Laaksonen e al. Ac a Ve Scand (2017) 59:17
DOI 10.1186/s13028-017-0286-z
RESEARCH
Is anspo dis ance co ela ed
wi hanimal wel a e andca cass quali y
o eindee (Rangi e a andus a andus)?
Sauli Laaksonen1*, Pikka Jokelainen2,3,4, Jy ki Pusenius5 and An i Oksanen6
Abs ac
Backg ound: Slaugh e eindee a e exposed o s ess caused by ga he ing, handling, loading and unloading, and
by condi ions in ehicles du ing anspo . These s ess ac o s can lead o comp omised wel a e and auma such
as b uises o ac u es, aspi a ion o umen con en , and abno mal odou in ca casses, and causing condemna ions
in mea inspec ion and lowe mea quali y. We in es iga ed he s a is ical associa ion o slaugh e anspo dis ance
wi h hese indices using mea inspec ion da a om yea s 2004–2016, including inspec ion o 669,738 eindee o igi-
na ing om Finnish eindee he ding a eas.
Resul s: Inc eased s ess and dec eased wel a e o eindee , as indica ed by highe incidence o ca cass condem-
na ion due o b uises o ac u es, aspi a ion o umen con en , o abno mal odou , we e posi i ely associa ed wi h
sys ems in ol ing sho e anspo dis ances o aba oi s. Signi ican di e ences in incidence o condemna ions we e
also de ec ed be ween aba oi s and eindee he ding coope a i es.
Conclusions: This s udy indica es ha in pa icula he sho -dis ance anspo s o eindee me i mo e a en ion.
While he esul s sugges ha ac o s associa ed wi h long dis ance anspo , such as d i e educa ion, uck design,
e e ina y supe ision, and specialis equipmen , may be a ou able o educing p e-slaugh e s ess in eindee
when compa ed wi h sho dis ance anspo sys ems, which occu in a a ie y o ehicle ypes and may be done by
un ained handle s. Fu he wo k is equi ed o elucida e he causal ac o s o he cu en esul s.
Keywo ds: Reindee , Mea inspec ion, S ess, Handling, T anspo , T auma, Aspi a ion o umen con en , Abno mal
odou , Wel a e
© The Au ho (s) 2017. 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 License
(h p://c ea i ecommons.o g/licenses/by/4.0/), which pe mi s un es ic ed use, dis ibu ion, and ep oduc ion in any medium,
p o ided you gi e app op ia e c edi o he o iginal au ho (s) and he sou ce, p o ide a link o he C ea i e Commons license,
and indica e i changes we e made. The C ea i e Commons Public Domain Dedica ion wai e (h p://c ea i ecommons.o g/
publicdomain/ze o/1.0/) applies o he da a made a ailable in his a icle, unless o he wise s a ed.
Backg ound
In Fennoscandia, semi-domes ica ed eindee a e g az-
ing mos o he yea eely on na u al pas u es. T adi-
ionally, eindee we e slaugh e ed on he ield du ing
ound-ups, and no anspo a ion o slaugh e houses
was needed. Field slaugh e acili ies we e e ec ed ad
hoc un il he 1980s, a which ime slaugh e ing mo ed
o mo e de eloped and mode n expo aba oi s. Nowa-
days, mos o he eindee in Finland a e slaugh e ed in
o icially app o ed aba oi s. The de elopmen o a ne -
wo k o egional aba oi s c ea ed he need o in ensi e
anspo a ion o li e eindee and led o he e olu ion o
eindee anspo a ion [1].
Mos o he anspo a ion o li e eindee by mo o
ehicles akes place o slaugh e in au umn and ea ly
win e [1]. The ehicles include ans and aile s, and
o longe dis ances, special eindee anspo ucks.
In addi ion o anspo ing o slaugh e , ehicle ans-
po a ion is occasionally used when eindee a e mo ed
be ween pas u es, o o supplemen a y eeding si es o
co als o win e mon hs. Mo o ehicles, helicop e s,
snow mobiles and quad bikes (ATVs) a e used as aids
when he ding and ga he ing eindee o summe o
au umn (slaugh e ) ound-ups.
In Finland, all animal anspo a ion is egula ed by
he Finnish Animal T anspo Ac (1429/2006) and he
Open Access
Ac a Ve e ina ia Scandina ica
*Co espondence: [email p o ec ed]
1 Depa men o Ve e ina y Biosciences, Facul y o Ve e ina y Medicine,
Uni e si y o Helsinki, P.O. Box 66, 00014 Helsinki, Finland
Full lis o au ho in o ma ion is a ailable a he end o he a icle
Page 2 o 8
Laaksonen e al. Ac a Ve Scand (2017) 59:17
Council Regula ion (EC) No 1/2005 on he p o ec ion o
animals du ing anspo and ela ed ope a ions. The e is
no speci ic ac o eindee and hus hese egula ions a e
also alid o he anspo a ion o eindee .
Any ex e nal s imulus ha challenges homeos asis can
be iewed as a s esso o animals [2]. Emo ional s imuli
a e he mos common and impo an s esso s in animals
wi h a highly de eloped ne ous sys em [3–6]. Animals
eac di e en ly when hey a e cap u ed, es ained, o
immobilized. E en animals ha seem o adap o he
si ua ion may su e om s ess and be ulne able o
ela ed damaging changes [7, 8]. T anspo a ion is known
o cause subs an ial s ess in domes ica ed animals [9,
10] and i likely p o okes an e en mo e se e e s ess
esponse in semi-domes ica ed animals.
The anspo a ion and i s impac on he wel a e o
semi-domes ica ed eindee has been an issue o con-
ce n in Fennoscandia. The anspo a ion o slaugh e
includes p e-slaugh e handling o he animals; ound-
ing up, he ding, holding in enclosu es, manual handling,
loading, oad anspo , and unloading. A e he ans-
po o eindee , aumas a e commonly ound [11–13].
