Abstract
Changes in pollutant loads in relatively dynamic river sediments, which contain very complex mixtures of compounds, can play a crucial role in the fate and effects of pollutants in fluvial ecosystems. The contamination of sediments by bioactive substances can be sensitively assessed by in vitro bioassays. This is the first study that characterizes detailed short- and long-term changes in concentrations of contaminants with several modes of action in river sediments. One-year long monthly study described seasonal and spatial variability of contamination of sediments in a representative industrialized area by dioxin-like and endocrine disruptive chemicals. There were significant seasonal changes in both antiandrogenic and androgenic as well as dioxin-like potential of river sediments, while there were no general seasonal trends in estrogenicity. Aryl hydrocarbon receptor-dependent potency (dioxin-like potency) expressed as biological TCDD-equivalents (BIOTEQ) was in the range of 0.5–17.7 ng/g, dry mass (dm). The greatest BIOTEQ levels in sediments were observed during winter, particularly at locations downstream of the industrial area. Estrogenicity expressed as estradiol equivalents (EEQ) was in the range of 0.02–3.8 ng/g, dm. Antiandrogenicity was detected in all samples, while androgenic potency in the range of 0.7–16.8 ng/g, dm dihydrotestosterone equivalents (DHT-EQ) was found in only 30 % of samples, most often during autumn, when antiandrogenicity was the least. PAHs were predominant contaminants among analyzed pollutants, responsible, on average, for 13–21 % of BIOTEQ. Longer-term changes in concentrations of BIOTEQ corresponded to seasonal fluctuations, whereas for EEQ, the inter-annual changes at some locations were greater than seasonal variability during 1 year. The inter- as well as intra-annual variability in concentrations of both BIOTEQ and EEQ at individual sites was greater in spring than in autumn which was related to hydrological conditions in the river. This study stresses the importance of river hydrology and its seasonal variations in the design of effective sampling campaigns, as well as in the interpretation of any monitoring results.
Similar content being viewed by others
Notes
Locality CR (oxbow lake) has no water discharge (lentic locality) and temperature was not measured, therefore, these two variables could not have been included in Fig. 5.
References
Babek O, Hilscherova K, Nehyba S, Zeman J, Famera M, Francu J, Holoubek I, Machat J, Klanova J (2008) Contamination history of suspended river sediments accumulated in oxbow lakes over the last 25 years. J Soils Sediments 8:165–176
Babich H, Borenfreund E (1990) Cytotoxic effects of food-additives and pharmaceuticals on cells in culture as determined with the Neutral Red Assay. J Pharm Sci 79:592–594
Babut M, Lopes C, Pradelle S, Persat H, Badot PM (2012) BSAFs for freshwater fish and derivation of a sediment quality guideline for PCBs in the Rhone Basin, France. J Soils Sediments 12:241–251
Behnisch PA, Hosoe K, Sakai S (2003) Brominated dioxin-like compounds: in vitro assessment in comparison to classical dioxin-like compounds and other polyaromatic compounds. Environ Int 29:861–877
Brack W, Klamer HJC, de Ada ML, Barcelo D (2007) Effect-directed analysis of key toxicants in European river basins—a review. Environ Sci Pollut Res 14:30–38
Brack W, Blaha L, Giesy JP, Grote M, Moeder M, Schrader S, Hecker M (2008) Polychlorinated naphthalenes and other dioxin-like compounds in Elbe River sediments. Environ Toxicol Chem 27:519–528
Brinkmann M, Hudjetz S, Kammann U, Hennig M, Kuckelkorn J, Chinoraks M, Cofalla C, Wiseman S, Giesy JP, Schaffer A, Hecker M, Wolz J, Schuttrumpf H, Hollert H (2013) How flood events affect rainbow trout: evidence of a biomarker cascade in rainbow trout after exposure to PAH contaminated sediment suspensions. Aquat Toxicol 128:13–24
Colombo JC, Cappelletti N, Lasci J, Migoya MC, Speranza E, Skorupka CN (2006) Sources, vertical fluxes, and equivalent toxicity of aromatic hydrocarbons in coastal sediments of the Rio de la Plata Estuary, Argentina. Environ Sci Technol 40:734–740
