Transformation of Oxidation Products and Reduction of Estrogenic

Jun 17, 2008 - FeOOHR), was synthesized and evaluated through transformation of a steroidal endocrine disrupting compounds (EDC), 17β- estradiol (E2)...
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Environ. Sci. Technol. 2008, 42, 5277–5284

Transformation of Oxidation Products and Reduction of Estrogenic Activity of 17β-Estradiol by a Heterogeneous Photo-Fenton Reaction Y A P I N G Z H A O , * ,†,‡ J I A N G Y O N G H U , * ,‡ AND WEI JIN§ Department of Environmental Science, East China Normal University, Shanghai 200062, China, Division of Environmental Science and Engineering, National University of Singapore, 119260, Singapore, and College of Environmental Science and Engineering, Tongji University, Shanghai 200092, China

Received December 29, 2007. Revised manuscript received April 23, 2008. Accepted April 23, 2008.

A novel photo-Fenton catalyst, R-FeOOH loaded resin (RFeOOHR), was synthesized and evaluated through transformation of a steroidal endocrine disrupting compounds (EDC), 17βestradiol (E2), under weak UV irradiation in the presence of H2O2. E2 photodegradation intermediates elucidated in detail by GC/ MS and LC/MS/MS analyses and detailed reaction pathways are proposed. A yeast-based estrogen screen for E2 and its photodegradation intermediates was performed to measure the reduction of estrogenic activity in different water matrices during the heterogeneous photo-Fenton process. The results showed that R-FeOOHR not only degraded E2 but also removed the estrogenic activity originating from E2, its degradation intermediates, and its products. However, the water matrix present in drinking water may impact estrogenic activity reduction. The results are important to evaluate the ability of photoFenton advanced oxidation processes in reducing EDCs and their associated estrogenicity from drinking water.

Introduction Most endocrine disrupting compounds (EDCs) are synthetic organic chemicals introduced into the environment by anthropogenic input, but they can also be naturally generated estrogenic hormones (e.g., estrone, 17β-estradiol) and therefore are ubiquitous in aquatic environments (1–4). EDCs may mimic hormonal activity and disturb the biological equilibrium of aquatic ecosystems and be harmful to the general health of the population (5, 6). In surface waters, estrogens are present at a level from picograms per liter to nanograms per liter (7, 8). 17β-Estradiol (E2) is a well-known natural EDC, by far the most endocrine disrupting chemical. Its concentration ranging from 6 to 66 ng/L also was reported in groundwater or river water (9). Its endocrine disrupting potency can be several thousands of times higher than that * Address correspondence to either author. Phone: 86-2162238393 (Y.Z.); 65-6516 4540 (J.H.). Fax: 86-21-62233670 (Y.Z.); 65-67744202 (J.H.). E-mail: [email protected] (Y.Z.); [email protected] (J.H.). † East China Normal University. ‡ National University of Singapore. § Tongji University. 10.1021/es703253q CCC: $40.75

