J. Anim. Sci. 2005. 83:2853-2862
© 2005 American Society of Animal Science
Effect of dietary fish oil substitution with linseed oil on the performance, tissue fatty acid profile, metabolism, and oxidative stability of Atlantic salmon1,2
D. Menoyo*,
,
C. J. López-Bote,3,
A. Obach
and
J. M. Bautista*
* Departamento de Bioquímica y Biologia Molécular IV and
and
Producción Animal, Facultad de Veterinaria, Universidad Complutense de Madrid, 28040 Madrid, Spain; and
and
Nutreco Aquaculture Research Centre, N-4001 Stavanger, Norway
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Abstract
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The objective of this experiment was to test the effect of total or partial substitution of dietary fish oil (FO) by linseed oil (LO) in Atlantic salmon feeding on performance, liver and muscle fatty acid composition, selected lipogenic and lipolytic enzyme activities, and flesh oxidative stability. For 12 wk, fish (220 ± 12 g of initial BW) were fed five experimental diets in which the FO was serially replaced by 25, 50, 75, and 100% LO. Total FO replacement by LO did not (P = 0.20) affect fish final weight, biometric indices, or i.m. fat contents. Liver and muscle neutral lipid (NL) composition responded to dietary treatments in different ways. Whereas the sum of n-3 PUFA in muscle followed a linear and quadratic pattern with increasing levels of LO, a linear (P = 0.005) effect was observed in the liver NL fraction. Total n-3 and n-6 PUFA contents in the polar lipid fraction (PL) were unaffected (P = 0.356) by dietary input of LO in muscle. Activity of liver glucose-6-P-dehydrogenase (G6PD) was greater with increasing levels of LO (P = 0.004). A time effect (P < 0.001) was observed in the concentration of lipid peroxidation products, expressed as thiobarbituric acid reactive substances, in fish flesh stored under refrigeration for 9 d; however, the progressive inclusion of LO in the feed did not affect (P = 0.125) flesh oxidation stability. In summary, LO can totally replace FO in Atlantic salmon feed without affecting growth performance and muscle susceptibility to lipid oxidation. Fatty acid metabolism in the liver was affected by LO, promoting G6PD activity and eicosatetraenoic acid accumulation; however, a 100% LO replacement decreased (P < 0.001) concentrations of eicosapentaenoic and docosahexaenoic acids in salmon muscle.
Key Words: Atlantic Salmon • Fatty Acid • Lipid Metabolism • Vegetable Oil
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Introduction
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Fish oil (FO) is a common fat source in fish diets because of its high proportion of long-chain, n-3 fatty acids, which are nutritionally essential to teleosts (NRC, 1993
). Because of predictable insufficient FO availability for fish feeding, however, alternative sources must be assessed (FAO, 2002). Studies performed in Atlantic salmon fed lipid rich diets containing high-oleic sunflower oil (Torstensen et al., 2000), rapeseed oil (Bell et al., 2001), palm oil (Bell et al., 2002), soybean oil (Grisdale Helland et al., 2002), and linseed oil (LO; Bell et al., 2003b) were found to have no detrimental effects on growth. Nonetheless, use of vegetable oil sources in fish feeding still needs to be evaluated in terms of flesh quality and metabolic use, especially whether the fish has the ability to elongate linoleic acid (18:3 n-3) to long-chain, n-3 fatty acids. Bell et al. (2003b) reported a significant loss of n-3 highly unsaturated fatty acids (HUFA) in the flesh of Atlantic salmon when FO was replaced with > 66% of vegetable oils. Conflicting reports on the effects of vegetable oils on lipogenic and lipolytic enzymes (Torstensen et al., 2000; Regost et al., 2003; Menoyo et al., 2003) suggest that different vegetable oils may have different effects on fish metabolism and that different species respond in different ways. In fish, the pentose phosphate pathway is active in the liver, where it provides the cytoplasmic reducing equivalents (NADPH; Alvarez et al., 2000). In the same way, fatty acid ß-oxidation is active in fish livers, where it is regulated by mitochondrial uptake of long-chain fatty acids through the activity of carnitine palmitoyltransferase I (Frøyland et al., 1998). Therefore, the objectives of this research were 1) to evaluate the influence of dietary fat source (FO vs. LO) and combinations for Atlantic salmon on fatty acid composition and liver metabolism, and 2) to relate these findings to susceptibility of flesh to lipid peroxidation.
