A Review on Reliable and Standardized Animal Models to Study the Pathogenesis of Schmallenberg Virus in Ruminant Natural Host Species.

Martinelle, Ludovic; Saegerman, Claude

doi:10.1007/978-1-0716-4338-9_16

Article (Scientific journals)

A Review on Reliable and Standardized Animal Models to Study the Pathogenesis of Schmallenberg Virus in Ruminant Natural Host Species.

Martinelle, Ludovic; Saegerman, Claude

2025 • In Methods in Molecular Biology, 2893, p. 207 - 222

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/331497

DOI
10.1007/978-1-0716-4338-9_16

PubMed
39671040

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

Review Reliable and Standardized Animal Models to Study SBV_Final.pdf

Author postprint (422.64 kB)

Download

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

Arboviruses; Culicoides; Experimental challenge; Infection; Schmallenberg; Vector-borne disease; Animals; Cattle; Pregnancy; Female; Placenta/virology; Cattle Diseases/virology; Orthobunyavirus/pathogenicity; Bunyaviridae Infections/virology; Bunyaviridae Infections/veterinary; Disease Models, Animal; Ruminants/virology; Bunyaviridae Infections; Cattle Diseases; Orthobunyavirus; Placenta; Ruminants; Molecular Biology; Genetics

Abstract :

[en] In the late summer of 2011, the Netherlands reported a cluster of reduced milk yield, fever, and diarrhea in dairy cattle. In March 2012, congenital malformations appeared, and Schmallenberg virus (SBV) was identified, becoming one of the few orthobunyaviruses distributed in Europe. Initially, little was known about the pathogenesis and epidemiology of these viruses in the European context, so assumptions were largely extrapolated from related viruses and other regions worldwide. To study SBV's pathogenesis and its ability to cross the placental barrier, standardized and repeatable models that mimic clinical signs observed in the field are essential. This review discusses some of the latest experimental designs for infectious disease challenges involving SBV, covering infectious doses, routes of infection, inoculum preparation, and origin. Special attention is given to the placental crossing associated with SBV.

Disciplines :

Veterinary medicine & animal health

Author, co-author :

Martinelle, Ludovic ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH) > FARAH: Productions animales durables

Saegerman, Claude ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires (DMI) > Epidémiologie et analyse des risques appliqués aux sciences vétérinaires

Language :

English

Title :

A Review on Reliable and Standardized Animal Models to Study the Pathogenesis of Schmallenberg Virus in Ruminant Natural Host Species.

Publication date :

2025

Journal title :

Methods in Molecular Biology

ISSN :

1064-3745

eISSN :

1940-6029

Publisher :

Springer, United States

Volume :

2893

Pages :

207 - 222

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

https://link.springer.com/content/pdf/10.1007/978-1-0716-4338-9_16

Available on ORBi :

since 09 May 2025

Statistics

Number of views

84 (0 by ULiège)