Published on Web 06/17/2008

 2008 American Chemical Society

of other synthetic chemicals such as nonylphenol; even as low a concentration as 1 ng/L estradiol can result in a distinctive endocrine disrupting effect in male trout (10–12). These events may occur at relative low, environmentally relevant concentrations of 0.1-20 ng/L that coincide with the peak of the dose-response curve for E2 of ∼1 nM (13, 14). At present, there is lack of criteria for EDCs in the latest draft of the WHO guidelines for drinking water quality, so much research has been conducted to study the positive effect of water treatment methods regarding the removal of EDCs. The removal of EDCs has not been achieved adequately in conventional chemical and biological processes and/or their sorption capacity on the sludge causes further concerns for sludge management. Activated carbon, which is known for its high adsorption capacity, will have to be replaced or regenerated very often, making this technique very expensive. A possible solution could be a self-regenerating matrix. Therefore, various advanced oxidation processes (AOPs) have been investigated to remove EDCs from the water matrix (15–17). Recently, many papers reported the deduction of estrogenic activity by various AOPs (ozonation, chlorination, UV/ H2O2 and TiO2 photocatalysis, etc.). Ohko et al. (18)reported the degradation of bisphenol A (BPA, 170 µM) and E2 (1 µM) in TiO2 (degussa P25) water suspensions by photocatalysis, respectively. Results showed that the estrogenic activity was almost lost concurrently with the initiation of photocatalytic degradation by an estrogen screening assay. E2 transformation also was demonstrated in a reaction system by TiO2 (18, 19). Several reaction products were identified but not enough to construct a detailed reaction pathway. Coleman et al. (20) compared temporal changes in the estrogenic activity of E2, estrone, and 17R-ethinylestradiol at environmentally relevant concentrations following both UVA photolysis and immobilized TiO2 photocatalysis. All three estrogens were decomposed with virtually all the estrogenic activity being removed within 55 min (20). TiO2 photocatalysis thus can be applied to water treatment to effectively remove natural and synthetic estrogens without producing biologically active intermediates. EDCs also were reported to react more rapidly with ozone than with chlorination. Hu et al. (21, 22) assessed the estrogenic activity potentially stemming from BPA and 4-nonylphenol (4-NP) chlorination in drinking water. Oxidation results suggested that the chlorinated BPA and 4-NP solution led to an increased estrogenic activity. Itoh et al. (23) also found a 2-3-fold increase in estrogenic effects in lake water after it was chlorinated. Moreover, Moriyama et al. (24) confirmed the formation of two products in highly chlorinated solutions after 60 min (4-chloro-EE2, 1-6 mol % and 2,4-dichloro-EE2, 3-25 mol %). The estrogenic activities of 4-chloro-EE2 were similar to those of the parent EE2. Huber et al. (25) investigated oxidation of the oral contraceptive 17R-ethinylestradiol (EE2) during ozonation and the estrogenic activity of its solution. It proved impossible to completely remove the estrogenic activity due to the slow reappearance of 0.1-0.2% of the initial EE2 concentration and incomplete mineralization after ozonation. Several studies reported and evaluated results regarding UV/H2O2 AOP oxidation of some EDCs (E2, EE2, BPA, and 4-NP). Synergistic effects or remaining estrogenic activity measured by Yes were observed by examining the oxidation of estrogenic activity associated with these EDCs via UV/ H2O2 (26, 27). Rosenfeldt et al. (28) suggested the presence of some oxidation byproducts that may retain estrogenic activity since complete mineralization of EDCs to carbon dioxide and water is impractical. While estrogens were VOL. 42, NO. 14, 2008 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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removed efficiently by such AOPs as O3, UV/TiO2, UV/H2O2, and chlorination, it is not well-established as to how efficiently they are removed by the photo-Fenton process (12). The degradation of estrogen (such as E2 and BPA, etc.) by a homogeneous photo-Fenton process or under an ultrasound assisting homogeneous Fenton process has been reported (29–31). However, the relationship of fate and estrogenic activity of E2 during these processes was not explored in detail. Hence, it is important to assess water treatment technologies with regard to their EDC removal potential and the associated estrogenicity. To overcome the weakness of conventional Fenton reactions (e.g., catalytic activity is efficient mainly in the pH range of 2.5 to ∼3, recycling of catalyst, etc.), we prepared a novel heterogeneous photo-Fenton catalyst, R-FeOOHR, and studied the influence of environmental factors on E2 degradation by R-FeOOHR (32). This study focused on an investigation of the transformation mechanism and reduction of estrogenic activity of E2 from Milli-Q water and drinking water by R-FeOOHR in a heterogeneous photo-Fenton process. The intermediates were identified by LC/MS/MS and GC/MS, and a photodegradation mechanism was provided in detail that would be useful to explain the loss of binding capacity of E2 to estrogen receptors. Because bioassays embody a high sensitivity for detecting the estrogenic activity of EDCs, Yes was used to assess the reduction of estrogenic activity for E2 solutions following this photo-Fenton process and the interference of the water matrix on E2 removal. This is particularly important given the relatively persistent and poorly characterized nature of the intermediate products of endocrine disruptors generated during this process. The result suggests that the heterogeneous photo-Fenton process is a potential AOP for eliminating steroid estrogenic compounds.

the 22 h irradiation. The recycling experiments were repeated 13 times under current experimental conditions. Photocatalyst samples also were analyzed by FTIR spectroscopy using a Jasco FTIR 430 spectrometer with an accessory for diffuse reflectance measurements (Jasco Co.). All photodegradation samples were concentrated by solid phase extraction (SPE). The amount of E2 in the test solutions was determined using liquid chromatography/triple quadrupole tandem mass spectrometry, equipped with a turbo ion spray interface (API2000 LC/MS/MS system, Applied Biosystems Asia Pte Ltd.) (32). Intermediates Analyses. Intermediates of 17β-estradiol photodegradation were identified in negative ion mode in m/z 40-350 by LC/MS/MS (32). Chemical analysis of intermediates of 17β-estradiol photodegradation also was carried out using a GC/MS system (QP2010, Shimadzu) equipped with a fused silica capillary column (DB-SMS, 30 m long, 0.32 mm i.d., 0.25 µm film thickness). A split-splitless injection port was used in the splitless mode at high pressure (19.2 kPa). The column temperature was programmed as follows: 2 min at 50 °C, 20 °C min-1 to 130 °C, 15 °C min-1 to 300 °C, and 8 min at 300 °C. The helium gas flow rate was 1.63 mL min-1 (at 50 °C). Electron impact was used for ionization of samples. Some of the intermediates were identified by the use of an identification program of the U.S. NIST library. Because the polarities of the intermediates are different, different peaks were observed in the chromatograph for the mixture at the operating conditions employed. Evaluation of Estrogenic Activities for Treated Water. The yeast colony (Saccharomyces cerevisiae strain BJ3505) was supplied by Gaido. Transcriptional estrogenic activities in response to a recombinant yeast-based estrogen assay were evaluated for the treated water as reported (14).

