Open Jou nal o Ve e ina y Medicine, 2015, 5, 61-67
Published Online Ma ch 2015 in SciRes. h p://www.sci p.o g/jou nal/oj m
h p://dx.doi.o g/10.4236/oj m.2015.53008
How o ci e his pape : Ko honen, H.T., Eskeli, P., Huuki, H. and Sepponen, J. (2015) Fo eleg Bending in Blue Foxes (Vulpes
lagopus) as E alua ed by Radiog aphy. Open Jou nal o Ve e ina y Medicine, 5, 61-67.
h p://dx.doi.o g/10.4236/oj m.2015.53008
Fo eleg Bending in Blue Foxes (Vulpes
lagopus) as E alua ed by Radiog aphy
Hannu T. Ko honen, Pekka Eskeli, Hanna Huuki, Juhani Sepponen
Na u al Resou ces Ins i u e Finland (Luke), Kannus, Finland
Email: hannu. .ko honen@luke. i
Recei ed 9 Feb ua y 2015; accep ed 3 Ma ch 2015; published 11 Ma ch 2015
Copy igh © 2015 by au ho s and Scien i ic Resea ch Publishing Inc.
This wo k is licensed unde he C ea i e Commons A ibu ion In e na ional License (CC BY).
h p://c ea i ecommons.o g/licenses/by/4.0/
Abs ac
The aim was o compa e adiog aphic X- ay da a o o eleg bending, mo ing di icul ies and body
size in ju enile blue oxes. Expe imen al g oups we e: 1) es ic ed eeding, Ca:P a io 1.5:1 (R 1);
2) es ic ed eeding, Ca:P a io 2.9:1 (R 2); 3) es ic ed eeding Ca:P a io 2.0:1 con ol le el (R 3);
4) ad libi um eeding, Ca:P a io 1.5:1 (AL 1); 5) ad libi um eeding, Ca:P a io 2.9:1 (AL 2); 6) ad li-
bi um eeding Ca:P a io 2.0:1 con ol le el (AL 3). Mo ing di icul ies and o eleg bending we e
e alua ed in li e animals. A pel ing, le o eleg was emo ed. X- ay pic u es we e aken om la -
e al iews. Dimensions o ulna and adius we e measu ed om he X- ay pic u es. Condi ions o
ca pal join and elbow join we e isually e alua ed. The esul s showed ha inal body weigh
was a ec ed by eeding in ensi y (P = 0.001). Ad libi um ed animals had mo e mo ing di icul ies
compa ed o es ic ed ones (P = 0.001). The Ca:P a io ended (P = 0.06) o ha e an e ec on ee
bending. Bending was g ea es in low Ca:P a io (1.5:1) and, co espondingly, leas in high Ca:P a-
io (2.9:1). Mo ing di icul ies we e mos common in hea ies animals. The mo ing di icul ies
ended (P = 0.07) o be posi i ely ela ed o ee bending. Maximum wid h o ulna was lowes in
low Ca:P a io die (1.5:1). Bending was nega i ely co ela ed wi h maximum wid h o ulna. I can
be concluded ha low Ca:P a io in he die (1.5:1) inc eases o eleg bending in ju eniles. Mo ing
di icul ies a e ela ed o o eleg bending and high body weigh .
Keywo ds
Vulpes lagopus, Foo Wel a e, Mo ing Di icul ies, Fee Bending, Blue Fox
1. In oduc ion
P onounced bending o o elegs is a common phenomenon in a m b ed blue oxes (Vulpes lagopus) oday [1].
Al hough he exac cause is unknown, excessi e nu i ion and body mass, apid g ow h and a he edi a y compo-
nen a e suspec ed o be con ibu ing ac o s. The body size o a m- aised blue oxes has d ama ically inc eased
H. T. Ko honen e al.
62
du ing he las decades. Nowadays oxes can weigh mo e han 20 kg whe e as 15 - 20 yea s ago hei a e age
weigh was less han 10 kg [2]. I is assumed ha s ong selec ion o la ge body size is linked wi h de elopmen-
al diso de o bones and join s [3]. This is a common p oblem, o example, in la ge size dog b eeds [4]-[6]. I
has led o a physiological adap ion wi h inc eased le els o g ow h ho mone (GH) and IGF. I may also be con-
nec ed o poo mine aliza ion o bones [7]. One c ucial componen in he die may be he p ope Ca:P a io
[8]-[11]. The e has been li le esea ch on whe he he Ca con en in mode n ox eed is s ill su icien o p o-
mo e a heal hy bone g ow h in la ge oxes, and whe he he e a e o he componen s in mode n eed ecommen-
da ions ha need o be changed o be e mee he nu ien equi emen s o mode n oxes. Howe e , o eleg
bending has become a po en ial wel a e p oblem in blue oxes [1]. The e o e, i is ou mos impo o unde s and
his p oblem in mo e de ails.
