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Prediction of Carcass Composition of Turkeys by Blood Lipids1
Prediction of Carcass Composition of Turkeys by Blood Lipids WAYNE L. BACON, KARL E. NESTOR, and EDWARD C. NABER Department of Poultry Science, The Ohio State University, Ohio Agricultural Research and Development Center, Wooster, Ohio 44691 (Received for publication October 26, 1988)
1989 Poultry Science 68:1282-1288 INTRODUCTION
In broilers, numerous workers have shown that a positive genetic correlation exists between BW and fat deposition, and that selection for increased growth rate (heavier BW) has resulted in excessive amounts of carcass fat at slaughter age (reviewed by Lin, 1981; Soller and Eitan, 1985). Some studies have also shown that different genetic stocks differ in the amount and percentage of carcass fat at market weight (reviewed by Lilburn, 1988). Selection for increased BW in commercial turkey breeding stocks is continuing, as is the tendency to market turkeys at heavier weights. In the future, carcass fat content of market turkeys may reach undesirable levels, as in broilers (Lilburn, 1988), as selection continues for increased BW in this species (Bacon and Nestor, 1985). Carcasses of female turkeys also accumulate increasingly more fat than those of male turkeys during the growing period, starting at ages of greater than 8 wk or BW greater than 3 kg (Leeson and Summers, 1980; Bacon et al., 1986). Lipid stored in adipose tissue is mainly triacylglyceride (TG) and is either absorbed
Salaries and research support provided by State and Federal funds appropriated to the Ohio Agricultural Research and Development Center, The Ohio State University. Manuscript number 266-88.
from the diet or synthesized de novo from other nutrients. After absorption, lipid of dietary origin is transported by the circulatory system from the gut to sites of utilization in the form of portomicrons (Bensadoun and Rothfield, 1972). Lipid synthesized de novo is transported from its site of origin in the liver to sites of utilization in the form of very low density lipoprotein (VLDL; Bensadoun and Kompiang, 1979). The TG transported to peripheral tissues by portomicrons and VLDL is hydrolyzed and removed from the lipoproteins primarily by lipoprotein lipase (Bensadoun and Kompiang, 1979). Lipoprotein lipase is found on the endothelial lining of capillary beds of adipose and muscle tissues (Borron et al, 1979). The nonesterified fatty acids (NEFA) released from TG in muscle tissue may ultimately be oxidized for energy or stored in limited quantities, whereas the NEFA released from TG in adipose tissue may be transported into adipocytes, re-esterified, and stored as TG in relatively large quantities. From 70 to 85% of the weight of adipose tissue may be fat (Nir et al, 1988). The metabolism of plasma lipoproteins has recently been reviewed by Griffin and Hermier (1988). Adipose tissue TG may undergo hydrolysis in periods of negative energy balance and be mobilized as NEFA. During periods of fasting, NEFA may increase three to four-fold in comparison to levels seen in turkeys fed ad libitum, whereas TG may decrease 60 to 75% in birds in the fasted state (Bacon, 1986).
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ABSTRACT Prediction of percentages of carcass fat or abdominal fat pad by blood plasma concentrations of triacylglycerides (TG) and nonesterified fatty acids (NEFA) was examined in growing turkeys fed diets low in fat. Both TG and NEFA were determined under ad libitum feeding and after overnight fasting conditions. Abdominal fat and blood plasma TG were significantly correlated (K.01). Males and females did not differ in NEFA concentration under ad libitum feeding, but males had higher concentrations of NEFA after overnight fasting (P<.05). The concentration of NEFA was not correlated with abdominal fat (P>.05). (Key words: carcass fat, abdominal fat, nonesterified fatty acids, triacylglycerides, turkeys)
CARCASS FAT PREDICTION IN TURKEYS
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TABLE 1. Ingredient composition and calculated composition of the diets used in Experiments 1 and 2 Experiment 1
Ingredient
Experiment 2 «w. i
52.70 29.10 5.00 5.00 2.50 2.50 2.00
51.65 27.90 5.00 2.50 5.00 2.50 2.50
.40 .50 .30 100.00
2.00 .40 .35 .20 100.00
17.8 2,860 1.1 .93 .60
18.8 2,870 1.3 1.00 .64
1 Premix 1 provided the following amounts per kilogram of diet: vitamin A, 8,700 IU; vitamin D3, 3,700 ICU; vitamin E, 60 IU; menadione sodium bisulfite, 3.0 mg; thiamine HC1,2.2 mg; riboflavin, 6.6 mg; niacin, 100 mg; Ca pantothenate, 15 mg; folacin, 1.1 mg; pyridoxine HC1, 2.2 mg; biotin, .16 mg; vitamin B12, 15 |ig; ethoxyquin, 125 mg; zinc, 105 mg; manganese, 83 mg; copper, 9 mg; iron, 30 mg; iodine, 1.1 mg; choline chloride, 1,000 mg; selenium, .2 mg; DL-methionine, 500 mg; and lysine HC1, 1,000 mg. 2
Premix 2 provided the same amounts of all substances listed in Premix 1 except that choline chloride was reduced to 870 mg, DL-methionine was increased to 800 mg, and lysine HC1 was omitted.
