INFECTIOUS SALMON ANEMIA

The aim of this work consists in the analysis of modern scientific conceptions about infectious salmon anemia (ISA) etiologically linked with ISAV (infectious salmon anemia virus) (Orthomyxoviridae, Isavirus). ISA is deadly disease of Salmonidae fishes.

Discussion. ISA began to extend actively among salmon breeding farms since the extremity of the XX century and poses nowadays serious threat of fishing industry as there are no not only anti-ISAV chemopreparates and effective vaccines, but also scientifically based ideas of ISAV ecology. In the offered review data on the discovery history, taxonomical status, virion morphology and genome structure as well as ecology of ISAV, clinical features, pathogenesis and laboratory diagnostics, actions in the epizootic foci for the prevention of further distribution and prophylaxis of ISA, arrangement for protection against salmon louses and utilized approaches to anti-ISAV vaccines development are discussed. There is very important that ISAV is capable to be transferred by salmon louses – pelagic crustaceans (Copepoda: Caligidae) that allows to classify ISAV as arbovirus ecological group which are transferred due to biological transmission by arthropods (copepods) to vertebrate animals (salmons). It is the only example known so far when representatives of Crustacea act as a vector for arboviruses.

Conclusion. Investigation of ISAV ecology turns into one of "touchstones" allowing to judge technological readiness of mankind to master resources of the World Ocean. 

1. Lvov D.K., ed. Rukovodstvo po virusologii. Virusy i virusnye infektcii cheloveka i zhyvotnyk [Handbook of Virology. Viruses and Viral Infections of Humans and Animals]. Moscow, Medical Information Agency, 2013, 1200 p. (In Russian)

2. Lvov D.K., Shchelkanov M.Yu., Alkhovsky S.V., Deryabin P.G. Zoonotic Viruses of Northern Eurasia. Taxonomy and Ecology. Elsevier Academic Press, 2015. 440 p.

3. Salama N.K., Murray A.G. A comparison of modelling approaches to assess the transmission of pathogens between Scottish fish farms: the role of hydrodynamics and site biomass. Prev. Vet. Med. 2013, vol. 108, no. 4, pp. 285–293. doi: 10.1016/j.prevetmed.2012.11.005.

4. Christiansen D.H., Østergaard P.S., Snow M., Dale O.B., Falk K. A low-pathogenic variant of infectious salmon anemia virus (ISAV-HPR0) is highly prevalent and causes a non-clinical transient infection in farmed Atlantic salmon (Salmo salar L.) in the Faroe Islands. J. Gen. Virol. 2011, vol. 92, pt. 4, pp. 909–918. doi: 10.1099/vir.0.027094-0.

5. Kibenge M.J., Iwamoto T., Wang Y., Morton A., Routledge R., Kibenge F.S. Discovery of variant infectious salmon anaemia virus (ISAV) of European genotype in British Columbia, Canada. Virol. J. 2016, vol. 13, no. 3. doi: 10.1186/s12985-015-0459-1.

6. Gustafson L., Ellis S., Bouchard D., Robinson T., Marenghi F., Warg J., Giray C. Estimating diagnostic test accuracy for infectious salmon anaemia virus in Maine, USA. J. Fish Dis. 2008, vol. 31, no. 2, pp. 117–125. doi: 10.1111/j.1365-2761.2007.00873.x.

7. Godoy M.G., Suarez R., Lazo E.S., Llegues K.O., Kibenge M.J., Wang Y., Kibenge F.S. Genetic analysis and comparative virulence of infectious salmon anemia virus (ISAV) types HPR7a and HPR7b from recent field outbreaks in Chile. Virol. J. 2014, vol. 11, no. 204. doi: 10.1186/s12985-014-0204-1.

8. Thorud K., Djupvik H.O. Infectious anaemia in Atlantic salmon (Salmo salar L.). Bull. Eur. Assoc. Fish Pathol. 1988, no. 8, pp. 109–111.

9. Vremennaya instruktciya po bor’be s zabolevaniem lososevykh ryb infektcionnoi anemiei [Temporary instruction for the protection against infectious anemia disease of samonids]. Approved 01.12.1970 by the head department of a veterinary medicine of the Ministry of Agriculture of the USSR. Moscow, Ministry of Agriculture Publ., 1970. 5 p.

10. Hastein T., Hill B.J., Winton J.R. Successful aquatic animal disease emergency programmes. Rev. Sci. Tech. 1999, vol. 18, pp. 214–227.