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Materials and Methods
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Fish Husbandry and Feeding
The trial was carried out at the Nutreco Aquaculture Research Center Lerang Research Station, Jørpeland, Norway. A total of 110 Atlantic salmon (Salmo salar) AquaGen strain, weighing approximately 220 g, were distributed randomly into five 1-m x 1-m circular tanks containing 500 L of sea water and were fed one of the five experimental diets for 12 wk. Fish were fed daily to satiation, and feed disappearance was monitored throughout the trial. Wasted feed was collected from the effluent water from each tank by a wire mesh collector and dried. Net feed intake was registered daily. Fish were subjected to a photoperiod regimen of 18 h light and 6 h dark, and the temperature over the whole experimental period ranged from 8 to 9°C. Experimental diets were produced at the Nutreco Technology Center (Stavanger, Norway) as extruded, sinking, 4-mm pellets. Basal composition of diets was the same except for the oil added during vacuum fat coating (Table 1). Batches of extruded pellets were produced from a common meal mixture and coated with FO that was serially replaced by 25, 50, 75, or 100% LO. The fatty acid composition of the experimental diets is presented in Table 2, and diets were formulated to contain targeted levels of 37% CP and 36% crude fat (DM basis).
Biological Parameters and Sample Collection
During the final sampling, 11 fish per tank were killed by a blow to the head and immediately exsanguinated in chilled seawater; weight and fork length were recorded. Then, fish were eviscerated, and the weight of viscera and liver was registered to assess the hepato-and viscerosomatic indexes. Livers were then cut into two pieces, and one portion was placed in liquid N2 and stored at –80°C for enzymatic analyses, whereas the other half was frozen and stored at –0°C for fatty acid analysis. Fish were filleted, and left fillets were immediately vacuum-packaged and frozen at –20°C for fatty acid analysis and lipid peroxidation tests.
Chemical Analyses of Flesh Samples and Lipid Peroxidation Assessment
Fatty acids of diets were extracted and quantified by the one-step procedure described by Sukhija and Palmquist (1988) in freeze-dried samples with pentadecanoic acid (15:0; Sigma, Alcobendas, Madrid, Spain) as internal standard. Neutral lipids (NL) and polar lipids (PL) from individual fillet and liver samples (five fish per tank) were extracted using the method of Marmer and Maxwell (1981). Before the analysis of fatty acids by gas chromatography, all lipid samples were methylated as described by López-Bote et al. (1997). Fatty acid methyl esters were then analyzed using gas chromatography (Model HP-6890; Hewlett Packard Co., Avondale, PA) equipped with flame ionization detection and a 30-m x 0.32-mm x 0.25-mm cross-linked polyethylene glycol capillary column (Hewlett-Packard-Innowax). Results were expressed as the percentage of each fatty acid with respect to the total fatty acids.
Lipid peroxidation products were determined as thiobarbituric acid reactive substances (TBARS) in fish flesh according to the procedure of Menoyo et al. (2002), and TBARS were expressed as µmol of malonaldehyde (MDA)/kg of wet tissue. Vitamin E isoforms were extracted and quantified in feed and muscle as described by Rey et al. (2001).
Mitochondrial Preparations, Soluble Extracts, and Enzyme Analyses
Mitochondrial extracts from liver were prepared as described by Menoyo et al. (2004), and the activity of carnitine palmitoyltransferase I (CPT I) was assayed according to procedures of Sanz et al. (2000). Liver homogenates and the activity of glucose-6-phosphate dehydrogenase (G6PD) were assayed as described by Bautista et al. (1988). All enzyme activity assays were performed in duplicate or triplicate at 30°C. Enzymatic activity units (IU), defined as µmoles of substrate converted to product per minute at the assay temperature, were expressed per milligram of hepatic soluble protein (specific activity). Soluble protein content of liver homogenates was determined by the method of Bradford (1976), using BSA as the standard. The L – [methyl-3H] carnitine hydrochloride (82.0 Ci/mmol) used in the CPT I determination was supplied by Amersham Pharmacia Biotech (Barcelona, Spain), whereas Sigma supplied the remaining reagents.
Statistical Analyses
Data were analyzed as a completely randomized design by the GLM procedure of SAS (SAS Inst., Inc., Cary, NC), with LO inclusion level as the lone fixed effect, and individual fish as the experimental unit. The Tukey’s test was used to separate treatment means, and regression analysis was used to measure the linear (L) or quadratic (Q) response to LO inclusion level. A repeated measure mean test was used to compare differences in TBARS concentrations between groups during stimulated lipid peroxidation (Morris, 1999).
