Abstract
Triclosan (TCS) is an antibacterial and antifungal agent widely used in personal care products, and it has been frequently detected in the aquatic environment. In the present study, the acute toxicity of TCS to Daphnia magna, Photobacterium phosphoreum, Danio rerio, and Limnodrilus hoffmeisteri was assessed under different pH conditions. Generally, TCS was more toxic to the four aquatic organisms in acidic medium. The LC50 values for D. magna and D. rerio were smaller among the selected species, suggesting that D. magna and D. rerio were more sensitive to TCS. In addition, the oxidative stress-inducing potential of TCS was evaluated in Carassius auratus at three pH values. Changes of superoxide dismutase (SOD) and catalase (CAT) activity, glutathione (GSH) level, and malondialdehyde (MDA) content were commonly observed in all TCS exposure groups, indicating the occurrence of oxidative stress in the liver of C. auratus. The integrated biomarker response (IBR) index revealed that a high concentration of TCS induced great oxidative stress in goldfish under acidic condition. This work supplements the presently available data on the toxicity data of TCS, which would provide some useful information for the environmental risk assessment of this compound.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adolfsson-Erici M, Pettersson M, Parkkonen J, Sturve J (2002) Triclosan, a commonly used bactericide found in human milk and in the aquatic environment in Sweden. Chemosphere 46(9–10):1485–1489. https://doi.org/10.1016/S0045-6535(01)00255-7
Ahn KC, Zhao B, Chen J, Cherednichenko G, Sanmarti E, Denison MS, Lasley B, Pessah IN, Kültz D, Chang DPY, Gee SJ, Hammock BD (2008) In vitro biologic activities of the antimicrobials triclocarban, its analogs, and triclosan in bioassay screens: receptor-based bioassay screens. Environ Health Perspect 116(9):1203–1210. https://doi.org/10.1289/ehp.11200
Asimakopoulos AG, Thomaidis NS, Kannan K (2014) Widespread occurrence of bisphenol A diglycidyl ethers, p-hydroxybenzoic acid esters (parabens), benzophenone type-UV filters, triclosan, and triclocarban in human urine from Athens, Greece. Sci Total Environ 470–471:1243–1249
Bedoux G, Roig B, Thomas O, Dupont V, Le Bot B (2012) Occurrence and toxicity of antimicrobial triclosan and by-products in the environment. Environ Sci Pollut Res Int 19(4):1044–1065
Beliaeff B, Burgeot T (2002) Integrated biomarker response: a useful tool for ecological risk assessment. Environ Toxicol Chem 21(6):1316–1322. https://doi.org/10.1002/etc.5620210629
Bradford MM (1976) A rapid and sensitive method for quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1–2):248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Brookes PS, Yoon Y, Robotham JL, Anders MW, Sheu SS (2004) Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am J Physiol Cell Physiol 287:817–833
Cherednichenko G, Zhang R, Bannister RA, Timofeyev V, Li N, Fritsch EB, Feng W, Barrientos GC, Schebb NH, Hammock BD, Beam KG, Chiamvimonvat N, Pessah IN (2012) Triclosan impairs excitation-contraction coupling and Ca2+ dynamics in striated muscle. Proc Natl Acad Sci U S A 109(35):14158–14163. https://doi.org/10.1073/pnas.1211314109
Ciba Specialty Chemicals (2001) General information on chemical, physical and microbiological properties of Irgasan DP300, Irgacare MP and Irgacide LP10. Brochure 2520. Publication AgB2520e.02. Basel, Switzerland
Ciniglia C, Cascone C, Giudice RL, Pinto G, Pollio A (2005) Application of methods for assessing the geno- and cytotoxicity of triclosan to C. ehrenbergii. J Hazard Mater 122:227–232
Claiborne A (1985) Catalase activity. In: Greenwald RA (ed) Handbook of methods for oxygen radical research. CRC, Boca Raton, pp 283–284
