1113192 TvD 137 nr 2 bw.indd

wetenschap
Redactioneel
De wetenschappelijke redactie van het
Tijdschrift voor Diergeneeskunde is er
trots op dat de diverse auteurs van dit
artikel er voor gekozen hebben om hun
bevindingen met betrekking tot het
Schmallenbergvirus in het Tijdschrift voor
Diergeneeskunde te publiceren en dat dit
op zo korte termijn na de ontdekking al
kon worden gerealiseerd. Eens te meer
blijkt het belang van de gd Veekijker
groot te zijn. Dit is een laagdrempelig
contactpunt waar een dierenarts direct
een ervaren collega aan de telefoon krijgt,
eentje die wel over die praktijkgrenzen
kan kijken en de juiste ingangen heeft
bij de referentie-instituten. Proficiat voor
de Gezondheidsdienst voor Dieren voor
deze signalering, vervolgstappen en nu
verslaglegging!
Schmallenberg, waren we daar ooit
niet eens op vakantie geweest? dr. Roel
Boosman wetenschappelijke redactie
Epizootic of ovine congenital
malformations associated with
Schmallenberg virus infection
*i
i
R. van den Brom (dvm) , S.J.M. Luttikholt (MSc) , K. Lievaarti
ii
Peterson (dvm, PhD) , N.H.M.T. Peperkamp (dvm) ,
iii
iv
M.H. Mars (dvm, PhD) , W.H.M. van der Poel (dvm, PhD) i
andP. Vellema (dvm, PhD)
TijdschrDiergeneeskd2012:106-111
abstract
Epizootic outbreaks of congenital malformations in sheep are
rare and have, to the best of our knowledge, never been reported
before in Europe. This paper describes relevant preliminary
findings from the first epizootic outbreak of ovine congenital
malformations in the Netherlands.
Between 25 November and 20 December 2011, congenital
malformations in newborn lambs on sheep farms throughout
the country were reported to the Animal Health Service in
Deventer. Subsequently, small ruminant veterinary specialists
visited these farms and collected relevant information from
farmers by means of questionnaires. The deformities varied from
iDepartmentofSmallRuminantHealth,AnimalHealthService,Deventer,
theNetherlands.
IIDepartmentofPathology,AnimalHealthService,Deventer,theNetherlands.
IIIDepartmentofDiagnostics,ResearchandEpidemiology,AnimalHealth
Service,Deventer,theNetherlands.
IVDepartmentofVirology,CentralVeterinaryInstitute,WageningenUniversity
Research,theNetherlands.
*Correspondingauthor:RenévandenBrom,dvm,DepartmentofSmall
RuminantHealth,gd-AnimalHealthServiceDeventer,p.o.Box9,7400
aaDeventer,theNetherlands.E-mail:[email protected]
106
mild to severe, and ewes were reported to have given birth to
both normal and deformed lambs; both male and female lambs
were affected. Most of the affected lambs were delivered at term.
Besides malformed and normal lambs, dummy lambs, unable to
suckle, were born also on these farms. None of the ewes had
shown clinical signs during gestation or at parturition. Dystocia
was common, because of the lambs’ deformities. Lambs were
submitted for post-mortem examination, and samples of brain
tissue were collected for virus detection. The main macroscopic
findings included arthrogryposis, torticollis, scoliosis and
kyphosis, brachygnathia inferior, and mild-to-marked hypoplasia of the cerebrum, cerebellum and spinal cord.
Preliminary data from the first ten affected farms suggest that
nutritional deficiencies, intoxication, and genetic factors are not
likely to have caused the malformations. Preliminary diagnostic
analyses of precolostral serum samples excluded border disease
virus, bovine viral diarrhoea virus, and bluetongue virus.
In December 2011, samples of brain tissue from 54 lambs
were sent to the Central Veterinary Institute of Wageningen
University Research, Lelystad. Real-time pcr detected the
presence of a virus, provisionally named the Schmallenberg
virus, in brain tissue from 22 of the 54 lambs, which originated
from seven of eight farms that had submitted lambs for
post-mortem examination. This Schmallenberg virus was first
reported in Germany and seems to be related to the Shamonda,
Aino, and Akabane viruses, all of which belong to the Simbu
serogroup of the genus Orthobunyavirus of the family Bunyaviridae. These preliminary findings suggest that the Schmallenberg
virus is the most likely cause of this epizootic of ovine congenital malformations, which is the first such outbreak reported in
Europe.
