Skip to main content
Top
Published in: Virology Journal 1/2013

Open Access 01-12-2013 | Research

Infectious salmon anaemia virus (ISAV) in Chilean Atlantic salmon (Salmo salar) aquaculture: emergence of low pathogenic ISAV-HPR0 and re-emergence of virulent ISAV-HPR∆: HPR3 and HPR14

Authors: Marcos G Godoy, Molly JT Kibenge, Rudy Suarez, Eduardo Lazo, Alejandro Heisinger, Javier Aguinaga, Diego Bravo, Julio Mendoza, Katerina O Llegues, Rubén Avendaño-Herrera, Cristian Vera, Fernando Mardones, Frederick SB Kibenge

Published in: Virology Journal | Issue 1/2013

Login to get access

Abstact

Infectious salmon anaemia (ISA) is a serious disease of marine-farmed Atlantic salmon (Salmo salar) caused by ISA virus (ISAV), which belongs to the genus Isavirus, family Orthomyxoviridae. ISA is caused by virulent ISAV strains with deletions in a highly polymorphic region (HPR) of the hemagglutinin-esterase (HE) protein (designated virulent ISAV-HPR∆). This study shows the historic dynamics of ISAV-HPR∆ and ISAV-HPR0 in Chile, the genetic relationship among ISAV-HPR0 reported worldwide and between ISAV-HPR0 and ISAV-HPR∆ in Chile, and reports the 2013 ISA outbreak in Chile. The first ISA outbreak in Chile occurred from mid-June 2007 to 2010 and involved the virulent ISAV-HPR7b, which was then replaced by a low pathogenic ISAV-HPR0 variant. We analyzed this variant in 66 laboratory-confirmed ISAV-HPR0 cases in Chile in comparison to virulent ISAV-HPR∆ that caused two new ISA outbreaks in April 2013. Multiple alignment and phylogenetic analysis of HE sequences from all ISAV-HPR0 viruses allowed us to identify three genomic clusters, which correlated with three residue patterns of ISAV-HPR0 (360PST362, 360PAN362 and 360PAT362) in HPR. The virus responsible for the 2013 ISAV-HPR∆ cases in Chile belonged to ISAV-HPR3 and ISAV-HPR14, and in phylogenetic analyses, both clustered with the ISAV-HPR0 found in Chile. The ISAV-HPR14 had the ISAV-HPR0 residue pattern 360PAT362, which is the only type of ISAV-HPR0 variant found in Chile. This suggested to us that the 2013 ISAV-HPR∆ re-emerged from ISAV-HPR0 that is enzootic in Chilean salmon aquaculture and were not new introductions of virulent ISAV-HPR∆ to Chile. The clinical presentations and diagnostic evidence of the 2013 ISA cases indicated a mixed infection of ISAV with the ectoparasite Caligus rogercresseyi and the bacterium Piscirickettsia salmonis, which underscores the need for active ISAV surveillance in areas where ISAV-HPR0 is enzootic, to ensure early detection and control of new ISA outbreaks, as it is considered a risk factor. This is the first report of ISA linked directly to the presence of ISAV-HPR0, and provides strong evidence supporting the contention that ISAV-HPR0 shows a strong relationship to virulent ISAV-HPR∆ viruses and the possibility that it could mutate to virulent ISAV-HPR∆.
Appendix
Available only for authorised users
Literature
2.
go back to reference Kibenge FSB, Godoy MG, Fast M, Workenhe S, Kibenge MJT: Countermeasures against viral diseases of farmed fish. Antiviral Res. 2012, 95: 257-281.PubMedCrossRef Kibenge FSB, Godoy MG, Fast M, Workenhe S, Kibenge MJT: Countermeasures against viral diseases of farmed fish. Antiviral Res. 2012, 95: 257-281.PubMedCrossRef
3.
go back to reference McCauley JW, Hongo S, Kaverin NV, Kochs G, Lamb RA, et al: Family Orthomyxoviridae. In Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses. Edited by: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ. 2011, San Diego, CA: Academic Press, 749-761. McCauley JW, Hongo S, Kaverin NV, Kochs G, Lamb RA, et al: Family Orthomyxoviridae. In Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses. Edited by: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ. 2011, San Diego, CA: Academic Press, 749-761.
