Piscine Orthoreovirus-1 Isolates Differ in Their Ability to Induce Heart and Skeletal Muscle Inflammation in Atlantic Salmon (Salmo salar).

Øystein Wessel,Magnus Devold,Håvard Aanes,Nina A Vatne,Morten Lund,Espen Rimstad,Marta Alarcon,Turhan Markussen,Makoto Inami,Ingvild B Nyman,Karen B Soleim,Gerrit Timmerhaus,Kannimuthu Dhamotharan,Marie Løvoll,Maria K Dahle,Elisabeth F Hansen

doi:10.3390/pathogens9121050

Abstract

Piscine orthoreovirus 1 (PRV-1) is the causative agent of heart and skeletal muscle inflammation (HSMI) in farmed Atlantic salmon (Salmo salar). The virus is widespread in Atlantic salmon and was present in Norway long before the first description of HSMI in 1999. Furthermore, in Canada the virus is prevalent in farmed Atlantic salmon but HSMI is not and Canadian isolates have failed to reproduce HSMI experimentally. This has led to the hypothesis that there are virulence differences between PRV-1 isolates. In this study we performed a dose standardized challenge trial, comparing six PRV-1 isolates, including two Norwegian field isolates from 2018, three historical Norwegian isolates predating the first report of HSMI and one Canadian isolate. The Norwegian 2018 isolates induced lower viral protein load in blood cells but higher plasma viremia. Following peak replication in blood, the two Norwegian 2018 isolates induced histopathological lesions in the heart consistent with HSMI, whereas all three historical Norwegian and the Canadian isolates induced only mild cardiac lesions. This is the first demonstration of virulence differences between PRV-1 isolates and the phenotypic differences are linked to viral proteins encoded by segment S1, M2, L1, L2 and S4.

Highlights

Piscine orthoreovirus 1 (PRV-1) is the causative agent of heart and skeletal muscle inflammation (HSMI), an important disease in farmed Atlantic salmon (Salmo salar) [1,2,3]
Six PRV-1 isolates were compared in a standardized challenge trial: two Norwegian field isolates collected from farmed Atlantic salmon in 2018 (NOR-2018/SF, NOR-2018/NL), three historical
All groups reached the peak of infection at 3–4 weeks post challenge but the viral load was significantly lower in the two NOR-2018 isolates (NOR-2018/SF, NOR-2018/NL), compared to the historical Norwegian (NOR-1997, NOR-1996, NOR-1988) and the Canadian isolate (CAN 16-005ND)

Summary

Introduction

Piscine orthoreovirus 1 (PRV-1) is the causative agent of heart and skeletal muscle inflammation (HSMI), an important disease in farmed Atlantic salmon (Salmo salar) [1,2,3]. All PRV-1 infected fish do not develop HSMI. This indicates that unknown viral, host or environmental factors are important for disease development. In 1999, the first outbreak of HSMI was described in farmed Atlantic salmon in Norway [1]. The disease spread along the coast and is causing numerous outbreaks each year in Norway [4]. The disease is characterized mainly by inflammation in the heart and skeletal muscle, Pathogens 2020, 9, 1050; doi:10.3390/pathogens9121050 www.mdpi.com/journal/pathogens

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