Holma‑Suu a i e al. En i on Sci Eu (2016) 28:5
DOI 10.1186/s12302‑016‑0071‑z
RESEARCH
Biomoni o ing o selec ed pe sis en
o ganic pollu an s (PCDD/Fs, PCBs andPBDEs)
inFinnish andRussian e es ial andaqua ic
animal species
A. Holma‑Suu a i1*, P. Ruokojä i2, A. A. Koma o 3, D. A. Maka o 3, V. V. O cha enko3, A. N. Panin3, H. Ki i an a2,
S. Laaksonen4, M. Nieminen5, M. Viluksela2,6 and A. Hallikainen7
Abs ac
Backg ound: The Finnish and Russian animal species (semi‑domes ica ed eindee , Finnish wild moose, Bal ic g ey
seal and Bal ic he ing) samples we e biomoni o ed in e es ial and aqua ic en i onmen s o polychlo ina ed
dibenzo‑p‑dioxins and dibenzo u ans (PCDD/Fs), polychlo ina ed biphenyls (PCBs) and polyb omina ed diphenyle h‑
e s (PBDEs).
Resul s: G ey seal (Halichoe us g ypus) was clea ly he mos con amina ed species. The mean PBDE concen a ion in
g ey seal was 115 ng/g a , and he highes WHO‑PCDD/F‑PCB‑TEQ ( oxic equi alen se by WHO) was 327 pg/g a .
In Finnish, eindee WHO‑PCDD/F‑TEQ a ied om 0.92 pg/g a in muscle o 90.8 pg/g a in li e . WHO‑PCDD/F‑TEQ
in moose li e samples was in he ange o 0.7–4.26 pg/g a , and WHO‑PCB‑TEQ in he ange o 0.42–3.34 pg/g a .
O e all moose had clea ly lowe PCDD/F and DL‑PCB concen a ions in hei li e han eindee .
Conclusions: Te es ial animals gene ally had low POP concen a ions, bu in eindee li e dioxin le els we e qui e
high. All Finnish and Russian eindee li e samples exceeded he EU maximum le el [8] o PCDD/Fs (10 pg/g a ),
which is cu en ly se o bo ine animals.
Keywo ds: Biomoni o ing, Animals, Dioxins, Li e , O gans
© 2016 Holma‑Suu a i e al. This a icle is dis ibu ed unde he e ms o he C ea i e Commons A ibu ion 4.0 In e na ional
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license, and indica e i changes we e made.
Backg ound
Polychlo ina ed dibenzo-p-dioxins and dibenzo u ans
(PCDD/Fs), dioxin-like PCBs (DL-PCBs) and polyb o-
mina ed diphenyle he s (PBDEs) a e lipophilic pe sis en
o ganic pollu an s wi h gene ally low wa e solubili ies.
They a e h ea ening animals and humans when en e ing
in o he e es ial and aqua ic ood chains [7]. These con-
aminan s can cause se e e heal h e ec s in humans and
wildli e. Wild e es ial animals, such as moose (Alces
alces) and semi-domes ica ed eindee (Rangi e a an-
dus a andus), a e known o accumula e en i onmen al
con aminan s e ec i ely, because hei die consis s o
plan s om na u al pas u es con amina ed due o long-
ange anspo o a mosphe ic emissions [13]. Based on
he s udies on he o he species ( o e.g. sheep), di e en
issues o eindee and moose a e assumed o ga he a -
ying concen a ions o con aminan s.
F om he aqua ic poin o iew, he Bal ic Sea is consid-
e ed o be one o he mos pollu ed wa e s in he wo ld con-
amina ed by Pe sis en o ganic pollu an s (POPs). They
a e discha ged om indus ialized coun ies su ounding
and anspo ed om dis an sou ces by an a mosphe ic
deposi ion [23, 33]. The e ha e been ema kable e o s o
es ic he usage and p oduc ion o he long- ange ans-
po ing and bioaccumula e chemicals. Howe e , hey s ill
can be ound om he ma ine en i onmen o he Bal-
ic Sea [5]. I is conside ed ha he ing (Clupea ha engus
Open Access
*Co espondence: [email p o ec ed]
1 Depa men o Biology, Uni e si y o Oulu, P.O. Box 3000, 90014 Oulu,
Finland
Full lis o au ho in o ma ion is a ailable a he end o he a icle
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Holma‑Suu a i e al. En i on Sci Eu (2016) 28:5
memb as) and g ey seal (Halichoe us g ypus) om he Bal-
ic Sea con ain highe PBDE le els han he same o simi-
la species om o he wa e s. The ad e se heal h e ec s
o o ganohalogen chemicals ha e been seen clea ly wi h
g ey seal, he popula ion o which declined o minimum
(abou 4000 indi iduals) in he mid-1970s in he Bal ic Sea
because o educ ion in p egnancy a es [12]. Thus, Bal ic
he ing and g ey seal may indica e well he con amina ion
in aqua ic en i onmen . Malla d (Anas pla y hynchos), o
i s pa , may indica e he con amina ion s a us o semi-
aqueous en i onmen .
A mosphe ic deposi ion is belie ed o be a majo
sou ce o some POPs in he Bal ic Sea [17, 33] and also
in e es ial en i onmen , e.g. in Finnish Lapland [11].
