Identification of estrogenic activity change in sewage, industrial and livestock effluents by gamma-irradiation

Radiation Physics and Chemistry 81 (2012) 1757–1762

Contents lists available at SciVerse ScienceDirect

Radiation Physics and Chemistry journal homepage: www.elsevier.com/locate/radphyschem

Identification of estrogenic activity change in sewage, industrial and livestock effluents by gamma-irradiation Byeong-Yong Ahn a, Sung-Wook Kang b, Jisu Yoo a, Woong-Ki Kim a, Paek-Hyun Bae a, Jinho Jung a,n a b

Division of Environmental Science and Ecological Engineering, Korea University, Seoul 136-713, Republic of Korea Toxicity Evaluation Team, Korea Conformity Laboratories, Incheon 406-840, Republic of Korea

H I G H L I G H T S c c c

Livestock effluent showed strong estrogenic activity due to E2, E1 and EE2. EE2 remained in all effluents after gamma-irradiation even at a dose of 10 kGy. DOMs in effluents inhibited degradation and activity of estrogenic compounds.

a r t i c l e i n f o

abstract

Article history: Received 8 June 2012 Accepted 21 June 2012 Available online 29 June 2012

In this study, reduction of estrogenic activity in three different types of effluents from sewage, industrial and livestock wastewater treatment plants by gamma-irradiation was investigated using the yeast two-hybrid assay. After gamma-ray treatment at a dose of 10 kGy, estrogenic activities of sewage, industrial and livestock effluents decreased from 4.4 to 3.0, 1.5 to 1.0 and 16 to 9.9 ng-EEQ L  1, respectively. The substantial reduction of estrogenic activity in livestock effluent was attributable to the degradation of 17b-estradiol (E2), estrone (E1) and 17a-ethynylestradiol (EE2). Although bisphenol A (BPA) was found at the highest concentration in all effluents, its contribution to the estrogenic activity was not significant due to its low relative estrogenic potency. Meanwhile, the calculated estrogenic activity based on concentrations of E2, E1, EE2 and BPA in the effluents significantly differed from the measured ones. Overestimation may have resulted by dissolved organic matters in effluents inhibiting the estrogenic activity of E2, E1, EE2 and BPA, whereas underestimation was likely due to estrogenic byproducts generated by gamma-irradiation. & 2012 Elsevier Ltd. All rights reserved.

Keywords: AOPs EDCs Estrogens Gamma rays Yeast two-hybrid assay

1. Introduction Endocrine disrupting chemicals (EDCs) are defined as exogenous agents that interfere with synthesis, secretion, transport, binding, action or elimination of natural hormones in the body, which are responsible for the maintenance of homeostasis, reproduction, development and/or behavior (Ankley et al., 1997; USEPA, 1997; Chen et al., 2010). Many studies showed that EDCs including 17b-estradiol (E2), 17a-ethynylestradiol (EE2), estrone (E1) and bisphenol A (BPA) from wastewater treatment plants (WWTPs) are a serious problem for aquatic ecosystems probably due to incomplete removal of these EDCs by conventional processes (Rutishauser et al., 2004; Sarmah et al., 2006; Ma et al., 2007; Kusk et al., 2011). For instance, Lu et al. (2010) demonstrated that significant concentrations of E1, E2 and EE2 as well as BPA were detected in effluents from municipal WWTPs in China, suggesting

n

Corresponding author. Tel.: þ82 2 3290 3066; fax: þ82 2 3290 3509. E-mail address: [email protected] (J. Jung).

0969-806X/$ - see front matter & 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.radphyschem.2012.06.012

that WWTPs were not able to fully remove those compounds. In South Korea, Duong et al. (2010) reported that E1, E2 and EE2 had about 90–95% of estrogenic activity in samples collected from surface waters in rivers and effluents of sewage treatment plants (STPs) adjacent to the river. The presence of estrogenic compounds in effluents from both WWTPs and STPs indicates the need for a new technology to complement the wastewater treatment system. Recently, advanced oxidation processes (AOPs) have emerged as an effective method to remove non-degradable substances, including estrogenic compounds (Auriol et al., 2006; Esplugas et al., 2007; Klavarioti et al., 2009). In particular, Silva et al. (2012) demonstrated that AOPs may be the most promising techniques to remove estrogenic steroid hormones; however, potential hazardous by-products should be evaluated in these treatments. Among AOPs, gamma-ray treatment shows high removal effi ciency because hydrated electrons (eaq ) and hydroxyl radicals (dOH) generated during the treatment process rapidly react with organic compounds (Pikaev, 1994; Shim et al., 2009; Kang et al., 2011); however, the application of this technique to remove estrogenic

