Hypoxia tolerance and responses to hypoxic stress during heart and skeletal muscle inflammation in Atlantic salmon (Salmo salar)

Heart and skeletal muscle inflammation (HSMI) is associated with Piscine orthoreovirus (PRV) infection and is an important disease in Atlantic salmon (Salmo salar) aquaculture. Since PRV infects erythrocytes and farmed salmon frequently experience environmental hypoxia, the current study examined mu...

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Published in:PLOS ONE
Main Authors: Lund, Morten, Krudtaa Dahle, Maria, Timmerhaus, Gerrit, Alarcon, Marta, Powell, Mark, Aspehaug, Vidar, Rimstad, Espen, Jørgensen, Sven Martin
Format: Text
Language:English
Published: Public Library of Science 2017
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Online Access:http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5507449/
http://www.ncbi.nlm.nih.gov/pubmed/28700748
https://doi.org/10.1371/journal.pone.0181109
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spelling ftpubmed:oai:pubmedcentral.nih.gov:5507449 2023-05-15T15:31:05+02:00 Hypoxia tolerance and responses to hypoxic stress during heart and skeletal muscle inflammation in Atlantic salmon (Salmo salar) Lund, Morten Krudtaa Dahle, Maria Timmerhaus, Gerrit Alarcon, Marta Powell, Mark Aspehaug, Vidar Rimstad, Espen Jørgensen, Sven Martin 2017-07-11 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5507449/ http://www.ncbi.nlm.nih.gov/pubmed/28700748 https://doi.org/10.1371/journal.pone.0181109 en eng Public Library of Science http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5507449/ http://www.ncbi.nlm.nih.gov/pubmed/28700748 http://dx.doi.org/10.1371/journal.pone.0181109 © 2017 Lund et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. CC-BY Research Article Text 2017 ftpubmed https://doi.org/10.1371/journal.pone.0181109 2017-07-30T00:06:29Z Heart and skeletal muscle inflammation (HSMI) is associated with Piscine orthoreovirus (PRV) infection and is an important disease in Atlantic salmon (Salmo salar) aquaculture. Since PRV infects erythrocytes and farmed salmon frequently experience environmental hypoxia, the current study examined mutual effects of PRV infection and hypoxia on pathogenesis and fish performance. Furthermore, effects of HSMI on hypoxia tolerance, cardiorespiratory performance and blood oxygen transport were studied. A cohabitation trial including PRV-infected post-smolts exposed to periodic hypoxic stress (4 h of 40% O2; PRV-H) at 4, 7 and 10 weeks post-infection (WPI) and infected fish reared under normoxic conditions (PRV) was conducted. Periodic hypoxic stress did not influence infection levels or histopathological changes in the heart. Individual incipient lethal oxygen saturation (ILOS) was examined using a standardized hypoxia challenge test (HCT). At 7 WPI, i.e. peak level of infection, both PRV and PRV-H groups exhibited reduced hypoxia tolerance compared to non-infected fish. Three weeks later (10 WPI), during peak levels of pathological changes, reduced hypoxia tolerance was still observed for the PRV group while PRV-H performed equal to non-infected fish, implying a positive effect of the repeated exposure to hypoxic stress. This was in line with maximum heart rate (fHmax) measurements, showing equal performance of PRV-H and non-infected groups, but lower fHmax above 19°C as well as lower temperature optimum (Topt) for aerobic scope for PRV, suggesting reduced cardiac performance and thermal tolerance. In contrast, the PRV-H group had reduced hemoglobin-oxygen affinity compared to non-infected fish. In conclusion, Atlantic salmon suffering from HSMI have reduced hypoxia tolerance and cardiac performance, which can be improved by preconditioning fish to transient hypoxic stress episodes. Text Atlantic salmon Salmo salar PubMed Central (PMC) PLOS ONE 12 7 e0181109
institution Open Polar
collection PubMed Central (PMC)
op_collection_id ftpubmed
language English
topic Research Article
spellingShingle Research Article
Lund, Morten
Krudtaa Dahle, Maria
