Lumpfish (Cyclopterus lumpus) used as cleaner fish: Characterization and suitability for human consumption

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ContentslistsavailableatScienceDirect

Applied Food Research

journalhomepage:www.elsevier.com/locate/afres

Lumpﬁsh (Cyclopterus lumpus) used as cleaner ﬁsh: Characterization and suitability for human consumption

Tatiana N. Ageeva

^∗

, Grete Lorentzen , Heidi A. Nilsen , Kjersti Lian

Noﬁma AS, Muninbakken 9-13, Breivika, P.O. Box 6122, Tromsø 9291, Norway

a r t i c le i n f o

Keywords:

Cleaner ﬁsh Nutritional value Pollutants

Proximate composition Food safety Processing

a b s t r a ct

Farmedlumpfish(Cyclopteruslumpus)isfrequentlyusedascleanerfishinNorwegiansalmonaquaculture.Dur- ingtheperiodinthenetcage,thelumpfishfeedonsalmonlice.Afteratime,thefishstopeatingtheliceand arethenwithdrawnfromthenetcagewithoutfurtherexploitation.Inthisstudy,thenutritionalvalueoflump- fishwascharacterizedtoassessitssuitabilityasahumanfood.Thelumpfishwerecollectedfromtwoseparate salmonaquaculturefacilitiesandanalyzedforproximatecomposition,aminoacids,fattyacids,vitamins,minerals,environmentalpollutants,andheavymetals.Thewaterandproteincontentwereapproximately90and6%, respectively.Theproteincontainedallessentialaminoacids.Thefatcontentrangedfrom0.9to3.7%withahigh levelofthelongchainpolyunsaturatedfattyacidsEPA(eicosapentaenoicacid;20:5n-3)andDHA(docosahex- aenoicacid;22:6n-3).LumpfishmaybeagoodsourceofB12andD3vitamins,however,thecontentofseveral mineralswaslow.TheenvironmentalpollutantsandheavymetalswerebelowtheEUmaximumlevels,making thelumpfishsafeforhumanconsumption.Overall,ourresultsindicateapotentialtoexploitthelumpfish,even afteritstimeasacleanerfish.

1. Introduction

InNorway,farmedlumpﬁsh(Cyclopteruslumpus)isanimportant speciestocontrolsealice(Lepeophtheirussalmonis(Krøyer1837))infes- tationsonsalmoninaquaculture.Thesealiceparasiteattachestothe skinandisconsideredbothahealth-andwelfareproblemforsalmon.

Thelumpfishfeedsonsealiceandthusreducestheproblemoftheinfes- tation(Imslandetal.,2014a,2018).Commonly,thelumpfishistrans- ferredintothesalmonnetcageataninitialweightofabout25gand staysthereuntiltheendofsalmonproductionafterreachingaweight ofabout500g(Powelletal.,2018).Anetcagewithabout200.000 salmonrequiresbetween8.000and16.000lumpfish(Nøstvoldetal., 2016).Themortalityofthelumpfishinthenetcagesisknowntobe high,butthesurvivalrateisrapidlyimproving,closeupto80%insome facilities(Nøstvoldetal.,2016).Re-useofthelumpfishascleanerfish isnotanoptionasitstopseatinglicewhenitbecomesmatureatabout 14– 16months(Brookeretal.,2018;Imslandetal.,2014b).

In2019,about43millionfarmedlumpfishwereusedintheNorwe- giansalmonaquacultureindustryascleanerfish,representingavalue of about 943 million Norwegiankroner (NOK) (Directorate of Fish- eries,2021).Apartfromthepurchasingcostsofabout21NOKperfish, additionalchargesarerelatedtofeedingandgeneralcare,whichcauses substantialexpensesfortheaquacultureindustry.Forinstance,in2016, thesecostswereestimatedto950millionNOK(Iversenetal.,2017).

∗Correspondingauthor.

E-mailaddress:tatiana.ageeva@noﬁma.no(T.N.Ageeva).

Still,thereisnoestablishedprocedurestoutilizethelumpﬁshafteruse.

Somesalmonproducerstradethelumpfishforensilagepurposesata price of2.5NOKperfish,while somefacilitiespaytogetridof the fish (Nøstvold etal.,2016).Thecurrent practicemaybe questioned duetothesocial,economic,environmental,sustainability,andethical aspects.Infact,apotentialfoodresourceispoorlyutilized,andtheabil- itytoenhancevaluecreationislost.Fromasustainabilityperspective, itisessentialtoexploitallavailablemarineresourcesinthebestway possible.Fromanethicalandsocialperspective,re-useofthelumpfish towardshumanconsumptioncouldbebeneficial bothfortheNorwe- gianaquacultureindustryandforthecommunity(Nytrø etal.,2015; Nøstvoldetal.,2016).Giventhegrowingworldpopulation,alternative sourcesofproteinsintendedforhumannutritionshouldbedeveloped tomeetfuturedemand(Damodaran,2008).Ourhypothesisisthatafter beingusedascleanerfishinsalmonaquaculture,lumpfishcanbeused foralimentarypurposes.

In general, risks associated with ingestion of seafood involve pathogens,toxins(i.e.,algaltoxins),andchemicalcontaminants(i.e., lead, mercury, cadmium,or PCBs)(Instituteof Medicineof the Na- tionalAcademies,2007).Seafoodconsumptionalsoimplieshealthben- eﬁtsduetonutritionalvalue,withomega-3polyunsaturatedfattyacids (PUFAs)asthemostwell-known(Chandraetal.,2019;Durmuş,2018; Weinbergetal.,2021).Seafoodcanbeavaluablesourceoffat-soluble vitamins(A,D,E),water-solublevitamins(B12andB6)(Lund,2013),

https://doi.org/10.1016/j.afres.2021.100008

Received16July2021;Receivedinrevisedform2September2021;Accepted13October2021 Availableonline20October2021

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Table1

Overviewofexaminedsampletypesandanalysesoflumpﬁshsampled.Batch1and2.