1758

B.-Y. Ahn et al. / Radiation Physics and Chemistry 81 (2012) 1757–1762

compounds is very limited. Indeed, previous studies mainly focused on degradation of pure chemicals in pure water or in model wastewater (Kimura et al., 2004, 2007). Thus, the purpose of this study was to evaluate the reduction of estrogenic activity in three kinds of effluents from an STP and industrial and livestock WWTPs by gamma-ray treatment. Additionally, the estrogenic activity in effluents was estimated by analyzing major estrogenic compounds, namely E2, EE2, E1 and BPA, and compared with the observed activity determined by the yeast two-hybrid assay.

2. Experimental 2.1. Sample preparation and gamma-ray treatment Three different effluents were collected from a sewage treatment plant in February, 2011, and industrial and livestock wastewater treatment plants in December, 2010 (Table 1). The collected samples were transported in an ice-box and then preserved in a cold storage at 4 1C. Estrogenic compounds, 17b-estradiol (97%), estrone (99%), 17a-ethynylestradiol (98%) and bisphenol A (98%), were purchased from Sigma-Aldrich Co. (USA) and used without further purification. Suwannee River natural organic matter (NOM) was purchased from the International Humic Substances Society (IHSS, Denver, USA). Sample solutions of E2, E1, EE2 and BPA were prepared with ultrapure water with resistivity of 18.2 MO cm  1. In the presence of NOM, the samples were allowed to stand for 24 h for equilibrium. Gamma-ray treatment was performed at room temperature with a high-level 60Co source (AECL IR79, Canada; Kang et al., 2011). The samples (three effluents and four estrogenic compounds) were prepared in 1 L amber bottles and irradiated with different absorbed doses of 1, 5 and 10 kGy. During gamma-ray treatment, air was constantly injected into the sample at 100 mL min  1.

temperature was programmed from 100 1C (held for 2 min) to 300 1C at 10 1C min  1, and then held for 10 min. Dissolved organic carbon (DOC) was analyzed using a Shimadzu TOC analyzer (model 5000 A, Kyoto, Japan). 2.3. Yeast two-hybrid assay The estrogen activity of the sample solution was measured by the yeast two-hybrid assay using a yeast b-galactosidase assay kit (Pierce, USA) and yeast cells (Saccharomyces cerevisiae Y190), into which medaka estrogen receptor (mERa) and the co-activator (TIF2) had been introduced (Shiraishi et al., 2003). Yeast culturing and the assay were conducted according to procedures published in the work of Kang et al. (2010). The absorbance at 420 nm for color absorbance and absorbance at 660 nm for turbidity from the yeast cell were read on a microplate spectrophotometer (Powerwave XS, Biotek, USA). The estrogenic activity was calculated as follows, and the results were used to calculate the relative estrogenic activity: estrogenic activity ðEAÞ ¼

1000  A420 t  V  OD660

ð1Þ

where t is the time of incubation (min), V is the volume of cells (mL), A420 is the absorbance at 420 nm, and OD660 is the optical density at 660 nm. The relative estrogenic activity was obtained by comparing estrogenic activity of the sample (EAsample) with the maximum estrogenic activity of E2 (EAmaximum,E2): relative estrogenic activity ðREAÞ ¼

EAsample  100 EAmaximum,E2

ð2Þ

Dose–response curves for estrogenic compounds were then fitted using the following equation to calculate EC50 (50% effective concentration of estrogenic compounds) values: a

