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Pathogens
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Heart and Skeletal Muscle Inflammation (HSMI) and Other Effects of...
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Heart and Skeletal Muscle Inflammation (HSMI) and Other Effects of Piscine orthoreovirus (PRV) Infections in Salmonids

A special issue of Pathogens (ISSN 2076-0817).

Deadline for manuscript submissions: closed (31 May 2021) | Viewed by 18039

Special Issue Editors

Dr. Maria K. Dahle

E-Mail Website
Guest Editor
Senior Researcher, Fish Health Research Group, Norwegian Veterinary Institute, ÅS, Norway
Interests: biochemistry; molecular; immunology; inflammation; infection; fish health; aquaculture
Special Issues, Collections and Topics in MDPI journals
Prof. Dr. Espen Rimstad

E-Mail Website
Guest Editor
Faculty of Veterinary Medicine, Norwegian University of Life Sciences
Interests: PCR; Proteins; Fish Ecology; Fish Biology; Veterinary Diagnostics; Aquaculture; Veterinary Medicine; Fish Diseases; Ferret

Special Issue Information

Dear Colleagues,

Heart and skeletal muscle inflammation (HSMI) in Atlantic salmon was first characterized as a disease that caused mortality in Norwegian aquaculture in 1999. A decade later the disease was associated with Piscine orthoreovirus (PRV), now shown to be the causative agent. PRV is a non-enveloped segmented double-stranded RNA-virus that infects red blood cells, heart and skeletal muscle, spleen and kidney of the salmon, triggers inflammation in muscle tissue and increased mortality related to stress. PRV-infection is extremely common in salmonid aquaculture, and farmed Atlantic salmon become persistently infected. Not all genetic variants of PRV-1 (Atlantic salmon) are reported to induce disease. In recent years, several novel genotypes of PRV have been characterized and shown to trigger disease in other salmonid species, including PRV-2 in Japanese Coho salmon and PRV-3 in rainbow trout.

This special issue aims to collect new research related to the consequences of PRV infection in both farmed and wild salmonids, and welcome manuscripts on detection and prevalence, molecular characterization, pathogenesis of disease, diagnostic methods, virus-host interaction, cell-based studies, vaccine development and other means of disease prevention or infection control.

Dr. Maria K Dahle
Prof. Espen Rimstad
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Pathogens is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2700 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • Heart and skeletal muscle inflammation
  • salmon
  • Piscine orthoreovirus
  • red blood cells
  • virus persistence
  • viral infection
  • double-stranded RNA virus

Published Papers (5 papers)