The objective of the present work was to determine whether carcass fatness of market age turkeys could be predicted by one or a combination of blood plasma lipid measurements. The authors specifically chose to measure plasma TG in turkeys fed low fat diets as an indicator of lipogenesis, and NEFA as an indicator of lipolysis; both were determined in samples collected before and after overnight fasting. Both males and females were studied, as were lines differing in growth rate. MATERIALS AND METHODS
Two experiments were conducted. In Experiment 1, 20-wk-old birds were used. These birds were of the RBC2 strain (Nestor et al., 1969) maintained at the Ohio Agricultural Research and Development Center. This strain was established 20 yr ago from elite commercial strains available at that time and has been maintained by random mating without selection. In Experiment 2, three lines were used at 16 wk of age. These lines were RBC2, F (a
line selected from the RBC2 for increased BW at 16 wk of age; Nestor, 1984) and N (a current commercial sire line). In both experiments, a low fat diet based on corn starch and soybean meal without added fat (Table 1) was fed for 1 wk prior to the experiment. Diets for each experiment were different; fat contents were calculated to be 1.1 and 1.3% for Experiments 1 and 2, respectively. The first blood sample was collected late in the photoperiod, and the feed was then removed just prior to the beginning of the scotoperiod. A second blood sample was collected just after the photoperiod began 12 h later. Turkeys were weighed when the first blood sample was collected. After the second blood sample was drawn, birds were slaughtered and percentages of carcass fat (dry matter basis), abdominal fat, leaf fat, and gizzard fat were determined in Experiment 1 as described previously (Bacon et ail., 1986). In Experiment 2, only abdominal fat was determined. Plasma was prepared using EDTA as an anticoagulant (1.5 mg/mL blood) and in the presence of 5 mg/mL protamine sulfate, as an
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Corn starch Soybean meal (44% CP) Meat scrap (50% CP) Menhaden fish meal (60% CP) Dehydrated alfalfa meal (17% CP) Dried whey product Wheat middlings Premix 1 Premix 2 2 Salt, fine (not iodized) Dicalcium phosphate (Dynafos) Ground limestone Total Calculated analysis CP ME (kcal/kg) Crude fat Calcium Total phosphorus
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TABLE 2. Means (± SD) for body weight, fat measurements, triacylgtyceride (TG), and nonesterified fatty acids (NEFA) in male and female turkeys (Experiment 1) Variable1
Males2
Body weight, kg, 20 wk Carcass fat, % DM Abdominal fat, g Leaf fat, g Gizzard fat, g TG-1. |lmol/mL TG-2, nmol/mL NEFA-1, umol/mL NEFA-2, umol/mL
9.39 19.00 22.00 12.40 9.66 1.097 .257 .118 .232
Females2 ± ± ± ± ± ± ± ± ±
.91 5.40 17.00 10.50 6.80 .210 .036 .045 .062
6.32 28.50 57.30 30.80 26.50 1.151 .370 .111 .193
± ± ± ± ± ± ± ± ±
Probability3 .49 6.30 28.00 15.30 14.80 .256 .093 .045 .048
<.01 <.01 <.01 <01 <.01 >.05 <.01 >.05 ^05
inhibitor of lipoprotein lipase (Berger and Abraham, 1977). Lipids from 1.00 mL of plasma were extracted with butanol: diisopropyl ether (40:60) by the method of Cham and Knowles (1976). After drying, plasma lipids were purified by dissolving in 5 mL chloroform:hexane:diethylether:formic acid (2:1:1:.04); phospholipids were removed with 500 mg silica gel (Biosil A, 200-325 mesh; BioRad, Richmond, CA) as reported by Homstein et al. (1967). Nonesterified fatty acids were determined on duplicate .10-mL equivalent aliquots of purified plasma lipids by the colorimetric method of Novak (1965). The TG was determined on duplicate .10-mL equivalent aliquots of purified plasma lipids by the colorimetric method of Biggs et al. (1975). Lipid concentrations in the first samples are abbreviated TG-1 and NEFA-1, and the concentrations in the second samples, collected after 12 h of fasting during the scotophase, are abbreviated TG-2 and NEFA-2. The analytical methods used have been described previously (Bacon, 1986; Scanes et al., 1986). In Experiment 1, effects of sex for each parameter were measured by ANOVA, and correlation coefficients were calculated between BW, TG-1, TG-2, NEFA-1, or NEFA-2 and leaf fat, gizzard fat, abdominal fat, and percentage of carcass fat. Correlation coefficients were calculated separately within each sex. In Experiment 2, an ANOVA was conducted with line and sex as main effects and line x sex as the interaction effect for BW, abdominal fat, TG-1, TG-2, NEFA-1, and NEFA-2 measurements. In Experiment 2,
correlation coefficients were calculated both before and after statistically removing the effects of line, sex, and the interaction of line x sex. Also in Experiment 2, multiple correlation coefficients were calculated within sex but across lines between abdominal fat and BW, TG-1, TG-2, NEFA-1, and NEFA-2. The computer program of Harvey (1977) was used to conduct the statistical analyses. RESULTS
For Experiment 1, females were smaller, had more carcass fat, and contained larger fat pads than did males (Table 2). No differences existed between sexes in the concentration of TG-1 and NEFA-1, measured in the plasma samples collected when the turkeys were fed ad libitum. However, after an overnight fast, the concentration of TG (TG-2) was greater in females, whereas no significant differences between concentrations of NEFA (NEFA-2) were observed for sex. Correlation coefficients calculated within sex for percentage of carcass, abdominal, gizzard, or leaf fat and BW, TG-1, TG-2, NEFA-1, or NEFA-2 values are presented in Table 3. These correlation coefficients indicate that a different relationship exists between fatness and plasma TG and NEFA concentrations in males and females. Body weight, TG1, and TG-2 were of greatest importance in predicting abdominal, leaf, and gizzard fat in females, whereas only TG-1 was of importance in predicting abdominal, leaf, and gizzard fat in males.
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'TG-1 = Plasma triacylglyceride in birds full fed a low fat diet; TG-2 = plasma triacylglyceride in birds after an overnight fast; NEFA-1 = plasma nonesterified fatty acids in birds full fed a low fat diet; NEFA-2 = plasma nonesterified fatty acids in birds after an overnight fast. 2 n = 9. 3 Based on 1 and 16 df.
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CARCASS FAT PREDICTION IN TURKEYS TABLE 3. Correlation coefficient among selected carcass composition traits within sex (Experiment 1) Sex
Variable
Carcass fat
Abdominal fat
Leaf fat
Gizzard fat
Male2
BW TG-1 TG-2 NEFA-1 NEFA-2 BW TG-1 TG-2 NEFA-1 NEFA-2
.40 .60 -.02 -.48 .55 .41 .60 .59 -.20 -.33
.40 .84** .19 -.23 .54 .83** .75* .72* -.36 .05
.40 .84** .18 -.26 .51 .73* .78* .53 -.41 -.01
.39 .81** .19 -.16 .56 .83** .82** .82** -.27 -.08
Female
For Experiment 2, the means of the various traits according to line, sex, and the interaction of line and sex are presented in Table 4. Body weights were smaller in RBC2, as expected, and males were heavier than females, also as expected. The least amount of abdominal fat
was found in the smaller RBC2; no significant differences between amounts were observed in the larger but equivalently sized F and N lines. Also as expected, males had less abdominal fat than females, but within this trait an interaction was present; females of the smaller RBC2
TABLE 4. Means of the various traits measured according to line, sex, and their interaction (Experiment 2)
(n) Line RBC-2 F N Sex M F Interaction3 RBC-2 x M RBC2 x F F x M F x F N x M N x F Error SD a,b
Abdominal fat
BW (16 wk)
Factor
(kg)
(g)
TG-1
TG-2
(%)
NEFA-1
NEFA-2
(Hmol/mL) —
61 61 57
6.26" 9.34a 9.34a
23.2" 63.6a 64.6a
.37 .67 .69
.845 .930 .916
.263" .394a .333 a
.140a .108" .119"
.389" .320" .319"
90 89
9.58a 7.06"
35.9" 65.0"
.38 .91
.692" 1.102a
.255" .405"
.123 .122
.368a .317"
17.2 29.3 43.6 81.0 47.2 82.1 21.9
.23 .57 .41 1.01 .44 1.01
.694 .995 .724 1.135 .657 1.175 .320
.238 .288 .288 .499 .239 .427 .153
.152 .128 .107 .109 .111 .128 .065
.394 .383 .369 .266 .340 .289 .146
31 30 30 31 29 28
7.40 5.13 10.71 8.00 10.62 8.05 .58
Means within factors and columns with no common superscripts are significantly different (P<.05). 'TG-1 = Plasma triacylglyceride in birds full fed a low fat diet; TG-2 = plasma triacylglyceride in birds after an overnight fast; NEFA-1 = plasma nonesterified fatty acids in birds full fed a low fat diet; NEFA-2 = plasma nonesterified fatty acids in birds after an overnight fast. RBC-2 = Randombred control line; F = 16-wk body weight selected line; N = a commercial sire line; M = males; F = females. interaction effects were present for abdominal fat and TG-2. These effects are attributed to smaller differences between the sexes within the RBC-2 line than within the F and N lines.