Results and Discussion Materials and Methods Chemicals. E2 (>98%; Sigma, 272.4 g/mol) was used without further purification. All the other chemicals and solvents of HPLC grade were purchased from Sigma-Aldrich. The water employed was purified by a Milli-Q system (Millipore Co.) with a resistivity higher than 18.2 M cm at 25 °C. The resin was Amberlite 200 with matrix of styrene-divinylbenzene, Na+ form (strongly acidic), and a particle size of 20-50 mesh (0.297-0.840 mm) (Fluka). The 0.1 mM stock solution was prepared by dissolving the desired amount of E2 into methanol and storing at 4 °C. Photo-Fenton Recycling Experiments. The photocatalyst R-FeOOHR was prepared according to ref 32. The photochemical reactor was made of an open cylindrical Pyrex container with a diameter of 19 cm and height of 9 cm and equipped with a magnetic stirring bar. A total of 1 L of the desired concentration of the E2 aqueous solution was prepared without adjusting the pH prior to the addition of the required amount of R-FeOOHR (5 g/L, 0.5 g Fe/L) and H2O2 (9.7 mM). The mixture was magnetically stirred at 200 rpm at 20 °C in an air cooled room. The experiments were conducted in an open reactor, and the lamps were not immersed in the solution, they were on top of the reactor. Irradiation was carried out with two 15 W black light lamps (Wuxing Co.) with 0.3 mW/cm2 irradiation intensity at the center of the reactor (measured by a UV radiometer, IL700, International Light) and a main emission wavelength of 365 nm. Because the concentration of 17β-estradiol is very low, weak UV irradiation avoided wasting the light energy. The main aim of choosing weak UV light (365 nm) provides promising technology for using natural light to degrade 17βestradiol. The distance between light source and surface of the solute was 5 cm. An ∼25 mL aliquot of the suspension was collected at regular intervals and analyzed for subsequent residual E2 concentrations and total dissolved iron during 5278

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Performance of E2 Decomposition by r-FeOOHR PhotoFenton Process. The novel photocatalyst R-FeOOHR was prepared by in situ hydrolysis of Fe (3+) ions inside the pores of photocatalytic carrier Amberlite 200 by carbamide (32). The polymer carriers make R-FeOOHR very easily separated from treated water systems. The crystalline pattern of loaded iron oxide on the resin is a typical pattern of crystalline R-FeOOH (goethite, syn). The morphology of R-FeOOHR confirmed the presence of R-FeOOH entities on the surface of resin as compared to noncoated resin (the gap on the surface of the resin was caused by the high vacuum of the SEM machine). The R-FeOOH entities were mainly onedimensional bars with a cross-section of 100 nm × 100 nm and a length of 300-400 nm except for a few irregular micrometer particles. Loaded R-FeOOH in the photocatalyst was 10 Fe wt % (i.e., 100 mg of Fe/g). The loaded R-FeOOH content in the polymer matrix was comparable to DeMarco, who reported that iron loaded on macroporous polystyrene beads functionalized with sulfonic acid groups could be 9-12 Fe wt % (33). A high content of iron in the Fenton catalyst inevitably increases the photocatalytic efficiency. The solution pH is also an important factor that dramatically influences the efficiency of the Fenton reaction. In previous work, we reported that the photodegradation process remained efficient and feasible from pH 3.07 to 11.00 (32). A good photocatalyst, in addition to its broad pH range of application, high photocatalytic capacity, and easy separation, must exhibit a superior self-regeneration ability for multiple uses. To verify the activity of the used catalyst and to check its lifetime, more than 13 experiments of the photocatalytic regenerablity of R-FeOOHR were conducted by a series of systematic experiments. After each photocatalytic cycle, R-FeOOHR was directly filtered and entered into the next photocatalytic cycle. After 13 photocatalytic cycles, and 8 h of photodegradation, the average residual E2

