Piscine Orthoreovirus (PRV) and Heart and Skeletal Muscle Inflammation (HSMI)

Preface

Fisheries and Oceans Canada (DFO) has received a number of inquiries regarding the presence of PRV (also known as Piscine Reovirus) and HSMI on the Pacific Coast.

The Government of Canada has an internationally recognized National Aquatic Animal Health Program (NAAHP) that is co-delivered by the Canadian Food Inspection Agency (CFIA) and DFO under the authority of CFIA's Health of Animals Act and Health of Animals Regulations. Under NAAHP, DFO's laboratory system provides the diagnostic testing, research and scientific advice regarding reportable pathogens of finfish, molluscs, and crustaceans.

In addition to the NAAHP, DFO's Pacific Aquaculture Management Division has a role in fish health management through its audit program that conducts fish health audits at up to 30 active farm sites per calendar quarter. As the primary regulator for aquaculture in BC, DFO works closely with the CFIA, the aquaculture industry and other partners to identify and manage potential risks to the health of wild and farmed salmon.

DFO also engages in research associated with other microbes that may impact salmonids but are not listed in acts and regulations. As a science-based department, DFO draws on existing scientific knowledge, conducts its own research and collaborates with others. Some of this research is being conducted under the Program for Aquaculture Regulatory Research (PARR), a DFO program that supports research on aquatic animal diseases. Additionally, the Strategic Salmon Health Initiative (SSHI), co-funded by DFO, Pacific Salmon Foundation and Genome BC, is an international consortium of scientists conducting research on microbes potentially impacting BC's wild, enhanced and farmed salmon. Both the PARR and the SSHI are also providing scientific data and information pertinent to PRV and HSMI in BC salmon.

Lay Summary:

PRV

Distribution and susceptible species

PRV is known to be present in Norway, the United Kingdom, Ireland, Chile, the United States and Canada (Biering and Garseth 2012; Kibenge et al. 2013; Siah et al. 2015). In Canada, testing of archived fish tissues indicated the presence of PRV in wild and farmed Pacific salmon since 1987 and possibly as early as 1977. Additional survey work through various labs and agencies in Canada and the United States has expanded the known host range of PRV in the North Pacific Ocean to include: Cutthroat Trout (Oncorhynchus clarkii), Chinook Salmon (Oncorhynchus tshawytscha), Sockeye Salmon (Oncorhynchus nerka), Steelhead Trout (Oncorhynchus mykiss), Coho Salmon (Oncorhynchus kisutch), Chum Salmon (Oncorhynchus keta) Pink Salmon (Oncorhynchus gorbusca) and farmed Atlantic Salmon (Salmo salar) (DFO 2015).  Detections have been made from both farmed and wild fish populations which have extended from the state of Washington north through BC to Alaska (DFO 2015; Marty et al. 2015; Siah et al. 2015, Miller et al. 2017, Morton et al. 2017, Purcell et al. 2017 ).

In North Atlantic waters PRV has been detected in both salmonid and non-salmonid fish which includes farmed and wild Atlantic Salmon (Salmo salar), wild Sea-Trout (Salmo trutta), Great Silver Smelt (Argentina silus), Atlantic Horse Mackerel (Trachurus trachurus), Atlantic Herring (Clupea harengus) and Capelin (Mallotus villosus) (Wiik-Nielson et al. 2012; Garseth et al. 2013). 

Genomic variability

Genomic sequencing of PRV from BC has revealed some genetic differences when compared to PRV from other regions (Kibenge et al. 2013; Siah et al. 2015). Based on an analysis of genetic differences,  Kibenge et al. 2013 proposed that PRV first arrived in BC from Norway sometime around 2007. However, recent testing of archived samples held by DFO has revealed that PRV has been present in salmonids on the Pacific coast of North America salmon since 1987 and possibly as early as 1977 (Marty et al. 2015; Siah et al. 2015).