4.
go back to reference Rimstad E, Mjaaland S, Snow M, Mikalsen AB, Cunningham CO: Characterization of the infectious salmon anemia virus genomic segment that encodes the putative hemagglutinin. J Virol. 2001, 75: 5352-5356.PubMedPubMedCentralCrossRef Rimstad E, Mjaaland S, Snow M, Mikalsen AB, Cunningham CO: Characterization of the infectious salmon anemia virus genomic segment that encodes the putative hemagglutinin. J Virol. 2001, 75: 5352-5356.PubMedPubMedCentralCrossRef
5.
go back to reference Krossøy B, Nilsen F, Falk K, Endresen C, Nylund A: Phylogenetic analysis of infectious salmon anaemia virus isolates from Norway, Canada and Scotland. Dis Aquat Org. 2001, 44: 1-6.PubMedCrossRef Krossøy B, Nilsen F, Falk K, Endresen C, Nylund A: Phylogenetic analysis of infectious salmon anaemia virus isolates from Norway, Canada and Scotland. Dis Aquat Org. 2001, 44: 1-6.PubMedCrossRef
6.
go back to reference Falk K, Aspehaug V, Vlasak R, Endresen C: Identification and characterization of viral structural proteins of infectious salmon anemia virus. J Virol. 2004, 78: 3063-3071.PubMedPubMedCentralCrossRef Falk K, Aspehaug V, Vlasak R, Endresen C: Identification and characterization of viral structural proteins of infectious salmon anemia virus. J Virol. 2004, 78: 3063-3071.PubMedPubMedCentralCrossRef
7.
go back to reference Aspehaug V, Mikalsen AB, Snow M, Biering E, Villoing S: Characterization of the infectious salmon anemia virus fusion protein. J Virol. 2005, 79: 12544-12553.PubMedPubMedCentralCrossRef Aspehaug V, Mikalsen AB, Snow M, Biering E, Villoing S: Characterization of the infectious salmon anemia virus fusion protein. J Virol. 2005, 79: 12544-12553.PubMedPubMedCentralCrossRef
8.
go back to reference Kibenge FS, Kibenge MJ, Gherardelli V, Mansilla S, Lisperger A, Jarpa M, Larroquete G, Avendão F, Lara M, Gallardo A, Godoy MG, Wang Y: 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. Virology J. 2009, 6: 88-CrossRef Kibenge FS, Kibenge MJ, Gherardelli V, Mansilla S, Lisperger A, Jarpa M, Larroquete G, Avendão F, Lara M, Gallardo A, Godoy MG, Wang Y: 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. Virology J. 2009, 6: 88-CrossRef
11.
go back to reference McBeath AJA, Bain N, Snow M: Surveillance for infectious salmon anaemia virus HPR0 in marine Atlantic salmon farms across Scotland. Dis Aquat Org. 2009, 87: 161-169.PubMedCrossRef McBeath AJA, Bain N, Snow M: Surveillance for infectious salmon anaemia virus HPR0 in marine Atlantic salmon farms across Scotland. Dis Aquat Org. 2009, 87: 161-169.PubMedCrossRef
12.
go back to reference Christiansen DH, Østergaard PS, Snow M, Dale OB, 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, 92: 909-918.PubMedCrossRef Christiansen DH, Østergaard PS, Snow M, Dale OB, 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, 92: 909-918.PubMedCrossRef
13.
go back to reference Mjaaland S, Hungnes O, Teig A, Dannevig BH, Thorud K, Rimstad E: Polymorphism in the infectious salmon anaemia virus haemagglutinin gene: importance and possible implications for evolution and ecology of infectious salmon anaemia disease. Virology. 2002, 304: 379-391.PubMedCrossRef Mjaaland S, Hungnes O, Teig A, Dannevig BH, Thorud K, Rimstad E: Polymorphism in the infectious salmon anaemia virus haemagglutinin gene: importance and possible implications for evolution and ecology of infectious salmon anaemia disease. Virology. 2002, 304: 379-391.PubMedCrossRef
14.
go back to reference Cunningham C, Gregory A, Black J, Simpson I, Raynard R: A novel variant of the infectious salmon anaemia virus (ISAV) haemagglutinin gene suggests mechanisms for virus diversity. Bull Eur Assoc Fish Pathol. 2002, 22: 366-374. Cunningham C, Gregory A, Black J, Simpson I, Raynard R: A novel variant of the infectious salmon anaemia virus (ISAV) haemagglutinin gene suggests mechanisms for virus diversity. Bull Eur Assoc Fish Pathol. 2002, 22: 366-374.
