animals
B ie Repo
E olu ion o he Se op e alence o Pes i i us and Respi a o y
Vi al In ec ions in Spanish Feedlo Lambs
Te esa Na a o 1,* , Au o a O ín1, Osca Cabezón2, Ma celo De Las He as 1, Delia Lacas a 1
and JoséMa ía González 1,3


Ci a ion: Na a o, T.; O ín, A.;
Cabezón, O.; De Las He as, M.;
Lacas a, D.; González, J.M. E olu ion
o he Se op e alence o Pes i i us
and Respi a o y Vi al In ec ions in
Spanish Feedlo Lambs. Animals 2021,
11, 160. h ps://doi.o g/10.3390/
ani11010160
Recei ed: 24 No embe 2020
Accep ed: 8 Janua y 2021
Published: 12 Janua y 2021
Publishe ’s No e: MDPI s ays neu-
al wi h ega d o ju isdic ional clai-
ms in published maps and ins i u io-
nal a ilia ions.
Copy igh : © 2021 by he au ho s. Li-
censee MDPI, Basel, Swi ze land.
This a icle is an open access a icle
dis ibu ed unde he e ms and con-
di ions o he C ea i e Commons A -
ibu ion (CC BY) license (h ps://
c ea i ecommons.o g/licenses/by/
4.0/).
1Depa men o Animal Pa hology, Uni e si y o Za agoza & Ag iFood Ins i u e o A agón (IA2),
50013 Za agoza, Spain; ao in@uniza .es (A.O.); lashe as@uniza .es (M.D.L.H.); dlacas a@uniza .es (D.L.);
[email p o ec ed] (J.M.G.)
2Wildli e Conse a ion Medicine Resea ch G oup, Depa men o Medicine and Animal Su ge y,
Au onomous Uni e si y o Ba celona, 08193 Ba celona, Spain; Osca [email p o ec ed]
3Gabine e Técnico Ve e ina io S.L., 50014 Za agoza, Spain
*Co espondence: e [email p o ec ed]
Simple Summa y:
The p esence o i uses, such as bo ine pa ain luenza ype 3, bo ine he pes i us
ype 1, bo ine espi a o y syncy ial i us and pes i i uses, has been widely demons a ed in sheep
in he pas , bu i is unknown how hese in ec ions may a ec he lambs du ing hei a ening pe iod
unde comme cial condi ions. In he p esen s udy, he exposu e o he a o emen ioned i uses was
s udied in 120 eedlo lambs h oughou he whole a ening pe iod. Se op e alences we e measu ed
by enzyme-linked immunoso ben assays (ELISA), ela ing hei p esence o heal h and p oduc ion
pa ame e s in he s udied lambs. Du ing he s udied pe iod, he lambs se ocon e ed agains 3 ou
o he 4 i uses analysed and only 10.8% o he lambs we e se onega i e o all he es ed i uses
h oughou he en i e s udy. Finally, no associa ions we e ound be ween he se ocon e sion o one
o mo e i uses and he p esence o espi a o y clinical signs o lung lesions a he slaugh e house.
In addi ion, no dis u bances we e obse ed in he pe o mance o he lambs, excep in he case o
pes i i us in ec ions, o which he p esence o an ibodies in he animals was associa ed wi h educed
inal weigh a he end o he a ening pe iod.
Abs ac :
The p esence o espi a o y i uses and pes i i uses in sheep has been widely demon-
s a ed, and hei abili y o cause inju y and p edispose o espi a o y p ocesses ha e been p o en
expe imen ally. A longi udinal obse a ional s udy was pe o med o de e mine he se op e alence
o bo ine pa ain luenza i us ype 3 (BPIV-3), bo ine espi a o y syncy ial i us (BRSV), bo ine
he pes i us ype 1 (BHV-1) and pes i i uses in 120 lambs a he beginning and he end o he a ening
pe iod. Du ing his ime, he animals we e clinically moni o ed, hei g ow h was eco ded, and
pos -mo em examina ions we e pe o med in o de o iden i y he p esence o pneumonic lesions in
he animals. Se ocon e sion o all i uses es ed excep BHV-1 was de ec ed a he end o he pe iod.