T auma may be caused by a physical impac by an le s,
hoo es, me al o wooden p ojec ions, o animals alling
and being ampled on by o he s. Such auma can ake
place any ime du ing handling, anspo , holding, o
s unning. B uises can a y in size, and be supe icial o
se e e and may be seen in di e en pa s o he ca cass o
e en o e he en i e ca cass.
Reindee , like wild animals, a e suscep ible o s ess
caused by human p esence, handling, cap u ing, and
anspo a ion. Manual handling and es ain ha e been
ound o be one o he majo s ess ac o s o eindee
[12–15]. The e a e indica ions o a cumula i e e ec o
epea ed s ess e en s. In he ded eindee , s ess asso-
cia ed lesions, such as abomasal haemo hage, as well
as myoca dial and muscula degene a ion ha e been
desc ibed [11, 13–15]. Physical auma also cause s ess,
bu as hey a e o en he esul o agg ession by o he ani-
mals in he c a e, hey may also be conside ed a esul o
s ess beha iou [12].
The de imen al e ec s o p e-slaugh e handling on
blood chemis y (aspa a e ansaminase (ASAT), u ea,
co isol) and muscle glycogen s o es can cause inc eased
pH alues esul ing in lowe mea quali y; hese e ec s
ha e been demons a ed in se e al Fennoscandian s ud-
ies [12–22]. Managemen and handling s ess a e also
e lec ed by an inc ease in numbe s o bo h imma u e
and ma u e neu ophils and a dec ease in lymphocy e
coun , which is co ela ed o he deg ee o s ess o which
he animals ha e been exposed. P olonged exposu e o
s ess esul s in a dec ease in he numbe o eosinophils
in pe iphe al blood [12].
Rehbinde e al. [12], Rehbinde [13] and Wiklund
e al. and [14, 20] demons a ed ha he use o a lasso
o cap u e eindee o slaugh e was he mos s ess ul
handling p ocedu e among hose s udied. In hese s ud-
ies, lo y anspo , helicop e he ding, and ixa ion o
animals by hand wi hou he use o a lasso esul ed in
lowe s ess esponses as measu ed by mea pH alues,
blood me aboli es used as s ess ma ke s i.e. ASAT, u ea
and co isol, and abomasal lesions, compa ed o he lasso
cap u e p ocedu e. The cal es ha e been epo ed o ha e
highe muscle pH [19] and plasma u ea [12, 13] alues
a e he ding and handling s ess han adul s. The au ho s
concluded ha cal es a e mo e suscep ible o s ess han
adul animals due o mo e igo ous physical exe ion
deple ing hei ene gy s o es mo e apidly. Exhaus ed
animals we e in gene al ound o ha e ex emely high
mea pH alues, wi h 31.1% o he ca casses being clas-
si ied as in e media e Da k, Fi m and D y mea (DFD)
(5.8<pH<6.2) and 31.2% as DFD (pH>6.2) [19].
Na u al long-du a ion s ess, such as ha sh wea he
and snow condi ions especially in win e ime, can also
cause poo e mea quali y; glycogen s o es a e used
be o e slaugh e and he pH- alue emains high [14, 23].
In addi ion, he animals’ physical condi ion and nu i-
ional s a us ha e a conside able e ec on hei abili y o
ole a e a ious s ess ac o s, such as lo y anspo and
holding [20].
Hy ä inen e al. [16] ound ele a ed se um u ea al-
ues associa ed wi h eindee ga he ings. Fu he mo e,
he le els we e co ela ed wi h he dis ance o he d i e
and ime spen in he co al. The s udy by Wiklund e al.
[15] con i med he inding ha a “s ess- la ou ” could
de elop in eindee mea a e in ensi e p e-slaugh e
handling o he animals. The animals cap u ed by use o
lasso o he ded by helicop e o p olonged h ee days
had he highes sco es o an unpleasan , s ong, e en
ac id smell, which was desc ibed by a ained expe
panel as a pungen odou , sickeningly swee odou , sha p
la ou , and sickeningly swee la ou [15]. I is com-
mon knowledge among eindee he de s ha animals
ha ha e been exposed o s ess ul p e-slaugh e han-
dling gi e mea wi h an un a ou able odou [15] which
is some imes e e ed o as “u ine smell” [1, 13]. Se e al
s udies ha e ied o co ela e he concen a ions o sub-
s ances such as pu escine, spe midine, spe mine, c e-
a ine, c ea inine, and dime hylamine in eindee mea
and plasma wi h he p esence o ‘s ess- la ou ’ in he
mea , bu he issue is s ill un esol ed, as e iewed by
Wiklund [15]. Acco ding o Rehbinde [13], deple ion
o muscula glycogen s o es, inc eased ca abolism o
muscula p o ein, muscula degene a ion, and inc eased
blood-u ea le els canno be excluded as a cause o an
al e ed and bad as e o he mea .
Page 3 o 8
Laaksonen e al. Ac a Ve Scand (2017) 59:17
In Sweden, lo y anspo did no a ec he ul ima e pH
o he muscles o bulls and cal es and he incidence o high
pH and in e media e DFD in eindee hinds was g ea e
only a e anspo o mo e han 500km [19]. In Finland,
Nieminen e al. s udied he impac o anspo a ion o
eindee in 1993 [24] and in 2000 [25]. In hese s udies,
he anspo a ion dis ances a ied om 30 o 400km and
anspo a ion imes om 1 o 5.5h. The eindee we e
epo ed o be peace ul and in good shape a e anspo -
a ion and only mino b uises we e de ec ed.