15.
go back to reference Cook-Versloot M, Griffiths S, Cusack R, McGeachy S, Ritchie R: Identification and characterization of infectious salmon anemia virus (ISAV) hemagglutinin gene highly polymorphic region (HPR) type 0 in North America. Bull Eur Assoc Fish Path. 2004, 24: 203-208. Cook-Versloot M, Griffiths S, Cusack R, McGeachy S, Ritchie R: Identification and characterization of infectious salmon anemia virus (ISAV) hemagglutinin gene highly polymorphic region (HPR) type 0 in North America. Bull Eur Assoc Fish Path. 2004, 24: 203-208.
16.
go back to reference Nylund A, Plarre H, Hodneland K, Devold M, Aspehaug V, Aarseth M, Koren C, Watanabe K: Haemorrhagic smolt syndrome (HSS) in Norway: pathology and associated virus-like particles. Dis Aquat Org. 2003, 54: 15-27.PubMedCrossRef Nylund A, Plarre H, Hodneland K, Devold M, Aspehaug V, Aarseth M, Koren C, Watanabe K: Haemorrhagic smolt syndrome (HSS) in Norway: pathology and associated virus-like particles. Dis Aquat Org. 2003, 54: 15-27.PubMedCrossRef
17.
go back to reference Nylund A, Plarre H, Karlsen M, Fridell F, Otten KF, Baratland A, Sæther PA: Transmission of infectious salmon anaemia virus in farmed populations of Atlantic salmon (Salmo salar). Arch Virol. 2007, 152: 151-179.PubMedCrossRef Nylund A, Plarre H, Karlsen M, Fridell F, Otten KF, Baratland A, Sæther PA: Transmission of infectious salmon anaemia virus in farmed populations of Atlantic salmon (Salmo salar). Arch Virol. 2007, 152: 151-179.PubMedCrossRef
18.
go back to reference Markussen T, Jonassen CM, Numanovic S, Braaen S, Hjortaas M, Nilsen H, Mjaaland S: Evolutionary mechanisms involved in the virulence of infectious salmon anaemia virus (ISAV), a piscine orthomyxovirus. Virology. 2008, 374: 515-527.PubMedCrossRef Markussen T, Jonassen CM, Numanovic S, Braaen S, Hjortaas M, Nilsen H, Mjaaland S: Evolutionary mechanisms involved in the virulence of infectious salmon anaemia virus (ISAV), a piscine orthomyxovirus. Virology. 2008, 374: 515-527.PubMedCrossRef
19.
go back to reference Lyngstad T, Hjortaas M, Kristoffersen A, Markussen T, Karlsen E, Jonassen C, Jansen P: Use of molecular epidemiology to trace transmission pathways for infectious salmon anaemia virus (ISAV) in Norwegian salmon farming. Epidemics. 2011, 3: 1-11.PubMedCrossRef Lyngstad T, Hjortaas M, Kristoffersen A, Markussen T, Karlsen E, Jonassen C, Jansen P: Use of molecular epidemiology to trace transmission pathways for infectious salmon anaemia virus (ISAV) in Norwegian salmon farming. Epidemics. 2011, 3: 1-11.PubMedCrossRef
20.
go back to reference Lyngstad TM, Kristoffersen AB, Hjortaas MJ, Devold M, Aspehaug V, Larssen RB, Jansen PA: Low virulent infectious salmon anaemia virus (ISAV-HPR0) is prevalent and geographically structured in Norwegian salmon farming. Dis Aquat Org. 2012, 101: 197-206.PubMedCrossRef Lyngstad TM, Kristoffersen AB, Hjortaas MJ, Devold M, Aspehaug V, Larssen RB, Jansen PA: Low virulent infectious salmon anaemia virus (ISAV-HPR0) is prevalent and geographically structured in Norwegian salmon farming. Dis Aquat Org. 2012, 101: 197-206.PubMedCrossRef
21.
go back to reference Plarre H, Nylund A, Karlsen M, Brevik Ø, Sæther PA, Vike S: Evolution of infectious salmon anaemia virus (ISA virus). Arch Virol. 2012, 157: 2309-2326.PubMedCrossRef Plarre H, Nylund A, Karlsen M, Brevik Ø, Sæther PA, Vike S: Evolution of infectious salmon anaemia virus (ISA virus). Arch Virol. 2012, 157: 2309-2326.PubMedCrossRef
22.
