Limitations and uncertainties of acute fish toxicity assessments can be reduced using alternative methods

Articles

Adriaens, E., Barroso, J., Eskes, C. et al. (2014). Retrospective analysis of the Draize test for serious eye damage/eye irritation: Importance of understanding the in vivo endpoints under UN GHS/EU CLP for the development and evaluation of in vitro test methods. Arch Toxicol 88, 701-723. doi:10.1007/s00204-013-1156-8

Awkerman, J. A., Raimondo, S., Jackson, C. R. et al. (2014). Augmenting aquatic species sensitivity distributions with interspecies toxicity estimation models. Environ Toxicol Chem 33, 688-695. doi:10.1002/etc.2456

Barroso, J., Pfannenbecker, U., Adriaens, E. et al. (2017). Cosmetics Europe compilation of historical serious eye damage/eye irritation in vivo data analysed by drivers of classification to support the selection of chemicals for development and evaluation of alternative methods/strategies: The Draize eye test Reference Database (DRD). Arch Toxicol 91, 521-547. doi:10.1007/s00204-016-1679-x

Bauer, J. F., Thomas, P. C., Fouchard, S. Y. et al. (2018a). High-accuracy prediction of mechanisms of action using structural alerts. Comput Toxicol 7, 36-45. doi:10.1016/j.comtox.2018.06.004

Bauer, J. F., Thomas, P. C., Fouchard, S. Y. et al. (2018b). A new classification algorithm based on mechanisms of action. Comput Toxicol 5, 8-15. doi:10.1016/j.comtox.2017.11.001

Bejarano, A. C., Raimondo, S. and Barron, M. G. (2017). Framework for optimizing selection of interspecies correlation estimation models to address species diversity and toxicity gaps in an aquatic database. Environ Sci Technol 51, 8158-8165. doi:10.1021/acs.est.7b01493

Belanger, S. E., Rawlings, J. M. and Carr, G. J. (2013). Use of fish embryo toxicity tests for the prediction of acute fish toxicity to chemicals. Environ Toxicol Chem 32, 1768-1783. doi:10.1002/etc.2244

Belanger, S. E., Sanderson, H., Embry, M. R. et al. (2015). It is time to develop ecological thresholds of toxicological concern to assist environmental hazard assessment. Environ Toxicol Chem 34, 2864-2869. doi:10.1002/etc.3132

Benfenati, E., Manganaro, A. and Gini, G. (2013). VEGA-QSAR: AI inside a platform for predictive toxicology. CEUR Workshop Proceedings. http://ceur-ws.org/Vol-1107/

Braunbeck, T., Böhler, S., Knörr, S. et al. (2020). Development of an OECD Guidance Document for the Application of OECD Test Guideline 236 (Acute Fish Embryo Toxicity Test): The chorion structure and biotransformation capacities of zebrafish as boundary conditions for OECD Test Guideline 236 – German contributions to OECD project 2.54: Guidance Document on IATA for Fish Acute Toxicity Testing. UBA Texte 94/2020. https://bit.ly/345BHsc

Bundesgesetzblatt Bundesministerium für Umwelt, Naturschutz und Reaktorsicherheit (2005). Bekanntmachung der Neufassung des Abwasserabgabegesetzes. Teil I, Nr. 5, ausgegeben zu Bonn am 25 Januar 2005. http://extwprlegs1.fao.org/docs/pdf/ger35872b.pdf

Busquet, F., Strecker, R., Rawlings, J. M. et al. (2014). OECD validation study to assess intra- and inter-laboratory reproducibility of the zebrafish embryo toxicity test for acute aquatic toxicity testing. Regul Toxicol Pharmacol 69, 496-511. doi:10.1016/j.yrtph.2014.05.018

Carr, G. J., Bailer, A. J., Rawlings, J. M. et al. (2018). On the impact of sample size on median lethal concentration estimation in acute fish toxicity testing: Is n = 7/group enough? Environ Toxicol Chem 37, 1565-1578. doi:10.1002/etc.4098

Connors, K. A., Beasley, A., Barron, M. G. et al. (2019). Creation of a curated aquatic toxicology database: EnviroTox. Environ Toxicol Chem 38, 1062-1073. doi:10.1002/etc.4382

de-Vlaming, V. and Norberg-King, T. (1999). A review of single species toxicity tests: Are the tests reliable predictors of aquatic ecosystem community responses? EPA/600/R-97/114. https://bit.ly/3c1FI3T