Tijdschrift voor DiergeneeskundeDeel137Aflevering 21februari2012
wetenschap
samenvatting
Epizoötie uitbraak van congenitale afwijkingen bij schapen
lammeren geassocieerd met infectie met het Schmallenbergvirus
Epizoötische uitbraken van congenitale afwijkingen bij schapenlammeren zijn zeldzaam en zijn, voor zover we na hebben kunnen gaan, niet
eerder beschreven in Europa. Dit artikel beschrijft de voorlopige
relevante bevindingen van de eerste epizoötische uitbraak van
congenitale afwijkingen bij lammeren in Nederland.
Tussen 25 november en 20 december 2011 werden bij gd Veekijker
Kleine Herkauwers congenitale afwijkingen bij lammeren gerapporteerd op schapenbedrijven verspreid over het land. Dierenartsen van de
sector Kleine Herkauwers van de gd hebben de bedrijven bezocht en
samen met de veehouder een vragenlijst ingevuld. De waargenomen
congenitale afwijkingen varieerden van mild tot zeer ernstig. Het betrof
zowel ram- als ooilammeren en in geval van meerlingen waren niet
altijd alle lammeren in de worp afwijkend. De meeste lammeren
werden na een normale draagtijd geboren. Naast afwijkende en
normale lammeren, zijn ook ‘domme’ lammeren geboren die niet in
staat waren om te drinken. Zowel tijdens de partus als gedurende de
dracht zijn door de schapenhouders geen klinische verschijnselen aan de
ooien waargenomen, anders dan dystocia ten gevolge van afwijkende
lammeren. Lammeren zijn ingestuurd voor pathologisch onderzoek en
hersenweefselmonsters zijn verzameld voor virologisch onderzoek. De
belangrijkste macroscopische bevindingen waren arthrogrypose,
torticollis, scoliose, kyphose, brachygnathia inferior en geringe tot
ernstige hypoplasie van grote en kleine hersenen en het ruggenmerg.
Gebaseerd op de voorlopige onderzoeksresultaten van de eerste tien
bedrijven lijken mogelijke oorzaken van congenitale afwijkingen bij
lammeren zoals voedingsdeficiënties, intoxicaties en genetische
factoren, onwaarschijnlijk. Voorlopige resultaten van aanvullend
onderzoek op precolostrale sera sluiten border disease virus, bovine
virus diarree virus en bluetongue virus uit als mogelijke oorzaak.
In december zijn hersenweefselmonsters van 54 lammeren opgestuurd
naar het Centraal Veterinair Instituut, Wageningen University
Research, Lelystad. Door middel van een ‘real-time’ pcr werd een
virus, dat voorlopig Schmallenbergvirus wordt genoemd, aangetoond
in de hersenen van 22 van de 54 lammeren, afkomstig van zeven van
de acht bedrijven die lammeren voor pathologisch onderzoek hadden
ingestuurd. Dit Schmallenbergvirus is voor het eerst beschreven in
Duitsland en lijkt het meest verwant aan het Shamonda-, Aino- en
Akabanevirus die alle behoren tot de Simbuserogroep van het genus
Orthobunyavirus van de familie Bunyaviridae.
Deze voorlopige bevindingen geven aan dat het Schmallenbergvirus de
meest waarschijnlijke oorzaak is van de waargenomen epizoötische
uitbraak van congenitale afwijkingen bij lammeren die nooit eerder in
Europa is beschreven.
introduction
Congenital malformations occur in different animal species,
including ruminants (1). The incidence of such malformations
has been reported to be 0.2-2.0% in newborn lambs in Australia
(2). Possible causes of congenital malformations in sheep are
genetic factors (3-5), teratogenic plants (6-8), nutritional
deficiencies (9, 10), and teratogenic viruses (11-31).