TABLE 1. Intermediates of E2 Photodegradation Detected by GC/MS

concentration was 32.6 µg/L with a standard deviation of 6.12% and an average iron leaching concentration of 0.5339 mg/L with a standard deviation of 0.245%. The surface of the resin was covered with R-FeOOH tightly and compactly to avoid OH radicals attacking its skeleton. The performance of R-FeOOHR basically remained at the level of an unused catalyst. The diffuse reflectance FTIR spectra of R-FeOOHR samples are shown in Figure S1. A very strong IR band at 3133 cm-1 is due to the presence of the OH stretching mode in R-FeOOH, whereas the IR band at 3420 cm-1 can be ascribed to stretching modes of surface H2O molecules or to the envelope of hydrogen bonded surface OH groups. Two typical bands of goethite at 902 and 801 cm-1 can be ascribed to Fe-O-H bending vibrations in R-FeOOH. The IR bands recorded at 630, 495, and 270 cm-1 were ascribed to Fe-O stretching vibrations (35). After 13 photocatalytic cycles of R-FeOOHR, the FTIR spectrum of R-FeOOHR was the same as the original catalyst. Results showed that the catalytic center R-FeOOH does not inactivate or change its chemical constituents. The resin carriers were not attacked by hydroxyl radicals in solution for R-FeOOH covering the whole surface of the resin. One study reported that in the first trial, the decomposition degree of phenol by TiO2 was 76%, while in the second trial, the decomposition degree was 32% and remained at about the same level during the third trial. New absorption bands in the region of 1200-1800 cm-1 also appeared in the spectra of the photocatalyst used in the reaction of phenol photo-oxidation by TiO2. These bands in the region of 1200-1800 cm-1 were assigned to CdO, C-H, C-C, and aromatic ring vibrations, which are due to carbon deposits on the catalyst surface (34). As compared to R-FeOOHR, TiO2 showed a poorer ability of reuse. Thus, selfregeneration of R-FeOOHR is possible. This can make this treatment process cost-effective, as the Fenton catalyst does not have to be replaced for a relatively long period of time. Photodegradation Mechanism of E2. The photocatalytic oxidation of organic compounds involves complicated multistage processes. However, only partial degradation

usually occurs, which often reduces the toxicity of the contaminants and increases the biodegradability of the residue. Also, it is sometimes possible for the process to generate products with the same or higher toxicity than the parent compounds (28). To elucidate the structures of the intermediates, the concentrated photodegradation sample was subjected to GC/MS and LC/MS/MS analysis. The identification of species was carried out through the use of an E2 photodegradation sample concentrated 1000fold by solid phase extraction (SPE) and then detected by GC/MS and an identification program obtained from NIST. GC/MS results (Table 1) obtained in the present study indicated the main identified peaks of 10-17β-dihydroxy1,4-estradien-3-one (DEO, RT 22.737 min), estrone (E1, (retention time) RT 24.560 min), 17β-estradiol (E2, RT 24.755 min), estra-1,3,5-(10),9(11)-tetraene-3,17-diol-(17β)- (ETD9, RT 24.911 min), and testosterone (TS, RT 25.286 min) with similarities of 89, 81, 92, 70, and 73%. Some peaks of intermediates were not identified clearly in the GC/MS analysis because other mass spectra look similar to each other, just as the peak at RT 24.350 min can be ascribed to DEO, androsta-4,16-dien-3-one (ADO), TS, and cis-TS, with a higher similarity (>68%). Ohko et al. (18) studied E2 photodegradation by TiO2 (degussa P25) and only identified three intermediates by GC/MS (DEO, ADO, and TS). They also reported BPA decomposed by TiO2 photocatalytic reactions and identified several intermediate products by LC/MS/MS analysis. The BPA degradation pathway was easily deduced because the BPA molecule is simpler than the E2 molecule. In this paper, under the current GC/MS conditions, estriol (E3) and estra-1,3,5(10)-triene-3,6,17-triol-(6R,17β)(ETT) (shown in Table 2), typical E2 degradation intermediates, could not be detected using standard substances. Because of the deficiencies of GC/MS, we attempted to elucidate the photodegradation mechanism of E2 by LC/ MS/MS. Table 2 lists the main fragments (m/z) and relative abundances (%) obtained by LC/MS/MS shown in Figure VOL. 42, NO. 14, 2008 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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TABLE 2. Intermediates of E2 Photodegradation Detected by LC/MS/MS

