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Effects of Implanting Beef Steers with Zeranol on Fatty Acid Composition of Subcutaneous and Intramuscular Fat1
The Professional Animal Scientist 22 (2006):301–306
Effects of Implanting Beef Steers with Zeranol on Fatty Acid Composition of Subcutaneous and 1 Intramuscular Fat R. M. IBRAHIM, J. A. MARCHELLO,2 and G. C. DUFF, PAS Department of Animal Sciences, College of Agriculture and Life Sciences, University of Arizona, Tucson 85721-0038
Abstract The effect of implanting with zeranol on modulation of fatty acid composition, including omega-3 and omega-6 fatty acids, of subcutaneous (s.c.) and i.m. fat of steers was investigated, and carcasses were evaluated for quality grade and yield grade components. Forty steers were divided into 2 groups (20 steers/group); both groups were fed the same diet. Steers were fed to a constant 10 mm fat thickness (measured by ultrasound). Implanting had no effect (P > 0.05) on quality or yield grade components, but the concentration of polyunsaturated fatty acids (PUFA), including n-3 and n6 fatty acids, was greater (P < 0.05) in the s.c. fat of implanted vs. non-implanted steers. Concentration of the saturated fatty acids (SFA) was less (P < 0.05) in the s.c. fat of implanted steers than in the s.c. fat of non-implanted steers. However, the amount of monounsaturated fatty acids was greater (P < 0.05) in the s.c. fat of non-implanted steers than in the s.c. fat of implanted
1
This study was supported, in part, by the Arizona Beef Council. 2 To whom correspondence should be addressed: [email protected]
steers. In the i.m. fat of implanted steers, the content of PUFA, including n-3 and n-6 fatty acids, and the amount of one monounsaturated fatty acid were greater (P < 0.05) than in the i.m. fat of non-implanted steers. The concentration of SFA was less (P < 0.05) in the i.m. fat of implanted vs. non-implanted steers. Implantation with zeranol caused an increase in the unsaturated:saturated fatty acid ratio and an increase in n-3:n-6 PUFA ratio. These results indicated that zeranol had no effect on carcass quality, but it had a positive effect in changing the fatty acid composition of the s.c. and the i.m. fat of steers from the saturated to unsaturated. Key words: fatty acids, omega-3, omega-6, steers, zeranol
Introduction The dietary fatty acid content is of great importance to human health (Department of Health, 1994). The Department of Health recommends the contribution of fat and saturated fatty acid (SFA) should not exceed 35 and 10% of total intake, respectively (Department of Health, 1994). High levels of fat consumption, and particularly of SFA, predispose humans to coronary heart diseases. Con-
sequently, the ratio of unsaturated to SFA should increase to around 0.45, and intakes of n-3 and n-6 polyunsaturated fatty acids (PUFA) should increase as well (Department of Health, 1994). Polyunsaturated fatty acids, including n-3 and n-6 fatty acids, have a wide range of biological roles and cellular functions. These include manufacture of prostaglandins (involved in hormone synthesis), enhancement of immune function, and regulation of response to pain and inflammation (Reavley, 1998). Shahidi and Finley (2001) noted that at high intakes of n-6 fatty acids, very low-density lipoprotein output decreases and highdensity lipoprotein cholesterol removal increases via enhanced activity of hepatic triacylglycerol lipase and hepatic scavenger receptor B-1. The main effect of n-3 fatty acids is to depress plasma triacylglycerols and postprandial lipemia via depressed output of very low-density lipoprotein and chylomicrons, respectively (Shahidi and Finley, 2001). Scollan et al. (2001) suggested that increasing the concentration of n-3 fatty acids in meat would lead to a beneficial change in fatty acid composition of beef. Therefore, it is necessary to identify strategies to increase concentration of PUFA in beef; particularly n-3
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and n-6. The objective of this study was to determine the effects of zeranol on the fatty acid composition of subcutaneous (s.c.) and i.m. lipid of steers.
Materials and Methods Forty crossbred Hereford steers born and raised at the University of Arizona V-V Ranch, near Camp Verde, Arizona were used in the study. Steers were weaned before being transferred to the University of Arizona feedlot in Tucson. On d 14 of the finishing period, steers were randomly divided into 2 groups of 20 animals each. One group was not implanted (NI) and the other group was implanted (I) with 36 mg of zeranol (Ralgro, Schering-Plough Animal Health Corp., Union, NJ). Steers within treatment were randomly housed in four, 43 × 37 m pens with 10 steers/pen. Steers were group-fed twice daily at 0600 and at 1700 h to ensure ad libitum intake. The diet used in this study was formulated according to NRC (1984). The diet (DM basis) was composed of 69.03% steam-flaked milo, 21.8% alfalfa, 0.73% limestone, 0.49% salt, 0.49% urea, 1.23% vitamin E mineral mixture, 0.038% vitamin A, 4.19% molasses, and 1.99% tallow. Calculated chemical composition of the diet was 86.5% DM, 12.5% CP, 5.59% ash, 6.45% ADF, 0.7% Ca, and 0.24% P. Steers reaching around 454 kg BW were monitored for fat thickness at 2wk intervals. This was performed by scanning between the 12th and 13th rib interface using Sonovet 600 ultrasound machine equipped with a probe size 7.5 MHz (Universal Medical Systems, Inc., Bedfordhill, NY). Those reaching a compositional endpoint of 10 mm fat thickness opposite the longissimus muscle at 3 quarters the distance from the dorsal aspect of the muscle were scheduled for slaughter; the animals were slaughtered in 3 groups at The University of Arizona Meat Science Laboratory, under federal inspection. Days on feed varied within and among groups as