Ini ially, BPIV-3 an ibodies we e he mos equen ly ound, while he mos common se ocon e sion
h ough he analysed pe iod occu ed o BRSV. Only 10.8% o he lambs showed no de ec able le els
o an ibodies agains any o he es ed i uses a he end o he su ey. In addi ion, no s a is ical
di e ences we e ound in he p esen a ion o espi a o y clinical signs, pneumonic lesions no in he
p oduc ion pe o mance be ween lambs ha se ocon e ed and hose which did no , excep in he
case o pes i i uses. The se ocon e sion o pes i i uses was associa ed wi h a educ ion in he inal
weigh o he lambs.
Keywo ds:
lamb; eedlo ; bo ine pa ain luenza i us ype 3 i us; bo ine espi a o y syncy ial i us;
bo ine he pes i us ype 1; pes i i us
Animals 2021,11, 160. h ps://doi.o g/10.3390/ani11010160 h ps://www.mdpi.com/jou nal/animals
Animals 2021,11, 160 2 o 7
1. In oduc ion
O ine espi a o y complex (ORC) is he second leading cause o disease in Span-
ish lamb eedlo s, a e coccidiosis, and is he p ima y cause o dea h in all ypes o
a ms, seasons, egions, b eeds and weigh s in he coun y [
1
]. ORC is caused by se e al
agen s, bu he i e mic oo ganisms p esen in mo e han wo- hi ds o he isola es a e
Mannheimia haemoly ica
,Pas eu ella mul ocida,Bibe s einia ehalosi,Mycoplasma spp. and
Esche ichia coli [
1
]. Howe e , he in ol emen o i al agen s in his disease has no been
cla i ied in lambs.
I is well known he ole o espi a o y i uses such as bo ine pa ain luenza i us ype
3 (BPIV-3), bo ine espi a o y syncy ial i us (BRSV), bo ine he pes i us ype 1 (BHV-1)
and pes i i uses in he de elopmen o bo ine espi a o y disease (BRD). In sheep and
lambs, e idence o na u al in ec ion by hese i uses has been epo ed by se e al au ho s
in di e en geog aphic loca ions [
2
–
5
]. In addi ion, expe imen al in ec ions pe o med in
di e en lamb models ha e p o en he abili y o espi a o y i uses o cause disease in
o ines [
6
–
11
]. Simila ly, despi e espi a o y lesions no being he main ea u e o pes i i us
in ec ions, lung damage has been no ed unde ce ain condi ions in ca le [
12
–
14
] bu
also in sheep in he case o expe imen al in ec ions wi h bo de disease i us (BDV) [
15
].
Likewise, o he pes i i uses di e en han BDV, such as bo ine i al dia hoea i us
(BVDV) ha e also demons a ed being able o in ec lambs [
14
]. The suscep ibili y o some
o hese i uses seems o be age-dependen , dec easing p og essi ely as he age o he
lamb inc eases [
15
,
16
]. Fu he mo e, unde expe imen al condi ions, he consequences
de i ed om hese in ec ions in lambs end o be mild unless hey a e combined wi h a
bac e ial in ec ion, especially by Pas eu ellaceae [
11
,
15
–
17
]. The mos common clinical
signs associa ed wi h espi a o y i uses a e nasal discha ge, achypnoea and e e [
16
].
Howe e , ansien immune supp ession has been desc ibed as one o he main pa hogenic
e ec s associa ed wi h hese i al in ec ions in ca le [
18
–
20
], also epo ed in o ines [
5
,
21
].
The aim o his s udy was o elucida e he impo ance o hese i uses in eedlo lambs
unde na u al condi ions h ough he obse a ion o he e olu ion o se ocon e sions
du ing he a ening pe iod. Heal h and p oduc ion da a om his pe iod we e also
analysed, e alua ing he in luence o he i al in ec ions on hese pa ame e s ha ha e a
ele an economic impac .
2. Ma e ials and Me hods
A longi udinal obse a ional s udy was conduc ed in a lamb eedlo loca ed in A agón
(No h-Eas e n Spain). One hund ed and wen y Rasa A agonesa clinically heal hy a en-
ing male lambs wi hou clinical signs o disease we e andomly selec ed h oughou all
seasons in wo yea s, dis ibu ed in 8 g oups o 15 animals each. Lambs we e ec ui ed a
weaning age (40–50 days old) wi h 12–15 kg o li e weigh . All he s udied animals we e
indi idually iden i ied and agged a he a m o o igin. On a i al a he eedlo , he lambs
we e classi ied and s ocked in g oups mixed wi h o he animals a a maximum densi y
o 1.67 lambs/m
2
, and a e six weeks o a ening (82–92 days old), hey we e sen o he
slaugh e house. Blood samples wi hou an icoagulan we e aken by jugula enipunc u e
om all he lambs a wo di e en momen s: on he a m o bi h, jus be o e he anspo
o he eedlo , and a he end o he a ening pe iod, p io o being anspo ed o he
slaugh e house. Immedia ely a e collec ion, he samples we e e ige a ed and sen o
he labo a o y, p ocessed o ob ain se a, aliquo ed and s o ed a
−
20
◦
C un il analysis. The
animals we e moni o ed daily o clinical signs o disease h oughou he s udy pe iod
by specialised pe sonnel, he same clinician h oughou he s udy, and hei weigh s we e
egis e ed weekly. Once in he slaugh e house, he ca casses’ weigh s we e eco ded a -
e e isce a ion. Finally, he isce a we e submi ed o he pa hology depa men o he
Ve e ina y Facul y o Za agoza o pos -mo em examina ion and iden i ica ion o g oss
pneumonic lesions.
