Mechanistic analysis of acute, Ni-induced respiratory toxicity in the rainbow trout (Oncorhynchus mykiss): An exclusively branchial phenomenon

Eric F. Pane, Aziz Haque, Chris M. Wood

Research output: Contribution to journalArticle

86 Citations (Scopus)

Abstract

In moderately hard Lake Ontario water (∼140 mg L-1 as CaCO3) waterborne Ni (9.7-10.7 mg Ni L-1) is acutely toxic to adult rainbow trout (Oncorhynchus mykiss) exclusively via branchial mechanisms. Ventilation in resting trout (evaluated using a ventilatory masking technique) was adversely affected, as ventilation rate (VR), ventilation volume (VG), opercular stroke volume (VSV) and resting oxygen consumption (ṀO2) were all increased, and oxygen extraction efficiency (U%) decreased over 48 h of Ni exposure. Extensive gill Ni accumulation (41-fold over control levels) during 82 h of waterborne Ni exposure resulted in marked ultrastructural damage to the respiratory epithelium of the gill, including swelling of the secondary lamellae evidenced by changes to both the lamellar region (increased secondary lamellar tissue volume (V SL/VLR)), and to the secondary lamellae themselves (increased volume of tissue lying outside the pillar system (V OPS/VSL)). Additionally, decreased lamellar height and increased lamellar width indicated a reduction in lamellar surface area available for gas diffusion. The relative diffusing capacity of experimental fish was only 59% of that of control fish. Infusion of Ni into the blood, achieving a similar time course and magnitude of plasma [Ni] elevation to that during waterborne exposure, failed to elicit any signs of respiratory toxicity typically diagnostic of acute, high level waterborne Ni exposure. Infusion of Ni into the blood for 96 h resulted in only minor accumulation of Ni in the gill, suggesting that acute Ni-induced respiratory toxicity is related to accumulation of high levels of Ni in the gill from the water. Additionally, infusion of Ni into the bloodstream led to significant extrabranchial Ni accumulation only in the kidney. White muscle, heart, liver, stomach, and intestine did not significantly accumulate Ni following infusion into the bloodstream and trapped plasma analysis revealed that, with the exception of the kidney, a substantial portion of Ni accumulated in tissues following infusion could be accounted for by extracellular (blood-bound) Ni.

Original languageEnglish
Pages (from-to)11-24
Number of pages14
JournalAquatic Toxicology
Volume69
Issue number1
DOIs
StatePublished - Jul 30 2004

Fingerprint

Oncorhynchus mykiss
rainbow
gills
toxicity
ventilation
Ventilation
blood
blood flow
Fishes
kidneys
respiratory mucosa
Kidney
plasma
Respiratory Mucosa
Water
Trout
Lake Ontario
Poisons
Ontario
fish

Keywords

  • Acute
  • Gill
  • Nickel
  • Rainbow trout
  • Respiratory

ASJC Scopus subject areas

  • Aquatic Science

Cite this

Mechanistic analysis of acute, Ni-induced respiratory toxicity in the rainbow trout (Oncorhynchus mykiss) : An exclusively branchial phenomenon. / Pane, Eric F.; Haque, Aziz; Wood, Chris M.

In: Aquatic Toxicology, Vol. 69, No. 1, 30.07.2004, p. 11-24.