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Results and Discussion
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Growth performance and dorsal muscle composition are presented in Table 3. No (P 
0.20) significant effect of dietary treatment was observed for final weight, condition factor, or viscero- and hepatosomatic indexes. This is in accordance with previous reports showing that feeding Atlantic salmon current commercial diets with 45 to 50% CP (provided mainly as fish meal) vegetable oils can replace portions of the FO without negative effects on growth and biometric indexes (Torstensen et al., 2000; Grisdale Helland et al., 2002; Bell et al., 2003b). Although some concern exists that feeding diets with vegetable oil may affect fish health (Bell et al., 1991; Thompson et al., 1996), no mortalities were recorded in the current study. Neutral (mainly triglycerides) and polar (mainly phospholipids) i.m. lipids did not (P > 0.07) differ among experimental groups. Triglycerides are the predominant lipid class in salmon muscle (Bell et al., 2003a). Results of this study suggest that LO does not promote changes in flesh adiposity compared with FO, thereby differing from results observed in fish of the same size with palm oil and rape-seed oil (Bell et al., 2001, 2002). Vegetable oils affect Atlantic salmon muscle fat content in different ways, with palm oil and 
50% rapeseed oil decreasing muscle adiposity (Bell et al., 2001, 2002), whereas LO had no effect on muscle adiposity. It is interesting to note that intrahepatic NL concentrations were greater (P < 0.003) in groups receiving either 75 or 100% LO than in those receiving 100% FO. This adiposity effect of vegetable oil in salmon liver also was observed when feeding a blend of LO and rapeseed oil (Tocher et al., 2001) or when rapeseed replaced > 50% of FO (Bell et al., 2001); however, the same effect was not observed with palm oil (Bell et al., 2002).
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Table 3. Effect of dietary fish and linseed oil combinations on weight, biometry measurements, and muscle and liver neutral lipids (NL) and polar lipids (PL)
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Liver G6PD and CPT I activities are shown in Figure 1. The activity of G6PD, which is the main donor of reducing power in the form of NADPH, increased (P = 0.004) with increasing levels of LO, showing a specific activity of 0.09 IU/mg of soluble protein in the liver of fish fed 0% LO and reaching the maximum activity of 0.15 IU/mg of soluble protein in fish fed diets with 100% LO. It has been well documented that the increasing elongation activity in Atlantic salmon is triggered by LO (Bell et al., 1993; Tocher et al., 2000). According to this, we observed the accumulation of eicosatetraenoic acid (20:4 n-3), which is the main product from the 
6 desaturation of linolenic acid (18:3 n-3) in the liver NL and PL fractions (Tables 4 and 5), with increasing inputs of LO. Thus, the increase in G6PD activity may be related to the greater concentration of intracellular NADPH needed to accomplish the elongation process. The carnitine shuttle, mediated by CPT I, is needed for long-chain fatty acids to cross the inner mitochondrial membrane and is tightly controlled by its inhibition of elevated levels of cellular malonyl-CoA (Zammit, 1999), the two-carbon donor needed for the elongation process. It is plausible, therefore, to relate fatty livers to a greater elongation process; however, we were unable to detect differences on CPT I activity in the liver (Figure 1).
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Figure 1. Effect of increasing linseed oil (% replacement of fish oil) in the feed of Atlantic salmon on liver glucose-6-phosphate dehydrogenase (G6PD) and carnitine palmitoyltransferase I (CPT I) activities. Bars that do not have a common letter differ, P = 0.004.
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Table 4. Effect of dietary fish and linseed oil combinations on selected fatty acids (g/100 g of total fatty acids) of neutral hepatic lipids
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Table 5. Effect of dietary fish and linseed oil combinations on selected fatty acids (g/100 g total fatty acids) of polar hepatic lipids
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It is generally accepted that dietary fatty acid profile is closely reflected in fatty acid composition of fish tissues (Rosenlund et al., 2001a; Bell et al., 2002; Caballero et al., 2002). Linseed oil (Table 2
) provided a lower concentration of total SFA, and a higher concentration of total n-6 fatty acids and total n-3 fatty acids than FO. As expected, n-3 fatty acids provided by LO were of shorter chain length (41.6% 18:3 n-3) and had less unsaturation than n-3 fatty acids provided by FO (13.6% eicosapentaenoic acid [20:5 n-3] and 15.3% docosahexaenoic acid [22:6 n-3]). It is interesting to note, however, that concentrations of myristic (14:0) and palmitic (16:0) acids were considerably greater in FO than in LO (6.9 and 19.8% vs. 1.1 and 8.7%, respectively), thereby leading to a general overall unsaturation (as assessed by the unsaturation index) and average fatty acid chain length similar between fat sources (2.27 vs. 2.18 and 18.3 vs. 18.1 for FO and LO, respectively). Diets with combinations of LO and FO showed intermediate values, and, interestingly, the unsaturation index decreased (P < 0.05) in the i.m. NL fraction when LO replaced FO (Table 4).