De ec ion o an ibodies agains he di e en i uses was pe o med by means o
comme cially a ailable enzyme-linked immunoso ben assay (ELISA) ki s: IDEXX PI-3
Animals 2021,11, 160 3 o 7
Ab Tes o BPIV-3 an ibody de ec ion (sensi i i y and speci ici y o 98.9% and 75.0%,
espec i ely, acco ding o he in o ma ion o he manu ac u e ’s alida ion da a epo );
IDEXX IBR gB X3 Ab o BHV-1 an ibodies ( epo ed sensi i i y and speci ici y o 100% and
99.8%, espec i ely); IDEXX BVDV p80 Ab in he case o pes i i uses (97.6% sensi i i y and
97.3% speci ici y), which de ec s p80 polypep ide, common o mos pes i i uses, including
BDV, BVDV and classical swine e e i us (CSFV) (IDEXX Labo a o ies, Mon pellie ,
F ance); and CIVTEST Bo is BRSV/VRS o BRSV (75.7% sensi i i y and 93.9% speci ici y)
(Labo a o ios Hip a S.A., Ame , Spain), acco ding o he manu ac u e ’s ins uc ions.
The se ological esul s we e ca ego ised as posi i e o nega i e, and se ocon e sion was
de ined as a change in he se ological s a us ( inal s. ini ial), excep in he case o BPIV-
3 de e mina ions, ha allowed alloca ion o each animal in o ou di e en ca ego ies
acco ding o hei op ical densi ies and based on cu -poin s p o ided by he manu ac u e .
The ca ego ies p o ided we e: (1) 20–40%, (2) 40–60%, (3) 60–80% and (4) 80–100% o
se oposi i i y. Acco ding o his, samples beyond 20% o se oposi i i y we e conside ed
posi i e, bu only di e ences o a leas wo inc easing ca ego ies be ween inal and ini ial
s a us we e indica i e o se ocon e sion.
S a is ical analysis was conduc ed h ough he s a is ical package IBM SPSS S a is ics
.22.0 (SPSS Inc., Chicago, IL, USA). The associa ion be ween se ocon e sion o he di e en
i uses, clinical signs o espi a o y disease and pneumonic lesions iden i ied a pos -
mo em s udy acco ding o he inal se ological s a us was e alua ed by Chi-squa e es ,
while Fishe ’s exac es was used when he sample size o a a iable was below 5. The
di e ences in he a e age daily gain we e analysed by means o non-pa ame ic es s o
wo independen samples wi h Mann–Whi ney U es . The inal weigh s we e analysed by
means o he uni a ia ed gene al linea model p ocedu e acco ding o he inal se ological
s a us and season as ixed ac o s and co a ia ed by ini ial weigh o he lambs. These
p ocedu es we e pe o med o each i us indi idually and also o all o hem collec i ely.
3. Resul s
Se oposi i i y was e idenced o all es ed i uses, excep o BHV-1, o which all
he animals we e se onega i e in he wo samplings, ei he in he eedlo o on he a m
o o igin (Table 1). A weaning, BPIV-3 an ibodies we e he mos equen ly de ec ed,
ollowed by pes i i us and BRSV (Table 1). Mo eo e , mul iple in ec ions we e ound in 19
o he 120 analysed animals, wi h 14 lambs posi i e o BPIV-3 and BRSV, 1 o BPIV-3 and
pes i i us, 1 o BRSV and pes i i us, and 3 o all o hem.
Table 1.