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TABLE 2. continued

S2. The m/z value for each peak corresponds to [M - 1]ions in the negative ion mode. For the sensitivity and specificity of LC/MS/MS, precursor ion (Q1)/product ions (Q3) of standard E3 and 2-HO-E2 confirmed the validity and specificity of these two intermediates (36). Specific Q1/Q3 ratios of intermediates (Figure S2b) also confirmed the presence of these specific intermediates (Table 2). However, the information of ADO in LC/MS/MS spectra was still lacking. The photodegradation reaction may be initiated by the addition of photocatalytically generated •OH to E2 undergoing different photodegradation pathways (37). There are two possible sites for the attack of •OH radicals: the aliphatic rings and the aromatic ring in the E2 structure. According to Ohko et al.’s (19) frontier electron density of E2, frontier electron densities were found to be higher at the phenol moiety of C1 to C5 at the phenolic ring and high at C6, C7, C11, and C12 atoms at aliphatic rings, sometimes even at C16. Thus, the reaction may be initiated by the addition of photocatalytically generated •OH to E2 through these carbon atoms. When •OH radicals attack the aliphatic rings, a number of intermediates (alcohols, ketones, and olefins) may be formed during the photocatalytic degradation of E2, such as E3, ETT, ETO, and ETD-9. These single aromatic intermediates are presumably further oxidized through ring rupturing reactions into aliphatic compounds containing acids and acetaldehyde. The attack of •OH radicals on the aromatic ring led to the formation of dihydroxy photoproducts and quinone-like products, such as 2-HO-E2, its isomers, and DEO. These products subsequently underwent •OH and HO2• attack, leading to complete mineralization (38). According to Table 2, the intermediates were produced in the subsequent reactions shown in Scheme (19, 39–41). The time dependences of the amounts of some intermediates can be detected under current experimental conditions shown in Figure S3. Three peaks appeared based on their order of RT in the LC/MS/MS chromatogram in

Figure S2a. However, the maxima peak areas relative to the initial E2 area were lower, ∼3.5% for TS, ∼1% for ETT, and below ∼8% for E1. Concentrations of intermediates ETT and TS were increased to maxima at 6 h under UV irradiation and then decreased to 0 with irradiation time. E1 was photodegraded with the same trend as that of E2, which was not like other intermediate photodegradation pathways. We rather think that E1 was not an intermediate of E2 photodegradation but an impurity of the E2 standard sample. Ohko et al. (19) also proved that E1 was not detected during photodegradation by TiO2. All of the peaks of E2 and its intermediates disappeared after 22 h of irradiation. Thus, it can be seen that the life spans of the intermediates formed at different stages of the reaction are short because the intermediates can undergo further fast oxidation. As to whether some intermediates, such as DEO, are generated by oxidation of the phenol moiety of E2 or hydroxyl substituted E2 products and E3 and ETT in subsequent photooxidation, it is reasonable to consider that the interaction between these intermediates and the human estrogen receptor (hER) should be changed. Because of conversion of the phenol moiety of E2 to a quinone-like moiety or increasing hydrophilicity by hydroxyl partly substituted E2, the intermediates should exhibit a much weaker estrogenic activity than that of E2 (19). Elimination of Estrogenic Activity of E2. It was found that many byproducts were formed in the heterogeneous photo-Fenton degradation of E2. The removal rate and reduction of transcriptional estrogenic activity of E2 in Milli-Q water and drinking water matrices (F- (0.45 mg/L), Cl- (12.91 mg/L), NO3- (4.16 mg/L), SO42- (14.57 mg/L), Na+ (2.19 mg/ L), K+ (6.43 mg/L), Ca2+ (14.28 mg/L), and humic acid (HA) (2.5 mg/L) spiked) were quantitatively evaluated in response to hER in a yeast assay screen (Figure 1). Five EDCs including E1, E2, E3, EE2, BPA, and natural organic matters (NOM, mainly HA) were spiked as a mixture in drinking water. VOL. 42, NO. 14, 2008 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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SCHEME 1. Simplified Mechanism of E2 Photodegradation

In Milli-Q water, the estrogenic activity of E2 photodegradation decreased from 1674 units to nearly zero with the E2 concentration decreasing from 272 to 1.8 µg/L after 22 h of irradiation photocatalyzed over R-FeOOHR. The binding affinity of E2 photodegradation samples with hER decreased with irradiation. The photodegradation rates and reduction of estrogenic activity for E2 can be determined from pseudofirst-order rate kinetics. The photodegradation of E2 over R-FeOOHR exhibited a removal rate of 0.25 h-1 (r2 ) 0.984) and an elimination rate of estrogenic activity of 0.37 h-1 (r2

FIGURE 1. Reduction of concentration and estrogenic activity of E2 during the photo-Fenton process. The 10 µL aliquots of the reaction mixture from an initial solution of E2 (272 µg/L) were sampled at frequent time intervals during reactions and were assayed for estrogenic activity in the recombinant yeast assay in (a) Milli-Q water and (b) drinking water. Inset is an estrogenic activity-diluted E2 concentration relationship curve. [E2]0 ) 272 µg/L; [H2O2] ) 9.7 mmol/L; pH ) 7.47; T ) 20 °C; and [r-FeOOHR] ) 5 g/L. 5282