Aspi a ion o umen con en du ing s unning is a com-
mon inding du ing slaugh e in p oduc ion uminan s,
leading o he condemna ion o lungs a mea inspec ion
[26]. The e is, howe e , appa en ly, no published da a o
he causes o incidence o his phenomenon. Aspi a ion
o umen con en is also o en seen du ing eindee mea
inspec ion. Hanssen e al. [27] epo ed he anspo a-
ion o eindee on lo ies o esul in mo e liquid umen
con en . In addi ion, a ma ked s ess esponse wi h abo-
masal e osions o ulce s will a ec he diges i e ac and
i s u iliza ion o odde [13, 15]. I is also common ha
diges i e diso de s occu amongs eindee a e sup-
plemen a y eeding [1, 28]. Reindee a e usually supple-
men a y ed wi h silage and pelle s [1], which o en leads
o ullness and dis ension o he umen. These eeds a e
medium o high p o ein ich, which g ea ly inc eases
hei wa e equi emen s. Fo example, adul emale ein-
dee ea ing pelle s ha e been epo ed o d ink 3.2–3.5l
o wa e pe day, while eindee ed lichens d ank only
0.1l pe day [29]. Mo e liquid umen con en may pe -
haps p edispose o egu gi a ion and aspi a ion o umen
con en du ing s unning.
The e has been a lo o public deba e conce ning he
long-dis ance anspo a ion o eindee by mo o ehi-
cles; in pa icula , wi h ega ds o he e ec o ans-
po a ion on he wellbeing o he eindee . The aim o
his s udy was o pa ially espond o hese conce ns by
explo ing whe he he dis ance o he anspo a ion o
li e eindee o aba oi s is associa ed wi h highe a es
o mea condemna ions. We ocused on inju ies, b uises
and ac u es, bu s ess- ela ed abno mal odou and
aspi a ion o umen con en we e also su eyed. The
ou comes in es iga ed a e no only indica o s o com-
p omised wel a e bu also ele an o he b and and ep-
u a ion o eindee mea p oduc ion.
Me hods
The eindee popula ion da a we e ob ained om da abase
o he Reindee He de s’ Associa ion. The eindee mea
inspec ion da a we e collec ed om o icial documen s
om mea inspec ion e e ina ians (see Addi ional ile1)
a all he app o ed eindee aba oi s o Finland, om he
slaugh e seasons (au umn and ea ly win e ) 2004–2005
o 2015–2016. The mea inspec ion and hygiene con ol in
aba oi s was conduc ed by e e ina ians who wo k unde
he con ol o Regional S a e Adminis a i e Agencies o
Lapland. Fo his s udy, he numbe o b uises and ac-
u es and s ess- ela ed abno mal odou and aspi a ion
o umen con en , which lead o pa ly o o al ca cass
condemna ions o human consump ion, we e included.
We eco ded he numbe o inspec ed eindee o igina -
ing om Finnish eindee he ding a eas (669,738 ein-
dee om 4208 slaugh e ba ches), he numbe and he
pe cen age o condemna ions due o b uises o ac u es,
aspi a ion o umen con en du ing s unning, and o gano-
lep ic e alua ions o abno mal odou .
S a is ical analyses
Fo s a is ical analyses, he anspo a ion dis ances we e
classi ied in o i e ca ego ies: 0=0km, eindee walk
om he ound-up co al o aba oi ; (1) 1–60km; (2)
61–150km; (3) 151–300km; (4)>300km. The anspo
dis ances o each slaugh e ba ch we e de ined o be he
sho es dis ance along he oad om he geog aphical
cen e o he eindee he ding coope a i e o he aba -
oi . In addi ion, he eindee we e classi ied acco ding o
hei egion o o igin: The Finnish eindee he ding a ea
was di ided in o he a ea speci ically in ended o ein-
dee he ding (A ea 2, no he n pa ) (Finnish Reindee
Husband y Ac , 14.9.1990/848) and he emainde (A ea
1, sou he n pa ) (Fig.1).
We analysed he associa ion be ween he occu ence o
b uises o ac u es, abno mal odou , and aspi a ion o
umen con en leading o condemna ions and he ans-
po dis ance o eindee o aba oi s using Spea man’s
ank co ela ion coe icien . The ela ionship be ween
he egional o igin o eindee and he p opo ion o con-
demna ions was analysed using wo by wo con ingency
ables and Chi squa ed es s.
The compa ison o p opo ion o condemna ions
be ween aba oi s and 56 eindee he ding coope a i es
was made by using non-pa ame ic K uskal–Wallis es
using slaugh e ba ch as a uni o obse a ion. In one
aba oi , animals we e bled in he ho izon al posi ion (as
opposed o e ical posi ion). To de e mine i he p opo -
ion o animals aspi a ing umen con en s di e ed in his
aba oi compa ed o he o he s, we used a pos hoc mul-
iple compa ison analysis iden i ying homogenous sub-
se s (signi icance le el 0.05).
All s a is ical analyses we e conduc ed using SPSS 19
so wa e.
Resul s
The eindee popula ion in Finland du ing he s udy
pe iod was on a e age 197,807 (190,776–209,365) indi-
iduals, o which an a e age o 102,778 (71,580–124,152)
Page 4 o 8
Laaksonen e al. Ac a Ve Scand (2017) 59:17
we e slaugh e ed annually. O he slaugh e ed eindee ,
77% we e cal es (6–8mon hs old). App oxima ely 74%
o he eindee we e slaugh e ed in 19 EU-app o ed
eindee aba oi s; he es we e slaugh e ed in he ield
o p i a e consump ion and di ec ma ke ing (Regional
S a e Adminis a i e Agencies o Lapland).
The inspec ion da a o 669,738 eindee (A ea 1,
234,821; A ea 2, 434,917) om 4208 slaugh e ba ches
(A ea 1, 2318; A ea 2, 1890) we e included in he s udy;
da a om 333 slaugh e ba ches we e excluded because
o missing in o ma ion. Eigh y- h ee pe cen o he
eindee we e slaugh e ed du ing Oc obe –Decembe .
