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Fate of Estrogens in a Municipal
concentrations for fish (5-9). Ozonation, UV-radiation,membrane filtration, and activated carbon adsorption are Sewage Treatment Plant
potential treatments that might improve the effectiveness ofestrogen removal in a STP (4, 5, 10-15). However, imple-mentation of these techniques would increase the cost of wastewater treatment. Alternatively, understanding the fate of estrogens within the STPs might yield removal methods B E N T H A L L I N G - S Ø R E N S E N , † A N D based on better management or minor modifications of The Danish University of Pharmaceutical Sciences,Institute of Analytical Chemistry, Universitetsparken 2, In batch experiments, Ternes et al. (16) investigated the DK-2100 Copenhagen, Denmark, EAWAG, basic aerobic microbial reactions of estrogens in contact with Ueberlandstrasse 133, 8600 Duebendorf, Switzerland, activated sludge taken from the old Wiesbaden plant, which removes BOD. Experiments were performed at 20 °C with a Kaiserin-Augusta-Anlagen 15-17, D-56068 Koblenz, Germany starting concentration of 1 µg/L and a total suspended solids(TSS) concentration of 0.52 g of TSS/L. Assuming a pseudo-first-order reaction (TSS ) constant): dC CE2 with the pseudo-first-order reaction constant kE2 ≈ 150 The fate of the highly potent endocrine disrupters estrone L/(g of TSS‚d), E2 was found to have a T1/2 of about 0.2 h with (E1), 17 -estradiol (E2), and 17R-ethinylestradiol (EE2) nearly all the E2 being converted to E1. E1 was removed was investigated in mechanical and biological sewage more slowly with a T1/2 of about 1.5 h at 20 °C in the same treatment as well as in sewage-sludge treatment at concentration range and with the same TSS concentration.
a municipal German sewage treatment plant (STP). The The pseudo-first-order reaction constant was therefore kE1 main outcome of the study was that a common municipal ≈ 20 L/(g of TSS‚d). In this study, EE2 was not degraded STP with an activated sludge system for nitrification significantly within 48 h. Layton et al. (17) conducted a similarstudy with estrogens using activated sludge from STPs and denitrification including sludge recirculation can operating in a warmer climate. E2 was mineralized to CO appreciably eliminate natural and synthetic estrogens. As within a few hours. Thus, an accumulation of E1 could not a consequence, the endocrine effects of biota in the be observed. As in the German study, EE2 was found to receiving waters should be significantly reduced. All estrogen metabolize much more slowly, even though 40% was concentrations decreased gradually along the treatment mineralized in 24 h. Activated sludge bacteria can therefore train. In the STP effluent, the steroid estrogen concentrations be expected to be more active at higher ambient temper- were always below the quantification limit of 1 ng/L. The elimination efficiency of the natural estrogens (E1 and E2) Estrogens from humans are largely excreted as conju- exceeded 98%, and EE2 was reduced by more than 90%.
gates, mainly glucuronides (18). In batch experiments, E2- The natural estrogens were largely degraded biologically in glucuronides were cleaved to E2 with pseudo-first-order the denitrifying and aerated nitrifying tanks of the activated reaction constants similar to those of E2 degradation, and sludge system, whereas EE2 was only degraded in the the E2 produced by the reaction was then oxidized to E1 nitrifying tank. Only about 5% of the estrogens are sorbed (16). In some studies, concentrations of E1 and E2 or estrogen onto digested sewage sludge. It is very likely that activity increased after primary settling as compared to the conjugates (glucuronides and sulfates) of the estrogens raw influent (19-21), while Holbrook et al. (13) found nointermediate increase in steroid estrogen concentrations at were cleaved into the parent compounds mainly in the first five U.S. STPs. It was suggested (19) that the intermediate increase of these concentrations could be explained bycleavage of conjugated steroid estrogens in the primaryclarifier. This assumption is consistent with the findings of Introduction
Adler et al. (22) that on average 58% of total E1, 50% of total Desbrow, Routledge, and their co-workers (1, 2) have reported E2, and 26% of total EE2 were conjugated in raw sewage that the estrogenic effect on fish caused by sewage treatment plant (STP) effluents may in some cases be attributed to the Matsui et al. (20) recently performed a detailed profile of presence of the natural estrogens 17 -estradiol (E2) and estrogen removal in a Japanese STP using an immunoassay estrone (E1) as well as the active ingredient of most birth- for E2 in combination with the yeast estrogen screening (YES) control drugs, 17R-ethinylestradiol (EE2). Recent publications assay for measuring estrogen activity. The estrogenicity suggest that steroids may be the main source of estrogenicity measured by YES tended to decline during the treatment in many municipal STPs (3, 4). Since the sources of natural train, but the major reduction was found in the denitrification estrogens cannot be eliminated, specific treatment processes step, which was also the first step in the active sludge in STPs must be optimized. To date, it is known that municipal treatment. It was further observed that the E2 concentrations STPs reduce steroid estrogens to some extent, although and estrogen activity of the dewatering liquid from the sludge frequently not to levels lower than the known effective treatment were even more than twice as high as the inflowto the plant. The aim of the current paper was to investigate * Corresponding author telephone: +49 261 13065560; fax: +49 the fate of E1, E2, and EE2 due to sorption and degradation 261 1305363; e-mail:
in each treatment step of a municipal STP with nitrification, The Danish University of Pharmaceutical Sciences.