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) 0.942). Ohko et al. (19) previously reported that the photocatalysis reaction with E2 began via oxidation of the phenol moiety, which is known to be critical for receptor binding and for conferral of estrogenicity to all steroid estrogens. It is likely that photocatalysis may quickly remove the capacity of E2 to bind to the estrogen receptor. If one or more products of the photocatalytic degradation of E2 retained a similar level of estrogenic activity as the parent compound, the rate of estrogenic activity removal would be retarded as compared to the photodegradation rate of the parent compound. However, there is no statistically significant difference between rate of oxidation and rate of reduction of estrogenic activity for E2 treated with R-FeOOHR. Therefore, it can be deduced that the observed degradation in the parent compound corresponds directly to a reduction in estrogenic activity that was the same as that of Rosenfeldt and Linden’s report (28). The similarity between E2 removal rate and estrogenic activity removal rate implies that none of the oxidation byproducts produced by R-FeOOHR are comparable to the parent compound in terms of estrogenic activity. The elimination of estrogenic activity of E2 is associated with the loss of the chemical structure similarity with E2 that enables these intermediates not to bind to hER. The activity-concentration relationship (dose-response curve) for E2 and its intermediates also was examined. The amount of intermediates during E2 photodegradation reached almost a maximum value in 6 h of treatment. The treated solution of 6 h (68.5 µg/L) and initial E2 solution (272 µg/L) were diluted 2-6 orders of magnitude, and the estrogenic activity of the diluted solutions was evaluated from the inset in Figure 1. It was found that the intermediates in 6 h of treatment had a smaller estrogenic activity than the initial E2 dose-response curve in this concentration region, suggesting that estrogenic activities induced by photodegradation intermediates were much lower than those of the parent compound E2 and thus would not elicit an estrogen receptormediated response. This means that there is no secondary risk to increase the estrogenic activity in treated water as a result of photocatalytic degradation of E2 by R-FeOOHR under weak UV irradiation.

In a drinking water system, the estrogenic activity increased from 1954 to 2291 units and then decreased to 260 units with the E2 concentration decreasing from 272 to 3.7 µg/L. This trend in the complex system was not like that of the E2 estrogenic activity in Milli-Q water. Different estrogens also will interact in synergy, thus making this system very complex. When the concentration of estrogens is too high, it inhibits the expression of the yeast-based estrogen assay. Until a suitable estrogenic concentration is reached, it will induce a change of the yeast-based enzyme expression. All photodegradation of EDCs over R-FeOOHR exhibited pseudofirst-order reaction kinetics, such as E1 (0.26, r2 ) 0.979), E2 (0.28, r2 ) 0.997), E3 (0.23, r2 ) 0.995), EE2 (0.28, r2 ) 0.996), and BPA (0.21, r2 ) 0.995). This trend should prove that EDCs experience almost the same photodegradation mechanism and that the phenol moiety of EDCs should be the starting point of photodegradation, so that the estrogenic activity of EDCs should almost be lost concurrently with photodegradation. This is known to be critical for receptor binding and for the conferral of estrogenic activity to all steroid estrogens (19). As long as the reaction time is long enough, the estrogenic activity of the EDC mixture will be eliminated in the end. The result is important in enabling us to estimate the interaction and/or combined estrogenic activity among mixtures of EDCs associated with their presence in a drinking water matrix. For the safe use of water, this heterogeneous photo-Fenton technology will need to be assessed for its capability of removing EDCs to ensure a safe and costeffective drinking water supply.

Acknowledgments Research support from the National University of Singapore, NSF of China (20707006), PCRRF07002, and the Doctoral Fund of the China Ministry of Education (20070269034) is greatly appreciated. The anonymous reviewers also are acknowledged for their improvement of the manuscript.

Supporting Information Available Figure S1: FTIR of R-FeOOHR before or after 13 times photodegradation cycle of E2 after 22 h of irradiation; Figure S2: (a) LC/MS/MS chromatograph and (b) MRM chromatographs; and Figure S3: concentrations of intermediates detected by LC/MS/MS with irradiation time. This material is available free of charge via the Internet at http:// pubs.acs.org.

Literature Cited (1) Boyd, G. R.; Reemtsma, H.; Grimm, D. A.; Mitra, S. Pharmaceuticals and personal care products (PPCPs) in surface and treated waster of Louisiana and Ontario, Canada. Sci. Total Environ. 2003, 311, 135–149. (2) Guillette, L. H. Endocrine-disrupting environmental contaminants and developmental abnormalities in embryos. Hum. Ecol. Risk Assess. 1995, 1 (2), 25–36. (3) Sonnenschein, C.; Soto, A. M. An update review of environmental estrogen and androgen mimics and antagonistics. J. Steroid Biochem. Mol. Biol. 1998, 65, 143–150. (4) Belfroid, A. C.; Van der Horst, A.; Vethaak, A. D.; Schafer, A. J.; Rijs, G. B. J.; Wegener, J.; Cofino, W. P. Analysis and occurrence of estrogenic hormones and their glucuronides in surface water and waste water in The Netherlands. Sci. Total Environ. 1999, 225, 101–108. (5) Aneck-Hahnl, N. H.; de Jager, C.; Bornman, M. S.; du Toit, D. Oestrogenic activity using a recombinant yeast screen assay (RCBA) in South African laboratory water sources. Water SA 2005, 31 (2), 253–256. (6) Michael, J. Are problems with male reproductive health caused by endocrine disruption? Occup. Med. Educ. 2001, 58, 281–288. (7) Baronti, C. R.; Curini, G. D.; Di Cocia, A; Gentili, A; Samperi, R. Monitoring natural and synthetic estrogens at activated treatment plants and in receiving river water. Environ. Sci. Technol. 2000, 34, 5059–5066.

