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1 Department of Pathology and Microbiology, Atlantic Veterinary College, University of Prince Edward Island, 550 University Avenue, Charlottetown, PEI C1A 4P3, Canada
2 Aquatic Diagnostic Services, Atlantic Veterinary College, University of Prince Edward Island, 550 University Avenue, Charlottetown, PEI C1A 4P3, Canada
3 New Brunswick Department of Agriculture, Fisheries and Aquaculture, Fredericton, NB, Canada
Correspondence
Frederick S. B. Kibenge
kibenge{at}upei.ca
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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90 %. These highly pathogenic strains also caused low mortality in rainbow trout, albeit later in infection. Viruses with a more delayed or protracted mortality phase resulting in cumulative mortalities of 50–89 % in Atlantic salmon were considered to be of intermediate pathogenicity and isolates with cumulative mortalities of 
49 % were considered to be of low pathogenicity. On this basis, three of the ISAV isolates showed a high-, eight an intermediate- and two a low-pathogenicity phenotype in Atlantic salmon. Coho salmon were resistant to all ISAV isolates. These results confirmed that there is variation in pathogenicity among ISAV strains for Atlantic salmon and rainbow trout, and that other salmonid species such as coho salmon can carry highly pathogenic strains of ISAV without showing signs of disease. The identified pathogenicity phenotypes may aid in the identification of molecular markers of ISAV virulence. |
INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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). It is a significant fish pathogen that has caused and continues to cause severe economic losses to the salmon-farming industry in the northern hemisphere. Clinical infectious salmon anaemia (ISA) is characterized by high mortality, with dead fish exhibiting exophthalmia, pale gills, ascites and haemorrhagic liver necrosis, and renal interstitial haemorrhage and tubular nephrosis (Evensen et al., 1991; Thorud & Djupvik, 1988). The virus has also been detected in diseased farmed coho salmon (Oncorhynchus kisutch) in Chile in 2000 (Kibenge et al., 2001a), in apparently normal seawater-farmed rainbow trout (Oncorhynchus mykiss) in Ireland in 2002 (Siggins, 2002), in apparently normal wild fish [sea trout and brown trout (Salmo trutta) and Atlantic salmon (Salmo salar)] from the same geographical locations as Atlantic salmon farms with clinical ISA in Scotland, UK (Cunningham et al., 2002; Raynard et al., 2001a), and in apparently normal non-salmonid marine fish [pollock (Pollachius virens) and Atlantic cod (Gadus morhua)] collected from cages with ISA-diseased salmon in Maine, USA (MacLean et al., 2003). These findings support the observation that natural clinical disease from ISAV only occurs in marine-farmed Atlantic salmon.
Under experimental conditions, ISAV may infect other fish, resulting in asymptomatic, probably life-long, carriers of the virus (Nylund et al., 1994, 1995, 1997, 2002; Rolland & Nylund, 1999). Rainbow trout, brown trout and Arctic char (Salvelinus alpinus) are reported to be resistant to experimental infection with the Scottish ISAV isolate 390/98 (Snow et al., 2001). The pacific salmonid species chum (Oncorhynchus keta), steelhead trout (O. mykiss), chinnok (Oncorhynchus tshawytscha) and coho salmon were also found to be resistant to experimental infection with a Norwegian strain and a Canadian strain of ISAV, even with doses as high as 108 TCID50 ml–1 that induced 98 % cumulative mortality in Atlantic salmon (Rolland & Winton, 2003).
It is assumed, but not yet proven, that there is variation in pathogenicity among ISAV strains. As only samples from clinical cases routinely receive appropriate diagnostic attention, naturally avirulent ISAV strains may be rarely isolated. Attempts to isolate virus from some natural ISA outbreaks (Mjaaland et al., 2002) and from some ISAV RT-PCR-positive fish (Devold et al., 2001; Kibenge et al., 2001a; Nylund et al., 2002; Raynard et al., 2001a; Snow et al., 2001) have not been successful. One possible explanation for this failure is that the available fish cell lines are not sensitive enough to grow low virus titres, in contrast to naïve Atlantic salmon. It is also not known whether the currently available fish cell lines are equally permissive to both pathogenic and non-pathogenic ISAV strains. Mjaaland et al. (2002) found no clear correlation between the replication properties of different ISAV isolates in SHK-1 cells and the development of cytopathic effects (CPE); however, the isolates that replicated well showed CPE either early or later in the infection.
