High-Load Reovirus Infections Do Not Imply Physiological Impairment in Salmon

Abstract

The recent ubiquitous detection of PRV among salmonids has sparked international concern about the cardiorespiratory performance of infected wild and farmed salmon. Piscine orthoreovirus (PRV) has been shown to create substantial viremia in salmon by targeting erythrocytes for principle replication. In some instances, infections develop into heart and skeletal muscle inflammation (HSMI) or other pathological conditions affecting the respiratory system. Critical to assessing the seriousness of PRV infections are controlled infection studies that measure physiological impairment to critical life support systems. Respiratory performance is such a system and here multiple indices were measured to test the hypothesis that a low-virulence strain of PRV from Pacific Canada compromises the cardiorespiratory capabilities of Atlantic salmon. Contrary to this hypothesis, the oxygen affinity and carrying capacity of erythrocytes were unaffected by PRV despite the presence of severe viremia, minor heart pathology and transient cellular activation of antiviral response pathways. Similarly, PRV-infected fish had neither sustained nor appreciable differences in respiratory capabilities compared with control fish. The lack of functional harm to salmon infected with PRV in this instance highlights that, in an era of unprecedented virus discovery, detection of viral infection does not necessarily imply bodily harm and that viral load is not always a suitable predictor of disease within a host organism.

Cross‐sectional study of histopathology and piscine orthoreovirus during a marine production cycle of farmed Atlantic salmon (Salmo salar L.) in British Columbia, Canada

“…None of these historic findings from BC were associated with cardiopathy. Controlled laboratory challenge with BC PRV-1 and Atlantic salmon causes minor heart lesions in a small proportion of the exposed fish, but lesion severity in the exposed fish is not sufficient to diagnose HSMI (Garver et al, 2016;Polinski, Marty, Snyman, & Garver, 2019) or impair cardiorespiratory function (Zhang et al, 2019).…”

Piscine orthoreovirus: Biology and distribution in farmed and wild fish

“…(b, c) Contrast summary for general trends in PRV phenotypic infection dynamics between Norway and Canada laboratory challenge of Atlantic Salmon (adapted from Polinski et al., 2019). In comparing challenge trials conducted in (b) Pacific Canada (Garver, Johnson, et al, 2016; Polinski et al., 2019; Zhang et al., 2019) with results from similar challenge trials conducted in (c) Norway (Finstad et al., 2014; Haatveit et al., 2017; Lund et al., 2017; Mikalsen et al., 2012; Wessel et al., 2017). Note that variance in experimental design exists between studies…”

“…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).…”

“…Similar to MRV, the majority of PRV infections do not appear to directly lyse the infected cells (Finstad et al., 2014; Polinski et al., 2019; Wessel, Olsen, et al, 2015). Rather, the pathogenic potential of PRV likely stems from the host‐directed killing of infected cells via an adaptive (T‐cell‐mediated) immune response (Mikalsen et al., 2012; Yousaf et al., 2012; Zhang et al., 2019). In some instances, this appears to result in immune cells targeting infected cardiomyocytes and cardiac epithelial cells such as during HSMI (Figure 4) (Mikalsen et al., 2012).…”

“…In others instances, infected erythrocytes have been suggested to become targeted for destruction and filtered out while passing through the liver or spleen resulting in reduced haematocrits or anaemia, such as possibly during erythrocytic inclusion body syndrome (EIBS) in Coho Salmon of Japan (Takano et al., 2016) or jaundice syndrome of Chinook Salmon ( Oncorhynchus tschawytscha ) in western North America (Di Cicco et al., 2018). The mechanisms for initiating these adaptive host responses to PRV (if they can be confirmed) are unknown, and it is also unclear why some cell types are more selectively targeted for destruction than others in different instances; for example, cardiomyocytes and not erythrocytes in Atlantic Salmon even though erythrocytes are the primary cell type infected (Zhang et al., 2019). Recent preliminary investigations have suggested that mechanisms of PRV pathogenesis are highly variable with regard to the host species, host strain (possibly even the individual), and to the PRV isolate involved (Polinski, Braceland, Booman, & Garver, 2018; Wessel, Dahle, et al, 2018).…”