In ou p e ious s udy [2], we p esen ed da a on he e ec s o ad libi um and es ic ed eeding wi h h ee Ca:P
a io die s on oo wel a e in blue oxes. De ailed desc ip ion o ee bending, abili y o mo e and beha io we e
gi en in ela ion o body weigh gain om weaning o pel ing. In he p esen s udy, we p o ide mo e de ailed
in o ma ion abou he ee bending in ju enile oxes. A adiog aphic examina ion (X- ay) was done om o e-
legs o hose animals employed in ou p e ious s udy [2]. The aim he e was o co ela e he X- ay analyses da a
wi h isual o eleg bending da a, mo ing di icul ies and body size.
2. Ma e ial and Me hods
This s udy was ca ied ou a MTT Ag i ood Resea ch Finland, Kannus, in wes e n Finland (63.54˚N, 23.54˚E).
The use o expe imen al animals was e alua ed and app o ed by he Animal Ca e Commi ee o E elä-Suomen
aluehallin o i as o (ESAVI/PH 1231 A/2013). The gene al heal h o animals was isually checked daily.
2.1. Expe imen al Se -Up and Animals
Animals and expe imen al se -up used o analyses in he p esen s udy a e desc ibed in de ails by [2]. Sho ly,
he ollowing se -up was employed: Expe imen al animals we e ju enile male blue oxes bo n in May 2013.
Expe imen s a ed a weaning on Augus 6 h and inished a pel ing on No embe 26 h. The e ec o es ic ed
and ad libi um eeding, as well as he Ca:P a io, on body mass, bending o ee and mo ing di icul ies we e
s udied. The ollowing expe imen al g oups we e compa ed: 1) es ic ed eeding, Ca:P a io 1.5:1 (R 1); 2) e-
s ic ed eeding, Ca:P a io 2.9:1 (R 2); 3) es ic ed eeding Ca:P a io 2.0:1 con ol le el (R 3); 4) ad libi um
eeding, Ca:P a io 1.5:1 (AL 1); 5) ad libi um eeding, Ca:P a io 2.9:1 (AL 2); 6) ad libi um eeding Ca:P a io
2.0:1 con ol le el (AL 3). The amoun o es ic ed eeding was se o be 60% - 70% o ad libi um le el.
Animals om same gene ic backg ound (same mo he ) we e e enly dis ibu ed o each s udy g oup. Li e -
ma es we e placed equally o g oups o homogenize he gene ic a iabili y. Body weigh s we e measu ed wi h a
Me le SM 15 balance, accu acy ±10 g.
Animals we e pai -housed in s anda d wi e-mesh cages measu ing 105 cm long × 120 cm wide × 70 cm high.
Each cage was u nished wi h a wi e-mesh pla o m (105 cm long × 25 cm wide) loca ed a 23 cm om he
ceiling. A bone (30 cm long × 7 cm diame e ) was placed in o cage loo as chewing and ac i i y objec .
2.2. E alua ion o Fo eleg Ca pal Join s and Mo ing
The o eleg ca pal join angle, as an indica o o leg weakness, and he ox’s abili y o mo e abou in he cage
we e e alua ed bo h li e and om ideo eco dings. Fo de ails, see [2]. The subjec i e e alua ion o o eleg
bending was done by one e alua o on a scale o 1 - 5 [2] [12]. In he wo s case (sco e 5 = e y poo ), he ca pal
join was bended o a 90˚ angle compa ed o no mal, only sligh angled ca pal join (sco e 1 = excellen ). Abili y
o mo e was e alua ed as ollows: I he e we e no di icul ies o mo e, si ua ion was sco ed o be 0. The animal
was ac i ely mo ing abou in he cage and was able o jump easily on o he pla o m. Mild di icul ies o mo e
we e sco ed as 1. The ox some imes mo ed abou in he cage and was somehow capable o jumping on he
pla o m, bu clea ly had some di icul ies o unwillingness o mo e. Ma ked di icul ies (sco e 2), i.e. he ox
emained si ing o lying s ill in he cage, e en when encou aged o mo e, we e no ound.