Creusot N, Tapie N, Piccini B, Balaguer P, Porcher JM, Budzinski H, Ait-Aissa S (2013) Distribution of steroid- and dioxin-like activities between sediments, POCIS and SPMD in a French river subject to mixed pressures. Environ Sci Pollut Res 20:2784–2794
Crommentuijn T, Sijm D, de Bruijn J, van den Hoop M, van Leeuwen K, van de Plassche E (2000) Maximum permissible and negligible concentrations for metals and metalloids in the Netherlands, taking into account background concentrations. J Environ Manage 60:121–143
de Deckere E, De Cooman W, Leloup V, Meire P, Schmitt C, von der Ohe PC (2011) Development of sediment quality guidelines for freshwater ecosystems. J Soils Sediments 11:504–517
Demirpence E, Duchesne MJ, Badia E, Gagne D, Pons M (1993) Mvln cells—a bioluminescent Mcf-7-derived cell-line to study the modulation of estrogenic activity. J Steroid Biochem Mol Biol 46:355–364
Directive 2000/60/EC of the European Parliament and of the Council of 23 October 2000 establishing a framework for Community action in the field of water policy, Brussels, p 72
Directive 2008/105/EC of the European Parliament and of the Council of 16 December 2008 on environmental quality standards in the field of water policy, amending and subsequently repealing Council Directives 82/176/EEC, 83/513/EEC, 84/156/EEC, 84/491/EEC, 86/280/EEC and amending Directive 2000/60/EC of the European Parliament and of the Council, Brussels, p 14
European Commission (2012) Proposal for a Directive of the European Parliament and of the Council amending Directives 2000/60/EC and 2008/105/EC as regards priority substances in the field of water policy 2011/0429 (COD), Brussels, p 35
Forstner U, Salomons W (2010) Sediment research, management and policy. J Soils Sediments 10:1440–1452
Forstner U, Heise S, Schwartz R, Westrich B, Ahlf W (2004) Historical contaminated sediments and soils at the river basin scale. J Soils Sediments 4:247–260
Galluba S, Oehlmann J (2012) Widespread endocrine activity in river sediments in Hesse, Germany, assessed by a combination of in vitro and in vivo bioassays. J Soils Sediments 12:252–264
Hayakawa K, Onoda Y, Tachikawa C, Hosoi S, Yoshita M, Chung SW, Kizu R, Toriba A, Kameda T, Tang N (2007) Estrogenic/antiestrogenic activities of polycyclic aromatic hydrocarbons and their monohydroxylated derivatives by yeast two-hybrid assay. J Health Sci 53:562–570
Higley E, Grund S, Jones PD, Schulze T, Seiler TB, Lubcke-von Varel U, Brack W, Wolz J, Zielke H, Giesy JP, Hollert H, Hecker M (2012) Endocrine disrupting, mutagenic, and teratogenic effects of upper Danube River sediments using effect-directed analysis. Environ Toxicol Chem 31:1053–1062
Hilscherova K, Kannan K, Kang YS, Holoubek I, Machala M, Masunaga S, Nakanishi J, Giesy JP (2001) Characterization of dioxin-like activity of sediments from a Czech river basin. Environ Toxicol Chem 20:2768–2777
Hilscherova K, Kannan K, Holoubek I, Giesy JP (2002) Characterization of estrogenic activity of riverine sediments from the Czech Republic. Arch Environ Contam Toxicol 43:175–185
Hilscherova K, Kannan K, Nakata H, Hanari N, Yamashita N, Bradley PW, McCabe JM, Taylor AB, Giesy JP (2003) Polychlorinated dibenzo-p-dioxin and dibenzofuran concentration profiles in sediments and flood-plain soils of the Tittabawassee River, Michigan. Environ Sci Technol 37:468–474
Hilscherova K, Dusek L, Kubik V, Cupr P, Hofman J, Klanova J, Holoubek I (2007) Redistribution of organic pollutants in river sediments and alluvial soils related to major floods. J Soils Sediments 7:167–177
Hilscherova K, Dusek L, Sidlova T, Jalova V, Cupr P, Giesy JP, Nehyba S, Jarkovsky J, Klanova J, Holoubek I (2010) Seasonally and regionally determined indication potential of bioassays in contaminated river sediments. Environ Toxicol Chem 29:522–534
Houtman CJ, Cenijn PH, Hamers T, Lamoree MH, Legler J, Murk AJ, Brouwer A (2004) Toxicological profiling of sediments using in vitro bioassays, with emphasis on endocrine disruption. Environ Toxicol Chem 23:32–40