HSMI

The disease HSMI was first reported in farmed Atlantic Salmon in Norway in 1999 (Kongtorp et al. 2004a) resulting in farm production losses.  Since then, the number of cases in Norway has steadily increased to a peak of 181 farm outbreaks reported in 2014.  HSMI continues to cause reduced survival of farmed fish in Norway (Marine Harvest 2015).  Similar or HSMI-like disease has also been reported in farmed Atlantic Salmon in Scotland (Ferguson et al. 2005) and Chile (Godoy et al. 2016). 

HSMI is characterized by mortality that ranges from negligible up to 20%, and morbidity (defined as the percentage of fish with indications of disease) that can be as high as 100% within affected populations (Kongtorp et al. 2004a). HSMI often occurs 5 to 9 months after transfer to seawater, occasionally in freshwater, and can last for several months (Kongtorp at el., 2009; Johansen at el., 2016).

In addition to morbidity, clinical signs may include accumulation of fluids in the body cavity (ascites), pale heart and liver, enlarged spleen and diffused, pinpoint hemorrhages in the internal organs (visceral petechiae). However, fish with HSMI do not necessarily all have the same clinical signs and during the early stages of the disease fish can appear healthy despite the presence of internal lesions. In Norway, the diagnosis of HSMI often occurs after fish have experienced a stressful event (Lovoll et al. 2012), as is true of many diseases.

Although field observations have suggested that surviving fish in affected sea cages may recover (unpublished field observations; Kongtorp et al., 2004a), non-lethal outbreaks are still considered a significant problem in Norwegian Atlantic salmon farming due to poor growth and general performance of fish following infection.

The disease HSMI is diagnosed by the occurrence of histopathologic lesions in the heart and skeletal muscle; moderate to severe panmyocarditis (inflammation in the compact and spongy layers of the myocardium); and myocardial degeneration and necrosis (Biering and Garseth 2012). The skeletal muscle also shows moderate to severe myodegeneration and necrosis of the red muscle fibres, as well as inflammation (Kongtorp et al. 2004a). Lesions in the skeletal muscle tend to occur mostly during the peak of the outbreak and, to a lesser extent, in the recovery phase (Kongtorp et al. 2006). Histopathological lesions in other organs include liver necrosis and congestion / hemorrhages in liver, kidney, spleen and gills (Kongtorp et al. 2004a).

PRV and association with disease

PRV was first identified through sequencing of heart tissue obtained from Atlantic Salmon (Salmo salar) farmed in Norway that displayed signs of HSMI and Cardiomyopathy Syndrome (Lovoll et al. 2010; Palacios et al. 2010).  PRV has consistently been observed concurrently with HSMI outbreaks on farms in Norway (Lovoll et al. 2012; Wiik-Nielsen et al. 2016)and injection of Norwegian Atlantic Salmon with PRV positive tissue homogenates from fish diagnosed with HSMI has, across multiple studies (Kongtorp et al. 2004a; Watanabe et al. 2006; Alne et al. 2009; Kongtorp and Taksdal 2009; Yousaf et al. 2014, Saddique 2014; Johansen et al. 2015; Johansen et al. 2016), resulted in the formation of heart and skeletal muscle lesions diagnostic of HSMI. 

Recently, PRV-like sequences were also found concurrently with three (HSMI-like) diseases in farmed salmonids: in Rainbow Trout in Norway, the disease grossly described as circulatory failure with haemorrhages and anaemia pathologically included liver necrosis and HSMI lesions (Olsen et al. 2015); in Coho Salmon in Chile, the disease grossly described as jaundice and anemia pathologically includes liver necrosis and HSMI-like lesions (Godoy et al. 2016) and; in farmed Coho Salmon in Japan with a condition noted as erythrocytic inclusion body syndrome (Takano et al. 2016).

Studies exposing Norwegian Atlantic salmon to purified PRV showed that exposed fish replicated virus and developed histophathological lesions diagnostic of HSMI, establishing PRV as the causative agent (Wessel et al 2017). Wessel et al. 2017 provides evidence that PRV infection can directly cause HSMI in Atlantic salmon yet acknowledges that it remains unclear as to why in many instances infections do not lead to disease.  In developing the ability to purify PRV, the authors have also made it possible for the research community to characterize potential PRV strain differences, host differences, and environmental factors required for disease development.

