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Very low embryonic crude oil exposures cause lasting cardiac defects in salmon and herring.

Incardona JP, Carls MG, Holland L, Linbo TL, Baldwin DH, Myers MS, Peck KA, Tagal M, Rice SD, Scholz NL - Sci Rep (2015)

Bottom Line: Crude oil disrupts excitation-contraction coupling in fish heart muscle cells, and we show here that salmon and herring exposed as embryos to trace levels of crude oil grow into juveniles with abnormal hearts and reduced cardiorespiratory function, the latter a key determinant of individual survival and population recruitment.The thresholds for developmental cardiotoxicity were remarkably low, suggesting the scale of the Exxon Valdez impact in shoreline spawning habitats was much greater than previously appreciated.Moreover, an irreversible loss of cardiac fitness and consequent increases in delayed mortality in oil-exposed cohorts may have been important contributors to the delayed decline of pink salmon and herring stocks in Prince William Sound.

View Article: PubMed Central - PubMed

Affiliation: Environmental and Fisheries Sciences Division, Northwest Fisheries Science Center, National Marine Fisheries Service, NOAA, 2725 Montlake Blvd. E., Seattle, WA 98112.

ABSTRACT
The 1989 Exxon Valdez disaster exposed embryos of pink salmon and Pacific herring to crude oil in shoreline spawning habitats throughout Prince William Sound, Alaska. The herring fishery collapsed four years later. The role of the spill, if any, in this decline remains one of the most controversial unanswered questions in modern natural resource injury assessment. Crude oil disrupts excitation-contraction coupling in fish heart muscle cells, and we show here that salmon and herring exposed as embryos to trace levels of crude oil grow into juveniles with abnormal hearts and reduced cardiorespiratory function, the latter a key determinant of individual survival and population recruitment. Oil exposure during cardiogenesis led to specific defects in the outflow tract and compact myocardium, and a hypertrophic response in spongy myocardium, evident in juveniles 7 to 9 months after exposure. The thresholds for developmental cardiotoxicity were remarkably low, suggesting the scale of the Exxon Valdez impact in shoreline spawning habitats was much greater than previously appreciated. Moreover, an irreversible loss of cardiac fitness and consequent increases in delayed mortality in oil-exposed cohorts may have been important contributors to the delayed decline of pink salmon and herring stocks in Prince William Sound.

No MeSH data available.


Related in: MedlinePlus

Distinct changes in spongy and compact myocardium in juvenile pink salmon following embryonic oil exposure.A subset of hearts from fish 8 months post-exposure for which dimensions were measured in Fig. 3 were sectioned and stained with hematoxylin/eosin. (A) Sections were selected that showed the atrium (a) and ventricle (v), with a clear midline plane through the bulbus arteriosus (ba) and ventricular-bulbar valve. (B) Cardiomyocyte diameters, (C), numbers of cardiomyocyte nuclei and (D) thickness of the compact myocardium were measured in the indicated areas (A, red squares, black circles, and blue squares respectively). (E) Levels of mRNA for atrial (nppa) and B-type natriuretic peptide (nppb) in pink salmon hearts normalized to the reference gene ef1α. All data are mean ± s.e.m. ANOVA showed significance for effect of oil exposure for compact myocardium thickness (P = 0.02) and density of nuclei (P < 0.0001). Asterisks indicate treatments that differed significantly from controls (Dunnett’s post-hoc test, α = 0.05).
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f4: Distinct changes in spongy and compact myocardium in juvenile pink salmon following embryonic oil exposure.A subset of hearts from fish 8 months post-exposure for which dimensions were measured in Fig. 3 were sectioned and stained with hematoxylin/eosin. (A) Sections were selected that showed the atrium (a) and ventricle (v), with a clear midline plane through the bulbus arteriosus (ba) and ventricular-bulbar valve. (B) Cardiomyocyte diameters, (C), numbers of cardiomyocyte nuclei and (D) thickness of the compact myocardium were measured in the indicated areas (A, red squares, black circles, and blue squares respectively). (E) Levels of mRNA for atrial (nppa) and B-type natriuretic peptide (nppb) in pink salmon hearts normalized to the reference gene ef1α. All data are mean ± s.e.m. ANOVA showed significance for effect of oil exposure for compact myocardium thickness (P = 0.02) and density of nuclei (P < 0.0001). Asterisks indicate treatments that differed significantly from controls (Dunnett’s post-hoc test, α = 0.05).

