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Current Risk Assessment Frameworks Misjudge Risks of Hydrophobic Chemicals Henriette Selck*,† and Valery E. Forbes‡ †

Department of Science and Environment, Roskilde University, Universitetsvej 1, 4000 Roskilde, Denmark College of Biological Sciences, University of Minnesota, 1475 Gortner Ave, St. Paul, Minnesota 55108, United States on their potential to persist (P) in the environment, bioaccumulate (B) in biota, and their toxicity (T): Compounds categorized as PBT are considered harmful to the environment, and will be listed in the “candidate list” for authorization, can be prioritized for assessment and eventually be allocated a deadline date after which their use is prohibited in the EU.4 Generally, authorization will not be granted for products containing PBT compounds.4 Because REACH not only regulates chemicals produced in the EU but also imported products and substances, its impact is global. The Toxic Substances Control Act (TSCA) in the U.S. is based on similar criteria.5 Given the potential economic and societal consequences of REACH and TSCA decisions, it is essential that the risk assessments on which such decisions are made are as accurate as possible. Historically, environmental aquatic risk assessment has focused on exposure via water, based on the assumption that only dissolved contaminants are available for uptake in biota. Consequently, much of the available standardized test guidelines6 and published literature are based on simple water-only exposure scenarios in which organisms are exposed to contaminants in dissolved form. Bioaccumulation is assessed based on a bioconcentration factor derived from water-only ur ability to ensure safe and sustainable use of the more exposures relating the contaminant concentration in an than 100 000 chemicals on the market relies on accurate organism to the concentration in water. Persistence is evaluated methods to assess risks to human health and the environment. by measuring the compound’s microbial degradation half-lives Despite increasing awareness that many organisms take up in water, sediment or soil (in the absence of eukaryotes). Here, hydrophobic organic chemicals (HOCs) through their diet a general assumption is that HOCs are persistent in the rather than by diffusion over body surfaces, the majority of environment due to their sorption to sediment.7 Toxicity is chemical regulatory frameworks assess environmental impacts usually focused on common pelagic test species (e.g., algae, of these chemicals on the basis of persistence, bioaccumulation daphnia, fish) in water-only exposures with mortality as the main endpoint. These approaches will lead to inaccurate risk potential and toxicity during exposure to water. HOCs do not assessments, especially for HOCs. HOCs exhibit low water dissolve well in the aquatic environment but sorb to suspended solubility and high affinity for organic matter (e.g., living and particulate matter, precipitate and concentrate in sediments, nonliving particles), which makes it extremely difficult to often to levels several orders of magnitude higher than in water. experimentally determine bioaccumulation and toxicity using Organisms that eat sediment are exposed to HOCs through standard water-only systems.7 their diet. We argue that restricting focus to water exposure and The continuing focus of existing risk assessment tools and ignoring eukaryote metabolism are likely to misjudge risk and methods on water exposure adds uncertainty to risk assesstherefore undermine the sustainable use of chemicals. ments of HOCs. First, in nature, particle-bound HOC Ensuring sustainable use of chemicals requires balancing the concentrations (e.g., in sediment) are magnitudes higher than benefits of chemical substances to human societies with their in the overlying water,7 suggesting that particle- and sedimentrisks to the environment and human health. Hydrophobic eating organisms are more appropriate as test species. Second, organic chemicals (HOCs) are an important class of substances increasing evidence shows that particle/sediment-associated worldwide, including petroleum, solvents, and pesticides, that HOCs are available for uptake in biota, and that the importance have a wide variety of industrial uses and that may pose risks 1 of particle ingestion increases with hydrophobicity, exceeding when released to the environment. The European Union that of uptake over respiratory surfaces via water exposure for regulation, REACH (Registration, Evaluation, Authorisation, and Restriction of Chemicals2), is the strictest chemical regulatory law to date and is expected to influence industries Received: January 15, 2018 worldwide.3 Under REACH, contaminants are assessed based ‡

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© XXXX American Chemical Society

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DOI: 10.1021/acs.est.8b00265 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

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Environmental Science & Technology

Figure 1. Scheme illustrating the diversity of the marine/estaurine benthic community regarding habitat, mobility, and feeding modes.12

as possible. This can only be accomplished by including aquatic sediments and the organisms that feed on them in assessing the environmental risks of HOCs. Figure 1

