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Dairy Science Department, South Dakota State University, Brookings 57007-0647
Corresponding author:
D. J. Schingoethe; e-mail:
david_schingoethe{at}sdstate.edu.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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Abbreviation key: CLA = conjugated linoleic acid, , DHA = docosahexaenoic acid, , EE = ether extract, , EPA = eicosapentaenoic acid, , ESB = extruded soybeans, , FA = fatty acids, , FFA = free fatty acid, , FO = fish oil, , TVA = transvaccenic acid
Key Words: conjugated linoleic acid • transvaccenic acid • rumen digesta
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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The cis-9, trans-11 CLA in ruminant products originates from the incomplete biohydrogenation of dietary linoleic acid by the rumen bacterium Butyrivibrio fibrisolvens and by endogenous synthesis from transvaccenic acid (trans-11 C18:1; TVA), another intermediate of biohydrogenation, in mammalian tissues (Harfoot and Hazlewood, 1988). In the rumen, dietary lipids are extensively hydrolyzed and the unsaturated free FA (FFA) are biohydrogenated to more saturated FFA such as stearic acid (C18:0) by the rumen microorganisms (Harfoot and Hazlewood, 1988). The FFA in the rumen can react with cations, resulting in the formation of FA salts. The activity of ruminal microbes to hydrolyze FA from dietary sources and to hydrogenate unsaturated FA is associated with the particulate phase of the ruminal environment (Hawk and Silcock, 1970). Harfoot et al. (1973) reported that 80% of the biohydrogenation of linoleic acid occurred in association with feed particles and that negligible changes occurred in the cell-free supernatant.
Our previous research (Donovan et al., 2000; AbuGhazaleh et al., 2002; Whitlock et al., 2002;) showed that feeding fish oil, extruded soybeans, or their combination led to significant increases in the concentration of CLA and TVA in milk fat. However, the effect of these fat supplements on ruminal FA profiles has not been investigated. Therefore, the objectives of this study were to determine the effect of feeding fish oil, extruded soybeans, or their blend on milk and rumen FA profiles, especially CLA and TVA. The effect of fat supplements on the various ruminal lipid fractions [FA-salts, FFA, and esterified lipid (neutral lipid)] was another objective.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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) were a 50:50 blend of forage and concentrate (DM basis). The forage component of the diet was a 50:50 blend of alfalfa hay and corn silage (DM basis). Dietary treatments consisted of either 0% supplemental fat (control diet), the control diet with 2% added menhaden fish oil (FO) (Omega Protein Co., Reedville, VA), the control diet with 2% added fat from extruded soybeans (ESB), and the control diet with 1% added menhaden FO and 1% added fat from ESB (FO+ESB). Diets were formulated to be isonitrogenous at 18% CP and to contain a surplus of major nutrients (NRC, 2001). The DM content of forages was measured weekly, and the amounts of forages fed adjusted to maintain a 50:50 forage-to-concentrate ratio.
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Cows were milked twice daily at 0430 and 1600 h. Milk weight was recorded at each milking; milk production during the last 5 d of each period was used for statistical analysis. Milk samples collected for the determination of protein, fat, lactose, and milk fatty acids were taken from four consecutive milkings (p.m. and a.m.) on d 20 and d 21 of each period. The 24-h composite of each cow’s milk was split into two portions for analysis. One portion was refrigerated at 4°C and sent to a laboratory to be analyzed for fat, protein, lactose, and SNF (AOAC, 1990) by mid-infrared spectrophotometry (Multispec; Foss Food Technology Corp., Eden Prairie, MN); SCC (AOAC, 1990) were determined using a Fossomatic 90 (Foss Food Technology Corp.). The remaining portion was stored at –20°C until analysis of fatty acids by GLC (AbuGhazaleh et al., 2002).
