Accumulation of dietary fish fatty acids in the body fat reserves of
some
carnivorous fur-bearing animals
Kirsti Rouvinen,JaakkoMäkelä,Tuomo Kiiskinen andSeppoNummela
Rouvinen,K., Mäkelä, J.,Kiiskinen, T.&Nummela,S.1992.Accumulationof dietary fish fattyacidsinthe body fatreserves ofsomecarnivorousfur-bearinganimals.
Agric. Sei.Finl. I: 483-489. (Agric. Res. Centre ofFinland, Fur Farming Res. Sta., SF-69100Kannus, Finland,Finnish Fur Breeders’ Association,P.0.80x 5, SF-01601 Vantaa, Finland, Agric.Res. Centre ofFinland,Inst. Anim. Prod.,SF-31600 Jokioinen, Finland and Agric. Res. Centre ofFinland,Centr.Lab.,SF-31600Jokioinen,Finland.)
Bodyfatcompositionof themink (Mustela vison),polecat(Mustela putorius),and the raccoondog (Nyctereutes procyonoides)wasstudied. The animalswerefed awetdiet, supplemented with 5 %lard (LA) orfish oil (FO) for5-6months. Atpelting, five animals per dietarygroupweresampled. Dietarylevels of cetoleic (C22:1to11),eico- sapentaenoic(EPA, C20:5<03), and docosahexaenoic (DHA, C22:6c03) acidswere0.4, 0.3,and0.5% inthe fat of theLA diet,and7.6,4.2and4.3% inthe FO diet,respectively.
Inthe FO diet, EPAandDHA accumulated especially in the liver and heart, while cetoleic acid showed thehighest affinitytothe heart muscle and subcutaneous fat. The highest levels ofEPAwere foundinraccoon dogs andpolecats fed the FO diet. The meanEPAlevelsranged from6.7-9.3% inthe liver fat and7.2-8.0% inthe heart muscle fat. Inthe mink,the corresponding valueswere 2.7%and 3.9%,respectively. DHA levelswere thehighest inthe liver fat of thepolecats, being 18.5% inthe FO diet.In addition,the liverinraccoondogsfed the FO diet (13.8%) differed significantlyfrom themink(9.4%). The differencesinthe accumulation of theselong-chainedmarinefatty acidswere apparentlycausedby speciesdifferencesinthe efficiency of theirperoxi- somal (1-oxidation.
Keywords: ferret,mink,polecat,raccoondog,cetoleicacid,omega-3 fatty acids, liver, heart,subcutaneous fat
Introduction
In monogastric animals, dietary fat has a strong influence on the fatty acid composition of the tissues and organs. Feeding vegetable oils and fish oils to mink and blue foxes has been shown to increase the levels of linoleic and omega-3 fatty acids,respectively, in the fat depots and the liver of
the animals (Rouvinen and Kiiskinen 1989, Skrede and Gulbrandsen 1985, Skrede 1984, Ahman 1965). In blue and silverfoxes, feeding an abundance of fish fat is known tocauseprominent accumulation of the typical fish fatty acids, i.e.
cetoleic (C
22:
Icol 1), eicosapentaenoic (EPA, C20:5c03) and docosahexaenoic (DHA, C22:6c03) acids, in their subcutaneous fat, liver tissue and Agric. Sei.Fint. 1 (1992)heart muscle (Rouvinen 1991,Rouvinen 1992).
In the rat, feeding fish oil or high erucic acid (C22;1c09) rapeseed oil has been shownto cause lipid infiltration,cell destruction, local inflamma- toryreactions and fibrousscartissue growth in the heart muscle (Beare-Rogers 1977, Kjnsella 1987). Accumulation of these long-chained fatty acids in body tissues is apparently due to their impaired oxidation. The 20 or 22 carbon atom- chained fattyacids should first be shortened in the peroxisomes to 16or 18 carbon atom-fattyacids before they can be metabolized by the mitochon-
drial p-oxidation (Opstvedt 1984).
Thepresentpaperreports the effects of feeding lardorfish oil supplemented dietson the body fat composition ofsome farm-raised carnivorous fur- bearinganimals, mink,polecat and theraccoondog.
