Ecotoxicology

, Volume 21, Issue 7, pp 2031–2050 | Cite as

Risk assessment of chlortetracycline, oxytetracycline, sulfamethazine, sulfathiazole, and erythromycin in aquatic environment: are the current environmental concentrations safe?

  • Kyunghee Ji
  • Sunmi Kim
  • Sunyoung Han
  • Jihyun Seo
  • Sangwoo Lee
  • Yoonsuk Park
  • Kyunghee Choi
  • Young-Lim Kho
  • Pan-Gyi Kim
  • Jeongim Park
  • Kyungho Choi
Article

Abstract

To understand potential risks of major pharmaceutical residues in waters, we evaluated ecotoxicities of five major veterinary pharmaceuticals, i.e., chlortetracycline, oxytetracycline, sulfamethazine, sulfathiazole, and erythromycin, which have been frequently detected in freshwater environment worldwide. We conducted acute and chronic toxicity tests using two freshwater invertebrates (Daphnia magna and Moina macrocopa) and a fish (Oryzias latipes). In general, D. magna exhibited greater sensitivity than M. macrocopa, and chronic reproduction was the most sensitive endpoints for both organisms. The population growth rate was adversely influenced by exposure to chlortetracycline, sulfamethazine, or sulfathiazole in water fleas, but reduction in population size was not expected. In O. latipes, the tested pharmaceuticals affected several reproduction related endpoints including time to hatch and growth. Based on the toxicity values from the present study and literature, algae appeared to be the most sensitive organism, followed by Daphnia and fish. Hazard quotients derived from measured environmental concentrations (MECs) and predicted no effect concentrations (PNECs) for erythromycin and oxytetracycline exceeded unity, suggesting that potential ecological effects at highly contaminated sites cannot be ruled out. Long-term consequences of veterinary pharmaceutical contamination in the environment deserve further investigation.

Keywords

Chronic toxicity Effective concentration Measured environmental concentration Veterinary pharmaceutical 

Supplementary material

10646_2012_956_MOESM1_ESM.doc (1.5 mb)
Supplementary material 1 (DOC 1,539 kb)