The emissions o PBDEs o en i onmen al compa men s
wi hin he Bal ic Sea egion we e ecen ly es ima ed
in he COHIBA P ojec (h p://www.cohibap ojec .
ne /home/en_GB/home/). While he emissions o land
ended o o igina e mainly om he applica ion o con-
amina ed sewage sludge, he main emissions o ai came
du ing se ice li e o lame- e a ded p oduc s in he o m
o elease om he indoo en i onmen , s eel indus y
and he acciden al i es o was e.
In o de o assess he exposu e o people o POPs, i is
impo an o no ice ha in Finland, hun ing is a popula
hobby among popula ion, and o e 300,000 people had
an o icial hun ing ca d in 2005 allowing hem o hun
acco ding o legisla ion (www.mmm. i). Hun ing big
game, like moose, esul s ha a g oup o people migh
consume mo e moose mea han po k o poul y mea .
On he o he hand, eindee husband y (including mea
p oduc ion and ou ism, by-p oduc s) is an impo an
li elihood in he no he n Finland and also in Russia.
Exposu e o POPs ia game mea , li e , and o he o gans
may be a p oblem in some speci ic popula ions [7].
The dis ibu ion o PCDD/Fs and DL-PCBs in ani-
mal body has been s udied in di e en animal species.
The e ha e been a ia ions in he concen a ions o
con aminan s in di e en issues. Al hough a y is-
sues a e known o be he pool o lipophilic POPs, ce -
ain o gans, such as li e , a e high- isk edible issues
o dioxin-like pollu an s [27]. Tissue dis ibu ion da a
ha e shown ha li e has a highe po en ial o accumu-
la e dioxin han he o he issues in a [34], bee ca -
le [31], pig [27] and eindee [29]. In he Danish s udy
li e , lea a , lank and shank o sheep we e analysed.
The highes PCDD/Fs we e obse ed in sheep li e
[20]. Fu he mo e, PCDD/Fs ha e been no iced o be
8–27 imes highe in li e o sheep han i s muscle is-
sue. Howe e , simila phenomenon had no seen wi h
he s udied cows [26].
In he s udy o pigs, i was ound ha li e was again he
main collec o o dioxins when compa ing compounds
in li e , lung, kidney, subcu aneous a , mesen e y and
muscle [27]. The p ope y o li e o accumula e diox-
ins appea ed also in he s udy o lamb o gans: li e had
clea ly highe PCDD/Fs han kidneys and hea [9]. O al
p oduc s (e.g. pa é, haggis, ipe and black budding) o
he animals (lamb, ox, dee and pig) ha e gene ally low
con aminan le els p obably as a esul o p ocessing o
dilu ion. On he o he hand, qui e high concen a ions o
PCDD/Fs and PCBs ha e been epo ed in some o als,
such as dee and lamb li e , and consump ion o po ions
mo e han 100g may he e o e lead o exceeded ole ably
daily in ake (TDI) (2pg WHO-TEQ/kg o body weigh )
[9, 7]. Fish and ish p oduc s play a signi ican ole in he
Finnish die a y in ake o polychlo ina ed dibenzo-p-di-
oxins, polychlo ina ed dibenzo u ans (PCDD/F; dioxins)
and polychlo ina ed biphenyls (PCB). I one conside s he
PCDD/F in ake, hen ish and ish p oduc s accoun ed
o 82%, and Bal ic he ing (C. ha engus L.) alone 52% o
he o al in ake [16].
In his s udy, POP concen a ions ha e been epo ed
in di e en e es ial and aqua ic animal species in Fin-
land and Russia. The pu pose was o epo POP con-
cen a ions in he aqua ic and e es ial game species
ep esen ing di e en en i onmen s and a iable ophic
le els in he ecosys em. Knowledge o o ganic pollu an s
in game and semi-domes ica ed animals is highly needed
in o de o gi e ad ice, i needed, o minimize he expo-
su e o he hun ing popula ion.
Me hods
Te es ial samples
O gans o Finnish and Russian semi-domes ica ed ein-
dee we e analysed o PCDD/Fs and DL-PCBs o igu e
ou how con aminan s a e dis ibu ed in he eindee
body. Reindee li e PCDD/F and DL-PCB concen a-
ions we e compa ed be ween adul eindee and ein-
dee cal es om Finnish Lapland and Kola Peninsula in
Russia. In addi ion, PCDD/Fs and DL-PCBs we e ana-
lysed in Finnish wild moose li e .
The eindee issue samples: muscle ( ump, ib and
shoulde muscle), li e , kidneys, abdominal a , lymph
nodes ( om ho acic ca i y) and bone ma ow ( om
legs), lungs, b ain, placen a ( om adul emale) and
spleen we e ga he ed om one adul emale (age ca.
10 yea s) and one male cal (age ca. 6 mon hs) om
sou he n eindee he ding a ea in Finland in 2008. In
addi ion, blood and udde samples we e ga he ed om
wo adul emale eindee (age ca. 10yea s) om no h-
e n eindee he ding a ea in Finland in 2010.
The Finnish eindee li e samples we e sampled in he
no he n (cal es n=5, adul n=5), middle (cal es n=3,
adul n=2) and sou he n (cal es n=3, adul n=1) Lap-
land in 2006 and 2010. The Russian eindee li e (n=7),
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Holma‑Suu a i e al. En i on Sci Eu (2016) 28:5
muscle (n=4) and kidney (n=3) samples we e ga he ed
om adul eindee in Lo oze o dis ic in Mu mansk
a ea, Kola Peninsula in 2013.
