Detection of genetic material of causative agents of animal viral diseases in blood-sucking dipterans from the Tyumen Region

The purpose of the research is to test blood-sucking dipterans collected in the Tyumen Region for genetic material of viruses that cause dangerous diseases in live-stock animals.
Materials and methods. From May to October 2021, blood-sucking insects of the Diptera order whose species membership was established by tabular keys were collected on pastures and farms in ten Tyumen Region districts. In 60 samples formed from the captured insects according to the taxonomic affiliation and the period and place of collection, the presence of genetic material of the leukemia provirus and the dermatitis nodularis virus of cattle (bovine) and the African swine fever virus was evaluated by polymerase chain reaction (PCR) in real time.
Results and discussion. Adult insects collected for the PCR analysis were blood-sucking flies (family Muscidae, genus Stomoxys), mosquitoes (family Culicidae, genus Aedes), midges (family Simuliidae, genera Byssodon and Schoenbaueria), horseflies (family Tabanidae, genera Hybomitra, Tabanus and Haematopota), and biting midges (family Ceratopogonidae, genus Culicoides). As a result of the PCR testing of the samples for the bovine leukemia provirus DNA, 1 out of 13 samples of Stomoxys spp. (7.7%) and 1 of 13 samples of Hybomitra spp. (7.7%) were positive. The bovine leukemia provirus DNA detected in blood-sucking insects indicates the presence of this pathogen in the insect collection area as well as their possible involvement in its spread. Further research is needed on the Stomoxys spp. and Hybomitra spp. vector competence in vivo, considering natural and climatic features of the Tyumen Region.

1. Aronova E. V., Salnikov N. I., Tsibanov S. G., Lunitsin A. V., Saryglar L. K., Yanjieva D. V., Murueva G. B. A study in the Republic Buryatia midges of genus Culicoides as potential vectors of agents transmissible animal diseases. Veterinariya = Veterinary Medicine. 2015; 7: 8-11 (In Russ.).

2. Burova O. A., Blokhin A. A., Zakharova O. I., Liskova E. A., Yashin I. V., Gladkova N. A. Vectors of vector-borne viral diseases of animals. Agrarnaya nauka Evro-Severo-Vostoka = Agricultural Science Euro-North-East. 2018; 5 (66): 4-17. (In Russ.)

3. Vlasov M. E., Sereda A. D., Balyshev V. M. African swine virus maintenance in stable flies (Stomoxys calcitrans) and blowflies (Calliphoridae). Veterinariya = Veterinary Medicine. 2019; 8: 22-25. (In Russ.) doi: 10.30896/0042-4846.2019.22.8.22-25

4. Domatskiy V. N., Fedorova O. A., Siben A. N Epizootological and epidemiological place of sanguivorous dipterans in a climate of the Arctic (Review). Rossiyskiy parazitologicheskiy zhurnal = Russian Journal of Parasitology. 2018; 12 (4): 73-76. (In Russ.) doi: 10.31016/1998-8435-2018-12-4-73-76

5. Donnik I. M., Gulyukin M. I., Busol V. A., Kovalenko L. V., Kovalenko A. M. Bovine leukemia virus infection – diagnostics, eradication, and anthropozoonotic potential (Background) (Review). Sel'skokhozyaystvennaya biologiya = Agricultural Вiology. 2021; 56 (2): 230-244. (In Russ.)

6. Zaberezhny A. D., Aliper T. I., Grebennikova T. V., Verkhovsky O. A., Sanchez-Vizcaino J. M., Mur Lina, Nepoklonov E. A., Lvov D. K. African swine fever in Russian Federation. Voprosy virusologii = Problems of Virology. 2012; 57 (5): 4-10. (In Russ.)

7. Mishchenko V. A., Petrova O. N., Karaulov A. K., Mishchenko A. V. Bovine leukemia problem. Vladimir: FGBU «VNIIZZh», 2018; 38. (In Russ.)

8. Sprygin A. V., Fedorova O. A., Babin Yu. Yu., Kononov A. V., Karaulov A. K. Blood-sucking midges from the genus Culicoides (Diptera: Ceratopogonidae) act as filed vectors of human and animal diseases. Sel'skokhozyaystvennaya biologiya = Agricultural Вiology. 2015; 50 (2): 183-197. (In Russ.)

9. Fedorova О. А., Novozenova V. S. Epizootic situation on transmissible animal diseases in the Tyumen region (2000-2020) Database registration certificate 2021620990, 05/18/2021. Application No. 2021620845 dated 04/27/2021. (In Russ.)

10. Chichkin A. N., Padilo L. P., Saltykov Yu. V., Podshibyakin D. V., Dresviannikova S. G., Dzhailidi G. A., Feodorova V. A. The study of insects of the order Diptera for the presence of the genetic material of the lumpy skin disease virus by a polymerase chain reaction. Veterinariya = Veterinary Medicine. 2020; 7: 24-31 (In Russ.)

