Abstract
Many widely used healthcare products contain antiseptics, whose persistence in aquatic environments, soils, and sediments leads to the contamination of ecosystems and adversely affects wildlife. Recently, the impact not only of high but also low doses of contaminants and mixtures of several chemicals has become a focus of concern. In this study, toxicity tests of the antiseptics triclosan (TCS) and triclocarban (TCC) were performed in an aquatic test medium using the nematode Caenorhabditis elegans. Nominal concentrations of TCS and TCC were tested in separate single-substance toxicity tests (96-h-exposure), focussing on growth and reproduction endpoints. Median effective concentrations (EC50s) from the single-substance tests were subsequently used to set up five different ratios of TCS:TCC mixtures leading to the same toxicity. Six dilutions of each mixture ratio were tested for effon reproduction of C. elegans. In the single-substance tests, TCC was about 30 times more toxic than TCS when considering effects on growth and concerning reproduction, TCC was about 50 times more toxic than TCS. For both substances, the toxic effect on reproduction was more pronounced than the one on growth. Low doses of TCS (1–10 µmol L−1) stimulated reproduction by up to 301% compared to the control, which might be due to endocrine disruption or other stress-related compensation responses (hormesis). Neither antiseptic stimulated growth. In the mixtures, increasing amounts of TCC inhibited the stimulatory effects of TCS on reproduction. In addition, the interactions of TCS and TCC were antagonistic, such that mixtures displayed lower toxicity than would have been expected when TCS and TCC mixtures adhered to the principle of concentration addition.
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References
Amorim MJB, Oliveira E, Soares AMVM, Scott-Fordsman JJ (2010) Predicted no effect concentration (PNEC) for triclosan to terrestrial species (invertebrates and plants). Environ Int 36:338–343
Allmyr M, Adolfsson-Erici M, McLachlan MS, Sandborgh-Englund G (2006) Triclosan in plasma and milk from Swedish nursing mothers and their exposure via personal care products. Sci Total Environ 372:87–93
Barros S, Montes R, Quintana JB, Rodil R, Oliveira JMA, Santos MM, Neuparth T (2017) Chronic effects of triclocarban in the amphipod Gammarus locusta: behavioural and biochemical impairment. Ecotoxicol Environ Saf 135:276–283
Baylay AJ, Spurgeon DJ, Svendsen C, Griffin JL, Swain SC, Sturzenbaum SR, Jones OAH (2012) A metabolomics based test of independent action and concentration addition using the earthworm Lumbricus rubellus. Ecotoxicology 21:1436–1447
Belz RG, Cedergreen N, Sorensen H (2008) Hormesis in mixtures—can it be predicted? Sci Total Environ 404:77–87
Bongers T, Ferris H (1999) Nematode community structure as a bioindicator in environmental monitoring. Trends Ecol Evol 14:224–228
Boyd WA, McBride SJ, Rice JR, Snyder DW, Freedman JH (2010) A high-throughput method for assessing chemical toxicity using a Caenorhabditis elegans reproduction assay. Toxicol Appl Pharmacol 245:153–159
Brausch JM, Rand GM (2011) A review of personal care products in the aquatic environment: environmental concentrations and toxicity. Chemosphere 82:1518–1532
Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77:71–94
Brinke M, Höss S, Fink G, Ternes TA, Heininger P, Traunspurger W (2010) Assessing effects of the pharmaceutical ivermectin on meiobenthic communities using freshwater microcosms. Aquat Toxicol 99:126–137
Brinke M, Heininger P, Traunspurger W (2011) A semi-fluid gellan gum medium improves nematode toxicity testing. Ecotoxicol Environ Safe 74:1824–1831
Calabrese EJ, Baldwin L (2001) Hormesis: a generalizable and unifying hypothesis. Crit Rev Toxicol 31:353–424
Calabrese EJ, Blain R (2005) The occurrence of hormetic responses in the toxicological literature, the hormesis database: an overview. Toxicol Appl Pharmacol 202:289–301
Cedergreen N, Ritz C, Streibig JC (2005) Improved empirical models describing hormesis. Environ Toxicol Chem 24:3166–3172
Chalew TEA, Halden RU (2009) Environmental exposure of aquatic and terrestrial biota to triclosan and triclocarban. J Am Water Resour Assoc 45:4–13
Chen J, Ahn KC, Gee NA, Ahmed MI, Duleba AJ, Zhao L, Gee SJ, Hammock BD, Lasley BL (2008) Triclocarban enhances testosterone action: a new type of endocrine disruptor? Endocrinology 149:1173–1179