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an independent endpoint (fat thickness) was chosen to normalize for expected individual variation. Feedlot performance data were not evaluated in this study. All factors used to determine USDA yield grade including hot carcass weight, longissimus area, estimated kidney, pelvic, and heart fat percentage (KPH), and fat thickness were recorded and quality grade, including marbling score, lean maturity, and skeletal maturity, was evaluated after a 48-h chill (USDA, 1989). At 1 wk postharvesting, the carcasses were fabricated into primal cuts, at which time a 2.54-cm thickness of longissimus was taken for a sample of i.m. and s.c. fat. Total lipids were determined using the chloroform, methanol, and water extraction procedure described by Wooten et al. (1979). Extractions were conducted in duplicate using an Omni-mixer (Dupont instruments, Newtown, CT) equipped with a 300 mL stainless steel cup. Approximately 12 to 13 g (wet basis) of homogenous tissue in the case of i.m. fat, and 4 to 5 g in the case of s.c. fat, were placed in the cup and mixed at high speed for times indicated after each of the following additions: 100 mL methanol, mixed for 60 sec; 100 mL chloroform, mixed for 120 sec; 50 mL distilled water and approximately 1.8 g zinc acetate, mixed for 30 sec. Contents of the cup were then filtered through preweighed Whatman No.1 (9 cm in diameter) filter paper (Fisher Scientific, Pittsburgh, PA) on a Buchner funnel (VWR International, West Chester, PA) and the cup was rinsed with chloroform. Filter paper and collected organic material were dried in vacuum oven for 12 h with pressure below 6.8 kg/25 mm2 at 75°C, then cooled in a desiccator for 45 min and weighed for calculation of DM and moisture. The filtrate was transferred to a 250-mL graduated cylinder and allowed to stand until 2 phases had clearly separated (15 min). Volume of the lower phase (chloroform layer) was recorded and the upper layer was removed by aspiration. A total of 10
mL of the chloroform layer was pipetted into a 50-mL beaker and evaporated to dryness at 75°C in a vacuum oven for 12 h with pressure below 6.8 kg/25 mm2. Weight of the residue was used to calculate total extractable lipid in the sample. Lipid was stored by dissolving the residue in the beaker using 4 to 5 mL of pentane and stirring thoroughly with a glass rod. The solution was subsequently transferred into a 6-mL vial and stored in a freezer (−20°C) until transesterification and analysis of fatty acids using GLC (Cramer and Marchello, 1964). Ten mg of the extracted lipid were transferred to a 10-mL vial and dissolved with 1 mL of methylene chloride. To this solution, 3 drops (approximately 50 mg) of methanolic sodium methoxide (25% wt/vol) were added and the mixture was vortexed for 2 min. Finally, 3 drops (approximately 50 mg) of glacial acetic acid were added and the solution was vortexed for 30 sec. The solution was stored at 4°C until purification, then used for gas chromatographic analysis of methyl ester fatty acids (Hlongwane et al., 2001). The transesterified sample was placed in a sublimation tube and fitted to a sublimation tube with a cold finger (a condensing unit that involves glass fingers with cold water running through) on sublimation apparatus and vacuum of 0.2 ± 0.15 mm Hg was applied. The tubes were lowered into a glycerol bath at 60 × 2°C. After a minimum of 1 h the sublimation tube was removed from the glycerol bath and the vacuum was turned off and cooled for 30 min. Sublimation tubes were dissociated and cold fingers were rinsed with pentane. Five-mL glass-stoppered tubes were held under the cold fingers to catch pentane rinsing. Pentane was evaporated off using a sand bath, and 1 mL of methylene chloride was added; the solution then was stored at 4°C until injection into the gas chromatograph (Cramer and Marchello, 1964). A Hamilton 10-µL syringe (Varian Inc., Walnut Creek, CA) was used for
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Zeranol and Fatty Acid Concentrations in Beef Steers
TABLE 1. Effect of zeranol implants on carcass characteristics in beef steers. Item Hot carcass weight, kg Marbling scorea Quality gradeb LMc area, cm2 KPH,d % USDA yield grade
Non-implanted
Implanted
SEM
P-value
284.46 514.00 11.40 74.0 2.17 2.60
282.27 546.00 11.80 78.8 1.90 2.28
7.58 9.47 0.15 10.5 0.06 0.12
0.75 0.09 0.10 0.49 0.25 0.19
a
Small = 500, modest =600, moderate = 700. Select = 9, choice = 12, prime = 15. c Longissimus muscle. d Kidney, pelvic, and heart fat. b
the introduction of samples into the gas chromatograph. Varian Star chromatograph 3900 (Varian Inc., Walnut Creek, CA) fitted with flame ionization detector was used for the analyses. One µL of each sample was injected into the chromatograph, which had operating conditions as follows: oven temperature, 185°C, held for 5 min then increased to 250°C at rate of 1.5°C/min, then held for 5 min; injector temperature, 250°C; detector temperature, 250°C; carrier gas (helium) flow, 30 mL/min; hydrogen flow, 30 mL/min; air flow, 300 mL/min; split ratio 1:100; capillary column 100 m × 0.25 mm, CP-select CB for FAME fused silica WCOT (chrompack-select cross bonded for fatty acids methyl esters fused silica wall-coated open tubular). Individual fatty acids were identified by retention time with reference to the fatty acids standards (Nu-Chek Prep, Inc., Elysian, MN). Data were statistically analyzed using SAS (SAS Inst., Inc., Cary, NC); the analysis was performed using analysis of variance (ANOVA). The statistical model included the effects of implant treatment as the only response variable.