Mentions: Changes in ventricular shape could be indicative of cardiac hypertrophy. Extensively characterized in mammals24 and occurring through similar pathways in salmon25, cardiac hypertrophy is initially a compensatory response to cardiac stress or injury. At the cellular level, hypertrophy in mammals is indicated primarily by changes in cardiomyocytes that occur concentrically (increased cross-sectional area of individual cardiomyocytes), or eccentrically (lengthening of individual cardiomyocytes). However, fish hearts have the capacity to regenerate cardiomyocytes26, and hypertrophy in fish also involves hyperplasia2527. We examined hearts dissected from pink salmon eight months post-exposure for histopathological evidence of hypertrophy. The fish ventricle consists of two anatomically distinct sections, an outer compact myocardium surrounding a spongy myocardium with numerous trabeculae projecting into the lumen, the latter making up the bulk of the ventricle. Individual cardiomyocyte lengths (eccentric hypertrophy) could not be measured in the spongy myocardium, but cardiomyocyte diameters were measured in cells randomly selected from three consistent areas (Fig. 4A). Analysis in fixed sections from 5–6 individuals for each treatment group showed a trend of increased cardiomyocyte width related to oil exposure with a mean (±s.e.m.) in controls of 4.03 ± 0.05  μm and ranging from 4.16 ± 0.05 to 4.24 ± 0.05  μm across oil-exposed groups (Fig. 4B). Although statistical significance was marginal (ANOVA P = 0.04 for effect of oil exposure, but slope of linear regression P = 0.1), this may be due in part to the relative insensitivity of the technique24. Oil exposure was associated significantly with hyperplasia in the spongy myocardium (ANOVA P < 0.0001), with an increase in the density of cardiomyocyte nuclei in the highest exposure group (123% of control, P = 0.0002; Fig. 4C). In contrast, the thickness of the compact myocardium was reduced significantly by oil exposure in all but the lowest treatment group (ANOVA P = 0.02; Fig. 4D), with control hearts averaging 17.6 ± 0.7  μm thick, and oil-exposed groups ranging from 12.2 ± 1.0 to 16.7 ± 1.4  μm. Other types of reactive changes were not obvious. We examined the mRNA expression levels of atrial and B-type natriuretic peptides (ANP/nppa and BNP/nppb) in salmon hearts, as these genes are strongly linked to cardiac hypertrophy in humans28. Although there was a trend of increasing nppa and nppb mRNA levels with ΣPAH in pink salmon (Fig. 4E), there was no statistically significant dose-response relationship, with only the lowest exposure group (tissue ΣPAH 222 ng/g) showing significantly higher expression of nppa at 2.5-times above control (P = 0.04, Dunnett’s method).


Very low embryonic crude oil exposures cause lasting cardiac defects in salmon and herring.

Incardona JP, Carls MG, Holland L, Linbo TL, Baldwin DH, Myers MS, Peck KA, Tagal M, Rice SD, Scholz NL - Sci Rep (2015)

Distinct changes in spongy and compact myocardium in juvenile pink salmon following embryonic oil exposure.A subset of hearts from fish 8 months post-exposure for which dimensions were measured in Fig. 3 were sectioned and stained with hematoxylin/eosin. (A) Sections were selected that showed the atrium (a) and ventricle (v), with a clear midline plane through the bulbus arteriosus (ba) and ventricular-bulbar valve. (B) Cardiomyocyte diameters, (C), numbers of cardiomyocyte nuclei and (D) thickness of the compact myocardium were measured in the indicated areas (A, red squares, black circles, and blue squares respectively). (E) Levels of mRNA for atrial (nppa) and B-type natriuretic peptide (nppb) in pink salmon hearts normalized to the reference gene ef1α. All data are mean ± s.e.m. ANOVA showed significance for effect of oil exposure for compact myocardium thickness (P = 0.02) and density of nuclei (P < 0.0001). Asterisks indicate treatments that differed significantly from controls (Dunnett’s post-hoc test, α = 0.05).
© Copyright Policy - open-access
Related In: Results  -  Collection

