Research Article: Wild and farmed salmon (Salmo salar) as reservoirs for infectious salmon anaemia virus, and the importance of horizontal- and vertical transmission

Date Published: April 16, 2019

Publisher: Public Library of Science

Author(s): Are Nylund, Jarle Brattespe, Heidrun Plarre, Martha Kambestad, Marius Karlsen, Uwe Fischer.

http://doi.org/10.1371/journal.pone.0215478

Abstract

The infectious salmon anaemia virus (ISAV) is an important pathogen on farmed salmon in Europe. The virus occurs as low- and high virulent variants where the former seem to be a continuous source of new high virulent ISAV. The latter are controlled in Norway by stamping out infected populations while the former are spreading uncontrolled among farmed salmon. Evidence of vertical transmission has been presented, but there is still an ongoing discussion of the importance of circulation of ISAV via salmon brood fish. The only known wild reservoirs are in trout (Salmo trutta) and salmon (Salmo salar). This study provides the first ISAV sequences from wild salmonids in Norway and evaluates the importance of this reservoir with respect to outbreaks of ISA among farmed salmon. Phylogenetic analyses of the surface protein hemagglutinin-esterase gene from nearly all available ISAV from Norway, Faeroe Islands, Scotland, Chile and wild salmonids in Norway show that they group into four major clades. Including virulent variants in the analysis show that they belong in the same four clades supporting the hypothesis that there is a high frequency of transition from low to high virulent variants in farmed populations of salmon. There is little support for a hypothesis suggesting that the wild salmonids feed the virus into farmed populations. This study give support to earlier studies that have documented local horizontal transmission of high virulent ISAV, but the importance of transition from low- to high virulent variants has been underestimated. Evidence of vertical transmission and long distance spreading of ISAV via movement of embryos and smolt is presented. We recommend that the industry focus on removing the low virulent ISAV from the brood fish and that ISAV-free brood fish salmon are kept in closed containment systems (CCS).

Partial Text

Infectious salmon anaemia virus (ISAV), an orthomyxovirus infecting farmed and wild members of the genus Salmo is an economically important pathogen of farmed Atlantic salmon (Salmo salar). It is also one of the most studied viruses among those causing mortalities in farmed Atlantic salmon. The disease, infectious salmon anaemia (ISA), was officially discovered in 1984 among salmon parr in a hatchery in Western Norway [1]. The disease resulted in about 80% mortality at the site. In the following years the disease emerged in marine farms along the Norwegian coast that received smolt from this hatchery [2]. The number of outbreaks increased steadily from 1984 until 1991, a year with around 80 outbreaks. The large losses due to ISA triggered changes in the production of Atlantic salmon and the production went from multiple to one single generation at each production site. This lead to a new situation in 1994 with only a single outbreak of ISA [3]. The pathology of ISA was first described in 1991 [4].

Low-virulent HPR0 ISA virus sequences have been obtained from all counties with commercial salmon farming in Norway, while ISA virus sequences from wild salmonids have only been obtained from the counties Rogaland, Sør Trøndelag, Nord Trøndelag and Finnmark (Fig 1). A total of 21 segment six sequences were obtained from wild salmonids in Norway (S1 Table). The prevalence of ISA virus in wild salmon (Salmo salar) and trout (Salmo trutta) in western Norway was low, 0.5% (2/436) and 1.6% (4/253), respectively. The densities of ISA virus RNA were also low in these samples and it was only possible to sequence segment six from one of the positives (R170/09), a trout collected in a river in Rogaland County (Fig 1 and S1 Table). This ISA virus had a deleted HPR (HPRΔ), but it is not known if this virus was virulent. The prevalence of ISA virus in salmonids collected in Nord- and Sør-Trøndelag, and Finnmark varied between the years of collection from 0.0% to 37.9% with the highest prevalence in wild salmon in Namsfjorden (Nord-Trøndelag) in 2017 (Fig 1 and Table 1). The prevalence of ISAV in the river Namsen that empties into Namsfjorden was only 5.0% the same year. Overall the prevalence’s of ISAV in the rivers are lower compared to that observed in the respective fjords (Table 1). The Ct values obtained for the elongation factor α, that was used as a control for the quality of the RNA extractions, ranged from 14.4 to 18.0 in the screening of the gill samples from the wild salmonids.

This is the first study of European ISA viruses from farmed Atlantic salmon (Salmo salar) that includes the majority of available segment six sequences in addition to 21 ISA viruses from wild salmon (Salmo salar) and trout (S. trutta) in Norway. The study includes more than 100 low virulent HPR0 ISA viruses. The focus is on information (geographical occurrence, variants, transmission and reservoirs) that can be obtained from phylogenetic analysis of segment six from high (HPRΔ) and low (HPR0) virulent ISA viruses from fresh and sea water in Norway, Scotland, Faeroe Islands and Chile. This segment has been used in several earlier studies of the relationship between existing ISA viruses and for inferring short and long distance transmission [33, 34, 37, 41, 43, 46, 48, 49, 51, 52, 53, 55, 58, 70, 71, 72]. Admittedly, the change from low to high virulent variants of ISA viruses is, based on existing knowledge, dependent on mutational changes in both segment five (fusion protein, F, gene) and segment six (hemagglutinin-esterase, HE, gene) [49, 50, 53, 56, 57, 58], but all HPRΔ variants have so far been of higher virulence than HPR0 variants. Hence, in this study all HPRΔ variants are listed as virulent while the HPR0 variants are listed as low virulent viruses.

 

Source:

http://doi.org/10.1371/journal.pone.0215478

 

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