Samples of ruminal contents were collected on d 20 and 21 of each period at 3 h after the morning feeding. Ruminal contents (approximately 450 g of whole ruminal contents) were removed by hand from four different locations in the rumen and mixed. Additional ruminal contents were taken and squeezed through four layers of cheesecloth and 100 ml of ruminal fluid was added to each sample. Ruminal samples were then placed into resealable plastic bags and stored on ice until processing in the laboratory. Every sample was mixed one more time by hand, subsampled (approximately 200 g), and frozen (–20°C). Frozen ruminal samples were freeze dried and ground to pass a 0.5-mm screen. The fatty acids in rumen digesta were determined by GLC of butyl esters (AbuGhazaleh et al., 2002). Individual fatty acids were identified by comparison of gas chromatography peaks with peaks of known standards (GLC-60; Nu Check Prep, Inc., Elysian, MN, and Matreya, Inc., Pleasant Gap, PA). Briefly, a 2-g sample of the dried rumen digesta was placed into 50-ml tubes with Teflon-lined screw caps, followed by the addition of 10 ml of a 1:1 mixture of acetone and ether and 75 µl of hydrochloric acid. The sample was gassed with N2, capped tightly, and heated in a water bath at 80°C for 2 h. After the sample cooled to room temperature, the solution was vortexed and centrifuged at 600 x g for 10 min, and the ether-acetone extract was transferred to a preweighed Roto-Vaporator flask. The particulate fraction was homogenized and extracted twice more with ether-acetone (1:1) to ensure removal of all fatty acids. The ether-acetone extracts were dried using Roto-Vaporator set at a temperature of 45°C, the outside of the flask was dried and placed in a dessicator for at least 4 h. Approximately 20 mg of the extracted fat was transferred into 13 x 100 mm test tubes with Teflon-lined screw caps and then analyzed for fatty acids (AbuGhazaleh et al., 2002). The lipids in the rumen digesta were then separated into FA salts, free FA, and neutral lipid fractions, essentially as described by Jenkins and Palmquist (1982) with modifications as follows. The FFA was separated from the neutral lipid by centrifugation after mixing with 0.02 M K2CO3. This was performed four times to ensure maximum separations, and samples were not dried. Samples were gassed with N2 before being heated in a water bath. Fatty acids were then analyzed by GLC after preparation of butyl esters (AbuGhazaleh et al., 2002). Fatty acid analysis of butyl esters was conducted using a HP 6890 GLC (Hewlett-Packard, Palo Alto, CA) with a Supelco 2380 fused silica capillary column (Supelco, Inc., Bellefonte, PA). Samples of alfalfa hay, corn silage, and concentrate mix were composited by period and dried at 55°C. Fat was extracted in a mixture of ether and acetone (1:1, vol/vol). Approximately 15 mg of the extracted fat was transferred into 16 x 150 mm test tubes with Teflon-lined screw caps and then analyzed for fatty acids as described by AbuGhazaleh et al. (2002).
Ruminal fluid samples for pH were collected on d 20 and 21 of each period at 3 h after the morning feeding. Samples were placed on ice until brought into the laboratory. A glass electrode was used to measure ruminal pH. Body weights and BCS (Wildman et al., 1982) were recorded at the beginning of the trial and the end of each period to determine mean BW, BW gain, BCS, and change in BCS.
Statistical Analysis
Data were analyzed as a Latin square with fixed effects of periods and treatments, the random effect was cow. Data were analyzed using the mixed model procedures of SAS (1996). Preplanned contrasts were control versus other treatment diets, FO (diet 2) versus ESB (diet 3), and FO and ESB (diet 2 and 3) versus FO + ESB (diet 4). Significance was declared at P < 0.05, unless otherwise noted.
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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. Diets were formulated to be isonitrogenous (18%); however, analyses ranged from 17.9 to 18.4% CP. Total mixed diets were relatively similar in NDF, ADF, and lignin. The control diet contained 3.1% EE (DM basis), and the EE content of the other diets was 4.9, 4.9, and 5.0% as a result of the addition of ESB and FO to the diet. Consequently, the diets containing supplemental fat had a higher NEL concentration (1.69 to 1.72 vs. 1.65 Mcal/kg for control diet).
Fatty acid compositions of TMR, forages, extruded soybeans, and menhaden fish oil are presented in Table 2. The fatty acid compositions measured were typical of the feeds. The lipid of corn silage and ESB contained the highest concentrations of linoleic acid (36.5 and 50.52 g/100 g of FA, respectively). The proportion of linolenic acid (C18:3 n3) in silage, alfalfa, and ESB averaged 6.58, 14.57, and 8.91 g/100 g of FA, respectively. Both C18:2 and C18:3 fatty acids serve as precursors of CLA produced by ruminal biohydrogenations (Harfoot and Hazlewood, 1988). Fish oil was characterized by its content of long chain (>C20) acids, being particularly rich in C20:5 n-3 (eicosapentaenoic acid, EPA) and C22:6 n-3 (docosahexaenoic acid, DHA; 11.64 and 8.17 g/100 g of FA, respectively). No trans fatty acids were detected in any of the feed ingredients.