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f4: Distinct changes in spongy and compact myocardium in juvenile pink salmon following embryonic oil exposure.A subset of hearts from fish 8 months post-exposure for which dimensions were measured in Fig. 3 were sectioned and stained with hematoxylin/eosin. (A) Sections were selected that showed the atrium (a) and ventricle (v), with a clear midline plane through the bulbus arteriosus (ba) and ventricular-bulbar valve. (B) Cardiomyocyte diameters, (C), numbers of cardiomyocyte nuclei and (D) thickness of the compact myocardium were measured in the indicated areas (A, red squares, black circles, and blue squares respectively). (E) Levels of mRNA for atrial (nppa) and B-type natriuretic peptide (nppb) in pink salmon hearts normalized to the reference gene ef1α. All data are mean ± s.e.m. ANOVA showed significance for effect of oil exposure for compact myocardium thickness (P = 0.02) and density of nuclei (P < 0.0001). Asterisks indicate treatments that differed significantly from controls (Dunnett’s post-hoc test, α = 0.05).
Mentions: Changes in ventricular shape could be indicative of cardiac hypertrophy. Extensively characterized in mammals24 and occurring through similar pathways in salmon25, cardiac hypertrophy is initially a compensatory response to cardiac stress or injury. At the cellular level, hypertrophy in mammals is indicated primarily by changes in cardiomyocytes that occur concentrically (increased cross-sectional area of individual cardiomyocytes), or eccentrically (lengthening of individual cardiomyocytes). However, fish hearts have the capacity to regenerate cardiomyocytes26, and hypertrophy in fish also involves hyperplasia2527. We examined hearts dissected from pink salmon eight months post-exposure for histopathological evidence of hypertrophy. The fish ventricle consists of two anatomically distinct sections, an outer compact myocardium surrounding a spongy myocardium with numerous trabeculae projecting into the lumen, the latter making up the bulk of the ventricle. Individual cardiomyocyte lengths (eccentric hypertrophy) could not be measured in the spongy myocardium, but cardiomyocyte diameters were measured in cells randomly selected from three consistent areas (Fig. 4A). Analysis in fixed sections from 5–6 individuals for each treatment group showed a trend of increased cardiomyocyte width related to oil exposure with a mean (±s.e.m.) in controls of 4.03 ± 0.05  μm and ranging from 4.16 ± 0.05 to 4.24 ± 0.05  μm across oil-exposed groups (Fig. 4B). Although statistical significance was marginal (ANOVA P = 0.04 for effect of oil exposure, but slope of linear regression P = 0.1), this may be due in part to the relative insensitivity of the technique24. Oil exposure was associated significantly with hyperplasia in the spongy myocardium (ANOVA P < 0.0001), with an increase in the density of cardiomyocyte nuclei in the highest exposure group (123% of control, P = 0.0002; Fig. 4C). In contrast, the thickness of the compact myocardium was reduced significantly by oil exposure in all but the lowest treatment group (ANOVA P = 0.02; Fig. 4D), with control hearts averaging 17.6 ± 0.7  μm thick, and oil-exposed groups ranging from 12.2 ± 1.0 to 16.7 ± 1.4  μm. Other types of reactive changes were not obvious. We examined the mRNA expression levels of atrial and B-type natriuretic peptides (ANP/nppa and BNP/nppb) in salmon hearts, as these genes are strongly linked to cardiac hypertrophy in humans28. Although there was a trend of increasing nppa and nppb mRNA levels with ΣPAH in pink salmon (Fig. 4E), there was no statistically significant dose-response relationship, with only the lowest exposure group (tissue ΣPAH 222 ng/g) showing significantly higher expression of nppa at 2.5-times above control (P = 0.04, Dunnett’s method).

Bottom Line: Crude oil disrupts excitation-contraction coupling in fish heart muscle cells, and we show here that salmon and herring exposed as embryos to trace levels of crude oil grow into juveniles with abnormal hearts and reduced cardiorespiratory function, the latter a key determinant of individual survival and population recruitment.The thresholds for developmental cardiotoxicity were remarkably low, suggesting the scale of the Exxon Valdez impact in shoreline spawning habitats was much greater than previously appreciated.Moreover, an irreversible loss of cardiac fitness and consequent increases in delayed mortality in oil-exposed cohorts may have been important contributors to the delayed decline of pink salmon and herring stocks in Prince William Sound.

View Article: PubMed Central - PubMed

Affiliation: Environmental and Fisheries Sciences Division, Northwest Fisheries Science Center, National Marine Fisheries Service, NOAA, 2725 Montlake Blvd. E., Seattle, WA 98112.

ABSTRACT
The 1989 Exxon Valdez disaster exposed embryos of pink salmon and Pacific herring to crude oil in shoreline spawning habitats throughout Prince William Sound, Alaska. The herring fishery collapsed four years later. The role of the spill, if any, in this decline remains one of the most controversial unanswered questions in modern natural resource injury assessment. Crude oil disrupts excitation-contraction coupling in fish heart muscle cells, and we show here that salmon and herring exposed as embryos to trace levels of crude oil grow into juveniles with abnormal hearts and reduced cardiorespiratory function, the latter a key determinant of individual survival and population recruitment. Oil exposure during cardiogenesis led to specific defects in the outflow tract and compact myocardium, and a hypertrophic response in spongy myocardium, evident in juveniles 7 to 9 months after exposure. The thresholds for developmental cardiotoxicity were remarkably low, suggesting the scale of the Exxon Valdez impact in shoreline spawning habitats was much greater than previously appreciated. Moreover, an irreversible loss of cardiac fitness and consequent increases in delayed mortality in oil-exposed cohorts may have been important contributors to the delayed decline of pink salmon and herring stocks in Prince William Sound.

No MeSH data available.


Related in: MedlinePlus