A Review of Border Disease Virus Infection in Ruminants: Molecular Characterization, Pathogenesis, Diagnosis and Control

Abstract

This review includes the recent studies of virological diagnosis, agent characterization, pathogenesis, and control of Border Disease BD infection caused by viruses in the genus Pestivirus. BD virus BDV , closely related to Bovine Viral Diarrhea Virus and Classical Swine Fever Virus, is classified in the genus Pestivirus of the family Flaviviridae. Based on phylogenetic analysis, ovine pestiviruses are segregated at least into six clusters, using the 5’-NTR and Npro gene region sequences. Phylogenetic analysis of BDV isolated from Turkey isolates reveal that the virus form a distinct cluster as BDV-7 and BDV-3, which isolates are being more closely related to CSFVs than to the known BDV-3 subgenotype that contains pig-derived Pestivirus obtained from sheep. BD infection is characterized by abortions, congenital abnormalities, and stillbirths, the birth of small weak lambs and persistent infections of the offspring in small ruminant flocks. On postmortem examination, porencephaly, hydranencephaly, hydrocephalus, and cerebellar hypoplasia are most marked lesions in aborted fetuses and neonatal animals. The gross and histologic lesions are generally consistent with bluetongue, akabane, and enzootic ataxia of small ruminants. Therefore, labeling the Pestivirus viral antigen and genome is essential to clarify the differential diagnosis. BD is reported worldwide and leads to significant losses in the ruminant population. In addition, the infected small ruminants play a key role in the spread of Pestivirus infections among ruminant population by interspecies transmission. The great importance of these reservoirs should not be forgotten in Pestivirus control programs.

Keywords

• Border disease,Pestivirus,Molecular characterization,Control

Ruminantlarda Border Hastalığı Üzerine Bir Derleme: Moleküler Tiplendirme, Patogenezis, Tanı ve Kontrol

Öz

Bu derleme; küçük ruminant sürülerinde abortlar, kongenital anomalili yavrular ve yaşama gücü zayıf yavruların doğumu ile karakterize olan ve pestivirusların neden olduğu Border Hastalığı BD hakkında son yıllarda gerçekleştirilen virolojik tanı, etken karakterizasyonu, patogenezis ve enfeksiyonun kontrolüne yönelik çalışmaları içermektedir. Sığır virus diare virus ve klasik domuz vebası virusu ile çok yakınlığı olan BD virus BDV , Flaviviridae ailesinin Pestivirus genusunda yer alır. 5’-NTR ve Npro gen bölgesini hedef alan filogenetik analizler koyun pestiviruslarını en az 6 alt grupta sınıflandırmaktadır. Türkiye küçük ruminantlardan elde edilen izolatların filogenetik analizlerinin sonuçları; BDV’ların, bilinen BDV-3 subgenomundan farklı olarak, BDV-3 ve BDV-7 olduğunu ortaya koymuştur. Her iki izolat genetik olarak aynı genustan klasik domuz vebası ile çok yakın ilişkili bulunmuştur. BD atıklar, konjenital anomaliler, yaşama gücü zayıf ve persiste enfekte zayıf yavru doğumları ile karakterizedir. Nekropsi muayenesinde, atık ve neonatal küçük ruminantlarda porensefali, hidranensefali, hidrosefalus ve serebellar hipoplazi en çok dikkati çeken bulgulardır. Makroskopik ve histopatolojik değişiklikler genellikle mavidil, akabane ve enzootik ataksi ile karışır. Ayırıcı tanı için, virolojik ve patolojik incelemelerde pestivirus antijen ve genomunu belirlemek gerekir. BD küçük ruminantlarda dünya genelinde yaygın bir hastalıktır ve önemli ekonomik kayıplara neden olur. Ayrıca, enfekte küçük ruminantlar, türler arası nakil nedeniyle, ruminant populasyonları arasında pestivirus enfeksiyonlarının yayılımında anahtar bir rol oynarlar. Pestivirus kontrol programlarında bu rezervuarların büyük önemi unutulmamalıdır.

