Investigación molecular de los virus más importantes que causan abortos en pequeños rumiantes: la importancia del virus akabane

Molecular investigation of most important viruses causing abortion in small ruminants: the importance of akabane virus

Objective. This study was aimed to investigate the presence of pestivirus, schmallenberg virus (SBV), akabane virus (AKAV), and determined the seasonal distribution in small ruminant abortion cases Materials and Methods. A total of 164 small ruminant aborted fetuses (39 goats and 125 sheep) were investigated in West Turkey between the years of 2015 and 2019. While the SBV and pestivirus were examined with real-time RT-PCR, the AKAV was examined with nested-PCR. Results. In this study, while four sheep (2.3%) were found to be pestivirus positive, nine sheep and one goat (5.9%) were found to be AKAV positive. SBV was detected in none of the animals. According to the results of the studies carried out, AKAV, a vector-borne virus, was detected more than other viruses in sheep and goat abortions in West Turkey. A positive akabane virus sample detected in sheep fetuses was sequenced based on the partial S segment. This sample showed 99-100% similarity to the Adana-15, Aksu-1, and Aksu-2 isolates previously detected in Southern Turkey. Phylogenetic analysis showed that the sequenced isolate in this study was clustered within genogroup Ib. Another important piece of data revealed in this study was the determination of the seasonal distribution of sheep and goat abortions. Abortion cases which started to increase in November reached a peak in February and declined till August. Conclusions. This is the first study in the Aegean Region (including seven provinces) in which three important viral agents were simultaneously investigated in small ruminant aborted fetuses.