Dimitrov, S., Detroyer, A., Piroird, C. et al. (2016). Accounting for data variability, a key factor in in vivo/in vitro relationships: Application to the skin sensitization potency (in vivo LLNA versus in vitro DPRA) example. J Appl Toxicol 36, 1568-1578. doi:10.1002/jat.3318

ECHA (2008). Guidance on Information Requirements and Chemical Safety Assessment. Chapter R.10: Characterisation of dose [concentration]-response for environment. Guidance for the implementation of REACH. https://bit.ly/37uWfg9

ECHA (2017a). Guidance on Information Requirements and Chemical Safety Assessment. Chapter R.11: PBT/vPvB assessment. Version 3.0. https://echa.europa.eu/guidance-documents/guidance-on-Information-requirements-and-chemical-safety-assessment

ECHA (2017b). Expert Workshop on the potential regulatory application of the Fish Embryo Acute Toxicity (FET) Test under REACH, CLP and the BPR, 3-4 May 2017 in Helsinki.

ECHA (2017c). Guidance on the Application of the CLP Criteria (Version 5.0). https://echa.europa.eu/guidance-documents/guidance-on-clp

EFSA (2014). Scientific opinion on good modelling practice in the context of mechanistic effect models for risk assessment of plant protection products. EFSA J 12, 3589. doi:10.2903/j.efsa.2014.3589

EFSA Scientific Committee, Benford, D., Halldorsson, T. et al. (2018). The principles and methods behind EFSA’s guidance on uncertainty analysis in scientific assessment. EFSA J 16, 235. doi:10.2903/j.efsa.2018.5122

European Commission (2020). Report on the statistics on the number of animals used for experimental and other scientific purposes in the member states of the European Union in 2015-2017. Commission staff working document. https://eur-lex.europa.eu/legal-content/EN/TXT/?qid=1581689520921&uri=CELEX:52020SC0010

Fischer, M., Belanger, S. E., Berckmans, P. et al. (2019). Repeatability and reproducibility of the RTgill-W1 cell line assay for predicting fish acute toxicity. Toxicol Sci 169, 353-364. doi:10.1093/toxsci/kfz057

Hahn, T., Diamond, J., Dobson, S. et al. (2014). Predicted no effect concentration derivation as a significant source of variability in environmental hazard assessments of chemicals in aquatic systems: An international analysis. Integr Environ Assess Manag 10, 30-36. doi:10.1002/ieam.1473

Helman, G., Shah, I., Williams, A. J. et al. (2019). Generalized read-across (GenRA): A workflow implemented into the EPA CompTox chemicals dashboard. ALTEX 36, 462-465. doi:10.14573/altex.1811292

Hoffmann, S., Kinsner-Ovaskainen, A., Prieto, P. et al. (2010). Acute oral toxicity: Variability, reliability, relevance and interspecies comparison of rodent LD50 data from literature surveyed for the ACuteTox project. Regul Toxicol Pharmacol 58, 395-407. doi:10.1016/j.yrtph.2010.08.004

Hoffmann, S., Kleinstreuer, N., Alépée, N. et al. (2018). Non-animal methods to predict skin sensitization (I): The Cosmetics Europe database. Crit Rev Toxicol 48, 344-358. doi:10.1080/10408444.2018.1429385

Hrovat, M., Segner, H. and Jeram, S. (2009). Variability of in vivo fish acute toxicity data. Regul Toxicol Pharmacol 54, 294-300. doi:10.1016/j.yrtph.2009.05.013

Hutchinson, T. H., Barrett, S., Buzby, M. et al. (2003). A strategy to reduce the numbers of fish used in acute ecotoxicity testing of pharmaceuticals. Environ Toxicol Chem 22, 3031-3036. doi:10.1897/02-558

IRGC (2017). Introduction to the IRGC Risk Governance Framework, revised version. International Risk Governance Center. doi:10.1007/978-1-4020-6799-0_6

ISO – International-Standard-Organization (1996a). Water quality – Determination of the acute lethal toxicity of substances to a freshwater fish [Brachydanio rerio Hamilton-Buchanan (Teleostei, Cyprinidae)] – Part 3: Flow-through method. ISO 7346-3:1996. doi:10.3403/00151595u