Analysis Batch 1 Batch 2

78 ± 39 g ¹ 231 ± 67 g ¹ 513 ± 84 g ¹

Proximate composition Whole fish Fillet Skin Fillet Gutted with head Fatty Acid composition Whole fish Gutted with head Total Amino Acid composition Whole fish

Vitamins (except D3) Gutted with head

Vitamin D3 Gutted with head

Minerals Whole ﬁsh

Metals Whole ﬁsh

Environmental pollutants Whole ﬁsh

1Bodyweight(averageweight±standarddeviation,SD).

anddiﬀerentminerals(phosphorus,selenium,zinc,potassium,magne- sium,etc.)(Godswilletal.,2020;Ruxton,2011).

Tothebestofourknowledge,papersdescribinglumpfish(pre-used ascleanerfishinsalmonaquaculture)concerningproximatecomposi- tion,vitamins,minerals,andpollutants,havenotbeenpublished.Thus, inthispaper,weaimedtoscreenandcharacterizethenutritionalvalue oflumpfishafterbeingusedasacleanerfish.Technologicalproperties oflumpfishwerealsoconsidered.

2. Materialsandmethods 2.1. Rawmaterial

Thelumpﬁshusedinthisstudyweresampledfromsalmonnetcages duringMarch2020(Batch1)andSeptember2020(Batch2).Forboth batches,thelumpﬁshweresuppliedfromVangsvik(Senja,Troms,and Finnmarkcounty,Norway).

Batch1.InJuly2019,thefirstgroupoflumpfish(bodyweight≈ 30 g)wastransferredtonetcageswithsalmonatKaranes (Karlsøy, Troms,andFinnmarkcounty,Norway).Additionalgroupsoflumpfish (alsobodyweight≈30g)weresuppliedtothesamenetcageabout every4thweekuntilOctober2019.Duringtheperiodinthenetcage, thelumpfishweresupplementaryfed(LumpfishGrower20mg,BioMar, Norway)onceaday.InMarch2020,thelumpfish(n=83)wereran- domlysampledfromthenetcage,stunnedbyablowonthehead,and exsanguinatedbyimmediatelycuttingtheventralanddorsalaorta.The fishwerethenbledfor30mininacontainer(100L)withrunningsea- water(≈5°C),distributedandpackedintoplasticbags,andstoredat -18°C.Thefollowingday,thefishwasshippedtoNofima,Tromsø,and transferredto-40°Cuponarrival.

Batch2.InSeptember2020,thelumpfishwereobtainedfromthe netcagewithsalmonatÅbornes(Hansnes,TromsandFinnmarkcounty, Norway).Thefirstgroupoflumpfish(bodyweight≈30g)wasadded tothenetcageinAugust2019.Additionallumpfish(alsobodyweight

≈30 g)weresuppliedapproximatelyevery4thweekduringthenet cageperiod.Thefishweresupplementaryfed(CleanLumpfish2-4mm, Skretting,Norway)onceaday.Lumpfish(n=10)wererandomlysam- pledonebyonefromthenetcageandslaughteredasdescribedabove.

TheﬁshwerethenpackedinStyrofoamboxeswithice,transportedto Noﬁma,Tromsø,within40min,andstoredat0°Cforabout16hbefore beingprocessed.

2.2. Preparationofsamples

Batch1.Thefrozenlumpfishinplasticbagswerethawedincirculat- ingtapwater(3.4°C),weighed,andsortedaccordingtosize.Thefish werethendividedintotwoweightgroups:small(n=57,78±39g) andlarge(n=26,231±67g).Fivefishfromthelargefishgroupwere gutted,filleted, skinned,andthepercentageproportionof thelumpfish’bodyfractionsweredetermined(Table1).Then,threegroupswere minced,namely(1)wholefishfromthesmallfishgroup,(2)filletsfrom largefish, and(3)skinfrom largefish usingagrinder(Kilia, TK20

ltr,Dorfmark,Germany).Thethreeminceswerethenpackedinplastic containers(KartellLabware,Noviglio,Italy)andfrozenat-40°Cuntil analyzed.

Batch2.Thetenice-storedlumpfish(bodyweight513±84g)were weighted,gutted,andcutintohead,skin,andfillets,followedbyweight registration. Then, the body fractions (excepttheviscera) from five lumpfishwerepooled,minced,andanalyzedasguttedfishwithhead (Table1).Theskinnedfilletsfrom theremainingfivefishwereused toanalyzeproximate(Table1).Thesetwominceswerepackedinplas- ticcontainersandfrozenat-40°C,similarlytoBatch1,beforebeing analyzed.

2.3. Analyticalmethods

TheanalyticalmethodsappliedaregiveninTable2. 3. Resultsanddiscussion

Therawmaterialvariationduetosizeandfractionsusedforanalyses isgiveninTable1.InBatch1,awideweightrangeoflumpﬁshwas obtained,astheﬁshwerenotsortedwhentakenoutfromthenetcage.

Thesmalllumpfish’sizevariedbetween22-150gandoflargelumpfish from151to384g.Thetotaltimeinthenetcageisnotknownasit could rangefrom4weeksto8monthsasnewfishweresuppliedin thenetcageevery4thweek.However,thereweremoresmall-sizedfish thanlargerones.DuringtheprocessingofBatch1,itwasobservedthat somelumpfishhadformulatedfeedresiduesintheirstomachs.Toavoid inaccuraciesintheresultsduetofeedremains,thelumpfishinBatch2 weregutted(Table1).

3.1. Technologicalpropertiesoflumpﬁsh

Lumpfishhasaparticularbodyshape,makingprocessing(e.g.,fil- leting)challenging.Inprofile,thebodyislongerthanitisincircumfer- ence,butitiscompactedanteriorlyandposteriorly(Davenport,1985; Powelletal.,2018).Allfishinourstudywerefilletedmanually,and thesmallerthefish,themorechallengingthefilletingbecame.

Table3showsthepercentagedistributionofthebodyfractionsof lumpfishfrombothbatches.Alllumpfishwerejuvenile,asnomature gonadsweredetected.InBatch1,thefractionsoffilletsandskinwere slightlylowerthanthecorrespondingvaluesforBatch2.Challengesdue tomanualfilletingandthesizevariationsoflumpfish,mayexplainthese differences.Thefilletfractionsobtainedinthisstudy(from15to19%) wereaboutthesameaspreviouslyreportedbyReykdaletal.(2012)and Ólafssonetal.(2009),14and23%oflumpfishbody,respectively.The fractionoftheviscerainlumpfishfromBatch1wastwiceasbigasfor Batch2,19and8%,respectively.Probably,thedifferencewascaused byfeedremainsinthestomachsinfishfromBatch1.