Hepatic and i.m. NL and PL fatty acid compositions are shown in Tables 4, 5, 6, and 7, respectively. The amount of MUFA was greater (P < 0.05) in the i.m. NL fraction than in the diet in response to the accumulation of oleic acid (18:1n-9). Selection of a given fatty acid to provide energy will depend on availability related to the amount and interactions with other dietary fatty acids (Bell et al., 2002). In general terms, when provided in excess, MUFA and 16:0 seem to be readily used for ß-oxidation in salmonids muscles. Similarly, linoleic acid (18:2 n-6), 18:3 n-3, and 20:5 n-3 are well oxidized when high amounts are included in the diet, which may be caused by a surplus of essential fatty acids (Kiessling and Keissling, 1993; Mckenzie et al., 1998; Bell et al., 2003b). Although oxidation could explain the relative high accumulation of 18:1n-9 in muscle samples in the current study, other metabolic regulation processes, such as changes in 9 desaturase activity, also might be involved; however, accumulation of 18:1n-9 was different in the NL fraction of liver and muscle (Tables 4 and 5). Whereas it followed a linear (R2 = 0.91; P < 0.001) pattern in muscle, a linear (R2 = 0.73; P < 0.001) and quadratic effect (R2 = 0.73; P < 0.01) was observed in the liver, where 18:1n-9 accumulation took place when LO was included at 75 and 100% (Table 4). Liver NL fatty acid composition reflected the effects of LO on the elongation and desaturation processes (Bell et al., 1993). The accumulation of 20:4n-3, the product of 6 desaturase, and the reduction of 20:4n-6 production are probably indications of competitiveness of substrates for the 5 desaturase (Bell et al., 1993). Thus, feeding diets containing 75 or 100% LO notably increased the accumulation of desaturated and elongated products from 18:3n3 in the liver (Tables 4 and 5), in particular the linear (R2 = 0.85; P < 0.001) and quadratic (R2 = 0.85; P < 0.001) effect of dietary LO inclusion level on 20:4n-3 accumulation in the liver.
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Table 6. Effect of dietary fish and linseed oil combinations on selected fatty acids (g/100 g of total fatty acids) of neutral intramuscular lipids
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Table 7. Effects of dietary fish and linseed oil combinations on selected fatty acids (g/100 g of total fatty acids) of polar i.m. lipids
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Results presented in Tables 4 and 6 clearly indicated that the proportion of 20:5n-3 and 22:6n-3 in salmon liver and muscle triglycerides decreased accordingly with the replacement of FO by LO. The proportion of 20:5n-3 decreased following a linear (R2 = 0.99; P < 0.001) and quadratic (R2 = 0.99; P < 0.001) pattern in the muscle, whereas it followed a linear (R2 = 0.88; P < 0.001) decrease in the liver (Tables 4 and 6). Conversely, 22:6n-3 decreased linearly (R2 = 0.98; P < 0.001) in the muscle NL fraction (Table 6) and followed a linear (R2 = 0.74; P < 0.001) and a quadratic (R2 = 0.74; P < 0.01) trend in the liver at the higher FO substitution levels (Table 4). Regardless of the amount of 22:6n-3 provided in the diet, this fatty acid was selectively deposited in both tissues (Tables 4 and 6), and, according to Bell et al. (2003b), this could be a consequence of the catabolic complexity necessary to yield energy and a consequence of the paramount role of 22:6n-3 as a cell membrane component (Tables 5 and 7).
Increasing levels of LO in the diet promoted a different pattern of individual fatty acid accumulation in liver and muscle PL and NL fractions (Table 8). Although total MUFA accumulated in the liver NL following a linear (R2 = 0.59; P < 0.001) and quadratic (R2 = 0.59; P < 0.03) fashion, there was a linear (R2 = 0.70; P < 0.001) decrease in muscle NL. Conversely, increasing substitution levels of dietary LO followed a different pattern, with n-3 fatty acids increasing linearly (R2 = 0.88; P < 0.001) and quadratically (R2 = 0.88; P < 0.01) in muscle NL as dietary LO increased; however, there was a linear (R2 = 0.29; P < 0.005) decrease in n-3 concentrations in liver NL (Table 8). The proportion of SFA tended to be diminished in the NL fraction of both tissues, decreasing linearly in the muscle (R2 = 0.96; P < 0.0001) and in a linear (R2 = 0.85; P < 0.001) and quadratic (R2 = 0.85; P < 0.007) fashion in the liver (Table 8). The fish tends to maximize the accumulation of n-3 HUFA in the PL fraction of both tissues; however, with the FO replacement, there was a progressive loss of n-3 HUFA in both tissues that was more marked in the liver than in the muscle at the high levels of LO inclusion.