denitrification, and both biological and chemical phosphate § Bundesanstalt fu¨r Gewa¨sserkunde (BfG).
FIGURE 1. Flow scheme of the Municipal STP Wiesbaden with sampling locations
Experimental Section
acetate and the instrument standard Mirex was used as thequality parameter for the analysis. Furthermore, as sewage Estrogens in Water. Estrogens were analyzed in water
sludges vary considerably between different STPs, the according to the method reported by Ternes et al. (19). The suitability of the method was confirmed for each type of analytes were extracted from filtered water samples onto sludge (at each sampling location) by spiking 100 ng/g of the RP-C18 cartridges. Extracts were cleaned with a deactivated estrogens in an individual recovery experiment. The main silica gel column. The estrogens were trimethylsilylized before quality criterion was that the recovery was within the 95% analyzing with GC-ion trap-MS. As against the original confidence interval range found for the different types of method, however, the brand of the RP-C18 solid-phase sludge used in the original evaluation method.
material was changed to RP-C18 Bulk Sorbent from SepartisGmbH (Grenzach-Wyhlen, Germany). Furthermore, an ad- Flow Scheme of Plant and Wastewater Characterization.
ditional cleanup step based on gel permeation chromatog- The schematic of the municipal STP Wiesbaden is shown in raphy (GPC) was introduced to remove matrix interference Figure 1. The mechanical treatment consists of a screen, an from raw sewage extracts. Details of the GPC method and aerated grit-removal tank, and a primary clarifier. The primary evaluation of the GPC procedure are reported by Ternes et sludge collected in the primary clarifier is pre-thickened and then pumped into the mesophilic digester (33 °C, 20-d A 10-point calibration was performed over the whole retention time). The primary effluent is directed to the procedure after spiking groundwater with the respective activated sludge system for biological and chemical phos- estrogens at concentrations between 0.25 and 100 ng/L. In phate removal, denitrification, and nitrification. Fe(II)Cl2 is each analysis series, a blank sample of deep groundwater added in the first denitrification tank for efficient mixing in was run in parallel. According to the evaluation method the water before oxidation to Fe(III) and subsequent pre- originally described (19), the recovery of the steroid estrogens cipitation with phosphate in the aerated nitrification tanks.
After settling in the secondary clarifier, the activated sludge g93%, and the relative standard deviation (RSD) of the is returned to the inlet of the first denitrification tank. Internal e14%. A further quality parameter designed to ensure that matrix effects did not influence the extraction or recirculation supplies additional nitrate to the inlet of the cleanup, not mentioned in the original description (19), was first tank to improve denitrification. The secondary effluent the ratio between the surrogate standard, 17 -estradiol-17- is released to the river Rhine after its suspended solids had acetate, and the instrumental standard, Mirex (CAS Registry been reduced in a rotary sieve (not indicated). The activated No. 2385-85-5). The average of this ratio was determined as sludge system is operated with a solids retention time of a mean of all calibration samples. The quantitative result of 11-13 d, which is typical for a nitrifying plant with pre- a real sample was only considered valid if this ratio deviated denitrification. The excess sludge is dewatered to about 5% less than 30% from the average value of the calibrations. The total solids concentration in a rotary sieve before being newly included GPC cleanup step exhibited a systematic loss of 11%. This loss was effectively corrected by the surrogate The digested sludge is thickened and then treated thermophilically at 200 °C (not indicated) for sludge reduction Estrogens in Sludge. The method used for measuring
before being dewatered in a filter press. The sludge liquid estrogens in sludge was recently described in Ternes et al.