11. Baldacchino F., Desquesnes M., Mihok S., Foil L. D., Duvallet G., Jittapalapong S. Tabanids: Neglected subjects of research, but important vectors of disease agents! Infection, Genetics and Evolution. 2014; 28. 596-615. https://doi.org/10.1016/j.meegid.2014.03.029

12. Barez P. Y., de Brogniez A., Carpentier A., Gazon H., Gillet N., Gutiérrez G., Hamaidia M., Jacques J. R., Perike S., Neelature Sriramareddy S., Renotte N., Staumont B., Reichert M., Trono K., Willems L. Recent Advances in BLV Research. Viruses. 2015; 7 (11): 6080–6088. https://doi.org/10.3390/v7112929

13. Buxton B. A., Hinkle N. C., Schultz R. D. Role of insects in the transmission of bovine leukosis virus: potential for transmission by stable flies, horn flies, and tabanids. Amer. J. Vet. Res. 1985; 46. 123–126.

14. Corredor-Figueroa A. P., Olaya-Galán N. N., Velandia-Álvarez S., Muñoz M., Salas-Cárdenas S. P., Ibáñez-Pinilla M., Patarroyo M. A., Gutiérrez M. F. Co-Circulation of Bovine Leukemia Virus Haplotypes among Humans, Animals, and Food Products: New Insights of Its Zoonotic Potential. Int. J. Environ. Res. Public Health. 2021; 18 (9): 4883. https://doi.org/10.3390/ijerph18094883

15. Dogan F., Bilge Dagalp S., Dik B., Farzani T. A., Alkan F. Detection of genotype 1 bovine leukemia virus from a C. schultzei pool: Do Culicoides spp. have a role on the transmission of bovine leukemia virus? Infect. Genet. Evol. 2020; 85: 104469. doi: 10.1016/j.meegid.2020.104469

16. Fila M., Woźniakowski G. African Swine Fever Virus - The Possible Role of Flies and Other Insects in Virus Transmission. J. Vet. Res. 2020; 64 (1): 1-7. doi: 10.2478/jvetres-2020-0001

17. Foil L. D., Seger C. L., French D. D., Issel C. J., McManus J. M., Ohrberg C. L., Ramsey R. T. Mechanical Transmission of Bovine Leukemia Virus by Horse Flies (Diptera: Tabanidae). Journal of Medical Entomology. 1988; 25 (5): 374–376. https:// doi.org/10.1093/jmedent/25.5.374

18. Herm R., Kirik H., Vilem A., Zani L., Forth J. H., Müller A., Michelitsch A., Wernike K., Werner D., Tummeleht L., Kampen H., Viltrop A. No evidence for African swine fever virus DNA in haematophagous arthropods collected at wild boar baiting sites in Estonia. Transbound Emerg Dis. 2021; 68 (5): 2696-2702. https:// doi.org/10.1111/tbed.14013

19. Inagaki H., Konnai S., Kaburagi H., Murota H., Takabatake N., Watari K., Okagawa T., Maekawa N., Murata S., Ohashi K. Vector transmission of bovine leukemia virus during summer season in Northern Hokkaido. Japan. J. Vet. Res. 2019; 67 (3): 235-239.

20. Inagaki Y., Kobayashi T., Suda Y., Kusama K., Imakawa K. Genetic variation in Japanese Holstein cattle for EBL development. BMC Vet. Res. 2020; 16. 407. https://doi.org/10.1186/s12917-020-02625-8

21. Issimov A., Kutumbetov L., Orynbayev M. B., Khairullin B., Myrzakhmetova B., Sultankulova K., White P. J. Mechanical Transmission of Lumpy Skin Disease Virus by Stomoxys Spp (Stomoxys Calsitrans, Stomoxys Sitiens, Stomoxys Indica), Diptera: Muscidae. Animals. 2020; 10 (3): 477. https://doi.org/10.3390/ani10030477

22. Kahana-Sutin E., Klement E., Lensky I., Gottlieb Y. High relative abundance of the stable fly Stomoxys calcitrans is associated with lumpy skin disease outbreaks in Israeli dairy farms. Medical and Veterinary Entomology. 2017; 31 (2): 150-160. https://doi.org/10.1111/mve.12217

23. Kohara J., Takeuchi M., Hirano Y., Sakurai Y., Takahashi T. Vector control efficacy of fly nets on preventing bovine leukemia virus transmission. J. Vet. Med. Sci. 2018; 80. 1524-1527. https://doi.org/10.1292/jvms.18-0199

24. Kuczewski A., Orsel K., Barkema H. W., Mason S., Erskine R., van der Meer F. Invited review: Bovine leukemia virus – Transmission, control, and eradication. Journal of Dairy Science. 2021; 104 (6): 6358-6375. https://doi.org/10.3168/jds.2020-18925

25. Limon G., Gamawa A. A., Ahmed A. I., Lyons N. A., Beard P. M. Epidemiological Characteristics and Economic Impact of Lumpy Skin Disease, Sheeppox and Goatpox Among Subsistence Farmers in Northeast Nigeria. Front. Vet. Sci. 2020; 7: 8. doi: 10.3389/fvets.2020.00008