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). This concurs with previous research in which no effect on production was observed when FO and ESB were added to the diet (Cant et al., 1997; Whitlock et al., 2002). Milk fat percentages and yield were not different among diets (P > 0.05). Although not significant (P > 0.05), the FO diet resulted in the lowest milk fat percentage, possibly because of the rapid availability of the oil in the rumen and its potential effect on fiber digestibility (Mohamed et al., 1988; Donovan et al., 2000). Dry matter intake was decreased (P < 0.05) with fat supplements, especially when FO was included in the diet. Fish oil has been shown to have a negative effect on DMI (Donovan et al., 2000; AbuGhazaleh et al., 2002; Whitlock et al., 2002). Body weight, BCS, and SCC (Table 3) were similar across all diets (P > 0.05).
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. Proportions of C6:0 to C14:0 FA were decreased (P < 0.05) with fat supplements. Addition of oil through seeds or as a free oil reduced the proportions of short-chain FA (C6:0 to C13:0) and medium-chain FA (C14:0, C15:0, C16:0, and C17:0). Similar differences were reported previously (Donovan et al., 2000; AbuGhazaleh et al., 2002; Whitlock et al., 2002). This apparent reduction in de novo synthesis of FA (
16:0) in the mammary gland has been reported with diets that increase the supply of long-chain FA (Grummer, 1991). The proportion of long-chain FA in milk fat was increased (P < 0.05) with fat supplements in this study (Table 4). As with our previous studies (Donovan et al., 2000; AbuGhazaleh et al., 2002; Whitlock et al., 2002), feeding FO, ESB, or their blend increased the proportion of unsaturated FA and decreased saturated FA in milk fat. In terms of human health, these alternations may represent an improvement in the FA profile of milk because medium-chain FA and saturated FA have been reported to constitute the hypercholesterolemic portion of milk fat (Ney, 1991).
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), daily production of cis-9, trans-11 CLA was increased (P < 0.05) by all fat supplements (87.7, 88.3, and 79.7 g/d for FO, ESB, and FO+ESB, respectively) compared with the control diet (39.7 g/d). Milk TVA was also affected by dietary treatments. The concentration of TVA in milk fat was increased 129% by the FO diet compared with the control diet, despite the fact that FO has very low concentration (< 3%) of both linoleic and linolenic acids, the precursors of TVA produced by ruminal biohydrogenations (Harfoot and Hazlewood, 1988; Griinari and Bauman, 1999). This increase in milk TVA and CLA with the FO diet supports our previous hypothesis (AbuGhazaleh et al., 2002) that FO stimulates TVA and CLA production from linoleic and linoleinc acid provided from other dietary sources. Milk TVA concentration was also increased (P < 0.05) by 136 and 102% when ESB and FO+ESB were fed, respectively, compared with the control diet. As with milk cis-9, trans-11 CLA, feeding FO+ESB diet did not lead to further increases in milk TVA concentration, possibly because of breed effect (Whitlock et al., 2002). Increasing milk TVA is beneficial since tissues in humans as well as in cows can synthesize cis-9, trans-11 CLA from TVA via the delta-9 desaturase reaction (Salminen et al., 1998). When all data were combined, the relationship between the concentration of CLA and TVA in milk fat was linear: milk CLA = 0.232 + 0.262 (TVA); r2 = 0.59, P < 0.01. This close relationship may reflect endogenous synthesis of CLA and a precursor:product relationship between TVA and CLA. Corl et al. (2001) reported that delta-9 desaturase activity is responsible for the production of at least 65% of the cis-9, trans-11 CLA in milk fat.