The a e age dis ance ha animals we e anspo ed o
slaugh e was 87km ( ange: 0–450km) in he whole a ea,
62km (10–390km) in he sou he n a ea (A ea 1), and
117km (0–450km) in he no he n a ea (A ea 2).
The mea inspec ion indings associa ed wi h pa o
whole ca cass condemna ion om 2004 o 2016 a e p e-
sen ed by egion in Table1, (Fig.1). B uises and ac u es,
and aspi a ion o umen con en , we e mo e common in
A ea 1 compa ed o A ea 2 (Table1; χ2=50.58, d =1,
P<0.001; χ2=2212.93, d =1, P<0.001; espec i ely).
The anspo dis ance o he aba oi was nega-
i ely co ela ed wi h he numbe o condemna ions
due o b uises/ ac u es (Spea man’s ank co ela ion
s=−0.20, N=4208, P<0.0005), aspi a ion o umen
con en ( s=−0.04, N=4208, P=0.005), and abno -
mal odou ( s=−0.04, N=4208, P=0.011). The co -
ela ions o aspi a ion o umen con en and abno mal
odou wi h a el dis ance we e howe e weak, whe eas
he nega i e co ela ion be ween he condemna ions due
o b uises and ac u es and anspo dis ance indica ed
a de ini e and s ong ela ionship.
The numbe o b uises and ac u es leading o con-
demna ions du ing eindee mea inspec ions a e p e-
sen ed by he i e anspo dis ance ca ego ies in
Table 2. Mul iple compa ison a e K uskal–Wallis
ANOVA indica ed ha he incidence o b uises and ac-
u es was lowe in he anspo a ion dis ance ca ego y
0 (no anspo ) han in he anspo a ion dis ance ca -
ego y 1 (1–60km) (P<0.05). The slaugh e ba ches we e
smalle in he ca ego ies o sho anspo han in he
ca ego y o no ehicle anspo (280 and 123 eindee
espec i ely).
The e we e signi ican di e ences be ween aba oi s in
he incidence o b uises and ac u es ( ange 0.20–2.02%,
Fig. 1 Finnish eindee he ding a ea indica ing he a ea speci ically
in ended o eindee he ding (A ea 2, no he n pa ) and he emain-
de (A ea 1, sou he n pa ). Fine lines a e he bo de s o eindee he d-
ing coope a i es and he ed s a s a e o icial eindee aba oi s
Table 1 Indica o s o comp omised wel a e o eindee leading omea inspec ion condemna ions inFinland (2004–
2016)
a The map showing he a eas: Fig.1
O igin o
eindee aNo o eindee Mean anspo a ion
dis ance (km) B uises and
ac u es (n, %) Aspi a ion o umen
con en (n, %) Abno mal
odou (n, %)
A ea 1 234,821 62 1533
0.6% 1265
0.54% 65
0.03%
A ea 2 434,917 117 2246
0.5% 36
0.008% 126
0.03%
Whole a ea 669,738 87 3779
0.6% 1301
0.2% 191
0.03%
Page 5 o 8
Laaksonen e al. Ac a Ve Scand (2017) 59:17
mean 0.71%, SD 2.93%; K uskal–Wallis es , H=564.73,
d =19, P<0.0005), umen con en aspi a ions ( ange
0.00–2.47, 0.50%, SD 3.02%; K uskal–Wallis es ,
H=660.94, d =19, P<0.0005) and abno mal odou
( ange 0.00–0.74%, 0.08%, SD 1.77%; K uskal–Wallis
es , H=109.54, d =19, P<0.0005) as well as be ween
all 56 eindee he ding coope a i es ( ange 0.00–7.69%,
0.74%, SD 3.07%; K uskal–Wallis es , H = 523.07,
d =55, P<0.0005), ( ange 0.00–3.22%, 0.53%, SD 3.15%;
K uskal–Wallis es , H=612.35, d =55, P<0.0005),
( ange 0.00–0.68%, 0.08%, SD 1.85%; K uskal–Wallis es ,
H=91.81, d =55, P=0.001), espec i ely.
Mul iple compa isons iden i ying homogenous sub-
se s (signi icance le el 0.05) indica ed ha condemna ion
caused by aspi a ion o umen con en was on a e age
highe in he aba oi in which he bleeding a e s un-
ning was done on animals ha we e lying ho izon ally
(2.4%), compa ed o hose in which he animals we e bled
while hanging e ically (0.2%).
Discussion
Ou esul s indica e ha he s udied indica o s o com-
p omised physical wel a e o slaugh e eindee a e asso-
cia ed wi h he dis ance o anspo a ion o slaugh e :
sho anspo dis ances we e associa ed wi h mo e
comp omised eindee wel a e and ca cass quali y. In
addi ion, we ound ha he incidence o hese indica o s
a ied signi ican ly among eindee he ding coope a i es
and aba oi s.
B uises and ac u es we e nega i ely associa ed wi h
anspo dis ance. This pe haps unexpec ed inding
could be explained by he ac ha mos long-dis ance
anspo o slaugh e eindee is done wi h ucks ha
a e speci ically designed o he anspo a ion o ein-
dee . These ucks mus be inspec ed and app o ed by
au ho i ies and he d i e mus be speci ically educa ed
o be quali ied and licenced o long- ange animal ans-
po a ion. The ucks ha e specially designed amps o
loading and unloading eindee wi h minimal manual
handling and hey a e sec ioned in o se e al pens ha
allow sepa a ion o cal es om adul animals, which
ma kedly educes b uising and o he inju ies [11]. Con-
e sely, anspo a ion o eindee o sho (unde
65km) dis ances does no equi e any quali ica ions o
app o als o he d i e s no he ehicles. Vans o ail-
e s, which may in some cases be un i , a e used o he
sho -dis ance anspo a ion, and he loading and
unloading is done manually, eindee by eindee . Ou
esul s, he e o e, sugges ha he quali y o he me hod
o anspo a ion mo e han compensa es he po en ial
nega i e e ec s o long-dis ance anspo a ion. How-
e e , he inding ha lowe p opo ion o eindee ha
we e slaugh e ed wi hou ehicle anspo had auma ic
lesions han eindee ha unde wen sho anspo ,
indica es he impac o manual loading, unloading and
he sui abili y o he anspo ehicle on he inju ies.