2.2. Chemical analysis

y¼

EDCs were extracted from the samples using liquid–liquid extraction (LLE) methods (Jin et al., 2004) with a 2 L separation funnel (Witeg, Germany). Samples were rigorously shaken for 3 min using dichloromethane (DCM) as solvent three times, and sodium sulfate was added into the extracted samples for dehydration and then was concentrated by a rotary evaporator. The residues were transferred to a reaction vial and gently evaporated to dryness under a stream of high purity nitrogen. After dissolving with 1 mL of dimethyl sulfoxide (DMSO), the solution was used for analysis of estrogenic compounds and estrogenic activity. Estrogenic compounds were analyzed using a GC-MSD 6890 (Agilent, USA) with a DB-5-ms column (15 m  250 mm id; 0.25 mm film thickness, J&W Scientific, USA). Helium (99.9999%) was used as a carrier gas at 1 mL min  1. The injector temperature was 280 1C and injections were made in the splitless mode. The column oven

where a is the maximum relative estrogenic activity, b the minimum relative estrogenic activity, and xo ¼EC50 (50% effective concentration of estrogenic chemicals). Relative potency was calculated as the ratio of EC50 for E2 (EC50,E2) to EC50 for estrogenic compounds (EC50,i):.

ð3Þ

1þ ðx=xo Þb

relative potency ðRPÞ ¼

EC 50,E2 EC 50,i

ð4Þ

The E2 equivalent (EEQi) concentration was obtained by multiplying relative potency (RP) with concentration of each estrogenic compound (Ci), and the EEQ value of effluent samples was calculated by the summation of EEQ i: EEQ ¼

X

RP  C i ¼

i

X

EEQ i

ð5Þ

i

Table 1 Characteristics of three wastewater treatment plants (WWTPs) and respective effluents investigated in this study. WWTPs

Sewage Industrial Livestock a

Capacity (m3 d  1)

40,000 189,000 (industrial), 90,000 (domestic) 2000

Biological nitrogen and phosphorus removal.

Advanced treatment

Bio-Denipho processa Coagulation/flocculation process Constructed wetland

Effluent pH

DO (mg L  1)

DOC (mg L  1)

7.0 6.8 6.8

9.0 3.0 6.8

4.6 4.5 67.5

B.-Y. Ahn et al. / Radiation Physics and Chemistry 81 (2012) 1757–1762

3. Results and discussion 3.1. Identification of estrogenic compounds in effluents The chemical structure and physicochemical properties of E2, E1, EE2 and BPA are shown in Table 2. In general, these estrogenic compounds are less volatile and hydrophobic. EE2, E1 and BPA were detected in sewage effluent at 22.05, 5.99, and 91.29 ng L  1, respectively, but E2 was not found (Table 3). Lee et al. (2007) demonstrated that removal rates of E1 and E2 in five STPs were approximately 89.0% and 73.1%, respectively; thus the concentrations of E1 and E2 found in effluents were 3.4 ng L  1 and 2.4 ng L  1 in average, respectively. Nelson et al. (2007) and Rutishauser et al. (2004) reported that a variety of estrogenic chemicals such as E2, E1, EE2 and BPA were detected up to 44 ng L  1 in sewage effluents. Concentrations of EE2 (14.56 ng L  1) and E1 (5.30 ng L  1) in industrial effluent were similar to those of sewage effluent, while the concentration of BPA (1501 ng L  1) was found to be much higher (Table 3). According to a study of Sun et al. (2008), natural estrogen (E1 and E2) was not detected in industrial effluent, whereas nonylphenol, octylphenol and BPA were found at concentrations of 13, 1.4 and 89 mg L  1, respectively. Staples et al. (1998) also reported that BPA mainly originated from industrial factories that manufacture adhesives, paw paints, building materials, paper coatings and dyes. E2, E1, EE2 and BPA were observed in the livestock effluent at concentrations 18.50, 42.77, 45.96 and 198 ng L  1, respectively (Table 3). In particular, concentration of E1 was about 8–9 times higher than that in other effluents. According to the results of Sarmah et al. (2006), the livestock effluent contained higher levels of E2 (28–289 ng L  1) and E1 (66–3057 ng L  1)

1759

compared to E2 (14 ng L  1) and E1 (19–84.7 ng L  1) in the sewage effluent. Relative potency of E1, EE2 and BPA compared to E2 was found to be 0.39, 0.11 and 3.00  10–3, respectively (Table 4). Lee et al. (2007) reported that the relative potencies for E1 and EE2 (0.88 and 0.951, respectively) were similar, whereas the values were quiet different (0.0144 and 0.1605, respectively) according to the work of Kang et al. (2010) using yeast two-hybrid assay. Duong et al. (2010) demonstrated that relative potencies derived from E-Screen assay for EE2, E1, and BPA, respectively were 1.0, 0.1, and 6.0  10–5. These findings suggest that estrogenic activity may vary according to different assays. As shown in Fig. 2, E2, E1 and EE2 mainly contributed to the estrogenic activity of sewage and livestock effluents while contribution from BPA was not significant due to its very low relative potency. However, estrogenic activity of industrial effluent was largely attributable to BPA because the concentration of BPA was over 100 times larger than those of other estrogenic chemicals.