Material and methods
Mink (Mustela vison), polecats (Mustela putorius) andraccoondogs (Nyctereutes procyonoides)were fed diets based onslaughterhouse offal, fish offal and cereals supplemented either with lard (LA) or fish oil (FO), at5% in the diet. The animals used were all bora during the spring of 1988,and were raised accordingtonormal fur farming practicesat the Veikkola Research Farm of the Finnish Fur Breeders’ Association, Kirkkonummi. The trial lasted from July until pelting during theautumn of 1988. Composition of the experimental diets is presented in Table 1. Feed samples for chemical analysis were taken on August 23rd, and onSep- tember 30th. Fatty acid compositionwas analyzed from feed samples takenonNovember 30th.
Five animals per dietary groupwere electrically executed for samplingonNovember30th, 1988. At sampling, the age ofthe animalswasapproximately 6-7 months. The mink and polecatswereallmales, but the raccoon dogs included both sexes, two males and three females per group. The animals were weighed and sampled for liver fat analysis, and samples for fatty acid analysisweretaken from
Table 1.Compositionofexperimentaldiets fromweaning to pelting 1988. LA=larddiet,FO=fish oil diet.
Diet
Ingredient,% LA FO
Slaughterhouseoffala) 15 15
Fish offal 30 30
Fish meal 1 1
Soybeanmeal 0.5 0.5
Comgluten I 1
Blood meal 1 1
Cerealsb) 13 13
Vitamins0* 1.5 1.5
Lard 5
Fish oil - 5
Water 32 32
a)LSOslaughterhouse,Forssa
1,1cooked cereal: wheat50%andbarley 50%.
c)1 kgmixturecontains;vitaminA, 500 000 IU;vitamin Ds, 50 000 IU;vitamin C,6 000mg; vitaminE,4 000mg;
vitaminK, 10mg; vitaminBi, 1 500mg; vitamin82,600 mg; vitamin812, 1mg;choline, 2 500mg;pantothenic acid, 500mg; nicotinicacid, 1 000mg;pyridoxin, 400mg;
folicacid, 50mg; andbiotin, 3mg.
the rump region of thecarcasses(subcutaneous fat), the liver and the heart. The weights of the sampled organs were also taken. The feed, tissue and fat samples were stored at-30°C until analyzed be- tweenJanuary 4th and March 13th, 1989.
The experimental diets were analyzed for dry matter(DM),ash,Kjeldahl nitrogen and crude fat.
The analyses wereperformed by the Feed Laborat- ory of the Finnish Fur BreedersAssociation,Vaasa.
Fatty acid composition of the diets and the tissue samplesweredetermined in the Central Laboratory of the Agricultural Research Centre of Finland. The method employed is described in detail by Rou-
vinen(1991). The liver fatcontentwasdetermined by the method of Maxwell etal. (1980) at the laboratory of the Institute of Animal Production, Animal NutritionSection, Jokioinen.
Statistical analysiswasperformed by the General Linear Models (GLM) procedure of the Statistical
Analysis System (SAS 1988). The model usedwas asfollows:
Agric. Sei.Fin!. 1(1992)
Yijk
n
+Sj+Dj+SDjj+ Cijkwherep is the generalmean,Sjis the species effect
(/ = 1-3), Dj is the dietary effect (j = 1-2), SD.j represents the species diet interaction andeijkis the errorterm. Differentiation among themeanvalues was done by Duncan’s multiple-range test. There were no statistical differences (p>0.05) between sexes in the fatty acid composition of the tissue samples taken from theraccoon dogs, therefore the meansgivenrepresent pooled data from bothsexes.
Results
Chemical composition of the experimental diets was similar in lard (LA) and fish oil (FO) sup- plemented groups (Table 2). Dietary fatcontentwas high, 27-30% inDM,which accounted for approxi- mately 50% of the metabolizable energy in both dietary groups.
Dietary fatty acid composition showeda great difference between the lard and fish oil sup- plemented diets (Table 3). The lard diet contained morestearic (C18;0) and oleic (C 18:1
co
9)acids,butin the fish oil diet the content of cetoleic (C
22:
Icol 1), eicosapentaenoic (C20:5c03) and do-Table2.Chemicalcompositionof the dietsduringthegrowth period 1988.DietssampledonAug.23rd andSept.30th.
