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Feeding encapsulated ground full-fat soybeans to increase polyunsaturated fat concentrations and effects on flavor volatiles in fresh lamb

Agricultural Experimental Station, University of Tennessee, Knoxville 37996

	Abstract

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This research assessed the potential of increasing PUFA concentrations and the effect on flavor volatiles in red meat by feeding ground, full-fat soybean supplemented in casein complex. Supplements consisted of untreated ground, full-fat soybean (CO) or ground, full-fat soybeans treated with acetaldehyde (AC) or diacetyl (DA) to form gels. On a DM basis, the control (CO), AC, and DA supplements contained 48.6, 50.0, and 49.1% CP and 17.3, 17.3, and 17.4% fat, respectively. Weaned feeder lambs (n = 18) were divided into three treatment groups with two pens of three lambs per group. One of three supplements (200 g of DM) plus 1 kg DM of a ground corn basal diet and 0.36 kg DM of grass hay was fed daily to each of six lambs in a group for 9 wk. Samples of the intramuscular (LM), intermuscular, subcutaneous, and kidney fat were obtained from each lamb carcass for determination of total lipid contents and fatty acid profiles. Flavor volatiles of broiled LM were also analyzed. Total fat content of the LM was 3.7, 4.6, and 2.6% for lambs consuming diets supplemented with CO, AC, and DA, respectively. Compared with lambs fed the untreated supplement (CO), lambs supplemented with AC or DA had 1) higher (P < 0.05) concentrations of linoleic (4.80 vs. 6.37 or 6.80%) and linolenic (0.28 vs. 0.43 or 0.45%) acids in the LM nonpolar lipids; 2) a higher (P < 0.05) concentration of linoleic acid (22.1 vs. 27.1 or 25.6%), but a lower (P < 0.05) concentration of oleic acid (17.2 vs. 13.0 or 13.1%), in the LM polar lipids; 3) a higher (P < 0.05) concentration of linoleic acid (3.77 vs. 6.13 or 6.06%) in subcutaneous fat; and 4) higher (P < 0.05) concentrations of linoleic (4.46 vs. 7.65 or 7.13%), linolenic (0.50 vs. 0.85 or 0.80%), and stearic (24.9 vs. 27.2 or 26.9%) acids, but a lower (P < 0.05) concentration of oleic acid (39.1 vs. 35.4 or 36.3%), in kidney fat. In broiled LM chops, 21 volatiles were identified, including seven alkanals, seven 2-alkenals, two 2,4-alkadienals, and five other compounds, but most differences in the volatile concentrations among lambs fed the different supplements did not correspond to concentration differences in their precursor fatty acids. Results indicated that compared with the untreated supplement (CO), AC and DA supplements protected linoleic (C18:2n6) and linolenic (C18:3n3) acids in soybean oil from degradation in the rumen of the lambs, resulting in increased deposition in the muscle and adipose tissues of lamb.

Key Words: Flavor Volatiles • Full-Fat Soybean • Lamb • Linoleic Acid • Linolenic Acid

	Introduction

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Consumption of red meat is considered a health risk factor because of its high levels of saturated fat (40 to 50%) and lower levels of polyunsaturated fat (Gallagher et al., 1992; Simopoulos, 1994; Vanderveen, 1996). In response to the concerns of the medical community and health-conscious consumers, researchers have sought to increase unsaturated fat concentrations in products from ruminants. However, efforts to increase the levels of PUFA in ruminant meat and milk had very limited success (Gulati et al., 1997a; Scollan et al., 2001) because ruminal microorganisms hydrogenate PUFA during digestion (Hartfoot and Hazelwood, 1988; Gulati et al., 1997b). Australian researchers (Cook et al., 1970; Scott et al., 1971) produced promising supplements that could increase the levels of PUFA by preventing ruminal biohydrogenation of unsaturated dietary fat during digestion. Yet these supplements contain formaldehyde, a known carcinogen that is not allowed in animal feed additives in the United States. Efforts to find an alternative to formaldehyde led researchers (Newberry, 1990; Dje, 1994) to develop soybean oil-protein supplements treated with acetaldehyde or diacetyl. Feeding these supplements to lactating ewes increased polyunsaturation in blood serum and milk fat (Dje, 1994), suggesting that feeding such supplements to ruminant animals would increase polyunsaturation in edible tissues.

