ContentslistsavailableatScienceDirect
Applied Food Research
journalhomepage:www.elsevier.com/locate/afres
Nutritional value and storage stability in commercially produced
organically and conventionally farmed Atlantic salmon ( Salmo salar L.) in Norway
Margrethe Esaiassen
a,∗, Tonje K. Jensen
a, Guro K. Edvinsen
a, Carina H.A. Otnæs
a, Tatiana N. Ageeva
b, Hanne K. Mæhre
aaUiT The Arctic University of Norway, Norwegian College of Fishery Science, N-9037 Tromsø, Norway
bNOFIMA AS, Division Seafood, N-9291 Tromsø, Norway
a r t i c le i n f o
Keywords:
Atlantic salmon farmed organic
biochemical composition colour stability lipid oxidation
a b s t r a ct
Salmonfeedshavechangedovertheyears,leadingtochangedbiochemicalcompositionofthefish.Themainaim ofthisstudywastocomparebiochemicalcompositionsandstoragestabilityofcommerciallyproducedorganic andconventionalsalmon.Organically(n=40)andconventionallyfarmedsalmon(n=39)weresampled.The fishwereanesthetized,killedbygillcuttingandbledbeforefilleting.Fishsamplesweresubjectedtoproximate analysis,fattyacidandaminoacidcomposition,alongwithcolourandTBARSanalyses.Thelipidcontentof organicallyandconventionallyfarmedsalmonwas13%and17%,respectively.Organicfishcontainedapprox- imately48%moreEPAandDHAthandidtheconventionalfish,17.2gkg−1vs.11.6gkg−1,respectively.The organicsalmonhadlowercoloursaturationthantheconventional,andTBARSwerehigherintheorganicthanin theconventionalsalmon.Toconclude,themaindifferencesbetweenfreshorganicandconventionalsalmonwere relatedtolipidcontentandfattyacidcomposition.Thehighenergylevelinbothgroupsshouldbeconsidered whenmakingdietaryrecommendations.Organicsalmonislessstableduetoitshighcontentoflong-chained unsaturatedfattyacids,andappearssimilartoconventionallyfarmedsalmonsomeyearsago.
1. Introduction
Seafood consumption has long been associated with a healthy lifestyleandreducedriskofseverallifestyle-relateddiseases,suchas cardiovasculardiseases(CVD).Thehealth benefitshavemainlybeen creditedtothehighamountsofthelong-chainedomega-3fattyacids, eicosapentaenoicacid(EPA)anddocosahexaenoicacid(DHA).Fishand seafoodarealsorichingoodqualityproteins,alongwithmicronutri- entssuchasiodine,selenium,vitaminsDandB12(Weichselbaumetal., 2013).However,inrecentyearsithasbeenquestionedwhethertoday’s farmedfisharestillashealth-promoting,duetoincreaseduseofveg- etablefeedcomponents.
Traditionally,aquaculturefeedscontainedmainlymarineingredi- ents,suchasfishmealandfishoilsfromsmallfishspeciesnotsuitedfor humanconsumption.Untilaround1990,aquaculturewasamarginalin- dustryinEurope,contributingtoapproximately7%ofthetotalfishpro- duction.Today,theaquaculturesharehasgrownto18%(FAO,2018), andthetraditionalfeedingredientshavebecomescarce.
Duringtheseyears,aquaculturehasalsobecomeanimportantin- dustryinNorway,withaproductionof1.35milliontonnesin2018and
∗Correspondingauthor:
E-mailaddress:margrethe.esaiassen@uit.no(M.Esaiassen).
avalueof67.8billionNOK(approximately8.3billionUSD).Atlantic salmon(SalmosalarL.)isbyfarthemostimportantspecies,accounting for1.28milliontonnesand64.5billionNOK(approximately7.9billion USD),an8.8-foldincreasefrom1990,whentheproductionwas145990 tonnes(StatisticsNorway,2020).Theremarkableincreaseinaquacul- tureproductionledtoincreaseddemandforfeedingredientsandfol- lowingthis,increasedprices(Olsenetal.,2014).Inordertofulfilthe demandforfeedatareasonablecost,theproportionofmarineingredi- entshasgraduallybeenreducedandswitchedwithplantingredients.A recentstudyshowedthattheproportionofmarineingredientshasbeen reducedfrom90%to30%duringtheperiod1990to2016(Aasetal., 2019).However,ashiftfrommainlymarinefeedingredientstoterres- trialfeedingredientswillinevitablyleadtoachangeinthebiochemical compositionofthefishmuscleandthespecificbiochemicalcomposition offarmedseafoodmaybeverydifferentfromitswildcounterpartsdue totheformulationofthefeeds(Jensenetal.,2012).
Inrecentyears,thishasraisedanincreasedinterestfororganicpro- ductionofsalmon.OrganicaquacultureisquitenewinNorway,asthe first organically producedsalmon reachedtheNorwegian market in 2011(SalMar,2020).Theproductionoforganicsalmonisstillquitelow,
https://doi.org/10.1016/j.afres.2021.100033
Received17September2021;Receivedinrevisedform3December2021;Accepted9December2021 Availableonline16December2021
2772-5022/© 2021TheAuthor(s).PublishedbyElsevierB.V.ThisisanopenaccessarticleundertheCCBYlicense(http://creativecommons.org/licenses/by/4.0/)
withonlytwocommercialproducersandaproductionaround16000 tonnesperyear.Organicaquacultureproductionissubjectedtostricter regulationsthanisconventionalaquaculture.Theregulationscoveris- suesregardingtheenvironment,fishwelfareandnutrition.Amongthe demandsforeco-certificationisthattheproportionofmarineingredi- entsinthefeedmustbehigherthaninconventionalfarming.Further shouldthemarineingredientsprimarilyoriginatefromtrimmingsoffish fromsustainablefisheriesandsyntheticantioxidantsandaminoacids arenotallowed(Lovdata,2017;TheEuropeanCommission,2008).
