Emerging substances—emerging problems?

We human beings are threatening our world and ourselves with problems ranging from global climate change, habitat change, and introduced species to eutrophication and toxic chemicals. The level of concern posed by new, emerging substances is presently unknown. Data necessary to properly evaluate their potential significance to human and ecological health do not exist. The purpose of this editorial is to provide background information regarding some key emerging substances and then to urge “big picture” risk assessments based on existing information to clearly delineate key uncertainties, focused research to reduce those key uncertainties, and risk—risk comparisons to determine management priorities. Emerging substances can be divided into four broad, if somewhat artificial, categories: polybrominated diphenyl ethers (PBDEs) and other global organic contaminants (also incorrectly called persistent organic pollutants, because contamination is not automatically pollution [1]), pharmaceuticals and personal care products, endocrine-modulating chemicals (EMCs; often less correctly called endocrine-disrupting chemicals), and nanotechnology products. These categories are artificial because they overlap; for example, many substances in the other three groups are also considered to be actual or potential EMCs. However, the categories provide a useful structure for the following discussion. Polybrominated diphenyl ethers are flame retardants found in a wide variety of products, including furniture foam, plastics, consumer electronics, wire insulation, and back coatings for draperies and upholstery. They slow both ignition and the rate of fire growth and, thus, save human lives and property. Three commercial mixtures exist with differing average amounts of bromination: penta-, octa-, and decabrominated diphenyl ethers. The former two mixtures are subject to a voluntary phase out; the latter mixture is considered to be the least toxic and is responsible for approximately 80% of PBDEs in the United States. Polybrominated diphenyl ethers are released from manufacturing or processing and from product aging and wear, and they are found in food, water, sediment, dust, and soil. Polybrominated diphenyl ethers are of concern because concentrations are increasing in the environment, including in the tissues of humans and other biota. Levels in humans are doubling every two to five years and are approximately 40-fold higher in North America than elsewhere (http://www.ecy.wa.gov/programs/eap/pbt/pbde/). Like other global organic contaminants, PBDEs are subject to long-range transport. For example, concentrations have increased in the tissues of Arctic biota, such as polar bears, in a fashion similar to that of other global organic contaminants [2, 3]. However, the environmental toxicity and effects of PBDEs remain to be fully assessed [4]. Other new, global organic contaminants include hexabromo-cyclodecane, perfluoroctane sulfonate, and siloxanes. Hexabromo-cyclodecane is used in polystyrene as part of thermal insulation and in upholstery textiles. Concentrations in polar bears and in open-ocean skipjack tuna are increasing, similar to those of PBDEs (D. Muir, Environment Canada, Burlington, ON, Canada, personal communication). Perfluoroctane sulfonates are found in stain-repellent coatings, shampoos, cosmetics, paint, batteries, waxes, polishes, antistatic and antifog products, food wraps, fire-fighting foams, and insecticides. They are also accumulating in biota at a distance from sources [5, 6]. Siloxanes are used as carriers in antiperspirants and deodorants, in hair shampoo conditioners, and in cleaning solvents. Environmental fate data for poly-dimethyl siloxanes indicate that primary environmental loadings are via wastewater treatment plants, landfills, and incineration. Virtually no data exist for volatile methyl siloxanes, which pose challenges regarding chemical analyses. Modeling indicates that major loadings are expected to be atmospheric. Again, the environmental toxicity and effects of these chemicals are virtually unknown. Pharmaceuticals and personal care products are defined as “All drugs (available by prescription or over-the-counter, including proteinaceous ‘biologics’); diagnostic agents (e.g., x-ray contrast media); ‘nutraceuticals’ (bioactive food supplements such as huperzine A); other consumer chemicals: fragrances (e.g., musks), sun-screen agents (e.g., methylbensylidene camphor). Pharmaceuticals and personal care products comprise an immense diversity of chemical substances, some that are not new (e.g., caffeine, nicotine, aspirin and others that are so new they have not yet been measured in the environment” (http://www.epa.gov/nerl/research/1999/html, go to “g8—14 html”). Usage of pharmaceuticals and personal care products is only expected to increase; witness, for example, the current emphasis on chemoprevention (e.g., tamoxifen for breast cancer, aspirin for colon cancer, preventive drugs for a possible global flu pandemic). Pharmaceuticals and personal care products are primarily released to the environment via sewage effluents (human excretion as well as disposal down the drain) and application of sewage sludge and manure to land [7, 8]. They have been widely detected in surface waters, soils, and groundwater. Concentrations in receiving waters range from ng/L to low-μg/L concentrations, with widely used pharmaceuticals, such as acetaminophen, ibuprofen, and sulfamethoxazole, reaching the highest concentrations. Concentrations are on the order of ng/g in sediments and ng/kg in biota. Modeling and measurements indicate concentrations are generally below levels of concern other than as regards increased microbial resistance (see, e.g., [9]). In at least one case, however, a potential risk has been identified [10], and scientific uncertainties remain. For example, risk assessments of musks (fragrances in cosmetics, soaps, detergents, and other common products) that have been conducted [11] or that are in progress indicate that they pose negligible environmental risk (D. Salvito, Research Institute for Fragrance Materials, Woodcliff Lake, NJ, USA, personal communication); however, concerns remain (see, e.g., [12]). Pharmaceuticals and personal care products have been the subject of national workshops (see, e.g., [13]) and are currently the subject of specific risk assessment—related research funded within the Sixth Framework Program of the European Union [14]. The European Union program is intended to address uncertainties concerning environmental effects and to