ARTICLE

pubs.acs.org/est

Seasonal Variation in the Occurrence and Removal of Pharmaceuticals

and Personal Care Products in Different Biological Wastewater
Treatment Processes
Qian Sui, Jun Huang, Shubo Deng, Weiwei Chen, and Gang Yu*
School of Environment, THU
VEOLIA Joint Research Center for Advanced Environmental Technology, Tsinghua University, Beijing
100084, China

bS Supporting Information
ABSTRACT: The occurrence of 12 pharmaceuticals and personal care
products (PPCPs) in two wastewater treatment plants in Beijing was
studied monthly over the course of one year. The removal of PPCPs by
three biological treatment processes including conventional activated
sludge (CAS), biological nutrient removal (BNR), and membrane
bioreactor (MBR) was compared during different seasons. Seasonal
variations of PPCPs in the wastewater influent were discrepant, while
in the wastewater effluent, most PPCPs had lower concentrations in the
summer than in the winter. For the easily biodegradable PPCPs, the
performance of MBR was demonstrated to be more stable than CAS or
BNR especially during winter months. Diclofenac, trimethoprim, meto-
prolol, and gemfibrozil could be moderately removed by MBR, while
their removal by CAS and BNR was much lower or even negligible.
Nevertheless, no removal was achieved regardless of the season or the
treatment processes for the recalcitrant PPCPs. Studies on the contribu-
tion of each tank of the MBR process to the total removal of four
biodegradable PPCPs indicated the oxic tank was the most important
unit, whereas membrane filtration made a negligible contribution to their elimination.

’ INTRODUCTION
Pharmaceuticals and personal care products (PPCPs) have
received growing global attentions as emerging contaminants
threatening drinking water safety and aquatic organisms.1
3
Considering the pathways by which PPCPs enter into the water
environment, effluent from wastewater treatment plants (WWTPs)
has been identified as an important source.4 A great deal of work has
been done to monitor the concentration in both influent and
effluent of WWTPs in many countries, and to evaluate the removal
efficiency of wastewater treatment processes.5
9 These studies have
provided necessary fundamental data helpful to the process im-
provement for higher removal efficiency in terms of PPCPs.
However, most reported studies have been based on very short
monitoring periods with only one or two sampling campaigns,
which made it difficult to describe the occurrence of PPCPs over an
extended period of time. The most comprehensive study was done
by Loraine and Pettigrove, who sampled four drinking water
treatment plants and a wastewater reclamation plant in San Diego
during a period of ten months. The results revealed that the seasonal
variations of some PPCPs were considerable.4 Therefore it is
necessary to study the seasonal variations of both occurrence and
removal of PPCPs in various processes of WWTPs.
Compared to the conventional activated sludge (CAS) pro-
cess most widely adopted, the emerging membrane bioreactor
(MBR) process has shown its advantage in removing bulk organic
matter.10 Evaluations of MBR’s potential for PPCPs removal from
municipal wastewaters have been conducted.11
13 In some re-
ports, more complete elimination of PPCPs was observed by MBR
than CAS;12
14 while in other studies, MBR and CAS were
comparable in PPCPs removal.11,15 Most of these results were
based on studies conducted over a short period or several
discontinuous periods of time, and the incomprehensive evalua-
tions might be the reason for the conflict. The only exception is a
2-year continuous investigation done by Zuehlke, which con-
firmed that removal efficiencies of some PPCPs fluctuated and
were temperature-dependent.16 However, this study focused on
limited types of PPCPs, such as phenazone-type pharmaceuticals
and estrogenic steroids. In addition, in most investigations, only
the influent and effluent were sampled in the MBR based
processes,13,16 which prevented the assessment of individual tanks’
contributions in PPCP removal by the MBR process.
Therefore, the major objective of the present study was to gain
an insight into the seasonal variations in the occurrence and
Received: January 20, 2011
Accepted: March 9, 2011
Revised: March 2, 2011
Published: March 23, 2011

