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      A review of the toxicology of oil in vertebrates: what we have learned following the Deepwater Horizon oil spill

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          Abstract

          In the wake of the Deepwater Horizon (DWH) oil spill, a number of government agencies, academic institutions, consultants, and nonprofit organizations conducted lab- and field-based research to understand the toxic effects of the oil. Lab testing was performed with a variety of fish, birds, turtles, and vertebrate cell lines (as well as invertebrates); field biologists conducted observations on fish, birds, turtles, and marine mammals; and epidemiologists carried out observational studies in humans. Eight years after the spill, scientists and resource managers held a workshop to summarize the similarities and differences in the effects of DWH oil on vertebrate taxa and to identify remaining gaps in our understanding of oil toxicity in wildlife and humans, building upon the cross-taxonomic synthesis initiated during the Natural Resource Damage Assessment. Across the studies, consistency was found in the types of toxic response observed in the different organisms. Impairment of stress responses and adrenal gland function, cardiotoxicity, immune system dysfunction, disruption of blood cells and their function, effects on locomotion, and oxidative damage were observed across taxa. This consistency suggests conservation in the mechanisms of action and disease pathogenesis. From a toxicological perspective, a logical progression of impacts was noted: from molecular and cellular effects that manifest as organ dysfunction, to systemic effects that compromise fitness, growth, reproductive potential, and survival. From a clinical perspective, adverse health effects from DWH oil spill exposure formed a suite of signs/symptomatic responses that at the highest doses/concentrations resulted in multi-organ system failure.

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          Most cited references171

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          Deepwater Horizon crude oil impacts the developing hearts of large predatory pelagic fish.

          The Deepwater Horizon disaster released more than 636 million L of crude oil into the northern Gulf of Mexico. The spill oiled upper surface water spawning habitats for many commercially and ecologically important pelagic fish species. Consequently, the developing spawn (embryos and larvae) of tunas, swordfish, and other large predators were potentially exposed to crude oil-derived polycyclic aromatic hydrocarbons (PAHs). Fish embryos are generally very sensitive to PAH-induced cardiotoxicity, and adverse changes in heart physiology and morphology can cause both acute and delayed mortality. Cardiac function is particularly important for fast-swimming pelagic predators with high aerobic demand. Offspring for these species develop rapidly at relatively high temperatures, and their vulnerability to crude oil toxicity is unknown. We assessed the impacts of field-collected Deepwater Horizon (MC252) oil samples on embryos of three pelagic fish: bluefin tuna, yellowfin tuna, and an amberjack. We show that environmentally realistic exposures (1-15 µg/L total PAH) cause specific dose-dependent defects in cardiac function in all three species, with circulatory disruption culminating in pericardial edema and other secondary malformations. Each species displayed an irregular atrial arrhythmia following oil exposure, indicating a highly conserved response to oil toxicity. A considerable portion of Gulf water samples collected during the spill had PAH concentrations exceeding toxicity thresholds observed here, indicating the potential for losses of pelagic fish larvae. Vulnerability assessments in other ocean habitats, including the Arctic, should focus on the developing heart of resident fish species as an exceptionally sensitive and consistent indicator of crude oil impacts.
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            Health of common bottlenose dolphins ( Tursiops truncatus ) in Barataria Bay, Louisiana, following the deepwater horizon oil spill.

            The oil spill resulting from the explosion of the Deepwater Horizon drilling platform initiated immediate concern for marine wildlife, including common bottlenose dolphins in sensitive coastal habitats. To evaluate potential sublethal effects on dolphins, health assessments were conducted in Barataria Bay, Louisiana, an area that received heavy and prolonged oiling, and in a reference site, Sarasota Bay, Florida, where oil was not observed. Dolphins were temporarily captured, received a veterinary examination, and were then released. Dolphins sampled in Barataria Bay showed evidence of hypoadrenocorticism, consistent with adrenal toxicity as previously reported for laboratory mammals exposed to oil. Barataria Bay dolphins were 5 times more likely to have moderate-severe lung disease, generally characterized by significant alveolar interstitial syndrome, lung masses, and pulmonary consolidation. Of 29 dolphins evaluated from Barataria Bay, 48% were given a guarded or worse prognosis, and 17% were considered poor or grave, indicating that they were not expected to survive. Disease conditions in Barataria Bay dolphins were significantly greater in prevalence and severity than those in Sarasota Bay dolphins, as well as those previously reported in other wild dolphin populations. Many disease conditions observed in Barataria Bay dolphins are uncommon but consistent with petroleum hydrocarbon exposure and toxicity.
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              Crude oil impairs cardiac excitation-contraction coupling in fish.