The sampling a eas o Finnish moose li e samples
loca ed in No he n (Koillismaa) and Cen al (No h-
Sa o) Finland. The moose li e samples we e pooled by
he sampling a ea, sex and age. Pooling esul ed in six
samples: ou om moose cal es, age <1yea (o which
wo we e indi idual moose li e s, one pool wi h wo sub-
samples and one pool wi h h ee subsamples), one young
adul , age 1.5 yea s (one subsample,) and one pooled
adul li e sample ( wo subsamples, ages 3 and 4yea s).
In addi ion o indi idual eindee and moose samples,
in 2007, in a egula ma ke su eillance, mea samples
o semi-domes ica ed eindee (n=9) and moose (n=3)
we e aken. Sampling and pooling complied he Commis-
sion egula ion 1883/2006/EC4 and was a ge ed o he
game o semi-domes ica ed eindee sold in ood s o es
ep esen ing di e en ypes and quali y o mea . Sam-
ples included ille , ende loin, lank and ump. Also he
muscle mea sample o Eu opean ha e (Lepus eu opaeus)
(n=1) was collec ed om adul ha e in sou he n Finland
in 2007.
Aqua ic andsemi‑aqua ic samples
The muscle samples (n=12) o Bal ic he ing we e ga h-
e ed om he Finnish ma ke in 2006 and 2007. O igin
o he ing was he Bal ic Sea; in pa icula Bo hnian Sea
and A chipelago Sea. A pa o he ing was sampled
om uniden i ied a ea (Finnish) o he Bal ic Sea. The
muscle samples o g ey seals we e ga he ed as six pooled
(3×300g) samples om di e en ca ching a eas om
he no he n o sou he n Finnish coas o he Bal ic Sea
in 2006–2007. The samples we e olled o aluminium oil
and packaged o Minig ip bags. The pooled muscle mea
sample o malla d (n=2) we e collec ed om malla d in
he middle o Finland in 2007.
Sample p epa a ion andanalyses
The issues we e cu using clean ins umen s and ni ic
glo es o p e en con amina ion. The samples we e
s o ed in polye hylene bags and p ese ed a −20°C un il
he analysis was accomplished. The chemical analyses
we e ca ied ou a he Chemical Exposu e Uni o he
Na ional Ins i u e o Heal h and Wel a e. The labo a o y
has been acc edi ed acco ding o he EN ISO/IEC 17025
s anda d by FINAS. The scope o acc edi a ion includes
PCDD/F and DL-PCB analyses om biological ma ices.
The Russian samples we e analysed wi h Wa e s Au o-
spec sys em in he Russian S a e Cen e o Quali y and
S anda diza ion o Ve e ina y D ugs and Feed (VGNKI).
The ins i u ion is ce i ied by RF S anda diza ion,
Me ology and Ce i ica ion Commi ee (Gos anda ) as
he Ve e ina y D ugs and Feed ce i ica ion and es ing
cen e.
A e homogeniza ion, he samples we e eeze d ied,
and a was ex ac ed wi h e hanol- oluene (15/85 %,
/ ) using Accele a ed Sol en Ex ac o (Dionex ASE
300) equipmen . The ex ac ion sol en was e apo a ed
o almos d yness and he samples we e ans e ed in o
hexane, om which he a con en was measu ed g a i-
me ically. 13C-labelled PCDD/PCDF (al oge he 16
s anda ds) we e used as in e nal s anda ds o quan i a e
he amoun o PCDDs/PCDFs. 13C-labelled PCB conge-
ne s we e used as in e nal s anda ds o non-o ho-PCBs.
13C-labelled PBDE s anda ds (BDE 28, 47, 77, 99, 100,
153, 183 and 209) we e used o quan i ica ion o PBDEs.
The eco e ies o he indi idual in e nal s anda ds o
PCDD/F and PCB congene s we e de e mined by adding
he eco e y s anda ds jus be o e mass spec al analysis.
The eco e ies o he in e nal s anda ds we e 60–120%.
The limi s o quan i ica ion (LOQ) o indi idual con-
gene s we e de e mined by a signal- o-noise a io o 3:1
[based on Commission egula ion (EU) No 252/2012] in
he ch oma og am o in case o analy e peak exis ing in
he blank sample, concen a ion o he analy e in blank
sample.
A e ha slu y wi h sodium sulpha e, silica gel, hex-
ane and concen a ed sulphu ic acid was mixed wi h a
sample. The sample slu y was pou ed in o an acidic mul-
ilaye silica gel column [wi h sodium sulpha e, sulphu ic
acid–silica gel (15 and 44% w/w) and silica gel laye s].
The sample was elu ed om he column wi h hexane and
concen a ed in o small olume (0.5ml) o hexane. The
sample was u he pu i ied and ac iona ed on a ca -
bon column wi h an alumina column on op o i . The
columns we e elu ed wi h 20% dichlo ome hane-hexane
( / ) and he elu e con ained o ho and mono-o ho sub-
s i u ed PCBs.
The sol en was e apo a ed in o 0.5ml o hexane, and
a e he addi ion o eco e y s anda ds, i was in o-
duced in o high- esolu ion gas ch oma og aphy–high-
esolu ion mass spec ome y (HRGC/HRMS; VG
70 SE o Au ospec Ul ima). The ca bon column was
hen in e ed and elu ed wi h oluene. A e he addi-
ion o eco e y s anda ds in o oluene ac ion, i was
e apo a ed in o 20µl o nonane. This ac ion con ain-
ing PCDD/Fs and non-o ho-PCBs was analysed wi h
HRGC/HRMS; VG 70 SE o Au ospec Ul ima. The col-
umn used o PCDD/Fs and PCBs was DB-Dioxin col-
umn (J&W Scien i ic, 60m, ID 0.25mm, 0.15µm). SIR
was used wi h 10,000 esolu ion.