Anahtar Kelimeler

• Border hastalığı,Pestivirus,Moleküler tiplendirme,Kontrol

Kaynakça

1. Arnal M, Fernandez-de-Luco D, Riba L, Maley M, Gilray J, Willoughby K, Vilcek S, Nettleton PF (2004). A novel pestivirus associated with deaths in Pyrenean chamois (Rupi- capra pyrenaica pyrenaica). Journal of General Virology, 85, 3653-3657.
2. Ataseven VS, Ataseven L, Tan T, Babür C, Oğuzoğlu TÇ (2006). Seropositivity of agents causing abortion in local goat breeds in Eastern and South-eastern Anatolia, Turkey. Revue de Médicine Véterinaire, 157, 11, 545-550.
3. Baigent SJ, Zhang G, Fray MD, Flick-Smith H, Goodbourn S and McCauley JW (2002). Inhibition of beta interferon transcription by noncytopathogenic bovine viral diarrhea virus is through an interferon regulatory factor-3-dependent mechanism. Journal of Virology, 76, 8979-8988.
4. Bauhofer O, Summerfield A, Sakoda Y, Tratschin JD, Hofmann MA and Ruggli N (2007). Classical swine fever virus Npro interacts with interferon regulatory factor 3 and induces its proteasomal degradation. Journal of Virology, 81, 3087-3096.
5. Becher P, Orlich M, Shannon AD, Horner G, König M, Thiel H-J (1997). Phylogenetic analysis of pestiviruses from domestic and wild ruminants. Journal of General Virology, 78, 1357-1366.
6. Becher P, Avalos Ramirez R, Orlich M, Cedillo Rosales S, König M, Schweizer M, Stalder H, Schirrmeier H and Thiel H-J (2003). Genetic and antigenic characterization of novel pestivirus genotypes: implications for classification. Virology, 311, 96-104.
7. Bendfeldt S, Ridpath JF, Neill JD (2007). Activation of cell signaling pathways is dependant on the biotype of bovine viral diarrhea viruses type 2. Virus Research, 126, 96-105.
8. Benedict CA, Norris PS, Ware CF (2002). To kill or be killed: viral evasion of apoptosis. Nature Immunology, 3,1013-1018.