Appa en se op e alence o he bo ine espi a o y syncy ial i us (BRSV), bo ine pa ain luenza i us ype 3
(BPIV-3) and pes i i us in 120 lambs a weaning (40–50 days old), a he end o he a ening pe iod (42 days la e ) and he
o al se ocon e sion ha occu ed du ing his pe iod.
BRSV BPIV-3 Pes i i us To al
No. Lambs %No. Lambs %No. Lambs %No. Lambs %
Se op e alence a
weaning 18 15.0
(8.6%, 21.4%) a70 58.3
(49.5%, 67.2%) a29 24.2
(16.5%, 31.8%) a85 70.8
Se op e alence a he
end o a ening pe iod 46 38.3
(29.6%, 47.0%) a105 87.5
(81.6%, 93.4%) a22 18.3
(11.4%, 25.3%) a107 89.1
Se ocon e sion du ing
a ening pe iod 43 35.8 30 25.0 6 5.0 58 48.3
a95% Con idence In e al.
A he end o he a ening pe iod, only 13 ou o he 120 s udied lambs (10.8%)
emained se onega i e o all he i uses es ed. Du ing his pe iod, he highes le el o
se ocon e sion occu ed o BRSV. Thus, 43 lambs inc eased hei an ibody le els eaching
a posi i e s a us by he end o he a ening pe iod, while 15 posi i e lambs a weaning
became se onega i e a he a he end o he same pe iod. Simila esul s we e obse ed
wi h BPIV-3, wi h 30 showing se ocon e sion a he end o he a ening pe iod, al hough
o hese animals, 8 we e al eady posi i e o his i us a he ini ial sample and inc eased
Animals 2021,11, 160 4 o 7
hei an ibody i e by he end o he s udy and addi ionally, 11 lambs became se onega i e
a he inal sample. Rega ding pes i i us, 13 and 6 lambs changed hei s a us o nega i e
o posi i e a he end o he s udy, espec i ely.
Finally, an associa ion was obse ed be ween BRSV and BPIV-3 exposu e (p= 0.006)
and he lambs ha se ocon e ed o BRSV p esen ed highe isk o se ocon e o BPIV-3
(RR = 2.342).
The mos equen ly epo ed clinical signs obse ed in he lambs h oughou he
s udied pe iod we e: dyspnoea, conjunc i i is, nasal discha ge and coughing. These
symp oms we e p esen alone o in combina ion in 9 o he lambs ha se ocon e ed o
BRSV, in 8 o hose se ocon e ing o BPIV-3 and 1 ou o 6 lambs ha se ocon e ed o
pes i i uses. Ne e heless, s a is ically signi ican associa ions be ween se ocon e sion
o any o he i uses s udied and he de ec ion o espi a o y clinical signs in he animals
we e no obse ed in his in es iga ion (Table 2). Simila ly, he iden i ica ion o g oss
pneumonic lesions a pos -mo em examina ion ne e e ealed any s a is ical ela ionship
wi h se ocon e sion o any o he i uses.
Table 2.
Di e ences in he p esen a ion o clinical signs, pneumonic lesions, a e age daily gain (ADG) and ca cass yield in
120 lambs du ing he a ening pe iod, acco ding o se ocon e sion o bo ine pa ain luenza i us ype 3 (BPIV-3), bo ine
espi a o y syncy ial i us (BRSV) o pes i i uses.
Se ocon e sion o Any Vi us
(BPIV-3, BRSV, Pes i i uses)
No Se ocon e sion
n= 62
Se ocon e sion
n= 58 p
Respi a o y clinical signs No. Lambs 8 14 0.112
% 12.9 24.1
Lung consolida ed lesions No. Lambs 19 19 0.807
% 30.6 32.8
A e age daily gain (kg/d) 0.305 ±0.0562 0.306 ±0.0685 0.646
Ca cass yield (%) 45.5 ±2.14 45.0 ±2.26 0.166
Final weigh (kg) 26.129 ±3.7413 26.245 ±3.5701 0.799
Rega ding he epe cussions o hese i al in ec ions on pe o mance, he a e age
daily gain (ADG), he inal weigh and he ca cass yield we e simila o all g oups o
animals, and no s a is ically signi ican associa ions we e ound be ween hem excep o
lambs ha se ocon e ed o pes i i uses (p< 0.05). These animals showed a mean inal
li e weigh 2.730 kg lowe (23.393 s. 26.123) compa ed wi h hose ha did no e idence
exposu e (p< 0.05).