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Research

22 pages, 10934 KiB  
Article
Piscine Orthoreovirus-1 Isolates Differ in Their Ability to Induce Heart and Skeletal Muscle Inflammation in Atlantic Salmon (Salmo salar)
by Øystein Wessel, Elisabeth F. Hansen, Maria K. Dahle, Marta Alarcon, Nina A. Vatne, Ingvild B. Nyman, Karen B. Soleim, Kannimuthu Dhamotharan, Gerrit Timmerhaus, Turhan Markussen, Morten Lund, Håvard Aanes, Magnus Devold, Makoto Inami, Marie Løvoll and Espen Rimstad
Pathogens 2020, 9(12), 1050; https://doi.org/10.3390/pathogens9121050 - 14 Dec 2020
Cited by 28 | Viewed by 5042
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 [...] Read more.
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. Full article
(This article belongs to the Special Issue Heart and Skeletal Muscle Inflammation (HSMI) and Other Effects of Piscine orthoreovirus (PRV) Infections in Salmonids)
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25 pages, 1620 KiB  
Article
Screening of Fish Cell Lines for Piscine Orthoreovirus-1 (PRV-1) Amplification: Identification of the Non-Supportive PRV-1 Invitrome
by Phuc H. Pham, Ehab Misk, Fotini Papazotos, Ginny Jones, Mark P. Polinski, Elena Contador, Spencer Russell, Kyle A. Garver, John S. Lumsden and Niels C. Bols
Pathogens 2020, 9(10), 833; https://doi.org/10.3390/pathogens9100833 - 12 Oct 2020
Cited by 17 | Viewed by 3272
Abstract
Piscine reovirus (PRV) is the causative agent of heart and skeletal muscle inflammation (HSMI), which is detrimental to Atlantic Salmon (AS) aquaculture, but so far has not been cultivatable, which impedes studying the disease and developing a vaccine. Homogenates of head kidney and [...] Read more.
Piscine reovirus (PRV) is the causative agent of heart and skeletal muscle inflammation (HSMI), which is detrimental to Atlantic Salmon (AS) aquaculture, but so far has not been cultivatable, which impedes studying the disease and developing a vaccine. Homogenates of head kidney and red blood cells (RBC) from AS in which PRV-1 had been detected were applied to fish cell lines. The cell lines were from embryos, and from brain, blood, fin, gill, gonads, gut, heart, kidney, liver, skin, and spleen, and had the shapes of endothelial, epithelial, fibroblast, and macrophage cells. Most cell lines were derived from the Neopterygii subclass of fish, but one was from subclass Chondrostei. Cultures were examined by phase contrast microscopy for appearance, and by quantitative polymerase chain reaction (qPCR) for PRV-1 RNA amplification and for the capacity to transfer any changes to new cultures. No changes in appearance and Ct values were observed consistently or transferable to new cultures. Therefore, 31 cell lines examined were unable to support PRV-1 amplification and are described as belonging to the non-supportive PRV-1 invitrome. However, these investigations and cell lines can contribute to understanding PRV-1 cellular and host tropism, and the interactions between virus-infected and bystander cells. Full article
(This article belongs to the Special Issue Heart and Skeletal Muscle Inflammation (HSMI) and Other Effects of Piscine orthoreovirus (PRV) Infections in Salmonids)
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20 pages, 2772 KiB  
Article
Emergence and Spread of Piscine orthoreovirus Genotype 3
by Juliane Sørensen, Niccolò Vendramin, Camilla Priess, Dhamotharan Kannimuthu, Niels Henrik Henriksen, Tine Moesgaard Iburg, Niels Jørgen Olesen and Argelia Cuenca
Pathogens 2020, 9(10), 823; https://doi.org/10.3390/pathogens9100823 - 07 Oct 2020
Cited by 8 | Viewed by 2661
Abstract
Piscine orthoreovirus (PRV) is a relevant pathogen for salmonid aquaculture worldwide. In 2015, a new genotype of PRV (genotype 3, PRV-3) was discovered in Norway, and in 2017 PRV-3 was detected for first time in Denmark in association with complex disease cases in [...] Read more.
Piscine orthoreovirus (PRV) is a relevant pathogen for salmonid aquaculture worldwide. In 2015, a new genotype of PRV (genotype 3, PRV-3) was discovered in Norway, and in 2017 PRV-3 was detected for first time in Denmark in association with complex disease cases in rainbow trout in recirculating aquaculture systems (RAS). To explore the epidemiology of PRV-3 in Denmark, a surveillance study was conducted in 2017 to 2019. Fifty-three farms, including both flow through and RAS, were screened for PRV-3. Of the farms examined, PRV-3 was detected in thirty-eight (71.7%), with the highest prevalence in grow-out farms. Notably, in Denmark disease outbreaks were only observed in RAS. Additionally, wild Atlantic salmon and brown trout populations were included in the screening, and PRV-3 was not detected in the three years where samples were obtained (2016, 2018, and 2019). Historical samples in the form of archived material at the Danish National Reference Laboratory for Fish Diseases were also tested for the presence of PRV-3, allowing us to establish that the virus has been present in Denmark at least since 1995. Sequence analyses of segment S1 and M2, as well as full genome analyses of selected isolates, did not reveal clear association between genetic makeup in these two segments and virulence in the form of disease outbreaks in the field. Full article