Number of downloads

43 (0 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Carrasco-Hernandez R, Jacome R, Lopez Vidal Y, Ponce de Leon S (2017) Are RNA viruses candidate agents for the next global pandemic? A review. ILAR J 58(3):343–358. https://doi.org/10.1093/ilar/ilx026
Adams MJ, Lefkowitz EJ, King AMQ, Harrach B, Harrison RL, Knowles NJ, Kro-pinski AM, Krupovic M, Kuhn JH, Mushegian AR, Nibert M, Sabanadzovic S, Sanfacon H, Siddell SG, Simmonds P, Varsani A, Zerbini FM, Gorbalenya AE, Davison AJ (2017) Changes to taxonomy and the international code of virus classification and nomenclature ratified by the international committee on taxonomy of viruses. Arch Virol 162(8):2505–2538. https://doi.org/10. 1007/s00705-017-3358-5
ICTV (2024) History of the taxon: species: Orthobunyavirus schmallenbergense (2023 Release, MSL #39). https://ictv.global/taxon omy/taxondetails?taxnode_id=202300126& t a x o n _ n a me = Or t h o b u n y a v i r u s % 2 0 schmallenbergense. Accessed 02/07/2024
Hughes HR, Adkins S, Alkhovskiy S, Beer M, Blair C, Calisher CH, Drebot M, Lambert AJ, de Souza WM, Marklewitz M, Nunes MRT, Shi 石晓宏 X, Ictv Report C (2020) ICTV virus taxonomy profile: peribunyaviridae. J Gen Virol 101(1):1–2. https://doi.org/10. 1099/jgv.0.001365
Kinney RM, Calisher CH (1981) Antigenic relationships among Simbu serogroup (Bunya-viridae) viruses. Am J Trop Med Hyg 30(6):1307–1318
De Regge N (2017) Akabane, Aino and Schmallenberg virus-where do we stand and what do we know about the role of domestic ruminant hosts and Culicoides vectors in virus transmission and overwintering? Curr Opin Virol 27:15–30. https://doi.org/10.1016/j. coviro.2017.10.004
Coetzee P, van Vuuren M, Venter EH, Stokstad M (2014) A review of experimental infections with bluetongue virus in the mammalian host. Virus Res 182:21–34. https://doi.org/10.1016/j.virusres.2013.12.044
Speder B (2014) Regulatory requirements for viral-challenge studies: influenza case study. London
Breard E, Schulz C, Sailleau C, Bernelin-Cottet C, Viarouge C, Vitour D, Guillaume B, Caignard G, Gorlier A, Attoui H, Gallois M, Hoffmann B, Zientara S, Beer M (2018) Bluetongue virus serotype 27: experimental infection of goats, sheep and cattle with three BTV-27 variants reveal atypical characteristics and likely direct contact transmission BTV-27 between goats. Transbound Emerg Dis 65(2):e251–e263. https://doi.org/10.1111/tbed.12780
MacLachlan NJ, Nunamaker RA, Katz JB, Sawyer MM, Akita GY, Osburn BI, Tabachnick WJ (1994) Detection of bluetongue virus in the blood of inoculated calves: comparison of virus isolation, PCR assay, and in vitro feeding of Culicoides variipennis. Arch Virol 136(1–2):1–8
Collins AB, Mee JF, Kirkland PD (2018) Pathogenicity and teratogenicity of Schmallenberg virus and Akabane virus in experimentally infected chicken embryos. Vet Microbiol 216: 31–37. https://doi.org/10.1016/j.vetmic. 2018.01.009
Laloy E, Breard E, Trapp S, Pozzi N, Riou M, Barc C, Breton S, Delaunay R, Cordonnier N, Chateau-Joubert S, Crochet D, Gouzil J, Hebert T, Raimbourg M, Viarouge C, Vitour D, Durand B, Ponsart C, Zientara S (2017) Fetopathic effects of experimental Schmallenberg virus infection in pregnant goats. Vet Microbiol 211:141–149. https://doi.org/10.1016/j.vetmic.2017.10.011
Tauscher K, Wernike K, Fischer M, Wegelt A, Hoffmann B, Teifke JP, Beer M (2017) Characterization of Simbu serogroup virus infections in type I interferon receptor knock-out mice. Arch Virol 162(10):3119–3129. ht t ps: //doi. org/10. 1007/s 00705-017-3475-1
Boshra HY, Charro D, Lorenzo G, Sanchez I, Lazaro B, Brun A, Abrescia NG (2017) DNA vaccination regimes against Schmallenberg virus infection in IFNAR(-/-) mice suggest two targets for immunization. Antiviral Res 141:107–115. https://doi.org/10.1016/j. antiviral.2017.02.013