Investigations into infectivity and disease causing potential of PRV

For Norwegian PRV strains the causality of HSMI has been conclusively demonstrated, but the disease causing potential of the North America strains in native species is uncertain.   To date, surveys conducted in North America have revealed that the presence of PRV genetic material in wild and cultured Chinook, coho and pink salmon and steelhead trout from Washington State, BC and Alaska where years of surveillance have reported no presence of HSMI (Marty et al. 2015; Siah et al. 2015, Purcell et al. 2017 ). Further, although HSMI has been repeatedly transmitted to naïve fish in Norway via injection of PRV-infected material obtained from fish with HSMI (Finstad et al. 2012; Mikalsen et al. 2012; Finstad et al. 2014), similar transmission studies on the BC variant of PRV conducted at DFO have failed to generate disease in Atlantic, sockeye, or chinook salmon (Garver et al. 2016a; Garver et al. 2016b). The exposed Sockeye, Chinook, and Atlantic Salmon became infected and supported high levels in the blood similar to observations from Norwegian challenge studies. However, unlike in Norway, as yet, all experimental exposures of the BC strain of PRV to Pacific and Atlantic salmon in BC have failed to induce disease or mortality. This suggests PRV in BC has a low ability to cause disease (low virulence) for these species (Garver et al. 2016a; Garver et al. 2016b).

In a collaborative study led by researchers at the DFO Pacific Biological Station, it was revealed that sockeye salmon infected with PRV exhibit a lack of response to the virus at 2 and 3 weeks after infection even though substantial viral amplification occurred during this period (Polinski et al. 2016). In contrast, when sockeye salmon were infected with infectious hematopoietic necrosis virus (IHNV), a highly pathogenic rhabdovirus enzootic to the west coast of North America, substantial changes in host immune pathways were observed including antiviral and inflammatory responses. Moreover, when sockeye salmon infected with PRV were subsequently exposed to IHNV, the PRV infection had no significant effect on the sockeye's response to the superinfecting IHNV. Consequently, concurrent infections of PRV and IHNV do not appear to significantly influence the infectivity or severity of IHNV-associated disease in sockeye although timing of virus exposures may prove to be an important factor for determining inter-viral relationships (Polinski et al. 2016).

DFO scientists, along with provincial and international colleagues, are conducting investigations to better understand the biology of PRV and HSMI in wild and farmed salmon on the west coast of North America. Examples include studies assessing the association between PRV infections and spawning success of sockeye salmon in the Fraser River (Miller et al. 2014), the potential association of PRV with disease in Pacific salmon, and the assessment of infectious agents and histological evidence of disease in farmed, wild, and enhancement salmon. Studies are also investigating whether infection with PRV in the absence of HSMI would affect how a fish may respond when exposed to other naturally occurring viruses.

Di Cicco et al. 2017 documented the first farm-level diagnosis of HSMI in BC. The study showed inflammatory lesions in heart and skeletal muscle tissue diagnostic of this disease in a longitudinal study from one Atlantic Salmon farm in BC. At an individual level, not all fish carried lesions in both heart and skeletal muscle at any given point in time, but at the farm level, both were present and diagnostic of the disease. There was no associated elevation in mortalities reported at the farm level. While this study was not designed to prove or disprove a cause and effect relationship between PRV and HSMI, PRV was found to be correlated with the development of lesions diagnostic of HSMI and spatially located within the affected tissue, consistent with HSMI etiology from other countries. The finding of inflammatory (myocarditis) heart lesions in this study is consistent with heart lesions of suspected viral origin that have been reported through the DFO audit program since 2008, and from industry fish possibly as early as 2002, but never diagnosed to a specific disease.

This webpage will be updated with the results of significant new studies periodically.


References

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