go back to reference Godoy MG, Aedo A, Kibenge MJT, Groman DB, Yason CV, Grothusen H, Lisperguer A, Calbucura M, Avendaño F, Imilán M, Jarpa M, Kibenge FSB: 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. 2008, 4: 28-PubMedPubMedCentralCrossRef Godoy MG, Aedo A, Kibenge MJT, Groman DB, Yason CV, Grothusen H, Lisperguer A, Calbucura M, Avendaño F, Imilán M, Jarpa M, Kibenge FSB: 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. 2008, 4: 28-PubMedPubMedCentralCrossRef
23.
go back to reference Vike S, Nylund S, Nylund A: ISA virus in Chile: evidence of vertical transmission. Arch Virol. 2009, 154: 1-8.PubMedCrossRef Vike S, Nylund S, Nylund A: ISA virus in Chile: evidence of vertical transmission. Arch Virol. 2009, 154: 1-8.PubMedCrossRef
24.
go back to reference Cottet L, Cortez-San Martin M, Tello M, Olivares E, Rivas-Aravena A, Vallejos E, Sandino AM, Spencer E: Bioinformatic analysis of the genome of infectious salmon anemia virus associated with outbreaks with high mortality in Chile. J Virol. 2010, 84: 11916-11928.PubMedPubMedCentralCrossRef Cottet L, Cortez-San Martin M, Tello M, Olivares E, Rivas-Aravena A, Vallejos E, Sandino AM, Spencer E: Bioinformatic analysis of the genome of infectious salmon anemia virus associated with outbreaks with high mortality in Chile. J Virol. 2010, 84: 11916-11928.PubMedPubMedCentralCrossRef
25.
go back to reference Mardones FO, Perez AM, Valdes-Donoso P, Carpenter TE: Farm-level reproduction number during an epidemic of infectious salmon anemia virus in southern Chile in 2007–2009. Prev Vet Med. 2011, 2011 (102): 175-184.CrossRef Mardones FO, Perez AM, Valdes-Donoso P, Carpenter TE: Farm-level reproduction number during an epidemic of infectious salmon anemia virus in southern Chile in 2007–2009. Prev Vet Med. 2011, 2011 (102): 175-184.CrossRef
26.
go back to reference Murray AG, Munro LA, Wallace IS, Berx B, Pendrey D, Fraser D, Raynard RS: Epidemiological investigation into the re-emergence and control of an outbreak of infectious salmon anaemia in the Shetland Islands, Scotland. Dis Aquat Org. 2010, 91: 189-200.PubMedCrossRef Murray AG, Munro LA, Wallace IS, Berx B, Pendrey D, Fraser D, Raynard RS: Epidemiological investigation into the re-emergence and control of an outbreak of infectious salmon anaemia in the Shetland Islands, Scotland. Dis Aquat Org. 2010, 91: 189-200.PubMedCrossRef
28.
go back to reference Kibenge FSB, Kibenge MJT, Wang Y, Qian B, Hariharan S, McGeachy S: Mapping of putative virulence motifs on infectious salmon anaemia virus surface glycoprotein genes. J Gen Virol. 2007, 88: 3100-3111.PubMedCrossRef Kibenge FSB, Kibenge MJT, Wang Y, Qian B, Hariharan S, McGeachy S: Mapping of putative virulence motifs on infectious salmon anaemia virus surface glycoprotein genes. J Gen Virol. 2007, 88: 3100-3111.PubMedCrossRef
29.
go back to reference Frank SA: Models of parasite virulence. Quarterly Rev Biol. 1996, 71: 37-78.CrossRef Frank SA: Models of parasite virulence. Quarterly Rev Biol. 1996, 71: 37-78.CrossRef
30.
go back to reference Galvani AP: Epidemiology meets evolutionary ecology. TRENDS Ecol Evol. 2003, 18: 132-139.CrossRef Galvani AP: Epidemiology meets evolutionary ecology. TRENDS Ecol Evol. 2003, 18: 132-139.CrossRef
31.
go back to reference Pulkkinen K, Suomalainen L-R, Read AF, Ebert D, Rintamäki P, Valtonen ET: Intensive fish farming and the evolution of pathogen virulence: the case of columnaris disease in Finland. Proc R Soc B. 2010, 277: 593-600.PubMedPubMedCentralCrossRef Pulkkinen K, Suomalainen L-R, Read AF, Ebert D, Rintamäki P, Valtonen ET: Intensive fish farming and the evolution of pathogen virulence: the case of columnaris disease in Finland. Proc R Soc B. 2010, 277: 593-600.PubMedPubMedCentralCrossRef
33.