11. Hovland T., Nylund A., Watanabe K., Endresen C. Observation of infectious salmon anemia virus in Atlantic salmon, Salmo salar L.. J. Fish Dis. 1994, vol. 17, pp. 291–296.

12. Dannevig B.H., Falk K., Krogsrud J. Infectivity of internal tissues of Atlantic salmon, Salmo salar L., experimentally infected with the aetiological agent of infectious salmon anemia (ISA). J. Fish. Dis. 1994, vol. 17, pp. 613–622.

13. Dannevig B.H., Falk K., Press C.M. Propagation of infectious salmon anaemia (ISA) virus in cell culture. Vet. Res. 1995, vol. 26, no. 5–6, pp. 438–442.

14. Falk K., Dannevig B.H. Demonstration of infectious salmon anaemia (ISA) viral antigens in cell cultures and tissue sections. Vet. Res. 1995, vol. 26, no. 5–6, pp. 499–504.

15. Dannevig B.H., Falk K., Namork E. Isolation of the causal virus of infectious salmon anaemia (ISA) in a long-term cell line from Atlantic salmon head kidney. J. Gen. Virol. 1995, vol. 76, pt. 6, pp. 1353–1359. doi: 10.1099/0022-1317-76-6-1353.

16. Sommer A.I., Mennen S. Multiplication and haemadsorbing activity of infectious salmon anaemia virus in the established Atlantic salmon cell line. J. Gen. Virol. 1997, vol. 78, pt. 8, pp. 1891–1895. doi: 10.1099/0022-1317-78-8-1891.

17. Mjaaland S., Rimstad E., Falk K., Dannevig B.H. Genomic characterization of the virus causing infectious salmon anemia in Atlantic salmon (Salmo salar L.): an Orthomyxo-like virus in a teleost. J. Virol. 1997, vol. 71, no. 10, pp. 7681–7686.

18. Krossoy B., Hordvik I., Nilsen F., Nylund A., Endresen C. The putative polymerase sequence of infectious salmon anemia virus suggests a new genus within the Orthomyxoviridae. J. Virol. 1999, vol. 73, no. 3, pp. 2136–2142.

19. Alkhovsky S.V., Lvov D.K., Shchelkanov M.Yu., Shchetinin A.M., Deryabin P.G., Lvov D.N., Lvov S.S., Samokhvalov E.I., Gitelman A.K., Botikov A.G., Krasnoslobodtsev K.G. Genetic characterization of Batken virus (BKNV) (Orthomyxoviridae, Thogotovirus) isolated from ixodidae ticks Hyalomma marginatum Koch, 1844 and mosquitoes Aedes caspius Pallas, 1771 and Culex hortensis Ficalbi, 1889 in Central Asia. Voprosy Virusologii [Problems in Virology]. 2014, vol. 59, no. 2, pp. 33–37. (In Russian)

20. Lvov D.K., Alkhovsky S.V., Shchelkanov M.Yu., Shchetinin A.M., Deryabin P.G., Aristova V.A., Gitelman A.K., Samokhvalov E.I., Botikov A.G. Taxonomic status of Tyulek virus (TLKV) (Orthomyxoviridae, Quaranjavirus, Quaranfil group) isolated from ticks Argas vulgaris Filippova, 1961 (Argasidae) from the birds burrow nest biotopes in the Kyrgyzstan. Voprosy Virusologii [Problems in Virology]. 2014, vol. 59, no. 2, pp. 28–32. (In Russian)

21. Shchelkanov M.Yu., Fedyakina I.T., Proshina E.S., Lvov D.N., Ponomarenko R.A., Chumakov V.M., Burtseva E.I., Galkina I.V., Lvov D.K. Taxonomic structure of Orthomyxoviridae: current views and immediate prospects. Vestnik Rossiiskoi Akademii Meditsinskikh Nauk [Annals of Russian Academy of Medical Sciences]. 2011, no. 5, pp. 12–19. (In Russian)

22. Hastings T., Olivier G., Cusack R., Bricknell I., Nylund A., Binde M., Munro P., Allan C. Infectious salmon anaemia. Bull. Euro. Assoc. Fish Pathol. 1999, vol. 19, pp. 286–288.