Cases of ovine congenital malformations were first reported
to the Dutch Animal Health Service (Gezondheidsdienst voor
Dieren, gd) on 25 November 2011. On 9 December, veterinary
Tijdschrift voor DiergeneeskundeDeel137Aflevering 21februari2012
Figure 1. The location of the 30 farms (red and blue dots) that
reported malformed lambs between 25 November and 20
December 2011.
Thereddotsindicatethefirsttenfarmsthataredescribedin
moredetail.On1January2012,morethan60sheepfarms
havereportedthebirthofmalformedlambs.
practitioners were informed and invited to report further cases
to the gd, and on 20 December disease manifestations were
made notifiable in the Netherlands. This paper describes
preliminary findings from the first ten farms on which malformed lambs were born, and the epizootic characteristics of
these malformations.
materials and methods
Sheep farmers reporting cases of ovine congenital malformations were invited to submit lambs for post-mortem examination to the gd. A questionnaire was drafted and farms were
visited by veterinarians from the gd specialized in small
ruminant health. This paper describes the preliminary observations, gross pathology, and laboratory results of lambs from the
first ten farms affected.
A questionnaire was used to obtain epidemiological and
clinical information during farm visits. The questionnaire
consisted of three parts. The first part focused on general farm
information, including the number of sheep, breeds, animal
movements, other animal species on the farm, and possible
contact with other animals, with special attention for other
ruminants. The second part consisted of questions related to the
health status, feeding regimen, vaccinations performed, and
drugs used. The third part consisted of questions regarding the
current breeding and lambing season and included questions
107
wetenschap
Picture 1. A lamb with congenital malformations: arthrogrypo-
Picture 2. A lamb with congenital malformations: scoliosis and
sis, kyphosis, and brachygnathia inferior.
about oestrus synchronization, age, breed, number, and origin of
the rams used, flock fertility, the start of the lambing season,
timing of births of lambs with malformations, ewe health status,
and malformations of the lambs.
Blood samples were collected from ewes that had given birth to
malformed lambs (maximum five samples per farm), and from
malformed lambs. Samples were tested for border disease virus
(bdv)/bovine viral diarrhoea virus (bvdv) (Priocheck ® bvdv Ab,
Prionics AG, Switzerland; idexx bvdv Ag/Serum Plus Test, idexx
Laboratories, Inc., Westbrook, Maine, u.s.a.), and bluetongue virus
(btv) (idexx Bluetongue Competition Ab Test, idexx Laboratories,
Inc., Westbrook, Maine, u.s.a.). The farmers were asked to submit
lambs with malformations for post-mortem examination. Foetal
blood, brain, and muscle samples and, if available, placental
membranes, were stored for future investigation. Brain tissue
samples were tested at the national reference laboratory, the
Central Veterinary Institute (cvi), Lelystad, the Netherlands, using
a real-time pcr developed by the Friedrich Loeffler Institute (fli).
Number of submitted lambs
torticollis.
The assay targets the L segment of a virus provisionally named the
Schmallenberg virus, a virus from the genus Orthobunyavirus of
the family Bunyaviridae (32).
results
The preliminary gross pathology findings and the location of the
reported farms with malformed lambs are presented in Table 1
and Figure 1. Preliminary findings from the first ten farms to
report congenital malformations, before disease manifestations
were made notifiable, are described in further detail. On farm A,
a ewe gave birth to a malformed lamb of approximately 115
days’ gestation with arthrogryposis and hydranencephaly. This
ewe was bought from farm B at approximately 100 days’
gestation. No lambs had been born on farm B at the time of
reporting of the first case on farm A; however, the farmer
reported that some of his ewes, found pregnant by ultrasonographic scanning earlier, seemed barren later on. From 6
December onwards, farms C, D, E, and F reported congenital
A
B
C
D
E
F
G
H
I
J
3
-
12
14
14
-
2
5
3
2
Number of submitted lambs
with multiple defects
2
-
10
12
9
-
2
5
3
2
25 Nov
25 Nov
6 Dec
7 Dec
8 Dec
9 Dec
12 Dec
13 Dec
14 Dec
14 Dec
Arthrogryposis
*
-
*
*
*
-
*
*
*
*
Torticollis
*
-
*
*
*
-
*
-
*
*
Kyphosis
*
-
*
*
*
-
-
*
*
-
Scoliosis
*
-
*
*
*
-
*
*
*
*
Brachygnatiainferior
-
-
*
*
*
-
-
*
*
*
Micro-/hydranencephaly
*
-
*
*
-
-
*
*
-
*
Hypoplasiacerebrum
-
-
-
-
*
-
-
-
*
-
Cerebellarhypoplasia
*
-
*
*
*
-
*
*
*
*
Hypoplasiaspinalcord
*
-
*
*
*
-
*
*
*
-
Date of reporting
Table 1. Gross pathology ﬁndings of 55 lambs on the ﬁrst ten reported farms (A to J), submitted between 25 November and 20 December 2011 for post-mortem examination.