LA=lard,FO=fishoil, DM=drymatter.
Diet
August September
Analyzed LA FO LA FO
DM,% 30.2 30.1 31.2 30.9
In DM,%
Ash 7.3 6.6 6.4 7.4
Protein 31.1 33.9 30.8 35.0
Fat 29.1 28.6 30.4 26.9
Carbohydrates10 32.5 30.9 32.4 30.7
a)calculatedasdifference.
cosahexaenoic (C22;6c03) acids was considerably higher.
Body weights of the animals and the weights of the liver and the heart did not differ between the dietarytreatments.The body weights for themink, polecats and the raccoon dogs were on average 2249 g, 2055 g, and 8709 g. The average weights of the liver and (heart) were 48.6 g, (10.6 g), 57.9 g, (8.5 g), and 208.7 g (32.7 g) for the mink, polecat and theraccoon dog, respectively. There were no species diet interactions.
Clear species differenceswerefound in the liver fat contentand body fat composition of the animals (Table 4). Besides higher fat content in the mink livers the variation in the fatcontentwas consider- ably higher for this species. Dietary background of the animals didnotaffect the liver fatcontent.
The fatty acid composition of the tissue samples strongly reflected the fatty acid profile of the diet- ary fats in all species and in all fat and organ samples studied (Table 4).Furthermore,interesting
Table 3. Fattyacid compositionof the diets. Determination ofsamplestakenonNov.30th, 1988. LA=larddiet, FO=fish oil diet.
Fattyacids
°/n in fat
Diet
%infat LA FO
C14:0 2.5 5.3
C 16:0 26.1 22.8
24.0
C18:0 8.6
Saturated Cl6:lto7 C18:lto9 C20:1t09
36.9 52.9
2.4 5.4
22.6 33.7
1.0 6.6
C22:1c09+ll1) 0.4 7.6
Monounsaturated C18:3w3
42.8 37.7
1.3 0.8
0.2 1.7
C18:4c03 C20:5c03 C22:6<03 Omega-3 C18:2c06 C20:4c06 Omega-6
0.3 4.2
4.3 0.5
12.3 1.9
7.1 7.5
0.2 0.2
8.0 7.5
11erucic acid (C22:1c09) and cetoleic acid (C22:Icol 1) not separated inthefattyacidanalysis.
Agric. Sei.Finl. 1(1992)
Table4.Liver fat content and the content ofcetoleic, eicosapentaenoic and docosahexaenoic acids inthe livertissue,heart muscle and subcutaneous fat of themink,polecatand theraccoondogfed two differentdiets, LA=lard,FO =fishoil.
ND=notdetected. Presented are means± S.D.
Fatty acids Mink Polecat Raccoon dog Significance
%infat LA FO LA FO LA FO Species Diet S xD
Liver
Fat% 13.7 a 11.8 a 7.3 b 5.1b
±4.4 ±7.0 ±l.O ±0.6
C22:1w9+ll1) 0.2 d I.oa o.2cd 0.6b
±O.O ±O.l ±O.O ±O.l
C20:5c03 0.4
e
2.7 d 2.2 d 6.7 b±O.l ±0.9 ±0.4 ±l.l
C22:6c03 2.9 d 9.4
c
8.4c
18.5a
±0.6 ±2.2 ±1.4 ±0.9
Heart
C22:1(09+l1 0.2 d 2.5 b 0.4 d 1.5
c
±O.l ±0.7 ±0.2 ±0.2
C20:5c03 I.lc 3.9 b 2.9 b 7.2
a
±O,l ±1.2 ±0.7 ±0.5
C22:6c03 6.Bbc 7.9 b 7.9 b 11.4
a
±0.7 ±1.9 ±1.3 ±l.l
Subcutaneousfat
C22:1c09+1l 0.3
c
3.2 b 0.2c
3.5ab±O.l ±0.6 ±O.l ±0,5
C20:5<03 ND 0.9 b 0.3
c
1.5a
ND ±0.3 ±O.O ±0.2
C22:6t03 0.5 d 2.4
c
l.Od 4.2a
±O.l ±l.l ±O,l ±0.5
4.3b 4.9b <O.OOl NS NS
±0.2 ±0.4
ND 0.4c <O.OOl <O.OOl <O.OOl
ND ±O.O
4.1c 9.3a <O.OOl <O.OOl <O.OOl
±0.4 ±0.5
8.2c 13.8b <O.OOl <O.OOl <O.Ol
±1.6 ±l.O
0.4d 3.1a <O.OOl <O,OOl <O.OOl
±O.l ±0.5
1.6c B.oa <O.OOl <O.OOl <O.OOl
±0.7 ±l.l
2.2d 5.5c <O.OOl <O.OOl <0,05
±0.6 ±0.3
0.4c 3.9a NS <O.OOl NS
±O.l ±0.3
0.3c 1.5a <O.OOl <O.OOl NS
±O.l ±0.2
0.9d 3.2b <O.OOl <O.OOl <0.05
±0.3 ±0.3
a-e: meanswithinrows havingdifferentpostscriptsaresignificantlydifferent (p<0.05)11 seeTable3.