highly hydrophobic chemicals (e.g., PAHs, PCBs). In other words, the HOC body burden in many aquatic organisms stems primarily from dietary uptake.7−11 Basing risk assessments on water exposure severely underestimates HOC bioaccumulation and, thus, trophic transfer in cases in which dietary uptake dominates. Third, the critical body residue (CBR; above which adverse effects occur) is related to uptake route. This means that organism body burden does not necessarily reflect toxicity. Although sparsely investigated, the general picture is that the CBR of HOCs depends on uptake route, with a higher CBR (i.e., lower toxicity) for contaminants taken up via food than from the dissolved phase.8 Guidelines considering water exposure alone in assessing CBR overestimate HOC toxicity in wildlife because current risk assessments consider wildlife body burdens that exceed CBR to indicate adverse impact. Fourth, the capacity of some sediment-feeding organisms to metabolize HOCs may exceed that of microbial degradation substantially,8,10 which leads to overestimates of P and B criteria.11Fifth, interactions between microbes and eukaryotes enhance microbial activity, which may further increase microbial degradation, thereby decreasing P below what is measured in standard tests. Applying inappropriate exposure scenarios for HOCs increases uncertainty in the categorization of chemicals and may lead to a requirement for substitution based on the wrong conclusions. Assumptions inherent in current approaches are appropriate for highly water-soluble compounds but add uncertaintyin both directionsfor HOCs. Ignoring dietary uptake underestimates B (and hence risk), whereas basing toxicity thresholds (CBRs) on water exposure overestimates T (and hence risk). Ignoring the role of eukaryotes and eukaryote-microbe interactions in HOC biodegradation may lead to overestimates of P (and hence risk). In combination, these interacting sources of uncertainty may lead to less risky chemicals being inadvertently substituted for more dangerous chemicals, which is clearly undesirable. Maximizing the benefits that society derives from chemicals while minimizing chemical risks to human health and the environment requires that risk assessments be based on valid assumptions and are as accurate



AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. ORCID

Henriette Selck: 0000-0002-2859-7596 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS H. Selck acknowledge the support of the Centre European des Silicones (CEH, Project no: 021444/5040/07/0226). REFERENCES

(1) Nicklisch, S. C. T.; Rees, S. D.; McGrath, A. P.; Gökirmak, T.; Bonito, L. T.; Vermeer, L. M.; Cregger, C.; Loween, G.; Sandin, S.; Chang, G.; Hamdoun, A. Global marine pollutants inhibit Pglycoprotein: Environmental levels, inhibitory effects, and cocrystal structure. Sci. Adv. 2016, 2 (4), e1600001. (2) EC: Regulation (EC) No 1907/2006 of the European Parliament and of the Council of 18 December 2006 concerning the Registration, Evaluation, Authorisation and Restriction of Chemicals (REACH), establishing a European Chemicals Agency, amending Directive 1999/ 45/EC and repealing Council Regulation (EEC) No 793/93 and Commission Regulation (EC) No 1488/94 as well as Council Directive 76/769/EEC and Commission Directives 91/155/EEC, 93/67/EEC, 93/105/EC and 2000/21/EC; 2006. http://eur-lex. europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:02006R190720161011&from=EN (accessed August 19, 2017). (3) Denison, R. A. Cross the pond: Assessing REACH’s first big impact on US companies and chemicals. www.edf.org/sites/default/ files/8538_Across_Pond_Report.pdf (accessed August 17, 2017). (4) Rauert, C.; Friesen, A.; Hermann, G.; Jöhncke, U.; Kehrer, A.; Neumann, M.; Prutz, I.; Schönfeld, J.; Wiemann, A.; Willhaus, K.; Wö l tjen, J.; Duquesne, S. Proposal for a harmonized PBT identification across different regulatory frameworks. Environ. Sci. Eur. 26, 9 (2014).910.1186/2190-4715-26-9 B

DOI: 10.1021/acs.est.8b00265 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

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Environmental Science & Technology (5) United States Environmental Protection Agency: the Frank R. Lautenberg chemical safety for the 21st century act. www.epa.gov/ assessing-and-managing-chemicals-under-tsca/frank-r-lautenbergchemical-safety-21st-century-act-1 (accessed September 19, 2017). (6) OECD guidelines for testing of chemicals. Overview. on water exposure. www.oecd-ilibrary.org/environment/oecd-guidelines-forthe-testing-of-chemicals-section-2-effects-on-biotic-systems_20745761 (accessed August 17, 2017). (7) McKay, D.; Powell, D. E.; Woodburn, K. B. Bioconcentration and aquatic toxicity of superhydrophobic chemicals: a modelling case study of cyclic volatile methyl siloxanes. Environ. Sci. Technol. 2015, 49, 11913−11922. (8) Selck, H.; Palmqvist, A.; Forbes, V. E. Biotransformation of dissolved and sediment-bound fluoranthene in the polychaete, Capitella sp. I. Environ. Toxicol. Chem. 2004, 22 (10), 2364−2374. (9) Lu, X.; Reible, D. D.; Fleeger, J. W. 2004. Relative importance of ingested sediment versus pore water as uptake routes for PAHs to the deposit-feeding oligochaete Ilyodrilus templetoni. Arch. Environ. Contam. Toxicol. 2004, 47, 207−214. (10) Dai, L.; Selck, H.; Salvito, D.; Forbes, V. E. Fate and effects of acetyl cedrene in sediment inhabited by the deposit feeder. Environ. Toxicol. Chem. 2012, 31 (11), 2639−2646. (11) Selck, H.; Drouillard, K.; Koelmans, A. A.; Palmqvist, A.; Ruus, A.; Salvito, D.; Schultz, I.; Stewart, R.; Weisbrod, A.; van den Brink, N.; van den Heuvel-Greve, M. Explaining variability of bioaccumulation measurements between laboratory and field using a modelling approach. Integr. Environ. Assess. Manage. 2012, 8 (1), 42−63. (12) http://slideplayer.com/slide/8493972/.

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DOI: 10.1021/acs.est.8b00265 Environ. Sci. Technol. XXXX, XXX, XXX−XXX