(8) Kuch, H. M.; Ballschmitter, K. Determination of endocrinedisrupting phenolic compounds and estrogens in surface and drinking water by HRGC-(NCI)-MS in the picogram per liter range. Environ. Sci. Technol. 2001, 35, 3201–3206. (9) Peterson, E. W.; Davis, R. K.; Orndorff, H. A. 17β-Estradiol as an indicator of animal waste contamination in mantled karst aquifers. J. Environ. Qual. 2001, 29, 826–834. (10) Purdom, C. E.; Hardiman, P. A.; Bye, V. J.; Eno, N. C.; Tyler, C. R.; Sumpter, J. P. Estrogenic effects of effluents from sewage treatment works. J. Chem. Ecol. 1994, 8, 275–285. (11) Jobling, S.; Nolan, M.; Tyler, C. R.; Brighty, G.; Sumpter, J. P. Widespread sexual disruption in wild fish. Environ. Sci. Technol. 1998, 32, 2498–2506. (12) Chen, C.; Wen, T.; Wang, G.; Cheng, H.; Lin, Y.; Lien, G. Determining estrogenic steroids in Taipei waters and removal in drinking water treatment using high-flow solid-phase extraction and liquid chromatography/tandem mass spectrometry. Sci. Total Environ. 2007, 378, 352–365. (13) Russo, J.; Tahin, Q.; Lareef, M. H.; Hu, Y.; Russo, I. H. Neoplastic transformation of human breast epithelial cells by estrogens and chemical carcinogens. Environ. Mol. Mutagen. 2002, 39 (2-3), 254–263. (14) Gaido, K. W.; Leonard, L. S.; Lovell, S.; Gould, J. C.; Babai, D.; Portier, C. J.; Mcdonnell, D. P. Evaluation of chemicals with endocrine modulating activity in a yeast-based steroid hormone receptor gene transcription assay. Toxicol. Appl. Pharmacol. 1997, 143, 205–212. (15) Belgiorno, V; Rizzo, L. F.; Despo, R.; Della, C.; Lofrano, G.; Nikolaou, A.; Naddeo, V.; Meric, S. Review on endocrine disrupting-emerging compounds in urban wastewater: Occurrence and removal by photocatalysis and ultrasonic irradiation for wastewater reuse. Desalination 2007, 215, 166–176. (16) Coleman, H. M.; Chiang, K.; Amal, R. Effects of Ag and Pt on photocatalytic degradation of endocrine disrupting chemicals in water. Chem. Eng. J. 2005, 113 (1), 65–72. (17) de Rudder, J.; Van de Wiele, T.; Dhooge, W.; Comhaire, F.; Verstraetea, W. Advanced water treatment with manganese oxide for the removal of 17R-ethynylestradiol (EE2). Water Res. 2004, 38, 184–192. (18) Ohko, Y.; Ando, I.; Niwa, C.; Tatsuma, T.; Yamamura, T.; Nakashima, T.; Kubota, Y.; Fujishima, A. Degradation of bisphenol A in water by TiO2 photocatalyst. Environ. Sci. Technol. 2001, 35, 2365–2368. (19) Ohko, Y.; Iuchi, K.; Niwa, C.; Tatsuma, T.; Nakashima, T.; Iguchi, T.; Kubota, Y.; Fujishima, A. 17β-Estradiol degradation by TiO2 photocatalysis as a means of reducing estrogenic activity. Environ. Sci. Technol. 2002, 36, 4175–4181. (20) Coleman, H. M.; Routledge, E. J.; Sumpter, J. P.; Eggins, B. R.; Byrne, J. A. Rapid loss of estrogenicity of steroid estrogens by UVA photolysis and photocatalysis over an immobilized titanium dioxide catalyst. Water Res. 2004, 38, 3233–3240. (21) Hu, J.; Aizawa, T.; Ookbo, S. Products of aqueous chlorination of bisphenol A and their estrogenic activity. Environ. Sci. Technol. 2002, 36, 1980–1987. (22) Hu, J.; Xie, G.; Aizawa, T. Products of aqueous chlorination of 4-nonylphenol and their estrogenic activity. Environ. Toxicol. Chem. 2002, 21 (10), 2034–2039. (23) Itoh, S.; Ueda, H.; Naasaka, T.; Nakanishi, G.; Sumitomo, H. Evaluating variation of estrogenic effect by drinking water chlorination with the MVLN assay. Water Sci. Technol. 2000, 42, 61–69. (24) Moriyama, K.; Matsufuji, H.; Chino, M.; Takeda, M. Identification and behavior of reaction products formed by chlorination of ethynylestradiol. Chemosphere 2004, 55, 839–847. (25) Huber, M.; Ternes, T.; Van Gunten, U. Removal of estrogenic activity and formation of oxidation products during ozonation of 17R-ethinylestradiol. Environ. Sci. Technol. 2004, 38, 5177– 5186. (26) Rosenfeldt, E. J.; Chen, P.; Kullman, S.; Linden, K. G. Destruction of estrogenic activity in water using UV advanced oxidation. Sci. Total Environ. 2007, 377, 105–113. (27) Chen, P.; Linden, K. G.; Hinton, D. E.; Kashiwada, S.; Rosenfeldt, E. J.; Kullman, S. W. Biological assessment of bisphenol A degradation in water following direct photolysis and UV advanced oxidation. Chemosphere 200665, 1094–1102. (28) Rosenfeldt, E. J.; Linden, K. G. Degradation of endocrine disrupting chemicals bisphenol A, ethinyl estradiol, and estradiol during UV photolysis and advanced oxidation processes. Environ. Sci. Technol. 2004, 38, 5476–5483. (29) Katsumata, H.; Kawabe, S.; Kaneco, S.; Suzuki, T.; Ohta, K. Degradation of bisphenol A in water by the photo-Fenton reaction. J. Photochem. Photobiol., A 2004, 162, 297–305. VOL. 42, NO. 14, 2008 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