Therefore, the objectives of this research were to produce a gel containing high levels of linoleic acid (ground whole soybeans) combined with casein treated with either acetaldehyde or diacetyl, and determine the extent of PUFA deposition in the body and muscle fats of lambs fed the two treated (acetaldehyde and diacetyl) soybean gel supplements. An additional objective was to evaluate the effect of feeding the supplements on the flavor volatile compounds in cooked LM.

	Materials and Methods

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Preparation of Feeding Supplements and Chemical Composition
Sodium hydroxide was dissolved in 80°C water to adjust pH to 11.0. Sodium caseinate (Erie National Food, Erie, IL) and soy lecithin (Knoxville, TN) were dispersed in the aqueous solution. Dried, ground, full-fat soybeans (28 to 50 mesh; Tyler Feed Service Inc., Madisonville, TN) were added and mixed with the solution in a Schnell Cutter (Couch Supply Inc., Kansas City, MO). The chemical agents, acetaldehyde or diacetyl (2,3-butanedione), were poured into the mixture to form a gel. All treated soybean supplements were then cooled, ground to pass a 0.625-cm screen (Hobart Grinder; Hobart Co., Troy, OH), and stored at 5°C in sealed bags for no longer than 3 wk. Representative 100-g samples of each supplement were powdered in liquid nitrogen and stored at –18°C.

Concentrations of moisture, fat, and protein in each feeding supplement (untreated, acetaldehyde- and diacetyl-treated) were determined. Moisture content (%) was determined by the oven-drying method (Method 4.1.02; AOAC, 1995), whereas total lipid content (%) was estimated by a chloroform-methanol extraction procedure (Melton et al. 1979). Protein content (%) of untreated (ground, whole soybeans) and protected soybean-oil supplements was determined by the Kjeldahl procedure (Method 4.2.05; AOAC, 1995).

Feeding Trial and Sampling
Eighteen feeder (Dorset and Suffolk crossbred) lambs (BW = 36.0 ± 1.65 kg) were assigned randomly to a basal diet (Table 1) supplemented with either: 1) untreated supplement of ground, full-fat soybeans; 2) acetaldehyde-treated, ground, full-fat soybeans; or 3) diacetyl-treated, ground, full-fat soybeans. Levels of soybeans were identical in all diets. Each treatment was replicated in two pens, with three lambs per pen. Pens were in an enclosed barn, and each lamb was allowed 0.465 m² of floor space and provided ad libitum access to water. Lambs were fed once daily one of three supplements (200 g of DM) plus 1 kg DM of ground corn basal diet consisting predominately of cracked corn and alfalfa pellets and 0.36 kg DM of grass hay. A 14-d adjustment period was used to adapt the lambs to new feeding facilities, and allow lambs to recover from stresses associated with weaning, after which lambs were fed supplements over a 9-wk growing period. Experimental procedures were conducted according to guidelines and approval of the University of Tennessee Institutional Animal Care and Use Committee.

Chemical Composition of LM and Fat Samples
The moisture content in the LM was determined by oven-drying (Method 4.1.02; AOAC, 1995). Total lipids were extracted and quantified by the procedure of Melton et al. (1979), modified by the addition of butylated hydroxytoluene (BHT) in chloroform used for extraction (0.013% [wt/vol]). Total lipids extracted from the LM of each lamb were separated into nonpolar and polar lipids fractions by the modified procedure of Melton et al. (1994). Briefly, 0.5 g of extracted total lipids from each LM was dissolved in 10 mL of hexane:diethyl ether (HX:DE; 92:8 vol/vol), and delivered onto a Bond-Elut 5-g silica cartridge (Phenomenex Inc., Harbor City, CA). In the loaded silica cartridge, nonpolar lipids were eluted with 40 mL of the HX:DE solvent under a vacuum of 5 mm Hg. Polar lipids (phospholipids) were then eluted from the silica cartridge with 40 mL of methanol.