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*TG-1 = Plasma triacylglyceride in birds full fed a low fat diet; TG-2 = plasma triacylglyceride in birds after an overnight fast; NEFA-1 = plasma nonesterified fatty acids in birds full fed a low fat diet; NEFA-2 = plasma nonesterified fatty acids in birds after an overnight fast. 2n = 9. *P<05. **P<.01.
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BACON ET AL.
TABLE 5. Correlation coefficients between abdominal fat, body weight (18 wk), and the triacylglycerol and nonesterified fatty acid measurements for Experiment 2: values before correction for line and sex effects (above the diagonal, df = 177) and values after correction for line and sex effects (below the diagonal, df = 172)1 Trait Abdominal fat BW TG-1 TG-2 NEFA-1 NEFA-2
Abdominal fat
BW .21*
.21** .41** .33** .02 -.07
.22** .12 .10 -.07
TG-1
TG-2
NEFA-1
NEFA-2
.52** -.22**
.53** -.05 .55**
-.08 -.11 .14 -.01
_ 27** -.08 .00 -.38** .14
.39** .16* .14
-.02 -.30**
.12
line exhibited less of an increase than males in comparison with the larger F and N lines. The concentration of NEFA-1 was greater in the smaller RBC2 line, but no differences were found between males and females (Table 4). In contrast, TG-1 values did not differ among lines, but were greater in females than in males in all three lines. The smaller and less fat RBC2 birds maintained larger concentrations of circulating NEFA after an overnight fast (NEFA-2). Also, males had larger NEFA2 concentrations than the fatter females on the average. The TG-2 concentrations were greater in the larger F and N line birds, and in females. Correlation coefficients across lines and sexes, and with and without the treatment effects statistically removed (residual correlations) are presented in Table 5 for abdominal fat, 18-wk BW, and the TG and NEFA concentrations. Both the total and residual correlations between abdominal fat and BW were small and positive. Abdominal fat was not, however, correlated with NEFA-1 either before or after statistical removal of treatment effects from the data. Abdominal fat was negatively correlated with NEFA-2 before, but not after, statistical removal of treatment effects (residual correlations). Abdominal fat was correlated with both TG-1 and TG-2, both before and after statistical removal of the treatment effects. In this experiment, the correlation coefficient of BW and TG-1 was positive and significant after statistical removal of treatment effects. Multiple correlation coefficients were calcu-
lated across lines, but within sex, between abdominal fat and BW, TG-1, TG-2, NEFA-1, and NEFA-2. For males, r = .74, with only BW and TG-1 significantly contributing to the multiple correlation coefficient. For females, r = .81, also with only BW and TG-1 significantly contributing to the correlation coefficient. For both males and females, TG-2, NEFA-1, and NEFA-2 did not significantly contribute to the multiple correlation coefficient. DISCUSSION
In both experiments, diets calculated to be very low in lipid content were fed for 1 wk prior to blood sampling. The use of a low fat diet in broilers when carcass fat content was estimated by plasma VLDL concentration has been reported to be advantageous (Whitehead and Griffin, 1982). A low fat diet was also used (Griffin and Whitehead, 1985) when plasma VLDL concentration was used to estimate carcass fat content in market turkeys. Because diets low in fat were used in the present work, the TG concentrations in the blood plasma were considered to be mainly of de novo origin. For Experiment 1, the concentration of TG-1 was in agreement with that previously reported from the authors' laboratory for ad libitum-fed male turkeys of various ages (6 to 66 wk; Bacon, 1986), but the concentration for TG-1 in Experiment 2 was somewhat less than previously reported and observed in Experiment 1. The concentrations of TG-1 observed for females were approximately the same in both experiments, and in
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'TG-1 = Plasma triacylglyceride in birds full fed a low fat diet; TG-2 = plasma triacylglyceride in birds after an overnight fast; NEFA-1 = plasma nonesterified fatty acids in birds full fed a low fat diet; NEFA-2 = plasma nonesterified fatty acids in birds after an overnight fast. *P<05. **P<.01.