References

  1. Ahlers J, Riedhammer C, Vogliano M, Ebert RU, Kϋhne R, Schϋϋrmann G (2006) Acute to chronic ratios in aquatic toxicity-variation across trophic levels and relationship with chemical structure. Environ Toxicol Chem 25:2937–2945CrossRefGoogle Scholar
  2. Allen WO, Gerald AL (2000) Effects of endocrine-active chemicals on the development of sex characteristics of Daphnia magna. Environ Toxicol Chem 19:2107–2113Google Scholar
  3. American Public Health Association (1992) Standard methods for the examination of water and wastewater, 18th edn. American Water Works Association, and Water Pollution Control Federation, Washington, DCGoogle Scholar
  4. Ando T, Nagase H, Eguchi K, Hirooka T, Nakamura T, Miyamoto K, Hirata K (2007) A novel method using cyanobacteria for ecotoxicity test of veterinary antimicrobial agents. Environ Toxicol Chem 26(4):601–606CrossRefGoogle Scholar
  5. Baguer AJ, Jensen J, Krogh PH (2000) Effects of the antibiotics oxytetracycline and tylosin on soil fauna. Chemosphere 40:751–757CrossRefGoogle Scholar
  6. Barnes KK, Kolpin DW, Furlong ET, Zaugg SD, Meyer MT, Barber LB (2008) A national reconnaissance of pharmaceuticals and other organic wastewater contaminants in the United Stated—I) groundwater. Sci Total Environ 402:192–200CrossRefGoogle Scholar
  7. Batt AL, Snow DD, Aga DS (2006) Occurrence of sulfonamide antimicrobials in private water wells in Washington County, Idaho, USA. Chemosphere 64:1963–1971CrossRefGoogle Scholar
  8. Boxall AB, Fogg LA, Blackwell PA, Kay P, Pemberton EJ (2002) Review of veterinary medicines in the environment. R&D Technical Report P6-012/8TR. UK Environment Agency, BristolGoogle Scholar
  9. Boxall AB, Kolpin DW, Halling-Sørensen B, Tolls J (2003) Are veterinary medicines causing environmental risks? Environ Sci Technol 37:286–294ACrossRefGoogle Scholar
  10. Brain RA, Johnson DJ, Richards SM, Sanderson H, Sibley PK, Solomon KR (2004) Effects of 25 pharmaceutical compounds to Lemna gibba using a seven-day static-renewal test. Environ Toxicol Chem 23(2):371–382CrossRefGoogle Scholar
  11. Calamari D, Zuccato E, Castiglioni S, Bagnati R, Fanelli R (2003) Strategic survey of therapeutic drugs in the Rivers Po and Lambro in northern Italy. Environ Sci Technol 37:1241–1248CrossRefGoogle Scholar
  12. Crane M, Watts C, Boucard T (2006) Chronic aquatic environmental risks from exposure to human pharmaceuticals. Sci Total Environ 367:23–41CrossRefGoogle Scholar
  13. De Liguoro M, Cibin V, Capolongo F, Halling-Sørensen B, Montesissa C (2003) Use of oxytetracycline and tylosin in intensive calf farming: evaluation of transfer to manure and soil. Chemosphere 52(1):203–212CrossRefGoogle Scholar
  14. De Liguoro M, Fioretto B, Poltronieri C, Gallina G (2009) The toxicity of sulfamethazine to Daphnia magna and its additivity to other veterinary sulfonamides and trimethoprim. Chemosphere 75:1519–1524CrossRefGoogle Scholar
  15. Di Delupis GD, Macri A, Civitareale C, Migliore L (1992) Antibiotics of zootechnical use: effects of acute high and low dose contamination on Daphnia magna Straus. Aquat Toxicol 22:53–60CrossRefGoogle Scholar
  16. Eguchi K, Nagase H, Ozawa M, Endoh YS, Goto K, Hirata K, Miyamoto K, Yoshimura H (2004) Evaluation of antimicrobial agents for veterinary use in the ecotoxicity test using microalgae. Chemosphere 57:1733–1738CrossRefGoogle Scholar
  17. European Commission (2003) Technical guidance document in support of Commission Directive 93/67 EEC on risk assessment for new notified substances, Commission Regulation (EC) No. 1488/94 on risk assessment for existing substances and Directive 98/8/EC of the European Parliament and of the Council concerning the placing of biocidal products on the market. Joint Research Centre, IspraGoogle Scholar