Duetothedemandsregardingmarineingredientsandadditives,it isbelievedthatthecompositionandqualityoftheorganicsalmonof todayisquitesimilartothatof theconventionalsalmon10-20years ago.Itisalsoacommonperceptionthatthecommerciallyavailableor- ganicsalmonislessfattyandlessredthantheconventional salmon.
Thelast fewyears, somestudieshavebeen publishedcomparingef- fectsofdifferentprocessingtechniquesonorganicallyandconvention- allyfarmedsalmon(Lerfalletal.,2016a;Lerfalletal.,2016b).How- ever,literatureavailableonthecompletebiochemicalcompositionof commerciallyavailableorganicsalmonoftodayisstillscarce.
Theaimofthisstudywasthustocomparethenutritionalvalueand storagestabilityofcommerciallyavailableorganicallyandconvention- allyproducedsalmoninNorwaytoday.
2. MaterialsandMethods 2.1. Experimentalconditions
Conventional andorganicsalmon (SalmosalarL.) were bothde- ployedtoseainSeptember2016.Forconventionalfish,smoltofthe RaumastrainrearedatFollafoss(n=172879,averageweight77g)were deployedtoseaatOterneset,Tromscounty,Norway(68.9°N,16.7°E).
Fororganicsalmon,smoltoftheAquagen strainrearedat Aquafarm (n=91467,averageweight60g)weredeployedtoseaatÅrberg,Troms county,Norway(69.2°N,16.9°E).Atbothlocations,feedingwasauto- matedandhandledfromaremotecentral.Theseacagesweremonitored byunderwatercamerastocontrolthefeedingbasedonthefish’sbe- haviourtoensurefeedinguntilapparentsatiation.Standardcommercial feedswereusedforbothconventionalandorganicsalmon.Theprotein contentinfeedusedforconventionalsalmonwas31%,andthelipid contentwas29%,whilefeedfororganicsalmonhad28%proteinand 33%lipids.Thesumofeicosapentaenoicacid(EPA)anddocosahex- aenoicacid(DHA)were5.3and12.8%oftotallipidinfeedforcon- ventionalandorganicsalmon,respectively.Conventionalsalmonwere slaughteredafter525days,whileorganicsalmonwereslaughteredafter 560daysinsea.
2.2. Samplingprocedures
Forcompositionalanalyses,fish(n=20)wererandomlysampled fromeachlocation2-3daysbeforeregularslaughtering.Thefishwere bathanesthetizedusingbenzocaine(30-40mgL−1),killedbygillcutting andbledoutincirculatingicewaterfor30min.Weightsandlengths ofwholefishwererecorded,beforethefishwerefilleted.Filletswere storedskin-oninicefor5-8hbeforefreezingat-50°Cuntilanalyses.
Priortoanalyses,thefishwerethawedatroomtemperatureand skinwasremoved. Visiblefatwasremoved fromthebellyflapsand dorsalfinareasandthewholefishfilletwasmincedusingaBoschPro PowerMFW68660(RobertBoschGmbH,Gerlingen,Germany).Minced fishsamplesweresubjectedtoproximateanalysis(water,ash,lipid,and protein),fattyacidcompositionandaminoacidcomposition.
Forstudiesof lipidoxidationandcolourstability,fishweresam- pledfromtheregularslaughteringlines(n=20fororganicsalmonand n=19forconventionalsalmon).Slaughteringwasperformedaccord- ingtostandardregulations.Immediatelyafterbleeding,thefishwere guttedandputinice fortransportationtotheNorwegianCollege of FisheryScience.Uponarrival,weightsandlengthswererecordedand
fishwerefilleted.Colourmeasurementswereperformedoneachofthe fillets.Thereafter,thefilletswerepackedinplasticbagsandstoredinice untilfurtheranalyses.After7daysonice,therightfilletwasweighed, thedriplosswasrecordedandcollected,andcolourwasmeasured.A sampleofthefilletintheregioncorrespondingtotheNorwegianquality cut(NQC)wasfrozenforlateranalysisofthiobarbituricacidreactive substances(TBARS).Onday18,thesameprocedureswereperformed ontheleftfillet.
All reagents used in these analyses were of analytical grade.
Dichloromethane and methanol were purchased from BDH (Poole, Dorset, UK). All other solventsand chemicalswere purchased from Merck(Darmstadt,Germany),unlessotherwisestated.
2.3. Analyticalmethods
2.3.1. Waterandash
Water and ash were determined gravimetrically using modi- fied versions of AOAC methods 925.04 and 938.08, respectively (Latimer,2019).Inshort,approximately5gofhomogenizedfishfillet wasdriedfor48hoursat105°C.Thewater-freematerialwasthereafter combustedat500°Cfor16h.
2.3.2. Lipidcontentandfattyacidcomposition
LipidswereextractedaccordingtoFolchetal.(1957),withthead- justmentsdescribedbyMaehreetal.(2014).Approximately1gofho- mogenizedfishfilletwasmixedwith20mLdichloromethane(DCM):
methanol(2:1v/v).Heptadecanoicacid(C17:0)wasaddedtoserveas internalstandard.Themixturewasshakenfor20minutes,followedby filtration.Thefiltratewaswashedwith4mL0.9%NaCl,followedby centrifugationat2000xgfor10min.Thewaterphasewasremoved, and thelipid phase wasevaporated underN2 until dryness. Weight wasrecordedandlipidcontentcalculated.Theextractedlipidwasre- dissolvedinDCM:methanol(2:1v/v)toafinalconcentrationof10mg mL−1.