1. Adu-Addai B, Koney EB, Addo P, Kaneene J, Mackenzie C, Agnew DW. Importance of infectious bovine reproductive diseases: an example from Ghana. Vet Rec. 2012; 17:47-48. https://dx.doi.org/10.1136/vr.100789
2. Borel N, Frey CF, Gottstein B, Hilbe M, Pospischil A, Franzoso FD, et al. Laboratory diagnosis of ruminant abortion in Europe. Vet J. 2014; 200(2):218-29. https://dx.doi.org/10.1016/j.tvjl.2014.03.015.
3. Lievaart-Peterson K, Luttikholt S, Peperkamp K, Van den Brom R, Vellema P. Schmallenberg disease in sheep or goats: Past, present and future. Vet Microbiol. 2015; 181:147-153. https://dx.doi.org/10.1016/j.vetmic.2015.08.005
4. Sozzi E, Lavazza A, Gaffuri A, Bencetti FC, Prosperi A, Lelli D, et al. Isolation and Full-Length Sequence Analysis of a Pestivirus from Aborted Lamb Fetuses in Italy. Viruses. 2019; 13:11(8):744. https://dx.doi.org/10.3390/v11080744
5. Sevik M. Genomic characterization of pestiviruses isolated from bovine, ovine and caprine foetuses in Turkey: A potentially new genotype of Pestivirus I species. Transbound Emerg Dis. 2020; https://dx.doi.org/10.1111/tbed.13691
6. Hoffmann B, Scheuch M, Hoper D, Jungblut R, Holsteg M, Schirrmeier H, et al. Novel Orthobunyavirus in cattle, Europe, 2011. Emerg Infect Dis. 2016; 18:469–472. https://dx.doi.org/10.3201/eid1803.111905
7. Maclachlan NJ, Dubovi EJ. Bunyaviridae. In: Fenner’s Veterinary Virology. Maclachlan NJ, Dubovi EJ. (editors) 5th edition. San Diego: Elsevier; 2016.
8. Brenner J, Rotenberg D, Jaakobi S, Stram Y, Guini-Rubinstein M, Menasherov S, et al. What can Akabane disease teach us about other arboviral diseases. Vet Ital. 2016; 52(3-4):353-362. https://dx.doi.org/10.12834/VetIt.547.2587.2
9. Tarlinton R, Daly J, Dunham S, Kydd J. The challenge of Schmallenberg virus emergence in Europe. Vet J. 2012; 194:10–1811. https://dx.doi.org/10.1016/j.tvjl.2012.08.017
10. Kirkland PD. Akabane virus infection. Rev Sci Tech. 2015; 34:403-410. https://dx.doi.org/10.20506/rst.34.2.2366/
11. Esteves F, Mesquita JR, Nóbrega C, Santos C, Monteiro A, Cruz R, et al. Epidemiology and Emergence of Schmallenberg Virus Part 1: Origin, Transmission and Differential Diagnosis. [Online]. London: IntechOpen; 2016. https://dx.doi.org/10.5772/64741
12. Schweizer M, Peterhans E. Pestiviruses. Annu Rev Anim Biosci. 2012; 2:141–163. https://dx.doi.org/10.1146/annurev-animal-022513-114209
13. Hofmann B, Depner K, Schirrmeier H, Beer M. A universal heterologous internal control system for duplex real-time RT-PCR assays used in a detection system for pestiviruses. J Virol Methods. 2006; 136:200–209. https://dx.doi.org/10.1016/j.jviromet.2006.05.020
14. Bilk S, Schulze C, Fischer M, Beer M, Hlinak A, Hoffmann B. Organ distribution of Schmallenberg virus RNA in malformed newborns. Vet Microbiol. 2012; 14:159(1-2):236-238. https://dx.doi.org/10.1016/j.vetmic.2012.03.035
15. Akashi H, Onuma S, Nagano H, Ohta M, Fukutomi T. Detection and differentiation of Aino and Akabane Simbu serogroup bunyaviruses by nested polymerase chain reaction. Arch Virol. 1999; 144:2101–2109. https://dx.doi.org/10.1007/s007050050625
16. Sevik M. A molecular and serological survey on akabane virus infection in small ruminants in the Mediterranean Region of Turkey. Small Rumin Res. 2017; 156:1-156. https://dx.doi.org/10.1016/j.smallrumres.2017.07.012
17. Oguzoglu TC, Toplu N, Koc BT, Dogan F, Epikmen ET, Ipek E, et al. First molecular detection and characterization of Akabane virus in small ruminants in Turkey. Arch Virol. 2015; 160:2623-2627. https://dx.doi.org/10.1007/s00705-015-2536-6
18. Dogan F. Epidemiologic investigation and possible vector identification of ruminant some arboviral infections (Akabane, Bluetongue and Schmallenberg) in Hatay province. [Ph.D Thesis]. Ankara University Institute of Health Sciences: Ankara, Turkey;. 2018. https://tez.yok.gov.tr/UlusalTezMerkezi/tezSorguSonucYeni.jsp
19. Brand SPC, Keeling MJ. The impact of temperature changes on vector-borne disease transmission: Culicoides midges and bluetongue virus. J R Soc Interface. 2017; 14:20160481. http://dx.doi.org/10.1098/rsif.2016.0481
20. Van Rijn F, Bulte E, Adekunle A. Social capital and agricultural innovation in SubSaharan Africa. Agric Syst. 2012; 108:112-122. https://dx.doi.org/10.1016/j.agsy.2011.12.003
21. Oguzoglu TC. Akabane virus infection in ruminants. Animal Health Prod and Hyg. 2018; 7:592–595. https://dergipark.org.tr/tr/download/article-file/1473870
22. Yilmaz H, Hoffman B, Turan N, Cizmecigil UY, Richt JA, Van der Poel WH. Detection and partial sequencing of Schmallenberg virus in cattle and sheep in Turkey. Vector Borne Zoonotic Dis. 2014; 14:233–235. https://dx.doi.org/10.1089/vbz.2013.1451
23. Tuncer-Goktuna P, Alpay G, Oner EB, Yesilbag K. The role of herpesviruses (BoHV-1 and BoHV-4) and pestiviruses (BVDV and BDV) in ruminant abortion cases in western Turkey. Trop Anim Health Prod. 2016; 48:1021–1027. https://dx.doi.org/10.1007/s11250-016-1050-5
24. Bulut H, Sozdutmaz I, Pestil Z, Abayli H, Sait A, Cevik A. High prevalence of bovine viral diarrhea virus-1 in sheep abortion samples with pestivirus infection in Turkey. Pak Vet J. 2018; 38:71-75. https://dx.doi.org/10.229261/pvj/2018.014
25. Albayrak H, Ozan E. The investigation of pestivirus and rift valley fever virus infections in aborted ruminant foetuses in the Blacksea Region in Turkey. Kafkas Univ Vet Fak Derg. 2012; 18:457-461. https://dx.doi.org/10.9775/kvfd.2011.5648
26. Hasircioglu S, Kale M, Acar A. Investigation of pestivirus infections in aborted sheep and goats in Burdur region. Kafkas Univ Vet Fak Derg. 2009; 15:163-167. http://vetdergikafkas.org/abstract.php?id=450
27. Gur S. A investigation of border disease virus in sheep in Western Turkey. Trop Anim Health Prod. 2009; 41:1409–1412. https://dx.doi.org/10.1007/s11250-009-9328-5
28. Albayrak H, Gumusova S, Ozan E, Yazici Z. Molecular detection of pestiviruses in aborted fetuses from provinces in northern Turkey. Trop Anim Health Prod. 2012; 44:677-680. https://dx.doi.org/10.1007/s11250-011-9955-5
29. Yang N, Cui X, Qian W, Yu S, Liu Q. Survey of nine abortifacient infectious agents in aborted bovine fetuses fromdairy farms in Beijing, China by PCR. Acta Vet Hung. 2012; 60:83-92. https://dx.doi.org/10.1556/AVet.2012.007
30. Morrell EL, Campero CM, Cantón GJ, Odeón AC, Moore DP, Odriozola E, et al. Current trends in bovine abortion in Argentina. Pesqui Vet Bras. 2019; 39:12-19. https://dx.doi.org/10.1590/1678-5150-pvb-5668.
31. Tuncer-Goktuna P, Yesilbag K. Evaluation of diagnostic methods for the detection of pestiviruses in clinical samples. Turkish J Vet Anim Sci. 2017; 41:175-179. https://dx.doi.org/10.3906/vet-1602-8
32. Sevik M. The role of pestiviruses (BDV and BVDV) in ruminant abortion cases in the Afyonkarahisar province. Kocatepe Veteriner Dergisi. 2018; 11:238-244. https://dx.doi.org/10.30607/kvj.418451
33. Albayrak H, Ozan E, Kadi H, Cavunt A, Tamer C. Seroprevalence of pestiviruses in some goat breeds in Samsun Province. Atatürk University J Vet Sci. 2016; 11:1-5. https://dx.doi.org/10.17094/avbd.21258
34. Alpay G, Oner EB, Yesilbag K. Seroepidemiology and molecular investigation of pestiviruses among sheep and goats in Northwest Anatolia. Turkish J Vet Anim Sci. 2018; 42:205-210. https://dx.doi.org/10.3906/vet-1711-83