differences between the individual fish fatty acids in their affinity to certain fat depots in different specieswere observed. In the FO diet,cetoleic acid accumulated especially in the heart muscle and the subcutaneous fat, while its levels in the liver fat werecomparatively low. The highest levels ofceto- leic acid werefound in the heart and subcutaneous fat of theraccoon dogs. Moreover, in all species studied the accumulation of EPA and DHA was moreprominent in the liver and heart tissue than in the subcutaneous fat. The highest levels of EPA were found in the tissues of theraccoon dogs and polecats fed the FO diet. Inaddition, the polecats andraccoon dogs fed the FO diet had significantly
higher levels of DHA in their livers than did the mink or the corresponding animals receiving the LA diet. The DHA levels in heartwerethehighest in polecats fed the FO diet.
Discussion
Fatty acid profiles of the lard and fish oil sup- plemented diets differed greatly reflecting thecom- position of the supplemental fat. Both feed mixtures contained, however, aconsiderableamount of fish offal, which contributed toomega-3 fatty acids in both diets.
Agric. Sei. Fint. 1 (1992)
The accumulation of the polyunsaturated omega- -3 fatty acidswasprominent in the fish oil diet forall fur animal species included in this study. There were also significant species differences,polecats and raccoon dogs having remarkably higher con- tents of these fatty acids in their tissues and espe- cially in the liver than the mink. These resultsare in agreementwith earlier studies with mink and blue fox (Rouvinen and Kiiskinen 1989),and with blue and silver foxes (Rouvinen 1991, Rouvinen 1992). The blue foxes fed afish oil supplemented diet tendedto concentratemoreomega-3 fatty acids in their livers than the mink (ROUVINEN and KIIS-
KINEN 1989), while in silver fox livers the levels of these fatty acidswere evenhigher than in blue foxes when the animals were fed the same diet (ROU-
VINEN 1991, Rouvinen 1992). In the earlier study (Rouvinen 1991), the fat accumulationpatterndif- fered between the fish oil and saturated fat diets. In the fish oildiet, the fatwas present in the liver in small droplets, which was considered to be un- physiological. Inaddition,the degenerative change- sobserved were more numerousandsevere in this dietarygroup(ROUVINEN 1991).
It is interestingto notethat the levels of DHA in the liver and heart tissues werevery high also for the LA diet. This may suggestthat evenvery low amountsof dietary DHA will accumulate in these tissues. Inaddition, significant species differences could be observed with the lowestamountof DHA found in the liver of themink, whereas in the heart the lowest amount was found in theraccoon dog.
Moreover,despite equalamountsof DHA and EPA within bothdiets,the accumulation of DHAwas in nearly allcasesmuchmore severethan ofEPA. The 22 carbon chain of DHA could simply be more difficulttoshortento 16or 18 carbons comparedto EPA molecule with only 20 carbonatoms.
In therat, dietary erucic acid and its omega-11 isomer, cetoleic acid, have been shownto cause lipid infiltrationand tissuedegeneration in the heart muscle (Beare-Rogers 1977, Kinsella 1987).