Ou esul ha he p opo ion o eindee ha ing
b uises/ ac u es de ec able in mea inspec ion did no
inc ease wi h he dis ance o anspo a ion o aba -
oi is in acco dance wi h o me s udies on he e ec s
o anspo a ion. In line wi h ou conclusions, p e ious
s udies [19, 20, 24, 25], epo ed ha lo y anspo did
no signi ican ly impai eindee mea quali y indices. In
addi ion, he his o ical mea inspec ion da a om yea s
1980–1986 [33] indica ed ha b uises and ac u es we e
common and we e de ec ed in 5.3% o he eindee . This
was in spi e o he ac ha only 11.5% o he eindee
we e anspo ed o he app o ed egional aba oi s and
he es we e slaugh e ed in he ield in connec ion o, o
e y nea he ound-up places, p ac ically wi h no need
o ehicle anspo [33].
The signi ican di e ences in he appea ance o b uises
and ac u es be ween indi idual coope a i es and aba -
oi s may be due o he di e en handling p ac ises. Fo
example, ound-ups and hei iming, main enance o
enclosu es, anspo co ido s and amps, ou ines
o loading and unloading he animals, wai ing imes in
co als and in aba oi s, and unde s anding he na u al
Table 2 B uises and ac u es leading ocondemna ions du ing eindee mea inspec ions, by anspo dis ance ca ego-
ies
T anspo dis ance Inspec ed
eindee (n) Inspec ions (n) Reindee in
inspec ions (mean) B uises and
ac u es (n) B uises and
ac u es (%)
km Ca ego y
0 0 129,521 464 280 590 0.45
1–60 1 260,688 2123 123 1970 0.75
61–150 2 124,402 1038 120 743 0.60
151–300 3 89,124 328 272 386 0.43
≥301 4 66,005 255 259 90 0.13
To al 669,740 4208 159 3779 0.56
Page 6 o 8
Laaksonen e al. Ac a Ve Scand (2017) 59:17
beha iou , as highligh ed in li e a u e [12–15, 34], as well
as he deg ee o ameness o eindee [13], may di e .
The e a e no s unning pens in Finnish eindee aba oi s
o suppo he animal, bu he es ain is done manually,
so b uising is also possible du ing he s unning and could
occu also a e s unning when he animal collapses on
he loo [35].
In o al, he cu en slaugh e wel a e condi ions in
Finland can be conside ed ela i ely good, wi h 0.6% o
slaugh e eindee ha ing de ec able inju ies, in pa icu-
la when compa ing wi h he si ua ion in pe iod 1980–
1986, when b uises and ac u es we e epo ed in 5.6%
o eindee [33]. The si ua ion has e ol ed in he same
way also in Sweden: du ing 2000–2007, he p opo ion
o inju ies was 1% [36] and du ing 2006–2013, auma o
ac u es we e egis e ed in 0.13% o eindee ca casses
and in 0.88% o he heads [37]. I mus be no ed ha ou
da a do no include he aumas in he head, which a e
ypically seen in an le s, because such auma do no usu-
ally lead o condemna ions.
The appa en ly educed incidence o b uises and
ac u es is likely due o he inc eased in o ma ion and
educa ion deli e ed by he Reindee He de s’ Associa-
ion and ela ed o ganiza ions and au ho i ies which
has led o imp o ed handling me hods and anspo s.
One con ibu ing ac o can also be he ac ha in
Finland, especially in he no he n eindee he ding
a ea, e e ina ians a e p esen p ac ically in e e y big-
ge slaugh e ound-up, adminis a ing an i-pa asi ic
ea men and a he same ime doing animal wel a e
wo k, o example inspec ing he i ness o animals o
anspo a ion.
Rumen con en can become mo e liquid because o
handling s ess [13, 15], anspo a ion [27] and supple-
men a y eeding [28, 29]. This may p edispose animals
o aspi a ion o liquid umen con en s du ing o a e
s unning. In ou s udy, aspi a ion o umen con en was
epo ed in 0.2% o Finnish slaugh e eindee . The nega-
i e co ela ion o he dis ance o slaugh e anspo was
no as clea as in b uises and ac u es, while he e we e
signi ican di e ences be ween indi idual coope a i es
and aba oi s. In addi ion, aspi a ion o umen con en
was a signi ican ly mo e common inding in he eindee
om A ea 1 compa ed o A ea 2, e lec ing dec eased
wel a e and suppo ing ha i could be associa ed wi h
handling, anspo , beha iou al and eeding s ess.
In he sou he n a ea, eindee a e o en held in lai age,
wai ing o he he d o g ow big enough o he slaugh e
ba ch, some imes se e al days. Du ing ha ime, hey a e
supplemen a y ed, usually wi h silage and pelle s, which
o en leads o he ullness and dis ension o he umen
(unpublished obse a ions).