The analysed PCDD/F congene s included 17 oxic
2378-subs i u ed congene s (2378-TCDD, 12378-PeCDD,
123478-HxCDD, 123678-HxCDD, 123789-HxCDD,
1234678-HpCDD, OCDD, 2378-TCDF, 12378-PeCDF,
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Holma‑Suu a i e al. En i on Sci Eu (2016) 28:5
23478-PeCDF, 123478-HxCDF, 123678-HxCDF, 234678-
HxCDF, 123789-HxCDF, 1234678-HpCDF, 1234789-
HpCDF, OCDF). PCB congene s included 12 dioxin-like
PCBs (Non-o ho-PCBs; -77, -81, -126, -169 and mono-
o ho-PCBs; -105, -114, -118, -123, -156, -157, -167,
-189). PBDEs consis ed o congene s BDE-28, -75, -71,
-47, -66, -77, -100, -119, -99, -85, -154, -153, -138, -183
and -209.
The esul s a e epo ed as a -based lowe bound con-
cen a ions i.e. he esul s below he limi o quan i ica-
ion (LOQ) a e ea ed as ze o.
Resul s anddiscussion
The a -based WHO-PCDD/F-TEQ and WHO-PCB-
TEQ concen a ions (lowe bound esul s) in Finnish
eindee a e shown in Fig.1.
I is seen ha he concen a ions o WHO-PCDD/F-
and WHO-PCB-TEQs we e qui e equal in he s udied
o gans. Howe e , he li e is an excep ion, because i
accumula es clea ly mo e dioxin-like compounds han
o he o gans. I may be he de oxi ica ion p ope ies o
li e , which makes i o ga he oxic compounds in he
g ea e ex en han he o he in e nal o gans [21]. Some
s udies ha e shown ha lipid di e ence in he issues and
he pollu an lipophilic p ope y conduc ed ans e , can-
no explain he ele a ed le els o dioxin-like compounds
in li e . This may be he esul o unc ion o CYP1A2
in he li e . CYP1A2 is an impo an de e minan o
PCDD/F seques a ion. In addi ion, li e ’s high po ency
o accumula ing pollu an s may come om hei physi-
ological unc ion as he bigges de oxi ica ion o gan in
mammals [27].
The eason o he ele a ed concen a ions in he li e
is called he i s -pass e ec . The enous blood om
he gas oin es inal ac o all mammals, i no all e -
eb a es, is collec ed in he po al ein sys em and hus
di ec ly passed o he li e be o e eaching he es o he
body. Thus, he li e will always accumula e highe con-
cen a ions compa ed o he o he o gans simply because
i is he o gan ha makes i s con ac wi hin he blood
low.
WHO-PCDD/F-TEQ con ibu ed mo e (69%) o o al
WHO-TEQ in li e while he con ibu ions o WHO-
PCDD/F-TEQ and WHO-PCB-TEQ we e mo e equal
in o he o gans. Howe e , WHO-PCB-TEQ sha ed 61%
o o al TEQ in bone ma ow sample and e en 92% o
o al TEQ in blood sample. The mos abundan PCDD/F
congene s in eindee in e nal o gans we e 23478-PeCDF
and 2378-TCDF. O he non-o ho PCBs, he domina ing
congene was PCB-126, bu also PCB-77 con ibu ed sig-
ni ican ly o he o al non-o ho-PCB sum, especially in
lymph nodes o eindee .
PCDD/F- and DL-PCB concen a ions (as a -based
WHO-TEQs) in Russian eindee o gan samples a e
shown in Table1.
I can be no ed ha PCDD/F le els in Russian ein-
dee muscle, kidney and li e samples a e close o Finn-
ish eindee samples, bu DL-PCB concen a ions in all
Fig. 1 WHO‑PCDD/F‑ and WHO‑PCB‑TEQs in di e en o gans o Finnish eindee
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Holma‑Suu a i e al. En i on Sci Eu (2016) 28:5
issues om Russia a e se e al- old highe han in issues
om Finland. The main con ibu o o oxici y equi a-
len s in Russian samples was PCB-126. Tha may be
poin a a common in ensi e PCB con amina ion sou ce
loca ed on he e i o y o Kola Peninsula.
Conside ing he ood sa e y aspec , i is seen ha
PCDD/Fs in Russian eindee muscle samples a e below
he limi s (3pg/g a in Russia, 2.5pg/g a in EU), bu
o al WHO-PCDD/F-PCB-TEQs a e o e he EU limi
(4pg/g a ). PCDD/Fs and DL-PCBs a e ca. wo imes
highe in kidneys han in muscle. PCDD/Fs in li e a e
highe by an o de o magni ude han he cu en Russian
limi s (6pg/g a ).
PCDD/F and DL-PCB concen a ions (as a -based
WHO-TEQs) in Finnish and Russian eindee li e sam-
ples a e shown in Fig.2. The esul s a e compa ed o ea -
lie s udies on eindee in Finland.
I is seen ha in Finnish Lapland eindee cal es had
highe WHO-PCDD/F- and WHO-PCB-TEQs han
adul eindee . The common end in Finnish eindee is
ha con aminan concen a ions inc ease om no he n
o sou he n a eas. Howe e , he highes o al TEQ le el is
obse ed in adul eindee li e om Kola dis ic , which
is high in he no h. I seems ha in Kola Peninsula, he e
may be he local pollu ion sou ces which a ec o he
con aminan concen a ions seen in eindee li e .