2.3. Radiog aphic Examina ion
A pel ing, le o eleg was emo ed and s o ed a −20˚C un il adiog aphic examina ion (X- ay). Radiological
H. T. Ko honen e al.
63
examina ion was ca ied ou a Nikula He osklinikka, Kaus inen, by an expe ienced e e ina y su geon. X- ay
pic u es we e aken om la e al iews by using Ajex 9015 HF po able X- ay machine (Ajex Medi ech LTD.,
Blackhills, USA) a 70 kW wi h 0.2 sec exposu e ime. Maximum and minimum wid h o ulna and adius we e
measu ed om he X- ay pic u es. Condi ion o ca pal join and elbow join we e isually e alua ed.
2.4. S a is ical Analyses
The s a is ical analyses we e ca ied ou using SAS/STAT so wa e, Ve sion 9.2 o he SAS Sys em o Win-
dows. Copy igh © 2009, SAS Ins i u e Inc. SAS and all o he SAS Ins i u e Inc. p oduc o se ice names a e
egis e ed adema ks o adema ks o SAS Ins i u e Inc., Ca y, NC, USA.
Measu emen s o ulna and adius we e analysed using he ollowing linea mixed model:
( )
ij i j ij
ij
µ α β αβ ε
Υ= + + + +
whe e μ was he gene al mean, αi was he ixed e ec o eeding in ensi y (R o AL), βj was he ixed e ec o
Ca:P a io (1.5:1, 2.9:1, and con ol le el 2.0:1) and (αβ)ij was he in e ac ion be ween ixed e ec s. εij was he
esidual e o . No mali y o esiduals was checked o each analysis using sca e plo s o esiduals and i ed
alues.
Co ela ions be ween each pa ame e we e calcula ed using Spea man co ela ions, since some o he pa-
ame e s (e.g. bending o ee and abili y o mo e) we e no no mally dis ibu ed.
3. Resul s
Dimensions o ulna and adius in ela ion o ee bending, mo ing di icul ies and body weigh s a e gi en in Ta-
ble 1. Feeding in ensi y o Ca:P a io did no a ec maximum o minimum wid h o adius. Fu he mo e, eed-
ing in ensi y did no signi ican ly a ec maximum wid h o ulna. A endency (P = 0.09) was ound ha maxi-
mum wid h o ulna was a ec by die , being highes (10.86 mm) in con ols (Ca:P a io 2.0:1) and lowes in
oxes wi h Ca:P a io 1.5:1, i.e. 10.42 mm on an a e age. Minimum wid h o ulna was no a ec by Ca:P a io.
Howe e , i was a ec ed by eeding in ensi y (P = 0.04; Table 1).
Final body weigh was a ec ed by eeding in ensi y, i.e. body weigh s we e signi ican ly highe (P = 0.001) in
ad libi um ed animals. Mo ing di icul ies we e a ec ed by eeding in ensi y, i.e. ad libi um animals we e ha -
ing signi ican ly mo e mo ing di icul ies compa ed o es ic ed ones (P = 0.001). Feeding in ensi y did no a -
ec he bending o ee . Howe e , Ca:P a io ended (P = 0.06) ha e an e ec on ee bending. Bending was
highes in low Ca:P a io (1.5:1) and lowes in high Ca:P a io (2.9:1).
The isual e alua ion o ca pal and elbow join s did no e eal any damages o diso de s in hose a eas. Bow-
ing o ulna and adius was no seen in adiog aphic examina ion. Examples o X- ay pic u es a e shown in Fig-
u e 1 and Figu e 2.
Table 2 p o ides c oss co ela ions be ween s udied a iables. A posi i e e y signi ican co ela ion was
ound be ween mo ing di icul y and inal body weigh . Mo ing di icul ies we e mos common in hea ies
animals and ice e sa. Bending o he ee was nega i ely co ela ed wi h maximum wi h o ulna, indica ing
ha mos bended o eleg has lowes wid h o ulna. Mo ing di icul ies ended (P = 0.07) o be posi i ely co e-
la ed o bending o ee . Maximum wid h o ulna co ela ed posi i ely wi h minimum wid h o ulna. Minimum
wid h o ulna co ela ed wi h minimum wid h o adius. Fu he mo e, maximum wid h o adius co ela ed posi-
i ely wi h minimum wid h o adius. Ini ial body weigh was co ela ed wi h minimum wid h o ulna and
maximum wid h o adius.
4. Discussion
One o he mos common medical diagnos ic p ocedu es is adiog aphy o X- ays. The g ea es bene i o X- ays
is hei abili y o pene a e issues and show in e nal s uc u es [7]. In he case o legs, he X- ays will be almos
ully abso bed by he bones, while he muscles and ligamen s will abso b a ying amoun o X- ays. The esul -
ing image will be one o he whi e bones including black ai su ounding he leg and a ious shades o g ey ep-
esen ing muscles e c. In he p esen s udy, we used X- ay analyses o e alua e condi ion o o eleg bones and
join s in blue oxes. This is now i s ime when his kind o analyses was done in a med oxes. Acco ding o
au ho ’s bes knowledge, no p e iously published da a a e a ailable.
