Is transport distance correlated with animal welfare and carcass quality of reindeer (Rangifer tarandus tarandus)?

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 hanimal wel a e andca 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 500km [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 400km and anspo a ion imes om 1 o 5.5h. 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 3.2–3.5l o wa e pe day, while eindee ed lichens d ank only 0.1l 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 ile1) 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=0km, eindee walk om he ound-up co al o aba oi ; (1) 1–60km; (2) 61–150km; (3) 151–300km; (4)>300km. 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 (6–8mon 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 87km ( ange: 0–450km) in he whole a ea, 62km (10–390km) in he sou he n a ea (A ea 1), and 117km (0–450km) 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 Table1, (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 (Table1; 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 (1–60km) (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 omea inspec ion condemna ions inFinland (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 65km) 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 ocondemna 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 (>10yea 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 ile1. 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.