Toxicological evaluation of inhalation exposure to benzene and toluene in a raptorial bird, the American kestrel, falco sparverius

Abstract

Benzene and toluene are representative volatile organic compounds (VOCs) released during production, storage, and transportation associated with the oil and gas industry. Benzene and toluene are chemicals of concern because they are released in greater and possibly more biologically significant concentrations than other compounds. Most studies of air pollution in high oil and gas activity areas have neglected to consider risks to top-level predators. Birds can be used as highly sensitive monitors of air quality. Since the avian respiratory tract is physiologically different from a rodent respiratory tract, effects of gases cannot be safely extrapolated from rodent studies. I hypothesized that benzene, being haematotoxic and immunotoxic, along with the neurological and possible endocrine disrupting effects of toluene would be more toxic in birds than in mammals. After two summers of experimental exposure of wild and captive American kestrels to high (10ppm and 80ppm) or environmentally relevant (0.1ppm and 0.8ppm) levels of benzene and toluene, respectively, altered immune, haematopoeitic, behavioural, and endocrine responses characteristic in mammals, were evident in the kestrels.There was a decreased cell mediated immune response as measured by delayed type hypersensitivity tests in all exposed birds (p = 0.028, 0.004). An increase in humoral immunity as compared to control individuals (p = 0.041, 0.031) was also apparent in both dose groups. Plasma retinol levels were decreased in 2005 and 2006 high dose individuals (p = 0.008, 0.048). The majority of haematopoeitic effects involved the erythroid lineage in the bone marrow and the polychromatophilic erythrocytes systemically. There were no significantly adverse responses in the bone marrow with regards to the granuloid lineage but systemically there was a prominent eosinophilia (p = 0.045) and basophilia (p = 0.006) in low exposure groups. The loss of communication between polychromatophilic erythrocytes in the post-mitotic pool within the bone marrow and the peripheral blood was present in low and high exposure individuals compared to control birds (p = 0.013, 0.402, 0.974). The number of polychromatophils in the circulation of low dose group individuals was decreased compared to control birds (p = 0.029). This may be a function of toluene’s inability to inhibit biotransformation enzymes at low concentrations leading to blood cell targeting by benzene’s increased phenolic metabolite production. This theory is corroborated by the possible decreased benzene metabolism and increased toluene distribution manifesting as increased aggressive responses such as wing beating and vocalization time in the high dose group (p = 0.025, 0.086). The work here has shown American kestrels are sensitive to the air contaminants, benzene and toluene. The present study illustrates the need for reference concentrations for airborne pollutants that are calculated based on data measuring sensitive endpoints specific for avian models. Future studies should evaluate immune, haematopoeitic, and behavioural endpoints, as well as develop more sensitive isoform specific enzyme activity assays to further determine the susceptibility of birds to inhaled toxicants.