CARCASS FAT PREDICTION IN TURKEYS
TG-1 did make a significant contribution. The concentrations of NEFA-1, when the turkeys were fed low fat diets ad libitum, are in agreement with those previously published from this laboratory for male turkeys fed commercial diets (Bacon, 1986). The concentrations of NEFA after 12 h fasting (NEFA-2) were less than previously reported after 24 to 48-h fasting (Bacon, 1986). Females in Experiment 2 had smaller amounts of NEFA-2 than did males, indicating a possible impairment of mobilization of NEFA in females in comparison with that in males, or a decreased rate of metabolism of NEFA in females in comparison with males. The present data are insufficient to provide an explanation for this observation. The concentration of NEFA-1 was not associated with carcass fatness in either experiment. However, in Experiment 2, there was a significant relationship between NEFA-2 and abdominal fat when treatment effects were not statistically removed during the analysis, but this effect was removed with statistical adjustment of the data. Also, with the multiple correlation analysis within sex, no association of NEFA-2 with abdominal fat was found. Thus, while the concentrations of NEFA-2 differed between sexes, they were of no value in predicting abdominal fat within a sex. As sex is easily determined, NEFA concentration would be of no practical value in predicting potential fatness of prospective breeder turkeys, either under ad libitum feeding or overnight fasting conditions. REFERENCES Bacon, W. L., 1986. Age and short-term feed restriction effects on plasma triglyceride and free-fatty acid concentrations in male turkeys. Poultry Sci. 65: 1945-1948. Bacon, W. L., and K. E. Nestor, 1985. Carcass composition changes with selection for growth in turkeys. Ohio Turkey Days, Department of Poultry Science, Ohio Agric. Res. Dev. Center, Wooster, OH. Dept. Series 90:30-35. Bacon, W. L., K. E. Nestor, and P. A. Renner, 1986. The influence of genetic increases in body weight and shank width on the abdominal fat pad and carcass composition of turkeys. Poultry Sci. 65:391-397. Bansadoun, A., and I. P. Kompiang, 1979. Role of lipoprotein lipase in plasma triglyceride removal. Fed. Proc. 38:2622-2626. Bensadoun, A., and A. Rothfield, 1972. The form of absorption of lipids in the chicken, Gallus domesticus. Proc. Soc. Exp. Biol. Med. 41:814-817. Berger, G. M., and P. R. Abraham, 1977. Selective protamine sulphate inactivation of lipoprotein lipase and hepatic lipase in human postheparin plasma: specific
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agreement with those previously reported for males (Bacon, 1986). The concentrations of TG-2 for males are in agreement with those previously reported after a 24-h fast (Bacon, 1986), and there is good agreement between the two experiments. However, in both experiments, TG-2 was greater in females than in males. An association of TG-2 with abdominal, gizzard and leaf fat was seen in females in Experiment 1. Also in Experiment 2, TG-2 was associated with abdominal fat, but the correlation coefficient decreased after statistical removal of treatment effects, including sex. Abdominal fat is associated with plasma TG in turkeys. This observation is in agreement with findings of Hermier et al. (1984), which show that males of a line of broiler chickens selected for increased abdominal fatness had greater circulating levels of TG after a 24-h fast than did males of a line selected for decreased abdominal fatness. The dynamics of changes in TG concentration with fasting were not studied in the current experiments. Whether the females would maintain greater concentrations of TG than males with increased duration of fasting is unknown. In a previous study with male turkeys (Bacon, 1986), concentrations less than those currently observed were not seen with 48-h fasting. It appears that males reach a constant baseline concentration of plasma TG within 12-h of fasting, whereas females may require a longer period of time to reach an equivalent constant baseline concentration, or alternatively maintain a greater baseline concentration of TG during fasting. The value of TG-2 in predicting carcass fatness and abdominal fat in males is questionable. In male chickens (Hermier et ai, 1984), a line selected for increased fatness had greater concentrations of TG after overnight (16 h) fasting than those of a line selected for leanness. Two hours after refeeding, the level of TG increased in both lines, but there was no difference between the lines. This observation is in agreement with the data presented in Table 4 in that the smaller line with less absolute and relative abdominal fat had smaller concentrations of TG after an overnight fast than the two larger lines that contained more abdominal fat. In females, TG-2 is of questionable value in predicting carcass fat and abdominal fat. With the multiple correlation analysis, TG-2 made no significant contribution when included in the analysis, whereas
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BACON ET AL. Lilburn, M. S., 1988. Commercial consequences of selecting for leanness in poultry. Pages 387-396 in: Leanness in Domestic Birds. Genetic, Metabolic and Hormonal Aspects. B. Leclercq and C. C. Whitehead, ed. Butterworths, London, England, U.K. Lin, C. Y., 1981. Relationship between increased body weight and fat deposition in broilers. World's Poult. Sci. J. 37:106-109. Nestor, K. E., 1984. Genetics of growth and reproduction in the turkey. 9. Long-term selection for increased 16week body weight. Poultry Sci. 63:2114-2122. Nestor, K. E., M. G. McCartney, and N. Bachev, 1969. Relative contributions of genetics and environment to turkey improvement. Poultry Sci. 48:1944-1949. Nir, I., Z. Nitsan, and S. Keren-Ziv, 1988. Fat deposition in birds. Pages 141-174 in: Leanness in Domestic Birds. Genetic, Metabolic and Hormonal Aspects. B. Leclercq and C. C. Whitehead, ed. Butterworths, London, England, U.K. Novak, M., 1965. Colorimetric ultramicro method for the determination of free fatty acids. J. Lipid Res. 6: 431-433. Scanes, C. G., D. R. Duyka, T. J. Lauterio, S. J. Bowen, L. M. Huybrechts, W. L. Bacon, and D. B. King, 1986. Effect of chicken growth hormone, triiodothyronine and hypophysectomy in growing domestic fowl. Growth 50:12-31. Soller, M., and Y. Eitan, 1985. Why docs selection for liveweight gain increase fat deposition? A Model. World's Poult. Sci. J. 40:5-9. Whitehead, C. C, and H. D. Griffin, 1982. Plasma lipoprotein concentration as an indicator of fatness in broilers: effect of age and diet. Br. Poult. Sci. 23:299-305.
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lipase levels in normals and Type I hyperlipoproteinaemia. Clin. Chem. Acta 81:219-228. Biggs, H. G., J. M. Erikson, and W. R. Moorhead, 1975. A manual colorimetric assay of triglycerides in serum. Clin. Chem. 21:437-441. Borron, D. C , L. S. Jensen, M. G. McCartney, and W. M. Britton, 1979. Comparison of lipoprotein lipase activities in chickens and turkeys. Poultry Sci. 58:659-662. Cham, B. E., and B. R. Knowles, 1976. A solvent system for delipidation of plasma or serum without protein precipitation. J. Lipid Res. 17:176-181. Griffin, H. D., and D. Hermier, 1988. Plasma lipoprotein metabolism and fattening in poultry. Pages 175-201 in: Leanness in Domestic Birds. Genetic, Metabolic and Hormonal Aspects. B. Leclercq and C. C. Whitehead, ed. Butterworths, London, England, U.K. Griffin, H. D., and C. C. Whitehead, 1985. Identification of lean and fat turkeys by measurement of plasma very low density lipoprotein. Br. Poult. Sci. 26:51-56. Harvey, W. R., 1977. User's Guide for LSML76 Mixed Model Least Squares and Maximum Likelihood Computer Program. The Ohio State University, Columbus, OH. Hermier, D., M. J. Chapman, and B. Leclercq, 1984. Plasma lipoprotein profile in fasted and refed chickens of two strains selected for high or low adiposity. J. Nutr. 114: 1112-1121. Homstein, I., P. F. Crowe, and J. B. Ruck, 1967. Separation of muscle lipids into cla ses by non-chromatographic techniques. Anal. Chem. 39:352-354. Leeson, S., and J. D. Summers, 1980. Production and carcass characteristics of the large turkey. Poultry Sci. 59: 1237-1245.