Several cases of unexplained cardiac failure have recently been reported in Finnish silver foxes
(SMEDS 1992). In the 1980’s, during the years of intensive fox production, the dietary composition of thewetfiir animal feed has changed considerably.
Meat and slaughter offal based ingredients have been replaced by fish offal and industrial fish dueto theirmore affordable price. Moreover, the use of fish oilas acheap energy supplement has increased.
It is thus reasonable tobelieve that there may be a connection between theaccumulation ofthe long- chained marine fattyacids,especially cetoleicacid, in the silver fox heart tissue and the pathological condition observed. Supportto this hypothesis may also be found from a recent work on blue fox vixens, where long-term fish feeding priortobreed- ing and suckling period was showntoincrease pup mortality (ROUVINEN andNIEMELÄ 1992).
The key enzymes of the peroxisomal and mito- chondrial [3-oxidation are the fatty acyl-CoA oxi- dase (FAO) and carnitine palmitoyl transferase (CPT), respectively. Their activities reflect theca- pacities of the corresponding oxidation pathways (Moves etal. 1991). The peroxisomal (3-oxidation is known tobe induced when the diet contains high fat levelsorfatty acids whicharepoor substrates for mitochondria (MOVESetal. 1991). In species, such as seals and salmon, which normally encounter polyunsaturated fatty acids in theirdiets,the mito- chondria are, however, better capable to oxidize
long-chained unsaturated fatty acids (Movesetal.
1991). In the rat, feeding marine oils is known to induce the peroxisomal (3-oxidation. This is con- sideredtobe the response ofanomnivore to spe- cific fatty acids whicharenotnormally obtained in the diet. It is essentially a detoxification response (Movesetal. 1991).
It is very likely that the differences in the accu- mulation of the long-chained marine fatty acids found in the present studyare caused by species differences in the efficiency of the peroxisomal (3- oxidation. This is apparently a consequence of adaptationtocertain foodsources during the evol- utionary development of the different fur animal species (Nelson and Ackman 1988). Unlike the foxes (Dekker 1983,FayandStephenson1989),
Agric. Sei.Fin!. 1 (1992)
raccoon dog (Mäkelä and Kiiskinen 1978) and polecat (Fox 1988), the mink seems to be well capable of utilizing the long-chained polyunsatu- rated fatty acids due to its adaptation toa semi- aquatic habitat (Kyneetal. 1989, Tolonen 1982).
Therefore, the other farm-raised carnivorous fur- bearers should not be fed fatty fish orfish oil in excess, since the20 and 22 carbon-atom fatty acids are more readily accumulated in the tissues and organs of thesespecies. Thepresentresultssuggest thatmore emphasis should be placed on aspecies
specific formulation of the diets for the farm-raised fur animals.
Acknowledgements. The FinnishMinistryofAgricultureand Forestryis thanked forfinancially supportingthisstudy.The authorsaregratefultoMr.Tapani Ratilainen,and to the staff of the Veikkola Research Farm fortakingcareof the animals andhelpingwith thesampling,and to the staffs of the labor- atories of the Finnish Fur Breeders Associationin Vaasa,and the Institute of AnimalProduction, Animal Nutrition Sec- tion, in Jokioinen,forcarrying outthe analyses.The kind helpofMr.StevenAlward,B.Sc.,inchecking theEnglishof thetypescriptis alsogreatly appreciated.
