Metoyo Et Al, 2005

Effect of dietary fish oil substitution with linseed oil on the performance, tissuefatty acid profile, metabolism, and oxidative stability of Atlantic salmon1,2

D. Menoyo,* C. J. Lopez-Bote,3 A. Obach, and J. M. Bautista*

Departamento de *Bioqumica y Biologia Molecular IV and Produccion Animal,Facultad de Veterinaria, Universidad Complutense de Madrid, 28040 Madrid, Spain; and

Nutreco Aquaculture Research Centre, N-4001 Stavanger, Norway

ABSTRACT: The objective of this experiment was totest the effect of total or partial substitution of dietaryfish oil (FO) by linseed oil (LO) in Atlantic salmon feed-ing on performance, liver andmuscle fatty acid composi-tion, selected lipogenic and lipolytic enzyme activities,and flesh oxidative stability. For 12 wk, fish (220 12g of initial BW) were fed five experimental diets inwhich the FO was serially replaced by 25, 50, 75, and100% LO. Total FO replacement by LO did not (P =0.20) affect fish final weight, biometric indices, or i.m.fat contents. Liver andmuscle neutral lipid (NL) compo-sition responded to dietary treatments in differentways. Whereas the sum of n-3 PUFA inmuscle followeda linear and quadratic pattern with increasing levelsof LO, a linear (P = 0.005) effect was observed in theliver NL fraction. Total n-3 and n-6 PUFA contents in

Key Words: Atlantic Salmon, Fatty Acid, Lipid Metabolism, Vegetable Oil

2005 American Society of Animal Science. All rights reserved. J. Anim. Sci. 2005. 83:28532862

Introduction

Fish oil (FO) is a common fat source in fish dietsbecause of its high proportion of long-chain, n-3 fattyacids, which are nutritionally essential to teleosts(NRC, 1993). Because of predictable insufficient FOavailability for fish feeding, however, alternativesources must be assessed (FAO, 2002). Studies per-formed in Atlantic salmon fed lipid rich diets containinghigh-oleic sunflower oil (Torstensen et al., 2000), rape-seed oil (Bell et al., 2001), palm oil (Bell et al., 2002),soybean oil (Grisdale Helland et al., 2002), and linseedoil (LO; Bell et al., 2003b) were found to have no detri-

1This research was partially financed by Ministerio de Ciencia yTecnologa (CICYT AGL-2001-1162).

2The authors are grateful to R. Prieto for technical assistance.3Correspondencephone: 34-91 394 3889; fax: 34-91-394 3824;

e-mail: [email protected] November 4, 2004.Accepted August 1, 2005.

2853

the polar lipid fraction (PL) were unaffected (P = 0.356)by dietary input of LO in muscle. Activity of liver glu-cose-6-P-dehydrogenase (G6PD) was greater with in-creasing levels of LO (P = 0.004). A time effect (P 66% of vegetable oils.Conflicting reports on the effects of vegetable oils onlipogenic and lipolytic enzymes (Torstensen et al., 2000;Regost et al., 2003; Menoyo et al., 2003) suggest thatdifferent vegetable oils may have different effects onfish metabolism and that different species respond indifferent ways. In fish, the pentose phosphate pathwayis active in the liver, where it provides the cytoplasmicreducing equivalents (NADPH; Alvarez et al., 2000). Inthe same way, fatty acid -oxidation is active in fishlivers, where it is regulated by mitochondrial uptake oflong-chain fatty acids through the activity of carnitinepalmitoyltransferase I (Fryland et al., 1998). There-fore, the objectives of this research were 1) to evaluatethe influence of dietary fat source (FO vs. LO) and com-