In addi ion, WHO-PCDD/F-TEQs we e qui e equal
in Russian adul eindee li e samples and sou he n
Lapland cal samples om Finland in 2006. Tha could
mean he e was also some local con amina ion sou ce o
PCDD/Fs in sou he n Lapland, oo. I is gene ally seen in
he Finnish samples ha li e accumula es mo e PCDD/
Fs han DL-PCBs. Howe e , in he cal and adul eindee
samples om no he n Lapland in 2010, he e we e mo e
DL-PCBs han PCDD/Fs o o al TEQs. Also adul ein-
dee samples om Kola dis ic had ela i ely big con i-
bu ion o DL-PCBs ha may indica e he con amina ion
sou ce nea he bo de a ea o No he n Finland and Rus-
sia in mo e ecen yea s, while he samples o hese a eas
had been collec ed in 2010–2013. The eindee samples
om no he n Lapland in 2006 had smalle con ibu ion
o DL-PCBs o o al TEQ han samples ga he ed in 2010.
The e could be a ying exposu e condi ions be ween he
yea s.
WHO-PCDD/F-TEQs and WHO-PCB-TEQs in Finn-
ish moose li e a e shown in Table2.
I can be seen ha a young adul moose om he cen-
al Finland had he highes WHO-PCDD-TEQ o he
all samples s udied (4.26 pg/g a ). This may indica e
Table 1 WHO-PCDD/F-TEQs andWHO-PCB-TEQs (pg/g a )
inRussian eindee o gan samples (mean alues)
Sample WHO‑PCDD/F‑TEQ WHO‑PCB‑TEQ
Reindee muscle (n = 4) 0.92 3.62
Reindee kidneys (n = 3) 2.03 9.2
Reindee li e (n = 4) 62.13 140.15
0.0
50.0
100.0
150.0
200.0
250.0
WHO-PCB-
TEQ pg/g a
WHO-
PCDD/F-TEQ
pg/g a
Fig. 2 WHO‑PCDD/F‑ and WHO‑PCB‑TEQs in eindee li e samples om Finnish Lapland and Kola Peninsula in Russia. *[13], **[29]

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Holma‑Suu a i e al. En i on Sci Eu (2016) 28:5
highe exposu e o PCDD/Fs in mo e sou he n egions
in Finland. The lowes WHO-PCDD/F-TEQ (0.7 pg/g
a ) and WHO-PCB-TEQ (0.42pg/g a ) concen a ions
we e seen in adul emale moose om no he n Fin-
land. Howe e , mos o he cal es om no he n Finland
had WHO-PCDD/F-TEQs and WHO-PCB-TEQs o e
3.0pg/g a .
Low concen a ions o WHO-PCB-TEQs o he cal es
and adul moose co ela ed wi h WHO-PCDD/F-TEQs:
One moose cal and one moose adul had lowe WHO-
PCB-TEQ concen a ions han he o he samples s udied
om he no he n Finland. Lowe WHO-PCB-TEQs o
hese samples may indica e di e en exposu e condi ions
o PCBs. I has been ound in ea lie s udies ha Finnish
eindee cal es’ li e s con ained mo e PCDD/Fs and DL-
PCBs han adul eindee li e s, which could be he case
o moose as well [24, 29].
The a con en s o he moose li e samples we e e y
simila (on a e age 5.3%), so hey do no explain a ia-
ion in con amina ion le els. An ea lie s udy does no
suppo he concep ha PCDD/Fs and DL-PCBs accu-
mula e in o li e issue ia he lipid pa i ioning only.
Ins ead, he e may be o he unc ionally impo an ac-
o s such as CYP1A2, in li e [29]. In his s udy, we do
no ha e in o ma ion on moose li e enzymes in a ela-
ion o con aminan accumula ion. Howe e , accumula-
ion o compounds in li e may be due o cy oplasmic
and mic osomal binding [6, 2]. Howe e , o he han he
DL-PCBs (namely non-DL-PCBs) can ac as inhibi o s o
CYPs and may hus lead o educed bio ans o ma ion.
In his s udy, adul moose om he no he n Finland
seemed o ha e somewha lowe DL-PCB concen a ions
han cal es om he same a ea, bu gene ally i seems
ha in no he n Finland, he e is highe exposu e o DL-
PCBs han in sou he n Finland. This is suppo ed by he
obse a ion ha WHO-PCB-TEQs we e gene ally highe
in he no he n han in sou he n Finland.
The mos abundan PCDD/F congene s ound in moose
li e samples we e 23478-PeCDF and 2378-TCDF. Also
123478-HxCDF, 123678-HxCDF and 234678-HxCDF
we e well ep esen a i e in some o he li e samples. O
he non-o ho dioxin-like PCBs, he mos domina ing
congene was clea ly PCB-126.
A Ge man s udy had obse ed ha li e o oe dee
(Cap eolus cap eolus) was highly con amina ed wi h
PCDD/Fs and DL-PCBs in na u al su oundings in Ge -
many (WHO-PCDD/F-PCB-TEQ61pg/g a ) [25]. High
le els ha e been de ec ed in Finnish eindee li e s [24,
30], oo. Howe e , PCDD/F and PCB le els in eindee
and moose muscle samples we e clea ly lowe han in
li e in Finland [30]. Whi e- ailed dee (Odocoileus i -
ginianus) sampled nea he magnesium smel e in Can-
ada had PCDD/F-TEQ concen a ion o 26pg/g a in
adipose issue [32], which is s ill below he concen a ion
in li e samples o eindee in his s udy.