Fatty acid composition of total lipids extracted from LM nonpolar and polar lipids, as well as subcutaneous, kidney, and intermuscular fat of each lamb, was analyzed by preparing fatty acid methyl esters (FAME) from 0.1 g of the extracted total lipid (AOCS, 1993). The FAME were analyzed with a Shimadzu GC (model GC-9A; Shimadzu Corp., Columbia, MD) equipped with an autoinjection system (AOC-9; Shimadzu Corp.). A 0.25-mm i.d. x 30-m long fused silica capillary column (SP-2330; Supelco Inc., Bellefonte, PA) was used to separate the methyl esters, which were detected with a flame ionization detector (FID). The injection temperature was 250°C, and the column temperature was programmed from 130 to 220°C at 2°C/min. Helium was the carrier gas with a flow rate at 50 mL/min and a split ratio of 30:1. The relative weight percents of individual FAME in each sample were calculated using corrected areas (AOCS, 1993). Fatty acids were identified by matching their retention times with those of known standards (Sigma Chemical Co., St. Louis, MO) including decanoic (C10:0), undecanoic (C11:0), lauric (C12:0), tridecanoic (C13:0), myristic (C14:0), myristoleic (C14:1n5), pentadecanoic (C15:0), palmitic (C16:0), isopalmitic (C16:0I), palmitoleic (C16:1n7), trans-7-hexadeanoic (C16:1n7t), margaric (C17:0), stearic (C18:0), oleic (C18:1n9), linoleic (C18:2n6), linolenic (C18:3n3), eicosanic (C20:0), 11-eicosenoic (C20:1n9), eicosatrienoic (C20:3n6), arachadonic (C20:4n6), eicosapentaenoic (C20:5n3), and docosatrienoic (C22:5n3) acids.

Flavor Volatile Extraction and Analysis
Loin chops from the 12th rib were broiled to an internal temperature of 71°C on an electric broiler (Farberware Co., Yonkers, NY). Flavor volatiles were extracted from the broiled LM by the steam distillation extraction (SDE) method of MacLeod and Cave (1975) as modified by Melton et al. (1993). Broiled LM was blended for 5 min with 650 mL of hot (70°C) HPLC-grade water and 0.2 mL of two internal standards (1.0 mg/mL of methyl laurate and methyl myristate; Sigma Chemical Co.). Blended samples were transferred to 1-L round-bottom flasks with an inlet side tube. The flask was attached to the SDE apparatus and was immersed in a 128°C silicone oil bath. A 125-mL Erlenmeyer flask containing 45 mL of methylene chloride (CH₂Cl₂) was attached to the SDE apparatus on a hot plate until CH₂Cl₂ boiled. Nitrogen gas was bubbled at a slow rate through the blended sample, passed over a dry ice-ethanol cold trap, and out of the SDE system. Dry ice was added to the cold trap every 15 to 20 min to maintain temperature at –60°C. Volatiles were extracted for 2.5 h. A 1-mL pyrogallol solution (0.1 mg/mL methanol) was then added to each extract to prevent oxidation of the volatiles. The extract was dried with anhydrous sodium sulfate and concentrated to 0.2 mL by the gas entrainment method of Melton et al. (1994).