Themajorfractionofallexaminedlumpﬁshconsistedofheadand skintogether,about47and53%inBatch1andBatch2,respectively.

This ishighercomparedtoafractionofabout40%aspreviouslyre- portedbyReykdaletal.(2012)andÓlafssonetal.(2009)butalmost

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Table2

Methodsforanalysesapplied.

Analyte Principle Refs.

Moisture Gravimetric analysis AOAC (2000) method 950.46

Ash Gravimetric analysis AOAC (2000) method 950.46

Fat Pulsed NMR Fiebig and Lüttke (2003)

Protein N ×6.25, Leco TruMac N analyzer Hamre and Mangor-Jensen (2006) Total Amino acids Ion exchange chromatography EU, (2009)

Fatty acids Transmethylation extraction and GC/FID ISO 12966-2:(2011

Vitamin A HPLC ISO 14565:(2000)

Vitamin E HPLC ISO 6867:(2000)

Vitamin B1 HPLC EN 14122:(2014)

Vitamin B9 SPR and HPLC Mæland et al. (2000)

Vitamin B12 HPLC Vyas et al. (2012)

Vitamin D3 HPLC EN 12821:(2009)

Heavy metals ICP-SFMS ISO 17294-2:(2016)

PCDD/Fs + PCBs + dl-PCBs HRGC/HRMS CSN EN 16190 (2018) GC/FID:gaschromatography/ﬂameionizationdetector.

HPLC:highperformanceliquidchromatography.

SPR:surfaceplasmonresonance.

ICP-SFMS:inductivelycoupledplasmasectorﬁeldmassspectrometry.

HRGC/HRMS:highresolutiongaschromatography/highresolutionmassspectrometry.

PCDD/Fs:polychlorinateddibenzodioxins/furans;PCB,polychlorinatedbiphenyls;dl-PCBs:dioxin-like PCBs.

Table3

Percentagedistributionofthebodyparts oflumpﬁsh,Batch1,n=5,andBatch2, n=10.

Fraction

Batch 1 Batch 2 264 ± 73 g ¹ 513 ± 84g ¹ Head (%) 18 ± 2 18 ± 1 Skin (%) 29 ± 5 35 ± 3 Fillet (%) 15 ± 5 19 ± 2 Bones (%) 13 ± 3 15 ± 2 Viscera (%) 19 ± 5 8 ± 1 1Bodyweight(averageweight±SD).

similartoabout50%,whichwasreportedbyParadisetal.(1975).The weightsofthefishusedinthosethreestudiesrangedfromabout1to 4.5kg,whiletheweightofthefishinourstudywasrelativelylower, whichisassumedtobethesourceofdifferences.Thelargefractionsof headandskinmaybeanissuewhenconsideringprocessingoptionsfor thelumpfish.

Traditionally, wild lumpfish have been harvested for their roe, which can be processed into a substitute for caviar, while the re- mainedbodyfractionsoftenarehandledaswaste(Davenport,1985; Johannesson,2006;Paradisetal.,1975;Powelletal.,2018).Insome countries,however,the lumpfishbody fractionsareused forhuman consumption.Forinstance,Icelandexportsfrozenlumpfish toChina (Þórðarsonetal.,2018).InRussia,thewildlumpfishfilletsarepopular ashot-smokedproductsorcannedfood(Nord-West,2021).

AccordingtoNøstvoldetal.(2016),thewholesmall-sizedlumpfish couldbeexportedtoAsia,whereconsumptionofportion-sizedwhole fish(withskin,bones,head,andviscera)iscommon.Anotheroptionis cuttingthefishfromtheventtotheneck,acrossthestomach(commonly referredtoas"Japanesecut"(VoldaUniversityCollege,Møreforsking Marine,ÅlesundHighSchool,SUROFI,TheNorwegianFishermen’sAs- sociation,2013).AJapanesecutsimplifiestheprocessingastraditional filletingofthesefishischallengingandtime-consuming.Apartfromthe Japanesecut,allfins(includingcaudalfin)andskinwereremoved,giv- ingaskinnedcarcassyieldofabout28and34%inBatch1andBatch 2,respectively.Itisworthmentioningthatthethicknessandelasticity oftheskinenabledeasymanualremoval.Besides,inouropinion,the

skinnedlumpfishcarcassappearsmoreappealingandsimilartoother fishspecies.Ifthelumpfish(afterbeingusedascleanerfish)shouldbe processedforotherpurposesthanensilage,thisproductmightbecon- sidered.

3.2. Proximatecomposition

Several factors can aﬀect ﬁsh species’ proximate composition, for instance, body size, season, feed access, and feed composition (Ageevaetal.,2017;Breck,2014;Joblingetal.,2008).

Theproximatecompositionsofthefeedsgiventolumpfishduringthe netcageperiodandlumpfishsamplesfrombatches1and2areshownin Table4.Allsamplesoflumpfishhadhighwatercontent(87.5–92.2%) andlowrangesofprotein(5.3–7.41%).Wholefish,skin,andguttedfish withhead,hadahigherashcontentthanfilletsfrombothbatches.This isexpectedasthecontentsofmineralsandtraceelementsarehigherin bonesandskinthaninmuscle(Lorentzenetal.,2001).

ThefatcontentinfilletsfromBatch1and2was3.7and0.9%,respectively.Basedonthefatcontentinthefeedsapplied,thedifferences arenotlikelytobelinkedtodifferencesofthefeedsasthesearenearly similar.TheresultsmayindicatethatthefishfromBach2wasnotfed sufficientlydespitebeing offered feed daily.Otherresearchersregis- teredanincreaseinfatcontent(from≈2.8to≈4.2%)infarmedlump- fishafterbeingkeptinanetcagewithsalmonforaboutsevenmonths (Espmarketal.,2020).Duringthisperiod,thelumpfishgainedweight from30to50gto230to500g.Theyconcludedthatthefishwerefed sufficiently,notnecessarilyonlycleanerfishfeedbutalsoplanktonand salmonpellets,enablingthemtobuild upthefatreserves.Ourstudy showsthattheproximatecompositiondependsonthefeedingregimen andgeneralaccesstofeedduringtheperiodinthenetcage.