1989 Poultry Science 68:1282-1288 INTRODUCTION
In broilers, numerous workers have shown that a positive genetic correlation exists between BW and fat deposition, and that selection for increased growth rate (heavier BW) has resulted in excessive amounts of carcass fat at slaughter age (reviewed by Lin, 1981; Soller and Eitan, 1985). Some studies have also shown that different genetic stocks differ in the amount and percentage of carcass fat at market weight (reviewed by Lilburn, 1988). Selection for increased BW in commercial turkey breeding stocks is continuing, as is the tendency to market turkeys at heavier weights. In the future, carcass fat content of market turkeys may reach undesirable levels, as in broilers (Lilburn, 1988), as selection continues for increased BW in this species (Bacon and Nestor, 1985). Carcasses of female turkeys also accumulate increasingly more fat than those of male turkeys during the growing period, starting at ages of greater than 8 wk or BW greater than 3 kg (Leeson and Summers, 1980; Bacon et al., 1986). Lipid stored in adipose tissue is mainly triacylglyceride (TG) and is either absorbed
Salaries and research support provided by State and Federal funds appropriated to the Ohio Agricultural Research and Development Center, The Ohio State University. Manuscript number 266-88.
from the diet or synthesized de novo from other nutrients. After absorption, lipid of dietary origin is transported by the circulatory system from the gut to sites of utilization in the form of portomicrons (Bensadoun and Rothfield, 1972). Lipid synthesized de novo is transported from its site of origin in the liver to sites of utilization in the form of very low density lipoprotein (VLDL; Bensadoun and Kompiang, 1979). The TG transported to peripheral tissues by portomicrons and VLDL is hydrolyzed and removed from the lipoproteins primarily by lipoprotein lipase (Bensadoun and Kompiang, 1979). Lipoprotein lipase is found on the endothelial lining of capillary beds of adipose and muscle tissues (Borron et al, 1979). The nonesterified fatty acids (NEFA) released from TG in muscle tissue may ultimately be oxidized for energy or stored in limited quantities, whereas the NEFA released from TG in adipose tissue may be transported into adipocytes, re-esterified, and stored as TG in relatively large quantities. From 70 to 85% of the weight of adipose tissue may be fat (Nir et al, 1988). The metabolism of plasma lipoproteins has recently been reviewed by Griffin and Hermier (1988). Adipose tissue TG may undergo hydrolysis in periods of negative energy balance and be mobilized as NEFA. During periods of fasting, NEFA may increase three to four-fold in comparison to levels seen in turkeys fed ad libitum, whereas TG may decrease 60 to 75% in birds in the fasted state (Bacon, 1986).
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ABSTRACT Prediction of percentages of carcass fat or abdominal fat pad by blood plasma concentrations of triacylglycerides (TG) and nonesterified fatty acids (NEFA) was examined in growing turkeys fed diets low in fat. Both TG and NEFA were determined under ad libitum feeding and after overnight fasting conditions. Abdominal fat and blood plasma TG were significantly correlated (K.01). Males and females did not differ in NEFA concentration under ad libitum feeding, but males had higher concentrations of NEFA after overnight fasting (P<.05). The concentration of NEFA was not correlated with abdominal fat (P>.05). (Key words: carcass fat, abdominal fat, nonesterified fatty acids, triacylglycerides, turkeys)
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TABLE 1. Ingredient composition and calculated composition of the diets used in Experiments 1 and 2 Experiment 1
Ingredient
Experiment 2 «w. i
52.70 29.10 5.00 5.00 2.50 2.50 2.00
51.65 27.90 5.00 2.50 5.00 2.50 2.50
.40 .50 .30 100.00
2.00 .40 .35 .20 100.00
17.8 2,860 1.1 .93 .60
18.8 2,870 1.3 1.00 .64
1 Premix 1 provided the following amounts per kilogram of diet: vitamin A, 8,700 IU; vitamin D3, 3,700 ICU; vitamin E, 60 IU; menadione sodium bisulfite, 3.0 mg; thiamine HC1,2.2 mg; riboflavin, 6.6 mg; niacin, 100 mg; Ca pantothenate, 15 mg; folacin, 1.1 mg; pyridoxine HC1, 2.2 mg; biotin, .16 mg; vitamin B12, 15 |ig; ethoxyquin, 125 mg; zinc, 105 mg; manganese, 83 mg; copper, 9 mg; iron, 30 mg; iodine, 1.1 mg; choline chloride, 1,000 mg; selenium, .2 mg; DL-methionine, 500 mg; and lysine HC1, 1,000 mg. 2
Premix 2 provided the same amounts of all substances listed in Premix 1 except that choline chloride was reduced to 870 mg, DL-methionine was increased to 800 mg, and lysine HC1 was omitted.
The objective of the present work was to determine whether carcass fatness of market age turkeys could be predicted by one or a combination of blood plasma lipid measurements. The authors specifically chose to measure plasma TG in turkeys fed low fat diets as an indicator of lipogenesis, and NEFA as an indicator of lipolysis; both were determined in samples collected before and after overnight fasting. Both males and females were studied, as were lines differing in growth rate. MATERIALS AND METHODS
Two experiments were conducted. In Experiment 1, 20-wk-old birds were used. These birds were of the RBC2 strain (Nestor et al., 1969) maintained at the Ohio Agricultural Research and Development Center. This strain was established 20 yr ago from elite commercial strains available at that time and has been maintained by random mating without selection. In Experiment 2, three lines were used at 16 wk of age. These lines were RBC2, F (a
line selected from the RBC2 for increased BW at 16 wk of age; Nestor, 1984) and N (a current commercial sire line). In both experiments, a low fat diet based on corn starch and soybean meal without added fat (Table 1) was fed for 1 wk prior to the experiment. Diets for each experiment were different; fat contents were calculated to be 1.1 and 1.3% for Experiments 1 and 2, respectively. The first blood sample was collected late in the photoperiod, and the feed was then removed just prior to the beginning of the scotoperiod. A second blood sample was collected just after the photoperiod began 12 h later. Turkeys were weighed when the first blood sample was collected. After the second blood sample was drawn, birds were slaughtered and percentages of carcass fat (dry matter basis), abdominal fat, leaf fat, and gizzard fat were determined in Experiment 1 as described previously (Bacon et ail., 1986). In Experiment 2, only abdominal fat was determined. Plasma was prepared using EDTA as an anticoagulant (1.5 mg/mL blood) and in the presence of 5 mg/mL protamine sulfate, as an
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Corn starch Soybean meal (44% CP) Meat scrap (50% CP) Menhaden fish meal (60% CP) Dehydrated alfalfa meal (17% CP) Dried whey product Wheat middlings Premix 1 Premix 2 2 Salt, fine (not iodized) Dicalcium phosphate (Dynafos) Ground limestone Total Calculated analysis CP ME (kcal/kg) Crude fat Calcium Total phosphorus
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BACON EJ AL.
