Abstract

Heart and skeletal muscle inflammation (HSMI) is a significant and often fatal disease of cultured Atlantic salmon in Norway. The consistent presence of Piscine orthoreovirus (PRV) in HSMI diseased fish along with the correlation of viral load and antigen with development of lesions has supported the supposition that PRV is the etiologic agent of this condition; yet the absence of an in vitro culture system to demonstrate disease causation and the widespread prevalence of this virus in the absence of disease continues to obfuscate the etiological role of PRV with regard to HSMI. In this study, we explore the infectivity and disease causing potential of PRV from western North America—a region now considered endemic for PRV but without manifestation of HSMI—in challenge experiments modeled upon previous reports associating PRV with HSMI. We identified that western North American PRV is highly infective by intraperitoneal injection in Atlantic salmon as well as through cohabitation of both Atlantic and Sockeye salmon. High prevalence of viral RNA in peripheral blood of infected fish persisted for as long as 59 weeks post-challenge. Nevertheless, no microscopic lesions, disease, or mortality could be attributed to the presence of PRV, and only a minor transcriptional induction of the antiviral Mx gene occurred in blood and kidney samples during log-linear replication of viral RNA. Comparative analysis of the S1 segment of PRV identified high similarity between this North American sequence and previous sequences associated with HSMI, suggesting that factors such as viral co-infection, alternate PRV strains, host condition, or specific environmental circumstances may be required to cause this disease.

Highlights

  • In 1999, a new and emerging disease syndrome was described by the observation of a unique set of pathological changes in the heart and skeletal muscles of farmed Atlantic salmon Salmo salar in Norway [1,2]

  • During this challenge the fish did not develop changes in hematocrit, heart and skeletal muscle inflammation (HSMI), increased mortality, or other signs of disease attributable to piscine orthoreovirus (PRV) infection (details of histopathological findings are in supporting information (S1 File); details of the entire sample inventory including viral load, hematocrit, and mortality results are in supporting information (S2 File))

  • A complete lack of associated lesions and mortality in infected populations exhibiting high viral loads indicates that western North American PRV is non-pathogenic

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Summary

Introduction

In 1999, a new and emerging disease syndrome was described by the observation of a unique set of pathological changes in the heart and skeletal muscles of farmed Atlantic salmon Salmo salar in Norway [1,2]. This disease, designated heart and skeletal muscle inflammation (HSMI), has become widespread and common among the Atlantic salmon farming industry in Norway and is known to cause increased mortalities as well as high morbidity that can reach upwards of 100% in affected cages [1,3]. Through the use of pyrosequencing, a novel virus denoted piscine orthoreovirus (PRV) was discovered in Atlantic salmon with HSMI [9]

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