Abstract
Study on effective disposal and utilization of sewage sludge has recently been the target of growing interest in China. However, potential risks are associated with the use of sludge due to its contamination with toxic organics, heavy metals and pathogenic microorganisms. In this study, a screening assessment was conducted on sewage sludge samples collected from 17 different sewage treatment plants in Beijing, based on a batch of in vitro bioassays, including a set of recombinant gene yeast assays for endocrine disruption, and an ethoxy resorufin-O-deethylase (EROD) assay using H4IIE cells for aryl hydrocarbon receptor (Ah-R) agonistic activities. Our results suggested that moderate levels of estrogen receptor agonistic activities (0.9 ng E2·g−1 to 6.8 ng E2·g−1, dw), but relative higher androgen receptor antagonistic activities (nd to 45%), progestin receptor antagonistic activities (nd to 80%) and Ah-R agonistic activities (1390 to 6740 pg 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD)·g−1, dw) were found in sewage sludge samples. However, there were no significant correlations between the toxic effects of sewage sludge and the sewage treatment processes. In addition, the 17β-estradiol (E2) equivalent quantity (EEQ) level of the sewage sludge was increased after the composting treatment, whereas the 2,3,7,8-tetrachlorodibenzo-p-dioxin toxic equivalent quantity (TEQ) level of sewage sludge composted was much lower than that of sewage sludge.
Article PDF
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Avoid common mistakes on your manuscript.
References
Wu J D, Xiong J X, Huang B B, Li W Z, Meng Q Y, He C L. Status and countermeasures of the sludge treatment and disposal in Beijing Municipal Sewage Treatment Plants. Beijing Water, 2010, (5): 4–6 (in Chinese)
Cargouët M, Perdiz D, Mouatassim-Souali A, Tamisier-Karolak S, Levi Y. Assessment of river contamination by estrogenic compounds in Paris area (France). The Science of the Total Environment, 2004, 324(1–3): 55–66
Chen J, Ahn K C, Gee N A, Gee S J, Hammock B D, Lasley B L. Antiandrogenic properties of parabens and other phenolic containing small molecules in personal care products. Toxicology and Applied Pharmacology, 2007, 221(3): 278–284
Roy P, Pereira B M. A treatise on hazards of endocrine disruptors and tool to evaluate them. Indian Journal of Experimental Biology, 2005, 43(11): 975–992
Sumpter J P, Jobling S. Vitellogenesis as a biomarker for estrogenic contamination of the aquatic environment. Environmental Health Perspectives, 1995, 103(Suppl 7): 173–178
Leusch F D L, van den Heuvel MR, Chapman H F, Gooneratne S R, Eriksson A M E, Tremblay L A. Development of methods for extraction and in vitro quantification of estrogenic and androgenic activity of wastewater samples. Comparative biochemistry and physiology. Toxicology & pharmacology, 2006, 143(1): 117–126
Kumar V, Chakraborty A, Viswanath G, Roy P. Androgenic endocrine disruptors in wastewater treatment plant effluents in India: their influence on reproductive processes and systemic toxicity in male rats. Toxicology and Applied Pharmacology, 2008, 226(1): 60–73
Sharpe R M, Skakkebaek N E. Are oestrogens involved in falling sperm counts and disorders of the male reproductive tract? Lancet, 1993, 341(8857): 1392–1396
Leon D Betowski, Douglas S Kendall, Christopher M Pace, Joseph R Donnelly. Characterization of groundwater samples from superfund sites by gas chromatography/mass spectrometry and liquid chromatography/mass spectrometry. Environmental Science & Technology, 1996, 30(12): 3558–3564