TABLE 2. Means (± SD) for body weight, fat measurements, triacylgtyceride (TG), and nonesterified fatty acids (NEFA) in male and female turkeys (Experiment 1) Variable1
Males2
Body weight, kg, 20 wk Carcass fat, % DM Abdominal fat, g Leaf fat, g Gizzard fat, g TG-1. |lmol/mL TG-2, nmol/mL NEFA-1, umol/mL NEFA-2, umol/mL
9.39 19.00 22.00 12.40 9.66 1.097 .257 .118 .232
Females2 ± ± ± ± ± ± ± ± ±
.91 5.40 17.00 10.50 6.80 .210 .036 .045 .062
6.32 28.50 57.30 30.80 26.50 1.151 .370 .111 .193
± ± ± ± ± ± ± ± ±
Probability3 .49 6.30 28.00 15.30 14.80 .256 .093 .045 .048
<.01 <.01 <.01 <01 <.01 >.05 <.01 >.05 ^05
inhibitor of lipoprotein lipase (Berger and Abraham, 1977). Lipids from 1.00 mL of plasma were extracted with butanol: diisopropyl ether (40:60) by the method of Cham and Knowles (1976). After drying, plasma lipids were purified by dissolving in 5 mL chloroform:hexane:diethylether:formic acid (2:1:1:.04); phospholipids were removed with 500 mg silica gel (Biosil A, 200-325 mesh; BioRad, Richmond, CA) as reported by Homstein et al. (1967). Nonesterified fatty acids were determined on duplicate .10-mL equivalent aliquots of purified plasma lipids by the colorimetric method of Novak (1965). The TG was determined on duplicate .10-mL equivalent aliquots of purified plasma lipids by the colorimetric method of Biggs et al. (1975). Lipid concentrations in the first samples are abbreviated TG-1 and NEFA-1, and the concentrations in the second samples, collected after 12 h of fasting during the scotophase, are abbreviated TG-2 and NEFA-2. The analytical methods used have been described previously (Bacon, 1986; Scanes et al., 1986). In Experiment 1, effects of sex for each parameter were measured by ANOVA, and correlation coefficients were calculated between BW, TG-1, TG-2, NEFA-1, or NEFA-2 and leaf fat, gizzard fat, abdominal fat, and percentage of carcass fat. Correlation coefficients were calculated separately within each sex. In Experiment 2, an ANOVA was conducted with line and sex as main effects and line x sex as the interaction effect for BW, abdominal fat, TG-1, TG-2, NEFA-1, and NEFA-2 measurements. In Experiment 2,
correlation coefficients were calculated both before and after statistically removing the effects of line, sex, and the interaction of line x sex. Also in Experiment 2, multiple correlation coefficients were calculated within sex but across lines between abdominal fat and BW, TG-1, TG-2, NEFA-1, and NEFA-2. The computer program of Harvey (1977) was used to conduct the statistical analyses. RESULTS
For Experiment 1, females were smaller, had more carcass fat, and contained larger fat pads than did males (Table 2). No differences existed between sexes in the concentration of TG-1 and NEFA-1, measured in the plasma samples collected when the turkeys were fed ad libitum. However, after an overnight fast, the concentration of TG (TG-2) was greater in females, whereas no significant differences between concentrations of NEFA (NEFA-2) were observed for sex. Correlation coefficients calculated within sex for percentage of carcass, abdominal, gizzard, or leaf fat and BW, TG-1, TG-2, NEFA-1, or NEFA-2 values are presented in Table 3. These correlation coefficients indicate that a different relationship exists between fatness and plasma TG and NEFA concentrations in males and females. Body weight, TG1, and TG-2 were of greatest importance in predicting abdominal, leaf, and gizzard fat in females, whereas only TG-1 was of importance in predicting abdominal, leaf, and gizzard fat in males.
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'TG-1 = Plasma triacylglyceride in birds full fed a low fat diet; TG-2 = plasma triacylglyceride in birds after an overnight fast; NEFA-1 = plasma nonesterified fatty acids in birds full fed a low fat diet; NEFA-2 = plasma nonesterified fatty acids in birds after an overnight fast. 2 n = 9. 3 Based on 1 and 16 df.
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CARCASS FAT PREDICTION IN TURKEYS TABLE 3. Correlation coefficient among selected carcass composition traits within sex (Experiment 1) Sex
Variable
Carcass fat
Abdominal fat
Leaf fat
Gizzard fat
Male2
BW TG-1 TG-2 NEFA-1 NEFA-2 BW TG-1 TG-2 NEFA-1 NEFA-2
.40 .60 -.02 -.48 .55 .41 .60 .59 -.20 -.33
.40 .84** .19 -.23 .54 .83** .75* .72* -.36 .05
.40 .84** .18 -.26 .51 .73* .78* .53 -.41 -.01
.39 .81** .19 -.16 .56 .83** .82** .82** -.27 -.08
Female
For Experiment 2, the means of the various traits according to line, sex, and the interaction of line and sex are presented in Table 4. Body weights were smaller in RBC2, as expected, and males were heavier than females, also as expected. The least amount of abdominal fat
was found in the smaller RBC2; no significant differences between amounts were observed in the larger but equivalently sized F and N lines. Also as expected, males had less abdominal fat than females, but within this trait an interaction was present; females of the smaller RBC2
TABLE 4. Means of the various traits measured according to line, sex, and their interaction (Experiment 2)
(n) Line RBC-2 F N Sex M F Interaction3 RBC-2 x M RBC2 x F F x M F x F N x M N x F Error SD a,b
Abdominal fat
BW (16 wk)
Factor
(kg)
(g)
TG-1
TG-2
(%)
NEFA-1
NEFA-2
(Hmol/mL) —
61 61 57
6.26" 9.34a 9.34a
23.2" 63.6a 64.6a
.37 .67 .69
.845 .930 .916
.263" .394a .333 a
.140a .108" .119"
.389" .320" .319"
90 89
9.58a 7.06"
35.9" 65.0"
.38 .91
.692" 1.102a
.255" .405"
.123 .122
.368a .317"
17.2 29.3 43.6 81.0 47.2 82.1 21.9
.23 .57 .41 1.01 .44 1.01
.694 .995 .724 1.135 .657 1.175 .320
.238 .288 .288 .499 .239 .427 .153
.152 .128 .107 .109 .111 .128 .065
.394 .383 .369 .266 .340 .289 .146
31 30 30 31 29 28
7.40 5.13 10.71 8.00 10.62 8.05 .58
Means within factors and columns with no common superscripts are significantly different (P<.05). 'TG-1 = Plasma triacylglyceride in birds full fed a low fat diet; TG-2 = plasma triacylglyceride in birds after an overnight fast; NEFA-1 = plasma nonesterified fatty acids in birds full fed a low fat diet; NEFA-2 = plasma nonesterified fatty acids in birds after an overnight fast. RBC-2 = Randombred control line; F = 16-wk body weight selected line; N = a commercial sire line; M = males; F = females. interaction effects were present for abdominal fat and TG-2. These effects are attributed to smaller differences between the sexes within the RBC-2 line than within the F and N lines.