  18. Fent K, Escher C, Caminada D (2006) Estrogen activity of pharmaceuticals and pharmaceutical mixtures in a yeast reporter gene system. Reprod Toxicol 22:175–185CrossRefGoogle Scholar
  19. Ferreira CS, Nunes BA, de Melo Henriques-Almeida JM, Guilhermino L (2007) Acute toxicity of oxytetracycline and florfenicol to the microalgae Tetraselmis chuii and to the crustacean Artemia parthenogenetica. Ecotoxicol Environ Saf 67(3):452–458CrossRefGoogle Scholar
  20. Forbes VE, Calow P (2002) Extrapolation in ecological risk assessment: balancing pragmatism and precaution in chemical controls legislation. Bio Sci 52:249–257Google Scholar
  21. Gallina G, Poltronieri C, Merlanti R, De Liguoro M (2008) Acute toxicity evaluation of four antibacterials with Daphnia magna. Vet Res Commun 32(Suppl 1):S287–S290CrossRefGoogle Scholar
  22. García-Galán MJ, Díaz-Cruz MS, Barceló D (2011) Occurrence of sulfonamide residues along the Ebro river basin removal in wastewater treatment plants and environmental impact assessment. Environ Int 37(2):462–473CrossRefGoogle Scholar
  23. Ginebreda A, Munoz I, de Alda ML, Brix R, Lopez-Doval J, Barcelo D (2010) Environmental risk assessment of pharmaceuticals in rivers: relationships between hazard indexes and aquatic macroinvertebrate diversity indexes in the Llobregat River (NE Spain). Environ Int 36(2):153–162CrossRefGoogle Scholar
  24. Gulkowska A, He Y, So MK, Yeung LWY, Leung HW, Giesy JP, Lam PKS, Martin M, Richardson BJ (2007) The occurrence of selected antibiotics in Hong Kong coastal waters. Mar Pollut Bull 54:1287–1306CrossRefGoogle Scholar
  25. Halling-Sørensen B (2000) Algal toxicity of antibacterial agents used in intensive farming. Chemosphere 40:731–739CrossRefGoogle Scholar
  26. Halling-Sørensen B, Nor Nielsen S, Lanzky PF, Ingerslev F, Holten-Lüzhøft HC, Jøbrgensen SE (1998) Occurrence, fate and effects of pharmaceutical substances in the environment. A review. Chemosphere 36:357–393CrossRefGoogle Scholar
  27. Hirsch R, Ternes TA, Haberer K, Mehlich A, Ballwanz F, Kratz KL (1998) Determination of antibiotics in different water compartments via liquid chromatography–electrospray tandem mass spectrometry. J Chromatogr A 815:213–223CrossRefGoogle Scholar
  28. Holten Lüzhøft HC, Halling-Sørensen B, Jørgensen SE (1999) Algal toxicity of antibacterial agents applied in Danish fish farming. Arch Environ Contam Toxicol 36:1–6CrossRefGoogle Scholar
  29. Hughes JS (1973) Acute toxicity of thirty chemicals to stripped bass (Morone saxatilis). Presented at the Western Association of State Game and Fish Commissioners in Salt Lake City, Utah, July 1973Google Scholar
  30. Isidori M, Lavorgna M, Nardelli A, Pascarella L, Parrella A (2005) Toxic and genotoxic evaluation of six antibiotics on non-target organisms. Sci Total Environ 346:87–98CrossRefGoogle Scholar
  31. Ji K, Choi K, Lee S, Park S, Khim JS, Jo EH, Choi KH, Zhang X, Giesy JP (2010) Effects of sulfathiazole oxytetracycline and chlortetracycline on steroidogenesis in the human adrenocarcinoma (H295R) cell line and freshwater fish Oryzias latipes. J Hazard Mater 182:494–502CrossRefGoogle Scholar
  32. Jia A, Hu J, Wu X, Peng H, Wu S, Dong Z (2011) Occurrence and source apportionment of sulfonamides and their metabolites in Liaodong Bay and the adjacent Liao River Basin, North China. Environ Toxicol Chem 30(6):1252–1260CrossRefGoogle Scholar
  33. Jiang L, Hu X, Yin D, Zhang H, Yu Z (2011) Occurrence, distribution and seasonal variation of antibiotics in the Huangpu River, Shanghai, China. Chemosphere 82:822–828CrossRefGoogle Scholar
  34. Jung J, Kim Y, Kim J, Jeong DH, Choi K (2008) Environmental levels of ultraviolet light potentiate the toxicity of sulfonamide antibiotics in Daphnia magna. Ecotoxicology 17:37–45CrossRefGoogle Scholar