Results and Discussion Carcass characteristics. The carcass characteristic results presented in Table 1 showed that implanting with
zeranol did not affect (P > 0.05) any of the characteristics including hot carcass weight, marbling score, quality grade, longissimus area, KPH area, and yield grade. Zeranol binds to estrogen receptor sites and increases uterine weights in rats (Katzenellenbogen et al., 1979). These estrogenic properties are believed to be the reason for increased protein deposition through upregulation of somatotropin secretion from the anterior pi-
tuitary and insulin secretion from βcells of the pancreas (Trenkle, 1983; Sharp and Dyer, 1971). Lemieux et al. (1990) found that an increase in protein deposition was concomitantly accompanied by mobilization of fat and reduction in fat gain with zeranol implants. Implanting with zeranol has been reported to decrease marbling scores in steers (Vanderwert, et al., 1985; Duckett et al., 1996, 1999). Moreover, implanting with zeranol in combination with trenbolone acetate reduced marbling score, percentage of the carcasses grading Choice, and KPH (Brethour, 1986; Johnson et al., 1996; Reiling and Johnson, 2003). Results presented in this study are in agreement with Sharp and Dyer (1971), Borger et al. (1973), Galbraith et al. (1983); Mader et al. (1985), Loy et al. (1988), Simms et al. (1988), Apple et al. (1991), and Samber et al. (1996). They found no differences between implanted steers with zeranol and control group for any of the carcass characteristics including hot carcass weight, marbling score, KPH, and yield and quality grade. However, McCann et al. (1991)
TABLE 2. Effect of zeranol implants on saturated fatty acids concentration of intramuscular and subcutaneous fat. Intramusculara
Subcutaneousa
Item
NI %
I%
SEM
P-value
NI %
I%
SEM
P-value
C6:0 C8:0 C10:0 C11:0 C12:0 C13:0 C14:0 C15:0 C16:0 C17:0 C18:0 C20:0 C21:0 C22:0 C23:0 C24:0
0.14 0.14 0.42 0.41 0.23 0.37 6.68 0.62 23.44 0.79 11.19 0.82 0.31 0.39 0.50 1.65
0.00 0.03 0.00 0.17 0.03 0.00 7.66 0.80 23.58 1.44 12.86 1.08 0.00 0.02 0.00 0.21
0.03 0.03 0.10 0.13 0.07 0.11 0.47 0.20 1.00 0.22 0.62 0.38 0.06 0.07 0.09 0.40
0.02 0.13 0.04 0.40 0.20 0.10 0.30 0.66 0.94 0.14 0.19 0.73 0.02 0.01 0.01 0.08
0.14 0.21 0.43 0.36 0.36 0.27 7.76 0.71 25.03 1.22 12.39 1.55 0.11 0.10 0.22 0.58
0.005 0.00 0.005 0.22 0.03 0.006 8.94 0.59 23.09 0.85 11.74 0.37 0.34 0.20 0.06 1.59
0.03 0.03 0.09 0.11 0.07 0.07 0.06 0.15 0.90 0.27 0.66 0.42 0.10 0.08 0.07 0.12
0.07 0.01 0.03 0.52 0.03 0.08 0.33 0.70 0.28 0.49 0.63 0.17 0.27 0.56 0.29 0.01
a
I = implanted with 36 mg zeranol; NI = not implanted (20 steers/treatment).
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TABLE 3. Effect of zeranol implants on unsaturated fatty acids concentration of intramuscular and subcutaneous fat. Intramusculara
Subcutaneousa
Item
NI %
I%
SEM
P-value
NI %
I%
SEM
P-value
C14:1T C14:1 C15:1 C16:1T C16:1 C17:1 C18:1 C18:1T C18:2T C18:2 C18:3 C18:3G C20:5 C20:3 C20:1 C20:2 C20:3G C20:4 C24:1 C22:1 C22:2 C22:3 C22:4 C22:5 C22:6
0.17 1.65 0.10 0.32 2.92 0.38 26.26 0.63 1.20 0.33 0.76 0.37 0.88 0.97 0.69 0.28 0.52 1.45 1.54 0.56 1.59 1.39 2.20 0.98 0.96
0.00 1.46 0.00 0.01 2.84 0.16 28.08 0.05 2.24 1.83 2.40 0.73 1.70 1.80 0.30 0.03 0.72 1.46 0.07 0.78 0.88 1.09 0.88 0.95 1.06
0.07 0.21 0.04 0.11 0.25 0.05 1.31 0.24 0.26 0.30 0.35 0.05 0.24 0.27 0.18 0.06 0.08 0.31 0.45 0.11 0.32 0.22 0.54 0.15 0.13
0.23 0.65 0.27 0.18 0.87 0.06 0.49 0.25 0.05 0.01 0.02 0.003 0.10 1.30 0.30 0.06 0.22 0.98 0.11 0.04 0.29 0.51 0.23 0.90 0.70
0.13 2.52 0.014 0.15 3.43 0.44 26.98 0.17 1.46 0.46 1.24 0.46 0.96 0.93 1.37 0.03 0.39 0.58 0.29 0.13 0.63 0.60 0.71 0.83 0.78
0.006 2.87 0.009 0.04 3.35 0.13 26.32 0.08 2.32 0.69 3.02 0.66 2.03 2.17 0.06 0.06 0.56 1.59 0.04 0.11 1.01 1.24 0.77 0.77 1.71
0.03 0.36 0.007 0.04 0.26 0.05 1.05 0.03 0.37 0.08 0.47 0.06 0.27 0.36 0.27 0.03 0.06 0.18 0.06 0.05 0.17 0.12 0.10 0.15 0.21
0.08 0.63 0.70 0.20 0.88 0.007 0.75 0.20 0.25 0.21 0.07 0.14 0.05 0.09 0.02 0.69 0.19 0.008 0.07 0.86 0.28 0.01 0.76 0.86 0.03
a
I = implanted with 36 mg zeranol; NI = not implanted (20 steers/treatment).
showed that zeranol implantation in steers increased ribeye area, whereas the other carcass characteristics including yield and quality grade remained unaffected, which supports the results obtained in this study. Fatty acid composition. Fatty acid composition of the i.m. and s.c. fat tissue is shown in Table 2. Im-
planting with zeranol reduced (P < 0.05) the concentration of SFA (C8:0, C10:0, and C12:0) and (C6:0, C10:0, C21:0, C22:0, and C23:0) in s.c. fat and i.m. fat of implanted steers respectively as compared with non-implanted steers. These results indicated that zeranol had the capability of altering some of
TABLE 4. Effect of zeranol implants on conjugated linoleic fatty acid (CLA) concentration of intramuscular and subcutaneous fat. Intramusculara Item
NI %
I%
Cis 9, trans11 Trans 10, cis12
0.04 0.40
0.009 0.00
a
Subcutaneousa SEM P-value
NI %
I%
0.01 0.19
0.01 0.52
0.009 0.04
0.19 0.32
SEM P-value 0.03 0.02
I = implanted with 36 mg zeranol; NI = not implanted (20 steers/treatment).