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*TG-1 = Plasma triacylglyceride in birds full fed a low fat diet; TG-2 = plasma triacylglyceride in birds after an overnight fast; NEFA-1 = plasma nonesterified fatty acids in birds full fed a low fat diet; NEFA-2 = plasma nonesterified fatty acids in birds after an overnight fast. 2n = 9. *P<05. **P<.01.
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BACON ET AL.
TABLE 5. Correlation coefficients between abdominal fat, body weight (18 wk), and the triacylglycerol and nonesterified fatty acid measurements for Experiment 2: values before correction for line and sex effects (above the diagonal, df = 177) and values after correction for line and sex effects (below the diagonal, df = 172)1 Trait Abdominal fat BW TG-1 TG-2 NEFA-1 NEFA-2
Abdominal fat
BW .21*
.21** .41** .33** .02 -.07
.22** .12 .10 -.07
TG-1
TG-2
NEFA-1
NEFA-2
.52** -.22**
.53** -.05 .55**
-.08 -.11 .14 -.01
_ 27** -.08 .00 -.38** .14
.39** .16* .14
-.02 -.30**
.12
line exhibited less of an increase than males in comparison with the larger F and N lines. The concentration of NEFA-1 was greater in the smaller RBC2 line, but no differences were found between males and females (Table 4). In contrast, TG-1 values did not differ among lines, but were greater in females than in males in all three lines. The smaller and less fat RBC2 birds maintained larger concentrations of circulating NEFA after an overnight fast (NEFA-2). Also, males had larger NEFA2 concentrations than the fatter females on the average. The TG-2 concentrations were greater in the larger F and N line birds, and in females. Correlation coefficients across lines and sexes, and with and without the treatment effects statistically removed (residual correlations) are presented in Table 5 for abdominal fat, 18-wk BW, and the TG and NEFA concentrations. Both the total and residual correlations between abdominal fat and BW were small and positive. Abdominal fat was not, however, correlated with NEFA-1 either before or after statistical removal of treatment effects from the data. Abdominal fat was negatively correlated with NEFA-2 before, but not after, statistical removal of treatment effects (residual correlations). Abdominal fat was correlated with both TG-1 and TG-2, both before and after statistical removal of the treatment effects. In this experiment, the correlation coefficient of BW and TG-1 was positive and significant after statistical removal of treatment effects. Multiple correlation coefficients were calcu-
lated across lines, but within sex, between abdominal fat and BW, TG-1, TG-2, NEFA-1, and NEFA-2. For males, r = .74, with only BW and TG-1 significantly contributing to the multiple correlation coefficient. For females, r = .81, also with only BW and TG-1 significantly contributing to the correlation coefficient. For both males and females, TG-2, NEFA-1, and NEFA-2 did not significantly contribute to the multiple correlation coefficient. DISCUSSION
In both experiments, diets calculated to be very low in lipid content were fed for 1 wk prior to blood sampling. The use of a low fat diet in broilers when carcass fat content was estimated by plasma VLDL concentration has been reported to be advantageous (Whitehead and Griffin, 1982). A low fat diet was also used (Griffin and Whitehead, 1985) when plasma VLDL concentration was used to estimate carcass fat content in market turkeys. Because diets low in fat were used in the present work, the TG concentrations in the blood plasma were considered to be mainly of de novo origin. For Experiment 1, the concentration of TG-1 was in agreement with that previously reported from the authors' laboratory for ad libitum-fed male turkeys of various ages (6 to 66 wk; Bacon, 1986), but the concentration for TG-1 in Experiment 2 was somewhat less than previously reported and observed in Experiment 1. The concentrations of TG-1 observed for females were approximately the same in both experiments, and in
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'TG-1 = Plasma triacylglyceride in birds full fed a low fat diet; TG-2 = plasma triacylglyceride in birds after an overnight fast; NEFA-1 = plasma nonesterified fatty acids in birds full fed a low fat diet; NEFA-2 = plasma nonesterified fatty acids in birds after an overnight fast. *P<05. **P<.01.