  35. Kim SD, Cho J, Kim IS, Vanderford BJ, Snyder SA (2007a) Occurrence and removal of pharmaceuticals and endocrine disruptors in South Korean surface, drinking, and waste waters. Water Res 41:1013–1021CrossRefGoogle Scholar
  36. Kim Y, Choi K, Jung JY, Park S, Kim P, Park J (2007b) Aquatic toxicity of acetaminophen, carbamazepine, cimetidine, diltiazem, and six major sulfonamides, and their potential ecological risks in Korea. Environ Int 33:370–375CrossRefGoogle Scholar
  37. Kim J, Park Y, Choi K (2009a) Phototoxicity and oxidative stress responses in Daphnia magna under exposure to sulfathiazole and environmental level ultraviolet B irradiation. Aquat Toxicol 91:87–94CrossRefGoogle Scholar
  38. Kim J, Lee M, Oh S, Ku JL, Kim KH, Choi K (2009b) Acclimation to ultraviolet irradiation affects UV-B sensitivity of Daphnia magna to several environmental toxicants. Chemosphere 77:1600–1608CrossRefGoogle Scholar
  39. Kim JW, Ishibashi H, Yamauchi R, Ichikawa N, Takao Y, Hirano M, Koga M, Arizono K (2009c) Acute toxicity of pharmaceutical and personal care products on freshwater crustacean (Thamnocephalus platyurus) and fish (Oryzias latipes). J Toxicol Sci 34(2):227–232CrossRefGoogle Scholar
  40. Kim J, Park J, Kim PG, Lee C, Choi K, Choi K (2010) 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 19:662–669CrossRefGoogle Scholar
  41. Kolpin DW, Furlong ET, Meyer MT, Thurman EM, Zaugg SD, Barber LB, Buxton HT (2002) Pharmaceuticals, hormones, and other organic wastewater contaminants in U.S. streams, 1999–2000: a national reconnaissance. Environ Sci Technol 36:1202–1211CrossRefGoogle Scholar
  42. Kümmerer K (2009) The presence of pharmaceuticals in the environment due to human use-present knowledge and future challenges. A review. J Environ Manag 90:2354–2366CrossRefGoogle Scholar
  43. Lalumera GM, Calamari D, Galli P, Castiglioni S, Crosa G, Fanelli R (2004) Preliminary investigation on the environmental occurrence and effects of antibiotics used in aquaculture in Italy. Chemosphere 54:661–668CrossRefGoogle Scholar
  44. López-Roldán R, de Alda ML, Gros M, Petrovic M, Martín-Alonso J, Barceló D (2010) Advanced monitoring of pharmaceuticals and estrogens in the Llobregat River basin (Spain) by liquid chromatography-triple quadrupole-tandem mass spectrometry in combination with ultra performance liquid chromatography-time of flight-mass spectrometry. Chemosphere 80:1337–1344CrossRefGoogle Scholar
  45. Lotka AJ (1993) A natural population norm. J Wash Acad Sci 3:241–248Google Scholar
  46. Luo Y, Xu L, Rysz M, Wang Y, Zhang H, Alvarez PJ (2011) Occurrence and transport of tetracycline, sulfonamide, quinolone, and macrolide antibiotics in the Haihe River Basin, China. Environ Sci Technol 45(5):1827–1833CrossRefGoogle Scholar
  47. Marking L, Howe GE, Crowther JR (1988) Toxicity of erythromycin, oxytetracycline and tetracycline administered to Lake Trout in water baths, by injection or by feeding. Prog Fish Cult 50:197–201CrossRefGoogle Scholar
  48. Meinertz JR, Schreier TM, Bernardy JA, Franz JL (2010) Chronic toxicity of diphenhydramine hydrochloride and erythromycin thiocyanate to Daphnia, Daphnia magna, in a continuous exposure test system. Bull Environ Contam Toxicol 85:447–451CrossRefGoogle Scholar
  49. Meinertz JR, Schreier TM, Bernardy JA (2011) Chronic toxicity of erythromycin thiocyanate to Daphnia magna in a flow-through, continuous exposure test system. Bull Environ Contam Toxicol 87:621–625CrossRefGoogle Scholar
  50. National Institute of Environmental Research (2006) Development of analytical method and study of exposure of pharmaceuticals and personal care products in environment (I). Ministry of Environment, KoreaGoogle Scholar