*:symptompresent
-:notsubmittedorsymptomnotpresent
108
Tijdschrift voor DiergeneeskundeDeel137Aflevering 21februari2012
wetenschap
malformations in lambs. Farm F reported two malformed lambs
out of four newborn, but did not submit lambs for post-mortem
examination. During the first 3 days of the following week,
malformed lambs were reported on farms G, H, I, and J.
The most pronounced malformations were arthrogryposis of
all legs with skeletal muscle dysplasia and deformities of the
cervical and thoracic vertebral column. The deformities varied
from mild to severe, affected both male and female lambs, and
some ewes with multiple lambs had given birth to both normal
and deformed lambs. Most of the affected lambs were delivered
at term; some lambs were stillborn, and a few severely deformed
lambs were born alive. Most of these lambs were not able to
stand or suckle. Besides malformed and normal lambs, dummy
lambs were born that were unable to suckle. Some farmers
reported blindness and abnormal behaviour. None of the
farmers reported clinical signs in the pregnant ewes at delivery
or earlier during gestation, with the exception of dystocia at
parturition due to the lambs’ deformities. Many ewes required
assistance at parturition and some died as a consequence of
uterine perforation. None of the people living or working on the
affected farms have reported clinical signs.
Affected farms had 10-600 sheep and animals did not come
into frequent contact with other species. The breeds on affected
farms included the white and blue Texel, Suffolk, Frisian Milk
Sheep, Flevolander, Swifter, Blessumer, Rouge de L’Ouest, and
crossbreds. While many farms had carried out vaccination and
treatment programmes in the same year, no single vaccine or
medication was used on all affected farms. The flocks were
healthy and had mainly grazed without supplementary feeding
during the breeding season and early gestation. On some farms
the ewes were synchronized. Different breeds of rams had been
used and some had also been used in preceding years. Fertility
rates were lower in some flocks, but higher rates of abortion had
not been reported. Ewes of different ages gave birth to malformed lambs. Four of the farms had also had a lambing period
in October and/or November, and none of the lambs had had
congenital malformations.
The main macroscopic changes were arthrogryposis (Picture
1), torticollis (Picture 2), scoliosis (Picture 2), kyphosis (Picture
1), brachygnathia inferior (Picture 1), and various degrees of
hypoplasia of the central nervous system (Pictures 3 and 4),
resulting in microcephaly, hydranencephaly, cerebellar
hypoplasia, and hypoplasia of the spinal cord. Preliminary
diagnostic analyses of blood samples from ewes and living
malformed lambs and precolostral serum samples from lambs
submitted for post-mortem examination excluded bdv, bvdv,
and btv.
Eight farms submitted lambs for post-mortem examination.
The Schmallenberg virus real-time pcr was positive in brain
tissue samples from 22 of 54 lambs originating from seven of
eight affected farms..
discussion
Ovine congenital malformations are not uncommon, but
usually only a few cases occur per farm (3, 33). Multiple cases of
congenital malformations on a farm may indicate a genetic
background, such as the inherited limb deformity called spider
lamb in pedigree Suffolk lambs (4), or the presence of teratogenic plants (8) or nutritional deficiencies (9, 10, 34). Teratogenic
viruses can cause epizootic outbreaks of congenital malformations in lambs on several farms with different breeds, different
management practices, and in a larger geographic area. Such
outbreaks are rare, but have been reported in Japan, Australia,
Israel, North America, and Africa (20, 21, 23-31).
Picture 3.
Hypoplasia
of the central
nervous
system:
cerebellar
hypoplasia.