Prior tofatty acid analysis trans-methylation was performed ac- cording toStoffelet al.(1959), withthemodifications describedby Maehreetal.(2013).Inshort,100μLofthe10mgmL−1lipidsolu- tionsweremixedwith900μLDCMand2mLacidifiedmethanol(2%
v/vH2SO4inmethanol).Themixturewasboiledfor1h,followedby additionof 3.5mLheptaneand3.5mL5%NaClandthoroughmix- ing.Theheptanephasewascollectedandconcentratedto100μLunder N2.Thereafterthesamplesweresubjectedtofattyacidanalysisasde- scribedbyMaehreetal.,(2013),usinganAgilent6890Ngaschromato- graphwithaflameionizationdetector(FID)(AgilentTechnologiesInc., SantoClara,CA,USA).AVarianCP7419capillarycolumn(VarianInc., Middelburg,theNetherlands)wasusedforseparation.Identificationof singlefattyacidswasperformedbycomparisonwithcommercialfatty acidstandardpurchasedfromSigma(SigmaChemicalsCo.,St.Louis, MO,USA)andNu-Chek(Nu-ChekPrepInc.,Elysian,MN,USA).
2.3.3. Proteincontentandaminoacidcomposition
Amino acidsweredetermined accordingtoMaehreetal.(2013). Approximately200mgofthehomogenizedfishfilletwasmixedwith 500μlof20mMnorleucine(internalstandard)and700μldistilledwa- ter.Concentratedhydrochloricacidwasaddedtoafinalconcentration of6M.ThesampleswereflushedwithN2for15sbeforehydrolysisat 110°Cfor24h,accordingtoMoore&Stein(1963).Afterhydrolysis,100 μlofthehydrolysatewasevaporatedunderN2tocompletedryness,and thereafterre-dissolvedin1mLlithiumbufferpH2.2.Allaminoacids wereanalyzedchromatographicallyusingaBiochrom 30aminoacid analyzerequippedwithalithiumionexchangecolumn(BiochromCo, Cambridge,UK)asdescribedbyMaehreetal.(2013).Proteincontentis givenasthesumofindividualaminoacidresidues(themolecularweight ofeachaminoacidlessthemolecularweightofwater)asrecommended bytheFoodandAgricultureOrganizationoftheUnitedNations(FAO, 2003).
2.3.4. Colourandthiobarbituricacidreactivesubstances(TBARS) Colouroffilletwasmeasuredaccordingtoinstrumentalcolouranal- ysis(CIELab1976)usingMinoltaChromameterCR-200(Minolta,Os- aka,Japan)calibratedtoawhitestandard.TheL∗,a∗ andb∗ values weremeasuredontheloinareaofeachfillet(from6cmto20cmfrom theanterioroffillet)intriplicate.Chroma(C∗)wascalculatedbyusing formulaC∗=√
(a∗2+b∗2)todeterminethecoloursaturation.Hue(h∗) representsthecolouranglebetweena∗andb∗,whereh∗=0°forreddish hueandh∗=90°foryellowishhue.Huewascalculatedusingformula h∗=tan−1(b∗/a∗).
Thiobarbituricacidreactivesubstances(TBARS)weredeterminedas describedbyKeetal.(1984)byweighingapproximately4goffilletina 50mLcentrifugetubeandadding15mL10%trichloroaceticacidwith 0.1%EDTAand0.1%propylgallate.Thesampleswerehomogenised usinganUltraTurraxT25homogeniser(IKAWerkeGmbH, Staufen, Germany)for1minat6000rpm,boiledfor30minandcooled.There- after,thesampleswerefilteredandmixed1:1with6gL−1thiobarbituric acid.Thismixturewasthenboiledforanother30min.Absorbancewas readat532nmusingaVisibleSpectrophotometerGenesys20(Thermo ScientificTM,Waltham, MA,USA)andcompared toa standardcurve madefrom malondialdehyde(MDA) withconcentrationsrangingbe- tween0and10nmolL−1.
2.4. Statistics
StatisticalanalysiswasperformedusingMinitab19(MinitabInc., PA,USA).Testsofnormality(RyanJoinertest)wasperformed.Fornor- mallydistributeddata,homogeneityofvariancewasexamined(Ftest), beforeperformingaStudent’st-test(basedonmeanvalues)forevalu- ationofstatisticaldifferences.Non-normallydistributeddatawerean- alyzedusingthenon-parametricMannWhitneytest(basedonmedian values).Means/medianswereconsideredsignificantlydifferentatp<
0.05.
3. Resultsanddiscussion 3.1. Proximatecomposition
Averageweightsandproximatecompositionsofthefishattimeof samplingareshowninTable1.Thefish(n=20)weresampledrandomly fromtheseacagesandtherewasawideweightrange,1800– 7200gfor organicfishand3650– 8150gforconventionalfish.Consideringthe totalamountofslaughteredfishintheproductions,i.e.around170000- 180000individualsintheconventionalproductionandaround90000 individualsintheorganicproduction,asamplingof20individualsfrom eachsiteisverysmallandtheresultsmustthusbeinterpretedwithcare.
Oneindividualfromtheorganicallyfarmedsalmonwasidentifiedasan outlier,definedasvalues±2SDofthemean,forseveraloftheanalytical variablesandwasthusexcludedfromthecalculations.