0.13 0.79
the s.c. and i.m. fatty acid concentrations in steers; which have a positive effect in human health. Saturated fatty acids have adverse effects on human health especially coronary heart disease (Department of Health, 1994). Zeranol implants decreased some of the SFA content in both s.c. and i.m. fat of implanted steers. On the other hand, it increased some of the PUFA content, which includes n-3 and n-6 fatty acids, in both tissues, as shown in Table 3; MUFA (C17:1, and C20:1) decreased (P < 0.05) in s.c. fat of implanted steers and C22:1 increased (P < 0.05) in i.m. fat of the same group, whereas PUFA C20:5, C20:4, C22:3, and C22:6 increased (P < 0.05) in s.c. fat of implanted steers, and C18:2T, C18: 2, C18:3, and C18:3G increased in i.m. fat of the same group. Polyunsaturated fatty acids help to lessen cholesterol and decrease platelet aggregation, thus decreasing the risk of heart disease (Reavley, 1998). The balance of C20:4 n-6 and C20:5 n-3 fatty acids determines the type and biological efficacy of eicosanoids, which in turn controls thrombosis and the immune and inflammatory responses (Freese and Mutanen, 1997). Dihomogamma-linoleic acid (C20:3 n-6) and C20:5 n-3 are precursors of the beneficial prostaglandins series 1 and 3, respectively, as opposed to the harmful series 2 (Reavley, 1998). The beneficial effects of series 1 and 3 are attributed to their ability to dilate blood vessels, reduce clotting, lower LDL cholesterol levels, and raise high-density lipoprotein cholesterol, and they have anti-inflammatory actions (Reavley, 1998). In the present study zeranol implants had a limited but significant effect on n-3 and n-6 fatty acids; it increased (P < 0.05) C22:6 and C20:4 in s.c. fat of implanted steers and C18:3, C18:2, and C18:3G (P < 0.05) in i.m. fat of the same group. Results in Table 4 showed that conjugated linoleic acid cis-9,trans-11 and trans-10,cis-12 were nonsignificantly greater (P > 0.05) in non-implanted samples. To our knowledge, no data in the literature had tested the hypothesis
Zeranol and Fatty Acid Concentrations in Beef Steers
that a 36-mg zeranol (resorcyclic acid lactone, Ralgro) implant can affect the s.c. and i.m. fatty acid composition in implanted steers. However, zeranol belongs to the same pharmacological group as the anabolic implant estradiol (Synovex; Dixon, 1983). Dawson et al. (1991) reported that the use of an estradiol-based implant (Synovex) decreased the proportion of C18:1 and increased the proportions of C18:0, C18:3, and C20:0 in the triacylglycerol fraction of the intramuscular lipid extracted from the longissimus of implanted Friesian steers. Also, these authors found that in the phospholipid fraction C18:1, C20:3, and C20:4 were reduced and C18:3, C20:5, and C22:6 were increased (Dawson et al., 1991). No effects were seen on SFA (C8:0, C10:0, C12:0, C14:0, C15:0, and C17:0), on C14:1, C16:1, and C20:4, or on odd-chain fatty acids in the i.m. lipid content of steers implanted with estradiol benzoate (Duckett et al., 1999). Yet, estradiol benzoate implanting increased C18:3 and C18:0 and reduced C18:1 (Duckett et al., 1999). These findings are in agreement with those of Kennett and Siebert (1987) who detected no change in concentrations of these fatty acids with implanting of estradiol plus progesterone; however, they found that implanting increased the percentages of C18:0 and C18:3 and reduced the percentage of C18:1. In conclusion, results of the present study demonstrated that zeranol implanting is capable of modulating some of the fatty acid composition as presented above. However, some questions still need to be answered regarding the molecular mechanism by which resorcyclic acid lactone (zeranol) alters the fatty acid composition of both s.c. and i.m. fat of implanted steers.
trations and decreased some of the SFA concentrations, resulting in greater PUFA:SFA ratio. Omega3:omega-6 fatty acids ratio was greater in i.m. and s.c. fat of implanted steers than in those of nonimplanted steers. These data imply that fatty acid profiles of beef fat can be improved from a human health perspective by implanting with zeranol.
Acknowledgment The authors thank Y. Sawires at the University of New Mexico for helpful scientific discussions.
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USDA. 1989. Official United States standards for grades of carcass beef. Agricultural Marketing Services, USDA, Washington, DC. Vanderwert, W., L. L. Berger, F. K. McKeith, A. M. Baker, H. W. Gonyou, and P. J. Bechtel. 1985. Influence of zeranol implants on growth, behavior and carcass traits in Angus and Limousin bulls and steers. J. Anim. Sci. 61:310. Wooten, R. A., C. B.Roubicek, J. A. Marchello, F. D. Dryden, and R. S. Swingle. 1979. Realimentation of cull range cows. 2. Changes in carcass traits. J. Anim. Sci. 48:823.