Dai ZM, Liu XM, Wu JJ, Xu JM (2013) Impacts of simulated acid rain on recalcitrance of two different soils. Environ Sci Pollut Res 20(6):4216–4224. https://doi.org/10.1007/s11356-012-1288-z
Damiens G, Gnassia-Barelli M, Loques F, Romeo M, Salbert V (2007) Integrated biomarker response index as a useful tool for environmental assessment evaluated using transplanted mussels. Chemosphere 66:574–583
Dautremepuits C, Marcogliese DJ, Gendron AD, Fournier M (2009) Gill and head kidney antioxidant processes and innate immune system responses of yellow perch (Perca flavescens) exposed to different contaminants in the St. Lawrence River, Canada. Sci Total Environ 407(3):1055–1064. https://doi.org/10.1016/j.scitotenv.2008.10.004
Dayan AD (2007) Risk assessment of triclosan [Irgasan®] in human breast milk. Food Chem Toxicol 45(1):125–129. https://doi.org/10.1016/j.fct.2006.08.009
De Schamphelaere KAC, Heijerick DG, Janssen CR (2004) Comparison of the effect of different pH buffering techniques on the toxicity of copper and zinc to Daphnia magna and Pseudokirchneriella subcapitata. Ecotoxicology 13(7):697–705. https://doi.org/10.1007/s10646-003-4429-9
Dhillon GS, Kaur S, Pulicharla R, Brar SK, Cledon M, Verma M, Surampalli RY (2015) Triclosan: current status, occurrence, environmental risks and bioaccumulation potential. Int J Envirn Res Public Health 12(5):5657–5684. https://doi.org/10.3390/ijerph120505657
Esterbauer H, Zollner H, Schaur RJ (1990) Aldehydes formed by lipid peroxidation: mechanisms of formation, occurrence, and determination. In: Vigo-Pelfrey C (ed) Membrane lipid oxidation. CRC, Boca Raton, pp 239–268
Fair PA, Lee HB, Adams J, Darling C, Pacepavicius G, Alaee M, Bossart GD, Henry N, Muir D (2009) Occurrence of triclosan in plasma of wild Atlantic bottlenose dolphins (Tursiops truncatus) and in their environment. Environ Pollut 157(8–9):2248–2254. https://doi.org/10.1016/j.envpol.2009.04.002
Flohe L, Otting F (1984) Superoxide dismutase assays. Method Enzym 105:93–104. https://doi.org/10.1016/S0076-6879(84)05013-8
Gao L, Yuan T, Cheng P, Bai QF, Zhou CQ, Ao JJ, Wang WH, Zhang HM (2015) Effects of triclosan and triclocarban on the growth inhibition, cell viability, genotoxicity and multixenobiotic resistance responses of Tetrahymena thermophila. Chemosphere 139:434–440. https://doi.org/10.1016/j.chemosphere.2015.07.059
He Q, Wang XH, Sun P, Wang ZY, Wang LS (2015) Acute and chronic toxicity of tetrabromobisphenol A to three aquaticspecies under different pH conditions. Aquat Toxicol 164:145–154. https://doi.org/10.1016/j.aquatox.2015.05.005
Hinther A, Bromba CM, Wulff JE, Helbing CC (2011) Effects of triclocarban, triclosan, and methyl triclosan on thyroid hormone action and stress in frog and mammalian culture systems. Environ Sci Technol 45(12):5395–5402. https://doi.org/10.1021/es1041942
Hua WY, Bennett ER, Letcher RJ (2005) Triclosan in waste and surface waters from the upper Detroit River by liquid chromatography–electrospray–tandem quadrupole mass spectrometry. Environ Int 31(5):621–630. https://doi.org/10.1016/j.envint.2004.10.019
Huang XL, Tu YN, Song CF, Li TC, Lin J, Wu YH, Liu JT, Wu CX (2016) Interactions between the antimicrobial agent triclosan and the bloom-forming cyanobacteria Microcystis aeruginosa. Aquat Toxicol 172:103–110. https://doi.org/10.1016/j.aquatox.2016.01.002
Hwang J, Suh SS, Chang M, Yun Park S, Ryu TK, Lee S, Lee TK (2014) Effects of triclosan on reproductive prarmeters and embryonic development of sea urchin, Strongylocentrotus nudus. Ecotoxicol Environ Saf 100:148–152. https://doi.org/10.1016/j.ecoenv.2013.10.029
Jollow DJ, Mitchell JR, Zampagilone N, Gilete JR (1974) Bromobenzene-induced liver necrosis: protective role of glutathione and evidence for 3,4-bromo benzene oxide as the hepatotoxic metabolite. Pharmacology 11(3):151–169. https://doi.org/10.1159/000136485