Theashcontent,reflectingthemineralcontent,wassimilarbetween groups.Forwater,protein,andlipidstherewerestatisticallysignificant differencesbetweentheorganicandtheconventionalfish.Thecalcu- latedenergylevelforthesalmoninthisstudywasaround7500kJkg−1 fortheorganicsalmonand8700kJkg−1fortheconventionalsalmon, respectively. Thisismainlyareflectionofthehigherlipidcontentof theconventionallyfarmedsalmon.Inthisstudy,thelipidcontentswere 169gkg−1and134gkg−1forconventionalandorganicsalmon,respec- tively.Inpreviousstudies,involvingconventionallyfarmedsalmonhar- vestedin1994-1996,2003,2010and2012,thelipidcontentswere100 gkg−1,74gkg−1,123gkg−1and140gkg−1,respectively(Belletal., 1998,Blanchetetal.,2005;Jensenetal.,2012;Lundebyeetal.,2017).
Thisindicatesthattherehasbeenatendencytowardsincreasinglipid contentof conventionallyfarmed fishduringthelastdecades. Inor- ganicsalmon,however,thelipidcontentwaswithinthesamerangeas thatofconventionallyfarmedfishin2010and2012.Althoughthelipid contentinorganicsalmonislowerthanintheconventionalsalmon,it isstillhighcomparedtoothermusclefoods,suchaschickenandbeef (NorwegianFoodSafetyAuthority, 2020).Intimes wherethepreva- lenceofobesityissteadilyincreasingglobally,thisshouldbeconsidered whendietaryrecommendationsregardingfishconsumptionaremade.
Theproteincontentinfarmedsalmonharvestedin2010(Jensenetal., 2012)washigherthanboththeconventionalandtheorganicsalmonin thepresentstudy,namely183gproteinkg−1fishmuscle.However,re- portedproteinishighlydependentonanalyticalmethods,makingdirect comparisonsbetweenstudiesdifficult(Maehreetal.,2018).
3.2. Fattyacidcomposition
Lipidsinfeedsarenormallypresentastriglycerides,i.e.threefatty acidsboundtoaglycerolskeleton.Duringdigestion,twoof thefatty acidsaredetachedfromtheglycerolskeletonandlipidsarethusab- sorbedasonemonoglycerideandtwofreefattyacids,withoutfurther decomposition(Thiboudeau&Patton,1999).Thefattyacid(FA)com- positioninthefeedswillthustoalargeextentbereflectedintheFA compositionofthesalmonmuscle.
Table 2showsthe amountsof themainFAsin organicandcon- ventionalsalmon,reportedbothincompositionalvalues(i.e.%ofto- talFA)andnutritionalvalues(i.e.gkg−1fishmuscle).Whenlooking atthecompositionalvalues,itisseenthattherearesignificantdiffer- encesbetweenconventionalandorganicsalmoninallFAs.However, due to theincreased lipid contentin the conventional salmoncom- paredtotheorganicsalmon,someofthese differencesareequalized
Table1
Proximatecomposition(water,ash,lipidandprotein)inorganicallyandconventionallyfarmed Atlanticsalmonattimeofslaughter(after18monthsinseacages).Valuesarepresentedas mean±SD(n=19fororganic,n=20forconventional)andingkg-1fishmuscle,unless otherwisestated.Differentlettersinthesamerowindicatesignificantdifferences(p<0.05) betweenorganicallyandconventionallyfarmedfish.
Organic salmon ( n = 19)
Conventional salmon
( n = 20) p -value Fish weight [g] 5476 ± 1427 5500 ± 1113 p = 0.954
Water 653 ± 18 A 613 ± 12 B p < 0.001
Ash † 12 ± 1 12 ± 1 p = 0.403
Lipid 134 ± 20 B 169 ± 15 A p < 0.001
Protein ∗ 146 ± 7 A 140 ± 7 B p = 0.008
Energy [kJ kg -1] ∗∗ 7478 ± 710 B 8707 ± 510 A p < 0.001
†Datawerenon-normallydistributed
∗Reportedassumofaminoacidresidueslessthemolecularweightofwater,asrecommended byFAO(2003)
∗∗EnergywascalculatedinaccordancewithEUCouncilDirective1169/2011,annexXIV (TheEuropeanCommission,2011).
Table2
CompositionofthemainfattyacidsinorganicallyandconventionallyfarmedAtlanticsalmonattimeofslaughter(after18monthsinseacages).
Valuesarepresentedasmean±SDandin%forcompositionandgFAkg-1fishmuscleforamount.Differentcapitallettersinthesamerowindicate significantdifference(p<0.05)innutritionalvaluebetweenorganicallyandconventionallyfarmedsalmon.