3.2. Reduction of estrogenic activity by gamma-ray treatment Estrogenic activity of livestock effluent (16 ng-EEQ L  1) was much higher than that of sewage and industrial effluents (4.4 and 1.5 ng-EEQ L  1, respectively) (Fig. 1). Sarmah et al. (2006) reported that activity of livestock effluent was in the range 32–519 ng-EEQ L  1 while that of sewage effluent ranged between 21 and 31 ng-EEQ L  1. The activity in livestock effluent was significantly reduced down to 9.9 ng-EEQ L  1 by gamma-ray treatment at a dose of 10 kGy, while no significant difference

Table 2 Physicochemical properties of estrogenic compounds, 17b-estradiol (E2), 17a-ethylestradiol (EE2), estrone (E1) and bisphenol A (BPA), used in this study. E2a

E1a

EE2a

BPAb

272.4 3.94 13

270.4 3.43 13

296.4 4.15 4.8

228.0 3.32 120

Chemical structure

Molecular weight (g mol  1) log Kow Water solubility at 20 1C (mg L  1) a b

Howard (1989). Ying et al. (2002)

Table 3 Degradation of 17b-estradiol (E2), estrone (E1), 17a-ethynylestradiol (EE2) and bisphenol A (BPA) in effluents by gamma-ray treatment. Detection limits of E2, E1, EE2, and BPA were 0.92, 3.45, 1.41 and 0.46 ng L  1, respectively. Samples

E2 (ng L  1)

E1 (ng L  1)

EE2 (ng L  1)

BPA (ng L  1)

Sewage effluent

0 kGy 1 kGy 5 kGy 10 kGy

N.D.a N.D. N.D. N.D.

5.997 2.65 4.327 1.77 4.587 1.12 5.687 0.39

22.05 7 0.18 13.68 7 0.89 14.72 7 13.51 12.57 7 10.91

91.29 7 16.50 39.46 7 15.29 13.85 7 3.05 N.D.

Industrial effluent

0 kGy 1 kGy 5 kGy 10 kGy

N.D. N.D. N.D. N.D.

5.307 2.61 3.667 0.10 N.D. N.D.

14.56 7 5.65 9.67 7 4.73 8.12 7 6.32 7.89 7 5.63

1501 79.66 N.D. N.D. N.D.

Livestock effluent

0 kGy 1 kGy 5 kGy 10 kGy

18.507 11.45 6.137 6.08 N.D. N.D.

42.77 722.31 21.97 715.98 5.617 3.36 N.D.

45.96 7 22.31 55.52 7 15.39 9.55 7 2.43 17.95 7 1.71

198 7 42.94 N.D. N.D. N.D.

a

Not detected.

1760

B.-Y. Ahn et al. / Radiation Physics and Chemistry 81 (2012) 1757–1762

Table 4 Relative potency of estrogenic activity for 17b-estradiol (E2), 17a-ethynylestradiol (EE2), estrone (E1) and bisphenol A (BPA). Regression parameters (a¼ maximum relative estrogenic activity, b ¼minimum relative estrogenic activity, xo ¼EC50 (50% effective concentration of estrogenic chemical)) were determined by fitting the dose–response curve using Eq. (3), and relative potency was determined using Eq. (4). Estrogenic compounds

E2 E1 EE2 BPA

Parameter a

b

xo (EC50, M) R2

100.00 71.06 94.89 36.03

 0.6468  0.4764  0.3411  0.5716

6.08  10  8 1.56  10  7 5.53  10  7 1.60  10  5

Relative potency

0.9807 1.00 0.9626 0.39 0.9825 0.11 0.9844 3.00  10  3

Fig. 1. Reduction of estrogenic activity in effluents from sewage, industrial and livestock wastewater treatment plants by gamma-ray treatment. Significant difference (po 0.05) is indicated as lowercase letters.

