Environmental Science and Pollution Research

, Volume 25, Issue 10, pp 9636–9646 | Cite as

The pH-dependent toxicity of triclosan to five aquatic organisms (Daphnia magna, Photobacterium phosphoreum, Danio rerio, Limnodrilus hoffmeisteri, and Carassius auratus)

  • Chenguang Li
  • Ruijuan Qu
  • Jing Chen
  • Shuo Zhang
  • Ahmed A. Allam
  • Jamaan Ajarem
  • Zunyao Wang
Research Article


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.


Triclosan Acute toxicity Oxidative stress pH effects Aquatic organisms 


Funding information

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).

Supplementary material

11356_2018_1284_MOESM1_ESM.docx (512 kb)
ESM 1 (DOCX 512 kb)


  1. 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. CrossRefGoogle Scholar
  2. 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. CrossRefGoogle Scholar
  3. 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 470–471:1243–1249CrossRefGoogle Scholar
  4. 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):1044–1065CrossRefGoogle Scholar
  5. Beliaeff B, Burgeot T (2002) Integrated biomarker response: a useful tool for ecological risk assessment. Environ Toxicol Chem 21(6):1316–1322. CrossRefGoogle Scholar
  6. 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. CrossRefGoogle Scholar
  7. 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 287:817–833CrossRefGoogle Scholar
  8. 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. CrossRefGoogle Scholar
  9. 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, SwitzerlandGoogle Scholar
  10. 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 122:227–232CrossRefGoogle Scholar
  11. Claiborne A (1985) Catalase activity. In: Greenwald RA (ed) Handbook of methods for oxygen radical research. CRC, Boca Raton, pp 283–284Google Scholar
  12. 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. CrossRefGoogle Scholar
  13. 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 66:574–583CrossRefGoogle Scholar
  14. 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. CrossRefGoogle Scholar
  15. Dayan AD (2007) Risk assessment of triclosan [Irgasan®] in human breast milk. Food Chem Toxicol 45(1):125–129. CrossRefGoogle Scholar
  16. 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. CrossRefGoogle Scholar
  17. 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. CrossRefGoogle Scholar
  18. 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 239–268Google Scholar
  19. 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. CrossRefGoogle Scholar
  20. Flohe L, Otting F (1984) Superoxide dismutase assays. Method Enzym 105:93–104. CrossRefGoogle Scholar
  21. 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. CrossRefGoogle Scholar
  22. 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. CrossRefGoogle Scholar
  23. 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. CrossRefGoogle Scholar
  24. 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. CrossRefGoogle Scholar
  25. 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. CrossRefGoogle Scholar
  26. 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. CrossRefGoogle Scholar
  27. 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. CrossRefGoogle Scholar
  28. Jungclaus GA, Lopez-Avila V, Hites RA (1978) Organic compounds in an industrial wastewater: a case study of their environmental impact. Environ Sci Technol 12:88–96CrossRefGoogle Scholar
  29. 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. CrossRefGoogle Scholar
  30. 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. CrossRefGoogle Scholar
  31. 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. CrossRefGoogle Scholar
  32. 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. CrossRefGoogle Scholar
  33. 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. CrossRefGoogle Scholar
  34. 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. CrossRefGoogle Scholar
  35. 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. CrossRefGoogle Scholar
  36. Lopez-Avila V, Hites RA (1980) Organic compounds in an industrial wastewater. Their transport into sediments. Environ Sci Technol 14(11):1382–1390. CrossRefGoogle Scholar
  37. 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. CrossRefGoogle Scholar
  38. Lushchak VI (2011) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101(1):13–30. CrossRefGoogle Scholar
  39. 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. CrossRefGoogle Scholar
  40. 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. CrossRefGoogle Scholar
  41. Mates JM (2000) Effects of antioxidant enzymes in the molecular control of reactive oxygen species toxicology. Toxicology 153(1–3):83–104. CrossRefGoogle Scholar
  42. McAvoy DC, Schatowitz B, Jacob M, Hauck A, Eckhoff WS (2002) Measurement of triclosan in wastewater treatment systems. Environ Toxicol Chem 21(7):1323–1329CrossRefGoogle Scholar
  43. McCord JM, Fridovich I (1969) Superoxide dismutase an enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244(22):6049–6055Google Scholar
  44. 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 13266-1991Google Scholar
  45. 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 13267-1991Google Scholar
  46. Ministry of Environmental Protection of the People’s Republic of China (1995) Water quality—determination of the acute toxicity—luminescent bacteria test. GB/T 15441-1995Google Scholar
  47. OECD (2004) OECD guideline for testing of chemicals—Daphnia sp., acute immobilisation test 202. In: Effects on biotic systems. OECD, Section 2Google Scholar
  48. 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. CrossRefGoogle Scholar
  49. Orvos DR, Versteeg DJ, Inauen J, Capdevielle M, Rosthenstein A, Cunningham V (2002) Aquatic toxicity of triclosan. Environ Toxicol Chem 21(7):1338–1349. CrossRefGoogle Scholar
  50. 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. CrossRefGoogle Scholar
  51. 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. CrossRefGoogle Scholar
  52. 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. CrossRefGoogle Scholar
  53. 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. CrossRefGoogle Scholar
  54. 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. CrossRefGoogle Scholar
  55. 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. CrossRefGoogle Scholar
  56. 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. CrossRefGoogle Scholar
  57. 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 186:1586–1593CrossRefGoogle Scholar
  58. 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. CrossRefGoogle Scholar
  59. Riva C, Cristoni S, Binelli A (2012) Effects of triclosan in the freshwater mussel Dreissena polymorpha: a proteomic investigation. Aqua Toxicol 118–119:62–71CrossRefGoogle Scholar
  60. 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. CrossRefGoogle Scholar
  61. 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. CrossRefGoogle Scholar
  62. 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. CrossRefGoogle Scholar
  63. 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. CrossRefGoogle Scholar
  64. 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:435–442Google Scholar
  65. 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 33:1222–1229Google Scholar
  66. 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. CrossRefGoogle Scholar
  67. 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. CrossRefGoogle Scholar
  68. 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. CrossRefGoogle Scholar
  69. 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. CrossRefGoogle Scholar
  70. 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. CrossRefGoogle Scholar
  71. 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. Google Scholar
  72. 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. CrossRefGoogle Scholar
  73. 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. CrossRefGoogle Scholar
  74. 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. CrossRefGoogle Scholar
  75. 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. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Chenguang Li
    • 1
  • Ruijuan Qu
    • 1
  • Jing Chen
    • 1
  • Shuo Zhang
    • 1
  • Ahmed A. Allam
    • 2
    • 3
  • Jamaan Ajarem
    • 2
  • Zunyao Wang
    • 1
  1. 1.State Key Laboratory of Pollution Control and Resources Reuse, School of the EnvironmentNanjing UniversityNanjingPeople’s Republic of China
  2. 2.Department of Zoology, Faculty of ScienceKing Saud UniversityRiyadhSaudi Arabia
  3. 3.Zoology Department, Faculty of ScienceBeni-Suef UniversityBeni SuefEgypt

Personalised recommendations