Organic salmon (n = 19) Conventional salmon (n = 20) Compositional
value (%)
Nutritional value (g kg -1fish muscle)
Compositional value (%)
Nutritional value (g kg -1fish muscle)
p -value
composition p -value amount 14:0 † 4.4 ± 0.1 6.0 ± 0.9 A 2.2 ± 0.1 4.1 ± 0.6 B p < 0.001 p < 0.001
16:0 12.9 ± 0.3 17.5 ± 2.8 9.4 ± 0.2 17.1 ± 2.0 p < 0.001 p = 0.596
18:0 3.1 ± 0.1 4.3 ± 0.7 2.4 ± 0.1 4.4 ± 0.5 p < 0.001 p = 0.614
Sum SFA 20.5 ± 0.4 27.7 ± 4.5 14.1 ± 0.3 25.5 ± 3.0 p < 0.001 p = 0.079 16:1 n-7 † 5.3 ± 0.1 7.1 ± 1.2 A 2.4 ± 0.1 4.3 ± 0.6 B p < 0.001 p < 0.001 18:1 n-9 † 16.4 ± 0.4 22.3 ± 3.7 B 40.2 ± 0.4 72.9 ± 8.9 A p < 0.001 p < 0.001 18:1 n-7 2.7 ± 0.1 3.6 ± 0.6 B 3.1 ± 0.0 5.5 ± 0.7 A p < 0.001 p < 0.001 20:1 n-9 8.4 ± 0.6 11.4 ± 1.4 A 5.0 ± 0.1 9.0 ± 1.1 B p < 0.001 p < 0.001 22:1 n-11 † 9.7 ± 0.6 13.1 ± 1.7 A 4.1 ± 0.1 7.4 ± 0.9 B p < 0.001 p < 0.001
22:1 n-9 2.1 ± 0.1 2.8 ± 0.4 1.5 ± 0.1 2.7 ± 0.3 p < 0.001 p = 0.447
Sum MUFA 44.6 ± 0.9 60.3 ± 8.7 B 56.2 ± 0.6 101.9 ± 12.5 A p < 0.001 p < 0.001 18:2 n-6 13.0 ± 0.3 17.6 ± 2.6 B 13.6 ± 0.2 24.7 ± 3.0 A p < 0.001 p < 0.001 18:3 n-3 † 2.4 ± 0.1 3.3 ± 0.5 B 5.5 ± 0.1 10.0 ± 1.3 A p < 0.001 p < 0.001 18:4 n-3 † 2.3 ± 0.1 3.1 ± 0.5 A 1.2 ± 0.0 2.1 ± 0.2 B p < 0.001 p < 0.001 20:2 n-6 0.8 ± 0.1 1.1 ± 0.2 B 1.1 ± 0.1 2.0 ± 0.2 A p < 0.001 p < 0.001 20:5 n-3 † 5.0 ± 0.3 6.8 ± 1.2 A 2.5 ± 0.1 4.6 ± 0.5 B p < 0.001 p < 0.001 22:5 n-3 1.9 ± 0.1 2.6 ± 0.5 A 1.1 ± 0.1 2.0 ± 0.3 B p < 0.001 p < 0.001 22:6 n-3 † 7.7 ± 0.3 10.4 ± 1.5 A 3.9 ± 0.2 7.0 ± 0.8 B p < 0.001 p < 0.001 Sum PUFA 33.2 ± 1.0 45.0 ± 6.9 B 28.9 ± 0.4 52.4 ± 6.2 A p < 0.001 p = 0.001 - where of PUFA n-3 19.4 ± 0.8 26.2 ± 4.2 14.2 ± 0.3 25.7 ± 3.0 p < 0.001 p = 0.634 - where of LC n-3-PUFA † 14.6 ± 0.7 19.8 ± 3.2 A 7.5 ± 0.2 13.6 ± 1.5 B p < 0.001 p < 0.001 - where of EPA + DHA † 12.7 ± 0.6 17.2 ± 2.8 A 6.4 ± 0.2 11.6 ± 1.3 B p < 0.001 p < 0.001 - where of PUFA n6 13.8 ± 0.4 18.7 ± 2.8 B 14.8 ± 0.2 26.7 ± 3.2 A p < 0.001 p < 0.001
n-6/n-3 † 0.7 ± 0.0 B 1.0 ± 0.0 A p < 0.001 p < 0.001
†Datawerenon-normallydistributed
whenlookingatthenutritionalvalues.Sincethisiswhatismostrele- vantinadietaryperspective,nutritionalvaluesarediscussedfurther.
AmongthesaturatedFAsthereareonlynon-significantdifferencesbe- tweenorganicandconventionalsalmon.Whenitcomestomonounsat- uratedFA(MUFA)andpolyunsaturatedFA(PUFA)composition,how- ever,therearepronounceddifferencesbetweenthegroups.Inthecon- ventionalsalmon,theMUFAs aredominatedbyone singleFA,oleic acid(C18:1,n-9),whiletheorganicsalmoncontainsrelativelymoreof thelong-chainMUFAsC20:1, n-9andC22:1,n-11. Thisreflects that theproportionofmarineingredientsintheorganicfeedishigherthan intheconventionalfeed,asthesetwoFAsarenotcommonlyfoundin plantoils(Zambiasietal.,2007).WhenitcomestothePUFAs,theor- ganicsalmoncontainsmoreofthelong-chainomega-3PUFAsthandoes theconventionalsalmon,whilethecontentsoflinoleicacid(LA;C18:2, n-6)andalpha-linolenicacid(ALA;C18:3,n-3)arehigherinthecon- ventionalsalmon.ThesetwoFAs,alongwitholeicacid,areverycom- moninplantoils,butonlyfoundinlowamountsinmarineorganisms (Sigurgisladottir&Palmadottir,1993).FromtheFAcompositionitis evidentthattheorganicsalmonalsoreceivessomeplantoilsintheir feed,asthecontentofLAandALAismuchhigherinorganicsalmon thaninwildsalmonwherethecontentisnormallyaround1.0– 1.5g kg−1(Jensenetal.,2012;Lundebyeetal.,2017).
Ahighintakeofseafoodhaslongbeenassociatedwithdecreasedrisk ofdevelopinglifestyle-relateddiseases,suchastypeIIdiabetes,cardio- vasculardiseasesandotherinflammatorydiseases(Weichselbaumetal., 2013).Therearemainlytwofactorsthatareassociatedtothesehealth benefits,namelyahighcontentofthelong-chainedn-3PUFAseicos- apentaenoicacid(EPA;C20:5,n-3)anddocosahexaenoic acid(DHA;
C22:6,n-3),alongwiththeratiobetweenomega-6andomega-3FAs.