Jungclaus GA, Lopez-Avila V, Hites RA (1978) Organic compounds in an industrial wastewater: a case study of their environmental impact. Environ Sci Technol 12:88–96
Kim J, Park J, Kim PG, Lee C, Choi K, Choi K (2010a) Implication of global environmental changes on chemical toxicity effect of water temperature, pH, and ultraviolet B irradiation on acute toxicity of several pharmaceuticals in Daphnia magna. Ecotoxicology 19(4):662–669. https://doi.org/10.1007/s10646-009-0440-0
Kim WK, Lee SK, Jung J (2010b) Integrated assessment of biomarker responses in common carp (Cyprinus carpio) exposed to perfluorinated organic compounds. J Hazard Mater 180(1–3):395–400. https://doi.org/10.1016/j.jhazmat.2010.04.044
Li CG, Qin L, Qu RJ, Sun P, Wang ZY (2016) Responses of antioxidant defense system to polyfluorinated dibenzo-p-dioxins (PFDDs) exposure in liver of freshwater fish Carassius auratus. Ecotoxicol Environ Saf 126:170–176. https://doi.org/10.1016/j.ecoenv.2015.12.036
Lin DS, Zhou QX, Xie XJ, Liu Y (2010) Potential biochemical and genetic toxicity of triclosan as an emerging pollutant on earthworms (Eisenia fetida). Chemosphere 81(10):1328–1333. https://doi.org/10.1016/j.chemosphere.2010.08.027
Lindström A, Buerge IJ, Poiger T, Bergqvist PA, Müller MD, Buser HR (2002) Occurrence and environmental behavior of the bactericide triclosan and its methyl derivative in surface waters and in wastewater. Environ Sci Technol 36(11):2322–2329. https://doi.org/10.1021/es0114254
Liu H, Sun P, Liu HX, Yang SG, Wang LS, Wang ZY (2015) Acute toxicity of benzophenone-type UV filters for Photobacterium phosphoreum and Daphnia magna: QSAR analysis, interspecies relationship and integrated assessment. Chemosphere 135:182–188. https://doi.org/10.1016/j.chemosphere.2015.04.036
Livingstone DR, Martinez PG, Michel X, Narbonne JF, O’Hara S, Ribera D, Winston GW (1990) Oxyradical production as a pollution-mediated mechanism of toxicity in the common mussel, Mytilus edulis L., and other molluscs. Funct Ecol 4(3):415–424. https://doi.org/10.2307/2389604
Lopez-Avila V, Hites RA (1980) Organic compounds in an industrial wastewater. Their transport into sediments. Environ Sci Technol 14(11):1382–1390. https://doi.org/10.1021/es60171a007
Luo Y, Su Y, Lin RZ, Shi HH, Wang XR (2006) 2-Chlorophenol induced ROS generation in fish Carassius auratus based on the EPR method. Chemosphere 65(6):1064–1073. https://doi.org/10.1016/j.chemosphere.2006.02.054
Lushchak VI (2011) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101(1):13–30. https://doi.org/10.1016/j.aquatox.2010.10.006
Lyndall J, Fuchsman P, Bock M, Barber T, Lauren D, Leigh K, Perruchon E, Capdevielle M (2010) Probabilistic risk evaluation for triclosan in surface water, sediments, and aquatic biota tissues. Integr Environ Asses 6(3):419–440. https://doi.org/10.1897/IEAM_2009-072.1
Marlatt VL, Veldhoen N, Lo BP, Bakker D, Rehaume V, Vallee K, Haberl M, Shang D, Van Aggelen GC, Skirrow RC, Elphick JR, Helbing CC (2013) Triclosan exposure alters postembryonic development in a Pacific tree frog (Pseudacris regilla) amphibian metamorphosis assay (TREEMA). Aquat Toxicol 126:85–94. https://doi.org/10.1016/j.aquatox.2012.10.010
Mates JM (2000) Effects of antioxidant enzymes in the molecular control of reactive oxygen species toxicology. Toxicology 153(1–3):83–104. https://doi.org/10.1016/S0300-483X(00)00306-1
McAvoy DC, Schatowitz B, Jacob M, Hauck A, Eckhoff WS (2002) Measurement of triclosan in wastewater treatment systems. Environ Toxicol Chem 21(7):1323–1329
McCord JM, Fridovich I (1969) Superoxide dismutase an enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244(22):6049–6055