The concentrated extract was analyzed with a mass spectrometer ([MS] QP1000; Shimadzu Corp.) and a gas chromatographer (C-9A; Shimadzu Corp.) equipped with a carbon dioxide cryogenic unit. A 60-m long (two 30-m columns joined by a butt connector) x 0.25-mm i.d. fused silica column (SP-2330; Supelco Inc.) was used to separate the flavor volatiles. Injection temperature was 250°C at a splitless mode of injection. The column temperature was programmed from 25 to 50°C (10°C/min), from 50 to 230°C (3°C/min), and holding at 230°C for 25 min. Mass spectra of the flavor volatiles in each treatment group were obtained at a gain of 4.5, 250°C ion source temperature, and an energy level of 70 eV. Positive identification of a flavor volatile component in a sample was determined by matching the sample mass spectrum and retention time with those of standards analyzed under the same MS-GC conditions. Tentative identification was also made by matching sample peak mass spectrum with that of known compounds through a computerized search of a mass spectra library (>70% similarity index).

Retention time of volatiles from GC-FID analysis was the same as that of standards from GC-FID analysis used for quantitative analysis. Each flavor volatile extract from the individual LM sample was analyzed with a Shimadzu GC (GC-9A; Shimadzu Corp.), equipped with the same column and conditions described for MS-GC. Different flavor volatile standards were injected into the column under the same conditions as the sample flavor volatile to determine and compare the retention time of each individual flavor volatile from MS-GC data. Quantitative analysis of the sample flavor volatile was done by the relative weight percents of the different flavor volatile in each sample calculated from the GC chromatogram using corrected areas.

Statistical Analyses
All data were analyzed as a completely randomized design using GLM procedure of SAS (SAS Inst. Inc., Cary, NC). Lamb was the experimental unit for diet treatments. Least squares means were calculated for moisture, total lipids, fatty acid, and flavor volatiles, and statistically separated by pairwise t-test (PDIFF option), protected by the ANOVA F-test (P 0.05).

	Results and Discussion

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Body Weight Gain
Daily weight gain by the lambs was not significantly different among the three supplements. The ADG was 238, 256, and 247 (±12.8) g/d for control, acetaldehyde, and diacetyl supplements, respectively.

Chemical Composition of Feeding Supplements
Moisture contents in the three different feeding supplements (untreated, acetaldehyde-treated, and diacetyl-treated) were 10.6, 61.1, and 60.7%, respectively. On a DM basis, supplements had similar CP (48.6 to 50.0%) and crude fat levels (17.3 to 17.4%).

Chemical Composition of LM and Fat Samples
No differences were found in the moisture and total lipid contents (P = 0.15 and 0.11, respectively) in the LM of lambs fed the untreated supplement than those fed the two treated (acetaldehyde and diacetyl) supplements (Table 2). However, lambs fed the diacetyl-treated supplement had lower (P < 0.05) amounts of total lipids in the LM than those fed the acetaldehyde-treated supplement. No (P > 0.05) differences were detected in the total lipid content of subcutaneous, kidney, and intermuscular fat depots among lambs fed the different supplements (Table 2). Results of the present study differ from those of Garrett et al. (1976), who reported that steers fed a formaldehyde-treated fat supplement were fatter at slaughter than those fed the basal diet because the protected supplement contained an additional fat source. This trend was also found in lambs fed unprotected corn oil supplements (Russo et al., 1999).

Of the SFA, lambs fed the acetaldehyde- or diacetyl-treated supplements had a lower percentage of C14:0 in the kidney fat than lambs fed the untreated supplement, but the C18:0 concentration was a higher (P < 0.05) in those fed treated supplements. Neither C14:0 nor C18:0 percent in kidney fat from lambs fed treated supplements was (P > 0.05) different (Table 4). Mean concentrations of C16:1n7 and C18:1n9 in the kidney fat of lambs fed the untreated supplement were higher (P < 0.05) than in the kidney fat of lambs fed the treated supplements; however, no differences were observed in either C16:1n7 or C18:1n9 (P = 0.30 and 0.34, respectively) concentration between lambs fed the acetaldehyde- and diacetyl-treated supplement. Lambs consuming the acetaldehyde-treated supplement had a higher (P < 0.05) percentage of C20:1n9 in their kidney fat than those fed the diacetyl-treated supplement, but C20:1n9 concentrations in lambs fed the treated supplement did not differ (P = 0.67) from concentrations in lambs fed the untreated supplement. Kidney fat of lambs fed the acetaldehyde- or diacetyl-treated supplements had higher (P < 0.05) levels of C18:2n6 and C18:3n3 than kidney fat from lambs fed the untreated supplement, but C18:2n6 and C18:3n3 concentrations were similar (P = 0.44 and 0.46, respectively) between the treated supplements.

