Cargando…

Long-term persistence of piscine orthoreovirus-1 (PRV-1) infection during the pre-smolt stages of Atlantic salmon in freshwater

Piscine orthoreovirus (PRV) causes heart and skeletal muscle inflammation (HSMI) in farmed Atlantic salmon. During salmon production cycles, HSMI has predominantly been observed after seawater transfer. More recently, better surveillance and longitudinal studies have detected occurrences of PRV-1 in...

Descripción completa

Detalles Bibliográficos
Autores principales: Kannimuthu, Dhamotharan, Roh, HyeongJin, Peñaranda, Ma. Michelle D., Wessel, Øystein, Mæhle, Stig, Berhe, Ghebretnsae Dawit, Nordbø, Joachim, Kvamme, Bjørn Olav, Morton, H. Craig, Grove, Søren
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10463814/
https://www.ncbi.nlm.nih.gov/pubmed/37644605
http://dx.doi.org/10.1186/s13567-023-01201-w
_version_ 1785098320011591680
author Kannimuthu, Dhamotharan
Roh, HyeongJin
Peñaranda, Ma. Michelle D.
Wessel, Øystein
Mæhle, Stig
Berhe, Ghebretnsae Dawit
Nordbø, Joachim
Kvamme, Bjørn Olav
Morton, H. Craig
Grove, Søren
author_facet Kannimuthu, Dhamotharan
Roh, HyeongJin
Peñaranda, Ma. Michelle D.
Wessel, Øystein
Mæhle, Stig
Berhe, Ghebretnsae Dawit
Nordbø, Joachim
Kvamme, Bjørn Olav
Morton, H. Craig
Grove, Søren
author_sort Kannimuthu, Dhamotharan
collection PubMed
description Piscine orthoreovirus (PRV) causes heart and skeletal muscle inflammation (HSMI) in farmed Atlantic salmon. During salmon production cycles, HSMI has predominantly been observed after seawater transfer. More recently, better surveillance and longitudinal studies have detected occurrences of PRV-1 in freshwater broodstock farms and hatcheries. However, very little is known about the viral kinetics of PRV-1 or disease development of HSMI during these pre-smolt stages. In this study, we conducted a long-term PRV-1 challenge experiment to examine the profile of viral load, infectiousness and/or clearance in Atlantic salmon during their development from fry to parr stage. Atlantic salmon fry (mean weight: 1.1 ± 0.19 g) were infected with PRV-1 (high virulent variant) via intraperitoneal (IP) injection. The viral load reached a peak at 2–4 weeks post-challenge (wpc) in heart and muscle tissues. The virus was detected at relatively high levels in whole blood, spleen, and head kidney tissues until 65 wpc. Heart and muscle lesions typical of HSMI were clearly observed at 6 and 8 wpc but then subsided afterwards resolving inflammation. Innate and adaptive immune responses were elicited during the early/acute phase but returned to basal levels during the persistent phase of infection. Despite achieving high viremia, PRV-1 infection failed to cause any mortality during the 65-week virus challenge period. Cohabitation of PRV-1 infected fish (10 and 31 wpc) with naïve Atlantic salmon fry resulted in very low or no infection. Moreover, repeated chasing stress exposures did not affect the viral load or shedding of PRV-1 at 26 and 44 wpc. The present findings provide knowledge about PRV-1 infection in juvenile salmon and highlight the importance of continued monitoring and management to prevent and mitigate the PRV-1 infection in freshwater facilities. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13567-023-01201-w.
format Online
Article
Text
id pubmed-10463814
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-104638142023-08-30 Long-term persistence of piscine orthoreovirus-1 (PRV-1) infection during the pre-smolt stages of Atlantic salmon in freshwater Kannimuthu, Dhamotharan Roh, HyeongJin Peñaranda, Ma. Michelle D. Wessel, Øystein Mæhle, Stig Berhe, Ghebretnsae Dawit Nordbø, Joachim Kvamme, Bjørn Olav Morton, H. Craig Grove, Søren Vet Res Research Article Piscine orthoreovirus (PRV) causes heart and skeletal muscle inflammation (HSMI) in farmed Atlantic salmon. During salmon production cycles, HSMI has predominantly been observed after seawater transfer. More recently, better surveillance and longitudinal studies have detected occurrences of PRV-1 in freshwater broodstock farms and hatcheries. However, very little is known about the viral kinetics of PRV-1 or disease development of HSMI during these pre-smolt stages. In this