ISO (1996b). Water quality – Determination of the acute lethal toxicity of substances to a freshwater fish [Brachydanio rerio Hamilton-Buchanan (Teleostei, Cyprinidae)] – Part 2: Semi-static method. ISO 7346-2:1996. doi:10.3403/00151583u

ISO (1996c). Water quality – Determination of the acute lethal toxicity of substances to a freshwater fish [Brachydanio rerio Hamilton-Buchanan (Teleostei, Cyprinidae)] – Part 1: Static method. ISO 7346-1:1996. doi:10.3403/00151583u

ISO (2016). Water quality – Determination of the acute toxicity of waste water to zebrafish eggs (Danio rerio). ISO 15088:2007. doi:10.31030/1495364

ISO (2019). Water quality – Determination of acute toxicity of water samples and chemicals to a fish gill cell line (RTgill-W1). ISO 21115:2019. doi:10.3403/30361171u

Jeram, S., Sintes, J. M., Halder, M. et al. (2005). A strategy to reduce the use of fish in acute ecotoxicity testing of new chemical substances notified in the European Union. Regul Toxicol Pharmacol 42, 218-224. doi:10.1016/j.yrtph.2005.04.005

Kluver, N., Konig, M., Ortmann, J. et al. (2015). Fish embryo toxicity test: Identification of compounds with weak toxicity and analysis of behavioral effects to improve prediction of acute toxicity for neurotoxic compounds. Environ Sci Technol 49, 7002-7011. doi:10.1021/acs.est.5b01910

Knillmann, S., Stampfli, N. C., Beketov, M. A. et al. (2012). Intraspecific competition increases toxicant effects in outdoor pond microcosms. Ecotoxicology 21, 1857-1866. doi:10.1007/s10646-012-0919-y

Lammer, E., Carr, G. J., Wendler, K. et al. (2009). Is the fish embryo toxicity test (FET) with the zebrafish (Danio rerio) a potential alternative for the fish acute toxicity test? Comp Biochem Physiol C Toxicol Pharmacol 149, 196-209. doi:10.1016/j.cbpc.2008.11.006

Lemke, A. (1981). Interlaboratory Comparision: Acute Testing Set. US-EPA EPA-600/S3-81-005. https://nepis.epa.gov/Exe/ZyPURL.cgi?Dockey=2000TSC7.TXT

Leontaridou, M., Urbisch, D., Kolle, S. N. et al. (2017). The borderline range of toxicological methods: Quantification and implications for evaluating precision. ALTEX 34, 525-538. doi:10.14573/altex.1606271

Lillicrap, A., Moe, S. J., Wolf, R. et al. (2020). Evaluation of a Bayesian network for predicting acute fish toxicity from fish embryo toxicity data. Integr Environ Assess Manag 16, 452-460. doi:10.1002/ieam.4258

Low, Y., Sedykh, A., Fourches, D. et al. (2013). Integrative chemical-biological read-across approach for chemical hazard classification. Chem Res Toxicol 26, 1199-1208. doi:10.1021/tx400110f

Luechtefeld, T., Marsh, D., Rowlands, C. et al. (2018). Machine learning of toxicological big data enables read-across structure activity relationships (RASAR) outperforming animal test reproducibility. Toxicol Sci 165, 198-212. doi:10.1093/toxsci/kfy152

Maertens, A., Anastas, N., Spencer, P. J. et al. (2014). Green toxicology. ALTEX 31, 243-249. doi:10.14573/altex.1406181

Moe, S. J., Madsen, A. L., Connors, K. A. et al. (2020). Development of a hybrid Bayesian network model for predicting acute fish toxicity using multiple lines of evidence. Environ Modell Softw 126, 104655. doi:10.1016/j.envsoft.2020.104655

Mora, C., Tittensor, D. P., Adl, S. et al. (2011). How many species are there on Earth and in the ocean? PLoS Biol 9, e1001127. doi:10.1371/journal.pbio.1001127

NRC – National Research Council (2007). Toxicity Testing in the 21st Century: A Vision and a Strategy. Washington, DC, USA: The National Academies Press. doi:10.17226/11970

Natsch, A., Laue, H., Haupt, T. et al. (2018). Accurate prediction of acute fish toxicity of fragrance chemicals with the RTgill-W1 cell assay. Environ Toxicol Chem 37, 931-941. doi:10.1002/etc.4027