3.3. Fattyacidcompositionandnutritionalevaluation

Table5givesanoverviewoftheamountsoftheprimaryfattyacids (FA)inlumpfishfromBatch1(wholefish)andBatch2(guttedwith head).Despitethedifferenceinthetypeofsamples,thetotalFAdistri- butionwasnearlysimilarinbothbatches.Thepercentageofsaturated FA(SFA)rangedfrom19.7to20.8%,monounsaturatedFA(MUFA)from 34.5to37.1%,andpolyunsaturatedFA(PUFA)from31.6to34.4%.

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Table4

Proximatecompositions(%)ofthefeedsgiventothelumpfish,LumpfishGrower20mgandCLEANLumpfish2– 4mm.Proximate compositions(%)andenergyofsampledlumpfish,Batch1,andBatch2.

Element Batch 1 Batch 2

Lumpfish Grower 20 mg ¹ Whole fish Fillet Skin CLEAN Lumpfish 2 – 4 mm ¹ Gutted with head Fillet

Ash 12 1.6 1.2 1.5 10.5 1.5 0.5

Water 8 91.5 87.5 92.1 n.a. 92.1 92.2

Protein 48 5.7 7.41 6.3 57 5.3 6.5

Fat 12 1.3 3.7 0.9 15 0.7 0.9

Energy (kcal/100g) 34 64 33 29 33

Energy (kJ/100g) 144 266 141 121 140

n.a.– notavailable.

1LumpﬁshGrower20mg(BioMar,2019);CLEANLumpﬁsh2–4mm(Skretting,2021).

Table5

Fattyacid(FA)fraction(%oftotalFA),andamountofFA(mg/g)inlumpﬁsh, Batch1andBatch2.

Fatty

acid Batch 1 (Whole ﬁsh) Batch 2 (Gutted with head) Fraction (%) Amount (mg/g) Fraction (%) Amount (mg/g)

14:0 2.7 0.4 4.5 0.3

16:0 14.0 1.8 10.9 0.8

18:0 4.1 0.5 4.3 0.3

16:1n-7 5.1 0.7 4.4 0.3

18:1n-9 25.6 3.3 16.9 1.2

20:1n-9 2.5 0.3 8.8 0.6

22:1n-9 1.3 0.2 7.0 0.5

18:2n-6 (LA) 10.8 1.41 5.0 0.4

18:3n-3 (ALA) 1.8 0.23 2.2 0.2

18:4n-3 1.0 0.13 2.0 0.1

20:2n-6 0.3 0.04 0.3 0.02

20:5n-3 (EPA) 8.3 1.08 9.0 0.6

22:5n-3 1.3 0.16 0.9 0.1

22:6n-3 DHA) 10.9 1.42 12.2 0.9

ΣSFA 20.8 2.7 19.7 1.4

ΣMUFA 34.5 4.5 37.1 2.6

ΣPUFA 34.4 4.5 31.6 2.3

Σn-3 23.2 3.0 26.3 1.9

Σn-6 11.1 1.5 5.3 0.42

n-6/n-3 0.5 0.2

LA:linoleicacid;ALA:alpha-linoleicacid;EPA:eicosapentaenoicacid;DHA:do- cosahexaenoicacid; SFA:saturated fatty acids;MUFA: monounsaturated fatty acids;PUFA:polyunsaturatedfattyacids.

Palmiticacid(16:0)dominatedintheSFAinbothbatches,witha slightlyhigherlevelinBatch1thaninBatch2.Thediﬀerenceincon- tentofpalmiticacidcouldbeexplainedbythelumpﬁshinBatch1not beinggutted.IthasbeenreportedthatpalmiticacidisadominantSFAin bothwildandfarmedcod(Jensenetal.,2013),salmon(Jensenetal., 2020),andotherseafoodspeciescaughtintheNortheasternMediter- raneancoast(Durmuş,2018).

Oleicacid(18:1n-9)wastheprimaryFAandtherebythemajorcon- tributortotheMUFA.OleicacidisthemostcommonMUFAinplants andanimals(Lund&Rustan,2020;Tvrzickaetal.,2011).

ThefractionofEFA linoleicacid(LA, 18:2n-6)wastwice ashigh inlumpfishfromBatch1(10.8%)comparedtoBatch2(5%).Thefish inBatch1wasnotgutted,whichisassumedtoexplainthedifference.

Thepercentageof𝛼-linoleicacid(ALA,18:3n-3)wasnearlythesame in bothbatches,1.8and2.2% inBatch1andBatch2,respectively.

LAisobservedatlowlevelsinfishoils(<2%)whileextensiveinveg- etableoils.Thus,LAandALAcanbeusedasmarkerstoverifyifthe fishhasbeenofferedvegetableoils(Lund&Rustan,2020;Olsen,2017; Tvrzickaetal.,2011).TheLAandALAlevelsindicateelevatedlevelsof vegetableoilsinthefeed.Nowadays,itisastandardproceduretoapply vegetableoilswhenmakingfishfeeds,anditisknownthatthedietary lipidcompositionofthefeedreflectsthetotalFAcompositionoffish (Joblingetal.,2008;Olsen,2017;Ytrestøyletal.,2015).Forinstance, thepercentageofLAinfarmedcod(4%)canbefourtimeshigherthan inwildcod(1%)(Jensenetal.,2013).

Thepercentagesofconditionally-EFAdocosahexaenoicacid(DHA, 22:6n-3)werealmostsimilarinbothbatches,about11and12%inBatch 1andBatch 2,respectively. Recommendations forminimum dietary intakeofEicosapentaenoicacid(EPA,20:5n-3)andDHA(EPA+DHA) rangesbetween250and450mg/day(Tvrzickaetal.,2011).Theresults suggestthatabout170goflumpﬁsh(guttedwithhead)wouldprovide 250 mgEPA+DHAandcovertherecommendeddietarydailyintake.

Toimprovethebeneﬁcialeﬀectsofthedietonhumanhealth,itisalso recommendedtoreducethen-6/n-3FAratio.Then-6/n-3ratioofthe westerndietisabout15–17/1(Jensenetal.,2013;Simopoulos,2008).