Effects of Implanting Beef Steers with Zeranol on Fatty Acid Composition of Subcutaneous and 1 Intramuscular Fat R. M. IBRAHIM, J. A. MARCHELLO,2 and G. C. DUFF, PAS Department of Animal Sciences, College of Agriculture and Life Sciences, University of Arizona, Tucson 85721-0038
Abstract The effect of implanting with zeranol on modulation of fatty acid composition, including omega-3 and omega-6 fatty acids, of subcutaneous (s.c.) and i.m. fat of steers was investigated, and carcasses were evaluated for quality grade and yield grade components. Forty steers were divided into 2 groups (20 steers/group); both groups were fed the same diet. Steers were fed to a constant 10 mm fat thickness (measured by ultrasound). Implanting had no effect (P > 0.05) on quality or yield grade components, but the concentration of polyunsaturated fatty acids (PUFA), including n-3 and n6 fatty acids, was greater (P < 0.05) in the s.c. fat of implanted vs. non-implanted steers. Concentration of the saturated fatty acids (SFA) was less (P < 0.05) in the s.c. fat of implanted steers than in the s.c. fat of non-implanted steers. However, the amount of monounsaturated fatty acids was greater (P < 0.05) in the s.c. fat of non-implanted steers than in the s.c. fat of implanted
1
This study was supported, in part, by the Arizona Beef Council. 2 To whom correspondence should be addressed: [email protected]
steers. In the i.m. fat of implanted steers, the content of PUFA, including n-3 and n-6 fatty acids, and the amount of one monounsaturated fatty acid were greater (P < 0.05) than in the i.m. fat of non-implanted steers. The concentration of SFA was less (P < 0.05) in the i.m. fat of implanted vs. non-implanted steers. Implantation with zeranol caused an increase in the unsaturated:saturated fatty acid ratio and an increase in n-3:n-6 PUFA ratio. These results indicated that zeranol had no effect on carcass quality, but it had a positive effect in changing the fatty acid composition of the s.c. and the i.m. fat of steers from the saturated to unsaturated. Key words: fatty acids, omega-3, omega-6, steers, zeranol
Introduction The dietary fatty acid content is of great importance to human health (Department of Health, 1994). The Department of Health recommends the contribution of fat and saturated fatty acid (SFA) should not exceed 35 and 10% of total intake, respectively (Department of Health, 1994). High levels of fat consumption, and particularly of SFA, predispose humans to coronary heart diseases. Con-
sequently, the ratio of unsaturated to SFA should increase to around 0.45, and intakes of n-3 and n-6 polyunsaturated fatty acids (PUFA) should increase as well (Department of Health, 1994). Polyunsaturated fatty acids, including n-3 and n-6 fatty acids, have a wide range of biological roles and cellular functions. These include manufacture of prostaglandins (involved in hormone synthesis), enhancement of immune function, and regulation of response to pain and inflammation (Reavley, 1998). Shahidi and Finley (2001) noted that at high intakes of n-6 fatty acids, very low-density lipoprotein output decreases and highdensity lipoprotein cholesterol removal increases via enhanced activity of hepatic triacylglycerol lipase and hepatic scavenger receptor B-1. The main effect of n-3 fatty acids is to depress plasma triacylglycerols and postprandial lipemia via depressed output of very low-density lipoprotein and chylomicrons, respectively (Shahidi and Finley, 2001). Scollan et al. (2001) suggested that increasing the concentration of n-3 fatty acids in meat would lead to a beneficial change in fatty acid composition of beef. Therefore, it is necessary to identify strategies to increase concentration of PUFA in beef; particularly n-3
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and n-6. The objective of this study was to determine the effects of zeranol on the fatty acid composition of subcutaneous (s.c.) and i.m. lipid of steers.
Materials and Methods Forty crossbred Hereford steers born and raised at the University of Arizona V-V Ranch, near Camp Verde, Arizona were used in the study. Steers were weaned before being transferred to the University of Arizona feedlot in Tucson. On d 14 of the finishing period, steers were randomly divided into 2 groups of 20 animals each. One group was not implanted (NI) and the other group was implanted (I) with 36 mg of zeranol (Ralgro, Schering-Plough Animal Health Corp., Union, NJ). Steers within treatment were randomly housed in four, 43 × 37 m pens with 10 steers/pen. Steers were group-fed twice daily at 0600 and at 1700 h to ensure ad libitum intake. The diet used in this study was formulated according to NRC (1984). The diet (DM basis) was composed of 69.03% steam-flaked milo, 21.8% alfalfa, 0.73% limestone, 0.49% salt, 0.49% urea, 1.23% vitamin E mineral mixture, 0.038% vitamin A, 4.19% molasses, and 1.99% tallow. Calculated chemical composition of the diet was 86.5% DM, 12.5% CP, 5.59% ash, 6.45% ADF, 0.7% Ca, and 0.24% P. Steers reaching around 454 kg BW were monitored for fat thickness at 2wk intervals. This was performed by scanning between the 12th and 13th rib interface using Sonovet 600 ultrasound machine equipped with a probe size 7.5 MHz (Universal Medical Systems, Inc., Bedfordhill, NY). Those reaching a compositional endpoint of 10 mm fat thickness opposite the longissimus muscle at 3 quarters the distance from the dorsal aspect of the muscle were scheduled for slaughter; the animals were slaughtered in 3 groups at The University of Arizona Meat Science Laboratory, under federal inspection. Days on feed varied within and among groups as