matters in wastewater. However, Bila et al. (2007) demonstrated that estrogenic activity still remained though the removal rate of estrogenic chemicals was up to 99% by ozonation. Almost all E2, E1 and BPA in three effluents were removed by gamma-ray treatment at a dose of 10 kGy, while EE2 was not completely removed (Table 3). As shown in Table 1, E2, E1 and EE2 have similar chemical structures except for the ethynyl group at position 17 in EE2, which makes the ring structure very stable against oxidation (Mes et al., 2005). Ning et al. (2007) also demonstrated that the ozone dose used for degrading EE2 was several times higher than that for E1. 3.3. Estimation of estrogenic activity in effluents There was no significant difference between the measured and calculated estrogenic activities of sewage effluent (Fig. 3a). However, estrogenic activity in industrial and livestock effluents was significantly overestimated particularly for doses 0 and 1 kGy (Fig. 3b and c). This might be caused by dissolved organic matters (DOMs) considering the DOC concentrations in these effluents (Table 1). In fact, endocrine disrupting chemicals were reported to be complexed with a wide variety of DOMs such as humic acid, fulvic acid and tannic acid, which disrupt the binding of compounds onto estrogen receptors (Yamamoto et al., 2003; Holbrook et al., 2005; Lee et al., 2011). In addition, Buckley (2010) demonstrated that antiestrogens in WWTP effluent accounted for approximately a 50% reduction in estrogenic activity of the effluent. In contrast, estrogenic activity in livestock effluent for doses of 5 and 10 kGy was significantly underestimated (Fig. 3c). This seemed to be due to the estrogenic by-products that were generated by radiation treatment. Kimura et al. (2004, 2007) demonstrated that estrogenic activity decreased slower than that expected from degradation of E2 by gamma-ray treatment due to formation of estrogenic by-products. Also, ozonation of E2 was found to produce 2-hydroxyestradiol having the estrogenic activity comparable to that of E2 (Bila et al., 2007). In order to identify the difference in calculated and measured estrogenic activities, E2, E1, EE2 and BPA were separately irradiated by gamma-rays in the presence of the Suwannee River natural organic matter (NOM). As shown in Fig. 4, the measured estrogenic activity was significantly lower than the calculated ones particularly for E2 and EE2, indicating inhibition of estrogenic activity by NOM. However, the measured estrogenic activity became higher than the calculated one for a dose of 5 kGy, which was likely attributable to the formation of estrogenic by-products from E2 and EE2. These findings clearly explain the absorbed dose-dependent difference between the calculated and measured estrogenic activities.

4. Conclusions

Fig. 2. Composition of estrogenic activity from 17b-estradiol (E2), 17a-ethynylestradiol (EE2), estrone (E1) and bisphenol A (BPA) in effluents from sewage, industrial and livestock wastewater treatment plants.

was observed for sewage and industrial effluents (Fig. 1). Kimura et al. (2007) reported that gamma-ray treatment at about 200 Gy was sufficient to eliminate the estrogenic activity of wastewater below 1 ng L  1, which largely depended on dissolved organic

Livestock effluent showed stronger estrogenic activity due to higher concentrations of E2, E1 and EE2 compared to sewage and industrial effluents, and this activity was not completely removed even after gamma-irradiation at a dose of 10 kGy. In particular, substantial concentrations of EE2 remained in all effluents after gamma-ray treatment, possibly due to low reactivity of EE2 toward water radiolysis intermediates produced by gammairradiation. Considering that concentrations of estrogenic compounds in the ng-EEQ L  1 range are enough to cause damages to aquatic organisms, more efficient treatment techniques in combination with ozone or catalysts, etc. should be further investigated. Dissolved organic matters seemed to influence the degradation of estrogenic compounds as well as to inhibit the expression of estrogenic activity in natural and waste waters. In addition,

B.-Y. Ahn et al. / Radiation Physics and Chemistry 81 (2012) 1757–1762

1761

Fig. 3. Comparison between calculated and measured estrogenic activities of sewage effluent (a), industrial effluent (b) and livestock effluent (c) treated by gammairradiation. Significant differences (*) between them are determined using one-way ANOVA (p o 0.05).

Fig. 4. Comparison between calculated (left bars) and measured (right bars) estrogenic activities of estrogenic compounds (10  3 M) treated by gammairradiation separately.

decomposition products from gamma-irradiation may increase the estrogenic activity in effluents. Thus, the underlying mechanisms in this treatment process should be further studied to provide an efficient and safe technique for estrogenic activity reduction in wastewater effluents.

