Research 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): dCCE2 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: ternes@bafg.de.
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).
VOL. 37, NO. 18, 2003 / ENVIRONMENTAL SCIENCE & TECHNOLOGY 9 4021 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 µg/(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 µg/(p 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
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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/
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Lessons Along the Path of Most Resistance WHAT FUNDERS SHOULD KNOW ABOUT THE KEEP ANTIBIOTICS WORKING COALITION In less than four years, an unusual mix of foundations and nonprofits has placed a little-known issue on the map, convinced a giant industry to begin changing its practices, and taken great strides towards protecting public health. The coalition’s story is still being w
TA no.79 DSC Measurement of Pharmaceuticals 2007.9 - Crystal polymorphism and crystallinity - In this brief, we measure Carbamazepine, an an-Differential scanning calorimetry (DSC) has been tiepileptic drug, and ursodeoxycholic acid, a chol-added as a general testing method to the Japanese eretic drug, to ascertain the differences of crystal Pharmacopoeia and is widely used to e