Ministry of Environmental Protection of the People’s Republic of China (1991a) Water quality-determination of the acute toxicity of substances to Daphnia (D. magna straus). GB/T 13266-1991
Ministry of Environmental Protection of the People’s Republic of China (1991b) Water quality-determination of the acute toxicity of substances to a freshwater fish (Brachydanio rerio Hamilton-Buchanan). GB/T 13267-1991
Ministry of Environmental Protection of the People’s Republic of China (1995) Water quality—determination of the acute toxicity—luminescent bacteria test. GB/T 15441-1995
OECD (2004) OECD guideline for testing of chemicals—Daphnia sp., acute immobilisation test 202. In: Effects on biotic systems. OECD, Section 2
Oliveira R, Domingues I, Grisolia CK, Soares AMVM (2009) Effects of triclosan on zebrafish early-life stages and adults. Environ Sci Pollut Res 16(6):679–688. https://doi.org/10.1007/s11356-009-0119-3
Orvos DR, Versteeg DJ, Inauen J, Capdevielle M, Rosthenstein A, Cunningham V (2002) Aquatic toxicity of triclosan. Environ Toxicol Chem 21(7):1338–1349. https://doi.org/10.1002/etc.5620210703
Palmer RK, Hutchinson LM, Burpee BT, Tupper EJ, Pelletier JH, Kormendy Z, Hopke AR, Malay ET, Evans BL, Velez A, Gosse JA (2012) Antibacterial agent triclosan suppresses RBL-2H3 mast cell function. Toxicol Appl Pharmacol 258(1):99–108. https://doi.org/10.1016/j.taap.2011.10.012
Pandey S, Parvez S, Sayeed I, Haque R, Bin-Hafeez B, Raisuddin S (2003) Biomarkers of oxidative stress: a comparative study of river Yamuna fish Wallago attu (Bl. & Schn.) Sci Total Environ 309(1–3):105–115. https://doi.org/10.1016/S0048-9697(03)00006-8
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(9):1384–1394. https://doi.org/10.1007/s10646-013-1124-3
Price OR, Williams RJ, Egmond RV, Wilkinson MJ, Whelan MJ (2010) Predicting accurate and ecologically relevant regional scale concentrations of triclosan in rivers for use in higher-tier aquatic risk assessments. Environ Int 36(6):521–526. https://doi.org/10.1016/j.envint.2010.04.003
Qu RJ, Wang XH, Feng MB, Li Y, Liu HX, Wang LS, Wang ZY (2013) The toxicity of cadmium to three aquatic organisms (Photobacterium phosphoreum, Daphnia magna and Carassius auratus) under different pH levels. Ecotoxicol Environ Saf 95:83–90. https://doi.org/10.1016/j.ecoenv.2013.05.020
Qu RJ, Feng MB, Wang XH, Qin L, Wang C, Wang ZY, Wang LS (2014) Metal accumulation and oxidative stress biomarkers in liver of freshwater fish Carassius auratus following in vivo exposure to waterborne zinc under different pH values. Aquat Toxicol 150:9–16. https://doi.org/10.1016/j.aquatox.2014.02.008
Qu RJ, Liu JQ, Wang LS, Wang ZY (2016) The toxic effect and bioaccumulation in aquatic oligochaete Limnodrilus hoffmeisteri after combined exposure to cadmium and perfluorooctane sulfonate at different pH values. Chemosphere 152:496–502. https://doi.org/10.1016/j.chemosphere.2016.03.024
Ramaswamy BR, Shanmugam G, Velu G, Rengarajan B, Larsson DG (2011) GC-MS analysis and ecotoxicological risk assessment of triclosan, carbamazepine and parabens in Indian rivers. J Hazard Mater 186:1586–1593
Rendal C, Kusk KO, Trapp S (2011) Optimal choice of pH for toxicity and bioaccumulation studies of ionizing organic chemicals. Environ Toxicol Chem 30(11):2395–2406. https://doi.org/10.1002/etc.641
Riva C, Cristoni S, Binelli A (2012) Effects of triclosan in the freshwater mussel Dreissena polymorpha: a proteomic investigation. Aqua Toxicol 118–119:62–71
Roberts J, Price OR, Bettles N, Rendal C, Egmond RV (2014) Accounting for dissociation and photolysis: a review of the algal toxicity of triclosan. Environ Toxicol Chem 33(11):2551–2559. https://doi.org/10.1002/etc.2710
Rodriguez-Ariza A, Peinado J, Pueyo C, Lopez-Barea J (1993) Biochemical indicators of oxidative stress in fish from polluted littoral areas. Can J Fish Aquat Sci 50(12):2568–2573. https://doi.org/10.1139/f93-280