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an independent endpoint (fat thickness) was chosen to normalize for expected individual variation. Feedlot performance data were not evaluated in this study. All factors used to determine USDA yield grade including hot carcass weight, longissimus area, estimated kidney, pelvic, and heart fat percentage (KPH), and fat thickness were recorded and quality grade, including marbling score, lean maturity, and skeletal maturity, was evaluated after a 48-h chill (USDA, 1989). At 1 wk postharvesting, the carcasses were fabricated into primal cuts, at which time a 2.54-cm thickness of longissimus was taken for a sample of i.m. and s.c. fat. Total lipids were determined using the chloroform, methanol, and water extraction procedure described by Wooten et al. (1979). Extractions were conducted in duplicate using an Omni-mixer (Dupont instruments, Newtown, CT) equipped with a 300 mL stainless steel cup. Approximately 12 to 13 g (wet basis) of homogenous tissue in the case of i.m. fat, and 4 to 5 g in the case of s.c. fat, were placed in the cup and mixed at high speed for times indicated after each of the following additions: 100 mL methanol, mixed for 60 sec; 100 mL chloroform, mixed for 120 sec; 50 mL distilled water and approximately 1.8 g zinc acetate, mixed for 30 sec. Contents of the cup were then filtered through preweighed Whatman No.1 (9 cm in diameter) filter paper (Fisher Scientific, Pittsburgh, PA) on a Buchner funnel (VWR International, West Chester, PA) and the cup was rinsed with chloroform. Filter paper and collected organic material were dried in vacuum oven for 12 h with pressure below 6.8 kg/25 mm2 at 75°C, then cooled in a desiccator for 45 min and weighed for calculation of DM and moisture. The filtrate was transferred to a 250-mL graduated cylinder and allowed to stand until 2 phases had clearly separated (15 min). Volume of the lower phase (chloroform layer) was recorded and the upper layer was removed by aspiration. A total of 10
mL of the chloroform layer was pipetted into a 50-mL beaker and evaporated to dryness at 75°C in a vacuum oven for 12 h with pressure below 6.8 kg/25 mm2. Weight of the residue was used to calculate total extractable lipid in the sample. Lipid was stored by dissolving the residue in the beaker using 4 to 5 mL of pentane and stirring thoroughly with a glass rod. The solution was subsequently transferred into a 6-mL vial and stored in a freezer (−20°C) until transesterification and analysis of fatty acids using GLC (Cramer and Marchello, 1964). Ten mg of the extracted lipid were transferred to a 10-mL vial and dissolved with 1 mL of methylene chloride. To this solution, 3 drops (approximately 50 mg) of methanolic sodium methoxide (25% wt/vol) were added and the mixture was vortexed for 2 min. Finally, 3 drops (approximately 50 mg) of glacial acetic acid were added and the solution was vortexed for 30 sec. The solution was stored at 4°C until purification, then used for gas chromatographic analysis of methyl ester fatty acids (Hlongwane et al., 2001). The transesterified sample was placed in a sublimation tube and fitted to a sublimation tube with a cold finger (a condensing unit that involves glass fingers with cold water running through) on sublimation apparatus and vacuum of 0.2 ± 0.15 mm Hg was applied. The tubes were lowered into a glycerol bath at 60 × 2°C. After a minimum of 1 h the sublimation tube was removed from the glycerol bath and the vacuum was turned off and cooled for 30 min. Sublimation tubes were dissociated and cold fingers were rinsed with pentane. Five-mL glass-stoppered tubes were held under the cold fingers to catch pentane rinsing. Pentane was evaporated off using a sand bath, and 1 mL of methylene chloride was added; the solution then was stored at 4°C until injection into the gas chromatograph (Cramer and Marchello, 1964). A Hamilton 10-µL syringe (Varian Inc., Walnut Creek, CA) was used for
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Zeranol and Fatty Acid Concentrations in Beef Steers
TABLE 1. Effect of zeranol implants on carcass characteristics in beef steers. Item Hot carcass weight, kg Marbling scorea Quality gradeb LMc area, cm2 KPH,d % USDA yield grade
Non-implanted
Implanted
SEM
P-value
284.46 514.00 11.40 74.0 2.17 2.60
282.27 546.00 11.80 78.8 1.90 2.28
7.58 9.47 0.15 10.5 0.06 0.12
0.75 0.09 0.10 0.49 0.25 0.19
a
Small = 500, modest =600, moderate = 700. Select = 9, choice = 12, prime = 15. c Longissimus muscle. d Kidney, pelvic, and heart fat. b
the introduction of samples into the gas chromatograph. Varian Star chromatograph 3900 (Varian Inc., Walnut Creek, CA) fitted with flame ionization detector was used for the analyses. One µL of each sample was injected into the chromatograph, which had operating conditions as follows: oven temperature, 185°C, held for 5 min then increased to 250°C at rate of 1.5°C/min, then held for 5 min; injector temperature, 250°C; detector temperature, 250°C; carrier gas (helium) flow, 30 mL/min; hydrogen flow, 30 mL/min; air flow, 300 mL/min; split ratio 1:100; capillary column 100 m × 0.25 mm, CP-select CB for FAME fused silica WCOT (chrompack-select cross bonded for fatty acids methyl esters fused silica wall-coated open tubular). Individual fatty acids were identified by retention time with reference to the fatty acids standards (Nu-Chek Prep, Inc., Elysian, MN). Data were statistically analyzed using SAS (SAS Inst., Inc., Cary, NC); the analysis was performed using analysis of variance (ANOVA). The statistical model included the effects of implant treatment as the only response variable.