23. Cook-Versloot M., Griffiths S., Cusack R., McGeachy S., Ritchie R. Identification and characterisation of infectious salmon anaemia virus (ISAV) haemagglutinin gene highly polymorphic region (HPR) type 0 in North America. Bull. Euro. Assoc. Fish Pathol. 2004, vol. 24, pp. 203–208.

24. McBeath A.J., Bain N., Snow M. Surveillance for infectious salmon anaemia virus HPR0 in marine Atlantic salmon farms across Scotland. Dis. Aquat. Organ. 2009, vol. 87, pp. 161–169. doi: 10.3354/dao02128.

25. Fourrier M., Lester K., Markussen T., Falk K., Secombes C.J., McBeath A., Collet B. Genotype promote viral fusion and activation by an ubiquitous host protease. PLoS One. 2015, vol. 10, no. 10, pp. e0142020. doi: 10.1371/journal.pone.0142020.

26. Markussen T., Sindre H., Jonassen C.M., Tengs T., Kristoffersen A.B., Ramsell J., Numanovic S., Hjortaas M.J., Christiansen D.H., Dale O.B., Falk K. Ultra-deep pyrosequencing of partial surface protein genes from infectious salmon anaemia virus (ISAV) suggest novel mechanisms involved in transition to virulence. PLoS One. 2013, vol. 8, pp. e81571. doi: 10.1371/journal. pone.0081571.

27. Cardenas C., Carmona M., Gallardo A., Labra A., Marshall S.H. Coexistence in field samples of two variants of the infectious salmon anemia virus: a putative shift to pathogenicity. PLoS One. 2014, vol. 9, pp. e87832. doi: 10.1371/journal.pone.0087832.

28. Kibenge F.S.B., Garate O.N., Johnson G., Arriagada R., Kibenge M.J.T., Wadowska D. Isolation and identification of infectious salmon anaemia virus (ISAV) from Coho salmon in Chile. Dis. Aquat. Org. 2001, vol. 45, pp. 9–18. doi: 10.3354/dao045009.

29. MacWilliams C., Johnson G., Groman D., Kibenge F.S.B. Morphologic description of infectious salmon anaemia virus (ISAV)-induced lesions in rainbow trout (Oncorhynchus mykiss) compared to Atlantic salmon (Salmo salar). Dis. Aquat. Org. 2007, vol. 78, pp. 1–12. doi: 10.3354/dao01866.

30. Nylund A., Wallace C., Hovland T. The possible role of Lepeophtheirus salmonis (Kroyer) in the transmission of infectious salmon anemia. In: Pathogens of wild and farmed fish: sea lice / Eds.: G. Boxshall, D. Defaye. – Chichester: Ellis Harwood Ltd., 1993, pp. 367–373.

31. Gustafson L., Ellis S., Robinson T., Marenghi F., Endris R. Efficacy of emamectin benzoate against sea lice infestations of Atlantic salmon, Salmo salar L.: evaluation in the absence of an untreated contemporary control. J. Fish Dis. 2006, vol. 29, no. 10, pp. 621–627. doi: 10.1111/j.1365-2761.2006.00761.x.

32. Gustafson L., Antognoli M., Lara Fica M., Ibarra R., Mancilla J., Sandoval del Valle O., Enriquez Sais R., Perez A., Aguilar D., Madrid E., Bustos P., Clement A., Godoy M.G., Johnson C., Remmenga M. Risk factors perceived predictive of ISA spread in Chile: applications to decision support. Prev. Vet. Med. 2014, vol. 117, no. 1, pp. 276–285. doi: 10.1016/j.prevetmed.2014.08.017.

33. Shchelkanov M.Yu., Kolobukhina L.V., Lvov D.K. Influenza: history, clinics, pathogenesis. Lechashchii Vrach [The Practitioner]. 2011, no. 10, pp. 33–38. (In Russian)

34. Weli S.C., Aamelfot M., Dale O.B., Koppang E.O., Falk K. Infectious salmon anaemia virus infection of Atlantic salmon gill epithelial cells. Virol. J. 2013, vol. 10, no. 5. doi: 10.1186/1743-422X-10-5.

35. Aamelfot M., McBeath A., Christiansen D.H., Matejusova I., Falk K. Infectious salmon anaemia virus (ISAV) mucosal infection in Atlantic salmon. Vet. Res. 2015, vol. 46, no. 120. doi: 10.1186/s13567-015-0265-1.