go back to reference Evensen O, Thorud KE, Olsen YA: A morphological study of the gross and light microscopic lesions of infectious anaemia in Atlantic salmon Salmo salar. Res Vet Sci. 1991, 51: 215-222. 35PubMedCrossRef Evensen O, Thorud KE, Olsen YA: A morphological study of the gross and light microscopic lesions of infectious anaemia in Atlantic salmon Salmo salar. Res Vet Sci. 1991, 51: 215-222. 35PubMedCrossRef
34.
go back to reference Speilberg L, Evensen O, Dannevig BH: A sequential study of the light and electron microscopical liver lesions of infectious anemia in Atlantic salmon Salmo salar L. Vet Pathol. 1995, 32: 466-478.PubMedCrossRef Speilberg L, Evensen O, Dannevig BH: A sequential study of the light and electron microscopical liver lesions of infectious anemia in Atlantic salmon Salmo salar L. Vet Pathol. 1995, 32: 466-478.PubMedCrossRef
35.
go back to reference Simko E, Brown LL, MacKinnon AM, Byrne PJ, Ostland VE, Ferguson HW: Experimental infection of Atlantic salmon, Salmo salar L., with infectious salmon naemia virus: a histopathological study. J Fish Dis. 2000, 23: 27-32.CrossRef Simko E, Brown LL, MacKinnon AM, Byrne PJ, Ostland VE, Ferguson HW: Experimental infection of Atlantic salmon, Salmo salar L., with infectious salmon naemia virus: a histopathological study. J Fish Dis. 2000, 23: 27-32.CrossRef
36.
go back to reference Jones SRM, Groman DB: Cohabitation transmission of infectious salmon anemia virus among freshwater-reared Atlantic salmon. J Aquat Ani Health. 2001, 13: 340-346.CrossRef Jones SRM, Groman DB: Cohabitation transmission of infectious salmon anemia virus among freshwater-reared Atlantic salmon. J Aquat Ani Health. 2001, 13: 340-346.CrossRef
37.
go back to reference Moneke E, Groman D, Johnson GR, Wright GM, Stryhn H, Ikede BO, Kibenge FSB: Correlation of virus distribution in tissues with histologic lesions in Atlantic salmon experimentally infected with infectious salmon anaemia virus. Vet Pathol. 2005, 42: 338-349.PubMedCrossRef Moneke E, Groman D, Johnson GR, Wright GM, Stryhn H, Ikede BO, Kibenge FSB: Correlation of virus distribution in tissues with histologic lesions in Atlantic salmon experimentally infected with infectious salmon anaemia virus. Vet Pathol. 2005, 42: 338-349.PubMedCrossRef
38.
go back to reference Munir K, Kibenge FSB: Detection of infectious salmon anaemia virus by real-time RT-PCR. J Virol Methods. 2004, 117: 37-47.PubMedCrossRef Munir K, Kibenge FSB: Detection of infectious salmon anaemia virus by real-time RT-PCR. J Virol Methods. 2004, 117: 37-47.PubMedCrossRef
39.
go back to reference Snow M, McKay P, McBeath AJA, Black J, Doig F, Kerr R, Cunningham CO, Nylund A, Devold M: 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 Standardization. 2006, 126: 133-145. Snow M, McKay P, McBeath AJA, Black J, Doig F, Kerr R, Cunningham CO, Nylund A, Devold M: 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 Standardization. 2006, 126: 133-145.
40.
go back to reference Palacios G, Lovoll M, Tengs T, Hornig M, Hutchison S, et al: Heart and skeletal muscle inflammation of farmed salmon is associated with infection with a novel reovirus. PLoS One. 2010, 5: e11487-PubMedPubMedCentralCrossRef Palacios G, Lovoll M, Tengs T, Hornig M, Hutchison S, et al: Heart and skeletal muscle inflammation of farmed salmon is associated with infection with a novel reovirus. PLoS One. 2010, 5: e11487-PubMedPubMedCentralCrossRef
41.
go back to reference Garver KA, Hawley LM, McClure CA, Schroeder T, Aldous S, Doig F, Snow M, Edes S, Baynes C, Richard J: Development and validation of a reverse transcription quantitative PCR for universal detection of viral hemorrhagic septicemia virus. Dis Aquat Org. 2011, 95: 97-112.PubMedCrossRef Garver KA, Hawley LM, McClure CA, Schroeder T, Aldous S, Doig F, Snow M, Edes S, Baynes C, Richard J: Development and validation of a reverse transcription quantitative PCR for universal detection of viral hemorrhagic septicemia virus. Dis Aquat Org. 2011, 95: 97-112.PubMedCrossRef
42.