Most experimental studies of ISAV infection in Atlantic salmon reported to date have used single ISAV isolates and/or different virus doses, making it difficult to extrapolate the relative levels of pathogenicity among different ISAV strains. These experiments investigated the effects of freshwater versus seawater, different routes of infection, different virus doses (Raynard et al., 2001b), the effects of mixed infection with togavirus-like virus (Kibenge et al., 2000a), the effects of vaccination with inactivated whole ISAV (Jones et al., 1999) and the relative resistance of pacific salmon to ISAV infection (Rolland & Winton, 2003). One study compared different ISAV isolates using MHC-compatible Atlantic salmon half-siblings (Mjaaland et al., 2005), but virus infection was by cohabitation transmission making it difficult to standardize the virus dose and hence limiting the range in death prevalence. Raynard et al. (2001b) showed that there is a relationship between the onset of mortality and the virus dose used to infect Atlantic salmon, with those fish that received a higher viral dose starting to die earlier than those given lower doses of the same virus.
The present study compared the pathogenicity of 13 different strains of ISAV isolated from different geographical regions between 1997 and 2004, used at an equal virus dose, for Atlantic salmon, coho salmon and rainbow trout in an attempt to identify and characterize the correlates of ISAV virulence. To our knowledge, this is the first systematic demonstration of virulence variation among ISAV isolates in Atlantic salmon and including a second fish species, Oncorhynchus spp., susceptible to clinical disease. The rainbow trout infection phenotype of ISAV is presented as a correlate of ISAV pathogenicity and may facilitate the identification of ISAV virulence genes.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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) were grown in Hanks' minimum essential medium (BioWhittaker) supplemented with 10 % fetal bovine serum, 2 mM L-glutamine, 1 % non-essential amino acids and 50 µg gentamicin ml–1. Cells were incubated at room temperature (24 °C) and the monolayer cultures were used 24 h after seeding. All viruses used in this study were received as SHK-1 cell line lysates except for isolate NBISA01, which was a CHSE-214 cell line lysate. The geographical origin, laboratory source and genotype of the 13 ISAV isolates used in this study are summarized in Table 1. The viruses were propagated and titrated in TO cells, as described previously (Kibenge et al., 2001b), prior to use in the in vivo infectivity assay.
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) to establish the ISAV-negative status of the stock before virus challenge. The fish were maintained in the Aquatic Animal Facility of the Atlantic Veterinary College (AVC) in 1 m diameter fibreglass-reinforced plastic tanks using a freshwater flow-through system at a temperature of approximately 11 °C. The Atlantic salmon, rainbow trout and coho salmon were acclimatized in separate tanks in freshwater for 2–4 weeks at a water flow rate of 3.5 l min–1. The experimental procedures used in this study were performed in accordance with the guidelines of the Canadian Council of Animal Care (Olfert et al., 1993). The fish were divided into groups: the uninfected control group consisted of 70–100 Atlantic salmon, 40 rainbow trout and 40 coho salmon, whilst each of the infected groups consisted of 30–50 Atlantic salmon, 10 rainbow trout and 10 coho salmon in each tank. For each trial, the uninfected control tank was located in a separate ‘clean’ room from the tanks with experimentally infected fish. For the experimental infection, the challenge fish were removed from the stock-holding tank and anaesthetized by immersion in an aerated solution of tricaine methanesulphonate (TMS-222; 100 mg l–1). Each fish was then challenged by the intraperitoneal route with 0.2 ml virus suspension containing approximately 106.0 TCID50 ISAV and was then returned to the respective study tank. In all trials, caution was taken to avoid contact between the tanks for the different ISAV isolates. Fish were fed once a day and the fish tanks were flushed once a day. All tanks were checked twice daily for mortality and the fish were observed for abnormal behaviour and external lesions for the duration of the study. All dead fish were necropsied and, where necessary, tissues (kidney, heart, spleen and pyloric caeca) were collected for virus detection by RT-PCR and histopathology. At the termination of the study at 58–76 days post-inoculation (p.i.), all surviving fish were necropsied and tissues (kidney, heart, spleen and pyloric caeca) were collected for virus detection by RT-PCR.
