Cardiac Arrhythmia Is the Primary Response of Embryonic Pacific Herring (Clupea pallasi) Exposed to Crude Oil during Weathering

Abstract

Teleost embryos develop a syndrome characterized by edema when exposed to water that weathers substrates contaminated with crude oil. Previous studies using zebrafish demonstrated that crude oil exposure causes cardiogenic edema, and that the most abundant polycyclic aromatic hydrocarbons (PAHs) in weathered crude oils (tricyclic fluorenes, dibenzothiophenes, and phenanthrenes) are cardiotoxic, causing arrhythmia through a pathway that does not require activation of the aryl hydrocarbon receptor (AHR). We demonstrate here for Pacific herring, a species impacted by the Exxon Valdez oil spill, that the developing heart is the primary target of crude oil exposure. Herring embryos exposed to the effluent of oiled gravel columns developed dose-dependent edema and irregular cardiac arrhythmia soon afterthe heartbeat was established. At a dose that produced cardiac dysfunction in 100% of exposed embryos, tissue levels of tricyclic PAHs were below 1 micromol/kg, suggesting a specific, high affinity target in the heart. These findings have implications for understanding the mechanism of tricyclic PAH cardiotoxicity, the development of biomarkers for the effects of PAH exposure in fish, and understanding the long-term impacts of oil spills and other sources of PAH pollution in aquatic environments.

Sublethal exposure to crude oil during embryonic development alters cardiac morphology and reduces aerobic capacity in adult fish

“…Oil exposure studies using zebrafish embryos demonstrated a heart failure syndrome that is lethal to larvae (13,14), findings that were validated in Pacific herring (15). As oil weathers, the proportional composition of dissolved-phase PAHs becomes dominated by the tricyclic fluorenes, dibenzothiophenes, and phenanthrenes (5,6,16), which were shown to be directly cardiotoxic (13,14).…”

“…As oil weathers, the proportional composition of dissolved-phase PAHs becomes dominated by the tricyclic fluorenes, dibenzothiophenes, and phenanthrenes (5,6,16), which were shown to be directly cardiotoxic (13,14). In herring embryos, cardiotoxicity occurred at tricyclic PAH concentrations in the tissue as low as 0.8 μmol/kg (150 ppb) wet weight, indicating a specific, high-affinity cellular target (15). Individual nonalkylated tricyclic PAHs caused atrioventricular conduction arrhythmias indistinguishable from those caused by drugs known to block potassium channels required for the repolarization phase of cardiac action potentials (13,14).…”

“…Individual nonalkylated tricyclic PAHs caused atrioventricular conduction arrhythmias indistinguishable from those caused by drugs known to block potassium channels required for the repolarization phase of cardiac action potentials (13,14). PAH mixtures from weathered crude oil caused more complex cardiac dysfunction, suggestive of additional targets, including pacemaker currents and plasma membrane or sarcoplasmic calcium channels (14,15). Consistent with genetic analyses of cardiac form and function in zebrafish (17,18), this oil-induced cardiac dysfunction affects later morphogenetic steps, such as looping of the atrial and ventricular chambers into their normal side-by-side positioning (13,14).…”

Oil spills and fish health: exposing the heart of the matter

“…We recently found that these more abundant chemicals in crude oil target the heart and can cause heart failure in developing fish embryos (Incardona et al, 2004(Incardona et al, , 2005(Incardona et al, , 2009; see figure in box). This implies that most of the conventional tools for assessing oil exposure have limited usefulness for understanding effects on fish at vulnerable early life stages.…”

“…More recent studies have built on these findings, with the goal of further sorting out which specific chemicals in complex oil mixtures are causing this early-life-stage toxicity in fish (Incardona et al, 2004(Incardona et al, , 2005(Incardona et al, , 2009). This more refined understanding is needed to develop next-generation biomarkers for oil exposure and to more accurately estimate the potential decline and recovery of fish populations that spawn in future spill zones.…”