4. Discussion
All he i uses s udied in he p esen s udy a e associa ed wi h pa hological e ec s in
ca le while he e is also e idence o hei in ec ion in sheep. Among he s udied i uses,
BHV-1 seems o be he leas common in o ines [
2
,
4
], al hough sheep exposed o BHV-1
ha e demons a ed no always exhibi ing a de ec able humo al immune esponse o i us
exc e ion [
8
]. Fo hese easons, he ansmission o his i us in small uminan s seems o
be in equen [8].
Se op e alences o BPIV-3, BRSV and pes i i uses ound in he p esen s udy a e
simila o hose epo ed in o he wo ks conduc ed in sheep, e en hough mos o hem
we e pe o med a lock le el and unde di e en p oduc ion sys ems. In gene al, he
li e a u e indica es widesp ead BPIV-3, wi h se op e alences highe han 70% in a ious
epo s [
2
,
22
,
23
], al hough low a es ha e been also epo ed [
4
,
24
]. Values gi en by o he
au ho s a e in acco dance wi h hose ob ained in his wo k (38.3%) ega ding BRSV and
end o be sligh ly lowe o hose eco ded o BPIV-3 (87.5%), which can be ound in a
wide ange (24%–71.5%) [
2
,
22
,
24
,
25
]. By con as , pes i i us an ibodies seem o be a lowe
alues in mos o he epo s om di e en coun ies, e en below 1% [
2
,
26
]. Howe e ,
Animals 2021,11, 160 5 o 7
in he case o Spanish a ening lambs, he epo ed se op e alences ange om 13.8%
o 28.6% [
5
,
27
], as he in ec ion is conside ed endemic in he coun y and, consequen ly,
highe se op e alences can be ound [28].
Fo all hese i uses, he e we e animals wi h de ec able le els o an ibodies a weaning
ime ha became se onega i e by he end o he s udied pe iod. Ma e nally de i ed
an ibodies ha e shown o emain de ec able in lambs o 2–5 mon hs, in he case o
BPIV-3 [
29
], and acco ding o he obse a ions pe o med in ca le, o 3–4 mon hs and
1–4 mon hs in he case o BRSV [
30
] and pes i i us, espec i ely [
31
,
32
]. Howe e , he
dynamics o he in ec ion h oughou he s udy ha e di e ed be ween he i uses. Whe eas
inc easing le els o an ibodies o BPIV-3 and BRSV we e de ec ed in he lambs be ween
ini ial and inal samplings, se ocon e sion o pes i i uses was no equen in he eedlo ,
despi e he ini ial se op e alence e ealing a signi ican p esence o he i us on he
a ms o o igin. In his sense, in a su ey pe o med in eedlo lambs in condi ions e y
simila o he p esen wo k, he au ho s obse ed ha he majo i y o pes i i us in ec ions
occu ed 27 days a e he a i al o he lambs a he eedlo . In addi ion, only 2 o he
17 animals in which he i us was p e iously de ec ed had se ocon e ed a he end o he
a ening pe iod, 42 days la e [
5
]. As a consequence o he long ime span o de ec able
se ocon e sion in esponse o pes i i us in ec ion [
33
], he iabili y o an ibody de ec ion
as a echnique o he in es iga ion o he dynamics o his pa icula in ec ion is educed
in Spanish a ening lambs due o hei sho eedlo s ay.
Despi e he ac ha he pa hogenici y o all ou s udied i uses has been demon-
s a ed h ough expe imen al in ec ions in se e al lamb models [
9
,
10
,
15
,
16
], clea pa ho-
logic consequences o he in ec ion we e no obse ed in he p esen su ey. In ca le,
a modes inc ease in he isk o su e ing om BRD a e se ocon e sion o each i us
sepa a ely has been obse ed, which p og essi ely inc eases wi h mul iple i al exposu es,
unde lining he impo ance o concu en in ec ions [
34
]. In he p esen s udy, concu en
in ec ions ha e been obse ed; howe e , no appa en pa hological consequences we e de-
ec ed. Finally, lambs which had se ocon e ed o pes i i uses du ing he a ening pe iod
showed a s a is ically-signi ican lowe mean inal li e weigh compa ed o hose ha did
no , al hough hese esul s should be in e p e ed wi h cau ion due o he educed sample
size. Howe e , simila obse a ions we e made by González e al. in eedlo lambs [
4
].
Likewise, in ca le, he milde e ec o BPIV-3 and BRSV compa ed o pes i i uses in ec-
ions was obse ed h ough he educed weigh o he a ec ed animals a he end o he
a ening pe iod [35].