Tijdschrift voor DiergeneeskundeDeel137Aflevering 21februari2012
109
wetenschap
Picture 4.
Hypoplasia
of the central
nervous
system:
microcephaly,
hydranen-
cephaly,
cerebellar
hypoplasia.
In Europe, epizootic outbreaks of ovine congenital malformations have, to the best of our knowledge, never been reported.
The affected farms were located throughout the Netherlands,
different breeds were involved, and pregnant ewes did not show
symptoms of disease. Not all farms applied oestrus synchronization or used the same vaccines or drugs. Feeding patterns, apart
from grazing, were also different on the different farms. Taking
this information into consideration, it would seem unlikely that
a genetic background, teratogenic plants, nutritional deficiencies, or teratogenic effects of vaccines or drugs are a possible
cause of these congenital malformations.
bdv, bvdv, and btv are the most plausible teratogenic viruses
in the Netherlands, and although a recent serological study
demonstrated a pestivirus prevalence of 45% in sheep in the
Netherlands (35), this causal agent could be excluded. btv-8 has
been demonstrated to cause hydranencephaly in cattle and sheep
(13, 14), and although btv has not been detected in the Netherlands since 2008, it was necessary to exclude this viral agent as a
possible cause. The fact that none of the farmers reported clinical
signs in the pregnant ewes during gestation or at parturition was
consistent with this virus not being the causative agent.
The next group of viruses reported to cause congenital
malformations in sheep are viruses of the genus Bunyaviridae.
Epizootic outbreaks caused by viruses of this family, such as
Akabane, Cache Valley, Main Drain, San Angelo, Lacrosse and
Rift Valley fever virus have been reported in Japan, Australia,
Israel, America, and Africa (20, 21, 23-31), and seroprevalence
without clinical features has been described in Cyprus (36) and
Turkey (37). Using brain samples, in 22 of 54 affected lambs
originating from seven of eight different farms, we detected a
virus provisionally named the Schmallenberg virus. On the basis
110
of its rna sequences, this virus seems most likely related to the
Shamonda, Aino and Akabane viruses, which all belong to the
Simbu serogroup of the genus Orthobunyavirus of the family
Bunyaviridae (32).
In conclusion, a virus of the genus Orthobunyavirus, provisionally called Schmallenberg virus, is regarded as the most
likely cause of the epizootic outbreak of ovine congenital
malformations. This is the first report of such malformations in
Europe.
acknowledgements
Monitoring of small ruminant health in the Netherlands is
financially supported by the Dutch Ministry of Economic
Affairs, Agriculture and Innovation (el&i) and the Product
Board for Livestock and Meat (pvv). We would like to thank our
colleagues, both at the Animal Health Service (gd) and the
Central Veterinary Institute (cvi), sheep farmers, and veterinarians who kindly provided information and submitted lambs for
post-mortem examination. We also want to thank M. Beer and
B. Hoffmann of the Friedrich Loeffler Institute, Riems, Germany,
for kindly sharing their rt-pcr assay for detection of the
Schmallenberg virus. The research on virus detection and
characterization at the Central Veterinary Institute of Wageningen University and Research was performed as part of the
research project “VirusTrack” commissioned by the Dutch
Ministry of Economic Affairs, Agriculture and Innovation.
references
1.GrantMaxieM.Jubb,Kennedy&Palmer’sPathologyofDomesticAnimals.
GrantMaxieM,editor:SaundersLtd.;5edition(April13,2007)2007April13,
2007.
Tijdschrift voor DiergeneeskundeDeel137Aflevering 21februari2012
wetenschap
2.DennisSandLeipoldHW.Ovinecongenitaldefects.VetBull1979;49:
233-239.
3.WhittingtonRJ,GlastonburyJR,PlantJWandBarryMR.Congenital
hydranencephalyandarthrogryposisofCorriedalesheep.Australian
veterinaryjournal.1988;65(4):124-127.Epub1988/04/01.
4.DohertyM,KelleyE,HealyA,CallananJ,CrosbyT,SkellyC,etal.Congenital
arthrogryposis:aninheritedlimbdeformityinpedigreeSuffolklams.The
VeterinaryRecord2000;146(26):748-753.
