Abstract
The effects of the antiepileptic drug carbamazepine (CBZ) were studied in three freshwater invertebrate species representing different taxonomic groups, life histories, and habitats in aquatic ecosystems. The oligochaete Lumbriculus variegatus was exposed by way of CBZ-spiked sediments at nominal concentrations between 0.625 and 10 mg/kg dry weight (dw) for 28 days. At the end of the test, reproduction and biomass were monitored as end points. The nonbiting midge Chironomus riparius was exposed to CBZ in a series of tests at nominal CBZ concentrations in sediment ranging from 0.16 to 100 mg/kg dw at 20°C and 23°C. Emergence and gender ratio were monitored at the end of the test. The freshwater snail Potamopyrgus antipodarum as the third test species was used in a chronic reproduction test for 28 days at aqueous CBZ concentrations from 0.4 to 250 mg/L. Whereas for the oligochaete and the snail no effects were observed, C. riparius exhibited a significant and concentration-dependent decrease of emergence in all test series. No observed effect concentrations and 10% effect concentrations were in the range of 33 to 140 and 70 to 210 μg/kg dw, respectively, based on measured CBZ concentrations in sediments. These low values indicate that CBZ may pose a potential threat for the survival of C. riparius and probably also for other aquatic insect populations in the field.
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References
Andreozzi R, Marotta R, Pinto G, Pollio A (2002) Carbamazepine in water: Persistence in the environment, ozonation treatment and preliminary assessment on algal toxicity. Water Res 36:2869–2877
American Society for Testing and Materials (1995) E 1706-95a: Standard test methods for measuring the toxicity of sediment-associated contaminations with freshwater invertebrates. American Society for Testing and Materials, West Conshohocken, PA
Belfroid A, Leonards P (1996) Effect of ethinyl oestradiol on the development of snails and amphibians (abstract PO/508). Society of Environmental Toxicology and Chemistry 17th Annual Meeting, Washington, DC, November 1996
Bertschy G, Bryois C, Bondolfi G, Velardi A, Budry P, Dascal D, et al. (1997) The association carbamazepine-mianserin in opiate withdrawl: A double blind pilot study versus clonidine. Pharmacol Res 35:451–456
Brinkhurst RO, Jamieson BGM (1971) Aquatic Oligochaeta of the World. Oliver and Boyd, Edinburgh, Great Britain
Brooks BW, Turner PK, Stanley JK, Weston JJ, Glidewell EA, Foran CM, et al. (2003a) Waterborne and sediment toxicity of fluoxetine to select organisms. Chemosphere 52:135–142
Brust K, Licht O, Hultsch V, Jungmann D, Nagel R (2001) Effects of terbutryn on aufwuchs and Lumbriculus variegatus in artificial indoor streams. Environ Toxicol Chem 20:2000–2007
Clara M, Strenn B, Kreuzinger N (2002) Verhalten ausgewählter Pharmazeutika in der Abwasserreinigung. Wiener Mitteilungen 178:113–138
Clara M, Strenn B, Kreuzinger N (2004) Carbamazepine as a possible anthropogenic marker in the aquatic environment: Investigations on the behaviour of carbamazepine in wastewater treatment and during groundwater infiltration. Water Res 38:947-954
Cleuvers M (2002) Aquatische Ökotoxikologie ausgewählter Arzneimittel. Algentest und akuter Daphnientest. UWSF - Z Umweltchem Ökotox 14:85–89
Drewes JE, Heberer T, Reddersen K (2002) Fate of pharmaceuticals during indirect potable reuse. Water Sci Technol 46:73–80
Duft M, Tillmann M, Oehlmann J (2002) Ökotoxikologische Sedimentkartierung der großen Flüsse Deutschlands. Final report of R&D project 299 24 275. German Federal Environment Agency, Berlin, Germany