EventhoughEPAandDHAcanbederivedfromALA,thisconversion rateislimitedinhigh-trophicspecies,suchasmammals(Brenna,2002) andsalmon(Ruyteretal.,2000).This meansthattheyareregarded assemi-essentialFAsandmustbeprovidedthroughthediet.Thepri- maryproducersofEPAandDHAarelow-trophicmarinespeciesthat formthebaseofthemarinefoodchain.Asthesespeciesarethenat-
uralfeedingsourceforshellfishandsmallfish,seafoodisthebest,if notonly,sourceofEPAandDHA.Asdescribed byAasetal.(2019), therewasasubstantialdecreaseintheproportionofmarineingredients insalmonfeedfrom1990to2016,andasaconsequenceofthisthere havebeensomeconcernsaboutwhetherthefarmedsalmonwouldstill beconsideredahealthyfoodorifitwouldturnintoa“swimmingveg- etable”.Asaconsequenceoftheseconcerns,alongwithreducedavail- ability/sustainabilityoftraditionalmarineingredients(fishmealand fishoil),therearecomprehensiveresearchactivitiesonalternativeand moresustainablemarinefeedingredients,suchasmarinemicroalgae andinsectmeal(Dineshbabuetal.,2019;Gongetal.,2019;Nogales- Meridaetal.,2019;Tibbettsetal.,2020).Whileinsectmealsofaris notcommonlyusedincommercialaquaculturefeeds,someofthelarge feedproducershavestartedaddingmicroalgaemealtotheirproducts (LerøySeafoodGroup,2016).
Theregulationsfororganicproductionofsalmonidsstatethatthe proportionofmarineingredientsshouldbeatleast40%(Lovdata,2017; TheEuropeanCommission,2008).Theproportionofmarineingredients in feedsfororganicsalmonisthusnormallyhigherthaninfeedsfor conventionalfish.KnowingthatmostoftheEPAandDHAinsalmon originatesfromthefeed,thecompositionwillbereflectedinthefish muscle.AsstatedintheMaterialsandMethodssection(Section2.1), thesumofEPAandDHAwere5.3and12.8%oftotallipidinfeedfor conventionalandorganicsalmon,respectively.And,asseeninTable2, thisisreflectedinthefishmuscle;thesumofEPAandDHAwere6.4
%oftotallipidintheorganicfishmuscle,whilethesumofEPAand DHAinorganicfishwere12.7%.Hence,theorganicfishinthisstudy containedapproximately48%moreEPAandDHAthandidthecon- ventionalfish,17.2gkg−1vs.11.6gkg−1,respectively.Comparedto thesumofEPAandDHAinconventionalfishharvestedin2010(10.3g kg−1;Jensenetal.,2012)and2012(14gkg−1;Lundebyeetal.,2017), bothorganicandconventionalsalmonfromthepresentstudycontain moreEPA+DHAthanfarmedsalmonharvestedin2010(Jensenetal., 2012),whiletheEPA+DHA contentsin the2012(Lundebyeetal., 2017) wereinbetweentheorganicandtheconventional fishinthis
study.TheEPAandDHAlevelsarealsocomparabletothelevelspre- sentedinarecentstudydescribingthefattyacidcompositioninfarmed NorwegiansalmoncommerciallyavailableintheUK(Spragueetal., 2020).Thereareonlyafewproducersofaquaculturefeedsglobally.
Thefeedformulationmaydifferslightlyfromoneproducertoanother, resultinginsomedifferencesintheFAcompositionofthefish.However, thefeedstendtobequitesimilar,atleastinmacronutrientcomposition.
Thetrendsinfeeddevelopmentisthussimilarandindicatethatalong withincreasingthelipidcontentandtheplantoilinclusioninthefeeds, therehasbeenafocusonkeepingtheEPA+DHAcontentatarecom- mendedlevel.
OfficialrecommendationsfordietaryintakeofEPA+DHAvarybe- tweencountriesandfoodorganizations,butaspresentedinaprevious reviewpaper,mostofthemagreeonanintakeintherangeof250– 500mg perdayeitherasseafood consumptionorasdietary supple- ments(Maehreetal.,2015).Allofthefishfromthementionedstudies aregoodsourcesofEPA+DHA,astherequiredamount forachiev- ing500mgperdayis30gfortheorganicsalmoninthepresentstudy (2018),36g forthe2012salmon(Jensenetal.,2012),43gforthe conventionalsalmoninthepresentstudy(2018),and49gforthe2010 salmon(Lundebyeetal.,2017),allwellbelowaregulardinnerportion (150g).Inotherwords,oneportionofconventionalsalmonfromthe presentandpreviousstudies(Jensenetal.,2012;Lundebyeetal.,2017) wouldcovertherequirementsfor3-4days,whileoneportionofthe organicsalmonwouldcovertherequirementsfor5days.
Theotherfactorrelatedtoloweringtheriskoflifestyle-relateddis- easesistheratiobetweenn-6andn-3FAs(Harris&vonSchacky,2004; Simopoulos,2008;Stanleyetal.,2007).Anoptimaln-6:n-3 ratiois suggestedtobeintherange2:1-5:1.However,inwesterndietstoday theactualratioisbetween15:1-17:1(Simopoulos,2008)andshould thusbereduced.Itis,however,importanttorememberthatthisratiois meanttobeameasureofthecompletedietandnotjustofsinglefood items.