Giesy J P, Hilscherova K, Jones P D, Kannan K, Machala M. Cell bioassays for detection of aryl hydrocarbon (AhR) and estrogen receptor (ER) mediated activity in environmental samples. Marine Pollutution Bulletin, 2002, 45(1–12): 3–16
Qiao M, Chen Y, Zhang Q H, Huang S B, Ma M, Wang C, Wang Z J. Identification of Ah receptor agonists in sediment of Meiliang Bay, Taihu Lake, China. Environmental Science & Technology, 2006, 40(5): 1415–1419
Shen C F, Huang S B, Wang Z J, Qiao M, Tang X J, Yu C N, Shi D Z, Zhu Y, Shi J Y, Chen X C, Setty K, Chen Y X. Identification of Ah receptor agonists in soil of E-waste recycling sites from Taizhou area in China. Environmental Science & Technology, 2008, 42(1): 49–55
Li J, Wang Z J, Ma M, Peng X Z. Analysis of environmental endocrine disrupting activities using recombinant yeast assay in wastewater treatment plant effluents. Bulletin of Environmental Contamination and Toxicology, 2010, 84(5): 529–535
Gaido KW, Leonard L S, Lovell S, Gould J C, Babaï D, Portier C J, McDonnell D P. Evaluation of chemicals with endocrine modulating activity in a yeast-based steroid hormone receptor gene transcription assay. Toxicology and Applied Pharmacology, 1997, 143(1): 205–212
Ma M, Li J, Wang Z J. Assessing the detoxication efficiencies of wastewater treatment processes using a battery of bioassays/biomarkers. Archives of Environmental Contamination and Toxicology, 2005, 49(4): 480–487
Routledge E J, Sumpter J P. Estrogenic activity of surfactants and some of their degradation products assessed using a recombinant yeast screen. Environmental Toxicology and Chemistry, 1996, 15(3): 241–248
Wang J, Xie P, Kettrup A, Schramm K W. Inhibition of progesterone receptor activity in recombinant yeast by soot from fossil fuel combustion emissions and air particulate materials. The Science of the Total Environment, 2005, 349(1–3): 120–128
Donato M T, Gómez-Lechón M J, Castell J V. A microassay for measuring cytochrome P450IA1 and P450IIB1 activities in intact human and rat hepatocytes cultured on 96-well plates. Analytical Biochemistry, 1993, 213(1): 29–33
Bradford M M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 1976, 72(1–2): 248–254
Hanberg A, Stahlberg M, Georgellis A, de Wit C, Ahlborg U G. Swedish dioxin survey: evaluation of the H-4-II E bioassay for screening environmental samples for dioxin-like enzyme induction. Pharmacology & Toxicology, 1991, 69(6): 442–449
Pöch G, Köck P, Reiffenstein R J, Pancheva S N. Uniform characterization of potentiation in simple and complex situations when agents bind to different molecular sites. Canadian Journal of Physiology and Pharmacology, 1995, 73(11): 1574–1581
Ma M, Rao K F, Wang Z J. Occurrence of estrogenic effects in sewage and industrial wastewaters in Beijing, China. Environmental pollution (Barking, Essex: 1987), 2007, 147(2): 331–336
C Desbrow, E J Routledge, G C Brighty, J P Sumpter, M Waldock. Identification of estrogenic chemicals in STW effluent. 1. Chemical fractionation and in vitro biological screening. Environmental Science & Technology, 1998, 32(11): 1549–1558
Viganò L, Benfenati E, Cauwenberge A, Eidem J K, Erratico C, Goksøyr A, Kloas W, Maggioni S, Mandich A, Urbatzka R. Estrogenicity profile and estrogenic compounds determined in river sediments by chemical analysis, ELISA and yeast assays. Chemosphere, 2008, 73(7): 1078–1089
Murk A J, Legler J, van Lipzig M M H, Meerman J H N, Belfroid A C, Spenkelink A, van der Burg B, Rijs G B J, Vethaak D. Detection of estrogenic potency in wastewater and surface water with three in vitro bioassays. Environmental toxicology and chemistry/SETAC, 2002, 21(1): 16–23
Körner W, Bolz U, Süßmuth W, Hiller G, Schuller W, Hanf V, Hagenmaier H. Input/output balance of estrogenic active compounds in a major municipal sewage plant in Germany. Chemosphere, 2000, 40(9–11): 1131–1142