Menoyo et al.2854

Table 1. Composition of experimental diets

Linseed oil, % replacement of fish oil

Ingredient, g/kg of DM 0 25 50 75 100

Fish meal-LT (71.8/8.4)a 632.0 632.0 632.0 632.0 632.0Corn gluten 30.1 30.1 30.1 30.1 30.1Wheat 70.0 70.0 70.0 70.0 70.0Fish oil 259.4 194.6 129.7 64.9 Linseed oil 64.9 129.7 194.6 259.4Mineral premixb 5.6 5.6 5.6 5.6 5.6Vitamin premixb 2.2 2.2 2.2 2.2 2.2Carophyll pink 0.6 0.6 0.6 0.6 0.6-Tocopherolc 321.4 323.8 318.9 318.6 350.1-Tocopherolc 9.6 30.3 41.6 50.2 80.2

aLT = low temperature (71.8 CP/8.4 moisture)bActive ingredients supplied per kilogram of feed. Minerals: 48 mg of CuSO4, 2.0 mg of KI, 109.4 mg of

MnSO4, 0.4 mg of Na2SeO3, and 257.1 mg of ZnSO4 (all mineral salts from Sigma, St. Louis, MO). Vitamins:5 mg of retinol acetate, 4.8 mg of vitamin D3, 300 mg of -tocopheryl acetate, 15.3 mg of thiamin-Cl, 26 mgof riboflavin, 15.3 mg of pyridoxine-Cl, 88.9 mg of Ca-pantothenate, 153.1 mg of niacin, 5.2 mg of folic acid,20.0 mg of vitamin B12, 150.0 mg of biotin, 408.2 mg of myo-inositol, 40.0 mg of vitamin K3, and 1 g ofascorbate polyphosphate (all vitamins from Hoffmann-La Roche, Basel, Switzerland).

cAnalyzed concentration, mg/kg of DM.

binations for Atlantic salmon on fatty acid compositionand liver metabolism, and 2) to relate these findings tosusceptibility of flesh to lipid peroxidation.

Materials and Methods

Fish Husbandry and Feeding

The trial was carried out at the Nutreco AquacultureResearch Center Lerang Research Station, Jrpeland,Norway. A total of 110 Atlantic salmon (Salmo salar)AquaGen strain, weighing approximately 220 g, weredistributed randomly into five 1-m 1-m circular tankscontaining 500 L of sea water and were fed one of thefive experimental diets for 12 wk. Fish were fed dailyto satiation, and feed disappearance was monitoredthroughout the trial. Wasted feed was collected fromthe effluent water from each tank by a wiremesh collec-tor and dried. Net feed intake was registered daily. Fishwere subjected to a photoperiod regimen of 18 h lightand 6 hdark, and the temperature over thewhole exper-imental period ranged from 8 to 9C. Experimentaldiets were produced at the Nutreco Technology Center(Stavanger, Norway) as extruded, sinking, 4-mm pel-lets. Basal composition of diets was the same exceptfor the oil added during vacuum fat coating (Table 1).Batches of extruded pellets were produced from a com-monmeal mixture and coated with FO that was seriallyreplaced by 25, 50, 75, or 100% LO. The fatty acidcomposition of the experimental diets is presented inTable 2, and diets were formulated to contain targetedlevels of 37% CP and 36% crude fat (DM basis).

Biological Parameters and Sample Collection

During the final sampling, 11 fish per tank werekilled by a blow to the head and immediately exsangui-nated in chilled seawater; weight and fork length were

recorded. Then, fish were eviscerated, and the weightof viscera and liver was registered to assess the hepato-and viscero-somatic indexes. Livers were then cut intotwo pieces, and one portion was placed in liquid N2 andstored at 80C for enzymatic analyses, whereas theother half was frozen and stored at 0C for fatty acidanalysis. Fishwere filleted, and left filletswere immedi-ately vacuum-packaged and frozen at 20C for fattyacid analysis and lipid peroxidation tests.