9

5283

(30) Torres, R. A.; Pe´trier, C.; Combet, E.; Moulet, F.; Pulgarin, C. Bisphenol A mineralization by integrated ultrasound-UV-iron (II) treatment. Environ. Sci. Technol. 2007, 41, 297–302. (31) Wang, L.; Zhang, F.; Liu, R.; Zhang, T.; Xue, X.; Xu, Q.; Liang, X. FeCl3/NaNO2: An efficient photocatalyst for the degradation of aquatic steroid estrogens under natural light irradiation. Environ. Sci. Technol. 2007, 41, 3747–3751. (32) Zhao, Y.; Hu, J. Photo-Fenton degradation of 17β-estradiol in presence of R-FeOOHR and H2O2. Appl. Catal., B 2008, 78 (34), 250–258. (33) DeMarco, M. J.; SenGupta, A. K.; Greenleaf, J. E. Arsenic removal using a polymeric/inorganic hybrid sorbent. Water Res. 2003, 37, 164–176. (34) Letter to the Editor. Photocatalytic labyrinth flow reactor with immobilized P25 TiO2 bed for removal of phenol from water. Appl. Catal., B 2003,46, 415-419. (35) Krehula, S.; Popovic, S.; Music, S. Synthesis of acicular R-FeOOH particles at a very high pH. Mater. Lett. 2002, 54, 108–113. (36) Becka, I.; Bruhn, R.; Gandrass, J.; Ruck, W. Liquid chromatography-tandem mass spectrometry analysis of estrogenic com-

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9

ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 42, NO. 14, 2008

(37)

(38)

(39)

(40) (41)

pounds in coastal surface water of the Baltic Sea. J. Chromatogr. A 2005, 1090, 98–106. Kaneco, S.; Katsumata, H.; Suzuki, T.; Ohta, K. Titanium dioxide mediated photocatalytic degradation of dibutyl phthalate in aqueous solutionsKinetics, mineralization, and reaction mechanism. Chem. Eng. J. 2006, 125, 59–66. Chhor, K.; Bocquet, J. F.; Colbeau-Justin, C. Comparative studies of phenol and salicylic acid photocatalytic degradation: Influence of adsorbed oxygen. Mater. Chem. Phys. 2004, 86, 123– 131. Kaneco, S.; Katsumata, H.; Suzuki, T.; Ohta, K. Titanium dioxide mediated photocatalytic degradation of dibutyl phthalate in aqueous solutionsKinetics, mineralization, and reaction mechanism. Chem. Eng. J. 2006, 125, 59–66. Du, P.; Moulijn, J. A.; Mul, G. Selective photo(catalytic) oxidation of cyclohexane: Effect of wavelength and TiO2 structure on product yields. J. Catal. 2006, 238, 342–352. Linsebgler, A. L.; Lu, G.; Yate, J. T. K. Photocatalysis on TiO2 surfaces: Principles, mechanisms, and selected results. Chem. Rev. 1995, 95, 735–758.

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