Du ing s unning, especially i he bol ing accu acy o
ca idge s eng h a e no ideal, he unconsciousness is
no immedia e and eindee con inue o b ea he which
can esul in egu gi a ion and aspi a ion o umen con-
en . I is known ha slaugh e wi hou s unning ( i ual
slaugh e ) inc eases he possibili y o aspi a ion o blood
and, in he case o uminan s, umen con en [30]. All
Finnish eindee aba oi s use pene a ing cap i e bol
pis ols o s un eindee . I is concluded ha an animal
e ec i ely s unned wi h a pene a ing cap i e bol pis-
ol, as indica ed by he p esence o ce ain signs and
he absence o o he s, like ailu e o collapse, hy hmic
b ea hing, eyeball o a ion and, posi i e co neal e lex,
has li le possibili y o a e e sal o he b ain unc ion
[31]. Howe e , in ca le, he p e alence o shallow dep h
o concussion ollowing cap i e bol shoo ing was 8% o
all ca le and 15% o young bulls, and 2.7% o animals
main ained spon aneous b ea hing [32]. I is likely ha
his happens also du ing eindee slaugh e .
The inding ha aspi a ion o umen con en was mo e
common i he bleeding was done when he eindee
we e in ho izon al posi ion compa ed o hose aba oi s
whe e eindee we e in a hanging posi ion, was no su -
p ising. I is logical ha he egu gi a ion can each lungs
mo e easily i he animal is in ho izon al posi ion du ing
commonly occu ing e lexi e gasping [32]. Aspi a ion o
umen con en is also a conce n o mea hygiene, since
po en ial pa hogens a e anspo ed o he clean side o
he aba oi and can con amina e o he ca casses and
o gans [38, 39].
“S ess la ou ” occu s in eindee mea a e in en-
si e handling o he animals p io o slaugh e [15, 18,
20]. In ou s udy, he inding egis e ed was abno mal
odou , which may include also o he odou s diagnosed by
mea inspec o s. A s ong abno mal odou which lead o
condemna ions was diagnosed in 0.03% o eindee . The
eal incidence o abno mal la ou is likely much highe ,
o example, Hanssen and Skei [40] de ec ed mode a e
ammonia-like ain in wo and a weak ain in se en sam-
ples o 29 eindee which had been anspo ed in lo ies
be o e slaugh e . Ne e heless, ou esul s show ha he
same end as o b uises, ac u es and umen con en
aspi a ion was also de ec ed in abno mal odou , ha ing a
nega i e co ela ion wi h anspo dis ance and wi h sig-
ni ican di e ences be ween aba oi s and coope a i es.
These pa e ns a e in acco dance wi h he published
iews ha de ec ing abno mal odou is ela ed o s ess
[15, 18, 20, 27, 40].
The e a e many mo e ac o s associa ed wi h anspo
and connec ed ope a ions ha could con ibu e o he
obse ed e ec o anspo dis ance and ha we e no
co e ed in his wo k. These include handling, holding,
Page 7 o 8
Laaksonen e al. Ac a Ve Scand (2017) 59:17
habi ua ion, sex e ec , socialisa ion, s unning, and he
slaugh e p ocess. The di e ences in incidence be ween
aba oi s and he ding coope a i es ein o ce his u he .
Ou s udy was based on he obse a ions and mea
inspec ion indings made by se e al e e ina ians,
which may cause bias on he esul s. All he eindee
mea inspec o s ha e pa icipa ed in educa ion o mea
inspec ion and ha monizing mea inspec ion decisions,
and he epo ing is simple. The s eng hs o he s udy
include a long s udy pe iod (>10yea s) and a la ge num-
be o obse a ions, and he da a we e collec ed om
o icial mea inspec ion decisions o condemna ions.
Because mino lesions and deep b uises, a e no always
de ec able in he mea inspec ion, he ue incidence o
hese indica o s is likely highe .
Conclusions
Long dis ance anspo o eindee in app o ed ein-
dee ucks and conduc ed by educa ed d i e s was asso-
cia ed wi h less s ess and auma o he animals han
anspo o sho dis ances, he la e equi ing mo e
manual handling, being conduc ed in a a ie y o ehicle
ypes, and by un ained handle s. Al hough he wel a e
o eindee du ing anspo a ions and connec ed ac i i-
ies has imp o ed, signi ican di e ences in incidence o
b uises o ac u es, aspi a ion o umen con en , and
abno mal odou we e de ec ed be ween aba oi s and
be ween eindee he ding coope a i es, emphasizing ha
he e s ill is oom o imp o emen . Al hough u he
esea ch is equi ed o elucida e he impac o all ac o s
ha a e in ol ed in anspo a ion and ha may be asso-
cia ed wi h s ess and wel a e o eindee , he esul s o
his s udy indica e ha in pa icula he sho -dis ance
anspo s and ela ed ope a ions me i mo e a en ion.
This is likely no limi ed o slaugh e anspo , bu a he
ele an o all anspo a ion o eindee e.g. o a eeding
co al o o a di e en pas u e a ea.
Au ho s’ con ibu ions
SL designed he s udy. JP pe o med he s a is ical analyses. The esul s we e
in e p e ed by SL, PJ and JP. SL and PJ d a ed he manusc ip . All au ho s
pa icipa ed in w i ing and edi ing o he manusc ip . All au ho s ead and
app o ed he inal manusc ip .
Au ho de ails
1 Depa men o Ve e ina y Biosciences, Facul y o Ve e ina y Medicine, Uni e -
si y o Helsinki, P.O. Box 66, 00014 Helsinki, Finland. 2 Es onian Uni e si y o Li e
Sciences, K eu zwaldi 62, 51014 Ta u, Es onia. 3 Facul y o Ve e ina y Medicine,
Uni e si y o Helsinki, P.O. Box 66, 00014 Helsinki, Finland. 4 S a ens Se um
Ins i u , A ille i ej 5, 2300, Copenhagen S, Denma k. 5 Na u al Resou ces
Ins i u e Finland, Yliopis oka u 6, 80100 Joensuu, Finland. 6 P oduc ion Animal
Addi ional ile
Addi ional ile1. Mea inspec ion decision o eindee slaugh e in
Finland ( ansla ed om Finnish).
and Wildli e Heal h Resea ch Uni , Finnish Food Sa e y Au ho i y E i a, Elek o-
niikka ie 3, 90590 Oulu, Finland.