Norberg-King, T. J., Embry, M. R., Belanger, S. E. et al. (2018). An international perspective on the tools and concepts for effluent toxicity assessments in the context of animal alternatives: Reduction in vertebrate use. Environ Toxicol Chem 37, 2745-2757. doi:10.1002/etc.4259

OECD (2004). Test No. 202: Daphnia sp. Acute Immobilisation Test. OECD Guidelines for the Testing of Chemicals, Section 2. OECD Publishing, Paris. doi:10.1787/9789264069947-en

OECD (2007). Guidance on Grouping of Chemicals. OECD Series on Testing and Assessment, No. 80. OECD Publishing, Paris. https://bit.ly/37so20A

OECD (2010). Short Guidance on the Threshold Approach for Acute Fish Toxicity. OECD Series of Testing and Assessment, No. 126. OECD Publishing, Paris. https://bit.ly/3mrLsHF

OECD (2011a). Validation Report (Phase 1) for the Zebrafish Embryo Toxicity Test. OECD Series of Testing and Assessment, No. 157. OECD Publishing, Paris. http://www.oecd.org/env/ehs/testing/48572244.pdf

OECD (2011b). Test No. 201: Freshwater Alga and Cyanobacteria, Growth Inhibition Test. OECD Guidelines for the Testing of Chemicals, Section 2. OECD Publishing, Paris. doi:10.1787/9789264069923-en

OECD (2012a). Fish Testing Framework. OECD Series of Testing and Assessment, No. 171. OECD Publishing, Paris. https://bit.ly/3r37l3A

OECD (2012b). Test No. 305: Bioaccumulation in Fish: Aqueous and Dietary Exposure. OECD Guidelines for the Testing of Chemicals. OECD Publishing, Paris. doi:10.1787/9789264185296-en

OECD (2012c). Validation Report (Phase 2) for the Zebrafish Embryo Toxicity Test. OECD Series of Testing and Assessment, No. 179. OECD Publishing, Paris. https://bit.ly/2LFH7Ut

OECD (2013). Test No. 236: Fish Embryo Acute Toxicity (FET) Test. OECD Guidelines for the Testing of Chemicals, Section 2. OECD Publishing, Paris. doi:10.1787/9789264203709-en

OECD (2014). New Guidance Document on an Integrated Approach to Testing and Assessment (IATA) for Skin Corrosion and Irritation. Series of Testing and Assessment, No. 203. OECD Publishing, Paris. https://bit.ly/38cGj1d

OECD (2016). Guidance Document on the Reporting of Defined Approaches to be Used Within Integrated Approaches to Testing and Assessment. OECD Series on Testing and Assessment, No. 255. OECD Publishing, Paris. https://bit.ly/37qsEo2

OECD (2018a). Guidance Document on Integrated Approaches to Testing and Assessment (IATA) for Serious Eye Damage and Eye Irritation. OECD Series on Testing and Assessment, No. 263. OECD Publishing, Paris. doi:10.1787/84b83321-en

OECD (2018b). Guidance Document on Good In Vitro Method Practice (GIVIMP). OECD Series of Testing and Assessment, No. 286. OECD Publishing, Paris. doi:10.1787/9789264304796-21-en

OECD (2019a). Guidance Document on Aqueous-Phase Aquatic Toxicity Testing of Difficult Test Chemicals. OECD Series of Testing and Assessment, No. 23 (second edition). OECD Publishing, Paris. doi:10.1787/0ed2f88e-en

OECD (2019b). Test Guideline No. 203: Fish, Acute Toxicity Testing. OECD Test Guidelines for the Testing of Chemicals, Section 2. OECD Publishing, Paris. doi:10.1787/9789264069961-en

Paparella, M., Colacci, A. and Jacobs, M. N. (2017). Uncertainties of testing methods: What do we (want to) know about carcinogenicity? ALTEX 34, 235-252. doi:10.14573/altex.1608281

Paparella, M., Bennekou, S. H. and Bal-Price, A. (2020). An analysis of the limitations and uncertainties of in vivo developmental neurotoxicity testing and assessment to identify the potential for alternative approaches. Reprod Toxicol 96, 327-336. doi:10.1016/j.reprotox.2020.08.002