Sim WJ, Lee JW, Shin S K, Song K B, Oh J E. Assessment of fates of estrogens in wastewater and sludge from various types of wastewater treatment plants. Chemosphere, 2011, 82(10): 1448–1453
Mahjoub O, Leclercq M, Bachelot M, Casellas C, Escande A, Balaguer P, Bahri A, Gomez E, Fenet H. Estrogen, aryl hysdrocarbon and pregnane X receptors activities in reclaimed water and irrigated soils in Oued Souhil area (Nabeul, Tunisia). Desalination, 2009, 246(1–3): 425–434
Luo J, Ma M, Wang D, Rao K, Wang Z. Assessing potential toxicities of sediments from typical rivers in Tianjin, China by using in vitro bioassays. China Environmental Science, 2008, 28(11): 968–973
Song M, Xu Y, Jiang Q, Lam P K, O’Toole D K, Giesy J P, Jiang G. Measurement of estrogenic activity in sediments from Haihe and Dagu River, China. Environment International, 2006, 32(5): 676–681
Xiao R Y, Wang Z J, Wang C X, Yu G. Soil screening for identifying ecological risk stressors using a battery of in vitro cell bioassays. Chemosphere, 2006, 64(1): 71–78
Dray J, Dray T F, Ullmann A. Hydrolyse des métabolites urinaires de différentes hormones stéroïdes par la-glucuronidase de “Escherichia coli”. Annales de l’Institut Pasteur, 1972, 123(6): 853–857
Tollefsen K E, Harman C, Smith A, Thomas K V. Estrogen receptor (ER) agonists and androgen receptor (AR) antagonists in effluents from Norwegian North Sea oil production platforms. Marine Pollutution Bulletin, 2007, 54(3): 277–283
Sohoni P, Sumpter J P. Several environmental oestrogens are also anti-androgens. The Journal of Endocrinology, 1998, 158(3): 327–339
Tamura H, Ishimoto Y, Fujikawa T, Aoyama H, Yoshikawa H, Akamatsu M. Structural basis for androgen receptor agonists and antagonists: interaction of SPEED 98-listed chemicals and related compounds with the androgen receptor based on an in vitro reporter gene assay and 3D-QSAR. Bioorganic & Medicinal Chemistry, 2006, 14(21): 7160–7174
Tran D Q, Klotz DM, Ladlie B L, Ide C F, McLachlan J A, Arnold S F. Inhibition of progesterone receptor activity in yeast by synthetic chemicals. Biochemical and Biophysical Research Communications, 1996, 229(2): 518–523
Li J, Li N, Ma M, Giesy J P, Wang Z J. In vitro profiling of the endocrine disrupting potency of organochlorine pesticides. Toxicology Letters, 2008, 183(1—3): 65–71
Stevens J, Green N J L, Jones K C. Survey of PCDD/Fs and nonortho PCBs in UK sewage sludges. Chemosphere, 2001, 44(6): 1455–1462
Clarke B, Porter N, Symons R, Blackbeard J, Ades P, Marriott P. Dioxin-like compounds in Australian sewage sludge—review and national survey. Chemosphere, 2008, 72(8): 1215–1228
Eljarrat E, Caixach J, Rivera J. A comparison of TEQ contributions from PCDDs, PCDFs and dioxin-like PCBs in sewage sludges from Catalonia, Spain. Chemosphere, 2003, 51(7): 595–601
Song M, Jiang Q, Xu Y, Liu H, Lam P K, O’Toole D K, Zhang Q, Giesy J P, Jiang G. AhR-active compounds in sediments of the Haihe and Dagu Rivers, China. Chemosphere, 2006, 63(7): 1222–1230
Engwall M, Schnürer A. Fate of Ah-receptor agonists in organic household waste during anaerobic degradation—estimation of levels using EROD induction in organ cultures of chick embryo livers. The Science of the Total Environment, 2002, 297(1–3): 105–108
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Liu, C., Xu, Y., Ma, M. et al. Evaluation of endocrine disruption and dioxin-like effects of organic extracts from sewage sludge in autumn in Beijing, China. Front. Environ. Sci. Eng. 8, 433–440 (2014). https://doi.org/10.1007/s11783-013-0594-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11783-013-0594-0