Heart and skeletal muscle inflammation (HSMI) disease diagnosed on a British Columbia salmon farm through a longitudinal farm study

Emiliano Di Cicco, Hugh W. Ferguson, Angela D. Schulze, Karia H. Kaukinen, Shaorong Li, Raphaël Vanderstichel, Øystein Wessel, Espen Rimstad, Ian Gardner, K. Larry Hammell, Kristina M. Miller

Research output: Contribution to journalArticle

27 Citations (Scopus)

Abstract

Heart and skeletal muscle inflammation (HSMI) is an emerging disease of marine-farmed Atlantic Salmon (Salmo salar), first recognized in 1999 in Norway, and later also reported in Scotland and Chile. We undertook a longitudinal study involving health evaluation over an entire marine production cycle on one salmon farm in British Columbia (Canada). In previous production cycles at this farm site and others in the vicinity, cardiac lesions not linked to a specific infectious agent or disease were identified. Histologic assessments of both live and moribund fish samples collected at the farm during the longitudinal study documented at the population level the development, peak, and recovery phases of HSMI. The fish underwent histopathological evaluation of all tissues, Twort's Gram staining, immunohistochemistry, and molecular quantification in heart tissue of 44 agents known or suspected to cause disease in salmon. Our analysis showed evidence of HSMI histopathological lesions over an 11-month timespan, with the prevalence of lesions peaking at 80-100% in sampled fish, despite mild clinical signs with no associated elevation in mortalities reported at the farm level. Diffuse mononuclear inflammation and myodegeneration, consistent with HSMI, was the predominant histologic observation in affected heart and skeletal muscle. Infective agent monitoring identified three agents at high prevalence in salmon heart tissue, including Piscine orthoreovirus (PRV), and parasites Paranucleospora theridion and Kudoa thyrsites. However, PRV alone was statistically correlated with the occurrence and severity of histopathological lesions in the heart. Immunohistochemical staining further localized PRV throughout HSMI development, with the virus found mainly within red blood cells in early cases, moving into the cardiomyocytes within or, more often, on the periphery of the inflammatory reaction during the peak disease, and reducing to low or undetectable levels later in the production cycle. This study represents the first longitudinal assessment of HSMI in a salmon farm in British Columbia, providing new insights on the pathogenesis of the disease.

Original languageEnglish (US)
Article numbere0171471
JournalPLoS One
Volume12
Issue number2
DOIs
StatePublished - Feb 1 2017
Externally publishedYes

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British Columbia
Salmon
Farms
salmon
Longitudinal Studies
Muscle
skeletal muscle
Myocardium
Skeletal Muscle
inflammation
heart
Inflammation
farms
lesions (animal)
Salmo salar
Fishes
Fish
Orthoreovirus
Tissue
longitudinal studies

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

Cite this

Di Cicco, E., Ferguson, H. W., Schulze, A. D., Kaukinen, K. H., Li, S., Vanderstichel, R., ... Miller, K. M. (2017). Heart and skeletal muscle inflammation (HSMI) disease diagnosed on a British Columbia salmon farm through a longitudinal farm study. PLoS One, 12(2), [e0171471]. https://doi.org/10.1371/journal.pone.0171471

Heart and skeletal muscle inflammation (HSMI) disease diagnosed on a British Columbia salmon farm through a longitudinal farm study. / Di Cicco, Emiliano; Ferguson, Hugh W.; Schulze, Angela D.; Kaukinen, Karia H.; Li, Shaorong; Vanderstichel, Raphaël; Wessel, Øystein; Rimstad, Espen; Gardner, Ian; Hammell, K. Larry; Miller, Kristina M.

In: PLoS One, Vol. 12, No. 2, e0171471, 01.02.2017.

Research output: Contribution to journalArticle

Di Cicco, E, Ferguson, HW, Schulze, AD, Kaukinen, KH, Li, S, Vanderstichel, R, Wessel, Ø, Rimstad, E, Gardner, I, Hammell, KL & Miller, KM 2017, 'Heart and skeletal muscle inflammation (HSMI) disease diagnosed on a British Columbia salmon farm through a longitudinal farm study', PLoS One, vol. 12, no. 2, e0171471. https://doi.org/10.1371/journal.pone.0171471
Di Cicco, Emiliano ; Ferguson, Hugh W. ; Schulze, Angela D. ; Kaukinen, Karia H. ; Li, Shaorong ; Vanderstichel, Raphaël ; Wessel, Øystein ; Rimstad, Espen ; Gardner, Ian ; Hammell, K. Larry ; Miller, Kristina M. / Heart and skeletal muscle inflammation (HSMI) disease diagnosed on a British Columbia salmon farm through a longitudinal farm study. In: PLoS One. 2017 ; Vol. 12, No. 2.
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abstract = "Heart and skeletal muscle inflammation (HSMI) is an emerging disease of marine-farmed Atlantic Salmon (Salmo salar), first recognized in 1999 in Norway, and later also reported in Scotland and Chile. We undertook a longitudinal study involving health evaluation over an entire marine production cycle on one salmon farm in British Columbia (Canada). In previous production cycles at this farm site and others in the vicinity, cardiac lesions not linked to a specific infectious agent or disease were identified. Histologic assessments of both live and moribund fish samples collected at the farm during the longitudinal study documented at the population level the development, peak, and recovery phases of HSMI. The fish underwent histopathological evaluation of all tissues, Twort's Gram staining, immunohistochemistry, and molecular quantification in heart tissue of 44 agents known or suspected to cause disease in salmon. Our analysis showed evidence of HSMI histopathological lesions over an 11-month timespan, with the prevalence of lesions peaking at 80-100{\%} in sampled fish, despite mild clinical signs with no associated elevation in mortalities reported at the farm level. Diffuse mononuclear inflammation and myodegeneration, consistent with HSMI, was the predominant histologic observation in affected heart and skeletal muscle. Infective agent monitoring identified three agents at high prevalence in salmon heart tissue, including Piscine orthoreovirus (PRV), and parasites Paranucleospora theridion and Kudoa thyrsites. However, PRV alone was statistically correlated with the occurrence and severity of histopathological lesions in the heart. Immunohistochemical staining further localized PRV throughout HSMI development, with the virus found mainly within red blood cells in early cases, moving into the cardiomyocytes within or, more often, on the periphery of the inflammatory reaction during the peak disease, and reducing to low or undetectable levels later in the production cycle. This study represents the first longitudinal assessment of HSMI in a salmon farm in British Columbia, providing new insights on the pathogenesis of the disease.",
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