5.TejedorMT,FerrerLM,MonteagudoLV,RamosJJ,LacastaDandClimentS.
19.TopluN,OguzogluTC,EpikmenETandAydoganA.Neuropathologicstudyof
borderdiseasevirusinnaturallyinfectedfetalandneonatalsmall
ruminantsanditsassociationwithapoptosis.Veterinarypathology2011;48
(3):576-583.Epub2010/05/13.
20.InabaY,KurogiHandOmoriT.Letter:Akabanedisease:epizooticabortion,
prematurebirth,stillbirthandcongenitalarthrogryposis-hydranencephaly
incattle,sheepandgoatscausedbyAkabanevirus.Australianveterinary
journal1975;51(12):584-585.Epub1975/12/01.
21.CoetzerJAandBarnardBJ.Hydropsamniiinsheepassociatedwith
Ovineheritablearthrogryposismultiplexcongenitawithprobablelethal
hydranencephalyandarthrogryposiswithwesselsbrondiseaseandrift
autosomalrecessivemutation.Journalofcomparativepathology2010;143
valleyfevervirusesasaetiologicalagents.TheOnderstepoortjournalof
(1):14-19.Epub2010/02/16.
6.JamesLF,KeelerRFandBinnsW.Sequenceintheabortiveandteratogenic
effectsoflocoweedfedtosheep.Americanjournalofveterinaryresearch.
1969;30(3):377-380.Epub1969/03/01.
7.PanterKE,KeelerRFandBakerDC.Toxicosesinlivestockfromthehemlocks
(ConiumandCicutaspp.).Journalofanimalscience1988;66(9):2407-2413.
Epub1988/09/01.
8.PanterKE,KeelerRF,BunchTDandCallanRJ.CongenitalskeletalmalformationsandcleftpalateinducedingoatsbyingestionofLupinus,Coniumand
Nicotianaspecies.Toxicon:officialjournaloftheInternationalSocietyon
Toxinology1990;28(12):1377-1385.Epub1990/01/01.
9.BarlowRM.Furtherobservationsonswayback.II.Histochemicallocalisation
ofcytochromeoxidaseactivityinthecentralnervoussystem.Journalof
comparativepathology1963;73:61-67.Epub1963/01/01.
10.BarlowRM.Furtherobservationsonswayback.I.Transitionalpathology.
Journalofcomparativepathology1963;73:51-60.Epub1963/01/01.
11.RichardsonC,TaylorWP,TerleckiSandGibbsEP.Observationsontransplacentalinfectionwithbluetonguevirusinsheep.Americanjournalof
veterinaryresearch1985;46(9):1912-1922.Epub1985/09/01.
12.FlanaganMandJohnsonSJ.TheeffectsofvaccinationofMerinoeweswith
veterinaryresearch1977;44(2):119-126.Epub1977/06/01.
22.ParsonsonIM,Della-PortaAJandSnowdonWA.Congenitalabnormalitiesin
newbornlambsafterinfectionofpregnantsheepwithAkabanevirus.
Infectionandimmunity1977;15(1):254-262.Epub1977/01/01.
23.CoetzerJA.ThepathologyofRiftValleyfever.I.Lesionsoccurringinnatural
casesinnew-bornlambs.TheOnderstepoortjournalofveterinaryresearch
1977;44(4):205-211.Epub1977/12/01.
24.HaugheyK,HarleyW,Della-PortaAandMurrayM.Akabanediseasein
sheep.Australianveterinaryjournal1988;65(5):136-140.
25.ChungS,LivingstonCJ,EdwardsJ,CrandellR,ShopeR,SheltonMetal.
EvidencethatCacheValleyvirusinducescongenitalmalformationsin
sheep.Veterinarymicrobiology1990;21(4):297-307.
26.ChungS,LivingstonCJ,JonesCandCollissonE.CacheValleyvirusinfection
inTexassheepflocks.JournaloftheAmericanVeterinaryMedical
Association1991;199(3):337-340.
27.CharlesJ.Akabanevirus.TheVeterinaryclinicsofNorthAmericaFood
animalpractice1994;10(3):525-546.
28.EdwardsJ.CacheValleyvirus.TheVeterinaryclinicsofNorthAmericaFood
animalpractice1994;10(3):515-524.