Duft M, Schulte-Oehlmann U, Tillmann M, Markert B, Oehlmann J (2003a) Toxicity of triphenyltin and tributyltin to the freshwater mudsnail Potamopyrgus antipodarum in a new sediment biotest. Environ Toxicol Chem 22:145–152
Duft M, Schulte-Oehlmann U, Weltje L, Tillmann M, Oehlmann J (2003b) Stimulated embryo production as a parameter of estrogenic exposure via sediments in the freshwater mudsnail Potamopyrgus antipodarum. Aquat Toxicol 64:437–449
Egeler P, Römbke J, Meller M, Knacker T, Franke C, Studinger G, et al (1997) Bioaccumulation of lindane and hexachlorobenzene to tubificid sludgeworms (Oligochaeta) under standardised laboratory conditions. Chemosphere 35:835-852
Egeler P, Römbke J, Meller M, Knacker T, Nagel R (1999) Bioaccumulation test with tubificid sludgeworms in artificial media –: Development of a standardisable method. Hydrobiologia 406:271–280
European Agency for the Evaluation of Medicinal Products (2003) Note for guidance on environmental risk assessment of medicinal products for human use. CPMP/SWP/4447/00 (draft)
European Union (2003) Technical Guidance Document on Risk Assessment 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, Parts I, II and IV. European Communities, 2003. EUR 20418 EN/1
Ferrari B, Paxeus N, Lo Giudice R, Pollio A, Garric J (2003) Ecotoxicological impact of pharmaceuticals found in treated wastewaters: Study of carbamazepine, clofibric acid, and diclofenac. Ecotoxicol Environ Saf 56:450–450
Ferrari B, Mons R, Vollat B, Fraysse B, Paxeus N, Lo Giudice R, et al. (2004) Environmental risk assessment of six human pharmaceuticals: Are the current environmental risk assessment procedures sufficient for the protection of the aquatic environment? Environ Toxicol Chem 23:1344–1354
Fiedler HJ, Rösler HJ (1993) Spurenelemente in der Umwelt. Gustav Fischer Verlag, Stuttgart, Germany
Furlong ET, Kinney CA, Ferrer I, Werner SL, Cahill JD, Ratterman G (2004) Pharmaceuticals and personal-care products in solids: Analysis and field results for sediment, soil and biosolid samples. Preprints of Extended Abstracts presented at the ACS National Meeting, American Chemical Society, Division of Environmental Chemistry 44:1320-1323
Groenendijk D, Kraak MHS, Admiraal W (1999) Efficient shedding of accumulated metals during metamorphosis in metal-adapted populations of the midge Chironomus riparius. Environ Toxicol Chem 18:1225–1231
Hatakeyama S (1987) Chronic effects of Cd on reproduction of Polypedilum nubifer (Chironomidae) through water and food. Environ Pollut 48:249–261
Heberer T (2002) Occurrence, fate and removal of pharmaceutical residues in the aquatic environment: A review of recent research data. Toxicol Lett 131:5–17
Heberer T, Reddersen K, Mechlinski A (2002) From municipal sewage to drinking water: Fate and removal of pharmaceuticals residues in the aquatic environment in urban areas. Water Sci Technol 46:81–86
Henry MG, Chester DN, Mauck WL (1986) Role to artificial burrows in Hexagenia toxicity tests: Recommendations for protocol development. Environ Toxicol Chem 5:553–559
Hubendick B (1950) The effectiveness of passive dispersal in Hydrobia jenkinsi. Zool Bidr Uppsala 28:493–504
Lam MW, Young CY, Brain RA, Johnson DJ, Hanson MA, Wilson CJ, et al. (2004) Aquatic persistence of eight pharmaceuticals in a microcosm study. Environ Toxicol Chem 23:1431–1440
Landsky PF, Halling-Sørensen B (1997) The toxic effect of the antibiotic metronidazole on aquatic organisms. Chemosphere 35:2553–2561