Anincreasinglevelofplantoilsinthefishfeedwillinevitablyin- creasethecontentofLA,whichisanabundantn-6FAinmostplant oils.ThecontentofALAvariesmorebetweendifferentplantoils,giving verydifferentn-6:n-3ratiosbetweendifferentplantoils(Zambiasietal., 2007).Theimpactonthen-6:n-3ratiointhefishwillthusdependon whichplantoilisused,alongwiththecontentofLCn-3PUFAs.Inthis study,therewassignificantdifferencebetweenthen-6:n-3ratioinor- ganicandconventionallyfarmedsalmon,itbeing
1:1.4intheorganicand1:1intheconventionalsalmon.Bothra- tiosarehowevercomparablewiththeratioof1:1.2infishharvested in2012.Inthe2010fishtheratiowas1:2.3,indicatinga“healthier” FAcomposition.However,whencomparingthecontentsofalltherel- evantFAs,itisseenthatallofthemhasincreasedsince2010,notonly theplant-basedones.Thissupportsthepreviouslymentionedfocusof keepingtheEPA+DHA contentatarecommendedlevelin thecon- ventionallyfarmedfish.Intheorganicfish,then-6:n-3ratioandthe contentofLAishigherthaninthe2010fish,whilelipidcontent,oleic acidandALAareapproximatelythesame.Thissupportstheimpression thattheorganicsalmonoftodayismoresimilartoconventionalfish someyearsagothanconventionalfishoftoday.
3.3. Aminoacidsandproteinquality
Withoutachievingthesameattentionasthechangeoflipidsources, alsotheproteinsourcesofthesalmonfeedhavechangedovertheyears, fromfishmealtoplantproteinssuchassoymeal(Aasetal.,2019).
Incontrast tothelipids,theaminoacidcompositionofthefeedwill notbedirectlyreflectedinthesalmonflesh.Thisisduetoadifferent mechanismofdigestionandabsorptioninthebody(Thiboudeau&Pat- ton,1999).Asonlyfreeaminoacidsmaybeabsorbedintheintestine, theproteinsinthefeedmustbehydrolysedtotheirconstitutingamino acidsbeforeabsorptioninthesmallintestine.Afteruptake,theamino acidsarere-synthesizedtonewproteinsintheliver.
Table3
Aminoacidcompositioninorganically(n=19)andconventionally(n=20) farmedAtlanticsalmonattimeofslaughter.Valuesarepresentedasmean
±SDandingAAkg-1fishmuscle.Differentcapitallettersinthesamerow indicatesignificantdifference(p<0.05)betweenorganicallyandconven- tionallyfarmedsalmon.
Organic salmon (n = 19)
Conventional salmon
(n = 20) p -value Essential amino acids (EAA)
Threonine 8.9 ± 0.6 8.7 ± 0.3 p = 0.168 Valine 9.1 ± 0.6 9.0 ± 0.3 p = 0.460 Methionine 5.9 ± 0.4 A 5.5 ± 0.4 B p = 0.010 Isoleucine 7.5 ± 0.4 7.6 ± 0.3 p = 0.681 Leucine 14.4 ± 0.8 14.4 ± 0.5 p = 0.982 Phenylalanine 7.8 ± 0.5 7.6 ± 0.3 p = 0.124 Lysine † 17.5 ± 1.1 A 16.7 ± 0.6 B p = 0.039 Histidine † 5.3 ± 0.3 4.8 ± 1.1 p = 0.565
Tryptophan n.a. n.a.
Non-essential amino acids + metabolites
Taurine 0.6 ± 0.2 A 0.4 ± 0.1 B p = 0.001 Aspartic acid ∗ 13.5 ± 0.8 13.6 ± 0.6 p = 0.603 Serine 7.3 ± 0.4 7.2 ± 0.3 p = 0.356 Glutamic acid ∗ 25.6 ± 1.7 25.5 ± 1.1 p = 0.801 Proline † 7.4 ± 0.4 B 8.3 ± 1.2 A p = 0.002 Glycine † 9.7 ± 0.7 A 9.3 ± 0.6 B p = 0.007 Alanine 11.4 ± 0.6 11.1 ± 0.4 p = 0.100 Cysteine † 0.5 ± 0.1 0.4 ± 0.2 p = 0.619 Tyrosine † 6.0 ± 1.0 4.5 ± 2.6 p = 0.334 b-Alanine 1.5 ± 0.1 B 1.6 ± 0.1 A p = 0.002 1-methyl Histidine † 3.5 ± 0.3 B 4.0 ± 0.8 A p = 0.001 Arginine 12.6 ± 0.8 A 10.5 ± 0.7 B p < 0.001 Sum Amino acids +
Metabolites 175.5 ± 8.5 A 169.1 ± 8.0 B p = 0.020 Sum EAA 76.0 ± 4.6 74.4 ± 3.1 p = 0.199
% EAA 44.7 ± 0,9 B 45.6 ± 0.8 A p = 0.001
∗Asasparagineandglutaminearepresentintheirdeaminatedformsaf- teracidichydrolysis,asparticacidandglutamicacidrepresentthesums ofasparticacid+asparagineandglutamicacid+glutamine,respectively;
n.a.=notanalysed.
†Datawerenon-normallydistributed.
Table3showstheaminoacidcompositionoftheorganicandconven- tionallyfarmedsalmon.Therearesomesignificantdifferencesbetween theorganicandtheconventionalfarmedsalmon.Thecontentsofpro- line,alongwiththemetabolitesb-Alanineand1-methylhistidine,are significantlyhigherintheconventionalsalmon,whilethecontentsof methionine,lysine,taurine,glycineandargininearesignificantlyhigher intheorganicsalmonthanintheconventionalsalmon.