WHO-PCDD/F-PCB-TEQ in moose muscle samples
in Sweden (on a e age 8.1pg/g a ) [3] has shown highe
le el han moose muscle samples [30], and acco ding o
his s udy, also moose li e samples in Finland. This may
indica e ha Finnish moose is less exposed o PCDD/
Fs and DL-PCBs. Howe e , con amina ions o Finnish
eindee li e do no suppo he idea o minimal en i-
onmen al pollu ion in Finland. The e also can be some
indi idual me abolic di e ences, which in luence o he
con amina ion le els in moose. A compa ison o WHO-
PCDD/F-TEQs and WHO-PCB-TEQs be ween Finnish
eindee and moose muscle and li e is shown in Fig.3.
I is clea ly seen ha moose ha e lowe concen a-
ions o PCDD/Fs and DL-PCBs in li e han eindee . I
could be possible ha he e a e na u ally mo e binding
CYP1A2 enzymes in eindee li e han in moose li e .
O he explana ion may be ha moose is me abolizing
hese compounds mo e e ec i ely han eindee . O , i
could be he di e ences in he die s o hese Ce id spe-
cies which ha e in luence o PCDD/F and DL-PCB le els
Table 2 WHO-PCDD/F- andPCB-TEQs (pg/g a ) inmoose li e samples
a Sample consis s o one indi idual. bSample consis s o wo o h ee indi iduals pooled oge he . Fa con en (%) a e ela i e o we weigh
Sample nFa % WHO‑PCDD/F‑TEQ WHO‑PCB‑TEQ
TEF 2005 (1998) TEF 2005 (1998)
No he n Finland
Moose cal male #1 1a4.9 3.03 (4.11) 3.34 (3.35)
Moose cal emale #2 1a5.4 1.08 (1.44) 0.94 (0.94)
Moose cal emale #3, (age 8 + 8 mon hs) 2b5.4 3.82 (5.34) 3.27 (3.27)
Moose cal emale #4 3b5.3 3.53 (4.86) 3.28 (3.28)
Moose adul emale #5, (age 3 + 4 yea s) 2b5.1 0.7 (0.98) 0.42 (0.42)
Cen al Finland
Moose young adul #6, (age 1.5 yea s) 1a5.4 4.26 (5.71) 2.65 (2.66)
Page 7 o 10
Holma‑Suu a i e al. En i on Sci Eu (2016) 28:5
in hei li e . I is also possible ha all hese explana ions
a e a ec ing o he ou come.
In ha e mea , he concen a ions o WHO-PCDD/F-
TEQ we e 1.2pg/g a and WHO-PCB-TEQ0.89pg/g
a . I is seen ha PCDD/Fs con ibu ed mo e o o al
WHO-TEQ in ha e. PBDE concen a ion was 1.7ng/g
a . BDE-209 was clea ly he mos domina ing PBDE con-
gene in ha e.
PBDE congene p o ile in eindee was la gely di e -
en han in Bal ic he ing and g ey seal. BDE-209 was he
mos domina ing congene ; i s sha e was as much as 79%
o o al PBDE sum. BDE-47 (6%), BDE-99 (6%) (Indi-
ca o s o Pen a-mix exposu e) and BDE-153 (5%) we e
h ee o he congene s building mainly PBDE congene
p o ile o eindee . BDE-154 and -183 (Oc a-mix conge-
ne s) we e obse ed o show low con ibu ion (1% om
o al sum) in eindee . An ea lie s udy wi h moose (A.
alces) in Finland had shown ha Pen a- and Oc a-BDEs
we e he mos domina ing PBDEs in muscle samples.
Howe e , BDE-209 has been obse ed o exis in high
le els (up o 177ng/g lipid weigh ) in moose muscle sam-
ples, oo [29]. I is concluded ha BDE-209 is minimally
abso bed om he gas oin es inal ac o mammals
because o i s high molecula mass [4]. Ou s udy, how-
e e , shows high BDE-209 le els in e es ial he bi o e
mammals.
The mean WHO-PCDD/F-TEQ was 22pg/g a and
WHO-PCB-TEQ191pg/g a in g ey seal (Table3). In
he mea o g ey seal, he concen a ion o dioxins was
clea ly highe when compa ed o esul s in e es ial ani-
mals implica ing hei di e en posi ion in he ood web.
The e may be ha m ul heal h e ec s o g ey seal because
o high dioxin con amina ion. The con ibu ion o PCB o
o al TEQ was highe in g ey seal while he opposi e was
ue o mea o moose, malla d and ha e (Table4) as well
as o li e o eindee .
I was obse ed ha g ey seal had clea ly he highes
mean PBDE concen a ions, 115ng/g lw) (Table5). The
secondly highes PBDE le el was obse ed o be in Bal-
ic he ing (12.2ng/g lw), ollowed by eindee (1.85ng/g
lw). The lipid con en was on a e age highes in Bal ic
he ing (9.5%). G ey seal (4.6%) and eindee (3.4%) had
mo e equal a con en s. The e o e, i is no a necessi y
o ha e a highes lipid con en o ha e he highes PBDE
le els in muscle issue as he esul s wi h g ey seal indi-
ca e. I may be s ill he ecophysiological ac o s, like eed-
ing beha iou and me abolic capaci y, which a ec o he
PBDE concen a ions de ec ed in animal issues.
