Piscine Reo-virus (PRV)
Fisheries and Oceans Canada (DFO) has received a number of inquiries regarding the presence of Piscine Reo-virus (PRV) on the Pacific Coast.
The Government of Canada has an internationally-recognized National Aquatic Animal Health Program (NAAHP) that is co-delivered with the Canadian Food Inspection Agency (CFIA) and Fisheries and Oceans Canada (DFO) under the authority of CFIA’s Health of Animals Act and Health of Animals Regulations. Under NAAHP, DFO’s National Aquatic Animal Health Laboratory System provides the diagnostic testing, research, and scientific advice regarding aquatic animal pathogens of finfish, molluscs, and crustaceans. As the primary regulator for aquaculture in British Columbia (BC), DFO works closely with the Canadian Food Inspection Agency (responsible for delivery of the National Aquatic Animal Health Program) as well as the aquaculture industry and other partners to identify and manage potential risks to the health of wild and farmed salmon.
Fisheries and Oceans Canada also engages in research associated with other microbes which may impact salmonids but are not listed in Acts and Regulations. A significant amount of research and science work has been and is continuing to be conducted regarding PRV. As a science-based Department, DFO draws both on existing scientific knowledge and conducts its own research and partners with others (such as with the Pacific Salmon Foundation and Genome BC on the Strategic Salmon Health Initiative) in researching reportable and emerging aquatic animal diseases.
The following summarizes DFO's current scientific understanding related to PRV and Heart and Skeletal Muscle Inflammation (HSMI). This information, as well as new and emerging science, will continue to inform our approach to the management of both wild fisheries and aquaculture in BC.
Piscine Reo-virus (PRV) in Norway and Internationally
Piscine Reo-virus (PRV) is a double stranded ribonucleic acid (RNA) virus related to the Reoviridae group. This virus was first identified through sequencing of heart tissue obtained from Atlantic Salmon (Salmo salar) farmed in Norway that displayed signs of two similar heart diseases, that is to say, Heart and Skeletal Muscle Inflammation (HSMI) and Cardiomyopathy Syndrome (CMS) (Palacios et al. 2010; Lovoll et al. 2010). More recently, PRV was found in association with HSMI lesions in farmed Atlantic salmon and HSMI-like lesions in farmed Coho Salmon in Chile (Godoy et al., 2016).
The disease HSMI was first observed by histology in 1999 in Atlantic Salmon farmed in Norway (Kongtorp et al., 2004). 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. Injection of Norwegian Atlantic Salmon with tissue homogenates from fish diagnosed with HSMI has, across multiple studies (Kongtorp et al. 2004; Watanabe et al. 2006; Alne et al. 2009, Kongtorp and Taksdal 2009; Yousaf et all. 2012; Finstad et al. 2014, Saddique 2014, Johansen et al. 2015, Johansen et al., 2016), resulted in the formation of heart and skeletal muscle lesions associated with HSMI. To date, HSMI has never been reproduced without the presence of PRV (Finstad 2014). While it is common for fish with HSMI to carry higher loads of PRV than disease-free fish (Finstad et al., 2012), high prevalence and load of PRV can be seen in apparently healthy fish with no or only low level of myocarditis lesions indicating that PRV may have a low virulence yet high replication ability (Wiik-Nielson et al., 2016). However, PRV is often localized within heart tissue in the region of inflammation and in affected cardiomyocytes (Finstad et al., 2012).
Because PRV has not yet been successfully cultured, a cause and effect relationship between PRV and HSMI in Atlantic Salmon farmed in Norway cannot be definitively established, but is still under investigation. Moreover, the fact that clinically healthy wild and farmed Atlantic Salmon collected from fresh and saltwater in Norway can also contain PRV, some with high loads, has led some researchers to question the role of PRV in the development of HSMI (Lovoll et al. 2012; Garseth et al. 2013; Marty et al. 2014). While the role of co-infection with other microbes and stress in the development of HSMI is under investigation (Garseth et al., 2013), it is apparent that PRV is present in both apparently healthy fish and fish with disease conditions other than HSMI (Wiik-Nielson et al., 2016).