9. Bielefeldt-Ohmann H, Tolnay AE, Reisenhauer CE, Hansen TR, Smirnova N, Van Campen H (2008). Transplacental infection with non- cytopathic bovine viral diarrhoea virus types 1b and 2: viral spread and molecular neuropathology. Journal of Comparative Pathology, 138, 72-85.
10. Bonjardim CA (2005). Interferons (IFNs) are key cytokines in both innate and adaptive antiviral immune responses and viruses counteract IFN action. Microbes and Infection, 7, 569-578.
11. Brun A, Lacoste F, Reynaud G, Kato F and Saint-Marc B (1993). Evaluation of the potency of an inactivated vaccine against border disease pestivirus infection in sheep. In: Proceedings of the Second Symposium on Pestiviruses, Edwards S., ed. Fondation Marcel Merieux, Annecy, France, 1–3 October 1992, 257-259.
12. Bruschke CJ, Hulst MM, Moormann RJ, van Rijn PA, van Oirschot JT (1997). Glycoprotein Erns of pestiviruses induces apoptosis in lymphocytes of several species. Journal of Virology, 71, 6692-6696.
13. Grummer B, Moennig V, Greiser-Wilke I (1998). Cytopathogenic bovine viral diarrhea viruses induce apoptosis in bovine cell cultures. Deutsche Tierärztliche Wochenschrift, 105, 29-31.
14. Grummer B, Bendfeldt S, Wagner B, Greiser-Wilke I (2002). Induction of the intrinsic apoptotic pathway in cells infected with cytopathic bovine viral diarrhoea virus. Virus Research, 90, 143-153.
15. Harasawa R and Giangaspero M (1998). A novel method for pestivirus genotyping based on palindromic nucleotide substitutions in the 5’-untranslated region. Journal of Virological Methods, 70, 225-230.
16. Hay S and Kannourakis G (2002). A time to kill: viral manipulation of the cell death program. Journal of General Virology, 83, 1547-1564.
17. Hewicker-Trautwein M and Trautwein G (1994). Porencephaly, hydranencephaly and leucoencephalopathy in ovine fetuses following transplacental infection with ovine virus diarrhoea virus: distribution of viral antigen and characterization of cellular response. Acta Neuropathologica, 87, 385-397.
18. Hewicker-Trautwein M (1994). Pestivirus-induzierte alterationen im zentralnervensystem von wiederkäuern. Tierärztliche Praxis, 22, 516-23.
19. Hilbe M, Camenisch U, Braun U, Peterhans E, Stalder H, Zlinszky K, Ehrensperger F (2009). Mucosal lesions in a sheep infected with the Border Disease Virus (BDV). Schweizer Archives Tierheilkunde, 151, 391-396.
20. Hilton L, Moganeradj K, Zhang G, Chen YH, Randall RE, McCauley JW and Goodbourn S (2006). The NPro product of bovine viral diarrhea virus inhibits DNA binding by interferon regulatory factor 3 and targets it for proteasomal degradation. Journal of Virology, 80, 11723-11732.
21. Hughes LE, Kershaw GF, Shaw IG (1959). Border Disease. An undescribed disease of sheep. The Veterinary Record, 71, 313-317.
22. Julia S, Craig MI, Jimenez LS, Pinto GB, Weber EL (2009). First report of BVDV circulation in sheep in Argentina. Preventive Veterinary Medicine, 90, 274-277.
23. Kautto AH, Alenius S, Mossing T, Becher P, Belak S, Larska M (2012). Pestivirus and alphaherpesvirus infections in Swedish reindeer (Rangifer tarandus tarandus L.). Veterinary Microbiology, 156, 64- 71.
24. Kawai T and Akira S (2006). Innate immune recognition of viral infection. Nature of Immunology, 7, 131-137.
25. Krametter-Froetscher R, Kohler H, Benetka V, Moestl K, Golja F, Vilcek S, Baumgartner W (2007). Influence of communal alpine pasturing on the spread of pestiviruses among sheep and goats in Austria: first identification of border disease virus in Austria. Zoonoses Public Health, 54, 209-213.
26. Kul O, Kabakci N, Ozkul A, Kalender H, Atmaca HT (2008). Concurrent peste des petits ruminants virus and pestivirus infection in stillborn twin lambs. Veterinary Pathology, 45, 191-196.
27. Lambot M, Hanon E, Lecomte C, Hamers C, Letesson J-J,Pastoret P-P (1998). Bovine viral diarrhoea virus induces apoptosis in blood mononuclear cells by a mechanism largely dependent on monocytes. Journal of General Virology, 79, 1745-1749.
28. Lamm CG, Broaddus CC, Holyoak GR (2009). Distribution of bovine viral diarrhea virus antigen in aborted fetal and neonatal goats by immunohistochemistry. Veterinary Pathology, 46, 54-58.
29. Lindenbach BD, Thiel HJ and Rice CM (2007). Flaviviridae: the viruses and their replication. In: Fields Virology (Knipe, DM & Howley, PM, eds), Lippincott-Raven Publishers, Philadelphia, PA, vol. 1, pp. 1101- 1152.
30. Liu L, Xia H, Wahlberg N, Belák S, Baule C (2009). Phylogeny, classification and evolutionary insights into pestiviruses. Virology, 385, 351–357.
31. Löken T, Krogsurud J, Bjerkas I (1991). Outbreaks of Border disease in goats induced by a pestivirus-contaminated orf vaccine with virus transmission to sheep and cattle. Journal of Comparative Pathology, 104, 195-209.
32. Marco I, Rosell R, Cabezón O, Mentaberre G, Casas E, Velarde R and Lavín S (2009). Border disease virus among chamois, Spain. Emerging Infectious Disease, 15, 448-451.
33. Martin C, Letellier C, Caij B, Gauthier D, Jean N, Shaffii A, Saegerman C (2011). Epidemiology of Pestivirus infection in wild ungulates of the French South Alps. Veterinary Microbiology, 147, 320-328.
