Infectious salmon anemia virus (ISAV) is an orthomyxovirus responsible for a significant disease of farmed Atlantic salmon. Fallowing and re-establishment of the Atlantic salmon farming industry in the Faroes following a recent devastating infectious salmon anaemia (ISA) disease epidemic provided a unique opportunity to study the risk of re-emergence of disease. Over 53 months, 2787 of 34 573 (8.1 %) apparently healthy Atlantic salmon analysed tested positive for ISAV by RT-PCR. Sequence analysis revealed the putative low-pathogenic ISAV-HPR0 subtype in all cases. Results demonstrated that ISAV-HPR0 appeared as a seasonal and transient infection without detectable ISA mortality or pathology. This finding, coupled to an apparent gill tropism of ISAV-HPR0, suggests ISAV-HPR0 causes a subclinical respiratory infection more like seasonal influenza, as opposed to the systemic infection and serious disease caused by highly pathogenic ISAV. The mean time before marine sites became infected was 7.7 months after transfer to seawater of the fish, suggesting a potentially unknown marine reservoir of infection. Sequence analysis identified two main subtypes of ISAV-HPR0 sequences, one of which showed close genetic association with ISAV isolates responsible for the disease outbreak in the Faroes. Thus ISAV-HPR0 might represent an ancestor of pathogenic variants and thus be a potential risk factor in the emergence of new strains of disease-causing ISAV. Our data, however, suggest that the risk of emergence of pathogenic ISAV variants from a reservoir of ISAV-HPR0 is low. This risk is probably being further reduced by practical management strategies adopted in the Faroes and aimed at reducing the potential for maintenance and adaptation of ISAV-HPR0.


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  1. Akaike, H.(1974). A new look at the statistical model identification. IEEE Trans Automat Contr 19, 716–722.[CrossRef] [Google Scholar]
  2. Anonymous(2000). ISA hits the Faroes. Fish Farming Int, 47.
  3. Anonymous(2005). Epizootiological investigation into a case of suspicion of infectious salmon anaemia (ISA) in Scotland in November. Fisheries Research Service Internal Report no 11/05.
  4. Aspehaug, V., Mikalsen, A. B., Snow, M., Biering, E. & Villoing, S.(2005). Characterization of the infectious salmon anemia virus fusion protein. J Virol 79, 12544–12553.[CrossRef] [Google Scholar]
  5. Bouchard, D., Brockway, D., Giray, C., Keleher, W. & Merril, P. L.(2001). First report of infectious salmon anaemia (ISA) in the United States. Bull Eur Assoc Fish Pathol 21, 86–88. [Google Scholar]
  6. Calendini, F. & Martin, J.-F.(2005). PaupUP v1.0.3.1 A free graphical frontend for paup* dos software.
  7. Cook-Versloot, M., Griffith, S., Cusack, R., McGeachy, S. & Ritchie, R.(2004). Identification and characterisation of infectious salmon anaemia virus (ISAV) haemagglutinin gene highly polymorphic region (HPR) type 0 in North America. Bull Eur Assoc Fish Pathol 24, 203–208. [Google Scholar]
  8. Cunningham, C. O., Gregory, A., Black, J., Simpson, I. & Raynard, R. S.(2002). A novel variant of the infectious salmon anaemia virus (ISAV) haemagglutinin gene suggests mechanisms for virus diversity. Bull Eur Assoc Fish Pathol 22, 366–374. [Google Scholar]
  9. Dale, O. B., Ørpetveit, I., Lyngstad, T. M., Kahns, S., Skall, H. F., Olesen, N. J. & Dannevig, B. H.(2009). Outbreak of viral haemorrhagic septicaemia (VHS) in seawater-farmed rainbow trout in Norway caused by VHS virus Genotype III. Dis Aquat Organ 85, 93–103.[CrossRef] [Google Scholar]
  10. Einer-Jensen, K., Ahrens, P., Forsberg, R. & Lorenzen, N.(2004). Evolution of the fish rhabdovirus viral haemorrhagic septicaemia virus. J Gen Virol 85, 1167–1179.[CrossRef] [Google Scholar]
  11. Evensen, O., Thorud, K. E. & Olsen, Y. A.(1991). A morphological study of the gross and light microscopic lesions of infectious anaemia in Atlantic salmon (Salmo salar). Res Vet Sci 51, 215–222.[CrossRef] [Google Scholar]