Acknowledgemen s
We hank he eindee he de s and eindee e e ina ians in Finland and he
c ew o Regional S a e Adminis a i e Agencies o Lapland o hei coope a-
ion in da a collec ion. Special hanks goes o Juho Tahkola. We also hank
Anniina Holma-Suu a i who was in ol ed in planning and d a ing o his
wo k and Susan Ku z o e ising he English o he manusc ip . This wo k was
done in he p ojec “Reindee heal h in he changing en i onmen 2015–2018”
unded by he Finnish Minis y o Ag icul u e and Fo es y (MAKERA).
Compe ing in e es s
The au ho s decla e ha hey ha e no compe ing in e es s.
A ailabili y o da a and ma e ials
The da ase s analysed du ing he cu en s udy a e no publicly a ailable due
o including con iden ial da a on diseases o eindee om eindee he ding
coope a i es and aba oi s. The decision o Regional S a e Adminis a i e
Agencies o Lapland Dno. LAAVI/171/03.02.01/2015.
Funding
The s udy was pa ly unded by he Finnish Minis y o Ag icul u e and
Fo es y (MAKERA).
Recei ed: 20 Oc obe 2016 Accep ed: 10 Ma ch 2017
Re e ences
1. Laaksonen S. Tunne po o–po on sai aude ja e eydenhuol o [Know he
eindee –diseases and heal h ca e o eindee ]. Riga: Li onia P in ; 2016.
2. Mobe g GP. Biological esponse o s ess: Key o assessmen o animal
well-being. In: Mobe g GP, edi o . Animal s ess. Bal imo e: Wa e ly P ess;
1985. p. 27–49.
3. Le i L. Emo ional s ess. P oceedings o an in e na ional symposium
a anged by he Swedish delega ion o applied medical de ense
esea ch, S ockholm, Feb ua y 5–6, 1965. Fo s a s-medicin. 1967;3:Suppl
2.
4. Selye H. S ess wi hou dis ess. New Yo k: Lippinco Williams & Wilkins;
1974.
5. S ephens DB. S ess and i s measu emen in domes ic animals: a e iew
o beha io al and physiological s udies unde ield and labo a o y
si ua ions. In: B andly CA, Co nelius CCE, edi o s. Ad ances in e e ina y
science and compa a i e medicine. New Yo k: Academic P ess; 1980. p.
179–210.
6. Becke BA. The phenomena o s ess: concep s and mechanisms associ-
a ed wi h s ess-induced esponses o he neu o-endoc ine sys em. Ve
Res Commun. 1987;11:444–56.
7. Ha hoo n AM. P oblems ela ed o cap u e. Anim Regul S ud.
1997;l:23–46.
8. Ba sch R, Connell EE, Imes GD, Schmid JM. A e iew o exe ional
habdomyolysis in wild and domes ic animals and man. Ve Pa hol.
1977;14:314–24.
9. D o ak M. Ad enoco ical ac i i y o young cal es in ela ion o anspo
and auma ic s ess. Docum Ve (B no). 1975;8:119–26.
10. Simensen E, Lakses ela B, Blom AK, Sjaas ad OV. E ec s o anspo a ions,
a high lac ose die and ACTH injec ions on he whi e blood cell coun ,
se um co isol and immunoglobulin G in young cal es. Ac a Ve Scand.
1980;21:278–90.
11. Ande sen G. T anspo skade på ein ed ulike anspo midle [T anspo
damage o eindee by di e en means o anspo ]. No sk Ve Tidsk .
1978;90:543–53.
12. Rehbinde C, Edq is L-E, Lunds om K, Villa ane F. A ield s udy o man-
agemen s ess in eindee (Rangi e a andus L.). Rangi e . 1982;2:2–21.
13. Rehbinde C. Managemen s ess in eindee . Rangi e . 1990;3:267–88.
14. Wiklund E, Ande sson A, Malm o s G, Lunds öm K. Muscle glycogen
le els and blood me aboli es in eindee (Rangi e a andus a andus L.)
a e anspo and lai age. Mea Sci. 1996;42:133–44.
Page 8 o 8
Laaksonen e al. Ac a Ve Scand (2017) 59:17
• We accep p e-submission inqui ies
• Ou selec o ool helps you o ind he mos ele an jou nal
• We p o ide ound he clock cus ome suppo
• Con enien online submission
• Tho ough pee e iew
• Inclusion in PubMed and all majo indexing se ices
• Maximum isibili y o you esea ch
Submi you manusc ip a
www.biomedcen al.com/submi
Submi you nex manusc ip o BioMed Cen al
and we will help you a e e y s ep:
15. Wiklund E, Malm o s G, Lunds öm K, Rehbinde C. P e-slaugh e
handling o eindee bulls (Rangi e a andus a andus L.)-e ec s on
echnological and senso y mea quali y, blood me aboli es and muscula
and abomasal lesions. Rangi e . 1996;3:109–17.
16. Hy ä inen H, Helle T, Nieminen M, Väy ynen P, Väy ynen R. Some e ec s
o handling eindee du ing ga he ings on he composi ion o hei
blood. Anim P od. 1976;22:105–14.
17. Nieminen M. The composi ion o eindee blood in espec o age,
season, cal ing and nu i ion. Oulu: Dep . o Zoology and Dep . o Physi-
ology, Uni e si y o Oulu; 1980.
18. Essén-Gus a sson B, Rehbinde C. The in luence o s ess on subs a e
u iliza ion in skele al muscle ib es o eindee (Rangi e a andus L.).
Rangi e . 1984;4:2–8.
19. Wiklund E, Ande sson A, Malm o s G, Lunds om K, Danell Ö. Ul ima e
pH alues in eindee mea wi h pa icula ega d o animal sex and age,
muscle and anspo dis ance. Rangi e . 1995;15:47–54.