Conside ing he indi idual PBDE congene s in Bal ic
he ing, a p opo ion o BDE-47 was ema kable, namely
59%, and i was ollowed by BDE-100 wi h 14% sha e
o o al PBDEs measu ed (Table2). Though, his indica es
0
2
4
6
8
10
12
14
16
18
20
22
24
26
28
30
32
34
36
38
40
42
44
46
48
50
52
54
WHO-PCDD/F-TEQ
WHO-PCB-TEQ
Samples s udied ea lie *
New samples
Fig. 3 WHO‑PCDD/F‑TEQs and WHO‑PCB‑TEQs (pg/g a , calcula ed as TEFs 1998) in Finnish moose li e compa ed o he ea lie esul s o con ami‑
nan s in eindee and moose issues. *[13, 29, 30]
Page 8 o 10
Holma‑Suu a i e al. En i on Sci Eu (2016) 28:5
s ong Pen a-mix exposu e o Bal ic he ing. Pa allel
esul s ha e been obse ed by p e ious s udies on Bal ic
he ing [15, 22]. BDE-47 is ypically ound om animals
in he ma ine en i onmen . Fo example, in he li e s o
pisci o ous co mo an s (Phaloc oco ax ca bo) BDE-47
con ibu ed 24-100% o he o al PBDEs p esen [1, 18].
Haglund e al. [10] ha e epo ed BDE-47 concen a ions
3.2–27µg/kg lipid weigh in di e en age g oups o Bal ic
he ing. Though, age- ela ed accumula ion o PBDEs in
ish had been obse ed [28]. Sha es o BDE-99, -154 and
-209 we e qui e equal (on a e age 6% o each) in Bal ic
he ing.
The mos dominan PBDE congene s in g ey seal we e
BDE-47 and -100 as hey we e in Bal ic he ing, oo
(Table2). BDE-47 was con ibu ed on a e age 68% o he
o al PBDE sum o g ey seal. Con ibu ion o BDE-100
was 9%. In con as o high BDE-47 concen a ion and
hus indica ion o he p esence o Pen a-BDE o mula-
ion, he Oc a-mix indica i e BDE-183 concen a ion was
negligible in he g ey seal samples ( ha was ue also o
Bal ic he ing). Howe e , BDE-154 and -153 (Oc a-mix
exposu e indica o s) ha e on a e age 5% ep esen a ion
o o al PBDE p o ile in g ey seal.
BDE-28 and -66 we e no seen in g ey seal samples
al hough hese congene s exis in Bal ic he ing sam-
ples (2% con ibu ion bo h). This may be explained by
he highe me abolic a e o hese congene s in g ey seal.
Te a- o Hexa-BDEs ha e been epo ed ound widely
om he wildli e in emo e a eas [14, 19].
The o e all PBDE congene p o ile o Bal ic he ing
e lec ed well a p o ile o g ey seal; co ela ion coe -
icien was 0.99 be ween he species. Only excep ions
we e ea ly men ioned BDE-66 and -28. Species-spe-
ci ic di e ences in accumula ion o compounds may be
Table 3 Dioxin concen a ions ing ey seal samples
Fa con en (%) a e ela i e o we weigh
a NO Non‑o ho‑PCB
Sample A ea Fa % PCDD/F
(pg/g a ) DL‑PCB
(pg/g a ) PCB (ng/g
a ) WHO‑PCDD/
F‑TEQ (pg/g
a )
WHO‑NO‑
PCB‑TEQa
(pg/g a )
WHO‑PCB‑
TEQ (pg/g a ) WHO‑PCDD/F‑
PCB‑TEQ (pg/g
a )
Seal No h‑Finland 9.5 76.7 557,503 22,900 23 46 190 213
Seal Sou h‑Wes ‑
Finland 9.2 81.7 229,718 7580 21.6 24.2 77 98.6
Seal Sou h‑Wes ‑
Finland 2.2 60.5 215,644 9450 12.6 17.9 70.8 83.4
Seal Sou h‑Finland 3.5 186 803,950 28,100 31.2 56.8 270 301.2
Seal Wes ‑Finland 2.4 107 517,230 15,000 33.5 50.5 192 225.5
Seal No h‑Finland 0.7 125 838,231 53,000 8.84 27.4 318 326.84
Table 4 Median uppe bound concen a ions o  WHO-
PCDD/F-TEQs andWHO-PCB-TEQs indi e en ma ke su -
eillance samples inFinland in2007
Fa con en (%) a e ela i e o we weigh
Sample nFa % WHO‑PCDD/F‑TEQ WHO‑PCB‑TEQ
Reindee
Fille 1 3.8 1.0 1.7
Rump 3 2.7 1.2 1.9
Tende loin 1 2.8 1.1 1.8
Flank 1 4.0 2.2 6.9
Moose
Rump 3 1.7 0.92 0.25
Malla d 1 19 0.88 0.047
Ha e 1 3.3 1.2 0.89
Table 5 PBDE concen a ions [mean, (SD), ange] alongwi h he a con en s ( ela i e owe weigh ) inaqua ic and e -
es ial samples
Sample nFa % PBDE (ng/g ww) PBDE (ng/g lw)
Bal ic he ing 12 9.5 (3.2) 6.0–19.0 0.4 (0.7) 0.0–2.0 12.2 (7.0) 4.2–26.3
G ey seal 6 4.6 (3.8) 0.7–9.5 5.2 (4.8) 0.74–13.4 115.0 (59.4) 47.6–212
Malla d 1 (sub‑n = 2) 19.5 0.17 0.88
Reindee 14 3.4 (1.34) 1.4–5.8 0.06 (0.11) 0.004–0.44 1.85 (2.52) 0.12–7.57
Moose 3 2 (0.96) 1.0–3.3 0.017 (0.006) 0.01–0.03 1.24 (0.94) 0.36–2.55
Eu opean ha e 1 3.3 0.06 103
Page 9 o 10
Holma‑Suu a i e al. En i on Sci Eu (2016) 28:5
caused by abso p ion e iciency, elimina ion a es and/o
me abolism.