26. Makhahlela N. B., Liebenberg D., van Hamburg H., Taioe M. O., Thankgod O., Ramatla T., Thekisoe O. M. M. Detection of pathogens of veterinary importance harboured by Stomoxys calcitrans in South African feedlots. Scientific African. 2022; 15. e01112. https://doi.org/10.1016/j.sciaf.2022.e01112

27. Mat B., Arikan M. S., Akin A. C., Çevrimli M. B., Yonar H., Tekindal M. A. Determination of production losses related to lumpy skin disease among cattle in Turkey and analysis using SEIR epidemic model. BMC Vet. Res. 2021; 17: 300. https://doi.org/10.1186/s12917-021-02983-x

28. Mellor P. S., Kitching R. P., Wilkinson P. J. Mechanical transmission of capripox virus and African swine fever virus by Stomoxys calcitrans. Research in Veterinary Science. 1987; 43. 109–112. https://doi.org/10.1016/S0034-5288(18)30753-7

29. Nakada S., Fujimoto Y., Kohara J., Adachi Y., Makita K. Estimation of economic loss by carcass weight reduction of Japanese dairy cows due to infection with bovine leukemia virus. Preventive Veterinary Medicine. 2022; 198: 105528. https://doi.org/10.1016/j.prevetmed.2021.105528

30. Nekoei S., Hafshejani T. T., Doosti A., Khamesipour F. Molecular detection of Bovine leukemia virus in peripheral blood of Iranian cattle, camel and sheep. Pol. J. Vet. Sci. 2015; 18. 703–707.

31. Ochiai C., Katagiri Y., Kobayashi S., Naitoh I., Yoneyama S., Tomita K., Dongze L., Hikono H., Murakami K. Development of a microchip electrophoresis-based, high-throughput PCR-RFLP method to type Tax 233 variants of bovine leukemia virus in Japan. Arch. Virol. 2020; 165. 2961–2966. https://doi.org/10.1007/s00705-020-04842-w

32. Olesen A. S., Hansen M. F., Rasmussen T. B., Belsham G. J., Bødker R., Bøtner A. Survival and localization of African swine fever virus in stable flies (Stomoxys calcitrans) after feeding on viremic blood using a membrane feeder. Veterinary Microbiology. 2018; 222. 25-29. https://doi.org/10.1016/j.vetmic.2018.06.010

33. Ooshiro M., Konnai S., Katagiri Y., Afuso M., Arakaki N., Tsuha O., Murata S., Ohashi K. Horizontal transmission of bovine leukemia virus from lymphocytotic cattle, and beneficial effects of insect vector control. Vet. Rec. 2013; 173 (21): 527. doi: 10.1136/vr.101833.

34. Panei C. J., Larsen A. E., Fuentealba N. A., Metz G. E., Echeverría M. G., Galosi C. M., Valera A. R. Study of horn flies as vectors of bovine leukemia virus. Open Vet. J. 2019; 9 (1): 33-37. doi: 10.4314/ovj.v9i1.6.

35. Saegerman C., Bertagnoli S., Meyer G., Ganière J. P., Caufour P., De Clercq K., Jacquiet P., Fournié G., Hautefeuille C., Etore F., Casal J. Risk of introduction of lumpy skin disease in France by the import of vectors in animal trucks. PLOS ONE. 2018; 13 (6): e0198506. https://doi.org/10.1371/journal.pone.0198506

36. Selim A., Marawan M. A., Ali A. F., Manaa E., AbouelGhaut H. A. Seroprevalence of bovine leukemia virus in cattle, buffalo, and camel in Egypt. Trop. Anim. Health Prod. 2020; 52. 1207–1210.

37. Sohier C., Haegeman A., Mostin L., De Leeuw I., Campe W. V., De Vleeschauwer A., Tuppurainen E., van den Berg T., De Regge N., De Clercq K. Experimental evidence of mechanical lumpy skin disease virus transmission by Stomoxys calcitrans biting flies and Haematopota spp. horseflies. Scientific reports. 2019; 9 (1): 20076. https://doi.org/10.1038/s41598-019-56605-6

38. Sprygin A., Pestova Y., Wallace D. B., Tuppurainen E., Kononov A. V. Transmission of lumpy skin disease virus: A short review. Virus Res. 2019; 269: 197637. https://doi.org/10.1016/j.virusres.2019.05.015

39. Turčinavičienė J., Petrašiūnas A., Bernotienė R., Masiulis M., Jonušaitis V. The contribution of insects to African swine fever virus dispersal: data from domestic pig farms in Lithuania. Med. Vet. Entomol. 2021; 35 (3): 484-489. doi: 10.1111/mve.12499.

40. Tzeng H. Y., Wu H. H., Ting L. J., Chang N. T., Chou Y. C., Tu W. C. Monitoring Taiwanese bovine arboviruses and non-arboviruses using a vectorbased approach. Med. Vet. Entomol. 2019; 33 (2): 195-202. doi: 10.1111/mve.12345.

41. You S., Liu T., Zhang M., Zhao X., Dong Y., Wu B., Wang Y., Li J., Wei X., Shi B. African swine fever outbreaks in China led to gross domestic product and economic losses. Nat. Food. 2021; 2. 802–808. https://doi.org/10.1038/s43016-021-00362-1