Chemical Analyses of Flesh Samples and LipidPeroxidation Assessment

Fatty acids of diets were extracted and quantifiedby the one-step procedure described by Sukhija andPalmquist (1988) in freeze-dried samples with pentade-canoic acid (15:0; Sigma, Alcobendas, Madrid, Spain)as internal standard. Neutral lipids (NL) and polarlipids (PL) from individual fillet and liver samples (fivefish per tank) were extracted using the method ofMarmer and Maxwell (1981). Before the analysis offatty acids by gas chromatography, all lipid sampleswere methylated as described by Lopez-Bote et al.(1997). Fatty acid methyl esters were then analyzedusing gas chromatography (Model HP-6890; HewlettPackard Co., Avondale, PA) equippedwith flame ioniza-tion detection and a 30-m 0.32-mm 0.25-mm cross-linked polyethylene glycol capillary column (Hewlett-Packard-Innowax). Results were expressed as the per-centage of each fatty acid with respect to the totalfatty acids.Lipid peroxidation products were determined as thio-

barbituric acid reactive substances (TBARS) in fishflesh according to the procedure of Menoyo et al. (2002),and TBARS were expressed as mol of malonaldehyde(MDA)/kg of wet tissue. Vitamin E isoforms were ex-tracted and quantified in feed and muscle as describedby Rey et al. (2001).

Linseed oil in salmon feeding 2855

Table 2. Fatty acid composition (%) of experimental diets


Fatty acid 0 25 50 75 100

Myristic acid (14:0) 6.9 4.9 3.8 2.7 1.1Palmitic acid (16:0) 19.8 15.6 13.6 11.6 8.7Stearic acid (18:0) 4.0 3.7 3.8 3.7 3.7Total SFA 31.7 24.9 21.7 18.4 13.5Palmitoleic acid (16:1n-7) 7.6 5.4 4.3 3.1 1.3Oleic acid (18:1n-9) 10.5 15.2 14.2 15.5 17.5Vaccenic acid (18:1n-7) 3.1 2.7 2.2 1.9 1.4Cetoleic acid (22:1n-11) 2.6 2.3 2.1 2.1 1.7Total MUFA 27.5 28.8 25.6 25.2 23.9Linoleic acid (18:2n-6) 3.6 6.9 8.5 10.1 12.7Arachidonic acid (20:4n-6) 0.9 0.7 0.5 0.4 0.2Total n-6 fatty acids 4.9 7.8 9.2 10.6 13.0Linolenic acid (18:3n-3) 1.2 13.1 23.0 30.1 41.6Stearidonic acid (18:4n-3) 2.9 2.1 1.6 1.2 0.5Eicosatrienoic acid (20:3n-3) 0.1 0.1 0.1 0.1 0.1Eicosatetraenoic acid (20:4n-3) 0.9 0.6 0.5 0.3 0.2Eicosapentaenoic acid (20:5n-3) 13.6 9.7 7.7 5.7 2.6Docosapentaenoic acid (22:5n-3) 1.6 1.2 0.9 0.7 0.3Docosahexaenoic acid (22:6n-3) 15.3 11.5 9.5 7.5 4.3Total n-3 fatty acids 35.7 38.4 43.4 45.6 49.5Total n-9 fatty acids 14.4 18.6 17.2 18.3 19.6n-3:n-6 ratio 7.3 4.9 4.7 4.3 3.8n-3 HUFAa 31.5 23.1 18.7 14.3 7.4UIb 2.27 2.20 2.24 2.21 2.18

aHighly unsaturated fatty acids (HUFA) include 20:3, 20:4, 20:5, 22:5, and 22:6.bUI = unsaturation index (average number of double bonds per fatty acid residue).

Mitochondrial Preparations, Soluble Extracts,and Enzyme Analyses

Mitochondrial extracts from liver were prepared asdescribed by Menoyo et al. (2004), and the activity ofcarnitine palmitoyltransferase I (CPT I) was assayedaccording to procedures of Sanz et al. (2000). Liver ho-mogenates and the activity of glucose-6-phosphate de-hydrogenase (G6PD) were assayed as described byBautista et al. (1988). All enzyme activity assays wereperformed in duplicate or triplicate at 30C. Enzymaticactivity units (IU), defined as moles of substrate con-verted to product per minute at the assay temperature,were expressed per milligram of hepatic soluble protein(specific activity). Soluble protein content of liver ho-mogenates 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 theCPT I determination was supplied by Amersham Phar-macia Biotech (Barcelona, Spain), whereas Sigma sup-plied the remaining reagents.