CARCASS FAT PREDICTION IN TURKEYS
TG-1 did make a significant contribution. The concentrations of NEFA-1, when the turkeys were fed low fat diets ad libitum, are in agreement with those previously published from this laboratory for male turkeys fed commercial diets (Bacon, 1986). The concentrations of NEFA after 12 h fasting (NEFA-2) were less than previously reported after 24 to 48-h fasting (Bacon, 1986). Females in Experiment 2 had smaller amounts of NEFA-2 than did males, indicating a possible impairment of mobilization of NEFA in females in comparison with that in males, or a decreased rate of metabolism of NEFA in females in comparison with males. The present data are insufficient to provide an explanation for this observation. The concentration of NEFA-1 was not associated with carcass fatness in either experiment. However, in Experiment 2, there was a significant relationship between NEFA-2 and abdominal fat when treatment effects were not statistically removed during the analysis, but this effect was removed with statistical adjustment of the data. Also, with the multiple correlation analysis within sex, no association of NEFA-2 with abdominal fat was found. Thus, while the concentrations of NEFA-2 differed between sexes, they were of no value in predicting abdominal fat within a sex. As sex is easily determined, NEFA concentration would be of no practical value in predicting potential fatness of prospective breeder turkeys, either under ad libitum feeding or overnight fasting conditions. REFERENCES Bacon, W. L., 1986. Age and short-term feed restriction effects on plasma triglyceride and free-fatty acid concentrations in male turkeys. Poultry Sci. 65: 1945-1948. Bacon, W. L., and K. E. Nestor, 1985. Carcass composition changes with selection for growth in turkeys. Ohio Turkey Days, Department of Poultry Science, Ohio Agric. Res. Dev. Center, Wooster, OH. Dept. Series 90:30-35. Bacon, W. L., K. E. Nestor, and P. A. Renner, 1986. The influence of genetic increases in body weight and shank width on the abdominal fat pad and carcass composition of turkeys. Poultry Sci. 65:391-397. Bansadoun, A., and I. P. Kompiang, 1979. Role of lipoprotein lipase in plasma triglyceride removal. Fed. Proc. 38:2622-2626. Bensadoun, A., and A. Rothfield, 1972. The form of absorption of lipids in the chicken, Gallus domesticus. Proc. Soc. Exp. Biol. Med. 41:814-817. Berger, G. M., and P. R. Abraham, 1977. Selective protamine sulphate inactivation of lipoprotein lipase and hepatic lipase in human postheparin plasma: specific
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agreement with those previously reported for males (Bacon, 1986). The concentrations of TG-2 for males are in agreement with those previously reported after a 24-h fast (Bacon, 1986), and there is good agreement between the two experiments. However, in both experiments, TG-2 was greater in females than in males. An association of TG-2 with abdominal, gizzard and leaf fat was seen in females in Experiment 1. Also in Experiment 2, TG-2 was associated with abdominal fat, but the correlation coefficient decreased after statistical removal of treatment effects, including sex. Abdominal fat is associated with plasma TG in turkeys. This observation is in agreement with findings of Hermier et al. (1984), which show that males of a line of broiler chickens selected for increased abdominal fatness had greater circulating levels of TG after a 24-h fast than did males of a line selected for decreased abdominal fatness. The dynamics of changes in TG concentration with fasting were not studied in the current experiments. Whether the females would maintain greater concentrations of TG than males with increased duration of fasting is unknown. In a previous study with male turkeys (Bacon, 1986), concentrations less than those currently observed were not seen with 48-h fasting. It appears that males reach a constant baseline concentration of plasma TG within 12-h of fasting, whereas females may require a longer period of time to reach an equivalent constant baseline concentration, or alternatively maintain a greater baseline concentration of TG during fasting. The value of TG-2 in predicting carcass fatness and abdominal fat in males is questionable. In male chickens (Hermier et ai, 1984), a line selected for increased fatness had greater concentrations of TG after overnight (16 h) fasting than those of a line selected for leanness. Two hours after refeeding, the level of TG increased in both lines, but there was no difference between the lines. This observation is in agreement with the data presented in Table 4 in that the smaller line with less absolute and relative abdominal fat had smaller concentrations of TG after an overnight fast than the two larger lines that contained more abdominal fat. In females, TG-2 is of questionable value in predicting carcass fat and abdominal fat. With the multiple correlation analysis, TG-2 made no significant contribution when included in the analysis, whereas
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BACON ET AL. Lilburn, M. S., 1988. Commercial consequences of selecting for leanness in poultry. Pages 387-396 in: Leanness in Domestic Birds. Genetic, Metabolic and Hormonal Aspects. B. Leclercq and C. C. Whitehead, ed. Butterworths, London, England, U.K. Lin, C. Y., 1981. Relationship between increased body weight and fat deposition in broilers. World's Poult. Sci. J. 37:106-109. Nestor, K. E., 1984. Genetics of growth and reproduction in the turkey. 9. Long-term selection for increased 16week body weight. Poultry Sci. 63:2114-2122. Nestor, K. E., M. G. McCartney, and N. Bachev, 1969. Relative contributions of genetics and environment to turkey improvement. Poultry Sci. 48:1944-1949. Nir, I., Z. Nitsan, and S. Keren-Ziv, 1988. Fat deposition in birds. Pages 141-174 in: Leanness in Domestic Birds. Genetic, Metabolic and Hormonal Aspects. B. Leclercq and C. C. Whitehead, ed. Butterworths, London, England, U.K. Novak, M., 1965. Colorimetric ultramicro method for the determination of free fatty acids. J. Lipid Res. 6: 431-433. Scanes, C. G., D. R. Duyka, T. J. Lauterio, S. J. Bowen, L. M. Huybrechts, W. L. Bacon, and D. B. King, 1986. Effect of chicken growth hormone, triiodothyronine and hypophysectomy in growing domestic fowl. Growth 50:12-31. Soller, M., and Y. Eitan, 1985. Why docs selection for liveweight gain increase fat deposition? A Model. World's Poult. Sci. J. 40:5-9. Whitehead, C. C, and H. D. Griffin, 1982. Plasma lipoprotein concentration as an indicator of fatness in broilers: effect of age and diet. Br. Poult. Sci. 23:299-305.
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lipase levels in normals and Type I hyperlipoproteinaemia. Clin. Chem. Acta 81:219-228. Biggs, H. G., J. M. Erikson, and W. R. Moorhead, 1975. A manual colorimetric assay of triglycerides in serum. Clin. Chem. 21:437-441. Borron, D. C , L. S. Jensen, M. G. McCartney, and W. M. Britton, 1979. Comparison of lipoprotein lipase activities in chickens and turkeys. Poultry Sci. 58:659-662. Cham, B. E., and B. R. Knowles, 1976. A solvent system for delipidation of plasma or serum without protein precipitation. J. Lipid Res. 17:176-181. Griffin, H. D., and D. Hermier, 1988. Plasma lipoprotein metabolism and fattening in poultry. Pages 175-201 in: Leanness in Domestic Birds. Genetic, Metabolic and Hormonal Aspects. B. Leclercq and C. C. Whitehead, ed. Butterworths, London, England, U.K. Griffin, H. D., and C. C. Whitehead, 1985. Identification of lean and fat turkeys by measurement of plasma very low density lipoprotein. Br. Poult. Sci. 26:51-56. Harvey, W. R., 1977. User's Guide for LSML76 Mixed Model Least Squares and Maximum Likelihood Computer Program. The Ohio State University, Columbus, OH. Hermier, D., M. J. Chapman, and B. Leclercq, 1984. Plasma lipoprotein profile in fasted and refed chickens of two strains selected for high or low adiposity. J. Nutr. 114: 1112-1121. Homstein, I., P. F. Crowe, and J. B. Ruck, 1967. Separation of muscle lipids into cla ses by non-chromatographic techniques. Anal. Chem. 39:352-354. Leeson, S., and J. D. Summers, 1980. Production and carcass characteristics of the large turkey. Poultry Sci. 59: 1237-1245.