produced after thickening and dewatering is sent to the (23). Sludge was freeze-dried, and aliquots of 0.5 g were successively extracted twice with methanol and subsequently Several parameters (e.g., BOD5, COD, ammonium, nitrate, twice with acetone. For each extraction step, the slurry of the phosphate, and T) were measured regularly according to sample in solvent was ultrasonicated for 10 min. The four German DIN standards at selected points in the treatment solvent fractions were combined, and a cleanup was carried process. The nitrogen levels are of special interest for out with GPC and silica gel. The extracts were then derivatized comparison with other STPs, as the current study suggests and analyzed by GC-ion trap-MS. Standards for the a link between steroid estrogen elimination, nitrification, calibration curve and a blank for each analysis series were and denitrification. On November 13, the nitrogen concen- made by spiking the combined solvent mixture used for trations in the secondary effluent were 1.0 mg of NH4-N/L extraction followed by the full cleanup procedure described and 7.3 mg of NO3-N/L. The ranges during the preceding 2 for native samples. The 9-point calibration curve was weeks were 0.6-1.3 mg of NH4-N/L and 6.3-7.6 mg of NO3- performed with the respective estrogens at concentrations N/L, which illustrates well-functioning nitrification and between 1 and 200 ng/g. The recoveries of the analytes were denitrification. On the sampling days, the water temperatures g83% with an RSD of e19%. As in the water analysis described in the biological treatment units were 16-17 °C. The average above, the ratio of the surrogate standard 17 -estradiol-17 - for the 2-week period preceding the sampling campaign was 4022 9 ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 37, NO. 18, 2003
TABLE 1. Measured Concentration and Mass Flux of Estrone (E1), 17 -Estradiol (E2), and 17 -Ethinylestradiol (EE2) in the STP Wiesbadene
Total concentration including fraction sorbed on suspended solids. b Average of nitrification and excess sludge. c Average of inlet and primary sludge. d Assumed to be similar as in digestion. e Boldface type indicates measured data. The range of minimum to maximum is indicated in parentheses. Italic type indicates estimated data. Regular type indicates calculated data.
FIGURE 2. Measured mass flux of estrone (E1) and 17 -estradiol (E2) in g/d. Adler et al. (22) estimated the conjugated (glucuronide, sulfate)
estrogen quantities for a municipal STP inlet to be about 130% of the nonconjugated compounds. The estimated inlet load of 14 g/d
corresponds to about 45 µ
g/(p d).
17.7 °C with extremes of 14.8 and 19.9 °C. Furthermore, the sampling days was apparent. The average of the measured inlet, return sludge, internal recirculation, and sludge streams concentrations from each treatment step was therefore as well as the sludge-liquid recycle streams were recorded calculated and used for the mass flux analysis and the and used for calculating the loads of estrogens and the dilution effects in the first denitrification tank. The water Estrogens Sorbed onto Sludge. Allowing for the quantifica- inflow to the STP was 66 000 m3 on November 13, which is tion of analytes in native samples, LOQs were set as the second within the range seen in the preceding 2 weeks of 40 000- lowest calibration point within the linear correlation curve 110 000 m3. On November 13, the return sludge flow and equal to 1.5 ng/g. At this level the signal/noise ratio internal recirculation were about 50% and 200% of the inlet determined from the chromatogram exceeded 10 to ensure a precise quantification. Each sludge sample analyzed was Sampling. The sampling locations are shown in Figure 1.
spiked with 50 ng/g of each estrogen in parallel to confirm Sampling was generally carried out at the outlet of each that the recoveries were in the range found during the method treatment step. The sewage was not accessible for sampling validation. The recoveries of the spiked sludge were not before the grit removal tank. Water samples were taken as statistically different from that was seen in the original 24-h flow-proportional composite samples (cooled at 4 °C) method evaluation. As in the analysis of water samples, no from the outlet of the grit-removal tank, the primary and systematic difference could be detected in concentrations secondary sedimentations being collected from midnight to between the two days. The results were consequently midnight. All other sludge-liquid and sludge samples were taken randomly between 9 a.m. and 11 a.m. The steps in thewater treatment process were sampled on November 13 and Measured Concentrations and Mass Flux Analyses of
14, 2001, while the sludge treatment process was only sampled Estrogens. Wastewater Treatment. The measured concentra-
on November 13. The retention time of the sludge in the tions of the estrogens are shown in Table 1. Since E2 can be digester is about 20 d. The samples taken from the digester naturally oxidized to E1 (the reverse reaction could theoreti- do not therefore correspond directly to the analyzed inlet cally occur under anaerobic conditions), the combined sludge but rather to the average load of the previous 20 d.