  12. Falk, K., Namork, E., Rimstad, E., Mjaaland, S. & Dannevig, B. H.(1997). Characterization of infectious salmon anemia virus, an orthomyxo-like virus isolated from Atlantic salmon (Salmo salar L.). J Virol 71, 9016–9023. [Google Scholar]
  13. Falk, K., Aspehaug, V., Vlasak, R. & Endresen, C.(2004). Identification and characterization of viral structural proteins of infectious salmon anemia virus. J Virol 78, 3063–3071.[CrossRef] [Google Scholar]
  14. Feldmann, A., Schäfer, M. K. H., Garten, W. & Klenk, H. D.(2000). Targeted infection of endothelial cells by avian influenza virus A/FPV/Rostock/34 (H7N1) in chicken embryos. J Virol 74, 8018–8027.[CrossRef] [Google Scholar]
  15. Felsenstein, J.(1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.[CrossRef] [Google Scholar]
  16. Fodor, E., Mingay, L. J., Crow, M., Deng, T. & Brownlee, G. G.(2003). A single amino acid mutation in the PA subunit of the influenza virus RNA polymerase promotes the generation of defective interfering RNAs. J Virol 77, 5017–5020.[CrossRef] [Google Scholar]
  17. Godoy, M. G., Aedo, A., Kibenge, M. J. T., Groman, D. B., Yason, C. V., Grothusen, H., Lisperguer, A., Calbucura, M., Avendaño, F. & other authors(2008). First detection, isolation and molecular characterization of infectious salmon anaemia virus associated with clinical disease in farmed Atlantic salmon (Salmo salar) in Chile. BMC Vet Res 4, 28.[CrossRef] [Google Scholar]
  18. Hall, T. A.(1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41, 95–98. [Google Scholar]
  19. Håstein, T., Hill, B. J. & Winton, J. R.(1999). Successful aquatic animal disease emergency programmes. Rev Sci Tech 18, 214–227. [Google Scholar]
  20. Johansen, R., Kongtorp, R. T., Borno, G., Skjelstad, H. R., Olsen, A. B., Flesja, K., Colquhoun, D., Orpetveit, I., Hansen, H. & other authors(2008).The Health Situation in Farmed Salmonids 2008, pp. 1–32. Oslo. : National Veterinary Institute. [Google Scholar]
  21. Kibenge, F. S., Godoy, M. G., Wang, Y., Kibenge, M. J., Gherardelli, V., Mansilla, S., Lisperger, A., Jarpa, M., Larroquete, G. & other authors(2009). Infectious salmon anaemia virus (ISAV) isolated from the ISA disease outbreaks in Chile diverged from ISAV isolates from Norway around 1996 and was disseminated around 2005, based on surface glycoprotein gene sequences. Virol J 6, 88.[CrossRef] [Google Scholar]
  22. Klenk, H. O.(2005). Infection of the endothelium by influenza virus. Thromb Haemost 94, 262–265. [Google Scholar]
  23. Krossøy, B., Devold, M., Sanders, L., Knappskog, P. M., Aspehaug, V., Falk, K., Nylund, A., Koumans, S., Endresen, C. & Biering, E.(2001). Cloning and identification of the infectious salmon anaemia virus haemagglutinin. J Gen Virol 82, 1757–1765. [Google Scholar]
  24. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A. & other authors(2007). Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948.[CrossRef] [Google Scholar]
  25. Mackay, I. M., Arden, K. E. & Nitsche, A.(2002). Real-time PCR in virology. Nucleic Acids Res 30, 1292–1305.[CrossRef] [Google Scholar]
  26. Markussen, T., Jonassen, C. M., Numanovic, S., Braaen, S., Hjortaas, M., Nilsen, H. & Mjaaland, S.(2008). Evolutionary mechanisms involved in the virulence of infectious salmon anaemia virus (ISAV), a piscine orthomyxovirus. Virology 374, 515–527.[CrossRef] [Google Scholar]
  27. McBeath, A. J., Bain, N. & Snow, M.(2009). Surveillance for infectious salmon anaemia virus HPR0 in marine Atlantic salmon farms across Scotland. Dis Aquat Organ 87, 161–169.[CrossRef] [Google Scholar]
  28. Mjaaland, S., Rimstad, E., Falk, K. & Dannevig, B. H.(1997). Genomic characterization of the virus causing infectious salmon anemia in Atlantic salmon (Salmo salar L.): an orthomyxo-like virus in a teleost. J Virol 71, 7681–7686. [Google Scholar]
  29. Mjaaland, S., Hungnes, O., Teig, A., Dannevig, B. H., Thorud, K. & Rimstad, E.(2002). Polymorphism in the infectious salmon anemia virus hemagglutinin gene: importance and possible implications for evolution and ecology of infectious salmon anemia disease. Virology 304, 379–391.[CrossRef] [Google Scholar]