H. T. Ko honen e al.
64
Table 1. The mean maximum and minimum wid h o ulna and adius is p esen ed in millime e s. S anda d de ia ions (SD)
in pa en hesis. Final and ini ial body weigh s in g ams. The le el o bending o ee was e alua ed acco ding o scale 1 - 5
whe e 1 = excellen , 2 = good, 3 = su icien , 4 = poo , 5 = e y poo . The bending is p esen ed as a numbe o animals wi h
bended ee in a g oup. Mo ing di icul ies is p esen ed as a numbe o animal ha ing sligh mo ing di icul ies. P1 = sig-
ni icance be ween es ic ed and ad libi um g oups; P2 = signi icance be ween Ca:P le els; P3 = signi icance be ween hei
in e ac ions. R 1: es ic ed eeding, Ca:P a io 1.5:1; R 2: es ic ed eeding, Ca:P a io 2.9:1; R 3: es ic ed eeding Ca:P a-
io 2.0:1 con ol le el; AL 1: ad libi um eeding, Ca:P a io 1.5:1; AL 2: ad libi um eeding, Ca:P a io 2.9:1; AL 3: ad libi-
um eeding Ca:P a io 2.0:1 con ol le el.
Va iable R 1 R 2 R 3 AL 1 AL 2 AL 3 P1 P2 P3
Ulnamax wid h 10.56 10.60 10.50 10.30 10.33 11.22 ns 0.09 0.04
(0.53) (0.52) (0.53) (0.48) (0.53) (0.83)
Ulnamin wid h 4.56 4.75 4.50 4.55 3.94 4.22 0.04 ns ns
(0.81) (0.86) (0.47) (0.60) (0.53) (0.51)
Radiusmax wid h 9.56 9.90 10.00 9.80 9.06 9.67 ns ns 0.08
(0.53) (1.29) (0.47) (0.42) (0.39) (0.87)
Radiusmin wid h 4.50 4.60 4.35 4.55 4.06 4.33 ns ns ns
(0.83) (0.88) (0.71) (0.83) (0.46) (0.71)
Final body weigh a 13374 14079 12775 18922 17834 17316 <0.001 ns ns
(1701) (1247) (1449) (1597) (2398) (2213)
Ini ial body weigh a 5105 5214 5193 5106 5184 5233 ns ns ns
(325) (229) (352) (462) (488) (824)
Mo ing di icul ies
Bending 1 1 0 9 6 4 <0.001 ns ns
Sco e 4a 6 1 7 8 6 3
Sco e 3a 2 8 1 2 4 6 ns 0.06 ns
Sco e 2a 2 1 2 0 0 1
aO iginal da a p esen ed in [2].
Table 2. Calcula ion o c oss co ela ion (Spea man) be ween di e en pa ame e s. S a is ical signi icance: *P < 0.05; **P <
0.01; ***P < 0.001; aP = 0.07.
Ulnamax Ulnamin Radiusmax Radiusmin Final BW Ini ial BW Bending
Mo ing 0.134 −0.027 0.020 0.069 0.574*** 0.066 0.236a
Ulnamax 0.352** 0.215 0.306* 0.109 0.218 −0.275*
Ulnamin 0.621*** 0.705*** 0.012 0.304* −0.055
Radiusmax 0.575*** 0.001 0.259* 0.052
Radiusmin 0.166 0.169 −0.045
Final BW 0.184 0.097
Ini ial BW 0.052
H. T. Ko honen e al.
65
Figu e 1. X- ay pic u e o o eleg. G oup AL 2 (Ca:P a io 2.9:1).
Body weigh 19.805 kg. Bending sco e = 4.
Figu e 2. X- ay pic u e o o eleg. G oup R 1 (Ca:P a io 1.5:1).
Body weigh 14.235 kg. Bending sco e = 2.

H. T. Ko honen e al.
66
The p esen s udy ma e ial was based on wo eeding le els, i.e. ad libi um and es ic ed ones. Fu he mo e, i
included da a om animals ed wi h h ee di e en Ca:P a ios, i.e. 1.5:1, 2.0:1 and 2.9:1. So, we had wide ange
o s udy ma e ial o e alua e o eleg-bending in luences. Ou X- ay pic u es did no e eal any cu ing o ulna
and adius bones. Bending o o eleg seen in li e animals is hus no due o cu ing o hese bones pe se, bu is
mainly a esul o p onounced bending in he a ea o ca pal join . Some bending may also occu a ound elbow
join .