Bothamountandqualityofdietaryproteinareimportantinorder tomaintainnormalgrowthandproductionofphysiologicallyimportant proteins.Proteinqualityisoftendefinedbyitsabilitytocoverthere- quirementsof essentialaminoacids,along withtheirabsorption and utilizationinthebody.TheWorldHealthOrganization(WHO)hassug- gesteda“referenceprotein” thatcontainstherequiredamountofeach oftheessentialaminoacids(FAO/WHO/UNU,2007).Acommonwayof determiningthequality,orthechemicalscore,ofdifferentfoodproteins istocomparethemwiththisreferenceprotein.Thechemicalscoreis foundbycalculatingtheratiobetweeneachoftheessentialaminoacids inafoodproteinversusthesameaminoacidinthereferenceprotein, andthelowestratioobtainedequalsthechemicalscoreoftheprotein.
Mostproteinofanimalorigin containsufficientamountsofallessen- tialaminoacidsandthushavechemicalscoresof1.Plantproteinsare, however,oftenlowinoneormoreessentialaminoacids.Forinstance, cerealsareoftendeficientinlysine,whilelegumesmaybedeficientin sulphurcontainingaminoacidssuchasmethionine.Inaddition,thedi- gestibilityofplantproteinsmaybelowerthanthatofanimalproteins duetoadifferentcellstructure(Friedman,1996).Anincreasedinclu- sionofplantproteinsattheexpenseofanimalproteinsourcesinafeed maythusleadtoloweramountsofessentialaminoacidsavailablefor
Figure1. Essentialaminoacidcompositionin organicallyandconventionallyfarmedAtlantic salmon(SalmosalarL.)proteinsrelativetothe referenceproteinsetbytheWHO.Thevalues aregivenasmean±SD(n=20)andin%of thereferenceprotein.
Table4
Colourcharacteristics(L∗,a∗,b∗,C∗andh∗)andthiobarbituricacidreactivesubstances(TBARS)inor- ganicallyandconventionallyfarmedAtlanticsalmonat0,7and18daysonice.Valuesarepresentedas mean±SD.Differentcapitallettersinthesamerowindicatesignificantdifference(p<0.05)between organicallyandconventionallyfarmedsalmonatthesamesamplingday.∗indicatesignificantdifference betweenday0andday7withineachgroup.∗∗indicatesignificantdifferencebetweenday0andday18 withineachgroup.†indicatesignificantdifferencebetweenday7andday18withineachgroup.
Organic salmon (n = 20) Conventional salmon (n = 19) p -value group L ∗
Day 0 41.5 ± 1.4 B 45.9 ± 2.0 A p < 0.001
Day 7 42.6 ± 1.5 ∗;B 50.6 ± 1.6 ∗;A p < 0.001
Day 18 45.0 ± 1.3 ∗∗;†;B 48.8 ± 2.1 ∗∗;†;A p < 0.001 p -value storage ∗p < 0.001; ∗∗p < 0.001; † p < 0.001 ∗p < 0.001; ∗∗p < 0.001; † p = 0.005
a ∗
Day 0 8.5 ± 1.0 B 9.6 ± 1.1 A p < 0.001
Day 7 9.9 ± 1.0 ∗;B 11.5 ± 1.6 ∗;A p < 0.001
Day 18 10.6 ± 1.1 ∗∗;B 11.7 ± 1.4 ∗∗;A p = 0.011
p -value storage ∗p < 0.001; ∗∗p < 0.001 ∗p < 0.001; ∗∗p < 0.001 b ∗
Day 0 9.9 ± 1.3 B 12.2 ± 1.5 A p < 0.001
Day 7 11.7 ± 1.3 ∗;B 14.8 ± 2.0 ∗;A p < 0.001
Day 18 12.6 ± 1.1 ∗∗;†;B 15.7 ± 1.8 ∗∗;A p < 0.001 p -value storage ∗p < 0.001; ∗∗p < 0.001; † p = 0.018 ∗p < 0.001; ∗∗p < 0.001
C ∗
Day 0 13.1 ± 1.6 B 15.6 ± 1.8 A p < 0.001
Day 7 15.3 ± 1.6 ∗;B 18.8 ± 2.6 ∗;A p < 0.001
Day 18 16.5 ± 1.6 ∗∗;†;B 19.6 ± 2.2 ∗∗;A p < 0.001 p -value storage ∗p < 0.001; ∗∗p < 0.001; † p = 0.025 ∗p < 0.001; ∗∗p < 0.001
h ∗
Day 0 49.2 ± 1.7 B 51.9 ± 1.7 A p < 0.001
Day 7 49.8 ± 1.4 B 52.3 ± 1.1 A p < 0.001
Day 18 50.1 ± 1.3 ∗∗;B 53.4 ± 1.8 ∗∗;†;A p < 0.001 p -value storage ∗∗p = 0.037 ∗∗p = 0.004; † p = 0.032
TBARS (μmol MDA-equivalents kg -1fish muscle)
Day 0 n.a. n.a.
Day 7 12.85 ± 2.07 A 8.72 ± 1.51 B p < 0.001
Day 18 22.52 ± 6.33 †;A 14.81 ± 4.58 †;B p < 0.001 p -value storage † p < 0.001 † p < 0.001
n.a.:notanalysed
re-synthesisofphysicallyimportantproteins.Thismay,inturn,leadto higherutilizationofmusclestorageproteins,andeventuallytoreduced growthanddevelopment.Inconventionalaquacultureitisthuscom- montoaddsyntheticaminoacidsinordertoensuresufficientamounts ofthemostexposedessentialaminoacids,especiallylysineandmethio- nine.Thisis,however,notallowedinorganicaquaculture.Here,po-
tentiallackof/lowamountsofessentialaminoacidsmustbeprevented throughadditionofingredientsnaturallyrichinfreeaminoacids,such asshellfishandmolluscs.
InFigure1, theamountsof essentialaminoacidsin organicand conventionalsalmonrelativetotheamountsofessentialaminoacidsin theWHOreferenceproteinareshown.