PRV has, to date, not been cultured in cells and its presence in tissues can be detected only by molecular methods (e.g. RT-PCR; Palacios et al., 2010) or by immunohistochemistry (Finstad et al. 2012). Like many diseases, detection of an infectious agent alone does not equate with detection of a disease. As PRV can be observed at high levels in Atlantic Salmon returning to spawn in freshwater, without any signs of disease, the detection of PRV by molecular methods alone cannot be used as a diagnosis for the disease HSMI (Garseth et al. 2013). The international standard applied for the diagnosis of HSMI requires histological examination of changes in heart and skeletal muscle (Finstad et al. 2012) and is not based on mere presence of PRV or clinical signs of disease (Kongtorp et al., 2006).
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). This virus has been found in a variety of species of salmonid and non-salmonid fish. In North Atlantic waters these include farmed and wild Atlantic Salmon (Salmo salar), wild Sea-Trout (Salmo trutta), wild Great Silver Smelt (Argentina silus), wild Atlantic Horse Mackerel (Trachurus trachurus), wild Atlantic Herring (Clupea harengus) and wild Capelin (Mallotus villosus) (Wiik-Nielson et al. 2012; Garseth et al. 2013; Miller et al. 2014).
Piscine Reo-virus (PRV) on the West Coast of North America
PRV was first detected on the West Coast of North America through RT-PCR tests from farmed Chinook Salmon (Oncorhynchus tshawytscha) collected in British Columbia (K.M. Miller, pers. Comm). Since that time, additional survey work through various labs and agencies in Canada and the United States has expanded the known host range of PRV to include: wild Cutthroat Trout (Oncorhynchus clarkii), wild Chinook Salmon, wild Sockeye Salmon (O. nerka), wild Steelhead Trout (Oncorhynchus mykiss), wild Coho Salmon (Oncorhynchus kisutch), wild Chum Salmon (Oncorhynchus keta) and farmed Atlantic Salmon (DFO, 2015). These species have all tested positive for PRV through molecular testing.
Genomic sequencing of PRV from British Columbia revealed some genetic differences when compared to PRV from the North Atlantic and Chile (Kibenge et al. 2013). Based on an analysis of these genetic differences, these authors proposed that PRV first arrived in British Columbia 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 for a much longer time than reported in that paper (archival material from 1988 through to 1994 was found to be positive for PRV through molecular screening).
Based on laboratory studies, DFO scientists have been investigating the infectivity and disease causing potential of PRV. To date, DFO scientists have demonstrated that PRV from British Columbia can infect Sockeye salmon, Chinook salmon, and Atlantic salmon. After infection, PRV can reach high levels in the blood and is capable of being present in Chinook, Sockeye and Atlantic Salmon for many months without causing disease or mortality, suggesting PRV in British Columbia is of low virulence for these species (Garver et al. 2016A and Garver et al. 2016B)
Lesions diagnostic of HSMI associated with limited impact on farm productivity were recently reported on a salmon farm in BC using Histology to examine inflammatory pathology in heart and skeletal muscle tissue (unpublished data from the Strategic Salmon Health Initiative). This finding is consistent with heart and skeletal muscle lesions that have been reported through the DFO audit program from 2013-2015. However, the current study was able to follow the lesions over time in a population providing considerable insight into the progression of the condition. 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. DFO will continue to assess new information as it becomes available and update this web page accordingly.
As the role of PRV in the aquatic ecosystem is not well understood, DFO scientists, along with provincial and international colleagues, are conducting investigations to better understand the biology of PRV in wild and farmed salmon on the West Coast of North America. Examples include studies assessing the association between PRV infection and spawning success of Sockeye Salmon in the Fraser River, 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. Additionally, studies are investigating whether infection with PRV of no or low virulence would affect how a fish may respond when exposed to other naturally occurring viruses.
- Alne H, Thomassen MS, Takle H, Terjesen BF, Grammes F, Oehme M, Refstie S, Sigholt T, Berge RK, Rorvik KA. 2009. Increased survival by feeding tetradecylthioacetic acid during a natural outbreak of heart and skeletal muscle inflammation in S0 Atlantic salmon, Salmo salar L. J. Fish Dis. 32, 953–961.