G owing pe iod including ac ual de elopmen o skele on bones and join s is in blue oxes om weaning in
July o mid-Sep embe . The ea e , ac ual body a ening p ocess will begin [2]. Ju enile oxes will p oduce ex-
cessi e subcu aneous a mainly om Oc obe onwa ds. Finally, pel ing is ca ied ou in la e No embe [13]
[14]. Mos p onouncedly bended o elegs, ela ed o excessi e body weigh s, will occu du ing Oc obe -No-
embe [2]. This is ac ually a a he sho pe iod o ime o ha e an in luence on o eleg condi ion and wel a e.
Bending o on ee was e alua ed in li e animals by a 5-poin scale. Howe e , he ex eme cases o e y
badly bended oo (sco e 5) no pe ec ly s aigh ee (sco e 1) we e no ound in he p esen s udy. Compa ison
he e was hus be ween sco e poin s 2, 3 and 4. Ou X- ay pic u es did no e eal any damages o diso de s in
s udied o eleg bones and join s. In his s udy ee bending wi h sco e poin s 2, 3 and 4 did no cause any X- ay
de ec able changes on o eleg bones and join in case o ju eniles. Acco ding o [1], he amoun o oxes wi h
wo se bending on u a ms a e ages nowadays 14%. Fu he s udies will be needed o cla i y he wel a e e -
ec s o o eleg bending in hose animals, and whe he o no he condi ion causes pain.
Two p e ious s udies [10] [11] a e a ailable in which die a y Ca and P concen a ions did no ha e any e ec
on bone mine aliza ion o b eaking s eng h in ju enile blue oxes. S udy by [8], on he o he hand, epo ed ha
die a y Ca and P ha e ce ain impac on he mine aliza ion o bones; low Ca:P a io in he die signi ican ly e-
duced he Ca and P concen a ions o ulna bones compa ed wi h he no mal die a y Ca:P a io. Despi e o lowe
mine aliza ion, howe e , signi ican di e ences in b eaking s eng h o ulna we e no ound. Fu he mo e, no
ela ionship was ound be ween Ca le el and oo bending. I was concluded ha he calcium le el in bones is
ei he no di ec ly ela ed o oo bending o lowe ing o Ca le el was no enough o cause any measu able e -
ec s. In he p esen , mine al con en o bones was no measu ed. The e o e, we do no know how die Ca:P
con en a ec ed on bone mine al con en . Dimensions o adius we e no a ec ed by Ca:P a io in he die .
Howe e , maximum wid h o ulna was lowes in low Ca:P a io (1.5:1). Co espondingly, ea ly s udy [8]
showed ha he e was a g ea e bone hickness in oxes ed on a high Ca die . They also no iced ha low die a y
Ca caused bowing o legs. In he p esen s udy, mos p onounced bending was also no iced wi h low Ca:P a io.
Ou co ela ion da a con i med he esul o ou p e ious s udy [2] ha mo ing di icul y is highly ela ed o
body weigh o animals. Thus, la ge-sized oxes wi h high inal weigh a e ypically ha ing mo ing di icul ies
he mos . Co ela ion da a also e ealed ha mo ing di icul y ended o be ela ed o bending o ee a new
inding which did no come ou in ou p e ious analyses [2]. Thus, i seems ob ious ha mo ing di icul ies a e
explained a leas by wo ac o s, i.e. high body weigh and bending o o eleg. Fu he mo e, bending he e
ended o be ela ed o Ca:P a io. Animals wi h low Ca:P a io used o ha e mos bended o elegs. We a e
emp ed o conclude, ha Ca:P a io, o a ce ain ex en , could be one o he easons o bending o ee . To-
ge he wi h high body weigh , bending o he on ee can cause mo ing di icul ies.
5. Conclusion
Low Ca:P a io in he die (1.5:1) migh inc ease o eleg bending in ju enile blue oxes. Howe e , in his s udy,
o eleg bending (sco e poin s 2, 3, 4 in scale 1 - 5) was no ound o cause diso de s o bones o join s o o eleg.
Mo ing di icul ies seem o be ela ed o o eleg bending and high body weigh in la e au umn. Fu he s udies
a e needed o con i m he wel a e e ec s o bending o ee . Bending, howe e , seems o be linked wi h mo ing
di icul ies, which may jeopa dize animal’s wellbeing.
Acknowledgemen s
This s udy was inancially suppo ed by he Finnish Fu B eede s’ Associa ion and MTT Ag i ood Resea ch
Finland. Special hanks o Nikula He osklinikka o aluable aid in adiog aphy.
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