5. Conclusions
The exposu e o lambs o BRSV, BPIV-3 and pes i i uses on he a ms, bu also in
he eedlo , has been demons a ed in his s udy, while no p oo o BHV-1 in ec ion was
de e mined. Howe e , despi e he p esence o hese i uses and hei abili y o cause
disease unde expe imen al condi ions, he de imen al e ec s de i ed om hei exposu e
in na u al condi ions we e no obse ed, wi h he excep ion o pes i i us in ec ion, which
e ealed a signi ican ad e se e ec on he inal weigh o he s udied lambs.
Au ho Con ibu ions:
Concep ualiza ion, A.O. and J.M.G.; me hodology, A.O., T.N. and. J.M.G.;
alida ion, M.D.L.H.; o mal analysis, J.M.G.; in es iga ion, T.N., O.C. and D.L.; da a cu a ion, J.M.G.;
w i ing—o iginal d a p epa a ion, T.N.; w i ing— e iew and edi ing, A.O., M.D.L.H., D.L. and
J.M.G.; supe ision, A.O. and J.M.G.; p ojec adminis a ion, A.O.; unding acquisi ion, A.O. and
J.M.G. All au ho s ha e ead and ag eed o he published e sion o he manusc ip .
Funding:
This esea ch was unded by he Spanish Minis y o Ag icul u e, Food and En i onmen ,
g an numbe 20140020001835; he Spanish Minis y o Economy and Compe i i eness, g an numbe
AGL2015-67690-R; and he A agón Go e nmen and he Eu opean Social Fund (Cons uyendo
A agón 2016–2020), g an numbe A15-17R. The APC was unded by he A agón Go e nmen and
he Eu opean Social Fund.

Animals 2021,11, 160 6 o 7
Ins i u ional Re iew Boa d S a emen :
The s udy was conduc ed acco ding o he guidelines o he
Decla a ion o Helsinki, and app o ed by he E hic Commi ee o Animal Expe imen s om he
Uni e si y o Za agoza (p o ocol code PI49-14, app o ed on 12 h o Decembe o 2014).
In o med Consen S a emen : No applicable.
Da a A ailabili y S a emen :
The da a p esen ed in his s udy a e a ailable on eques om he
co esponding au ho . The da a a e no publicly a ailable due o p i acy easons.
Acknowledgmen s:
The au ho s u he acknowledge Ch is ina Summe s o eading and e ision
o he manusc ip .
Con lic s o In e es :
The au ho s decla e no con lic o in e es . The unde s had no ole in he design
o he s udy; in he collec ion, analyses, o in e p e a ion o da a; in he w i ing o he manusc ip , o
in he decision o publish he esul s.
Re e ences
1.
Gonzalez, J.; Bello, J.M.; Rod iguez, M.; Na a o, T.; Lacas a, D.; Fe nández, A.; De las He as, M. Lamb eedlo p oduc ion in
Spain: Mos ele an heal h issues. Small Rumin. Res. 2016,142, 83–87. [C ossRe ]
2.
Calde on Gonçal es, R.; da Sil a, A.A.; Fe ei a, D.O.L.; Ma condes, J.S.; Pi uco, E.M.; Dias, A. De ec ion o se um an ibodies o
pa ain luenza ype 3 i us, espi a o y syncy ial i us, bo ine i al dia hea i us, and he pes i us ype 1 in sheep in he Region
o Bo uca u, São Paulo - B azil. J. Ve . Med. Anim. Heal. 2011,3, 1–5.
3.
Da ies, D.H.; Jones, S. Se ological e idence o espi a o y syncy ial i us in ec ion in lambs. N. Z. Ve . J.
1985
,33, 155. [C ossRe ]
[PubMed]
4.
Giangaspe o, M.; Sa ini, G.; O usa, R.; Osawa, T.; Ha asawa, R. P e alence o an ibodies agains Pa ain luenza i us ype 3,
Respi a o y synci ial i us and bo ine He pes i us ype 1 in sheep om No he n P e ec u es o Japan. Ve . I al.
2013
,49,
285–289.
5.
González, J.M.; Lacas a, D.; Fe e , L.M.; Figue as, L.; Ramos, J.J.; De las He as, M. Na u al bo de disease i us in ec ion in
eedlo lambs. Ve . Rec. 2014,174, 69. [C ossRe ] [PubMed]
6.
Al-Da aji, A.M.; Cu lip, R.C.; Lehmkuhl, H.D.; G aham, D.L. Expe imen al in ec ion o lambs wi h bo ine espi a o y syncy ial
i us and Pas eu ella haemoly ica: Pa hologic s udies. Am. J. Ve . Res. 1982,43, 224–229. [PubMed]
7.