Coogan MA, Edziyie RE, La Point TW, Venables BJ (2007) Algal bioaccumulation of triclocarban, triclosan, and methyl-triclosan in a North Texas wastewater treatment plant receiving stream. Chemosphere 67:1911–1918
Coogan MA, LaPoint TW (2008) Snail bioaccumulation of triclocarban, triclosan and methyltriclosan in a North Texas, USA, stream affected by wastewater treatment plant runoff. Environ Toxicol Chem 27:1788–1793
Crofton KM, Paul KB, Devito MJ, Hedge JM (2007) Short-term in vivo exposure to the water contaminant triclosan: evidence for disruption of thyroxine. Environ Toxicol Pharmacol 24:194–197
Dhillon GS, Kaur S, Pulicharla R, Brar SK, Cledón M, Verma M, Surampalli R (2015) Triclosan: current status, occurrence, environmental risks and bioaccumulation potential. Int J Environ Res Public Health 12:5657–5684
Ding T, Li K, Yang M, Bao L, Li J, Yang B, Gan J (2018) Biodegradation of triclosan in diatom Navicula sp.: kinetics, transformation products, toxicity evaluation and the effects of pH and potassium permanganate. J Hazard Mater 334:200–209
Dussault ÈB, Balakrishnan VK, Sverko E, Solomon KR, Sibley PK (2008) Toxicity of human pharmaceutical and personal care products to benthic invertebrates. Environ Toxicol Chem 27:425–432
Escalada MG, Harwood JL, Maillard JY, Ochs D (2005) Triclosan inhibition of fatty acid synthesis and its effect on growth of Escherichia coli and Pseudomonas aeruginosa. J Antimicrob Chemother 55:879–882
Geiß C, Ruppert K, Heidelbach T, Oehlmann J (2016) The antimicrobial agents triclocarban and triclosan as potent modulators of reproduction in Potamopyrgus antipodarum (Mollusca: Hydrobiidae). J Environ Sci Health Part A 51:1173–1179
Giudice BD, Young TM (2010) The antimicrobial triclocarban stimulates embryo production in the freshwater mudsnail Potamopyrgus antipodarum. Environ Toxicol Chem 29:966–970
González-Pérez BK, Sarma SSS, Castellanos-Páez ME, Nandini S (2018) Multigenerational effects of triclosan on the demography of Plationus patulus and Brachionus havanaensis (ROTIFERA). Ecotoxicol Environ Saf 147:275–282
Halden RU, Paull DH (2005) Co-occurrence of triclocarban and triclosan in U.S. water resources. Environ Sci Technol 39:1420–1426
Halden RU (2014) On the need and speed of regulating triclosan and triclocarban in the United States. Environ Sci Technol 48:3603–3611
Höss S, Weltje L (2007) Endocrine disruption in nematodes: effects and mechanisms. Ecotoxicology 16:15–28
Höss S, Williams PL (2009) Ecotoxicity testing with nematodes. In: Wilson MJ, Kakouli-Duarte T eds Nematodes as environmental indicators. CAB International, Wallingford, CT, p 208–224
International Organization for Standardization (2010) Water quality—determination of the toxic effect of sediment and soil samples on growth, fertility and reproduction of Caenorhabditis elegans (Nematoda). ISO 10872:2010, Geneva
Kostrouch Z, Kostrouchova M, Rall JE (1995) Steroid/thyroid hormone receptor genes in Caenorhabditis elegans. Proc Natl Acad Sci 92:156–159
Liu F, Ying GG, Yang LH, Zhou QX (2009) Terrestrial ecotoxicological effects of the antimicrobial agent triclosan. Ecotoxicol Environ Saf 72:86–92
Ludewig AH, Kober-Eisenmann C, Weitzel C, Bethke A, Neubert K, Gerisch B, Hutter H, Anetbi A (2017) A novel nuclear receptor/coregulator complex controls C. elegans lipid metabolism, larval development, and aging. Genes Dev 18:2120–2133
Martínez-Paz P, Morales M, Urien J, Morcillo G, Martínez-Guitarte JL (2017) Endocrine-related genes are altered by antibacterial agent triclosan in Chironomus riparius aquatic larvae. Ecotoxicol Environ Saf 140:185–190
McMurry LM, Oethinger M, Levy SB (1998) Triclosan targets lipid synthesis. Nature 394:531–532
Mimoto A, Fujii M, Usami M, Shimamura M, Hirabayashi N, Kaneko T, Sasagawa N, Ishiura S (2007) Identification of an estrogenic hormone receptor in Caenorhabditis elegans. Biochem Biophys Res Commun 364:883–888
Orvos DR, Versteeg DJ, Inauen J, Capdevielle M, Rothenstein A, Cunningham V (2002) Aquatic toxicity of triclosan. Environ Toxicol Chem 21:1338–1349
Peng Y, Luo Y, Nie XP, Liao W, Yang YF, Ying GG (2013) Toxic effects of triclosan on the detoxification system and breeding of Daphnia magna. Ecotoxicology 22:1384–1394
Perron MM, Ho KT, Cantwell MG, Burgess RM, Pelletier MC (2012) Effects of triclosan on marine benthic and epibenthic organisms. Environ Toxicol Chem 31:1861–1866
Qifeng B, Li G, Tao Y (2012) Toxicity of low concentration exposures of triclosan and triclocarban on Tetrahymena thermophila. Environ Chem 31:720–725
R Development Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org