However,theratioshouldbefiveorfewer(Olsen,2017).Then-6/n-3 ratioswere0.5inlumpfishfromBatch1and0.2inlumpfishfromBatch 2,respectively.Bothratioswerelow;hence,theconsumptionoflump- fishcouldcontributetoareductionofthen-6/n-3ratiooftheregular diet.

3.4. Aminoacids(AA)proﬁleandproteinquality

Table6showsthetotalAAcompositioninthewholelumpﬁshfrom Batch1.

Theresultsindicatethatlumpﬁshcontainsallessentialaminoacids (EAA),andthepercentageofEAAis36.0%.Itisstatedthatameantotal proteinreqirementconsistsof27%EAAand73%non-EAA,andhealthy adultsrequireapproximately0.66gofproteinperkgbodyweightper daytomaintainbodynitrogenhomeostasis(FAO/WHO/UNU,2007).

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Fig.1. Essentialaminoacidsin proteinof lumpﬁshrelativetothe estimatedrequire- mentsinadultssetbyWHOwhentherefer- encelevelissetto100%.His– Histidine,Thr – Threonine,Val– Valine,Ile– Isoleucine, Leu– Leucine,Lys– Lysine,Met– Methion- ine,Phe+Tyr– PhenylalanineandTyrosine aresummarized.

Table6

Totalaminoacidcompositioninwhole lumpﬁsh,Batch1.

Amino

acid Batch 1 (Whole ﬁsh) mg/g

Essential amino acids Histidine 1.6 Threonine 2.4

Valine 2.9

Isoleucine 2.6 Leucine 3.2

Lysine 3.2

Methionine 1.5 Phenylalanine 2.9 Tryptophan ¹ n.a.

Conditionally essential amino acids Tyrosine 0.9

Glycine 9.2 Arginine 4.9 Proline 4.0 Non-essential amino acids

Serine 3.4

Alanine 4.2 Cysteine 0.5 Aspartic acid 4.6 Glutamic acid 6.9

ΣTAA 58.9

ΣEAA 21.2

% EAA 36.0

TAA:totalaminoacids.

EAA:essentialaminoacids.

n.a.– notanalyzed.

1Tryptophanisdecomposedduring hydrolysiswith6Mhydrochloricacid.

AmongtheEAAs,thelevelsofhistidine(His)andmethionine(Met)were thelowest(approximately1.5mg/g),threonine(Thr)andisoleucine (Ile)slightlyhigher(near2.5mg/g),valine,leucine,lysine,(Val,Leu, Lys)andphenylalanine(Phe)atthehighest(approximately3mg/g).

Toevaluatethedietaryproteinquality,acomparisonwitha"referenceprotein"forhumansissuggestedbytheWorldHealthOrganization (WHO)(Damodaran,2008;FAO/WHO/UNU,2007).Referenceprotein includestheminimumrequiredamountofEAAs.Bycalculatingthera- tiobetweeneach EAAbothinadietaryproteinandinthereference protein,acomparisonisenabled.AnAAgivingthelowestvalueisthe

mostlimitingAA.High-qualityproteinsincludeallEAAatlevelsabove the"reference"levelof100%.

Fig.1showsthepercentagecomparisonofeachEAAinlumpfishand thesimilarEAAintheWHOreferenceproteinwhenthereferenceEAA levelissetto100%.OnlyLeuwasslightlylowerinlumpfishthantheref- erencelevel,whichisassumedtoberelatedtothesamplingmethod(see chapter2.2.).However,lumpfishproteinprovidesasufficientamount oftheremainingEAAs,especiallyHis,Thr,Ile,Met,andPhe.Theresults suggestthatlumpfishproteinsareofgoodqualityandcanbeapplied forhumanconsumption.However,moreresearchisneededtoobtainin- formationaboutthedigestibilityandthequalityofproteins,especially fromlumpfishfillets.

3.5. Vitamins

Table7showsthelevelsofselectedvitaminsinlumpﬁsh(Batch1, guttedwithhead).VitaminsAandB9werebelowtheminimumdetec- tionlimits,<60.0μg/100gand<25.0μg/100g,respectively(datanot shown),whiletheremainingvitaminswereabovethedetectionlimit.

Forcomparisonpurposes,theEU recommendedlevelsforPopulation ReferenceIntakes(PRIs)ortheAdequateIntake(AIs)areadded.

ItappearsthattheanalyzedlumpﬁshisasourceofvitaminB12.For example,adailyintakeof220gmeetsthevitaminB12requirement for humans(Table7).VitaminB12ismainlyfoundinadiet ofani- malorigin,andseafoodisaparticularlygoodsourceinthetypicaldiet (NordicCouncilofMinisters,2014).

VitaminD3wasanalyzedinlumpfish(guttedwithhead)fromBatch 2,whichwereolderandhadbeenfedwithdifferentfeedscomparedto lumpfishinBatch1(seechapter2.1).WildfishgetvitaminD3through diet (planktonor otherfish),andfarmedfish mustbefedwithfeed containingadequatelevelofvitaminD(Waagbø etal.,2001).Itseems thattheanalyzedfishcouldbeagoodsourceforvitaminD3,andbased onthePRI,160glumpfishcouldprovidethedailyrequirementfora healthyperson(Table7).

TheconcentrationsofvitaminB1andvitaminB3inlumpfishwere higherthanthecorrespondingAIs(Table7),thelatterwasstilllower thanthetolerableupperintakelevel(ULs)(EFSANDAPanel,2014).Re- gardingvitaminB1,therearenoreportsofadverseeffects,evenatdaily dosesuptoseveralhundredmilligrams(EFSA,2006).Duetothelack ofscientificreportsondose-responseintakeandextremelylowtoxicity, noULofvitaminB1wasendorsed(EFSA,2006).

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Table7

Vitaminsinlumpﬁsh(guttedwithhead,Batch1)accompaniedwithEUrec- ommendedintake-levels,PopulationReferenceIntakes(PRIs)andAdequate Intakes(AIs),formalesandfemales(≥18yearsold).PRIsareinplainand AIsinboldtype.