Statistical Analyses

Data were analyzed as a completely randomized de-sign by the GLM procedure of SAS (SAS Inst., Inc.,Cary, NC), with LO inclusion level as the lone fixedeffect, and individual fish as the experimental unit. TheTukeys 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 comparedifferences in TBARS concentrations between groupsduring stimulated lipid peroxidation (Morris, 1999).

Results and Discussion

Growth performance and dorsal muscle compositionare presented in Table 3. No (P 0.20) significant effectof dietary treatment was observed for final weight, con-dition factor, or viscero- and hepato-somatic indexes.This is in accordance with previous reports showingthat feeding Atlantic salmon current commercial dietswith 45 to 50% CP (provided mainly as fish meal) vege-table oils can replace portions of the FO without nega-tive effects on growth and biometric indexes (Tors-tensen et al., 2000; Grisdale Helland et al., 2002; Bell etal., 2003b). Although some concern exists that feedingdiets with vegetable oil may affect fish health (Bell etal., 1991; Thompson et al., 1996), no mortalities wererecorded in the current study. Neutral (mainly triglyc-erides) and polar (mainly phospholipids) i.m. lipids didnot (P > 0.07) differ among experimental groups. Tri-glycerides are the predominant lipid class in salmonmuscle (Bell et al., 2003a). Results of this study suggestthat LO does not promote changes in flesh adipositycompared with FO, thereby differing from results ob-served in fish of the same size with palm oil and rape-seed oil (Bell et al., 2001, 2002). Vegetable oils affectAtlantic salmon muscle fat content in different ways,with palm oil and 50% rapeseed oil decreasing muscle

Menoyo et al.2856

Table 3. Effect of dietary fish and linseed oil combinations on weight, biometry measure-ments, and muscle and liver neutral lipids (NL) and polar lipids (PL)


Item 0 25 50 75 100 Pooled SEa P < F

Weight, g 525.86 543.00 526.81 537.71 556.07 13.54 0.396Length, cm 33.28 33.66 33.19 33.60 33.52 0.27 0.376Condition factor, % 1.43 1.42 1.44 1.42 1.47 0.02 0.205VSI, %b 11.49 11.47 11.31 10.96 11.31 0.17 0.488HSI, %c 1.50 1.42 1.48 1.45 1.45 0.03 0.723Muscle NL, % 5.87 7.34 6.24 5.61 7.08 0.43 0.071Muscle PL, % 1.25 1.19 0.92 0.90 0.95 0.15 0.300Liver NL, % 3.07x 3.53xyz 3.44xy 5.48z 5.31yz 0.47 0.003Liver PL, % 1.26 1.38 1.46 1.31 1.31 0.06 0.149

an = 11 for weight, length, condition factor, VSI, and HSI; n = 5 for muscle NL, muscle PL, liver NL, andliver PL.

bViscero-somatic index (VSI) = carcass weight BW1 100.cHepato-somatic index (HSI) = liver weight BW1 100.x,y,zMeans within a row with different superscripts differ, P < 0.05.

adiposity (Bell et al., 2001, 2002), whereas LO had noeffect on muscle adiposity. It is interesting to note thatintrahepaticNL concentrationswere greater (P < 0.003)in groups receiving either 75 or 100% LO than in thosereceiving 100% FO. This adiposity effect of vegetableoil in salmon liver also was observed when feeding ablend of LO and rapeseed oil (Tocher et al., 2001) orwhen rapeseed replaced >50% of FO (Bell et al., 2001);however, the same effect was not observed with palmoil (Bell et al., 2002).Liver G6PD and CPT I activities are shown in Figure