Raut SA, Angus RA (2010) Triclosan has endocrine-disrupting effects in male western mosquitofish, Gambusia affinis. Environ Toxicol Chem 29:1287–1291
Ristau K, Akgül Y, Bartel AS, Fremming J, Müller MT, Reiher L, Stapela F, Splett JP, Spann N (2015) Toxicity in relation to mode of action for the nematode Caenorhabditis elegans: acute-to-chronic ratios and quantitative structure–activity relationships. Environ Toxicol Chem 34:2347–2353
Ritz C (2009) Toward a unified approach to dose-response modeling in ecotoxicology. Environ Toxicol Chem 29:220–229
Rowett CJ, Hutchinson TH, Comber SD (2016) The impact of natural and anthropogenic dissolved organic carbon (DOC), and pH on the toxicity of triclosan to the crustacean Gammarus pulex (L.). Sci Total Environ 565:222–231
Schultz MM, Bartell SE, Schoenfuss HL (2012) Effects of triclosan and triclocarban, two ubiquitous environmental contaminants, on anatomy, physiology, and behaviour of the fathead minnow (Pimephales promelas). Arch Environ Contam Toxicol 63:114–124
Singer H, Müller S, Tixier C, Pillonel L (2002) Triclosan: occurrence and fate of a widely used biocide in the aquatic environment: field measurements in wastewater treatment plants, surface waters, and lake sediments. Environ Sci Technol 36:4998–5004
Snyder EH, O’Connor GA, McAvoy DC (2011) Toxicity and bioaccumulation of biosolids-borne triclocarban (TCC) in terrestrial organisms. Chemosphere 82:460–467
Tamura I, Kagota K, Yasuda Y, Yoneda S, Morita J, Nakada N, Kameda Y, Kimura K, Tatarazako N, Yamamoto H (2012) Ecotoxicity and screening level ecotoxicological risk assessment of five antimicrobial agents: triclosan, triclocarban, resorcinol, phenoxyethanol and p-thymol. J Appl Toxicol 33:1222–1229
Tatarazako N, Ishibashi H, Teshima K, Kishi K, Arizono K (2004) Effects of triclosan on various aquatic organisms. Environ Sci 11:133–140
Traunspurger W, Haitzer M, Höss S, Beier S, Ahlf W, Steinberg C (1997) Ecotoxicological assessment of aquatic sediments with Caenorhabditis elegans (Nematoda)—a method for testing liquid medium and whole-sediment samples. Environ Toxicol Chem 16:245–250
Traunspurger W, Michiels IC, Eyualem-Abebe (2006) Composition and distribution of free-living freshwater nematodes: global and local perspectives. In: Abebe E, Andrassy I, Traunspurger W (eds) Freshwater nematodes: ecology and taxonomy. CABI Publishing, Wallingford, p 46–76
Ura K, Kai T, Sakata S, Iguchi T, Arizono K (2002) Aquatic acute toxicity testing using the nematode Caenorhabditis elegans. J Health Sci 48:583–586
Wang P, Du Z, Gao S, Zhang X, Giesy JP (2016) Impairment of reproduction of adult zebrafish (Danio rerio) by binary mixtures of environmentally relevant concentrations of triclocarban and inorganic mercury. Ecotoxicol Environ Saf 134:124–132
Weltje L, Vom Saal FS, Oehlmann J (2005) Reproductive stimulation by low doses of xenoestrogens contrasts with the view of hormesis as an adaptive response. Hum Exp Toxicol 24:431–437
Witorsch RJ (2014) Risk assessment of triclosan [Irgasan] in human breast milk. Crit Rev Toxicol 44:535–555
Xu X, Lu Y, Zhang D, Wang Y, Zhou X, Xu H, Mei Y (2015) Toxic assessment of triclosan and triclocarban on Artemia salina. Bull Environ Contam Toxicol 95:728–733
Yang LH, Ying GG, Su HC, Strauber JL, Adams MS, Binet MT (2007) Growth-inhibiting effects of 12 antibacterial agents and their mixtures on the freshwater microalga Pseudokirchneriella subcapitata. Environ Toxicol Chem 27:1201–1208
Zhang L, Niu J, Wang Y (2016) Full life-cycle toxicity assessment on triclosan using rotifer Brachionus calyciflorus. Ecotoxicol Environ Saf 127:30–35
Acknowledgements
We thank Stefanie Gehner for her support during the lab work, Prof. Dr. Walter Traunspurger for helpful remarks and the German Federal Environmental Foundation (DBU) for supporting this project.
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Nicole Spann currently works for an independent scientific consulting company offering services for the registration of agrochemicals. The remaining author declares that she has no conflict of interest
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Vingskes, A.K., Spann, N. The toxicity of a mixture of two antiseptics, triclosan and triclocarban, on reproduction and growth of the nematode Caenorhabditis elegans. Ecotoxicology 27, 420–429 (2018). https://doi.org/10.1007/s10646-018-1905-9
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DOI: https://doi.org/10.1007/s10646-018-1905-9