(This article belongs to the Special Issue Heart and Skeletal Muscle Inflammation (HSMI) and Other Effects of Piscine orthoreovirus (PRV) Infections in Salmonids)
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13 pages, 849 KiB  
Article
Health Surveillance of Wild Brown Trout (Salmo trutta fario) in the Czech Republic Revealed a Coexistence of Proliferative Kidney Disease and Piscine Orthoreovirus-3 Infection
by Ľubomír Pojezdal, Mikolaj Adamek, Eva Syrová, Dieter Steinhagen, Hana Minářová, Ivana Papežíková, Veronika Seidlová, Stanislava Reschová and Miroslava Palíková
Pathogens 2020, 9(8), 604; https://doi.org/10.3390/pathogens9080604 - 24 Jul 2020
Cited by 5 | Viewed by 2328
Abstract
The population of brown trout (Salmo trutta fario) in continental Europe is on the decline, with infectious diseases confirmed as one of the causative factors. However, no data on the epizootiological situation of wild fish in the Czech Republic are currently [...] Read more.
The population of brown trout (Salmo trutta fario) in continental Europe is on the decline, with infectious diseases confirmed as one of the causative factors. However, no data on the epizootiological situation of wild fish in the Czech Republic are currently available. In this study, brown trout (n = 260) from eight rivers were examined for the presence of viral and parasitical pathogens. Salmonid alphavirus-2, infectious pancreatic necrosis virus, piscine novirhabdovirus (VHSV) and salmonid novirhabdovirus (IHNV) were not detected using PCR. Cell culturing showed no viruses as well, and serological analysis of 110 sera did not detect any specific antibodies against VHSV or IHNV. Fish from two rivers were positive for the presence of piscine orthoreovirus-3 (PRV-3), subtype PRV-3b. However, none of the PRV-3-positive fish showed gross pathologies typically associated with PRV infections. By far the most widespread pathogen was Tetracapsuloides bryosalmonae which was confirmed in each of the examined locations, with a prevalence of up to 65% and 100%, as established by immunohistochemistry and PCR, respectively. Furthermore, up to 43.8% of fish showed signs of proliferative kidney disease caused by T. bryosalmonae, suggesting that this parasite is a main health challenge for brown trout in the Czech Republic. Full article
(This article belongs to the Special Issue Heart and Skeletal Muscle Inflammation (HSMI) and Other Effects of Piscine orthoreovirus (PRV) Infections in Salmonids)
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16 pages, 5193 KiB  
Article
Dissemination of Piscine orthoreovirus-1 (PRV-1) in Atlantic Salmon (Salmo salar) during the Early and Regenerating Phases of Infection
by Kannimuthu Dhamotharan, Håvard Bjørgen, Muhammad Salman Malik, Ingvild B. Nyman, Turhan Markussen, Maria K. Dahle, Erling Olaf Koppang, Øystein Wessel and Espen Rimstad
Pathogens 2020, 9(2), 143; https://doi.org/10.3390/pathogens9020143 - 20 Feb 2020
Cited by 11 | Viewed by 3504
Abstract
Piscine orthoreovirus-1 (PRV-1) can cause heart and skeletal muscle inflammation (HSMI) in farmed Atlantic salmon (Salmo salar), but the line of events from infection, pathologic change, and regeneration has not been thoroughly described. In this study, the cellular localization and variation [...] Read more.
Piscine orthoreovirus-1 (PRV-1) can cause heart and skeletal muscle inflammation (HSMI) in farmed Atlantic salmon (Salmo salar), but the line of events from infection, pathologic change, and regeneration has not been thoroughly described. In this study, the cellular localization and variation of PRV-1 RNA and protein levels were analyzed at different times post-exposure in experimentally infected Atlantic salmon. Immunohistochemistry, flow cytometry, and Western blot were used for assessment of the presence of the PRV-1 σ1 protein, while RT-qPCR and in situ hybridization were performed for viral RNA. Histopathologic evaluation demonstrated that PRV-1 infection induced heart lesions typical of HSMI, such as severe epicarditis and myocarditis with degeneration of cardiomyocytes, necrosis, and diffuse cellular infiltration. PRV-1 infection of erythrocytes and the peak viral plasma level preceded virus presence in cardiomyocytes and hepatocytes. Arginase-2-positive, macrophage-like cells observed in the heart indicated possible polarization to M2 macrophages and the onset of regenerative processes, which may contribute to the recovery from HSMI. The virus was cleared from regenerating heart tissue and from hepatocytes, but persisted in erythrocytes. Full article
(This article belongs to the Special Issue Heart and Skeletal Muscle Inflammation (HSMI) and Other Effects of Piscine orthoreovirus (PRV) Infections in Salmonids)
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