36. Hellebø A., Vilas U., Falk K., Vlasak R. Infectious salmon anemia virus specifically binds to and hydrolyzes 4-O-acetylated sialic acids. J. Virol. 2004, vol. 78, no. 6, pp. 3055–3062.

37. Shchelkanov M.Yu., Kolobukhina L.V., Lvov D.K. Human coronaviruses (Nidovirales, Coronaviridae): increased level of epidemic threat. Lechashchii Vrach [The Practitioner]. 2013, no. 10, pp. 49–54. (In Russian)

38. Nerette P., Stryhn H., Dohoo I., Hammell L. Using pseudogold standards and latent-class analysis in combination to evaluate the accuracy of three diagnostic tests. Prev Vet Med. 2008, vol. 85, no. 3-4, pp. 207–225. doi: 10.1016/j.prevetmed.2008.01.011.

39. Kibenge M.T., Opazo B., Rojas A.H., Kibenge F.S. Serological evidence of infectious salmon anaemia virus (ISAV) infection in farmed fishes, using an indirect enzyme-linked immunosorbent assay (ELISA). Dis. Aquat. Organ. 2002, vol. 51, no. 1, pp. 1–11. doi: 10.3354/dao051001.

40. Hoare R., Thompson K.D., Herath T., Collet B., Bron J.E., Adams A. Development, characterisation and application of monoclonal antibodies for the detection and quantification of infectious salmon anaemia virus in plasma samples using luminex bead array technology. PLoS One. 2016, vol. 11, no. 7, pp. e0159155. doi: 10.1371/journal.pone.0159155.

41. O'Shea B., Wadsworth S., Pino Marambio J., Birkett M.A., Pickett J.A., Mordue Luntz A.J. Disruption of host-seeking behaviour by the salmon louse, Lepeophtheirus salmonis, using botanically derived repellents. J. Fish Dis. 2016. doi: 10.1111/jfd.12526.

42. Dempster T., Kristiansen T.S., Korsøen Ø.J., Fosseidengen J.E., Oppedal F. Technical note: modifying Atlantic salmon (Salmo salar) jumping behavior to facilitate innovation of parasitic sea lice control techniques. J. Animal Sci. 2014, vol. 89, no. 12, pp. 4281–4285. doi: 10.2527/jas.2011-3894.

43. Leclercq E., Davie A., Migaud H. Delousing efficiency of farmed ballan wrasse (Labrus bergylta) against Lepeophtheirus salmonis infecting Atlantic salmon (Salmo salar) post-smolts. Pest Manag. Sci. 2014, vol. 70, no. 8, pp. 1274–1282. doi: 10.1002/ps.3692.

44. Lauscher A., Krossøy B., Frost P., Grove S., König M., Bohlin J., Falk K., Austbø L., Rimstad E. Immune responses in Atlantic salmon (Salmo salar) following protective vaccination against infectious salmon anemia (ISA) and subsequent ISA virus infection. Vaccine. 2011, vol. 29, no. 37, pp. 6392–6401. doi: 10.1016/j.vaccine.2011.04.074.

45. Wolf A., Hodneland K., Frost P., Hoeijmakers M., Rimstad E. Salmonid alphavirus-based replicon vaccine against infectious salmon anemia (ISA): impact of immunization route and interactions of the replicon vector. Fish Shellfish Immunol. 2014, vol. 36, no. 2, pp. 383–392. doi: 10.1016/j.fsi.2013.12.018.

46. Rivas-Aravena A., Fuentes Y., Cartagena J., Brito T., Poggio V., La Torre J., Mendoza H., GonzalezNilo F., Sandino A.M., Spencer E. Development of a nanoparticle-based oral vaccine for Atlantic salmon against ISAV using an alphavirus replicon as adjuvant. Fish Shellfish Immunol. 2015, vol. 45, no. 1, pp. 157–166. doi: 10.1016/j.fsi.2015.03.033.

47. Chang C.J., Robertsen C., Sun B., Robertsen B. Protection of Atlantic salmon against virus infection by intramuscular injection of IFNc expression plasmid. Vaccine. 2014, vol. 32, no. 36, pp. 4695–4702. doi: 10.1016/j.vaccine.2014.05.059.

48. Caruffo M., Maturana C., Kambalapally S., Larenas J., Tobar J.A. Protective oral vaccination against infectious salmon anaemia virus in Salmo salar. Fish Shellfish Immunol. 2016, vol. 54, pp. 54–59. doi: 10.1016/j.fsi.2016.03.009.