The proportion of C18:0 FA in milk fat was not different (P = 0.62) between control and fat supplemented diets. However, cows fed FO had the lowest proportion of C18:0 compared with other diets. The same response was also reported by Whitlock et al. (2002). This decrease in the concentration of C18:0 with the FO diet was also seen in the ruminal FA (Table 5), which might imply that FO may have caused more incomplete biohydrogenation of fatty acids in the rumen possibly by altering the rumen microbial ecosystem. Harfoot and Hazlewood (1988) indicated that biohydrogenation of unsaturated FA in the rumen involves several biochemical steps, and they suggested that no single species of rumen bacteria can catalyze the complete biohydrogenation sequence. Kemp and Lander (1984) divided bacteria into two groups based on the reactions and end products of biohydrogenation: Group A, which hydrogenates linoleic and linolenic acids and forms TVA as an end product; and group B, which hydrogenates TVA and forms C18:0 as an end product. The possibility of altering the rumen ecosystem with the FO is further supported by the significant increase in the TVA to C18:0 ratio in the rumen digesta with FO diet compared with the other diets (Table 5). The proportions of other C18:1 FA isomers (trans-6, trans-9, cis-6, and cis-11 C18:1) in milk fat were increased (P < 0.05) with fat supplements compared with the control diet. Except for cis-9 C18:1, there were no differences in the proportions of C18:1 FA isomers between fat supplements. The smaller proportion of cis-9 C18:1 in milk fat from cows fed FO was also reported by Whitlock et al. (2002) and Donovan et al. (2000).
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). Omega-3 fatty acids have many health benefits including the ability to decrease cardiovascular disease (Hirai et al., 1980) and rheumatoid arthritis (Kremer et al., 1987). Milk EPA and DHA concentrations were increased (P < 0.05) with FO supplements compared with the control and ESB diets (Table 4); however, the magnitude of increased concentrations in milk fat was still low compared with the concentration of EPA and DHA in the diet. This low transfer efficiency has been reported previously (Donovan et al., 2000; AbuGhazaleh et al., 2002; Whitlock et al., 2002), and it has been attributed to both their biohydrogenation in the rumen and their association with plasma lipoproteins which are not good substrates for mammary lipoprotein lipase (Mansbridge and Blake, 1997). Another possibility for this low transfer efficiency is that these FA are preferentially partitioned towards other tissues in the body (Ashes et al., 1992).
Fatty Acid Composition of Ruminal Digesta
The other objective of this study was to determine the effect of treatments on ruminal FA profiles, especially TVA and CLA. The rumen is the site of an intense microbial lipid metabolism. Lipolysis of dietary glycolipids, phospholipids, and triglycerides leads to FFA that are hydrogenated by microbes to more saturated end products. The initial step in the biohydrogenation of linoleic acid (the main FA in the diets; Table 2) is an isomerization reaction that converts the cis-12 double bond to trans-11 isomers (CLA formation). Once the CLA is formed by the action of isomerase (group A microorganisms), then biohydrogenation of the cis-9 bond occurs by microbial reductase (group A microorganisms; TVA formation). The extent to which TVA is hydrogenated by group B microorganisms to C18:0 depends on conditions in the rumen (Jenkins 1993). At 3 h after feeding, the extent of biohydrogenation of unsaturated FA was reflected by: 1) accumulation of trans fatty acids in the rumen, especially TVA; 2) the change in the percentages of saturated and unsaturated FA in the rumen digesta compared with dietary FA; and 3) greater concentration of C18:0 in the rumen compared with dietary FA (Tables 2 and 5).
The concentration of TVA in ruminal digesta was increased (P < 0.01) by fat supplements compared with control diet (Table 5); however, there were no significant differences (P = 0.51) between fat supplements. This increase (P < 0.05) in TVA concentration and in TVA to C18:0 ratio is an indication of incomplete biohydrogenation of unsaturated FA with fat supplements. Harfoot et al. (1973) reported that a concentration of linoleic acid exceeding 1.0 mg/ml of culture contents interfered with biohydrogenation of TVA, leading to the accumulation of TVA at the expense of C18:0. Beam et al. (2000) reported the overall rate of biohydrogenation of linoleic acid was 14.3% h-1, but declined by 1.2% h-1 for each percentage unit increase in linoleic acid added to the substrate. Accumulation of linoleic acid, however, cannot be the only cause of incomplete biohydrogenation because the FO diet had the highest TVA to C18:0 ratio, although its dietary linoleic acid concentration was the least. The mechanism(s) of inhibition is(are) not clear but might involve an inhibition of the enzyme that catalyzes the final biohydrogenation step in the rumen possibly by altering group B microorganism populations. The concentration of CLA in ruminal digesta was also increased (P < 0.01) with fat supplements compared with the control diet (Table 5), with the greatest CLA concentration appearing when cows were fed the FO diet. The greater TVA to CLA ratio in the rumen digesta compared with milk indicated that fat supplements increased milk CLA concentration mainly by increasing ruminal production of TVA, which also illustrates the significant role that mammary delta-9 desaturase plays in milk CLA production.