- Biering E, Garseth AH. 2012. Heart and Skeletal Muscle Inflammation (HSMI) of Farmed Atlantic Salmon (Salmo salar L.) and the Associated Piscine Reovirus (PRV). In: Feist S, editor. ICES Identification Leaflets for Diseases and Parasites of Fish and Shellfish. Copenhagen: International Council for the Exploration of the Sea; p. 6.
- DFO. 2015. Assessment of the Occurrence, Distribution and Potential Impacts of Piscine Reovirus on the West Coast of North America. DFO Can. Sci. Advis. Sec. Sci. Resp. 2015/037.
- Ferguson HW, Kongtorp RT, Taksdal T, Graham D, and Falk K. 2005. An Outbreak of Disease Resembling Health and Skeletal Muscle Inflammation in Scottish Farmed Salmon, Salmo salar L., with Observations on Myocardial Regeneration. Journal of Fish Diseases 28:119-123.
- Finstad, OW, Falk K, Lovoll M, Evensen O, and Rimstad R. 2012. Immunohistochemical Detection of Piscine Reovirus (PRV) in Hearts of Atlantic Salmon Coincides with the Course of Heart and Skeletal Muscle Inflammation (HSMI). Veterinary Research. 43: 27.
- Finstad ØW: Pathogenesis of Piscine orthoreovirus (PRV) infection in Atlantic salmon (Salmo salar). Philosophiae Doctor (PhD) Thesis 2014:28. Norwegian University of Life Science; 2014.
- Finstad OW, Dahle MK, Lindholm TH, Nyman IB, Lovoll M, Wallace C, Olsen CM, Storset AK, Rimstad E. 2014. Piscine orthoreovirus (PRV) infects Atlantic salmon erythrocytes. Vet. Res. 45, 35.
- Garseth AH, Fritsvold C, Opheim M, Skjerve E and Biering E. 2013. Piscine Reovirus (PRV) in Wild Atlantic Salmon, Salmo salar L., and Sea-Trout, Salmo trutta L., in Norway. Journal of Fish Diseases 36,483-493.
- Garver KA, Marty GD, Cockburn SN, Richard J, Hawley LM, Müller A, et al. (2016A) Piscine reovirus, but not Jaundice Syndrome, was transmissible to Chinook Salmon, Oncorhynchus tshawytscha (Walbaum), Sockeye Salmon, Oncorhynchus nerka (Walbaum), and Atlantic Salmon, Salmo salar L. Journal of Fish Diseases 39,117-128.
- Garver KA, Johnson SC, Polinski MP, Bradshaw JC, Marty GD, Snyman HN, et al. (2016B) Piscine Orthoreovirus from Western North America Is Transmissible to Atlantic Salmon and Sockeye Salmon but Fails to Cause Heart and Skeletal Muscle Inflammation. PLoS ONE 11(1): e0146229. doi:10.1371/journal.pone.0146229
- Godoy MG, Kibenge MJT, Wang Y, Suarez R, Leiva C, Vallejos F and Kibenge FSB. 2016. First description of clinical presentation of piscine orthoreovirus (PRV) infections in salmonid aquaculture in Chile and identification of a second genotype (Genotype II) of PRV. Virology Journal 13:98 DOI 10.1186/s12985-016-0554-y.
- Johansen LH, Thim HL, Jorgensen SM, Afanasyev S, Strandskog G, Taksda T, Fremmerlid K, McLoughlin M, Jorgensen JB, Krasnov A. 2015. Comparison of transcriptomic responses to pancreas disease (PD) and heart and skeletal muscle inflammation (HSMI) in heart of Atlantic salmon (Salmo salar L.). Fish Shellfish Immunol. 46, 612–623.
- Johansen LH, Dahle MK, Wessel Ø, Timmerhaus G, Løvoll M, Røsæg M, Jørgensen SM, Rimstad E, Krasnov A. 2016. Differences in gene expression in Atlantic salmon parr and smolt after challenge with Piscine orthoreovirus (PRV). Molecular Immunology 73 138–150
- Kibenge MJT, Iwamoto T, Wang Y, Morton A, Godoy MG and Kibenge F. 2013. Whole-Genome Analysis of Piscine Reovirus (PRV) Shows PRV Represents a New Genus in Family Reoviridae and its Genome Segment S1 Sequences Group it into Two Separate Sub-Genotypes. Virology Journal 10:230.
