Piscine Orthoreovirus (PRV)-3, but Not PRV-2, Cross-Protects against PRV-1 and Heart and Skeletal Muscle Inflammation in Atlantic Salmon.

Muhammad Salman Malik,Anne Berit Olsen,Eva Stina Edholm,Jorunn B Jørgensen,Monica Nordberg,Stine Braaen,Tomokazu Takano,Steingrim Svenning,Lena H Teige,Marit M Amundsen,Øystein Wessel,Espen Rimstad,Maria K Dahle,Kannimuthu Dhamotharan

doi:10.3390/vaccines9030230

Abstract

Heart and skeletal muscle inflammation (HSMI), caused by infection with Piscine orthoreovirus-1 (PRV-1), is a common disease in farmed Atlantic salmon (Salmo salar). Both an inactivated whole virus vaccine and a DNA vaccine have previously been tested experimentally against HSMI and demonstrated to give partial but not full protection. To understand the mechanisms involved in protection against HSMI and evaluate the potential of live attenuated vaccine strategies, we set up a cross-protection experiment using PRV genotypes not associated with disease development in Atlantic salmon. The three known genotypes of PRV differ in their preference of salmonid host species. The main target species for PRV-1 is Atlantic salmon. Coho salmon (Oncorhynchus kisutch) is the target species for PRV-2, where the infection may induce erythrocytic inclusion body syndrome (EIBS). PRV-3 is associated with heart pathology and anemia in rainbow trout, but brown trout (S. trutta) is the likely natural main host species. Here, we tested if primary infection with PRV-2 or PRV-3 in Atlantic salmon could induce protection against secondary PRV-1 infection, in comparison with an adjuvanted, inactivated PRV-1 vaccine. Viral kinetics, production of cross-reactive antibodies, and protection against HSMI were studied. PRV-3, and to a low extent PRV-2, induced antibodies cross-reacting with the PRV-1 σ1 protein, whereas no specific antibodies were detected after vaccination with inactivated PRV-1. Ten weeks after immunization, the fish were challenged through cohabitation with PRV-1-infected shedder fish. A primary PRV-3 infection completely blocked PRV-1 infection, while PRV-2 only reduced PRV-1 infection levels and the severity of HSMI pathology in a few individuals. This study indicates that infection with non-pathogenic, replicating PRV could be a future strategy to protect farmed salmon from HSMI.

Highlights

Infections represent a constant challenge and threat against fish health and welfare in aquaculture
The results show that Piscine orthoreovirus (PRV)-3 infection in Atlantic salmon, in contrast to PRV-2, blocks a secondary infection with Piscine orthoreovirus-1 (PRV-1), and that cross-protective antibodies may be one of the mechanism involved
We found a contradictory effect on PRV-1 infection and Heart and skeletal muscle inflammation (HSMI)

Summary

Introduction

Infections represent a constant challenge and threat against fish health and welfare in aquaculture. Modern farming of Atlantic salmon (Salmo salar) is characterized by highdensity populations, rapid growth, short production cycles, and artificial adaptation to sea water. This life cycle does not ensure natural pathogen exposure in early life or the natural training of the fish innate immune system [1]. High-density populations increase infection pressure, and transportation and handling procedures increase disease susceptibility due to stress [2]. In Atlantic salmon aquaculture, vaccines have been effective in protecting the fish from many diseases, but several viral diseases remain unsolved challenges [3].

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