Da ies, D.H.; Jones, B.A.H.; Thu ley, D.C. In ec ion o speci ic-pa hogen- ee lambs wi h pa ain luenza i us ype 3,
Pas eu ella haemoly ica and Mycoplasma o ipneumoniae.Ve . Mic obiol. 1981,6, 295–308. [C ossRe ]
8.
Hage, J.J.; Vellema, P.; Schukken, Y.H.; Ba kema, H.W.; Rijsewijk, F.A.M.; an Oi scho , J.T.; Wen ink, G.H. Sheep do no ha e a
majo ole in bo ine he pes i us 1 ansmission. Ve . Mic obiol. 1997,57, 41–54. [C ossRe ]
9.
Lehmkuhl, H.D.; Cu lip, R.C. Expe imen al pa ain luenza ype 3 in ec ion in young lambs: Clinical, mic obiological, and
se ological esponse. Ve . Mic obiol. 1983,8, 437–442. [C ossRe ]
10.
Meehan, J.T.; Lehmkuhl, H.D.; Cu lip, R.C.; Bolin, S.R. Acu e pulmona y lesions in sheep expe imen ally in ec ed wi h bo ine
i al dia hoea i us. J. Comp. Pa hol. 1998,119, 277–292. [C ossRe ]
11.
T igo, F.J.; B eeze, R.G.; E e mann, J.F.; Gallina, A.M. Pa hogenesis o expe imen al bo ine espi a o y syncy ial i us in ec ion in
sheep. Am. J. Ve . Res. 1984,45, 1663–1670. [PubMed]
12.
Monies, R.J.; Pa on, D.J.; Vilcek, S. Mucosal disease-like lesions in sheep in ec ed wi h Bo de disease i us. Ve . Rec.
2004
,155,
765–769. [PubMed]
13.
Thab i, F.; F onza oli, L.; Dlissi, E.; Guibe , J.-M.; Hammami, S.; Pepin, M.; Russo, P. Expe imen al model o Bo de Disease Vi us
in ec ion in lambs: Compa a i e pa hogenici y o pes i i uses isola ed in F ance and Tunisia. Ve . Res.
2002
,33, 35–45. [C ossRe ]
[PubMed]
14.
Ne le on, P.F.; Willoughby, K. Bo de Disease. In Diseases o Sheep, 4 h ed.; Ai ken, I.D., Ed.; Blackwell Publishing: Edinbu gh,
UK, 2007; pp. 119–127.
15.
De scheid, R.J.; Acke mann, M.R. Pe ina al Lamb Model o Respi a o y Syncy ial Vi us (RSV) In ec ion. Vi uses
2012
,4, 2359–2378.
[C ossRe ]
16.
Lehmkuhl, H.D.; Cu lip, R.C. Expe imen al espi a o y syncy ial i us in ec ion in eede -age lambs. Am. J. Ve . Res.
1979
,40,
1729–1730.
17.
Da ies, D.H.; Dungwo h, D.L.; Humph eys, S.; Johnson, A.J. Concu en in ec ion o lambs wi h pa ain luenza i us ype 3 and
Pasieu eiia haemoly ica.N. Z. Ve . J. 1977,25, 263–265. [C ossRe ]
18. B ode sen, B.W. Bo ine Respi a o y Syncy ial Vi us. Ve . Clin. Food Anim. P ac . 2010,26, 323–333. [C ossRe ]
19.
Jones, C.; Chowdhu y, S. Bo ine He pes i us Type 1 (BHV-1) is an Impo an Co ac o in he Bo ine Respi a o y Disease Complex.
Ve . Clin. Food Anim. P ac . 2010,26, 303–321. [C ossRe ]
20.
Ridpa h, J. The Con ibu ion o In ec ions wi h Bo ine Vi al Dia hea Vi uses o Bo ine Respi a o y Disease.
Ve . Clin. Food Anim. P ac .
2010,26, 335–348. [C ossRe ]
21.
Keles, I.; Woldehiwe , Z.; Mu ay, R.D. In- i o s udies on mechanisms o immunosupp ession associa ed wi h bo ine espi a o y
syncy ial i us. J. Comp. Pa hol. 1998,118, 337–345. [C ossRe ]
Animals 2021,11, 160 7 o 7
22.