29.EdwardsJ,KarabatsosN,CollissonEanddelaConchaBermejilloA.Ovine
anattenuatedAustralianbluetonguevirusserotype23atdifferentstagesof
fetalmalformationsinducedbyinuteroinoculationwithMainDrain,San
gestation.Australianveterinaryjournal.1995;72(12):455-457.Epub
Angelo,andLaCrosseviruses.AmJTropMedHyg1997;56(2):171-176.
1995/12/01.
13.VercauterenG,MiryC,VandenbusscheF,DucatelleR,VanderHeydenS,
VandemeulebrouckeEetal.Bluetonguevirusserotype8-associated
congenitalhydranencephalyincalves.Transboundaryandemerging
diseases.2008;55(7):293-298.Epub2008/05/28.
14.WoudaW,PeperkampNH,RoumenMP,MuskensJ,vanRijnAandVellemaP.
Epizooticcongenitalhydranencephalyandabortionincattledueto
bluetonguevirusserotype8intheNetherlands.Tijdschriftvoordiergeneeskunde2009;134(10):422-427.Epub2009/06/16.
15.BarlowRM.Morphogenesisofhydranencephalyandotherintracranial
malformationsinprogenyofpregnantewesinfectedwithpestiviruses.
30.HunterP,ErasmusBJandVorsterJH.TeratogenicityofamutagenisedRift
Valleyfevervirus(MVP12)insheep.TheOnderstepoortjournalofveterinary
research2002;69(1):95-98.Epub2002/07/03.
31.KimY,KweonC,TarkD,LimS,YangD,HyunBetal.Developmentof
inactivatedtrivalentvaccinefortheteratogenicAino,AkabaneandChuzan
viruses.Biologicals2011;39(3):152-157.doi:10.1016/j.biologicals.2011.02.004
EpubMar21.
32.AnovelOrthobunyavirusinfectioninGermancattle.[databaseonthe
Internet].ProMed.2011.Availablefrom:http://www.promedmail.org/direct.
php?id=20111119.3404.
33.DennisSM.PerinatallambmortalityinWesternAustralia.7.Congenital
Journalofcomparativepathology1980;90(1):87-98.Epub1980/01/01.
defects.Australianveterinaryjournal1975;51(2):80-82.Epub1975/02/01.
16.PlantJW,WalkerKH,AclandHMandGardGP.Pathologyintheovinefoetus
34.MatthewsJ.Diseasesofthegoat,3rded.Oxford,OX42DQ,UnitedKingdom:
causedbyanovinepestivirus.Australianveterinaryjournal1983;60(5):
137-140.Epub1983/05/01.
17.Hewicker-TrautweinMandTrautweinG.Porencephaly,hydranencephaly
andleukoencephalopathyinovinefetusesfollowingtransplacental
infectionwithbovinevirusdiarrhoeavirus:distributionofviralantigenand
characterizationofcellularresponse.Actaneuropathologica1994;87(4):
385-397.Epub1994/01/01.
18.TopluN,OguzogluTCandAlbayrakH.DualInfectionofFetalandNeonatal
SmallRuminantswithBorderDiseaseVirusandPestedesPetitsRuminants
BlackwellPublishingLtd;2009,Feb4.
35.OrselK,AntonisAF,OosterlooJC,VellemaPandvanderMeerFJ.SeroprevalenceofantibodiesagainstpestivirusesinsmallruminantsinThe
Netherlands.Tijdschriftvoordiergeneeskunde2009;134(9):380-384.Epub
2009/06/02.
36.SellersRandHernimanKA.NeutralisingantibodiestoAkabanevirusin
ruminantsinCyprus.TropAnimHealthProd1981;13(1):57-60.
37.TaylorWP,andMellorPS.ThedistributionofAkabanevirusintheMiddle
East.Epidemiologyandinfection1994;113(1):175-185.Epub1994/08/01.
Virus(PPRV):NeuronalTropismofPPRVasaNovelFinding.Journalof
comparativepathology2011.Epub2011/09/09.
Tijdschrift voor DiergeneeskundeDeel137Aflevering 21februari2012
Artikelingediend:27december2011
Artikelgeaccepteerd:9januari2012
111

Download Report