Feeding extruded, full-fat soybeans (25.6% DM) to beef steers for 111 d failed to alter C18:2n6 concentrations in muscle tissues (Madron et al., 2002). In addition, a daily intake of soybean oil (5% DM) for 102 d could not increase the content of C18:2n6 (3.9%) in loin from heifers (Beaulieu et al., 2002). However, feeding a formaldehyde-treated casein-safflower oil supplement to ruminant animals resulted in increased levels of C18:2n6 and decreased amounts of C16:0, C16:1n7, and C18:1n9 in subcutaneous and internal body fat of beef steers (Faichney et al., 1972; Dinius et al., 1975; Garrett et al., 1976) and lambs (Scott et al., 1971). Formo et al. (1979) noted that feeding a formaldehyde-casein-safflower oil supplement increased C18:2n6 content of veal fat from 3% to approximately 12% with a simultaneous decrease in C16:0 content, which was substantially greater than that found in the present investigation. One reason for the discrepancy was that the formaldehyde supplement provided the total dietary fat requirement for veal calves (Formo et al., 1979), whereas, in the present study, only a minor portion of lambs’ daily dietary fat intake was supplied by the treated supplements; the majority of their fat intake was supplied by corn in the basal diet. Corn in the basal diet contained 3.22% crude fat and the each lamb ate an average of 1.0 kg of the diet daily; thus, lambs consumed 32.2 g/d of fat from corn. Each lamb consumed an average of approximately 34 g of protected soybean oil from the diacetyl- and acetaldehyde-treated supplements.

Flavor Volatiles in Broiled Longissimus Muscle
Twenty-five flavor volatiles were isolated, but only 21 compounds were positively identified (Table 5). Octanal, nonanal, and t-2-decenal are formed from the oxidation of C18:1n9 (Belitz, 1987; deMan, 1990). Higher (P < 0.05) concentrations of one, or more, of these volatiles in cooked LM were expected because of the higher level of C18:1n9 in the polar lipids of the LM from lambs fed the untreated supplement compared with lambs fed the treated supplements (Table 3); however, there were no (P = 0.54 to 0.88) differences in the percent concentrations of these aldehyde flavor volatile compounds in the broiled LM chops of lambs fed the treated supplements. Only lambs fed the untreated supplement had higher (P < 0.05) concentrations of nonanal in their broiled chops compared with chops from lambs fed the treated supplements. However, nonanal concentrations did not differ (P = 0.83) between chops of lambs fed the treated supplements. Pentanal, hexanal, heptanal, t-2-heptenal, t-2-octenal, and t-2-nonenal are derived from the oxidation of C18:2n6 (Belitz, 1987; deMan, 1990), yet no differences (P = 0.12 to 0.99) were detected in the percent concentrations of the saturated aldehydes (pentanal, hexanal, and heptanal) in LM chops among the dietary supplements. Broiled chops from lambs fed the untreated supplement tended to have higher (P = 0.10) levels of t-2-octenal and t-2-nonenal volatiles than did chops from lambs fed the treated supplements. Although t-2-octenal concentrations did not differ (P = 0.20) between chops of lambs fed the treated supplements, the level of t-2-nonenal tended to be higher (P = 0.07) in broiled LM of lambs fed the acetaldehyde-treated supplement than in lambs fed the diacetyl-treated supplement. Because C18:2n6 concentrations were increased by feeding the treated supplements, concentrations of all volatiles derived from C18:2n6 were expected to be higher (P < 0.05) in LM of lambs fed the chemically treated supplements than in meat from lambs fed the untreated supplement. However, this was not the case, and reasons for these discrepancies are not known at this time. The t-2-pentenal, t-2-hexenal, 2-n-pentylfuran (Belitz, 1987; deMan, 1990), and benzaldehyde (Pokorny, 1989) are flavor compounds derived from the oxidation of C18:3n3. Only the percentage of t-2-hexenal tended to be higher (P = 0.09) in the LM of lambs fed treated supplements than in lambs fed the untreated supplement, yet there was no difference (P = 0.73) in the concentrations of t-2-hexenal in broiled LM of lambs fed the treated supplements (Table 5). Perhaps the higher concentration of C18:3n3 in the nonpolar lipids of the LM of lambs fed the treated supplements contributed to the higher concentrations of t-2-hexenal.