concentrations of E1 and E2 were calculated. These combined In general, the total concentrations of suspended solids in values facilitate a comparison of their fate in the different the 24-h composite samples of the main water flow path treatment processes. The concentrations of the estrogens were low (<200 mg of TSS/L). Particles collected by filtering decreased with successive treatments through the STP.
these water samples were extracted in the same way as the The E1 and EE2 concentrations were reduced by 50% and sludge samples, and the extracts were combined with the 70%, respectively, in the first denitrification tank due mainly water extracts for a combined analysis of the total concen- to the dilution of the primary effluent by the return sludge tration. The estrogens were measured separately in sludge and the internal recirculation with low estrogen concentra- and water in samples taken from the activated sludge process.
tions. However, the E2 concentrations were comparable, The concentrations of suspended solids were quantified by which might be due to the cleavage of conjugated E2 by sludge bacteria and a reduction of E1 to E2. Comparing theloads (Figure 2), it is obvious that more nonconjugated E1 Results and Discussion
and E2 were discharged from the first reactor than the Performance of Analytical Methods and Limit of Quanti-
maximum quantity which had entered it, while the input fication (LOQ). Estrogens in the Water Phase. The LOQ was
and output of EE2 (Figure 3) were approximately equal. The calculated according to the German DIN 32645 (24) with a results underscored the assumption that conjugates (glu- confidence interval of 99% using the standard deviation of curonides, sulfates) of E1 and/or E2 not measured in the a linear regression curve. Since the calculated LOQ values inlet were cleaved. Another reason might be the strong daily were always between the first and second calibration points, variations of the natural estrogens in the inlet. The activated the LOQ used was set as the second lowest calibration point sludge samples are grab samples taken between 9 a.m. and of the linear correlation corresponding to 1 ng/L to ensure 11 a.m. during peak load (urine peak) whereas the primary and secondary effluents were 24-h flow-proportional samples.
The differences between the measured concentrations In the second denitrification tank and the following on the 2 d at each treatment step were similar to or less than aerated reactor, the natural estrogens are further reduced by the analytical variations found in the validation of the biological degradation so that a total of more than 98% is analytical method. No systematic difference between the two eliminated (Figure 2). Of particular interest is the high 4024 9 ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 37, NO. 18, 2003
FIGURE 3. Measured mass flux of 17r-ethinylestradiol (EE2) in g/d. Adler et al. (22) estimated the conjugated (glucuronide, sulfate) EE2
quantities for a municipal STP inlet to be about 35% of the nonconjugated EE2. The estimated inlet load of about 0.7 g/d yields 2.3 µ
d), which corresponds to the annual 50 kg of EE2 consumption in Germany.

elimination of both compounds under denitrifying condi- ng/L, respectively. Since the dissolved concentration of the digester liquid is similar to that of the inlet and the primary About 90% of the EE2 was eliminated (Figure 3), which effluent, we assume that the sorbed E1 and E2 concentration must be due mainly to aerobic biological degradation. In in the primary sludge (suspended solids separated in the contrast, the batch experiments with activated sludge from primary clarifier) is also in the same range as in the digested the old plant that removed only BOD did not exhibit more sludge. On this assumption, the detected inlet and outlet than minor reduction (16). The activated sludge system of loads of the digester are about the same (Figure 2 and Table the new upgraded nutrient-removal plant has a substantially 1), and we can assume that natural estrogens are not degraded longer sludge retention time (SRT ) 11-13 d) than the old appreciably under the methanogenic conditions in the one (SRT < 4 d), which might allow the growth of micro- digester. The sorbed concentrations of EE2 are either slightly above or below the LOQ, which only allows us to conclude The concentrations of sorbed estrogens appear to decrease that the sorbed load in the excess and digested sludge is slightly along the treatment train (Table 1). However, when lower than 6% of the inlet load (Figure 3 and Table 1).