  51. National Institute of Environmental Research (2007) Development of analytical method and study of exposure of pharmaceuticals and personal care products in environment (II). Ministry of Environment, KoreaGoogle Scholar
  52. National Institute of Environmental Research (2008) Development of analytical method and study of exposure of pharmaceuticals and personal care products in environment (III). Ministry of Environment, KoreaGoogle Scholar
  53. National Institute of Environmental Research (2009) Development of analytical method and study of exposure of pharmaceuticals and personal care products in environment (IV). Ministry of Environment, KoreaGoogle Scholar
  54. National Institute of Environmental Research (2010) Development of analytical method and study of exposure of pharmaceuticals and personal care products in environment (V). Ministry of Environment, KoreaGoogle Scholar
  55. Oh S, Choi K (2012) Optimal conditions for three brood chronic toxicity test method using a freshwater macroinvertebrate Moina macrocopa. Environ Monit Assess 184:3687–3695CrossRefGoogle Scholar
  56. Ok YS, Kim SC, Kim KR, Lee SS, Moon DH, Lim KJ, Sung JK, Hur SO, Yang JE (2010) Monitoring of selected veterinary antibiotics in environmental compartments near a composting facility in Gangwon Province, Korea. Environ Monit Assess 174(1–4):693–701Google Scholar
  57. Organization for Economic Co-operation and Development (1992) OECD guideline for testing of chemicals, Test No. 210: fish, early-life stage toxicity test. Section 2: effects on biotic systems. Paris, FranceGoogle Scholar
  58. Organization for Economic Co-operation and Development (2008) OECD guideline for testing of chemicals, Test No. 211: Daphnia magna reproduction test. Section 2: effects on biotic systems. Paris, FranceGoogle Scholar
  59. Pailler JY, Krein A, Pfister L, Hoffmann L, Guignard C (2009) Solid phase extraction coupled to liquid chromatography-tandem mass spectrometry analysis of sulfonamides, tetracyclines, analgesics and hormones in surface water and wastewater in Luxembourg. Sci Total Environ 407:4736–4743CrossRefGoogle Scholar
  60. Park S, Choi K (2008) Hazard assessment of commonly used agricultural antibiotics on aquatic ecosystems. Ecotoxicology 17:526–538CrossRefGoogle Scholar
  61. Pomati F, Netting AG, Calamari D, Neilan BA (2004) Effects of erythromycin, tetracycline and ibuprofen on the growth of Synechocystis sp. and Lemna minor. Aquat Toxicol 67:387–396CrossRefGoogle Scholar
  62. Pro J, Ortiz JA, Boleas S, Fernández C, Carbonell G, Tarazona JV (2003) Effect assessment of antimicrobial pharmaceuticals on the aquatic plant Lemna minor. Bull Environ Contam Toxicol 70:290–295CrossRefGoogle Scholar
  63. Quinn B, Gagné F, Blaise C (2008) An investigation into the acute and chronic toxicity of eleven pharmaceuticals (and their solvents) found in wastewater effluent on the cnidarians, Hydra attenuata. Sci Total Environ 389:306–314CrossRefGoogle Scholar
  64. Roberts PH, Thomas KV (2006) The occurrence of selected pharmaceuticals in wastewater effluent and surface waters of the lower Tyne catchment. Sci Total Environ 356:143–153CrossRefGoogle Scholar
  65. Sanderson H, Ingerslev F, Brain RA, Halling-Sørensen B, Bestari JK, Wilson CJ, Johnson DJ, Solomon KR (2005) Dissipation of oxytetracycline, chlortetracycline, tetracycline and doxycycline using HPLC-UV and LC/MS/MS under aquatic semi-field microcosm conditions. Chemosphere 60:619–629CrossRefGoogle Scholar
  66. Sanderson H, Laird B, Pope L, Brain R, Wilson C, Johnson D, Bryning G, Peregrine AS, Boxall ABA, Solomon K (2007) Assessment of the environmental fate and effects of ivermectin in aquatic mesocosm. Aquat Toxicol 85:229–240CrossRefGoogle Scholar
  67. Sim WJ, Lee JW, Oh JE (2010) Occurrence and fate of pharmaceuticals in wastewater treatment plants and rivers in Korea. Environ Pollut 158(5):1938–1947CrossRefGoogle Scholar