study, we conducted a long-term PRV-1 challenge experiment to examine the profile of viral load, infectiousness and/or clearance in Atlantic salmon during their development from fry to parr stage. Atlantic salmon fry (mean weight: 1.1 ± 0.19 g) were infected with PRV-1 (high virulent variant) via intraperitoneal (IP) injection. The viral load reached a peak at 2–4 weeks post-challenge (wpc) in heart and muscle tissues. The virus was detected at relatively high levels in whole blood, spleen, and head kidney tissues until 65 wpc. Heart and muscle lesions typical of HSMI were clearly observed at 6 and 8 wpc but then subsided afterwards resolving inflammation. Innate and adaptive immune responses were elicited during the early/acute phase but returned to basal levels during the persistent phase of infection. Despite achieving high viremia, PRV-1 infection failed to cause any mortality during the 65-week virus challenge period. Cohabitation of PRV-1 infected fish (10 and 31 wpc) with naïve Atlantic salmon fry resulted in very low or no infection. Moreover, repeated chasing stress exposures did not affect the viral load or shedding of PRV-1 at 26 and 44 wpc. The present findings provide knowledge about PRV-1 infection in juvenile salmon and highlight the importance of continued monitoring and management to prevent and mitigate the PRV-1 infection in freshwater facilities. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13567-023-01201-w. BioMed Central 2023-08-29 2023 /pmc/articles/PMC10463814/ /pubmed/37644605 http://dx.doi.org/10.1186/s13567-023-01201-w Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Kannimuthu, Dhamotharan
Roh, HyeongJin
Peñaranda, Ma. Michelle D.
Wessel, Øystein
Mæhle, Stig
Berhe, Ghebretnsae Dawit
Nordbø, Joachim
Kvamme, Bjørn Olav
Morton, H. Craig
Grove, Søren
Long-term persistence of piscine orthoreovirus-1 (PRV-1) infection during the pre-smolt stages of Atlantic salmon in freshwater
title Long-term persistence of piscine orthoreovirus-1 (PRV-1) infection during the pre-smolt stages of Atlantic salmon in freshwater
title_full Long-term persistence of piscine orthoreovirus-1 (PRV-1) infection during the pre-smolt stages of Atlantic salmon in freshwater
title_fullStr Long-term persistence of piscine orthoreovirus-1 (PRV-1) infection during the pre-smolt stages of Atlantic salmon in freshwater
title_full_unstemmed Long-term persistence of piscine orthoreovirus-1 (PRV-1) infection during the pre-smolt stages of Atlantic salmon in freshwater
title_short Long-term persistence of piscine orthoreovirus-1 (PRV-1) infection during the pre-smolt stages of Atlantic salmon in freshwater
title_sort long-term persistence of piscine orthoreovirus-1 (prv-1) infection during the pre-smolt stages of atlantic salmon in freshwater
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10463814/
https://www.ncbi.nlm.nih.gov/pubmed/37644605
http://dx.doi.org/10.1186/s13567-023-01201-w
work_keys_str_mv AT kannimuthudhamotharan longtermpersistenceofpiscineorthoreovirus1prv1infectionduringthepresmoltstagesofatlanticsalmoninfreshwater
AT rohhyeongjin longtermpersistenceofpiscineorthoreovirus1prv1infectionduringthepresmoltstagesofatlanticsalmoninfreshwater
AT penarandamamichelled longtermpersistenceofpiscineorthoreovirus1prv1infectionduringthepresmoltstagesofatlanticsalmoninfreshwater
AT wesseløystein longtermpersistenceofpiscineorthoreovirus1prv1infectionduringthepresmoltstagesofatlanticsalmoninfreshwater
AT mæhlestig longtermpersistenceofpiscineorthoreovirus1prv1infectionduringthepresmoltstagesofatlanticsalmoninfreshwater
AT berheghebretnsaedawit longtermpersistenceofpiscineorthoreovirus1prv1infectionduringthepresmoltstagesofatlanticsalmoninfreshwater
AT nordbøjoachim longtermpersistenceofpiscineorthoreovirus1prv1infectionduringthepresmoltstagesofatlanticsalmoninfreshwater
AT kvammebjørnolav longtermpersistenceofpiscineorthoreovirus1prv1infectionduringthepresmoltstagesofatlanticsalmoninfreshwater
AT mortonhcraig longtermpersistenceofpiscineorthoreovirus1prv1infectionduringthepresmoltstagesofatlanticsalmoninfreshwater
AT grovesøren longtermpersistenceofpiscineorthoreovirus1prv1infectionduringthepresmoltstagesofatlanticsalmoninfreshwater