Vitamin

Batch 1(Gutted with head) Unit

PRI / AI ¹

Unit Males Females

E 1.26 mg/100g 13 11 mg/day

B1 ² 1.2 mg/MJ 0.1 0.1 mg/MJ

B2 0.2 mg/100g 1.6 1.6 mg/day

B3 (total) ² 5.3 mg/MJ 1.6 1.6 mg/MJ

B6 0.05 mg/100g 1.7 1.6 mg/day

B12 1.8 μg/100g 4.0 4.0 μg/day

D3 ³ 9.2 μg/100g 15 15 μg/day

1 PRIisthedailydietaryintakelevelthatissuﬃcienttomeetthenutrient requirementof97.5%ofhealthyindividualsinaparticularstageoflifeand gendergroup(EFSA,2017).AIistheaverageobservedorexperimentally determinedestimatesofnutrientintakebyagroupofhealthypeopleas- sumedtobesatisfactory.AIisusedwhenthereisnosuﬃcientinformation toestablishaPRI.

2 ForvitaminB1andvitaminB3,thePRIsareexpressedasamountsper MJofcaloriesconsumed.MJ=megajoule=239kcal.VitaminB3(niacin) 0.64mg/100g=5.3mg/MJ.VitaminB10.14mg/100g=1.2mg/MJ.

3 VitaminD3wasanalyzedinlumpﬁsh(guttedwithhead),Batch2.Vi- taminD33.68IU/g=9.2μg/100g.Underconditionsofassumedminimal cutaneousvitaminDsynthesis.Inthepresenceofendogenouscutaneousvi- taminDsynthesis,therequirementfordietaryvitaminDisloworcanbe evenzero.

Table8

Mineralsinlumpﬁsh(wholeﬁsh,Batch1)accompaniedbyPopulation ReferenceIntakes(PRIs)andAdequateIntakes(AIs),formalesandfemales(≥18yearsold).PRIsareinplainandAIsinboldtype,respectively.

Mineral

Batch 1

(Whole ﬁsh) Unit

PRIs and AIs ¹

Unit Males Females Macrominerals

Na 324 mg/100g n.d. n.d.

P 292 mg/100g 550 550 mg/day

Ca 232 mg/100g 1000 ² 1000 ² mg/day

K 150 mg/100g 3500 3500 mg/day

Mg 21.8 mg/100g 350 300 mg/day

S 81.5 mg/100g n.d. n.d.

Microminerals

Se 22.5 μg/100g 70 70 μg/day

Mo 3.35 μg/100g 65 65 μg/day

V 0.755 μg/100g n.d. n.d.

Zn 0.695 mg/100g 16.3 12.7 mg/day

Fe 0.348 mg/100g 11 16 mg/day

Mn 0.101 mg/100g 3.0 3.0 mg/day

Cu 0.048 mg/100g 1.6 1.5 mg/day

n.d.– notdetermined.

1PRIisthedailydietaryintakelevelthatissuﬃcienttomeetthenu- trientrequirementof97.5%ofhealthyindividualsinaparticularstage oflifeandgendergroup(EFSA,2017).AIistheaverageobservedor experimentallydeterminedestimatesofnutrientintakebyagroupof healthypeopleassumedtobesatisfactory.AIisusedwhenthereisno suﬃcientinformationtoestablishaPRI.

2Agegroup≥18-24years.Foragegroup≥25yearsthePRIofCais 950mg/daybothformalesandfemales.

4. Minerals

Table8showsthecontentofmacromineralsandmicromineralsin lumpﬁshfromBatch1(wholeﬁsh).Likevitamins,thecontentsofdif- ferent minerals were evaluated based on PRIs and AIs. Nickel(Ni), Cobalt(Co),andChromium(Cr)werebelowthedetectionlimits,<0.02,

< 0.004 and < 0.02mg/kg, respectively (data not shown). Sodium (Na)wasthemajorconstituentinthelumpﬁsh.AccordingtoEuropean

Table9

Environmentalpollutantsandheavymetalsinwholefarmedlumpﬁsh.

Compound

Batch 1 EU maximum levels Unit Whole lumpﬁsh Wet weight ﬁsh ¹

Sum ICES-6 PCBs ² 1.1 75 ng/g

Sum TEQ 12 dl-PCBs ³ 0.22 6.5 ⁵ pg/g

Sum TEQ 17 PCDD/Fs ⁴ 0.25 pg/g

Hg 0.00438 0.5 mg/kg

Pb 0.0161 0.3 mg/kg

Cd 0.00692 0.05 mg/kg

As 0.255 mg/kg

1Whereﬁshareexpectedtobeeatenwhole,themaximumlevelapplies tothewholeﬁshEU,2006,EU,2011).

2SumICES-6PCBincludesPCB28,52,101,138,153,and180.

3SumTEQ12dl-PCBincludesPCB77,81,105,114,118,123,126, 156,157,167,169,and189.

4Sum TEQ 17 PCDD/PCDF includes 2378-TCDD, 12378-PeCDD, 123478-HxCDD, 123678-HxCDD, 123789-HxCDD, 1234678-HpCDD andOCDD; 2378-TCDF, 12378-PeCDF, 23478-PeCDF, 123478-HxCDF, 123678-HxCDF, 123789-HxCDF, 234678-HxCDF, 1234678-HpCDF, 1234789-HpCD,OCDF.

5SumofPCDD/Fsanddl-PCBs.SumofPCDD/Fsis3.5pg/gwetweight.

FoodSafetyAuthority(EFSA)(EFSANDAPanelEFSAPanelonNutri- tion,NovelFoodsandFoodAllergens,2019),nosufficientdatatoen- dorseNa’srecommendedlevelintakeisgiven.However,theEFSApanel consideredthattheNaintakeof2.0g/daywassufficienttoreduceriskof cardiovasculardiseasesandtomaintaintheNa-balanceformostadults, includingpregnantandlactatingwomen.Inthatcontext,alumpfishof 250gmaycontributewithonly0.8gNaandcouldtherebybeconsid- eredsuitableforlow-sodiumdiets.Thisisnotsurprising,asingeneral, theNacontentinfishmuscleisrelativelylow(Huss,1995).

Assumingaconsumptionofa100glumpﬁsh,thecontentsof the macromineralsphosphorus(P),calcium(Ca),potassium(K),andmag- nesium(Mg)wereallbelowthecorrespondentPRIsorAIs(Table8).

However,byconsumingawholelumpﬁshof250g,thecontributionof P(730mg)ishigherthanthecorrespondingvalueforAI(550mg/day).