  68. Tuc Dinh Q, Alliot F, Moreau-Guigon E, Eurin J, Chevreuil M, Labadie P (2011) Measurement of trace levels of antibiotics in river water using on-line enrichment and triple-quadrupole LC-MS/MS. Talanta 85(3):1238–1245CrossRefGoogle Scholar
  69. US Environmental Protection Agency (2002) Methods for measuring the acute toxicity of effluents and receiving waters to freshwater and marine organisms, 5th edn. EPA-821-R-02-012. Office of Research and Development, Washington DCGoogle Scholar
  70. Uyaguari M, Key P, Moore J, Jackson K, Scott G (2009) Acute effects of the antibiotic oxytetracycline on the bacterial community of the grass shrimp, Palaemonetes pugio. Environ Toxicol Chem 28(12):2715–2724CrossRefGoogle Scholar
  71. Wei R, Ge F, Huang S, Chen M, Wang R (2010) Occurrence of veterinary antibiotics in animal wastewater and surface water around farms in Jiangsu Province, China. Chemosphere 82(10):1408–1414CrossRefGoogle Scholar
  72. Wilford WA (1966) The toxicity of nine therapeutic and herbicidal compounds to stripped bass. Prog Fish Cult 31(1):27–32Google Scholar
  73. Wollenberger L, Halling-Sørensen B, Kusk KO (2000) Acute and chronic toxicity of veterinary antibiotics to Daphnia magna. Chemosphere 40:723–730CrossRefGoogle Scholar
  74. Xu WH, Zhang G, Zou SC, Li XD, Liu YC (2007) Determination of selected antibiotics in the Victoria Harbour and the Pearl River, South China using high-performance liquid chromatography-electrospray ionization tandem mass spectrometry. Environ Pollut 145:672–679CrossRefGoogle Scholar
  75. Yang S, Carlson KH (2004) Solid-phase extraction-high-performance liquid chromatography-ion trap mass spectrometry for analysis of trace concentrations of macrolide antibiotics in natural and waste water matrices. J Chromatogr A 1038:141–155CrossRefGoogle Scholar
  76. Yang LH, Ying GG, Su HC, Stauber JL, Adams MS, Binet MT (2008) Growth-inhibiting effects of 12 antibacterial agents and their mixtures on the freshwater microalga Pseudokirchneriella subcapitata. Environ Toxicol Chem 27(5):1201–1208CrossRefGoogle Scholar
  77. Yang JF, Ying GG, Zhao JL, Tao R, Su HC, Liu YS (2011) Spatial and seasonal distribution of selected antibiotics in surface waters of the Pearl Rivers, China. J Environ Sci Health B 46(3):272–280CrossRefGoogle Scholar
  78. Zeeman MG (1995) Ecotoxicity testing and estimation methods developed under Section 5 of the Toxic Substances Control Act (TSCA). In: Rand GM (ed) Fundamentals of aquatic toxicology, 2nd edn. Taylor & Francis, Philadelphia, pp 703–716Google Scholar
  79. Zhang D, Lin L, Luo Z, Yan C, Zhang X (2011) Occurrence of selected antibiotics in Jiulongjiang River in various seasons, South China. J Environ Monit 13:1953–1960CrossRefGoogle Scholar
  80. Zounková R, Klimešová Z, Nepejchalová L, Hilscherová K, Bláha L (2011) Complex evaluation of ecotoxicity and genotoxicity of antimicrobials oxytetracycline and flumequine used in aquaculture. Environ Toxicol Chem 30(5):1184–1189CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Kyunghee Ji
    • 1
  • Sunmi Kim
    • 1
  • Sunyoung Han
    • 1
  • Jihyun Seo
    • 1
  • Sangwoo Lee
    • 1
  • Yoonsuk Park
    • 1
  • Kyunghee Choi
    • 2
  • Young-Lim Kho
    • 3
  • Pan-Gyi Kim
    • 4
  • Jeongim Park
    • 5
  • Kyungho Choi
    • 1
  1. 1.School of Public HealthSeoul National UniversitySeoulKorea
  2. 2.National Institute of Environmental ResearchIncheonKorea
  3. 3.School of Human & Environmental SciencesEulji UniversitySeongnamKorea
  4. 4.College of Natural SciencesYongin UniversityYonginKorea
  5. 5.College of Natural SciencesSoonchunhyang UniversityAsanKorea

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