develop screening approaches for testing, bioaccumulation, and environmental risk. Endocrine-modulating chemicals are substances derived from both anthropogenic and natural sources. The primary effect of these chemicals is to modify the function of the endocrine system in organisms, including humans, thus affecting the way in which the organism or its progeny develop, grow, or reproduce. These chemicals are ubiquitous in the environment from both natural and anthropogenic sources [15]. To date, evidence for the adverse effects of EMCs focuses on wildlife rather than on humans and remains controversial [16]. Currently, we have no clear indication of adverse human responses to EMCs in drinking water or food. Suggestions of decreased human sperm counts and increased cancers are controversial and remain to be proven; life-style choices, such as smoking, obesity, and diet, appear to have a much greater influence on human health [17]. Effects on wildlife related to EMCs include feminization of sea birds and alligators, apparently because of DDT; feminization of marine snails because of tributyltin; improper development of trout, apparently because of polychlorinated biphenyls and dioxins; feminization or hemaphrodization of fish near some freshwater sewage treatment outfalls [18, 19]; and abnormalities in sexual development of amphipods [20]. Laboratory studies have shown that chlordane and p,p′-dichlorodiphenyltrichloroethane can induce feminization in turtles [21], that some freshwater fish are remarkably sensitive to estrogenic steroids [19], but also that other freshwater fish are relatively insensitive [22]. Evidence for endocrine modulation in wild populations of marine aquatic organisms is restricted to gastropod mollusks, crustaceans, and some fish species [23]. Effects of EMCs may be less in salt water than in freshwater [24]. In some cases, the effects of EMCs may be reversible [25]. Determining any environmental effects of EMCs is difficult at best, because exposures occur at very low levels, effects tend to be subtle, and their manifestation may take years. The ability of single-species laboratory tests to predict the effects of EMCs in the field is doubtful [26], and standard laboratory toxicity test results can be confounded by the presence of natural parasites associated with the test organisms, which have the ability to mediate endocrine pathways [27]. Endocrine-modulating chemicals can affect three general aspects of endocrine function: neural input to the endocrine system, hormonal modulation of the nervous system, and regulation of hormone and receptor biosynthesis, secretion, and metabolism. To date, evidence for effects of EMCs on wildlife outside the laboratory does not extend beyond highly exposed, localized populations. Nanotechnology products comprise existing, new manufactured matter at 1 to 100 nm, such as fullerenes (C60), nano-tubes, quantum dots, and NiO2. Uses are increasing and include golf balls, nanotherapeutic pharmaceuticals, fabrics, cosmetics, ski wax, energy storage products, and so on. Releases to the environment occur during production and following use. The U.S. Environmental Protection Agency is conducting active research into their fate, transport, and ecotoxicology, including production of a Science Policy White Paper from their Cross-Agency Nanotechnology Workgroup (http://www.nano.gov and http://www.epa.gov/ncer/nano). The Organization for Economic Cooperation and Development recently (December 7–9, 2005) hosted an international workshop in Washington, DC, regarding definitions, nomenclature, classification, and human health effects but has not yet focused explicitly on potential environmental effects. The toxicology of nanotechnology products remains to be determined. For example, although antimicrobial activity has been documented [28, 29], the aquatic toxicology of nanotechnology products is virtually unknown. Three mechanisms are possible: Ingestion (e.g., filter feeders), physical disruption, and gill irritation. Lovern and Klaper [30] demonstrated that the behavior of the daphnid Daphnia magna was affected in the laboratory following exposure to fullerenes (∼1 nm; “soccer balls”) and TiO2, and they speculated that the observed behavioral changes could increase predation and, possibly, trophic transfer. Oberdörstere [31] found that fullerenes at concentrations of 1 mg/L caused oxidative damage to the brains of largemouth bass (Micropterus salmoides). In contrast, Ingle et al. [32] showed that quantum dots (microcrystals of CdS, CdTe, or CdSe with a diameter of approximately 3 nm covered by a ZnS shell, which is covered in turn by a layer of covalently bonded organic ligands) were absorbed by the daphnid Ceriodaphnia dubia with no apparent ill effects. Templeton et al. [33] showed that single-walled, nonpurified carbon nanotubes, which have high rigidity, delayed development of meiobenthic estuarine copepodites; however, the same nanotubes were not toxic above environmentally realistic concentrations following electrochemical purification. The reasons for these differences are presently unknown. It is clear that emerging substances provide extensive opportunities for worthwhile research [34], with the emphasis on worthwhile. By this, I mean that the research must focus on the bigger picture, not on minutiae. In other words, it must be both relevant [35] and answer the “So what?” question [36]. Specifically, we need to know the level of information necessary to determine, with reasonable certainty, whether these substances pose unacceptable risks to the environment, including human health. We also need to know how any such risks compare to related risks. For instance, is global warming, which is shrinking polar bear habitats and reducing their ability to forage for food, of more concern than PBDEs and other global organic contaminants accumulating in their tissues? Do the benefits provided by emerging substances outweigh their real (or potential) environmental risks? In the specific case of PBDEs, for example, do reduced human fatalities as a result of fire outweigh potential toxic effects? Similar questions need to be posed for pharmaceuticals but are less applicable to other emerging substances, such as personal care products, which would weigh very lightly in the balance with potential environmental effects. At present, necessary specific and comparative risk assessments have not been conducted, and necessary data for informed decision-making are lacking. Studies that can provide such information are badly needed.

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