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Agric. Sei. Fin!. 1 (1992)
ManuscriptreceivedJuly 1992 Kirsti Rouvinen
AgriculturalResearch Centre ofFinland FurFarmingResearch Station
SF-69100Kannus,Finland Presentaddress:
Nova ScotiaAgricultural College, DepartmentosAnimal Science, P.0.80x550, Truro,
Nova Scotia,B2N5E3 Canada
Jaakko Mäkelä
Finnish Fur Breeders’ Association, P.0.80x 5,SF-01601Vantaa,Finland TuomoKiiskinen
AgriculturalResearch Centre ofFinland, Institute of Animal Production
SF-31600Jokioinen,Finland SeppoNummela
AgriculturalResearch Centre ofFinland Central Laboratory
SF-31600Jokioinen,Finland
SELOSTUS
Rehunkalaperäisten rasvahappojen kertyminen eräidenlihaasyövien turkiseläinten ruhon rasvavarastoihin
KirstiRouvinen, JaakkoMäkelä,TuomoKiiskinen jaSeppoNummela
Maatalouden tutkimuskeskusjaSuomenTurkiseläintenKasvattajainLiitto ry
Minkeillä ja siniketuilla rehunkasviöljylisäyksen tiedetään lisäävänlinolihapon määrääjakalaöljytäydennyksen puoles- taanomega-3 rasvahappojen pitoisuutta elimistössä. Sini-ja hopeaketuilla kalarasvaruokinnan on todettu aiheuttavan tyypillisten kalarasvahappojen, kutenketoleeni-,eikosapen- taeeni- (EPA) ja dokosaheksaeenihappojen (DHA) kerty- mistä nahanalaisrasvakudokseen, maksaan ja sydänlihak- seen.Rehunkalarasvatäydennyksen tai erukahappopitoisen rypsiöljyruokinnan tiedetään myös aiheuttavan rotalla rap- peutumamuutoksia sydänlihaksessa.
Tässä selostetussa tutkimuksessa selvitettiinminkin, hil- lerinja supikoiranruhon rasvakoostumusta. Eläimiä ruokit- tiin5-6kuukaudenajan jokolaardilla taikalaöljyllä täyden- netyllä,kalaanja teurasjätteeseen pohjautuvallarehuvaliolla.
Rasvalisä rehussa oli5%tuorepainosta.Laardirehussa keto- leeni-,EPÄ- ja DHA-pitoisuudet olivat0.4, 0.3 ja 0.5 % rehunrasvassa. Vastaavat tasotkalaöljyrehussa olivat 7.6, 4.2 ja4,3%.Kustakinryhmästätutkittiin viisi eläintä. Eläi- mistä otettiin näytteetmaksasta,sydänlihaksesta janahana- laisrasvakudoksesta rasvahappoanalyysiä varten.
Kaikilla tutkituilla eläinlajeilla ruhon rasvakoostumus riippui voimakkaasti rehun rasvakoostumuksesta. Ka-
laöljyrehullaEPÄjaDHAvarastoituivaterityisestimaksaan ja sydänlihakseen,kun taasketoleenihappopitoisuudet olivat
korkeimmat sydänlihaksessa ja nahanalaisrasvassa. Kor- keimmatEPA-pitoisuudet analysoitiin kalaöljyrehulla ruo- kittujen supikoirien jahillereiden kudoksista. Pitoisuudet vaihtelivat 6.T-9.3 %maksanrasvassa ja 7.2-8.0%sydänli- haksenrasvassa. Minkeillä vastaavatpitoisuudet olivat ai- noastaan2.7%ja 3.9%.DHA-pitoisuudet olivat korkeim- mat kalaöljyllä ruokittujen hillereiden maksakudoksessa (18.5 %). Lisäksi supikoirien maksojen DHA-pitoisuudet (13.8 %)olivat merkitsevästi minkkien arvoja korkeammat (9.4%).
Tutkittujen pitkäketjuisten kalarasvahappojen kertyminen kudoksiin on todennäköisesti seurausta niiden riittämättö- mästäperoksisomaalisesta P-oksidaatiostaelimistössä. Evo- lutiivisenkehityksensä aikana erieläinlajit ovat sopeutuneet parhaiten hyödyntämään tiettyjäravintolähteitä. Puoliksi ve-
sielämään sopeutuneena lajinaminkkinäyttää pystyvänhyö- dyntämään kalalletyypillisiä, pitkäketjuisia, monityydytty- mättömiärasvahappoja muitatässätutkittujatarhaturkiseläi- miä paremmin. Saatuihin tuloksiin perustuen kalaöljyn käyttöä rehun yksinomaisena rasvalähteenä ketun, supi- koiran jahillerin rehussa tulisi välttää.Enemmänhuomiota tulisi kiinnittää myös lajikohtaiseen rehuvaliosuunnitteluun tarhatuilla turkiseläimillä.
Agric. Sei.Fin!. 1 (1992)