Con e as-Luna, M.; Ramí ez-Ma ínez, L.; Sil a Sa mien o, E.; Lazo, C.; To es, A.; Sánchez-Be ancou , J. E idence o espi a o y
syncy ial i us and pa ain luenza-3 i us in Mexican sheep. Vi usDisease 2017,28, 102–110. [C ossRe ] [PubMed]
23.
Lehmkuhl, H.D.; Cu lip, R.C.; Bolin, S.R.; B ogden, K.A. Se oepidemiologic su ey o an ibodies o selec ed i uses in he
espi a o y ac o lambs. Am. J. Ve . Res. 1985,46, 2601–2604. [PubMed]
24.
Yesilbag, K.; Güngö , B. An ibody p e alence agains espi a o y i uses in sheep and goa s in No h-Wes e n Tu key. T op. Anim.
Heal h P od. 2008,41, 421–425. [C ossRe ] [PubMed]
25.
Giangaspe o, M.; Vanopdenbosch, E.; Nishikawa, H.; Tabbaa, D. P e alence o an ibodies agains espi a o y i uses (pa ain-
luenza i us ype 3, espi a o y syncy ial i us, eo i us and adeno i us) in ela ion o p oduc i i y in Sy ian Awassi sheep.
T op. Anim. Heal h P od. 1997,29, 83–91. [C ossRe ] [PubMed]
26.
Hecke , R.A.; Dubuc, C.; B iscoe, M.R.; Range , M. P e alence o bo de disease i us in ec ion in a small g oup o Canadian
sheep. Can. Ve . J. 1994,35, 379–381. [PubMed]
27.
Valdazo-González, B.; Ál a ez, M.; Sand ik, T. P e alence o bo de disease i us in Spanish lambs. Ve . Mic obiol.
2008
,128,
269–278. [C ossRe ]
28.
Valdazo-González, B.; Ál a ez-Ma ínez, M.; G eise -Wilke, I. Gene ic yping and p e alence o Bo de disease i us (BDV) in
small uminan locks in Spain. Ve . Mic obiol. 2006,117, 141–153. [C ossRe ]
29.
Da ies, D.H.; Da is, G.B.; P ice, M.C. A longi udinal se ological su ey o espi a o y i us in ec ions in lambs. N. Z. Ve . J.
1980
,
28, 125–127. [C ossRe ]
30.
Van de Poel, W.H.; Middel, W.G.; Schukken, Y.H. An ibody i e agains bo ine espi a o y syncy ial i us in colos um- ed
dai y cal es bo n in a ious seasons. Am. J. Ve . Res. 1999,60, 1098–1101.
31.
Lanyon, S.R.; Sims, S.K.; Cockc o , P.D.; Reichel, M.P. Compa ison o se um, ea no ches, and nasal and sali a swabs o Bo ine
i al dia hea i us an igen de ec ion in colos um- ed pe sis en ly in ec ed (PI) cal es and non-PI cal es. J. Ve . Diagnos ic In es ig.
2014,26, 783–787. [C ossRe ]
32.
Pal i, V.; Houe, H.; Philipsen, J. S udies on he decline o Bo ine Vi us Dia hoea Vi us (BVDV) ma e nal an ibodies and
de ec abili y o BVDV in pe sis en ly in ec ed cal es. Ac a Ve . Scand. 1993,34, 105–107. [C ossRe ] [PubMed]
33.
Ga cía-Pé ez, A.L.; Minguijón, E.; Ba andika, J.F.; Adu iz, G.; Po edano, I.; Jus e, R.A.; Hu ado, A. De ec ion o Bo de Disease
Vi us in Fe uses, S illbi hs, and Newbo n Lambs om Na u al and Expe imen al In ec ions. J. Ve . Diagn. In es ig.
2009
,21,
331–337. [C ossRe ] [PubMed]
34.
Hay, K.E.; Ba nes, T.S.; Mo on, J.M.; G a el, J.L.; Commins, M.A.; Ho wood, P.F.; Amb ose, R.C.; Clemen s, A.C.A.; Mahony, T.J.
Associa ions be ween exposu e o i uses and bo ine espi a o y disease in Aus alian eedlo ca le. P e . Ve . Med.
2016
,127,
121–133. [C ossRe ] [PubMed]
35.
Ma in, S.; Nagy, E.; A ms ong, D.; Rosendal, S. The associa ions o i al and mycoplasmal an ibody i e s wi h espi a o y
disease and weigh gain in eedlo cal es. Can. Ve . J. 1999,40, 560–567, 570.