Heart and skeletal muscle inflammation (HSMI) disease diagnosed on a British Columbia salmon farm through a longitudinal farm study

Abstract

Heart and skeletal muscle inflammation (HSMI) is an emerging disease of marine-farmed Atlantic Salmon (Salmo salar), first recognized in 1999 in Norway, and later also reported in Scotland and Chile. We undertook a longitudinal study involving health evaluation over an entire marine production cycle on one salmon farm in British Columbia (Canada). In previous production cycles at this farm site and others in the vicinity, cardiac lesions not linked to a specific infectious agent or disease were identified. Histologic assessments of both live and moribund fish samples collected at the farm during the longitudinal study documented at the population level the development, peak, and recovery phases of HSMI. The fish underwent histopathological evaluation of all tissues, Twort’s Gram staining, immunohistochemistry, and molecular quantification in heart tissue of 44 agents known or suspected to cause disease in salmon. Our analysis showed evidence of HSMI histopathological lesions over an 11-month timespan, with the prevalence of lesions peaking at 80–100% in sampled fish, despite mild clinical signs with no associated elevation in mortalities reported at the farm level. Diffuse mononuclear inflammation and myodegeneration, consistent with HSMI, was the predominant histologic observation in affected heart and skeletal muscle. Infective agent monitoring identified three agents at high prevalence in salmon heart tissue, including Piscine orthoreovirus (PRV), and parasites Paranucleospora theridion and Kudoa thyrsites. However, PRV alone was statistically correlated with the occurrence and severity of histopathological lesions in the heart. Immunohistochemical staining further localized PRV throughout HSMI development, with the virus found mainly within red blood cells in early cases, moving into the cardiomyocytes within or, more often, on the periphery of the inflammatory reaction during the peak disease, and reducing to low or undetectable levels later in the production cycle. This study represents the first longitudinal assessment of HSMI in a salmon farm in British Columbia, providing new insights on the pathogenesis of the disease.

Molecular testing of adult Pacific salmon and trout (Oncorhynchus spp.) for several RNA viruses demonstrates widespread distribution of piscine orthoreovirus in Alaska and Washington

“…Surveys conducted in Norway indicate that PRV is widespread and is a consistent finding in Atlantic salmon diagnosed with HSMI, as well as in asymptomatic farmed and wild Atlantic salmon, sea trout ( Salmo trutta L.) and several marine fish species (Biering & Garseth, ; Garseth et al., ; Løvoll et al., ; Wiik‐Nielsen et al., ). Recently, HSMI was diagnosed in an Atlantic salmon farm in BC as part of a longitudinal study of a full production cycle; PRV was the only pathogen statistically associated with heart lesion presence and severity (Di Cicco et al., ). That study also reported that the fish were test negative for SAV and PMCV.…”

“…Controlled laboratory studies in Atlantic, Chinook and sockeye salmon indicate that North American strains of PRV are highly transmissible but infection with the virus did not lead to the development of HSMI (Garver, Johnson et al., ; Garver, Marty et al., ). However, HSMI has been diagnosed in fish from Atlantic salmon farms in BC (Di Cicco et al., ), and more controlled studies are needed to fully assess the differences obtained between laboratory studies and field observations of farmed BC salmon.…”

“…Since initiation of this study, others have confirmed that PRV is present in Pacific salmon and trout, as well as farmed Atlantic salmon, from the west coast of North America through molecular surveys (Kibenge et al., ; Marty, Morrison, Bidulka, Joseph, & Siah, ; Siah et al., ). Recently, HSMI was diagnosed in a BC Atlantic salmon farm during a longitudinal monitoring study (Di Cicco et al., ).…”

Hypoxia tolerance and responses to hypoxic stress during heart and skeletal muscle inflammation in Atlantic salmon (Salmo salar)

“…HSMI has also been reported in farmed Atlantic salmon in Scotland [3], Chile [4] and Canada [5]. The disease is characterized by panmyocarditis (including cellular epicarditis), myocyte necrosis and inflammation in red skeletal muscle [2].…”

Little evidence to suggest salmonid freshwater reservoirs of piscine orthoreovirus (PRV)

“…Heart and skeletal muscle inflammation (HSMI) is an important disease in marine production of farmed Atlantic salmon in Norway (Hjeltnes, Bang‐Jensen, Bornø, Haukaas, & Walde, ; Kongtorp, Kjerstad, Taksdal, Guttvik, & Falk, ). The disease has also been detected in Scotland (Ferguson, Kongtorp, Taksdal, Graham, & Falk, ), Chile (Godoy et al., ) and Canada (Di Cicco et al., ). In 2010, it was shown that HSMI is associated with piscine orthoreovirus (PRV) infection (Palacios et al., ), and in 2017, infection with purified PRV firmly demonstrated the causal relationship between PRV infection and HSMI in Atlantic salmon (Wessel et al., ).…”