrate utilization in ruminant adipose tissues. In: S. B. Smith and D. R. Smith (ed.) The Biology of Fat in Meat Animals: Current Advances. p 166. American Society of Animal Science, Champaign, IL. Steel, R. G. D., and J. H. Torrie. 1981. Principles and Procedures of Statistics: A Biometrical Approach. 2nd ed. McGraw-Hill Publishing Co., London. Storlien, L. H., A. B. Jenkins, D. J. Chisholm, W. S. Pascoe, S. Khouri, and E. W. Kraegen. 1991. Influence of dietary fat composition on development of insulin resistance in rats: relationship to muscle triglyceride and w-3 fatty acids in muscle phospholipids. Diabetes 40:280–289. Storlien, L. H., D. A. Pan, A. D. Kriketos, J. O’Connor, I. D. Caterson, G. J. Cooney, A. B. Jenkins, and L. A. Baur. 1995. Skeletal muscle membrane and storage lipids, muscle fibre type and insulin resistance. Proc. Nutr. Soc. Aust. Annu. Conf. 19:26–32. Valentine, S. C., and B. D. Bartsch. 1987. Fermentation of hammermilled barley, lupin, pea and faba bean grain in the rumen of dairy cows. Anim. Feed Sci. Technol. 16:261–271. Vatansever, L., E. Kurt, M. Enser, N. D. Scollan, R. I. Richardson, G. R. Nute, and J. D. Wood. 1998. The quality of beef from steers fed supplements of n-3 polyunsaturated fatty acids. In: Proc. 44th Int. Congr. Meat Sci. Technol., Barcelona, Spain. pp 656–657. Wood, J. D. 1990. Consequences for meat quality of reducing carcass fatness. In: J. D. Wood and A. V. Fisher (ed.) Reducing Fat in Meat Animals. p 344. Elsevier, Barking, U.K. Yu, P., A. R. Egan, and B. J. Leury. 2000. Predicting in sacco rumen degradation kinetics of raw and dry roasted faba beans (Vicia faba) and lupin seeds (Lupinus albus) by laboratory techniques. Asian-Australas. J. Anim. Sci. 13:1377–1387.

Downloaded from jas.fass.org by guest on May 24, 2011

Citations

This article has been cited by 2 HighWire-hosted articles: http://jas.fass.org/content/80/3/628#otherarticles

Downloaded from jas.fass.org by guest on May 24, 2011