Poskin A, Verite S, Comtet L, Van der Stede Y, Cay B, De Regge N (2015) Persistence of the protective immunity and kinetics of the isotype specific antibody response against the viral nucleocapsid protein after experimental Schmallenberg virus infection of sheep. Vet Res 46:119. https://doi.org/10.1186/s13567-015-0260-6
Dagnaw M, Solomon A, Dagnew B (2024) Serological prevalence of the Schmallenberg virus in domestic and wild hosts worldwide: a systematic review and meta-analysis. Front Vet Sci 11:1371495. https://doi.org/10.3389/fvets.2024.1371495
Drolet BS, Reister LM, Lehiy CJ, Van Rijn PA, Bowen RA (2015) Effect of Culicoides sonorensis salivary proteins on clinical disease outcome in experimental bluetongue virus serotype 8 infection of Dorset sheep. Vet Ital 51(4):379–384. https://doi.org/10.12834/VetIt.496.2398.1
Darpel KE, Langner KF, Nimtz M, Anthony SJ, Brownlie J, Takamatsu HH, Mellor PS, Mertens PP (2011) Saliva proteins of vector Culicoides modify structure and infectivity of bluetongue virus particles. PLoS One 6(3): e17545. https://doi.org/10.1371/journal. pone.0017545
Wernike K, Eschbaumer M, Breithaupt A, Hoffmann B, Beer M (2012) Schmallenberg virus challenge models in cattle: infectious serum or culture-grown virus? Vet Res 43:84. https://doi.org/10.1186/1297-9716-43-84
Wernike K, Hoffmann B, Breard E, Botner A, Ponsart C, Zientara S, Lohse L, Pozzi N, Viarouge C, Sarradin P, Leroux-Barc C, Riou M, Laloy E, Breithaupt A, Beer M (2013) Schmallenberg virus experimental infection of sheep. Vet Microbiol 166(3–4):461–466. https://doi.org/10. 1016/j.vetmic.2013.06.030
Varela M, Schnettler E, Caporale M, Murgia C, Barry G, McFarlane M, McGregor E, Piras IM, Shaw A, Lamm C, Janowicz A, Beer M, Glass M, Herder V, Hahn K, Baumgartner W, Kohl A, Palmarini M (2013) Schmallenberg virus pathogenesis, tropism and interaction with the innate immune system of the host. PLoS Pathog 9(1):e1003133. https://doi. org/10.1371/journal.ppat.1003133
Kraatz F, Wernike K, Hechinger S, Konig P, Granzow H, Reimann I, Beer M (2015) Deletion mutants of Schmallenberg virus are aviru-lent and protect from virus challenge. J Virol 89(3):1825–1837. https://doi.org/10.1128/JVI.02729-14
Hofmann MA, Mader M, Fluckiger F, Renzullo S (2015) Genetic stability of Schmallenberg virus in vivo during an epidemic, and in vitro, when passaged in the highly susceptible porcine SK-6 cell line. Vet Microbiol 176(1–2):97–108. https://doi.org/10.1016/j.vetmic.2015.01.010
Venter GJ, Mellor PS, Wright I, Paweska JT (2007) Replication of live-attenuated vaccine strains of bluetongue virus in orally infected South African Culicoides species. Med Vet Entomol 21(3):239–247. https://doi.org/10.1111/j.1365-2915.2007.00687.x
Horne KM, Vanlandingham DL (2014) Bunyavirus-vector interactions. Viruses 6(11):4373–4397. https://doi.org/10.3390/v6114373
Le Coupanec A, Babin D, Fiette L, Jouvion G, Ave P, Misse D, Bouloy M, Choumet V (2013) Aedes mosquito saliva modulates Rift Valley fever virus pathogenicity. PLoS Negl Trop Dis 7(6):e2237. https://doi.org/10.1371/jour nal.pntd.0002237
Martinelle L, Poskin A, Dal Pozzo F, Mostin L, Van Campe W, Cay AB, De Regge N, Saegerman C (2017) Three different routes of inoculation for experimental infection with Schmallenberg virus in sheep. Transbound Emerg Dis 64(1):305–308. https://doi.org/10.1111/tbed.12356
Nicolas JF, Guy B (2008) Intradermal, epidermal and transcutaneous vaccination: from immunology to clinical practice. Expert Rev Vaccines 7(8):1201–1214. https://doi.org/10.1586/14760584.7.8.1201
Umeshappa CS, Singh KP, Channappanavar R, Sharma K, Nanjundappa RH, Saxena M, Singh R, Sharma AK (2011) A comparison of intradermal and intravenous inoculation of bluetongue virus serotype 23 in sheep for clinico-pathology, and viral and immune responses. Vet Immunol Immunopathol 141(3–4):230–238. https://doi.org/10. 1016/j.vetimm.2011.03.005