20. Wiklund E. P e-slaugh e handling o eindee (Rangi e a andus a andus
L.) e ec s on mea quali y. Uppsala: Depa men o Food Science, Swed-
ish Uni e si y o Ag icul u al Sciences; 1996.
21. Wiklund E, Rehbinde C, Malm o s G, Hansson I, Danielsson-Tham
M-L. Ul ima e pH alues and bac e iological condi ion o mea and
s ess me aboli es in blood o anspo ed eindee bulls. Rangi e .
2001;21:3–12.
22. Wiklund E, Malm o s G, Fins ad G. Renkö - ä de all id mö , go och
ny ig ? [Reindee mea - i is always ende , as y and heal hy?]. Rangi e
Repo . 2007;12:71–7 (in Swedish wi h English abs ac ).
23. Pe ajä E. DFD mea in eindee mea . P oceedings: 29 h eu opean con-
g ess o mea esea ch wo ke s. I aly: Salsomaggio e; 1983. p. 117–24.
24. Nieminen M, Kumpula J, Soppela P, Heiska i U, Ris o A, Kan ola P. Teu -
aspo ojen elä änäkulje us, kulje uskokeilu ja u kimusp ojek i [T anspo
o li ing eindee o slaugh e house]. Ro aniemi: Po o u kimus; 1993.
25. Nieminen M. Teu aspo ojen elä änä kulje us–käsi elyn ja uokinnan
aiku ukse po oon sekä lihan kemialliseen koos umukseen ja laa uun
[T anspo o li ing eindee o slaugh e house– he impac o handling
and anspo o he composi ion and quali y o eindee mea ]. Finland:
Riis a- ja kala alouden u kimuslai os; 2000.
26. Gil JI, Du ão JC. A colou a las o mea inspec ion. Boca Ra on: Taylo &
F ancis; 1990.
27. Hanssen I, Ky kjebø A, Ops ad PK, P øsch R. Physiological esponses and
e ec on mea quali y in eindee (Rangi e a andus) anspo ed on lo -
ies. Ac a Ve Scand. 1984;25:128–38.
28. Nilsson A, Olsson I, Ling all P. Compa ison be ween g ass-silage o
di e en d y ma e con en ed o eindee du ing win e . Rangi e .
1996;16:21–30.
29. Soppela P, Nieminen M, Saa ela S. Wa e equi emen s o cap i e eindee
hinds wi h a i icial eeding. Rangi e Special Issue. 1988;1988(2):74–5.
30. Zoe hou CM. Ri ual slaugh e and he eedom o eligion: some e lec-
ions on a s unning ma e . Human Righ s Q. 2013;3:651–72.
31. G ego y N, Shaw F. Pene a ing cap i e bol s unning and exsanguina ion
o ca le in aba oi s. J Appl Anim Wel Sci. 2000;3:215–30.
32. G ego y NG, Lee CJ, Widdicombe JP. Dep h o concussion in ca le sho
by pene a ing cap i e bol . Mea Sci. 2007;77:499–503.
33. Rahkio M. Po on, hi en ja alkohän äpeu an lihan a kas us iedo
Suomessa uosina 1980–1986 [The mea inspec ion da a o eindee ,
moose and whi e- ailed dee in Finland in 1980–1986]. Helsinki: Eläin-
lääke ie eellinen ko keakoulu; 1988.
34. Mejdell CM, Heggs ad E, Hagen A, G øndahl AM. Hånd e ing og anspo
a am ein ed slak ing – dy e el e dsmessige u o d inge [Handling
and anspo o eindee a slaugh e - animal wel a e p oblems]. No sk
Ve Tidsk . 2014;2:126.
35. Belk KE, Scanga JA, Smi h GC, G andin T. The ela ionship be ween good
handling/s unning and mea quali y in bee , po k, and lamb. P oceedings
o he In e na ional Cong ess Animal Handling and S unning Con e ence
on Feb ua y 21–22, 2002 a he Ame ican Mea Ins i u e Founda ion.
2002. h p://www.g andin.com/mea /hand.s un. ela e.quali y.h ml.
Accessed Dec 2016.
36. Mossing T. Sammans ällning a besik nings esul a id enslak 2000–
2007 [Summa y o inspec ion esul s o eindee slaugh e in 2000–2007].
Umeå uni e si e . Gå d & Dju hälsan. 2007. h p://www.ga dochdju h-
alsan.se/upload/documen s/Dokumen /S a sida_And a_dju slag/
Ren/101020_ en_ appo _ enslak .pd . Accessed Dec 2016.
37. S a is ik ynd egis e ing id slak 2006–2013 [S a is ics o indings egis-
a ion a slaugh e 2006–2013]. Gå d & Dju hälsan. h p://www.ga doch-
dju halsan.se/upload/documen s/Dokumen /S a sida_And a_dju slag/
Ren/S a is ik_ ynd egis e ing_ id_slak _2006-2013.pd . Accessed Dec
2016.
38. Laaksonen S, Oksanen A, Julmi J, Zwei el C, F ed iksson-Ahomaa M,
S ephan R. P esence o oodbo ne pa hogens, ex ended-spec um
β-lac amase -p oducing En e obac e iaceae, and me hicillin- esis an
S aphylococcus au eus in slaugh e ed eindee in no he n Finland and
No way. Ac a Ve Scand. 2017;59:2. doi:10.1186/s13028-016-0272-x.
39. Zwei el C, Fie z L, Ce nela N, Laaksonen S, F ed iksson-Ahomaa M,
S ephan R. Cha ac e is ics o Shiga oxin-p oducing E. coli O157 in slaugh-
e ed eindee om no he n Finland. J Food P o . 2017;3:454–8.
40. Hanssen I, Skei T. Lack o co ela ion be ween ammonia-like ain and
polyamine le els in eindee mea . Ve Rec. 1990;127:622–3.