Acknowledgments This work was supported by the National Research Foundation of Korea (NRF) grant (Grant Code: 2009-0078350) funded by the Korean government (MEST).

References Ankley, G.T., Johnson, R.D., Toth, G., Folman, L.C., Detenbeck, N.E., Bradbury, S.P., 1997. Development of a research strategy for assessing the ecological risk of endocrine disruptors. Toxicolology 1, 71–106. Auriol, M., Youssef, F.M., Tyagi, R.D., 2006. Endocrine disrupting compounds removal from wastewater, a new challenge. Process. Biochem. 41, 525–539. Bila, D., Montalvao, A.F., Azevedo, D.A., Dezotti, M., 2007. Estrogenic activity removal of 17b-estradiol by ozonation and identification of by-products. Chemosphere 69, 736–746. Buckley, J., 2010. Quantifying the antiestrogen activity of wastewater treatment plant effluent using the yeast estrogen screen. Environ. Toxicol. Chem. 29, 73–78.

Chen, T.S., Chen, T.C., Yeh, K.J., Chao, H.R., Liaw, E.T., Hsieh, C.Y., Chen, K.C., Hsieh, L.T., Yeh, Y.L., 2010. High estrogen concentrations in receiving river discharge from a concentrated livestock feedlot. Sci. Total Environ. 408, 3223–3230. Duong, C.N., Ra, J.S., Cho, J., Kim, S., Choi, H.K., Park, J.H., Kim, K.W., Inam, E., Kim, S.D., 2010. Estrogenic chemicals and estrogenicity in river waters of South Korea and seven Asian countries. Chemosphere 78, 286–293. Esplugas, S., Bila, D.M., Krause, L.T., Dezottiet, M., 2007. Ozonation and advanced oxidation technologies to remove endocrine disrupting chemicals (EDCs) and pharmaceuticals and personal care products (PPCPs) in water effluents. J. Hazard. Mater. 149, 631–642. Holbrook, R.D., Novak, J.T., Love, N.G., 2005. Impact of activated sludge-derived colloidal organic carbon on behavior of estrogenic agonist recombinant yeast bioassay. Environ. Toxicol. Chem. 24, 2717–2724. Howard, P.H., 1989. Handbook of Environmental Fate and Exposure Data, vol. 1. Lewis Publishers, Chelsea. Jin, X., Jiang, G., Huang, G., Liu, J., Zhou, Q., 2004. Determination of 4-tertoctylphenol, 4-nonylphenol and bisphenol A in surface waters from the Haihe River in Tianjin by gas chromatography–mass spectrometry with selected ion monitoring. Chemosphere 56, 1113–1119. Kang, S.W., Seo, J.H., Lee, B.C., Kim, S.J., Jung, J., 2010. Reduction of estrogenic activity by gamma-ray treatment. J. Korean Soc. Water Qual 26, 948–953. Kang, S.W., Shim, S.B., Park, Y.K., Jung, J., 2011. Chemical degradation and toxicity reduction of 4-chlorophenol in different matrices by gamma-ray treatment. Radiat. Phys. Chem. 80, 487–490. Kimura, A., Taguchi, M., Arai, H., Hiratsuka, H., Namba, H., Kojima, T., 2004. Radiation-induced decomposition of trace amounts of 17b-estradiol in water. Radiat. Phys. Chem. 69, 295–301. Kimura, A., Taguchi, M., Ohtani, Y., Shimada, Y., Hiratsuka, H., Kojima, T., 2007. Treatment of wastewater having estrogen activity by ionizing radiation. Radiat. Phys. Chem. 76, 699–706. Klavarioti, M., Mantzavinos, D., Kassinos, D., 2009. Removal of residual pharmaceuticals from aqueous systems by advanced oxidation processes. Environ. Int. 35, 402–417. ¨ Kusk, K.O., Kruger, T., Long, M., Taxvig, C., Lykkesfeldt, A.E., Frederiksen, H., Andersson, A.M., Andersen, H.R., Hansen, K., Nellemann, C., Bonefeld-Jørgensen, E.C., 2011. Endocrine potency of wastewater: contents of endocrine disrupting chemicals and effects measured by in vivo and in vitro assays. Environ. Toxicol. Chem. 30, 413–426. Lee, B.C., Lee, J.H., Kim, H.Y., Duong, C.N., Ra, J.S., Chang, N.I., Kim, H.K., Kim, S.D., 2007. Evaluation of the estrogenic chemicals and activity using E-screen and yeast two-hybrid assay in 5 sewage treatment plants. Korean Soc. Environ. Eng. 29, 1145–1153. Lee, J., Cho, J., Kim, S.H., Kim, S.D., 2011. Influence of 17b-estradiol binding by dissolved organic matter isolated from wastewater effluent on estrogenic activity. Ecotoxicol. Environ. Saf. 74, 1280–1287. Lu, G., Zhang, H., Wang, C., 2010. Assessment of estrogenic activity conducted by combining bioassay and chemical analyses of the effluent from wastewater treatment plants in Nanjing, China. Environ. Toxicol. Chem. 29, 1279–1286. Ma, M., Rao, K., Wang, Z., 2007. Occurrence of estrogenic effects in sewage and industrial wastewaters in Beijing China. Environ. Pollut. 147, 331–336. Mes, T., Zeeman, G., Lettinga, G., 2005. Occurrence and fate of estrone, 17bestradiol and 17a-ethynylestradiol in STPs for domestic wastewater. Rev. Environ. Sci. Biotechnol. 4, 275–311. Nelson, J., Bishay, F., Roodselaar, A., Ikonomou, M., Law, F., 2007. The use of in vitro bioassays to quantify endocrine disrupting chemicals in municipal wastewater treatment plant effluents. Sci. Total. Envinron. 374, 80–90. Ning, B., Graham, n., Zhang, Y., Nakonechny, M., Gamal, M., 2007. Degradation of endocrine disrupting chemicals by ozone/AOPs 29, 153–176Ozone- Sci. Eng. 29, 153–176. Pikaev, K., 1994. Environmental applications of radiation technology. High Energy Chem. 28, 5–16.