Alexandersen S, Quan M, Murphy C, Knight J, Zhang Z (2003) Studies of quantitative parameters of virus excretion and transmission in pigs and cattle experimentally infected with foot-and-mouth disease virus. J Comp Pathol 129(4):268–282
Howey R, Quan M, Savill NJ, Matthews L, Alexandersen S, Woolhouse M (2009) Effect of the initial dose of foot-and-mouth disease virus on the early viral dynamics within pigs. J R Soc Interface 6(39):835–847. https://doi. org/10.1098/rsif.2008.0434
Quan M, Murphy CM, Zhang Z, Alexandersen S (2004) Determinants of early foot-and-mouth disease virus dynamics in pigs. J Comp Pathol 131(4):294–307. https://doi.org/10. 1016/j.jcpa.2004.05.002
Poskin A, Martinelle L, Mostin L, Van Campe W, Dal Pozzo F, Saegerman C, Cay AB, De Regge N (2014) Dose-dependent effect of experimental Schmallenberg virus infection in sheep. Vet J 201(3):419–422. https://doi.org/10.1016/j.tvjl.2014.05.031
Pages N, Breard E, Urien C, Talavera S, Viarouge C, Lorca-Oro C, Jouneau L, Charley B, Zientara S, Bensaid A, Solanes D, Pujols J, Schwartz-Cornil I (2014) Culicoides midge bites modulate the host response and impact on bluetongue virus infection in sheep. PLoS One 9(1):e83683. https://doi.org/10. 1371/journal.pone.0083683
Bishop JV, Mejia JS, Perez de Leon AA, Tabachnick WJ, Titus RG (2006) Salivary gland extracts of Culicoides sonorensis inhibit murine lymphocyte proliferation and no production by macrophages. Am J Trop Med Hyg 75(3):532–536
Limesand KH, Higgs S, Pearson LD, Beaty BJ (2003) Effect of mosquito salivary gland treatment on vesicular stomatitis New Jersey virus replication and interferon alpha/beta expression in vitro. J Med Entomol 40(2):199–205
Boorman J (1974) The maintenance of laboratory colonies of Culicoides variipennis (Coq.), C. nubeculosus (Mg.) and C. riethi Kieff. (Dip-tera, Ceratopogonidae). Bull Entomol Res 64(3):371–377. https://doi.org/10.1017/S0007485300031254
Veronesi E, Antony F, Gubbins S, Golding N, Blackwell A, Mertens PP, Brownlie J, Darpel KE, Mellor PS, Carpenter S (2013) Measurement of the infection and dissemination of bluetongue virus in culicoides biting midges using a semi-quantitative rt-PCR assay and isolation of infectious virus. PLoS One 8(8): e70800. https://doi.org/10.1371/journal. pone.0070800
Evermann JF, McKeirnan AJ, Wilbur LA, Levings RL, Trueblood ES, Baldwin TJ, Hugh-banks FG (1994) Canine fatalities associated with the use of a modified live vaccine administered during late stages of pregnancy. J Vet Diagn Invest 6(3):353–357
Wilbur LA, Evermann JF, Levings RL, Stoll IR, Starling DE, Spillers CA, Gustafson GA, McKeirnan AJ (1994) Abortion and death in pregnant bitches associated with a canine vaccine contaminated with bluetongue virus. J Am Vet Med Assoc 204(11):1762–1765
Breard E, Belbis G, Hamers C, Moulin V, Lilin T, Moreau F, Millemann Y, Montange C, Sailleau C, Durand B, Desprat A, Viarouge C, Hoffmann B, de Smit H, Goutebroze S, Hudelet P, Zientara S (2011) Evaluation of humoral response and protective efficacy of two inactivated vaccines against bluetongue virus after vaccination of goats. Vaccine 29(13):2495–2502. https:// doi.org/10.1016/j.vaccine.2010.12.105
Martinelle L, Dal Pozzo F, Sarradin P, Van Campe W, De Leeuw I, De Clercq K, Thys C, Thiry E, Saegerman C (2016) Experimental bluetongue virus superinfection in calves previously immunized with bluetongue virus serotype 8. Vet Res 47(1):73. https://doi.org/10. 1186/s13567-016-0357-6
Eschbaumer M, Wackerlin R, Savini G, Zientara S, Sailleau C, Breard E, Beer M, Hoffmann B (2011) Contamination in bluetongue virus challenge experiments. Vaccine 29(26):4299–4301. https://doi.org/10. 1016/j.vaccine.2011.04.049