RT-PCR.
Total RNA was extracted from 300 µl clarified tissue homogenates of pooled organ tissues (kidney, heart, liver and spleen) of fish mortalities or hearts of the surviving fish using TRIzol reagent (Invitrogen Life Technologies) following the manufacturer's protocol. The RT-PCR primers and conditions and the thermal cycler used to detect ISAV by RT-PCR have been described previously (Kibenge et al., 2000b). PCR products were resolved by electrophoresis on a 1 % agarose gel and visualized under 304 nm UV light after staining with ethidium bromide (Sambrook et al., 1989).
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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). A total of five experimental trials (1–5) were performed in this study. These trials were designed according to the fish infection model originally used to reproduce ISA mortality and gross pathology experimentally at the AVC Aquatic Animal Facility (Kibenge et al., 2000a), which is now used routinely (Moneke et al., 2003).
The cumulative percentage mortalities from ISAV-injected fish in the five trials are summarized in Table 2. The fish mortality data from trials 3 and 5 were compromised because of an aggressive fungal infection (in the control Atlantic salmon group, control coho salmon group and groups infected with ISAV isolates 810/9/99 and RPC/NB 98-0280-2 in trial 3, and in the control Atlantic salmon group and the group infected with RPC/NB 01-0973-3 in trial 5) that was successfully controlled with formalin bath treatment. Fungal infections are not uncommon in fish challenge trials (Rolland & Winton, 2003) and both prophylactic and therapeutic formalin bath treatments are routine additions to experimental protocols. No gross clinical signs of ISA were observed in any of the fish and they were not counted with the ISAV-induced mortalities. In addition, the Atlantic salmon that died at 7 days p.i. in the group infected with isolate RPC/NB 01-0973-3 in trial 4 had no gross pathology lesions and this fish was also not counted with the ISAV-induced mortalities. All groups infected with ISAV experienced mortality among Atlantic salmon, with cumulative percentage mortalities ranging from 10 to 100 %, occurring between 10 and 41 days p.i., and exhibited gross lesions characteristic of ISAV infection (Thorud & Djupvik, 1988). Some of the ISAV-infected groups also experienced mortality in rainbow trout, with cumulative percentage mortalities ranging from 10 to 50 %, occurring between 13 and 40 days p.i. and exhibited gross lesions consistent with ISA observed in Atlantic salmon, which included moderate haemorrhage in pyloric caeca, pale gills and dark liver. There was no mortality in the coho salmon in any of the ISAV-injected groups during any of the trials. No mortalities occurred in any of the control groups during trials 1, 2 and 4.
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; Mjaaland et al., 2002; Nylund et al., 1995, 1997, 2003). For example, it was suggested that ISAV may have been introduced to Norway with the importation of rainbow trout from North America (Krossøy et al., 2001). It has been suggested that there are natural reservoirs for the virus, probably in fish occurring in the coastal areas where ISA outbreaks frequently occur. Thus, the virulence of ISAV is intrinsically linked to its emergence as a pathogen in marine-farmed Atlantic salmon (Nylund et al., 2003). The correlates of ISAV pathogenicity, however, are as yet poorly understood. For any virus, virulence varies over a wide range: from strains that almost always cause inapparent infections, to those that usually cause disease, to those that usually cause death (Murphy et al., 1999). As virus virulence is dependent on both virus factors and host factors, and as there are no available inbred Atlantic salmon lines, precise measures of virulence of ISAV are impossible. Thus, we undertook a systematic study in which all ISAV isolates were used at an equal virus dose for Atlantic salmon, coho salmon and rainbow trout. To quantify virus titres of the different viruses in order to use equivalent amounts of virus, all of the viruses were propagated and titrated in TO cells.