1762

B.-Y. Ahn et al. / Radiation Physics and Chemistry 81 (2012) 1757–1762

Rutishauser, B.V., Pesonen, M., Escher, B.I., Ackermann, G.E., Aerni, H.R., Suter, M.J., Eggen, R.I., 2004. Comparative analysis of estrogenic activity in sewage treatment plant effluents involving three in vitro assays and chemical analysis of steroids. Environ. Toxicol. Chem. 23, 857–864. Sarmah, A.K., Northcott, G.L., Leusch, F.D., Tremblay, L.A., 2006. A survey of endocrine disrupting chemicals (EDCs) in municipal sewage and animal waste effluents in the Waikato region of New Zealand. Sci. Total Environ. 355, 135–144. Shim, S.B., Jo, H.J., Jung, J., 2009. Toxicity identification of gamma-ray treated phenol and chlorophenols. J. Radioanal. Nucl. Chem. 280, 41–46. Shiraishi, F., Okuma, T., Nomachi, M., Serizawa, S., Nishikawa, J., Edmonds, J.S., Shiraishi, H., Morita, M., 2003. Estrogenic and thyroid hormone activity of a series of hydroxy-polychlorinated biphenyls. Chemosphere 52, 33–42. Silva, C.P., Otero, M., Esteves, V., 2012. Processes for the elimination of estrogenic steroid hormones from water: a review. Environ. Pollut. 165, 38–58.

Staples, C.A., Dorn, P.B., Klecka, G.M., O’Block, S.T., 1998. A review of environmental fate, effects, and exposures of bisphenol A. Chemosphere 36, 2149–2173. Sun, Q., Deng, S., Huang, J., Shen, G., Yu, G., 2008. Contributors to estrogenic activity in wastewater from a large wastewater treatment plant in Beijing, China. Environ. Toxicol. Phar. 25, 20–26. USEPA, 1997. Special Report on Environmental Endocrine Disruptors: an Effect Assessment and Analysis. EPA630/R-96/012, USEPA, Washington, DC. Yamamoto, H., Liljestrand, H.M., Shimizu, Y., Morita, M., 2003. Effects of physical– chemical characteristics on the sorption of selected endocrine disruptors by dissolved organic matter surrogates. Environ. Sci. Technol. 37, 2646–2657. Ying, G.G., Kookana, R.S., Ru, Y.J., 2002. Occurrence and fate of hormone steroids in the environment. Environ. Int. 28, 545–551.