Hunt JCR (2002) Floods in a changing climate: a review. Phil Trans R Soc A Math Phys Eng Sci 360:1531–1543
Jaffe R (1991) Fate of hydrophobic organic pollutants in the aquatic environment—a review. Environ Pollut 69:237–257
Janosek J, Hilscherova K, Blaha L, Holoubek I (2006) Environmental xenobiotics and nuclear receptors—interactions, effects and in vitro assessment. Toxicol in Vitro 20:18–37
Jarosova B, Blaha L, Vrana B, Randak T, Grabic R, Giesy JP, Hilscherova K (2012) Changes in concentrations of hydrophilic organic contaminants and of endocrine-disrupting potential downstream of small communities located adjacent to headwaters. Environ Int 45:22–31
Jobling S, Tyler CR (2003) Endocrine disruption in wild freshwater fish. Pure Appl Chem 75:2219–2234
Kannan K, Yun SH, Ostaszewski A, McCabe JM, Mackenzie-Taylor D, Taylor AB (2008) Dioxin-like toxicity in the Saginaw river watershed: polychlorinated dibenzo-p-dioxins, dibenzofurans, and biphenyls in sediments and floodplain soils from the Saginaw and Shiawassee rivers and Saginaw bay, Michigan, USA. Arch Environ Contam Toxicol 54:9–19
Kaplan S (2013) Review: pharmacological pollution in water. Crit Rev Environ Sci Technol 43:1074–1116
Kidd KA, Blanchfield PJ, Mills KH, Palace VP, Evans RE, Lazorchak JM, Flick RW (2007) Collapse of a fish population after exposure to a synthetic estrogen. Proc Natl Acad Sci U S A 104:8897–8901
Koh CH, Khim JS, Kannan K, Villeneuve DL, Senthilkumar K, Giesy JP (2004) Polychlorinated dibenzo-p-dioxins (PCDDs), dibenzofurans (PCDFs), biphenyls (PCBs), and polycyclic aromatic hydrocarbons (PAHs) and 2,3,7,8-TCDD equivalents (TEQs) in sediment from the Hyeongsan River, Korea. Environ Pollut 132:489–501
Kukucka P, Audy O, Prokes R, Komprdova K, Klanova J (2010) Temporal and spatial trends of selected POPs in riverine sediments: What can we learn for assessment of risks associated with frequent flood events? Organohalogen Compd 72:134–137
Luan TG, Yu KSH, Zhong Y, Zhou HW, Lan CY, Tam NFY (2006) Study of metabolites from the degradation of polycyclic aromatic hydrocarbons (PAHs) by bacterial consortium enriched from mangrove sediments. Chemosphere 65:2289–2296
Luo JP, Lei BL, Ma M, Zha JM, Wang ZJ (2011) Identification of estrogen receptor agonists in sediments from Wenyu River, Beijing, China. Water Res 45:3908–3914
Machala M, Vondracek J, Blaha L, Ciganek M, Neca J (2001) Aryl hydrocarbon receptor-mediated activity of mutagenic polycyclic aromatic hydrocarbons determined using in vitro reporter gene assay. Mutat Res Genet Toxicol Environ Mutagen 497:49–62
Martinez-Gomez C, Lamoree M, Hamers T, van Velzen M, Kamstra JH, Fernandez B, Benedicto J, Leon VM, Vethaak AD (2013) Integrated chemical and biological analysis to explain estrogenic potency in bile extracts of red mullet (Mullus barbatus). Aquat Toxicol 134:1–10
Novak J, Jalova V, Giesy JP, Hilscherova K (2009) Pollutants in particulate and gaseous fractions of ambient air interfere with multiple signaling pathways in vitro. Environ Int 35:43–49
Oh SM, Choung SY, Sheen YY, Chung KH (2000) Quantitative assessment of estrogenic activity in the water environment of Korea by the E-SCREEN assay. Sci Total Environ 263:161–169
Peck M, Gibson RW, Kortenkamp A, Hill EM (2004) Sediments are major sinks of steroidal estrogens in two United Kingdom rivers. Environ Toxicol Chem 23:945–952
Prokes R, Vrana B, Klanova J (2012) Levels and distribution of dissolved hydrophobic organic contaminants in the Morava river in Zlin district, Czech Republic as derived from their accumulation in silicone rubber passive samplers. Environ Pollut 166:157–166
Song MY, Jiang QT, Xu Y, Liu HX, Lam PKS, O’Toole DK, Zhang QH, Giesy JP, Jiang GB (2006) AhR-active compounds in sediments of the Haihe and Dagu Rivers, China. Chemosphere 63:1222–1230
Streck G (2009) Chemical and biological analysis of estrogenic, progestagenic and androgenic steroids in the environment. Trac Trends Anal Chem 28:635–652
Sumpter JP (2005) Endocrine disrupters in the aquatic environment: an overview. Acta Hydrochim Hydrobiol 33:9–16