- Kongtorp RT, Taksdal T, Lyngøy A. 2004. Pathology of Heart and Skeletal Muscle Inflammation (HSMI) in Farmed Atlantic salmon Salmo salar. Diseases of Aquatic Organisms 59:217-224.
- Kongtorp RT, Halse M, Taksdal T, Falk K. 2006. Longitudinal study of a natural outbreak of heart and skeletal muscle inflammation in Atlantic salmon, Salmo salar L. J. Fish Dis. 29, 233–244.
- Kongtorp RT & and Taksdal T. 2009. Studies with experimental transmission of heart and skeletal muscle inflammation in Atlantic salmon, Salmo salar L. J Fish Dis. 32, 253–262
- Løvoll M, Wiik-Nelson J, Grove S, Wiik-Nelson C, Kristoffersen AB, Faller R, Poppe T, Jung J, Pedamallu CS, Nederbragt AJ, Meyerson M, Rimstad E and Tengs T. 2010. A Novel Totivirus and Piscine Reovirus (PRV) in Atlantic Salmon (Salmo salar) with Cardiomyopathy Syndrome (CMS). Virology Journal 7:309.
- Løvoll M, Allercon M, Jensen BB, Taksdal AB, Kristoffersen AB, and Tengs T. 2012. Quantification of Piscine Reovirus (PRV) at different stages of Atlantic salmon Salmo salar production. Diseases of Aquatic Organisms 99:7-12.
- Marty, G.D., Morrison, D.B., Bidulka, J., Joseph, T. and Siah, A., 2015. Piscine reovirus in wild and farmed salmonids in British Columbia, Canada: 1974–2013. Journal of fish diseases, 38(8), pp.713-728.
- Mikalsen AB, Haugland O, Rode M, Solbakk IT, Evensen O. 2012. Atlantic salmon reovirus infection causes a CD8T cell myocarditis in Atlantic salmon (Salmo salar L.). PLoS One 7, e37269.
- Miller, K.M., Teffer, A., Tucker, S., Li, S., Schulze, A.D., Trudel, M., Juanes, F., Tabata, A., Kaukinen, K.H., Ginther, N.G. and Ming, T.J., 2014. Infectious disease, shifting climates, and opportunistic predators: cumulative factors potentially impacting wild salmon declines. Evolutionary applications 7(7), pp.812-855.
- Palacios G, Lovoll M, Tengs T, et al. 2010. Heart and Skeletal Muscle Inflammation of Farmed Salmon is Associated with Infection With a Novel Reovirus. PLOS One 5(7): e11487.
- Saddique MA. 2014. Study of the Piscine orthoreovirus (PRV) associated with heart and skeletal muscle inflammation (HSMI) in Atlantic salmon. Msc Thesis, Hedmark University College
- Watanabe K, Karlsen M, Devold M, Isdal E, Litlabo A, Nylund A. 2006. Virus-like particles associated with heart and skeletal muscle inflammation(HSMI). Dis. Aquat. Organ. 70, 183–192.
- Wiik-Nielsen CR, Løvoll M, Sandlund N, et al. 2012. First Detection of Piscine Reovirus (PRV) in Marine Fish Species. Diseases of Aquatic Organisms. 97:255-258.
- Wiik-Nielson J, Alarcon M, Bang Jensen B, Haugland O and Mikalsen AB. 2016. Viral co-infections in farmed Atlantic salmon, Salmo salar L., displaying myocarditis. Journal of Fish Diseases doi:10.1111/jfd.12487.
- Yousaf MN, Koppang EO, Skjødt K, Köllner B, Hordvik I, Zou J, Secombes C, Powell MD. 2012. Cardiac pathological changes of Atlantic salmon (Salmo salar L.) affected with heart and skeletal muscle inflammation (HSMI). Fish & Shellfish Immunology 33 (2012) 305e315
- Date modified: