Consequences of Piscine orthoreovirus genotype 1 (PRV‐1) infections in Chinook salmon (Oncorhynchus tshawytscha), coho salmon (O. kisutch) and rainbow trout (O. mykiss)

Abstract

Piscine orthoreovirus genotype 1 (PRV‐1) is the causative agent of heart and skeletal muscle inflammation (HSMI) in farmed Atlantic salmon (Salmo salar L.). The virus has also been found in Pacific salmonids in western North America, raising concerns about the risk to native salmon and trout. Here, we report the results of laboratory challenges using juvenile Chinook salmon, coho salmon and rainbow trout injected with tissue homogenates from Atlantic salmon testing positive for PRV‐1 or with control material. Fish were sampled at intervals to assess viral RNA transcript levels, haematocrit, erythrocytic inclusions and histopathology. While PRV‐1 replicated in all species, there was negligible mortality in any group. We observed a few erythrocytic inclusion bodies in fish from the PRV‐1‐infected groups. At a few time points, haematocrits were significantly lower in the PRV‐1‐infected groups relative to controls, but in no case was anaemia noted. The most common histopathological finding was mild, focal myocarditis in both the non‐infected controls and PRV‐1‐infected fish. All cardiac lesions were judged mild, and none were consistent with those of HSMI. Together, these results suggest all three species are susceptible to PRV‐1 infection, but in no case did infection cause notable disease in these experiments.

Piscine orthoreovirus: Biology and distribution in farmed and wild fish

“…Of particular note in considering PRV‐2 relative to other PRV genogroups is the staggering quantity of virus generated during peak infection (approximately one trillion reverse‐transcribed genomic copies per mL blood) in both experimentally and naturally infected fish (Takano et al., 2016). These quantities appear to be 10–1,000 times greater than peak loads generated during robust PRV‐1 infections of Atlantic Salmon (Garver, Johnson, et al, 2016; Polinski et al., 2019; Zhang et al., 2019) and at least 1,000–10,000 times higher than the most extreme PRV‐1 infections reported in Pacific Sockeye (Polinski et al., 2016), Coho, Chinook Salmon or Rainbow Trout (Purcell et al., 2020).…”

“…Some experiments with Pacific ( Oncorhynchus sp.) salmon have also indicated a potential for a reduced haematocrit to occur during this period in some species (Purcell et al., 2020; Takano et al., 2016).…”

“…Namely, its impact varies widely from region to region and its ubiquitous nature is often associated with diseases for which a causative link cannot be established. It should be noted that in controlled experimental trials, PRV has (as yet) never caused clinical morbidity or mortality in salmon even during extreme blood infections (Garver, Johnson, et al, 2016; Polinski et al., 2019; Purcell et al., 2020; Takano et al., 2016; Wessel et al., 2017), nor has it contributed to clinical morbidity or mortality during experimental trials in accompaniment with stressors such as smoltification, viral co‐infection, hypoxia, or exhaustive chasing (Garver, Johnson, et al, 2016; Lund et al., 2016, 2017; Polinski et al., 2016; Zhang et al., 2019). However, this does not negate the fact that all three genogroups of PRV can at the very least cause mild to moderate disease in an experimental setting and almost certainly contribute to clinical disease states in farmed salmon stocks, which in some situations result in significant morbidity or mortality (Olsen et al., 2015; Takano et al., 2016; Vendramin, Kannimuthu, et al, 2019; Wessel et al., 2017).…”

“…Although it is probable that PRV‐1a can and occasionally does contribute to both conditions, the role for how or if PRV‐1a acts as the aetiological mediator of these relatively rare diseases in Pacific Canada is far from clear. Specifically, neither the jaundice/anaemia syndrome nor severe cardiomyopathy has been successfully transmitted to naive Chinook or Atlantic Salmon in laboratory challenge trials in Pacific Canada and Washington state despite the successful passage and development of high‐load PRV blood infections within both species (Garver, Marty, et al, 2016; Polinski et al., 2019; Purcell et al., 2020). This type of passage experiment is not only critical for establishing and identifying pathogenicity of a microbial agent (Fredericks & Relman, 1996) but also is what has been used to establish PRV‐1's ability to cause HSMI in Norway (Wessel et al., 2017).…”

“…Two farm‐level cases of HSMI‐like disease have been suggested to date (Di Cicco et al., 2017; Polinski et al., 2019), but unlike in Norway, this disease could not be transmitted to naïve fish in a laboratory setting (Polinski et al., 2019). Indeed, PRV‐1a has failed to cause severe heart lesions or any severity of skeletal muscle inflammation following experimental challenge of Atlantic or Pacific salmon in Western North America (Garver, Johnson, et al, 2016; Polinski et al., 2019; Purcell et al., 2020; Zhang et al., 2019). Ongoing laboratory investigations directly comparing PRV‐1 isolated in both Norway (a PRV‐1b subtype) and the Eastern Pacific (a PRV‐1a subtype) have also preliminarily identified that the PRV‐1a from the Eastern Pacific is of lower virulence to Norwegian Atlantic Salmon (Wessel, Dahle, et al, 2018).…”