r 2011 American Chemical Society 3341 dx.doi.org/10.1021/es200248d | Environ. Sci. Technol. 2011, 45, 3341–3348
Environmental Science & Technology
Table 1. Operational Parameters of the Wastewater Treat-
ment Processes Investigated
WWTP A WWTP B
process CAS MBR BNR
capacity (  103 m3) 40 60 600
hydraulic retention time (h) 4.5
5.5 15.8
18.6 10.7
sludge retention time (d) 5 18
23 13
17
mixed liquor suspended solid (mg/L) 1.5
2.5 7.0
9.4 2.8
3.5
removal of PPCPs in two municipal WWTPs in Beijing. Special
emphasis was placed on the comparison of three biological
treatment processes, including a CAS and an MBR process in
parallel and a biological nutrient removal (BNR) process, over
the course of one year. A secondary objective was to understand
PPCPs removal contributions of each tank in the MBR-based
biological treatment process.
’ EXPERIMENTAL SECTION
Chemicals. Standards of 12 PPCPs, sulpiride (SP), N,N-
diethyl-meta-toluamide (DEET), caffeine (CF), chloramphe-
nicol (CP), trimethoprim (TP), diclofenac (DF), propranolol
(PPN), metoprolol (MTP), carbamazepine (CBZ), clofibric
acid (CA), bezafibrate (BF), gemfibrozil (GF) (Figure S1 in the
Supporting Information), as well as the internal standard (IS)
13
C-phenacetin and 3D-mecoprop, were purchased from Sig-
ma-Aldrich (Steinheim, Germany) and Dr. Ehrenstorfer
(Augsburg, Germany). These PPCPs were frequently detected
in the wastewaters of many countries,5
7 consumed in China,
and included in our previous studies regarding the analytical
method and preliminary survey.8,17 Methanol and formic acid
(Dikma, USA) were HPLC grade, and ultrapure water was
produced by a Milli-Q unit (Millipore, USA). Stock solutions of
individual compounds were prepared in methanol, and a
mixture standard solution was prepared by diluting the stock
solutions before each analytical run. All the solutions were
stored at 4 °C in the dark.
Sampling and Analysis. Two WWTPs in Beijing were
selected for investigation. WWTP A employs an MBR process
and a CAS process in parallel, which are fed with the same raw
wastewater. WWTP B employs a BNR process, with a config-
uration similar to the MBR in WWTP A: both utilize anaerobic,
anoxic, and oxic (A/A/O) tanks. All three processes operated
efficiently during our sampling. Schematic diagrams and detailed
information of these treatment processes are shown in Table 1
and Supporting Information 2.
Grab samples of wastewater influent and secondary effluent
were collected monthly for a whole year (Feb 2009
Jan 2010) at
fixed times (MBR effluent sample was not collected in March
2009 due to the maintenance of MBR). Although this sampling
strategy was limited by the lack of autosamplers, it was still
deemed acceptable, as the relative standard deviations (RSDs) of
the concentrations of most PPCPs in the grab and 2 h-composi-
tion samples did not exceed 30% in the influent and 15% in the
effluent (Supporting Information 3). In Nov 2009 and Jan 2010,
additional samples of the mixed liquor from the anaerobic tank,
anoxic tank, and oxic tank of MBR process were collected. All
samples were collected in duplicate (500 mL for influents and
1000 mL for the others) in prewashed amber glass bottles, kept in
3342
ARTICLE
a cooler, and transported to the laboratory. Immediately after
delivery to the laboratory, all influent and effluent samples were
filtered through prebaked (400 °C, >4 h) glass microfiber filters
(GF/F, Whatman). The mixed liquor samples were centrifuged
at 3000 rpm for 3 min first, and then the supernatant was
collected and filtered as described above. The PPCPs were
extracted and analyzed by the method reported before,8,17 and
briefly described in Supporting Information 4.
Quality Assurance and Quality Control (QA/QC). Strict QA/
QC was implemented to ensure the identification and accurate
quantification of the target PPCPs, as described previously.8,17
Median instrument, laboratory, and field blanks were all below
limit of quantification (LOQ), and only concentrations detected
three times above them were reported.18 As duplicate samples
were collected and analyzed, mean concentrations were adopted,
and the deviations of duplicate samples were less than 20%. For the
statistical analysis, the concentrations below LOQ were replaced
by 50% of the LOQ.19,20
’ RESULTS AND DISCUSSION
Occurrence in Overall. The concentrations and the detection
frequencies of PPCPs in all the wastewater influent and effluent
samples are present in Table 2. All the investigated PPCPs except
CA, CP, and PPN were found in every influent sample. CF
showed the highest contamination level, with a median concen-
tration of 5650 ng/L. DEET, DF, TP, SP, and MTP followed, of
which median concentrations were above 100 ng/L. For the
wastewater effluent samples, DF and TP were identified as the
predominant PPCPs, with concentrations of 35.3
463 ng/L and
6.6
772 ng/L, respectively; while BF, CA, CF, CP, GF, and PPN
had concentrations lower than 50 ng/L and low detection
frequencies (<100%). The concentration levels in the present
study were quite similar to the pilot survey conducted in the
summer of 2008, when four WWTPs including WWTP B were
investigated.8 In addition, a wider range of PPCP concentrations
was found in this study, which reflected the fluctuation of PPCP
concentrations during long-term monitoring.
Occurrence in Seasonal Variation. In the WWTP influents,
PPCPs showed discrepant seasonal variations, some of which can
be explained by the specific usage of PPCPs belonging to
different therapeutic classes. Antibiotic CP showed highest
concentrations in winter and lowest concentrations in summer
in the WWTP influents (Figure 1a). As CP is mainly used to cure
infections of the respiratory tract, which occur more frequently
during colder months, the consumption of CP is higher during
winter.21 Slightly higher concentrations of antilipidemic BF
during winter season than summer season were found, but the
differences were not significant (Figure 1b). It was reported that
concentration level of blood lipid in humans was greater in winter
than in summer,22 and the consumption of antilipidemic drugs in
China was found to be slightly higher in winter.23 Pronounced
higher concentration of DEET in the summer was observed
(Figure 1c), which might be due to more use of repellents in the
summer.4 MTP showed two concentration peaks in December/
January and July/August (Figure 1d). The concentration peak in
winter season was consistent with the fact that blood pressures
have been shown to be greater in winter,24 and thus an increased
dosage of antihypertensive would be expected. However, as
blood pressures were relatively lower in summer, the other
concentration peak of MTP in summer could not be explained.
dx.doi.org/10.1021/es200248d |Environ. Sci. Technol. 2011, 45, 3341–3348
Environmental Science & Technology ARTICLE