1. The activity of G6PD, which is the main donor ofreducing power in the form of NADPH, increased (P =0.004) with increasing levels of LO, showing a specificactivity of 0.09 IU/mg of soluble protein in the liver offish fed 0% LO and reaching the maximum activity of0.15 IU/mg of soluble protein in fish fed diets with 100%LO. It has been well documented that the increasingelongation activity in Atlantic salmon is triggered byLO (Bell et al., 1993; Tocher et al., 2000). According tothis, we observed the accumulation of eicosatetraenoicacid (20:4 n-3), which is the main product from the 6desaturation of linolenic acid (18:3 n-3) in the liverNL and PL fractions (Tables 4 and 5), with increasinginputs of LO. Thus, the increase in G6PD activity maybe related to the greater concentration of intracellularNADPH needed to accomplish the elongation process.The carnitine shuttle, mediated by CPT I, is needed forlong-chain fatty acids to cross the inner mitochondrialmembrane and is tightly controlled by its inhibition ofelevated 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 agreater elongation process; however, we were unableto detect differences on CPT I activity in the liver (Fig-ure 1).It is generally accepted that dietary fatty acid profile

is closely reflected in fatty acid composition of fish tis-sues (Rosenlund et al., 2001a; Bell et al., 2002; Cabal-lero et al., 2002). Linseed oil (Table 2) provided a lower

concentration of total SFA, and a higher concentrationof total n-6 fatty acids and total n-3 fatty acids thanFO. As expected, n-3 fatty acids provided by LO wereof shorter chain length (41.6% 18:3 n-3) and had lessunsaturation than n-3 fatty acids provided by FO(13.6% eicosapentaenoic acid [20:5 n-3] and 15.3% doco-sahexaenoic acid [22:6 n-3]). It is interesting to note,

Figure 1. Effect of increasing linseed oil (% replacementof fish oil) in the feed of Atlantic salmon on liver glucose-6-phosphate dehydrogenase (G6PD) and carnitine palmi-toyltransferase I (CPT I) activities. Bars that do not havea common letter differ, P = 0.004.


Table 4. Effect of dietary fish and linseed oil combinations on selected fatty acids (g/100g of total fatty acids) of neutral hepatic lipids


Item 0 25 50 75 100 Pooled SE P < F

No. of fish 5 5 5 5 5Myristic acid (14:0) 1.84z 1.64z 1.30z 1.32z 0.66y 0.14

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Table 5. Effect of dietary fish and linseed oil combinations on selected fatty acids (g/100g total fatty acids) of polar hepatic lipids



No. of fish 5 5 5 5 5Myristic acid (14:0) 2.12z 1.54y 1.41y 1.17x 0.67w 0.06


Table 6. Effect of dietary fish and linseed oil combinations on selected fatty acids (g/100g of total fatty acids) of neutral intramuscular lipids



No. of fish 5 5 5 5 5Myristic acid (14:0) 5.43z 4.03y 3.40x 2.71w 1.48v 0.08

Menoyo et al.2860

Table 8. Effects of different levels of dietary linseed oil (LO; % of total added fat) on fattyacid classes (g/100 g of total fatty acids) in muscle and liver neutral lipids (NL) and polarlipids (PL)a

P-value

Fatty acid Intercept LO LO2 R2 Pooled SE Linear Quadratic

Muscle NLSaturated y = 27.08 0.09 0.96 0.31


concentration was almost five times greater in muscleof fish fed 100% compared with 0% LO (Figure 3). -Tocopherol has a greater antioxidant effect than othervitamin E isoforms in Atlantic salmon tissue (Parazoet al., 1998) and pork (Rey et al., 1998). Although -tocopherol seems to be more active than -tocopherolbecause of its tissue localization and mobilization (Par-azo et al., 1998; Bell et al., 2000), additional researchis warranted to assess their potential as ante- and post-mortem antioxidants in fish muscle.

Implications

Dietary linseed oil can totally replace fish oil in high-energy diets for Atlantic salmon weighing approxi-mately 520 g without affecting fish performance andfillet peroxidative stability.Nonetheless, fatty acid com-position in muscle and liver was changed, leading to adecrease in the concentration of n-3 highly unsaturatedfatty acids in fish flesh when diets with greater linseedoil contents were fed.

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Metoyo Et Al, 2005