Leppänen MT, Kukkonen JVK (1998) Factors affecting feeding rate, reproduction and growth of the oligochaete Lumbriculus variegatus (Müller). Hydrobiologia 377:183–194
Liebig M, (2005) Untersuchungen zu Umweltrisikoabschätzungen von Humanpharmaka und Inhaltsstoffen von Körperpflegeprodukten vor dem Hintergrund europäischer Bewertungskonzepte. Doctoral thesis, University Frankfurt am Main
Litchfield J, Wilcoxon F (1949) A simplified method of ecological dose-effect experiments. J Pharmacol Exp Ther 96:99–113
Löffler D (2003) Fate of human and veterinary pharmaceuticals in water/sediment: Test systems by analysis via LC-tandem MS and radio-TLC. Dissertation, Johannes Gutenberg University Mainz
Löffler D, Ternes TA (2003) Analysis of acidic pharmaceuticals, antibiotics and ivermectin in river sediment using LC-tandem MS. J Chromatogr A 2021:133-144
Löffler D, Roembke J, Meller M, Ternes TA (2004) Environmental fate of pharmaceuticals in water/sediment systems. Environ Sci Tech (in press)
McCahon CP, Pascoe D (1991) Brief-exposure of first and forth instar Chironomus riparius larvae to equivalent assumed doses of cadmium: Effects on adult emergence. Water Air Soil Pollut 60:396–403
Metcalfe CD, Koenig BG, Bennie DT, Servos M, Ternes TA, Hirsch R (2003a) Occurrence of neutral and acidic drugs in the effluents of Canadian sewage treatment plants. Environ Toxicol Chem 22:2872–2880
Metcalfe CD, Miao XS, Koenig BG, Struger J (2003b) Distribution of acidic and neutral drugs in surface waters near sewage treatment plants in the lower Great Lakes, Canada. Environ Toxicol Chem 22:2881–2889
Montgomery SA, Schatzberg AF, Guelfi JD, Kaspar S, Nemeroff C, Swann A, et al. (2000) Pharmacotherapy of depression and mixed states in bipolar disorder. J Affect Disord 59:39–56
Organisation for Economic Co-operation and Development (2002) OECD Guidelines for Testing of Chemicals - 308. Aerobic and Anaerobic Transformation in Aquatic Sediment Systems. Organisation for Economic Co-operation and Development, Paris, France
Organisation for Economic Co-operation and Development (2004) OECD Guidelines for Testing of Chemicals - 218. Sediment-Water Chironomid Toxicity Test Using Spiked Sediment, Organisation for Economic Co-operation and Development, Paris, France
Oetken M, Ludwichowski KU, Nagel R (2001) Validation of the preliminary EU concept of assessing the impact of chemicals to organisms in sediment by using selected substances. Report R&D project 29967411. German Federal Environment Agency, Berlin, Germany
Oetken M, Stachel B, Pfenninger M, Oehlmann J (2004) Impact of a flood disaster on sediment toxicity in a major river system–the Elbe flood 2002 as a case study. Environ Pollut 134:87–95
Pfluger P, Prietz A, Wasserrab B, Koster C, Knörzer B, Dietrich D (2000) Untersuchungen zur aquatischen Toxizität und zur endokrinen Wirkung von Carbamazepin. Konstanz, EUREGIO Ökotoxikologie Service Labor, Universität Konstanz, pp 1–34
Phipps GL, Ankley GT, Benoit DA, Mattson VR (1993) Use of the aquatic oligochaete Lumbriculus variegatus for assessing the toxicity and bioaccumulation of sediment-associated contaminants. Environ Toxicol Chem 12:269–279
Ristola T, Pellinen J, Ruokolainen M, Kostamo A, Kukkonen JVK (1999) Effect of sediment type, feeding level, and larval density on growth and development of a midge (Chironomus riparius). Environ Toxicol Chem 18:756–764
Sacher F, Lochow E, Bethmann D, Brauch HJ (1998) Vorkommen von Arzneimittelwirkstoffen in Oberflächengewässern. Vom Wasser 90:233-243
Sachs L, (1992) Angewandte Statistik. Volume 7. Auflage. Springer-Verlag, Berlin, Germany