Urbatzka R, van Cauwenberge A, Maggioni S, Vigano L, Mandich A, Benfenati E, Lutz I, Kloas W (2007) Androgenic and antiandrogenic activities in water and sediment samples from the river Lambro, Italy, detected by yeast androgen screen and chemical analyses. Chemosphere 67:1080–1087
Vermeirssen ELM, Korner O, Schonenberger R, Suter MJF, Burkhardt-Holm P (2005) Characterization of environmental estrogens in river water using a three pronged approach: active and passive water sampling and the analysis of accumulated estrogens in the bile of caged fish. Environ Sci Technol 39:8191–8198
Vigano L, Benfenati E, van Cauwenberge A, Eidem JK, Erratico C, Goksoyr A, Kloas W, Maggioni S, Mandich A, Urbatzka R (2008) Estrogenicity profile and estrogenic compounds determined in river sediments by chemical analysis, ELISA and yeast assays. Chemosphere 73:1078–1089
Vinggaard AM, Niemela J, Wedebye EB, Jensen GE (2008) Screening of 397 chemicals and development of a quantitative structure-activity relationship model for androgen receptor antagonism. Chem Res Toxicol 21:813–823
Vondracek J, Machala M, Minksova K, Blaha L, Murk AJ, Kozubik A, Hofmanova J, Hilscherova K, Ulrich R, Ciganek M, Neca J, Svrckova D, Holoubek I (2001) Monitoring river sediments contaminated predominantly with polyaromatic hydrocarbons by chemical and in vitro bioassay techniques. Environ Toxicol Chem 20:1499–1506
Wang X, Lin L, Luan T, Yang L, Tam NFY (2012) Determination of hydroxylated metabolites of polycyclic aromatic hydrocarbons in sediment samples by combining subcritical water extraction and dispersive liquid-liquid microextraction with derivatization. Anal Chim Acta 753:57–63
Weiss JM, Hamers T, Thomas KV, van der Linden S, Leonards PEG, Lamoree MH (2009) Masking effect of anti-androgens on androgenic activity in European river sediment unveiled by effect-directed analysis. Anal Bioanal Chem 394:1385–1397
Weiss JM, Simon E, Stroomberg GJ, de Boer R, de Boer J, van der Linden SC, Leonards PEG, Lamoree MH (2011) Identification strategy for unknown pollutants using high-resolution mass spectrometry: androgen-disrupting compounds identified through effect-directed analysis. Anal Bioanal Chem 400:3141–3149
Wilson VS, Bobseine K, Lambright CR, Gray LE (2002) A novel cell line, MDA-kb2, that stably expresses an androgen- and glucocorticoid-responsive reporter for the detection of hormone receptor agonists and antagonists. Toxicol Sci 66:69–81
Wolz J, Schulze T, Lubcke-von Varel U, Fleig M, Reifferscheid G, Brack W, Kuhlers D, Braunbeck T, Hollert H (2011) Investigation on soil contamination at recently inundated and non-inundated sites. J Soils Sediments 11:82–92
Zhao JL, Ying GG, Yang B, Liu S, Zhou LJ, Chen ZF, Lai HJ (2011) Screening of multiple hormonal activities in surface water and sediment from the pearl river system, South China, using effect-directed in vitro bioassays. Environ Toxicol Chem 30:2208–2215
Acknowledgments
This research was supported by projects ENVISCREEN (Ministry of Education, Youth and Sports of Czech Republic No. 2B08036) and CETOCOEN (CZ.1.05/2.1.00/01.0001) from the European Regional Development Fund. We acknowledge Klara Komprdova, Roman Prokes, and Ondrej Sanka for their technical assistance. Prof. Giesy was supported by the Canada Research Chair program, a Visiting Distinguished Professorship in the Department of Biology and Chemistry and State Key Laboratory in Marine Pollution, City University of Hong Kong, the 2012 “Great Level Foreign Experts” (#GDW20123200120) program, funded by the State Administration of Foreign Experts Affairs, the P.R. China to Nanjing University and the Einstein Professor Program of the Chinese Academy of Sciences.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Ester Heath
Rights and permissions
About this article
Cite this article
Macikova, P., Kalabova, T., Klanova, J. et al. Longer-term and short-term variability in pollution of fluvial sediments by dioxin-like and endocrine disruptive compounds. Environ Sci Pollut Res 21, 5007–5022 (2014). https://doi.org/10.1007/s11356-013-2429-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-013-2429-8