The 13 ISAV isolates varied in their mortality patterns for Atlantic salmon, reflecting a variation in their virulence, as depicted in Figs 1 and 2 and summarized in Table 2
. Thus, the most virulent virus strains, NBISA01, RPC/NB 98-049-1 and 810/9/99, had the highest mortality of >90 %. Fish infected with these viruses had the most acute mortality phase in Atlantic salmon, starting between 10 and 13 days p.i. and lasting for only 9–15 days. The Atlantic salmon mortality of the less-virulent ISAV isolates either lasted longer and/or started later, portraying a protracted mortality phase. For example, for isolates U5575-1 and 485/9/97 with mortalities of 64 and 60 %, respectively, the first mortality occurred at 18 days p.i. and the last at 39 and 41 days p.i., respectively. For isolates RPC/NB 01-0973-3 and RPC/NB 04-085-1, which were even less virulent with mortalities of 28.6 and 18.2 %, respectively, the first mortality occurred later at 22 and 21 days p.i., respectively. When the ISAV isolates were ranked based on their ability to kill Atlantic salmon, the isolates with the highest cumulative percentage mortalities (i.e. >90 %) and some with medium cumulative percentage mortalities (65–85 %) also killed rainbow trout (Table 2). The cumulative percentage mortality in rainbow trout was always lower than in Atlantic salmon. In addition, the mortality phase in ISAV-infected rainbow trout was protracted in that it started later and/or lasted longer than in Atlantic salmon for the same virus isolates. Thus, for isolate NBISA01, mortality in rainbow trout started at 13 days p.i. (compared with 10 days p.i. in Atlantic salmon) and stopped at 27 days p.i. (compared with 19 days p.i. in Atlantic salmon) (Table 2). On the basis of these data, the in vivo correlates of virulence of ISAV include the following: (i) cumulative percentage mortality in Atlantic salmon; the most pathogenic strains had mortality levels of >90 %; (ii) nature of the mortality phase (i.e. time of onset and duration of mortality) in Atlantic salmon; the most pathogenic strains had an acute mortality phase that started at 10–13 days p.i. and lasted for 9–15 days; and (iii) mortality in rainbow trout, with systemic haemorrhagic lesions that were consistent with those typically seen in Atlantic salmon infected with ISAV. Previous analyses of natural ISA disease patterns (Mjaaland et al., 2002) and experimental ISA disease in a cohabitant challenge model (Mjaaland et al., 2005) also suggest a grouping of two main forms, acute and protracted. The shorter duration of the mortality phase in the present study would be analogous to acute disease, whilst the longer duration of mortality would be analogous to protracted disease. Table 3 summarizes a traceback on some of the ISAV isolates used in the present study. Isolate RPC/NB 01-0973-3 was associated with an acute natural disease pattern and isolate RPC/NB 04-085-1 was non-pathogenic in natural infections, but both isolates had a protracted experimental disease pattern. This indicates that the natural disease may not necessarily correlate with the experimental disease. However, of more significance is the fact that we could separate ISAV isolates into those that killed rainbow trout and those that did not, and this separation appeared to correlate with ISAV pathogenicity in Atlantic salmon. Thus, the rainbow trout infection phenotype might facilitate the identification of ISAV virulence genes.