Results and Discussion Carcass characteristics. The carcass characteristic results presented in Table 1 showed that implanting with
zeranol did not affect (P > 0.05) any of the characteristics including hot carcass weight, marbling score, quality grade, longissimus area, KPH area, and yield grade. Zeranol binds to estrogen receptor sites and increases uterine weights in rats (Katzenellenbogen et al., 1979). These estrogenic properties are believed to be the reason for increased protein deposition through upregulation of somatotropin secretion from the anterior pi-
tuitary and insulin secretion from βcells of the pancreas (Trenkle, 1983; Sharp and Dyer, 1971). Lemieux et al. (1990) found that an increase in protein deposition was concomitantly accompanied by mobilization of fat and reduction in fat gain with zeranol implants. Implanting with zeranol has been reported to decrease marbling scores in steers (Vanderwert, et al., 1985; Duckett et al., 1996, 1999). Moreover, implanting with zeranol in combination with trenbolone acetate reduced marbling score, percentage of the carcasses grading Choice, and KPH (Brethour, 1986; Johnson et al., 1996; Reiling and Johnson, 2003). Results presented in this study are in agreement with Sharp and Dyer (1971), Borger et al. (1973), Galbraith et al. (1983); Mader et al. (1985), Loy et al. (1988), Simms et al. (1988), Apple et al. (1991), and Samber et al. (1996). They found no differences between implanted steers with zeranol and control group for any of the carcass characteristics including hot carcass weight, marbling score, KPH, and yield and quality grade. However, McCann et al. (1991)
TABLE 2. Effect of zeranol implants on saturated fatty acids concentration of intramuscular and subcutaneous fat. Intramusculara
Subcutaneousa
Item
NI %
I%
SEM
P-value
NI %
I%
SEM
P-value
C6:0 C8:0 C10:0 C11:0 C12:0 C13:0 C14:0 C15:0 C16:0 C17:0 C18:0 C20:0 C21:0 C22:0 C23:0 C24:0
0.14 0.14 0.42 0.41 0.23 0.37 6.68 0.62 23.44 0.79 11.19 0.82 0.31 0.39 0.50 1.65
0.00 0.03 0.00 0.17 0.03 0.00 7.66 0.80 23.58 1.44 12.86 1.08 0.00 0.02 0.00 0.21
0.03 0.03 0.10 0.13 0.07 0.11 0.47 0.20 1.00 0.22 0.62 0.38 0.06 0.07 0.09 0.40
0.02 0.13 0.04 0.40 0.20 0.10 0.30 0.66 0.94 0.14 0.19 0.73 0.02 0.01 0.01 0.08
0.14 0.21 0.43 0.36 0.36 0.27 7.76 0.71 25.03 1.22 12.39 1.55 0.11 0.10 0.22 0.58
0.005 0.00 0.005 0.22 0.03 0.006 8.94 0.59 23.09 0.85 11.74 0.37 0.34 0.20 0.06 1.59
0.03 0.03 0.09 0.11 0.07 0.07 0.06 0.15 0.90 0.27 0.66 0.42 0.10 0.08 0.07 0.12
0.07 0.01 0.03 0.52 0.03 0.08 0.33 0.70 0.28 0.49 0.63 0.17 0.27 0.56 0.29 0.01
a
I = implanted with 36 mg zeranol; NI = not implanted (20 steers/treatment).
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TABLE 3. Effect of zeranol implants on unsaturated fatty acids concentration of intramuscular and subcutaneous fat. Intramusculara
Subcutaneousa
Item
NI %
I%
SEM
P-value
NI %
I%
SEM
P-value
C14:1T C14:1 C15:1 C16:1T C16:1 C17:1 C18:1 C18:1T C18:2T C18:2 C18:3 C18:3G C20:5 C20:3 C20:1 C20:2 C20:3G C20:4 C24:1 C22:1 C22:2 C22:3 C22:4 C22:5 C22:6
0.17 1.65 0.10 0.32 2.92 0.38 26.26 0.63 1.20 0.33 0.76 0.37 0.88 0.97 0.69 0.28 0.52 1.45 1.54 0.56 1.59 1.39 2.20 0.98 0.96
0.00 1.46 0.00 0.01 2.84 0.16 28.08 0.05 2.24 1.83 2.40 0.73 1.70 1.80 0.30 0.03 0.72 1.46 0.07 0.78 0.88 1.09 0.88 0.95 1.06
0.07 0.21 0.04 0.11 0.25 0.05 1.31 0.24 0.26 0.30 0.35 0.05 0.24 0.27 0.18 0.06 0.08 0.31 0.45 0.11 0.32 0.22 0.54 0.15 0.13
0.23 0.65 0.27 0.18 0.87 0.06 0.49 0.25 0.05 0.01 0.02 0.003 0.10 1.30 0.30 0.06 0.22 0.98 0.11 0.04 0.29 0.51 0.23 0.90 0.70
0.13 2.52 0.014 0.15 3.43 0.44 26.98 0.17 1.46 0.46 1.24 0.46 0.96 0.93 1.37 0.03 0.39 0.58 0.29 0.13 0.63 0.60 0.71 0.83 0.78
0.006 2.87 0.009 0.04 3.35 0.13 26.32 0.08 2.32 0.69 3.02 0.66 2.03 2.17 0.06 0.06 0.56 1.59 0.04 0.11 1.01 1.24 0.77 0.77 1.71
0.03 0.36 0.007 0.04 0.26 0.05 1.05 0.03 0.37 0.08 0.47 0.06 0.27 0.36 0.27 0.03 0.06 0.18 0.06 0.05 0.17 0.12 0.10 0.15 0.21
0.08 0.63 0.70 0.20 0.88 0.007 0.75 0.20 0.25 0.21 0.07 0.14 0.05 0.09 0.02 0.69 0.19 0.008 0.07 0.86 0.28 0.01 0.76 0.86 0.03
a
I = implanted with 36 mg zeranol; NI = not implanted (20 steers/treatment).
showed that zeranol implantation in steers increased ribeye area, whereas the other carcass characteristics including yield and quality grade remained unaffected, which supports the results obtained in this study. Fatty acid composition. Fatty acid composition of the i.m. and s.c. fat tissue is shown in Table 2. Im-
planting with zeranol reduced (P < 0.05) the concentration of SFA (C8:0, C10:0, and C12:0) and (C6:0, C10:0, C21:0, C22:0, and C23:0) in s.c. fat and i.m. fat of implanted steers respectively as compared with non-implanted steers. These results indicated that zeranol had the capability of altering some of
TABLE 4. Effect of zeranol implants on conjugated linoleic fatty acid (CLA) concentration of intramuscular and subcutaneous fat. Intramusculara Item
NI %
I%
Cis 9, trans11 Trans 10, cis12
0.04 0.40
0.009 0.00
a
Subcutaneousa SEM P-value
NI %
I%
0.01 0.19
0.01 0.52
0.009 0.04
0.19 0.32
SEM P-value 0.03 0.02
I = implanted with 36 mg zeranol; NI = not implanted (20 steers/treatment).