  30. Mullins, J. E., Groman, D. & Wadowska, D.(1998). Infectious salmon anaemia in salt water Atlantic salmon (Salmo salar L.) in New Brunswick, Canada. Bull Eur Assoc Fish Pathol 18, 110–114. [Google Scholar]
  31. Nylund, A. & Jakobsen, P.(1995). Sea trout as a carrier of infectious salmon anaemia virus. J Fish Biol 47, 174–176.[CrossRef] [Google Scholar]
  32. Nylund, A., Wallace, C. & Hovland, T.(1993). The possible role of Lepeophtheirus salmonis (Krøyer) in the transmission of infectious salmon anaemia. In Pathogens of Wild and Farmed Fish: Sea Lice, vol. 28, p. 367–373. Edited by Boxshall, G. & Defaye, D.. London. : Ellis Horwood Ltd. [Google Scholar]
  33. Nylund, A., Kvenseth, A. M., Krossoy, B. & Hodneland, K.(1997). Replication of the infectious salmon anaemia virus (ISAV) in rainbow trout, Oncorhynchus mykiss (Walbaum). J Fish Dis 20, 275–279.[CrossRef] [Google Scholar]
  34. Nylund, A., Devold, M., Mullins, J. E. & Plarre, H.(2002). Herring (Clupea harengus): a host for infectious salmon anemia virus (ISAV). Bull Eur Assoc Fish Pathol 22, 311–318. [Google Scholar]
  35. Nylund, A., Devold, M., Plarre, H., Isdal, E. & Aarseth, M.(2003). Emergence and maintenance of infectious salmon anaemia virus (ISAV) in Europe: a new hypothesis. Dis Aquat Organ 56, 11–24.[CrossRef] [Google Scholar]
  36. Nylund, A., Plarre, H., Karlsen, M., Fridell, F., Ottem, K. F., Bratland, A. & Saether, P. A.(2007). Transmission of infectious salmon anaemia virus (ISAV) in farmed populations of Atlantic salmon (Salmo salar). Arch Virol 152, 151–179.[CrossRef] [Google Scholar]
  37. Posada, D.(2008). jModelTest: phylogenetic model averaging. Mol Biol Evol 25, 1253–1256.[CrossRef] [Google Scholar]
  38. Rimstad, E., Mjaaland, S., Snow, M., Mikalsen, A. B. & Cunningham, C. O.(2001). Characterization of the infectious salmon anemia virus genomic segment that encodes the putative hemagglutinin. J Virol 75, 5352–5356.[CrossRef] [Google Scholar]
  39. Rodger, H. D., Turnbull, T., Muir, F., Millar, S. & Richards, R. H.(1998). Infectious salmon anaemia (ISA) in the United Kingdom. Bull Eur Assoc Fish Pathol 18, 115–116. [Google Scholar]
  40. Snow, M., Raynard, R. S. & Bruno, D. W.(2001). Comparative susceptibility of Arctic char (Salvelinus alpinus), rainbow trout (Oncorhynchus mykiss) and brown trout (Salmo trutta) to the Scottish isolate of infectious salmon anaemia virus. Aquaculture 196, 47–54.[CrossRef] [Google Scholar]
  41. Snow, M., Raynard, R., Bruno, D. W., van Nieuwstadt, A. P., Olesen, N. J., Løvold, T. & Wallace, C.(2002). Investigation into the susceptibility of saithe Pollachius virens to infectious salmon anaemia virus (ISAV) and their potential role as a vector for viral transmission. Dis Aquat Organ 50, 13–18.[CrossRef] [Google Scholar]
  42. Snow, M., McKay, P., McBeath, A. J., Black, J., Doig, F., Kerr, R., Cunningham, C. O., Nylund, A. & Devold, M.(2006). Development, application and validation of a Taqman real-time RT-PCR assay for the detection of infectious salmon anaemia virus (ISAV) in Atlantic salmon (Salmo salar). Dev Biol (Basel) 126, 133–145, discussion 325–326. [Google Scholar]
  43. Stagg, R. M.(2003). The eradication of clinical infectious salmon anaemia from Scotland. In International Response to Infectious Salmon Anemia: Prevention, Control, and Eradication: Proceedings of a Symposium 3–4 September 2002. Edited by O. Miller & R. C. Cipriano. New Orleans, LA: Department of Agriculture, Animal and Plant Health Inspection Service.
  44. Swofford, D. L.(2002).paup*: Phylogenetic analysis using parsimony (and other methods), version 4. Sunderland, MA: Sinauer Associates.
  45. Thorud, K. & Djupvik, H. O.(1988). Infectious anaemia in Atlantic salmon (Salmo salar L.). Bull Eur Assoc Fish Pathol 8, 109–111. [Google Scholar]
  46. Vike, S., Nylund, S. & Nylund, A.(2009). ISA virus in Chile: evidence of vertical transmission. Arch Virol 154, 1–8.[CrossRef] [Google Scholar]

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