Prieto, P., Graepel, R., Gerloff, K. et al. (2019). Investigating cell type specific mechanisms contributing to acute oral toxicity. ALTEX 36, 39-64. doi:10.14573/altex.1805181

Rawlings, J. M., Belanger, S. E., Connors, K. A. et al. (2019). Fish embryo tests and acute fish toxicity tests are interchangeable in the application of the threshold approach. Environ Toxicol Chem 38, 671-681. doi:10.1002/etc.4351

Rufli, H. (2012). Introduction of moribund category to OECD fish acute test and its effect on suffering and LC50 values. Environ Toxicol Chem 31, 1107-1112. doi:10.1002/etc.1779

Russell, W. M. S. and Burch, R. L. (1959). The Principles of Humane Experimental Technique. https://caat.jhsph.edu/principles/the-principles-of-humane-experimental-technique

Schlenk, D., Celander, M., Gallagher, E. et al. (2008). Biotransformation in fishes. In R. T. Di Giulio and D. E. Hinton (eds), The Toxicology of Fishes. Boca Raton, USA: CRC Press. doi:10.1201/9780203647295

Scholz, S., Sela, E., Blaha, L. et al. (2013). A European perspective on alternatives to animal testing for environmental hazard identification and risk assessment. Regul Toxicol Pharmacol 67, 506-530. doi:10.1016/j.yrtph.2013.10.003

Scholz, S., Klüver, N. and Kühne, R. (2016). Analysis of the relevance and adequateness of using Fish Embryo Acute Toxicity (FET) Test Guidance (OECD 236) to fulfil the information requirements and addressing concerns under REACH. Report ECHA-UFZ contract ECHA/2014/341, 1-105.

Stengel, D., Wahby, S. and Braunbeck, T. (2018). In search of a comprehensible set of endpoints for the routine monitoring of neurotoxicity in vertebrates: Sensory perception and nerve transmission in zebrafish (Danio rerio) embryos. Environ Sci Pollut Res Int 25, 4066-4084. doi:10.1007/s11356-017-0399-y

Tanneberger, K., Knobel, M., Busser, F. J. et al. (2013). Predicting fish acute toxicity using a fish gill cell line-based toxicity assay. Environ Sci Technol 47, 1110-1119. doi:10.1021/es303505z

Thomas, P. C., Bicherel, P. and Bauer, F. J. (2019). How in silico and QSAR approaches can increase confidence in environmental hazard and risk assessment. Integr Environ Assess Manag 15, 40-50. doi:10.1002/ieam.4108

US EPA (2001). Final Report: Interlaboratory Variability Study of EPA Short-term Chronic and Acute Whole Effluent Toxicity Test Methods, Vol. 1. EPA 821-B-01-004. Office of Water, U.S. Environmental Protection Agency, Washington, D.C. https://bit.ly/3nraCaU

US EPA (2016). OCSPP 850.1075: Freshwater and Saltwater Fish Acute Toxicity Test. Ecological Effects Test Guidelines. https://www.epa.gov/test-guidelines-pesticides-and-toxic-substances/series-850-ecological-effects-test-guidelines

Vinken, M. and Blaauboer, B. J. (2017). In vitro testing of basal cytotoxicity: Establishment of an adverse outcome pathway from chemical insult to cell death. Toxicol In Vitro 39, 104-110. doi:10.1016/j.tiv.2016.12.004

Volz, D. C., Belanger, S., Embry, M. et al. (2011). Adverse outcome pathways during early fish development: A conceptual framework for identification of chemical screening and prioritization strategies. Toxicol Sci 123, 349-358. doi:10.1093/toxsci/kfr185

WHO – World Health Organization and IPCS – International Programme on Chemical Safety (‎2018)‎. Guidance document on evaluating and expressing uncertainty in hazard characterization. 2nd edition. World Health Organization. https://apps.who.int/iris/handle/10665/259858

Zhao, Q., De Laender, F. and Van Den Brink, P. J. (2020). Community composition modifies direct and indirect effects of pesticides in freshwater food webs. Sci Total Environ 739, 139531. doi:10.1016/j.scitotenv.2020.139531

Zindler, F., Beedgen, F., Brandt, D. et al. (2019). Analysis of tail coiling activity of zebrafish (Danio rerio) embryos allows for the differentiation of neurotoxicants with different modes of action. Ecotoxicol Environ Saf 186, 109754. doi:10.1016/j.ecoenv.2019.109754