ThereisnoestablishedULforP,butitisindicatedthatnormalhealthy individualstolerateuptoatleast3000mgPperdayavoidingadverse eﬀects(EFSA,2006).Piscommonlyfoundinfoodasphosphates,especially in protein-richfoodslike ﬁsh(200mg/100g) (EFSA, 2006).

Sulfur(S)isabundantinnatureandisoftennotincludedasarequired micromineralinhumandiet.ThemostimportantsourcesofSaretwo sulfur-containingaminoacids,methionine,andcysteine,whichareused tosynthesizemostproteinsinthebody(Lorentzenetal.,2001).

Asregardsthemicrominerals,thecontentsofallcompoundsin100g lumpfishwerelowerthancorrespondedPRIsorAIs.Still,itseemsthat iflumpfishofabout250giseatenaswholefish,thecontributionof selenium(Se)(56.25μg)ismorethanhalfofthecorrespondedAI(70 μg/day),whichisencouraging.Vanadium(V)isnotconsideredessential forhumansandhasnonutritionalvalue,andthus,recommendedintake levelsarenotestablished(EFSA,2004).

4.1. Environmentalpollutantsandheavymetals

Theenvironmentalpollutantsandheavy metalsdetectedinlump- fishfromBatch1(wholefish)areshowninTable9.Thelevelsofenvi- ronmentalpollutantswerelow,andinsomecases,belowthedetection limit.Infact,theSUMICES-6PCBsandtheSUMTEQ12and17,were68 and30timesbelowtheEUmaximumlevelforfishmuscle(EU,2011).

Thelevelsoftheheavymetalsmercury(Hg),lead(Pb),andcadmium (Cd)inthelumpﬁshsampleswere116,18,and7timeslowerthanthe EUmaximumlevels(EU,2006).Thearsenic(As)analyzedreferstothe totallevel,notdistinguishingbetweenorganicandinorganic.Approxi- mately97-99%ofthetotalamountofarsenicfoundinﬁshandseafood

(7)

isfoundasorganiccompounds.Thisformisnotharmfulforhumanor ﬁshhealth(Cubaddaetal.,2017).

5. Conclusions

Toevaluatethe usabilityof anew foodresource, a screening of potentialpositiveandnegativepropertiesisconsideredvaluable.Posi- tiveattributesincludeaprevalenceofvitamins,essentialaminoacids, andfattyacids,whilenegativeattributesarecommonlyassociatedwith PCBsandheavy metals.Also,thetechnicalaspectsandtheabilityto processarerelevant.Thelumpﬁshinvestigatedhadhighwatercontent andlowproteincontent.However,theproteinwasofgoodqualityand agoodsourceforallessentialaminoacids.Thefatcontentvariedbe- tweenthebatchesinthisstudy,indicatingavariationdependentonthe handlingandfeedingregimenduringthenetcageperiod.

Thefattyacidcompositionisconsideredbeneficialconcerningthe EPAandDHAcontent.Providedadailyconsumptionof170glumpfish, therecommendeddailydietaryintakeof250mgofEPA+DHAwillbe covered.Furthermore,itappearsthatlumpfishcouldbeagoodvita- minsource.Forinstance,160-220glumpfishcouldsupplythedaily requirementforhumansofvitaminsD3andB12.Thecontentsofsev- eralmineralswerelow,andthefishcouldbeconsideredsuitablefor low-sodiumdiets.Thecontentsofenvironmentalpollutantsandmetals werelowerthantheestablishedEUmaximumlevels,makingthelump- fishasafeproductforhumanconsumption.

Theprocessingoflumpﬁshmaybechallengingasthelumpﬁshhave analmostsphericalbodyshape,withalargefractionofheadandskin.

Ifthelumpfish(afterbeingusedascleanerfish)shouldbeprocessedfor purposesotherthanensilage,smalllumpfishcouldbeusedasawhole orasaproductskinnedcarcass.Inouropinion,thelatterhasamore ordinaryandattractiveappearance.

However,itisessentialtomentionthattheresultspresentedcov- erstwobatchesandshouldtherebybeconsideredasindicative.Cor- respondinganalysesfromseveralaquaculturefacilitiesshouldbeper- formedaimingatthebigpictureofvariation.Also,thescreeningand characterizationoflumpfish shouldbe conductedboth onindividual fishandpooledsamples.Inaddition,ifthefishistobeconsideredfor consumptionasawholefish,feeddeprivationbeforeslaughtermustbe considered.Theresultspresentedinthisstudyareconsideredpromis- inginviewofpossibilitiesforimprovedafter-useasanalternativeto theusetoday.

Funding

The results presented are deliverables from the projects "Lump- ﬁsh4Food" and "CleanCatch". The corresponding projectshave been fundedbytheResearchCouncilofNorway[NFR,grantno.301494], andFHF-NorwegianSeafoodResearchFund[FHF,grantno.901560].

DeclarationofCompetingInterest

Theauthorsdeclarethattheyhavenoknowncompetingﬁnancial interestsorpersonalrelationshipsthatcouldhaveappearedtoinﬂuence theworkreportedinthispaper.

CRediTauthorshipcontributionstatement

TatianaN. Ageeva: Conceptualization, Methodology, Validation, Investigation,Resources,Visualization,Writing– originaldraft,Writing – review&editing.GreteLorentzen:Supervision,Validation,Investi- gation,Writing– originaldraft,Writing– review&editing. HeidiA.

Nilsen:Supervision,Validation,Investigation,Writing– originaldraft, Writing– review&editing.KjerstiLian:Conceptualization,Methodol- ogy,Validation,Investigation,Resources,Visualization,Writing– originaldraft,Writing– review&editing.

Acknowledgments

TheauthorswouldliketothankHanneMæhre(NoﬁmaAS)forsu- pervisionduringvalidationofproteinquality.

References

Ageeva, T. N., Jobling, M., Olsen, R. L., & Esaiassen, M. (2017). Gender-speciﬁc responses of mature Atlantic cod (Gadus morhua L.) to feed deprivation. Fisheries Research, 188 , 95–99. 10.1016/j.ﬁshres.2016.12.010 .

BioMar. (2019). Datasheet: Rognkjeks, Lumpﬁsh Grower 20mg . Norway: BioMar . Breck, J. E. (2014). Body composition in ﬁshes: Body size matters. Aquaculture, 433 , 40–

49. 10.1016/j.aquaculture.2014.05.049 .

