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

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.

Download Full-text

Evolution of the Piscine orthoreovirus Genome Linked to Emergence of Heart and Skeletal Muscle Inflammation in Farmed Atlantic Salmon (Salmo salar)

Viruses ◽

10.3390/v11050465 ◽

2019 ◽

Vol 11 (5) ◽

pp. 465 ◽

Cited By ~ 10

Author(s):

Kannimuthu Dhamotharan ◽

Torstein Tengs ◽

Øystein Wessel ◽

Stine Braaen ◽

Ingvild B. Nyman ◽

...

Keyword(s):

Skeletal Muscle ◽

Atlantic Salmon ◽

Salmo Salar ◽

Muscle Inflammation ◽

Atlantic Salmon Salmo Salar ◽

The North ◽

Farmed Atlantic Salmon ◽

Associated Pair ◽

Viral Sequences ◽

Selection Of

Heart and skeletal muscle inflammation (HSMI) in farmed Atlantic salmon (Salmo salar) was first diagnosed in Norway in 1999. The disease is caused by Piscine orthoreovirus-1 (PRV-1). The virus is prevalent in farmed Atlantic salmon, but not always associated with disease. Phylogeny and sequence analyses of 31 PRV-1 genomes collected over a 30-year period from fish with or without HSMI, grouped the viral sequences into two main monophylogenetic clusters, one associated with HSMI and the other with low virulent PRV-1 isolates. A PRV-1 strain from Norway sampled in 1988, a decade before the emergence of HSMI, grouped with the low virulent HSMI cluster. The two distinct monophylogenetic clusters were particularly evident for segments S1 and M2. Only a limited number of amino acids were unique to the association with HSMI, and they all located to S1 and M2 encoded proteins. The observed co-evolution of the S1-M2 pair coincided in time with the emergence of HSMI in Norway, and may have evolved through accumulation of mutations and/or segment reassortment. Sequences of S1-M2 suggest selection of the HSMI associated pair, and that this segment pair has remained almost unchanged in Norwegian salmon aquaculture since 1997. PRV-1 strains from the North American Pacific Coast and Faroe Islands have not undergone this evolution, and are more closely related to the PRV-1 precursor strains not associated with clinical HSMI.

Download Full-text

Longitudinal study of a natural outbreak of heart and skeletal muscle inflammation in Atlantic salmon, Salmo salar L.

Journal of Fish Diseases ◽

10.1111/j.1365-2761.2006.00710.x ◽

2006 ◽

Vol 29 (4) ◽

pp. 233-244 ◽

Cited By ~ 56

Author(s):

R T Kongtorp ◽

M Halse ◽

T Taksdal ◽

K Falk

Keyword(s):

Skeletal Muscle ◽

Longitudinal Study ◽

Atlantic Salmon ◽

Salmo Salar ◽

Muscle Inflammation ◽

Atlantic Salmon Salmo Salar ◽

Natural Outbreak

Download Full-text

Studies with experimental transmission of heart and skeletal muscle inflammation in Atlantic salmon,Salmo salarL.

Journal of Fish Diseases ◽

10.1111/j.1365-2761.2008.00983.x ◽

2009 ◽

Vol 32 (3) ◽

pp. 253-262 ◽

Cited By ~ 26

Author(s):

R T Kongtorp ◽

T Taksdal

Keyword(s):

Skeletal Muscle ◽

Atlantic Salmon ◽

Experimental Transmission ◽

Muscle Inflammation

Download Full-text

The Effects of Heart and Skeletal Muscle Inflammation and Cardiomyopathy Syndrome on Creatine Kinase and Lactate Dehydrogenase Levels in Atlantic Salmon (Salmo salarL.)

The Scientific World JOURNAL ◽

10.1100/2012/741302 ◽

2012 ◽

Vol 2012 ◽

pp. 1-9 ◽

Cited By ~ 13

Author(s):

Muhammad Naveed Yousaf ◽

Mark D. Powell

Keyword(s):

Skeletal Muscle ◽

Creatine Kinase ◽

Lactate Dehydrogenase ◽

Atlantic Salmon ◽

Serum Enzymes ◽

Muscle Inflammation ◽

Study Population ◽

Positive Correlations ◽

Farmed Atlantic Salmon ◽

Potential Use

Heart and skeletal muscle inflammation (HSMI) and cardiomyopathy syndrome (CMS) are putative viral cardiac diseases of Atlantic salmon. This study examined the levels and correlated the serum enzymes creatine kinase (CK) and lactate dehydrogenase (LDH) to the histopathology of clinical outbreaks of HSMI and chronic CMS in farmed Atlantic salmon. A total of 75 fish from 3 different HSMI outbreaks, 30 chronic CMS fish, and 68 fish from 3 nondiseased fish groups were used as the study population (N=173). Serum CK and LDH levels correlated significantly with the total inflammation and total necrosis scores for HSMI fish (P=0.001). However, no correlation was identified for enzyme levels and histopathology scores for chronic CMS fish. The significantly increased CK and LDH levels and their positive correlations to histopathology differentiate HSMI from CMS clinically suggesting the potential use of enzymes for screening for HSMI is promising.

Download Full-text

Pathology of heart and skeletal muscle inflammation (HSMI) in farmed Atlantic salmon Salmo salar

Diseases of Aquatic Organisms ◽

10.3354/dao059217 ◽

2004 ◽

Vol 59 ◽

pp. 217-224 ◽

Cited By ~ 90

Author(s):

RT Kongtorp ◽

T Taksdal ◽

A Lyngøy

Keyword(s):

Skeletal Muscle ◽

Atlantic Salmon ◽

Salmo Salar ◽

Muscle Inflammation ◽

Atlantic Salmon Salmo Salar ◽

Farmed Atlantic Salmon

Download Full-text

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

Pathogens ◽

10.3390/pathogens9121050 ◽

2020 ◽

Vol 9 (12) ◽

pp. 1050 ◽

Cited By ~ 1

Author(s):

Øystein Wessel ◽

Elisabeth F. Hansen ◽

Maria K. Dahle ◽

Marta Alarcon ◽

Nina A. Vatne ◽

...

Keyword(s):

Skeletal Muscle ◽

Atlantic Salmon ◽

Salmo Salar ◽

Phenotypic Differences ◽

Muscle Inflammation ◽

Atlantic Salmon Salmo Salar ◽

Canadian Isolate ◽

Cardiac Lesions ◽

Farmed Atlantic Salmon ◽

Protein Load

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.

Download Full-text