34. Meyers G, Thiel H-J (1996). Molecular characterization of pestiviruses. Advences Virus Research, 47, 53-118.
35. Monies RJ, Paton DJ, Vilcek S (2004). Mucosal disease-like lesions in sheep infected with Border disease virus. The Veterinary Record, 155, 765-769.
36. Neill JD (2005). Interactions of virus and host bovine viral diarrhea virus diagnosis, management, and control. Sagar M. Goyal and Julia F. Ridpath (Eds.). Blackwell Publishing, Ames, Iowa, pp.177-194.
37. Nettleton PF (2000). Border disease. In: Diseases of sheep. Blackwell Science, Oxford UK, pp. 95-102.
38. Oguzoglu TC, Floegel-Niesmann G, Frey H-R, Moennig V (2001). Zur differentialdiagnostik klassische schweinepest/border disease: seroepidemiologische untersuchung einer pestivirusinfektion auf einem schaf- und schweinehaltenden betrieb. Deutsche Tierärztliche Wochenschrift, 108, 5, 210-213.
39. Oguzoglu TC (2002). Serologische differential diagnostik der klassischen schweinepest (ksp) mit border disease (BD). Inaugural Dissertation. Hannover, Germany.
40. Oguzoglu T C (2008). Sınır hastalığı (Border Disease). Ankara Üniversitesi Veteriner Fakültesi Dergisi, 55, 69-74.
41. Oguzoglu TC, Tan MT, Toplu N, Demir AB, Bilge-Dagalp S, Karaoglu T, Ozkul A, Alkan F, Haas L, Greiser-Wilke I (2009). Border disease virus (BDV) infections of small ruminants in Turkey: a new BDV subgroup. Veterinary Microbiology, 135, 374-379.
42. OIE (2009). Manual of diagnostic tests and vaccines for terrestrial animals. Chapter 2.7.1 Border Disease p: 963-967.
43. Rasmussen TB, Reimann I, Uttenthal A, Leifer I, Depner K, Schirrmeier H, Beer M (2010). Generation of recombinant pestiviruses using a full-genome amplification strategy. Veterinary Microbiology, 142, 13-17.
44. Ruggli N, Bird BH, Liu L, Bauhofer O, Tratschin JD and Hofmann MA (2005). N(pro) of classical swine fever virus is an antagonist of double-stranded RNA-mediated apoptosis and IFN-alpha/beta induction. Virology, 340, 265-276.
45. Seago J, Hilton L, Reid E, Doceul V, Jeyatheesan J, Moganeradj K, McCauley J, Charleston B, Goodbourn S (2007). The Npro product of classical swine fever virus and bovine viral diarrhea virus uses a conserved mechanism to target interferon regulatory factor-3. Journal of General Virology, 88, 3002-3006.
46. Schaller P, Vogt HR, Strasser M, Nettleton PF, Peterhans E, Zanoni R (2000). Seroprevalence of maedi-visna and border disease in Switzerland. Schweizer Archives Tierheilkunde, 142, 145-153.
47. Schirrmeier H, Depner K, Strebelow G, Buettner M (1999). Border disease antibodies in German pig herds. In: Report of the Annual Meeting of National Swine Fever Laboratories, Ploufragan, 1999. Commission of the European Community, Brussels, pp. 60–62.
48. Schweizer M and Peterhans E (2001). Noncytopathic bovine viral diarrhea virus inhibits double-stranded RNA-induced apoptosis and interferon synthesis. Journal of Virology, 75, 4692-4698.
49. Schweizer M, Matzener P, Pfaffen G, Stalder H, Peterhans E (2006). “Self” and “Nonself” manipulation of interferon defense during persistent infection: bovine viral diarrhea virus resists alpha/beta interferon without blocking antiviral activity against unrelated viruses replicating in its host cells. Journal of Virology, 80, 6926- 6935.
50. Thabti F, Letellier C, Hammami S, Pepin M, Ribiere M, Mesplede A, Kerkhofs P, Russo P, (2005). Detection of a novel border disease virus subgroup in Tunisian sheep. Archives of Virology, 150, 215- 229.
51. Thiel H-J, Collett MS, Gould EA, Heinz FX, Houghton M, Meyers G, Purcell RH and Rice CM (2005). Flaviviridae. In: virus taxonomy. Eighth report of the international committee on taxonomy of viruses, Fauquet C.M., Mayo M.A., Maniloff J., Desselberger U. & Ball L.A., eds. Elsevier Academic Press, pp. 981-998.
52. Toplu N, Oğuzoğlu TC, Epikmen ET and Aydoğan A (2010). Neuropathologic study of border disease virus in naturally infected fetal and neonatal small ruminants and its association with apoptosis. Veterinary Pathology, 48, 576-583.
53. Toplu N, Oguzoglu TC and Albayrak H (2012). Dual infection of fetal and neonatal small ruminants with border disease virus and peste des petits ruminants virus (pprv): neuronal tropism of pprv as a novel finding. Journal of Comparative Pathology, 146, 289-297.
54. Vassilev VB, Donis RO (2000). Bovine viral diarrhea virus induced apoptosis correlates with increased intracellular viral RNA accumulation. Virus Research, 69, 95-107.
55. Vilcek S, Paton DJ (2000). A RT-PCR assay for the rapid recognition of Border disease virus. Veterinary Research, 31, 437-445.
56. Wohlsein P, Trautwein G, Depner KR, Hübschle OJ, Liess B (1992). Pathomorphological and immunohistological findings in progeny of goats experimentally infected with pestiviruses. Zentralblatt für Veterinärmedizin B, 39, 1-9.
57. Zhang G, Aldridge S, Clarke MC, Mc Cauley JW (1996). Cell death induced by cytopathic bovine viral diarrhoea virus is mediated by apoptosis. Journal of General Virology, 77, 1677-1681.