Scharf S, Loos S, Uhl M, Kreuzinger N (2004) Untersuchung von Donausedimenten und Schwebstoffen auf ausgewählte organische Stoffe. Report BE-249. Federal Environment Agency, Vienna, Austria
Schulte-Oehlmann U, (1997) Fortpflanzungsstörungen bei Süß-und Brackwasserschnecken—Einfluß der Umweltchemikalie Tributylzinn. Wissenschaft und Technik Verlag, Berlin, Germany
Schulte-Oehlmann U, Tillmann M, Casey D, Duft M, Markert B, Oehlmann J (2001) Östrogenartige Wirkungen von Bisphenol A auf Vorderkiemerschnecken (Mollusca: Gastropoda: Prosobranchia). UWSF—Z Umweltchem Ökotox 13:319-333
Schulz R, (1997) Aquatische Ökotoxikologie von Insektiziden—Auswirkungen diffuser Insektizideinträge aus der Landwirtschaft auf Fließgewässerlebensgemeinschaften. Ecomed-Verlag, Landsberg/Lech
Schwabe U, Paffrath D (2003) Arzneiverordnungs—Report 2002. Springer-Verlag, Berlin, Germany
Schweinfurt H, Länge R, Günzel P (1996) Environmental fate and ecological effects of steroidal estrogens. Presentation at the 3rd Eurolab Symposium—Testing and Analysis for Industrial Competitiveness and Sustainability, Berlin, Germany, June 5 to 7, 1996
Sternebring B, Liden A, Andersson K, Melander A (1992) Carbamazepine kinetics and adverse effects during and after ethanol exposure in alcoholics and healthy volunteers. Eur J Clin Pharmacol 43:393–397
Strayer DL (1999) Effects of alien species on freshwater mollusks in North America. J N Am Benthol Soc 18:74–98
Ternes TA (1998) Occurrence of drugs in German sewage treatment plants and rivers. Water Res 32:3245–3260
Ternes TA (2001) Analytical methods for the determination of pharmaceuticals in aqueous environmental samples. Trends Anal Chem 20:419–434
Ternes TA, Bonerz M., Schmidt T (2001) Determination of neutral pharmaceuticals in wastewater and rivers by liquid chromatography-electrospray tandem mass spectrometry. J Chromatogr A 938:175–185
Timmermans KR, (1991) Trace metal ecotoxicokinetics of chironomids. Doctoral thesis, University Amsterdam
Tixier C, Singer HP, Oellers S, Muller SR (2003) Occurrence and fate of carbamazepine, clofibric acid, diclofenac, ibuprofen, ketoprofen, and naproxen in surface waters. Environ Sci Tech 37:1061–1068
United States Environmental Protection Agency (2000) Computer program: EPI-Suite Version 3.11. Available at: http://www. epa.gov/opptintr/exposure/docs/episuite.htm. Accessed: March 2005
West CW, Ankley GT (1998) A laboratory assay to assess avoidance of contaminated sediments by the freshwater oligochaete Lumbriculus varigatus. Arch Environ Contam Toxicol 35:20–24
Wiegel S, Aulinger A, Brockmeyer R, Harms H, Löffler J, Reincke H, et al. (2004) Pharmaceuticals in the river Elbe and its tributaries. Chemosphere 57:107–126
Young WF, Whitehouse P, Johnson I, Sorokin N (2002) Proposed predicted-no-effect-concentrations (PNECs) for natural and synthetic steroid oestrogens in surface waters. Research and Development, Technical Report P2-T04/1. Environment Agency, Bristol, UK
Acknowledgments
We thank G. Elter, Y. Gerasymchyk, and M. Hasenbank for excellent technical assistance and V. Hecker for support during the experiments. This research was funded through the Centre of Environmental Research (ZUF), University Frankfurt am Main.
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Oetken, M., Nentwig, G., Löffler, D. et al. Effects of Pharmaceuticals on Aquatic Invertebrates. Part I. The Antiepileptic Drug Carbamazepine. Arch Environ Contam Toxicol 49, 353–361 (2005). https://doi.org/10.1007/s00244-004-0211-0
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DOI: https://doi.org/10.1007/s00244-004-0211-0