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Table 8. Effects of different levels of dietary linseed oil (LO; % of total added fat) on fatty acid classes (g/100 g of total fatty acids) in muscle and liver neutral lipids (NL) and polar lipids (PL)a
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Previous studies performed with Atlantic salmon have shown a lack of an effect of vegetable oils on fillet quality measurements (Rosenlund et al., 2001b; Rørå et al., 2003) and organoleptic attributes (Obach et al., 2001). One of the most important quality attributes in fish is its nutritional value as a source of PUFA (Boggio et al., 1985). Salmon rich in PUFA is, however, more susceptible to lipid oxidation, yielding undesirable lipid oxidation products that negatively affect quality characteristics. Although it is well known that unsaturated fatty acids of the PL fraction are the main reason for fish flesh peroxidation during storage (Monahan, 2000), the susceptibility of flesh to oxidation also depends on the balance of pro- and antioxidants (López-Bote, 2000). The effects of experimental diets on TBARS concentration in fish flesh stored under refrigeration for 9 d and on the muscular contents of 
- and 
-tocopherols are shown in Figures 2 and 3, respectively. A time effect (P < 0.001) on TBARS formation was observed during storage (Figure 2); however, no dietary effect was observed on TBARS concentration (P = 0.125). When feeding rainbow trout diets containing either herring oil or lard (approximately 10% DM), Boggio et al. (1985) failed to detect differences in TBARS concentration in frozen stored fillets, although higher TBARS were detected in the fillet of fish fed lower amounts of -tocopheryl acetate ( 50 mg/kg of diet). Conversely, Olsen et al. (1999) reported increasing TBARS values in response to increasing dietary PUFA levels in Arctic charr, which indicated that supplying -tocopherol above requirements does not improve oxidative stability. Our laboratory previously reported higher TBARS values in the flesh of Atlantic salmon fed a diet containing a rich n-3 HUFA FO than when feeding diets formulated with FO that was less rich in n-3 fatty acids (Menoyo et al., 2002). When Atlantic salmon were marketed at approximately 5 kg, Menoyo et al. (2002) demonstrated that inclusion of lower levels of -tocopheryl acetate in the diet (170 mg/kg of feed, on average) was not sufficient to palliate peroxidation effects between treatments. Overall unsaturation and total n-3 HUFA concentrations were greater in i.m. lipids in fish receiving a diet containing FO than in those receiving LO; therefore, a higher oxidation would be expected.
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Figure 2. Effect of dietary linseed oil inclusion level (0, 25, 50, 75, and 100% replacement of fish oil) on thiobarbituric acid reactive substances (TBARS; µmol of malondialdehyde [MDA]/kg of wet tissue) concentration along fish flesh stored under refrigeration for 9 d (P < 0.001 for time effect).
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In the present experiment, dietary oils provided not only a different source of fatty acids but also a different supply of natural antioxidants (Table 1), which might affect susceptibility of tissues to lipid peroxidation (Jensen et al., 1998; Mortensen and Skibsted, 2000). Both - and -tocopherol were greater (P < 0.02) in muscle of fish fed the 100% LO diet, and muscle -tocopherol concentration was almost five times greater in muscle of fish fed 100% compared with 0% LO (Figure 3). -Tocopherol has a greater antioxidant effect than other vitamin E isoforms in Atlantic salmon tissue (Parazo et al., 1998) and pork (Rey et al., 1998). Although -tocopherol seems to be more active than -tocopherol because of its tissue localization and mobilization (Parazo et al., 1998; Bell et al., 2000), additional research is warranted to assess their potential as ante- and postmortem antioxidants in fish muscle.
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Implications
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Dietary linseed oil can totally replace fish oil in high-energy diets for Atlantic salmon weighing approximately 520 g without affecting fish performance and fillet peroxidative stability. Nonetheless, fatty acid composition in muscle and liver was changed, leading to a decrease in the concentration of n-3 highly unsaturated fatty acids in fish flesh when diets with greater linseed oil contents were fed.
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Footnotes
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1 This research was partially financed by Ministerio de Ciencia y Tecnología (CICYT AGL-2001-1162). 
2 The authors are grateful to R. Prieto for technical assistance.
3 Correspondence—phone: 34-91 394 3889; fax: 34-91-394 3824; e-mail: clemente{at}vet.ucm.es.
Received for publication November 4, 2004.
Accepted for publication August 1, 2005.
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Abstract
Introduction