The flavor volatile compounds, 2-cyclohexene-1-one, t,t-2,4 undecadienal, t,t-2,4-dodecanal, and 2-pentadecenal, are not derived from the oxidation of any fatty acid measured in the LM. The relative concentrations of 2-cyclohexene-1-one, t,t-2,4-undecadienal, and 2-pentadecenal were not different (P = 0.09 to 0.75) among lambs fed the different dietary supplements (Table 5). However, the level of t,t-2,4-undecadienal in broiled LM of lambs fed the untreated supplement tended to be higher (P = 0.09) than in lambs fed the treated supplements.

Park et al. (1976) found that the levels of t,t-2,4-decadienal and cis--dode-6-enollactone were higher in the cooked lamb flavor volatiles from lambs fed formaldehyde-protected supplements (sunflower seed-casein and safflower oil-casein) than those fed a basal diet. Protected supplements also produced approximately 20% C18:2n6 in muscle lipids compared with 3 to 4% C18:2n6 in muscle lipids of lambs consuming the basal diet (Park et al., 1976). Linoleic acid is the precursor of both t,t-2,4-decadienal and cis--dode-6-enollactone, as well as n-hexanal, t-2-heptenal, and 2-octenal (Park et al., 1976; Belitz, 1987); however, neither t,t-2,4-decadienal nor cis--dode-6-enolactone were detected in the broiled LM flavor volatiles in this study. Park et al. (1976) observed higher levels of n-hexanal, t-2-heptenal, and t-2-octenal in cooked meat flavor volatiles of lambs fed formaldehyde-protected supplements than in the basal diet. In contrast with results of Park et al. (1976), the level of t-2-octenal tended to be lower (P = 0.10), but hexanal and t-2-heptenal concentrations were not (P = 0.61) affected, in the LM from lambs fed the protected supplements. Perhaps the reason for these opposing results is the much lower levels of C18:2n6 in the LM lipids of lamb fed the protected supplements in the present study compared with Park et al. (1976).

	Implications

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Results of the present study indicated that concentrations of PUFA (linoleic and linolenic acids) in ground, full-fat soybeans treated with either acetaldehyde or diacetyl seem to be protected from biohydrogenation in the rumen, producing increased deposition of these acids in tissue of lambs. In the intramuscular fat of the longissimus muscle, concentrations of linoleic acid increased by 133% without altering volatile flavors when the lambs fed protected soybeans. These findings indicate that soybeans can be used in a new way to provide healthier ruminant animal products for humans. This may open new market for soybean growers by incorporation of soybeans into ruminant diets.

¹ Correspondence: Fort Valley State Univ., Agric. Res. Stn., 1005 State University Dr., Fort Valley, GA 31030-4313 (phone: 478-825-6865; fax: 478-825-6376; e-mail: leej{at}fvsu.edu).

Received for publication March 12, 2004. Accepted for publication May 10, 2004.

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