Rowett CJ, Hutchinson TH, Comber SDW (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. https://doi.org/10.1016/j.scitotenv.2016.04.170
Song SB, Xu Y, Zhou BS (2006) Effects of hexachlorobenzene on antioxidant status of liver and brain of common carp (Cyprinus carpio). Chemosphere 65(4):699–706. https://doi.org/10.1016/j.chemosphere.2006.01.033
Stephensen E, Sturve J, Főrlin L (2002) Effects of redox cycling compounds on glutathione content and activity of glutathione-related enzymes in rainbow trout liver. Comp Biochem Physiol 133C:435–442
Tamura I, Kagota KI, 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
Van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Phar 13(2):57–149. https://doi.org/10.1016/S1382-6689(02)00126-6
Villalaín J, Mateo CR, Aranda FJ, Shapiro S, Micol V (2001) Membranotropic effects of the antibacterial agent triclosan. Arch Biochem Biophys 390(1):128–136. https://doi.org/10.1006/abbi.2001.2356
Von Der Ohe PC, Schmitt-Jansen M, Slobodnik J, Brack W (2012) Triclosan—the forgotten priority substance? Environ Sci Pollut Res Int 19(2):585–591. https://doi.org/10.1007/s11356-011-0580-7
Wang XN, Liu ZT, Yan ZG, Zhang C, Wang WL, Zhou JL, Pei SW (2013) Development of aquatic life criteria for triclosan and comparison of the sensitivity between native and non-native species. J Hazard Mater 260:1017–1022. https://doi.org/10.1016/j.jhazmat.2013.07.007
Wang XN, Liu ZT, Wang WH, Yan ZG, Zhang C, Wang WL, Chen LH (2014) Assessment of toxic effects of triclosan on the terrestrial snail (Achatina fulica). Chemosphere 108:225–230. https://doi.org/10.1016/j.chemosphere.2014.01.044
Wood CM (2001) Toxic responses of the gill. In: Schlenk DS, Benson WH (eds) Target organ toxicity in marine and freshwater teleosts, vol 1. Taylor and Francis, London, pp 1–89. https://doi.org/10.1201/9781315109244-2
Wu WJ, Hu YY, Guo Q, Yan J, Chen YC, Cheng JH (2015) Sorption/desorption behavior of triclosan in sediment–water–rhamnolipid systems: effects of pH, ionic strength, and DOM. J Hazard Mater 297:59–65. https://doi.org/10.1016/j.jhazmat.2015.04.078
Zhang JF, Shen H, Wang XR, Wu JC, Xue YQ (2004) Effects of chronic exposure of 2, 4-dichlorophenol on the antioxidant system in liver of freshwater fish Carassius auratus. Chemosphere 55(2):167–174. https://doi.org/10.1016/j.chemosphere.2003.10.048
Zhang X, Yang FX, Zhang XL, Xu Y, Liao T, Song SB, Wang JW (2008) Induction of hepatic enzymes and oxidative stress in Chinese rare minnow (Gobiocypris rarus) exposed to waterborne hexabromocyclododecane (HBCDD). Aquat Toxicol 86(1):4–11. https://doi.org/10.1016/j.aquatox.2007.07.002
Zhao JL, Zhang QQ, Chen F, Wang L, Ying GG, Liu YS, Yang B, Zhou LJ, Liu S, Su HC, Zhang RJ (2013) Evaluation of triclosan and triclocarban at river basin scale using monitoring and modeling tools: implications for controlling of urban domestic sewage discharge. Water Res 47(1):395–405. https://doi.org/10.1016/j.watres.2012.10.022
Funding
This research was financially supported by the National Natural Science Foundation of China (No. 21577063, 21377051) and the Major Science and Technology Program for Water Pollution Control and Treatment of China (No. 2012ZX07506-001).
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Markus Hecker
Electronic supplementary material
ESM 1
(DOCX 512 kb)
Rights and permissions
About this article
Cite this article
Li, C., Qu, R., Chen, J. et al. The pH-dependent toxicity of triclosan to five aquatic organisms (Daphnia magna, Photobacterium phosphoreum, Danio rerio, Limnodrilus hoffmeisteri, and Carassius auratus). Environ Sci Pollut Res 25, 9636–9646 (2018). https://doi.org/10.1007/s11356-018-1284-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-018-1284-z