Timmerhaus, Gerrit
Alarcon, Marta
Powell, Mark
Aspehaug, Vidar
Rimstad, Espen
Jørgensen, Sven Martin
Hypoxia tolerance and responses to hypoxic stress during heart and skeletal muscle inflammation in Atlantic salmon (Salmo salar)
topic_facet Research Article
description Heart and skeletal muscle inflammation (HSMI) is associated with Piscine orthoreovirus (PRV) infection and is an important disease in Atlantic salmon (Salmo salar) aquaculture. Since PRV infects erythrocytes and farmed salmon frequently experience environmental hypoxia, the current study examined mutual effects of PRV infection and hypoxia on pathogenesis and fish performance. Furthermore, effects of HSMI on hypoxia tolerance, cardiorespiratory performance and blood oxygen transport were studied. A cohabitation trial including PRV-infected post-smolts exposed to periodic hypoxic stress (4 h of 40% O2; PRV-H) at 4, 7 and 10 weeks post-infection (WPI) and infected fish reared under normoxic conditions (PRV) was conducted. Periodic hypoxic stress did not influence infection levels or histopathological changes in the heart. Individual incipient lethal oxygen saturation (ILOS) was examined using a standardized hypoxia challenge test (HCT). At 7 WPI, i.e. peak level of infection, both PRV and PRV-H groups exhibited reduced hypoxia tolerance compared to non-infected fish. Three weeks later (10 WPI), during peak levels of pathological changes, reduced hypoxia tolerance was still observed for the PRV group while PRV-H performed equal to non-infected fish, implying a positive effect of the repeated exposure to hypoxic stress. This was in line with maximum heart rate (fHmax) measurements, showing equal performance of PRV-H and non-infected groups, but lower fHmax above 19°C as well as lower temperature optimum (Topt) for aerobic scope for PRV, suggesting reduced cardiac performance and thermal tolerance. In contrast, the PRV-H group had reduced hemoglobin-oxygen affinity compared to non-infected fish. In conclusion, Atlantic salmon suffering from HSMI have reduced hypoxia tolerance and cardiac performance, which can be improved by preconditioning fish to transient hypoxic stress episodes.
format Text
author Lund, Morten
Krudtaa Dahle, Maria
Timmerhaus, Gerrit
Alarcon, Marta
Powell, Mark
Aspehaug, Vidar
Rimstad, Espen
Jørgensen, Sven Martin
author_facet Lund, Morten
Krudtaa Dahle, Maria
Timmerhaus, Gerrit
Alarcon, Marta
Powell, Mark
Aspehaug, Vidar
Rimstad, Espen
Jørgensen, Sven Martin
author_sort Lund, Morten
title Hypoxia tolerance and responses to hypoxic stress during heart and skeletal muscle inflammation in Atlantic salmon (Salmo salar)
title_short Hypoxia tolerance and responses to hypoxic stress during heart and skeletal muscle inflammation in Atlantic salmon (Salmo salar)
title_full Hypoxia tolerance and responses to hypoxic stress during heart and skeletal muscle inflammation in Atlantic salmon (Salmo salar)
title_fullStr Hypoxia tolerance and responses to hypoxic stress during heart and skeletal muscle inflammation in Atlantic salmon (Salmo salar)
title_full_unstemmed Hypoxia tolerance and responses to hypoxic stress during heart and skeletal muscle inflammation in Atlantic salmon (Salmo salar)
title_sort hypoxia tolerance and responses to hypoxic stress during heart and skeletal muscle inflammation in atlantic salmon (salmo salar)
publisher Public Library of Science
publishDate 2017
url http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5507449/
http://www.ncbi.nlm.nih.gov/pubmed/28700748
https://doi.org/10.1371/journal.pone.0181109
genre Atlantic salmon
Salmo salar
genre_facet Atlantic salmon
Salmo salar
op_relation http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5507449/
http://www.ncbi.nlm.nih.gov/pubmed/28700748
http://dx.doi.org/10.1371/journal.pone.0181109
op_rights © 2017 Lund et al
http://creativecommons.org/licenses/by/4.0/
This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
op_rightsnorm CC-BY
op_doi https://doi.org/10.1371/journal.pone.0181109
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