The degree of biohydrogenation of individual FA could not be estimated in this study; however, others (Emanuelson et al., 1991; Wu et al., 1991; Kalscheur et al., 1997; Wachira et al., 2000) have reported different rates of biohydrogenation of C18:3, C18:2, and C18:1 FA. Wachira et al. (2000) reported that biohydrogenation of C18:2 and C18:3 ranged between 80 and 93% when lambs were fed FO and/or whole linseed. Wu et al. (1991) observed a lower biohydrogenation of C18:1, where the level of biohydrogenation varied from 71% when cows were offered a linseed diet to 60% when cows were offered a FO diet. Beam et al. (2000) reported that the factors with greatest influence on rates of biohydrogenation of soybean oil were the amount of added fat and the number of double bonds in FA. Variation in rates was relatively small due to diet, time of day that the inoculum was collected, or degree of esterification of the added fat (Beam et al., 2000).
The higher proportion of C18:0 in the ruminal digesta compared with diet is also an indication of biohydrogenation of unsaturated FA in the rumen (Table 5 and 2). The flow of C18:0 into the duodenum for the different diets was not estimated in this study. However, Christensen et al. (1998) reported that the flow of C18:0 to the duodenum ranged from 1802 to 600% of intake for cows fed a low fat diet plus nicotinic acid and a high fat diet without nicotinic acid. Also a high fat diet decreased the flow of C18:0 to the duodenum as a percentage of intake (1700 vs. 602%) (Christensen et al., 1998).
Eicosapentaenoic acid and DHA concentrations in ruminal digesta were increased (P < 0.01) with FO supplements compared with the control and ESB diets. However, there was a substantial decrease in the concentration of EPA and DHA in the ruminal digesta fatty acids compared with dietary FA, probably caused by biohydrogenation of EPA and DHA. Wachira et al. (2000) reported biohydrogenation values between 72 to 79% for EPA and DHA in diets that contained FO or linseed and FO.
Another objective of the study was to determine whether the different lipid fractions in the rumen responded the same to treatments. Ruminal lipids were fractionated into FA-salts, FFA, and neutral lipids, and only the FA of interest were reported (Table 6). It was not possible to determine the percentages of each fraction or if there were any changes in these percentages because of treatments, as total rumen DM content was not estimated. Emanuelson et al. (1991) reported that less than 10% of the total FA were present as FFA, and approximately 20% of total FA were present as neutral lipid when cows were fed rapeseed or tallow. However, Bateman and Jenkins (1998) reported that FFA represented 25% of the total FA, and neutral lipid represented only 7% of the total FA when cows were fed soybean oil. These differences between studies may be due to supplemental fats that have different rates of lipolysis and biohydrogenation and to time of sampling. The FA-salts had a greater proportion of saturated FA (C16:0, C18:0) and a lesser proportion of unsaturated FA (cis-9 cis-12 C18:2, cis-9 C18:1) compared with other fractions, suggesting that saturated FA react more extensively with cations. The effect of dietary treatments on ruminal TVA and CLA were also reflected in the different ruminal lipid fractions. The higher proportions of cis-9 cis-12 C18:2, C18:3 n3, EPA, and DHA in neutral lipid compared with the FA-salts and FFA is an indication of incomplete lipolysis of these FA 3h after feeding. Emanuelson et al. (1991) reported that the relative amounts of the different fatty acids in the FA-salts fraction were low 2 h after feeding but increased with time, at least up to 6 h after feeding.
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CONCLUSIONS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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FOOTNOTES |
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Received for publication January 25, 2002. Accepted for publication March 26, 2002.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSREFERENCES |
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