considering the variations between the two days and the Recommendations for Treatment Plant Design and
analytical RSD up to 19%, no significant difference could be Further Investigations. Because the degradation kinetics of
found. Thus, the estrogen contamination of the activated E1 and E2 shown in the aerobic batch experiments of Ternes sludge in the tanks ranged from 7.8 to 13 ng/g for the sum et al. (16) are similar to first-order reactions, a reactor cascade of E1 and E2 and from less than 1.5 to 3 ng/g for EE2. Similar or plug-flow reactor is significantly more efficient than a results with respect to the elimination of EE2 in activated single-reactor system. In a single reactor, the degradation sludge systems were found by Busch et al. (25). The strong efficiency can be additionally decreased due to a hydraulic decrease of concentration from the first to the second reactor short circuit between the inlet and the outlet. In their profile despite the almost equal amounts of sorbed E1 and E2 in the of a Japanese STP, Matsui et al. (20) also found that activated sludge of the same sample (Table 1) indicates slow denitrification is an important treatment step for removing sorption kinetics and no equilibrium between the sorbed natural steroid estrogens. However, the oxidation products of E1 are still unknown. It can only be concluded that the The Wiesbaden STP was also investigated in 1997 (19).
estrogenicity is lost during denitrification because the YES Then, only partial removal of estrogens was detected. The assay response and that the estrogen concentrations de- STP effluent had average concentrations of 2 ng/L of EE2, 5 creased. Thus, anoxic and aerobic degradation of E1 and E2 ng/L of E2, and 24 ng/L of E1. The old activated sludge system will have to be further investigated in batch experiments consisted of a fully mixed reactor system with BOD removal.
with sludge from other nutrient-removal plants in the lower In the spring of 2001, the activated sludge system was enlarged and upgraded for all-year nitrification and denitrification EE2 was degraded significantly (about 90%) only after the (Figure 1). In June 2001, the estrogen concentrations in the Wiesbaden plant was upgraded from removing BOD to effluent decreased below the quantification limit of 1 ng/L removing nutrients with solid retention times of 11-13 d.
for the three major estrogens E1, E2, and EE2 with this Since the biodegradation of EE2 is not described in the literature, anoxic and aerobic degradation as well as anaerobic In August 2002, the estrogen concentrations were still transformation should be investigated in a full-scale nutrient- below the LOQ, whereas the internal recirculation is pumped removal plant as well as in batch tests to obtain a better into the second tank, making the first tank anaerobic and description of the elimination mechanisms and kinetics. Due inducing enhanced biological phosphate elimination. At this to the strong daily variation of ammonia originating from time, iron(II) chloride was added to the secondary clarifier urine, the daily variation of estrogens resulting from the peak in order to avoid disrupting the removal of biological urine load in the morning hours has to be considered in phosphate while still precipitating the remaining phosphate.
future experiments on full-scale plants.
Sludge Treatment. A clear increase of natural estrogen concentrations in the water and sludge phases was observed Acknowledgments
by comparing excess and digested sludge. The excess sludgeleaving the secondary clarifier exhibited only low estrogen This study was part of the EU Poseidon Project (EVK1-CT- concentrations. The dissolved E1 was found at 1.4 ng/L, 2000-00047), which was financially supported by grants whereas the other estrogens were below the LOQ. However, obtained from the EU Commission within the Energy, digester liquid from dewatering of digested sludge contained Environment and Sustainable Development Program of the much higher E2 and E1 concentrations with 5.4 and 67.1 fifth framework. We also thank the Danish University of VOL. 37, NO. 18, 2003 / ENVIRONMENTAL SCIENCE & TECHNOLOGY 9 4025
Pharmaceutical Sciences for additional financial support. We (12) Fuerhacker, M.; Durauer, A.; Jungbauer, A. Chemosphere 2001,
thank Ms. Kessler from STP Wiesbaden for her support during (13) Holbrook, R.; Novak, J.; Grizzard, T.; Love, N. Environ. Sci. Technol. 2002, 36, 4533-4539.
Note Added after ASAP
(14) Ternes, T. A.; Meisenheim, M.; McDowell, D.; Sacher, F.; Brauch, H.-J.; Haist-Gulde, B.; Preuss, G.; Wilme, U.; Zulei-Seibert, N.
This paper was released ASAP on 07/26/2003 with an incorrect Environ. Sci. Technol. 2002, 36, 3855-3863.
version of Table 1. The correct version was posted 08/05/ (15) Kamiya, T.; Yamauchi, T.; Hirotsuji, J.; Fujita, M. Removal of Main Endocrine Disruption Chemicals in Sewage Effluent byOzonation; IWA: Melbourne, 2002; e21649a.
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