0.13 0.79
the s.c. and i.m. fatty acid concentrations in steers; which have a positive effect in human health. Saturated fatty acids have adverse effects on human health especially coronary heart disease (Department of Health, 1994). Zeranol implants decreased some of the SFA content in both s.c. and i.m. fat of implanted steers. On the other hand, it increased some of the PUFA content, which includes n-3 and n-6 fatty acids, in both tissues, as shown in Table 3; MUFA (C17:1, and C20:1) decreased (P < 0.05) in s.c. fat of implanted steers and C22:1 increased (P < 0.05) in i.m. fat of the same group, whereas PUFA C20:5, C20:4, C22:3, and C22:6 increased (P < 0.05) in s.c. fat of implanted steers, and C18:2T, C18: 2, C18:3, and C18:3G increased in i.m. fat of the same group. Polyunsaturated fatty acids help to lessen cholesterol and decrease platelet aggregation, thus decreasing the risk of heart disease (Reavley, 1998). The balance of C20:4 n-6 and C20:5 n-3 fatty acids determines the type and biological efficacy of eicosanoids, which in turn controls thrombosis and the immune and inflammatory responses (Freese and Mutanen, 1997). Dihomogamma-linoleic acid (C20:3 n-6) and C20:5 n-3 are precursors of the beneficial prostaglandins series 1 and 3, respectively, as opposed to the harmful series 2 (Reavley, 1998). The beneficial effects of series 1 and 3 are attributed to their ability to dilate blood vessels, reduce clotting, lower LDL cholesterol levels, and raise high-density lipoprotein cholesterol, and they have anti-inflammatory actions (Reavley, 1998). In the present study zeranol implants had a limited but significant effect on n-3 and n-6 fatty acids; it increased (P < 0.05) C22:6 and C20:4 in s.c. fat of implanted steers and C18:3, C18:2, and C18:3G (P < 0.05) in i.m. fat of the same group. Results in Table 4 showed that conjugated linoleic acid cis-9,trans-11 and trans-10,cis-12 were nonsignificantly greater (P > 0.05) in non-implanted samples. To our knowledge, no data in the literature had tested the hypothesis
Zeranol and Fatty Acid Concentrations in Beef Steers
that a 36-mg zeranol (resorcyclic acid lactone, Ralgro) implant can affect the s.c. and i.m. fatty acid composition in implanted steers. However, zeranol belongs to the same pharmacological group as the anabolic implant estradiol (Synovex; Dixon, 1983). Dawson et al. (1991) reported that the use of an estradiol-based implant (Synovex) decreased the proportion of C18:1 and increased the proportions of C18:0, C18:3, and C20:0 in the triacylglycerol fraction of the intramuscular lipid extracted from the longissimus of implanted Friesian steers. Also, these authors found that in the phospholipid fraction C18:1, C20:3, and C20:4 were reduced and C18:3, C20:5, and C22:6 were increased (Dawson et al., 1991). No effects were seen on SFA (C8:0, C10:0, C12:0, C14:0, C15:0, and C17:0), on C14:1, C16:1, and C20:4, or on odd-chain fatty acids in the i.m. lipid content of steers implanted with estradiol benzoate (Duckett et al., 1999). Yet, estradiol benzoate implanting increased C18:3 and C18:0 and reduced C18:1 (Duckett et al., 1999). These findings are in agreement with those of Kennett and Siebert (1987) who detected no change in concentrations of these fatty acids with implanting of estradiol plus progesterone; however, they found that implanting increased the percentages of C18:0 and C18:3 and reduced the percentage of C18:1. In conclusion, results of the present study demonstrated that zeranol implanting is capable of modulating some of the fatty acid composition as presented above. However, some questions still need to be answered regarding the molecular mechanism by which resorcyclic acid lactone (zeranol) alters the fatty acid composition of both s.c. and i.m. fat of implanted steers.
trations and decreased some of the SFA concentrations, resulting in greater PUFA:SFA ratio. Omega3:omega-6 fatty acids ratio was greater in i.m. and s.c. fat of implanted steers than in those of nonimplanted steers. These data imply that fatty acid profiles of beef fat can be improved from a human health perspective by implanting with zeranol.
Acknowledgment The authors thank Y. Sawires at the University of New Mexico for helpful scientific discussions.
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Duckett, S. K., D. G .Wagner, F. N. Owens, H. G. Dolezal, and D. R. Gill . 1999. Effect of anabolic implants on beef intramuscular lipid content. J. Anim. Sci. 77:1100. Freese, R., and M. Mutanen.1997. Alpha-linolenic acid and marine long-chain n-3 fatty acids differ only slightly in their effects on hemostatic factors in healthy subjects. Am. J. Clin. Nutr. 66:591. Galbraith, H., J. R. Scaife, G. F. M. Paterson, and E. A. Hunter. 1983. Effect of trenbolone acetate combined with estradiol-17β on the response of steers to changes in dietary protein. J. Agri. Sci. (Camb.) 101:249. Hlongwane, C., I. G. Delves, L. W. Wan, and F. O. Ayorinde. 2001. Comparative quantitative fatty acid analysis of triglycerols using matrix-assisted laser desorption/ionization time of flight mass spectrometry and gas chromatography. Rapid Commun. Mass Spectrom. 15:2027. Johnson, B. J., P. T. Anderson, J. C. Meiseke, and W. R. Dayton. 1996. Effect of a combined trenbolone acetate and estradiol implant on feedlot performance, carcass characteristics, and carcass composition of feedlot steers. J. Anim. Sci. 74:363.
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