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). The pyloric caeca had multifocal regions of mild congestion and haemorrhage within the lamina propria vasculature (Fig. 3b). Affected heart tissue contained moderate diffuse endocardial hyperplasia with evidence of a mild to moderate mononuclear cell infiltrate and phagocytosis of debris and effete erythrocytes (Fig. 3c). The gill demonstrated moderate diffuse filamental arteriole congestion and lamellar telangiectasia. Changes in the spleen included mild diffuse sinusoidal congestion and increased frequency of erythrophagia, and for the liver a mild peribilliary cuffing by mononuclear leukocytes. These lesions were consistent with those typically seen in Atlantic salmon infected with ISAV and are consistent with a clinical diagnosis of ISA in rainbow trout. Moreover, since histological analysis was performed only on the fish mortalities, we could not categorically rule out histopathological lesions in any surviving fish during the mortality phase. It is noteworthy that changes seen for the kidney (interstitial haemorrhage), gill (filamental arteriole congestion), spleen (diffuse sinusoidal congestion and erythrophagia) and pyloric caeca (congestion of the lamina propria vasculature) were all consistent with lesions typically seen in Atlantic salmon with ISA in both naturally acquired (Mullins et al., 1998) and experimentally induced scenarios (Jones & Groman, 2001). The finding of endocarditis, in association with the above tissue changes was, however, unexpected, as ISAV in Atlantic salmon typically does not produce significant inflammation to heart tissues.
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. Virus was detected in fish tissues throughout the mortality period in Atlantic salmon mortalities. Most mortalities that occurred during the middle of the mortality period (15–22 days p.i.) for all virus groups tested were positive for ISAV, whereas at the end of the mortality period (23–42 days p.i.), only about 50 % of the mortalities were positive for ISAV and these were mainly from viruses of lower pathogenicity for Atlantic salmon. In case of the rainbow trout mortalities, virus was detected in fish tissues during the beginning and middle of the mortality period only. The heart tissues from all surviving fish were also tested for virus by RT-PCR. All samples were negative except for one pool sample from Atlantic salmon infected with ISAV isolate 485/9/97, indicating that most surviving fish were free of virus regardless of the ISAV isolate used. As there was no mortality among ISAV-injected coho salmon, there were no data on virus presence in coho salmon tissues. However, it is unlikely that this fish species does not get infected with ISAV. In a preliminary study (data not shown), we observed histopathological lesions characteristic of ISA in the absence of mortality in coho salmon. Moreover, others have detected ISAV titres of 102.5–103 TCID50 g–1 in coho salmon randomly sampled 13–15 days after injection with 108 TCID50 virus ml–1 (Rolland & Winton, 2003), indicating that this fish species undergoes asymptomatic infection.
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). Moreover, other wild birds are as susceptible as domestic poultry to highly pathogenic avian influenza, but they can also carry low-pathogenic strains of the virus, which, if introduced into domestic poultry, can spread and mutate to the highly pathogenic form. Thus, it is more likely that the emergence of ISAV as a fish pathogen is a reflection of variation in virus–host interactions similar to the situation with avian influenza in poultry. For example, domestic poultry (order Galliformes) are not the natural hosts of avian influenza A viruses (Perdue et al., 1999; Suarez & Schultz-Cherry, 2000). However, people have altered the epidemiological variables of avian influenza A viruses by creating new ecological niches via bird captivity and domestication, industrial agriculture, national and international commerce and non-traditional raising practices (Swayne, 2000). In these new ecosystems, pathogenic and non-pathogenic micro-organisms can be transmitted within and between avian species (or fish species, in the case of ISAV) and adapt to new host species. In conclusion, we have demonstrated experimentally that the cumulative percentage mortality and the duration of mortality in Atlantic salmon associated with a particular virus strain are indicators of ISAV virulence. Whereas to date ISAV has only been isolated from healthy rainbow trout and is not known to cause natural clinical disease in fish other than farmed Atlantic salmon, here we report the first experimentally induced clinical disease associated with high mortality due to experimental infection with ISAV in a fish species other than Atlantic salmon. We identified three ISAV isolates that were highly pathogenic in Atlantic salmon and of low pathogenicity in rainbow trout. This rainbow trout infection phenotype might facilitate the identification of ISAV virulence genes.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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Received 28 November 2005;
accepted 19 April 2006.
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