Dal Pozzo F, Martinelle L, Thys C, Sarradin P, De Leeuw I, Van Campe W, De Clercq K, Thiry E, Saegerman C (2013) Experimental co-infections of calves with bluetongue virus serotypes 1 and 8. Vet Microbiol 165(1–2):167–172. https://doi.org/10. 1016/j.vetmic.2013.01.016
Rasmussen LD, Savini G, Lorusso A, Bellacicco A, Palmarini M, Caporale M, Rasmussen TB, Belsham GJ, Botner A (2013) Transplacental transmission of field and rescued strains of BTV-2 and BTV-8 in experimentally infected sheep. Vet Res 44:75. https://doi.org/10.1186/1297-9716-44-75
Vandenbussche F, Sailleau C, Rosseel T, Desprat A, Viarouge C, Richardson J, Eschbaumer M, Hoffmann B, De Clercq K, Breard E, Zientara S (2015) Full-genome sequencing of four bluetongue virus serotype 11 viruses. Transbound Emerg Dis 62(5):565–571. https://doi.org/10.1111/tbed.12178
Doceul V, Lara E, Sailleau C, Belbis G, Richardson J, Breard E, Viarouge C, Dominguez M, Hendrikx P, Calavas D, Desprat A, Languille J, Comtet L, Pourquier P, Eleouet JF, Delmas B, Marianneau P, Vitour D, Zientara S (2013) Epidemiology, molecular virology and diagnostics of Schmallenberg virus, an emerging orthobunyavirus in Europe. Vet Res 44:31. https://doi.org/10.1186/1297-9716-44-31
Garigliany MM, Bayrou C, Kleijnen D, Cassart D, Desmecht D (2012) Schmallenberg virus in domestic cattle, Belgium, 2012. Emerg Infect Dis 18(9):1512–1514. https://doi.org/10.3201/eid1809.120716
Parsonson IM, McPhee DA, Della-Porta AJ, McClure S, McCullagh P (1988) Transmission of Akabane virus from the ewe to the early fetus (32 to 53 days). J Comp Pathol 99(2):215–227
Charles JA (1994) Akabane virus. Vet Clin North Am Food Anim Pract 10(3):525–546
Amoroso EC (1961) Histology of the placenta. Br Med Bull 17:81–90
Wooding FB (1992) Current topic: the syne-pitheliochorial placenta of ruminants: binucle-ate cell fusions and hormone production. Placenta 13(2):101–113
Wooding P, Burton G (2008) Comparative placentation. Springer, Cambridge
King GJ, Atkinson BA, Robertson HA (1979) Development of the bovine placentome during the second month of gestation. J Reprod Fertil 55(1):173–180
Martinelle L, Poskin A, Dal Pozzo F, De Regge N, Cay B, Saegerman C (2015) Experimental infection of sheep at 45 and 60 days of gestation with Schmallenberg virus readily led to placental colonization without causing congenital malformations. PLoS One 10(9): e0139375. https://doi.org/10.1371/journal. pone.0139375
Szabo KT (1989) Congenital malformations in laboratory and farm animals. Academic Press
Coppock RW, Dziwenka MM (2017) Chapter 72 – teratogenesis in livestock. In: Press A (ed) Reproductive and developmental toxicology, 2nd edn. Elsevier, pp 1391–1408. ht t ps: //doi. or g/10. 1016/B978-0-12-804239-7.00072-X
Evans HE, Sack WO (1973) Prenatal development of domestic and laboratory mammals: growth curves, external features and selected references. Zentralbl Veterinarmed C 2(1):11–45
Schultz RD, Dunne HW, Heist CE (1973) Ontogeny of the bovine immune response. Infect Immun 7(6):981–991
Silverstein AM, Uhr JW, Kraner KL, Lukes RJ (1963) Fetal response to antigenic stimulus. II. Antibody production by the fetal lamb. J Exp Med 117:799–812
Fahey KJ, Morris B (1978) Humoral immune responses in foetal sheep. Immunology 35(4):651–661
De Regge N, van den Berg T, Georges L, Cay B (2013) Diagnosis of Schmallenberg virus infection in malformed lambs and calves and first indications for virus clearance in the fetus. Vet Microbiol 162(2–4):595–600. https://doi. org/10.1016/j.vetmic.2012.11.029
Coetzee P, Stokstad M, Myrmel M, Mutowembwa P, Loken T, Venter EH, Van Vuuren M (2013) Transplacental infection in goats experimentally infected with a European strain of bluetongue virus serotype 8. Vet J 197(2):335–341. https://doi.org/10.1016/j. tvjl.2013.01.005
Poskin A, Martinelle L, Van der Stede Y, Saegerman C, Cay B, De Regge N (2017) Genetically stable infectious Schmallenberg virus persists in foetal envelopes of pregnant ewes. J Gen Virol 98(7):1630–1635. https://doi.org/10.1099/jgv.0.000841