Brooker, A. J., Papadopoulou, A., Gutierrez, C., Rey, S., Davie, A., & Migaud, H. (2018).

Sustainable production and use of cleaner ﬁsh for the biological control of sea lice: Recent advances and current challenges. Veterinary Record, 183 (12) 383-383.

10.1136/vr.104966 .

Chandra, A., Røsjø, H., Eide, I. A., Vigen, T., Ihle-Hansen, H., Orstad, E. B., Rønning, O. M., Lyngbakken, M. N., Berge, T., & Schmidt, E. B. (2019). Plasma marine n-3 polyunsat- urated fatty acids and cardiovascular risk factors: Data from the ACE 1950 study.

European Journal of Nutrition , 1–11. 10.1007/s00394-019-02007-3 .

CSN EN 16190. (2018). Soil treated biowaste and sludge - Determination of dioxins and furans and dioxin-like polychlorinated biphenyls by gas chromatography with high resolution mass selective detection . European Standards https://www.en-standard.eu/

csn-en-16190-soil-treated-biowaste-and-sludge-determination-of-dioxins-and-furans- and-dioxin-like-polychlorinated-biphenyls-by-gas-chromatography-with-high- resolution-mass-selective-detection-hr-gc-ms/ .

Cubadda, F., Jackson, B. P., Cottingham, K. L., Van Horne, Y. O., & Kurzius-Spencer, M (2017). Human exposure to dietary inorganic arsenic and other arsenic species: State of knowledge, gaps and uncertainties. Science of The Total Environment, 579 , 1228–

1239. 10.1016/j.scitotenv.2016.11.108 .

Damodaran, S. (2008). Amino acids, peptides, and proteins. In S. Damodaran, K. L. Parkin,

& O. R. Fennema (Eds.), Fennema’s food chemistry. (pp. 217–329). CRC Press, Taylor

& Francis Group .

Davenport, J. (1985). Synopsis of biological data on the lumpsucker, Cyclopterus lum- pus (Linnaeus, 1758) . Food and Agriculture Organization of the United Nations http://www.fao.org/3/ap950e/ap950e.pdf .

Directorate of Fisheries. (2021). Cleanerfish (Lumpfish and Wrasse). Retrieved from https://www.fiskeridir.no/English/Aquaculture/Statistics/Cleanerfish-Lumpfish- and-Wrasse . Accessed April 19, 2021

Durmu ş , M. (2018). Fish oil for human health: Omega-3 fatty acid proﬁles of marine seafood species. Food Science and Technology, 39 (suppl 2), 454–461.

10.1590/fst.21318 .

EFSA. (2004). Opinion of the scientiﬁc panel on dietetic products, nutrition and allergies [NDA] related to the tolerable upper intake level of vanadium. EFSA Journal, 2 (3), 1–22. 10.2903/j.efsa.2004.33 .

EFSA NDA Panel (EFSA Panel on Dietetic Products, Nutrition and Allergies). (2014). Sci- entiﬁc opinion on dietary reference values for niacin. EFSA Journal, 12 (7), 3759.

10.2903/j.efsa.2014.3759 .

(2019). Scientiﬁc opinion on dietary reference values for sodium: 17(9) (p. 5778). EFSA Journal. doi:10.2903/j.efsa.2019.5778 .

EN 12821. (2009). Foodstuﬀs - Determination of vitamin D by high performance liquid chromatography - Measurement of cholecalciferol (D3) or ergocalciferol (D2) (CEN/TC 275) . European Committee for Standardization https://standards.cen.eu/dyn/www/

f?p = 204:110:0::::FSP_PROJECT,FSP_ORG_ID:27772,6256&cs = 1D597F7B81605 B657692E8499FFEB199E .

EFSA (2006). Tolerable upper intake levels for vitamins and minerals. Scientific Com- mittee on Food & Scientific Panel on Dietetic Products Nutrition and Allergies . Euro- pean Food Safety Authority https://www.efsa.europa.eu/sites/default/files/efsa_rep/

blobserver_assets/ndatolerableuil.pdf .

EFSA. (2017). Overview on the dietary reference values (DRVs) for the European Union pop- ulation as derived by the European Food Safety Authority Panel on Dietetic Products, Nu- trition & Allergies (NDA) (summary of dietary reference values – version 4 (September 2017)) . EFSA https://www.efsa.europa.eu/sites/default/ﬁles/assets/DRV_Summary_

tables_jan_17.pdf .

EN 14122. (2014). Foodstuﬀs - Determination of vitamin B1 by high performance liquid chromatography . European Committee for Standardization (CEN/TC 275) https://

standards.cen.eu/dyn/www/f?p = 204:110:0::::FSP_PROJECT,FSP_ORG_ID:35371, 6256&cs = 16A0010D4EC5A335FFA820611D07D89FC .

EN 14152. (2014). Foodstuﬀs – Determination of vitamin B2 by high performance liquid chromatography . European Committee for Standardization (CEN/TC 275) https://standards.cen.eu/dyn/www/f?p = CENWEB:110:::::FSP_ORG_ID,FSP_

PROJECT:6256,35372&cs = 18B4038E3E617D97B66EBAA7588ABC51F .

EN 14663. (2005). Foodstuﬀs – determination of vitamin B6 (including its glyco- sylated forms) by HPLC . European Committee for Standardization (CEN/TC 275) https://standards.cen.eu/dyn/www/f?p = 204:110:0::::FSP_PROJECT,FSP_ORG_ID:

22286,6256&cs = 1508A6973E4266B34D137507A0BDC32DE .

EN 15652. (2009). Foodstuﬀs - Determination of niacin by HPLC . European Com- mittee for Standardization (CEN/TC 275) https://standards.cen.eu/dyn/www/

f?p = 204:110:0::::FSP_PROJECT,FSP_ORG_ID:27776,6256&cs = 1575593E5D0157 E75CC20B786F8C76A52 .

Espmark, Å. M. O., Noble, C., Kolarevic, J., Berge, G. M., Aas, G. H., Tuene, S. A., Iversen, M. H., Wergeland, H. I., Johansen, L. H., & Burgerhout, E. (2020). Welfare in cleaner ﬁsh – operational welfare indicators (OWI) – RENSVEL . [in Norwegian]: Noﬁma