go back to reference Holopainen R, Honkanen J, Jensen BB, Ariel E, Tapiovaara H: Quantitation of ranaviruses in cell culture and tissue samples. J Virol Meth. 2011, 171: 225-233.CrossRef Holopainen R, Honkanen J, Jensen BB, Ariel E, Tapiovaara H: Quantitation of ranaviruses in cell culture and tissue samples. J Virol Meth. 2011, 171: 225-233.CrossRef
43.
go back to reference Hodneland K, Bratland A, Christie KE, Endresen C, Nylund A: New subtype of almonid alphavirus (SAV), Togaviridae, from Atlantic salmon Salmo salar and rainbow trout Oncorhynchus mykiss in Norway. Dis Aquat Org. 2005, 66: 113-120.PubMedCrossRef Hodneland K, Bratland A, Christie KE, Endresen C, Nylund A: New subtype of almonid alphavirus (SAV), Togaviridae, from Atlantic salmon Salmo salar and rainbow trout Oncorhynchus mykiss in Norway. Dis Aquat Org. 2005, 66: 113-120.PubMedCrossRef
44.
go back to reference Corbeil S, McColl KA, Crane MSJ: Development of a TaqMan quantitative PCR assay for the identification of Piscirickettsia salmonis. Bull Eur Assoc Fish Pathol. 2003, 23: 95-101. Corbeil S, McColl KA, Crane MSJ: Development of a TaqMan quantitative PCR assay for the identification of Piscirickettsia salmonis. Bull Eur Assoc Fish Pathol. 2003, 23: 95-101.
45.
go back to reference Kulldorff M, Heffernan R, Hartman J, Assunção R, Mostashari F: A space-time per-mutation scan statistic for disease outbreak detection. PLoS Med. 2005, 2: 216-224.CrossRef Kulldorff M, Heffernan R, Hartman J, Assunção R, Mostashari F: A space-time per-mutation scan statistic for disease outbreak detection. PLoS Med. 2005, 2: 216-224.CrossRef
46.
go back to reference Kulldorff M, Feuer EJ, Miller BA, Freedman LS: Breast cancer clusters in the northeast United States: a geographic analysis. Am J Epidemiol. 1997, 146: 161-170.PubMedCrossRef Kulldorff M, Feuer EJ, Miller BA, Freedman LS: Breast cancer clusters in the northeast United States: a geographic analysis. Am J Epidemiol. 1997, 146: 161-170.PubMedCrossRef
48.
go back to reference R Development Core Team: R: A language and environment for statistical computing. 2008, Vienna, Austria: R Foundation for Statistical Computing, ISBN 3-900051-07-0, URL http://www.R-project.org R Development Core Team: R: A language and environment for statistical computing. 2008, Vienna, Austria: R Foundation for Statistical Computing, ISBN 3-900051-07-0, URL http://​www.​R-project.​org
49.
go back to reference Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A: Geneious v6.0.4. 2012, Available from http://www.geneious.com Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A: Geneious v6.0.4. 2012, Available from http://​www.​geneious.​com
50.
go back to reference Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ: Basic local alignment search tool. J Mol Biol. 1990, 215: 403-410.PubMedCrossRef Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ: Basic local alignment search tool. J Mol Biol. 1990, 215: 403-410.PubMedCrossRef
51.
go back to reference Saitou N, Nei M: The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987, 4: 406-425.PubMed Saitou N, Nei M: The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987, 4: 406-425.PubMed
Metadata
Title
Infectious salmon anaemia virus (ISAV) in Chilean Atlantic salmon (Salmo salar) aquaculture: emergence of low pathogenic ISAV-HPR0 and re-emergence of virulent ISAV-HPR∆: HPR3 and HPR14
Authors
Marcos G Godoy
Molly JT Kibenge
Rudy Suarez
Eduardo Lazo
Alejandro Heisinger
Javier Aguinaga
Diego Bravo
Julio Mendoza
Katerina O Llegues
Rubén Avendaño-Herrera
Cristian Vera
Fernando Mardones
Frederick SB Kibenge
Publication date
01-12-2013
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2013
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/1743-422X-10-344

Other articles of this Issue 1/2013

Virology Journal 1/2013 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.