Consortium E (2014) Schmallenberg virus Technical and scientific studies. Final report. Wageningen
Wernike K, Elbers A, Beer M (2015) Schmallenberg virus infection. Rev Sci Tech 34(2):363–373
Veldhuis AM, Carp-van Dijken S, van Wuijckhuise L, Witteveen G, van Schaik G (2014) Schmallenberg virus in Dutch dairy herds: potential risk factors for high within-herd seroprevalence and malformations in calves, and its impact on productivity. Vet Microbiol 168(2–4):281–293. https://doi. org/10.1016/j.vetmic.2013.11.021
Dominguez M, Gache K, Touratier A, Perrin JB, Fediaevsky A, Collin E, Breard E, Sailleau C, Viarouge C, Zanella G, Zientara S, Hendrikx P, Calavas D (2014) Spread and impact of the Schmallenberg virus epidemic in France in 2012-2013. BMC Vet Res 10:248. ht t ps: //doi. org/10. 1186/s 12917-014-0248-x
Dominguez M, Hendrikx P, Zientara S, Calavas D, Jay M, Touratier A, Languille J, Fediaevsky A (2012) Preliminary estimate of Schmallenberg virus infection impact in sheep flocks – France. Vet Rec 171(17):426. https://doi.org/10.1136/vr.100883
Saegerman C, Martinelle L, Dal Pozzo F, Kirschvink N (2014) Preliminary survey on the impact of Schmallenberg virus on sheep flocks in south of Belgium. Transbound Emerg Dis 61(5):469–472. https://doi.org/10.1111/tbed.12047
Belgian Biosafety Server (2018) Service Biosafety and Biotechnology (SBB) https://www. biosafety.be/content/tools-belgian-classifica tion-micro-organisms-based-their-biological-risks. Accessed 15/08/2018
Eschbaumer M, Wackerlin R, Rudolf M, Keller M, Konig P, Zemke J, Hoffmann B, Beer M (2010) Infectious blood or culture-grown virus: a comparison of bluetongue virus challenge models. Vet Microbiol. S0378-1135(10)00227-0 [pii]. https://doi.org/10. 1016/j.vetmic.2010.05.004
Spencer TE, Forde N, Lonergan P (2016) Insights into conceptus elongation and establishment of pregnancy in ruminants. Reprod Fertil Dev 29(1):84–100. https://doi.org/10.1071/RD16359
Martinelle L, Dal Pozzo F, Kirschvink N, De la Grandiere MA, Thiry E, Saegerman C (2012) Le virus Schmallenberg ou l’émergence du premier Orthobunyavirus du sérogroupe Simbu en Europe. Ann Med Vet 156:7–24
Afonso A, Abrahantes JC, Conraths F, Veldhuis A, Elbers A, Roberts H, Van der Stede Y, Meroc E, Gache K, Richardson J (2014) The Schmallenberg virus epidemic in Europe-2011-2013. Prev Vet Med 116(4):391–403. https://doi.org/10.1016/j. prevetmed.2014.02.012
Assis Neto AC, Pereira FT, Santos TC, Ambro-sio CE, Leiser R, Miglino MA (2010) Morpho-physical recording of bovine conceptus (Bos indicus) and placenta from days 20 to 70 of pregnancy. Reprod Domest Anim 45(5):760–772. https://doi.org/10.1111/j. 1439-0531.2009.01345.x
Spencer TE, Johnson GA, Bazer FW, Bur-ghardt RC (2004) Implantation mechanisms: insights from the sheep. Reproduction 128(6):657–668. https://doi.org/10.1530/rep.1.00398
Bryden MM, Evans HE, Binns W (1972) Embryology of the sheep. I. Extraembryonic membranes and the development of body form. J Morphol 138(2):169–185. https://doi.org/10.1002/jmor.1051380204
Jordan RK (1976) Development of sheep thymus in relation to in utero thymectomy experiments. Eur J Immunol 6(10):693–698. https://doi.org/10.1002/eji.1830061007
Khaksary-Mahabady M, Khazaeel K, Pour-mahdi Borujeni M, Yazdanjoo B (2018) Morphometric development of sheep (Ovis aries) lymph nodes in fetal period. Vet Res Forum 9(2):121–128. https://doi.org/10.30466/VRF.2018.30833
Maddox JF, Mackay CR, Brandon MR (1987) Ontogeny of ovine lymphocytes. II. An immu-nohistological study on the development of T lymphocytes in the sheep fetal spleen. Immunology 62(1):107–112
Agerholm JS, Hewicker-Trautwein M, Peperkamp K, Windsor PA (2015) Virus-induced congenital malformations in cattle. Acta Vet Scand 57:54. https://doi.org/10. 1186/s13028-015-0145-8