Research output: Contribution to journalArticle

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abstract = "In moderately hard Lake Ontario water (∼140 mg L-1 as CaCO3) waterborne Ni (9.7-10.7 mg Ni L-1) is acutely toxic to adult rainbow trout (Oncorhynchus mykiss) exclusively via branchial mechanisms. Ventilation in resting trout (evaluated using a ventilatory masking technique) was adversely affected, as ventilation rate (VR), ventilation volume (VG), opercular stroke volume (VSV) and resting oxygen consumption (ṀO2) were all increased, and oxygen extraction efficiency (U{\%}) decreased over 48 h of Ni exposure. Extensive gill Ni accumulation (41-fold over control levels) during 82 h of waterborne Ni exposure resulted in marked ultrastructural damage to the respiratory epithelium of the gill, including swelling of the secondary lamellae evidenced by changes to both the lamellar region (increased secondary lamellar tissue volume (V SL/VLR)), and to the secondary lamellae themselves (increased volume of tissue lying outside the pillar system (V OPS/VSL)). Additionally, decreased lamellar height and increased lamellar width indicated a reduction in lamellar surface area available for gas diffusion. The relative diffusing capacity of experimental fish was only 59{\%} of that of control fish. Infusion of Ni into the blood, achieving a similar time course and magnitude of plasma [Ni] elevation to that during waterborne exposure, failed to elicit any signs of respiratory toxicity typically diagnostic of acute, high level waterborne Ni exposure. Infusion of Ni into the blood for 96 h resulted in only minor accumulation of Ni in the gill, suggesting that acute Ni-induced respiratory toxicity is related to accumulation of high levels of Ni in the gill from the water. Additionally, infusion of Ni into the bloodstream led to significant extrabranchial Ni accumulation only in the kidney. White muscle, heart, liver, stomach, and intestine did not significantly accumulate Ni following infusion into the bloodstream and trapped plasma analysis revealed that, with the exception of the kidney, a substantial portion of Ni accumulated in tissues following infusion could be accounted for by extracellular (blood-bound) Ni.",
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N2 - In moderately hard Lake Ontario water (∼140 mg L-1 as CaCO3) waterborne Ni (9.7-10.7 mg Ni L-1) is acutely toxic to adult rainbow trout (Oncorhynchus mykiss) exclusively via branchial mechanisms. Ventilation in resting trout (evaluated using a ventilatory masking technique) was adversely affected, as ventilation rate (VR), ventilation volume (VG), opercular stroke volume (VSV) and resting oxygen consumption (ṀO2) were all increased, and oxygen extraction efficiency (U%) decreased over 48 h of Ni exposure. Extensive gill Ni accumulation (41-fold over control levels) during 82 h of waterborne Ni exposure resulted in marked ultrastructural damage to the respiratory epithelium of the gill, including swelling of the secondary lamellae evidenced by changes to both the lamellar region (increased secondary lamellar tissue volume (V SL/VLR)), and to the secondary lamellae themselves (increased volume of tissue lying outside the pillar system (V OPS/VSL)). Additionally, decreased lamellar height and increased lamellar width indicated a reduction in lamellar surface area available for gas diffusion. The relative diffusing capacity of experimental fish was only 59% of that of control fish. Infusion of Ni into the blood, achieving a similar time course and magnitude of plasma [Ni] elevation to that during waterborne exposure, failed to elicit any signs of respiratory toxicity typically diagnostic of acute, high level waterborne Ni exposure. Infusion of Ni into the blood for 96 h resulted in only minor accumulation of Ni in the gill, suggesting that acute Ni-induced respiratory toxicity is related to accumulation of high levels of Ni in the gill from the water. Additionally, infusion of Ni into the bloodstream led to significant extrabranchial Ni accumulation only in the kidney. White muscle, heart, liver, stomach, and intestine did not significantly accumulate Ni following infusion into the bloodstream and trapped plasma analysis revealed that, with the exception of the kidney, a substantial portion of Ni accumulated in tissues following infusion could be accounted for by extracellular (blood-bound) Ni.

AB - In moderately hard Lake Ontario water (∼140 mg L-1 as CaCO3) waterborne Ni (9.7-10.7 mg Ni L-1) is acutely toxic to adult rainbow trout (Oncorhynchus mykiss) exclusively via branchial mechanisms. Ventilation in resting trout (evaluated using a ventilatory masking technique) was adversely affected, as ventilation rate (VR), ventilation volume (VG), opercular stroke volume (VSV) and resting oxygen consumption (ṀO2) were all increased, and oxygen extraction efficiency (U%) decreased over 48 h of Ni exposure. Extensive gill Ni accumulation (41-fold over control levels) during 82 h of waterborne Ni exposure resulted in marked ultrastructural damage to the respiratory epithelium of the gill, including swelling of the secondary lamellae evidenced by changes to both the lamellar region (increased secondary lamellar tissue volume (V SL/VLR)), and to the secondary lamellae themselves (increased volume of tissue lying outside the pillar system (V OPS/VSL)). Additionally, decreased lamellar height and increased lamellar width indicated a reduction in lamellar surface area available for gas diffusion. The relative diffusing capacity of experimental fish was only 59% of that of control fish. Infusion of Ni into the blood, achieving a similar time course and magnitude of plasma [Ni] elevation to that during waterborne exposure, failed to elicit any signs of respiratory toxicity typically diagnostic of acute, high level waterborne Ni exposure. Infusion of Ni into the blood for 96 h resulted in only minor accumulation of Ni in the gill, suggesting that acute Ni-induced respiratory toxicity is related to accumulation of high levels of Ni in the gill from the water. Additionally, infusion of Ni into the bloodstream led to significant extrabranchial Ni accumulation only in the kidney. White muscle, heart, liver, stomach, and intestine did not significantly accumulate Ni following infusion into the bloodstream and trapped plasma analysis revealed that, with the exception of the kidney, a substantial portion of Ni accumulated in tissues following infusion could be accounted for by extracellular (blood-bound) Ni.

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