Conclusions
Dioxin concen a ions in he mea o semi-domes ica ed
eindee and e es ial game animals we e gene ally low.
Howe e , eindee li e con ained abou 20 imes mo e
PCDD/Fs when compa ed o eindee mea . PCDD/Fs
we e qui e equally dis ibu ed in he lipid compa men in
all Finnish eindee issues, despi e he a ying a con en s
in di e en issues. Howe e , in li e he e was o e whelm-
ingly highes PCDD/F le el. Tha may be he esul o exis -
ing CYP1A2 and high a ini y o dioxin-like compounds
o i . DL-PCBs we e beha ed wi h simila manne han
PCDD/Fs. Howe e , he e was somewha highe DL-PCB
concen a ion in bone ma ow han in o he o gans. Again
li e was an excep ion wi h he highes DL-PCB load.
Reindee li e samples showed a ying concen a ions
o PCDD/Fs and DL-PCBs. Finnish eindee cal es had
highe con aminan le els han adul eindee , bu adul
eindee om Kola Peninsula showed o ha e he highes
concen a ion o o al TEQ (ca. 190pg/g a ). All Finnish
and Russian eindee li e samples exceeded he EU max-
imum le el o PCDD/Fs (10pg/g a ), which is cu en ly
se o bo ine animals.
A young adul moose om he cen al Finland had he
highes concen a ions o PCDD/Fs and DL-PCBs o all
moose li e samples s udied. Gene ally s udied cal es
om he no he n sampling si e had equal concen a-
ions o WHO-PCDD/F- and WHO-PCB-TEQs in hei
li e . O e all moose had clea ly lowe PCDD/F and DL-
PCB concen a ions in hei li e han eindee . The e
could be di e ences be ween he die s o me abolic
capaci ies o bo h.
G ey seal had clea ly he highes mean PBDE concen-
a ions. The secondly highes PBDE le el was obse ed
o be in Bal ic he ing, ollowed by eindee . PBDE con-
gene p o iles we e e y simila in Bal ic he ing and g ey
seal ( ep esen ing an aqua ic ood chain). Howe e , PBDE
p o iles in e es ial en i onmen di e ed signi ican ly
om aqua ic one. This may indica e di e en deposi ion
mechanisms and exposu e o PBDEs and also possible
di e en bio ans o m capaci y o animals.
Being he bi o es, e es ial animals ha e congene
p o iles close o deposi ed ( echnical) mix u es o PCBs
and PBDEs when compa ed o e.g. Bal ic Sea seal ( e a-
and pen a congene s o PCBs and congene s BDE47, 99
and 100 con ibu e signi ican ly).
Au ho s’ con ibu ions
AHS pe o med sampling and da a analyses and w o e he manusc ip . PR
pe o med chemical analyses and p epa ed he manusc ip . AK pe o med
da a analyses. DM pe o med da a analyses and p epa ed he manusc ip . VO
pe o med da a analyses. AP pe o med da a analyses. HK pe o med chemi‑
cal analyses and p epa ed he manusc ip . SL pe o med sampling and da a
analyses and p epa ed he manusc ip . MN p epa ed he manusc ip . MV p e‑
pa ed he manusc ip p epa ing. AH pe o med da a analyses and p epa ed
he manusc ip . All au ho s ead and app o ed he inal manusc ip .
Au ho de ails
1 Depa men o Biology, Uni e si y o Oulu, P.O. Box 3000, 90014 Oulu,
Finland. 2 Depa men o En i onmen al Heal h, Na ional Ins i u e o Heal h
and Wel a e, P.O. Box 95, 70701 Kuopio, Finland. 3 The All‑Russian S a e
Cen e o Quali y and S anda diza ion o Ve e ina y D ugs and Feed (VGNKI),
Z enigo odskoe Highway 5, Moscow, Russian Fede a ion 123022. 4 Uni e si y
o Helsinki, Nu miniemen ie 2, 93600 Kuusamo, Finland. 5 Reindee Resea ch
S a ion, Finnish Game and Fishe ies Resea ch Ins i u e, Toi oniemen ie 246,
99100 Kaamanen, Finland. 6 Depa men o En i onmen al and Biological
Sciences, Uni e si y o Eas e n Finland, 70211 Kuopio, Finland. 7 Risk Assess‑
men Resea ch Uni , Finnish Food Sa e y Au ho i y E i a, Mus ialanka u 3,
00790 Helsinki, Finland.
Acknowledgemen s
Finnish Food Sa e y Au ho i y E i a, Finnish Cul u al Founda ion and Thule‑
ins i u e and Oulun läänin Talousseu an maa aloussää iö a e acknowledged
o unding o his s udy. The s a o Uni o Chemical Exposu e in THL is
hanked o hei echnical assis ance.
Compe ing in e es s
The au ho s decla e ha hey ha e no compe ing in e es s.
Recei ed: 13 Oc obe 2015 Accep ed: 27 Janua y 2016
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