              Crude oil is known to disrupt cardiac function in fish embryos. Large oil spills, such as the Deepwater Horizon (DWH) disaster that occurred in 2010 in the Gulf of Mexico, could severely affect fish at impacted spawning sites. The physiological mechanisms underlying such potential cardiotoxic effects remain unclear. Here, we show that crude oil samples collected from the DWH spill prolonged the action potential of isolated cardiomyocytes from juvenile bluefin and yellowfin tunas, through the blocking of the delayed rectifier potassium current (I(Kr)). Crude oil exposure also decreased calcium current (I(Ca)) and calcium cycling, which disrupted excitation-contraction coupling in cardiomyocytes. Our findings demonstrate a cardiotoxic mechanism by which crude oil affects the regulation of cellular excitability, with implications for life-threatening arrhythmias in vertebrates.
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                Author and article information

                Journal
                Journal of Toxicology and Environmental Health, Part B
                Journal of Toxicology and Environmental Health, Part B
                Informa UK Limited
                1093-7404
                1521-6950
                November 17 2021
                September 19 2021
                November 17 2021
                : 24
                : 8
                : 355-394
                Affiliations
                [1 ]Conservation Medicine, National Marine Mammal Foundation, San Diego, California, United States
                [2 ]Department of Animal Science, Michigan State University, East Lansing, Michigan, United States
                [3 ]College of Veterinary Medicine, Illinois at Urbana-Champaign, Brookfield, Illinois, United States
                [4 ]Zoological Pathology Program, Huxley College of the Environment, Western Washington University, Bellingham, Washington, United States
                [5 ]College of Marine Sciences, University of South Florida, St. Petersburg, Florida, United States
                [6 ]Lethbridge, Alberta, Canada
                [7 ]Department of Pathobiology and Veterinary Sciences, University of Connecticut, Storrs, Connecticut, United States
                [8 ]Office of Response and Restoration, NOAA, Silver Spring, Maryland, United States
                [9 ]Department of Pharmacology and Toxicology, University of Texas Medical Branch, Galveston, Texas, United States
                [10 ]Marine Science Institute, University of Texas at Austin, Port Aransas, Texas, United States
                [11 ]Division of Coastal Sciences, School of Ocean Science and Engineering, University of Southern Mississippi, Gulfport, Mississippi, United States
                [12 ]RSMAS, University of Miami, Miami, Florida, United States
                [13 ]URIKA, LLC, Mukilteo, Washington, United States
                [14 ]NOAA Environmental Conservation Division, Northwest Fisheries Science Center, Seattle, Washington, United States
                [15 ]Department of Health and Human Services, National Institute of Environmental Health Sciences, National Institutes of Health, North Carolina, United States
                [16 ]Boulder, Colorado, United States
                [17 ]University of Maryland Center of Environmental Science, Chesapeake Biological Laboratory, Solomons, Maryland, United States
                [18 ]Health and Environment Division, Abt Associates, Boulder, Colorado, United States
                [19 ]Department of Epidemiology, LSU School of Public Health, New Orleans, Louisiana, United States
                [20 ]Advanced Environmental Research Institute and Department of Biological Sciences, University of North Texas, Denton, Texas, United States
                [21 ]NOAA Office of Protected Resources, National Marine Fisheries Service, Silver Spring, Maryland, United States
                [22 ]Department of Preventive Medicine and Biostatistics, Uniformed Services University, Bethesda, Maryland, United States
                [23 ]Environmental Laboratory of Forensics, Mote Marine Laboratory, Sarasota, Florida, United States
                [24 ]School of Veterinary Medicine, One Health Institute, University of California, Davis, California, United States
                [25 ]Sea Mammal Research Unit, Scottish Oceans Institute, University of St Andrews, St Andrews, UK
                Article
                10.1080/10937404.2021.1975182
                34542016
                82fac9fb-9948-4a1a-9114-ee7cdb62c142
                © 2021

                http://creativecommons.org/licenses/by-nc-nd/4.0/

                History

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