Table 2. Concentrations and Detection Frequencies of PPCPs in the Wastewater Influents and Effluents of CAS, BNR, and MBR
Processes Throughout the Year

influent (n = 24) effluent (n = 35)

concentration (ng/L) concentration (ng/L)

a
PPCPs max min mean median freq. (%) max min mean median freq.a (%)

BF 159 16.8 72.6 62.8 100 51.4 n.d.b 16.1 11.4 91

b
CA 56.2 n.d. 28.5 29.6 79 44.9 n.d.b 16.3 14.4 77
CBZ 233 34.3 76.3 70.7 100 277 47.7 88.2 70.6 100
CF 11400 4050 5860 5650 100 1020 n.d.b 108 4.6 66
CP 71.9 n.d.b 30.4 25.9 92 46.9 n.d.b 6.6 2.6 57
DEET 1520 124 464 327 100 235 21.6 99.7 101 100
DF 438 112 286 283 100 463 35.3 185 175 100
GF 359 44.8 116 99.7 100 326 n.d.b 66.9 34.3 77
MTP 159 58.4 103 103 100 268 34.3 105 98.7 100
PPN 3.3 n.d.b 1.7 n.d. 4 8.3 n.d.b 3.7 3.9 91
SP 301 64.9 126 121 100 262 70.7 135 120 100
TP 570 109 320 272 100 772 6.6 226 170 100
a
Freq. refers to frequency of detection. b n.d. refers to not detected, meaning the concentration is below LOQ.

For other PPCPs in the WWTP influents, no significant differ-
ences by season were observed.
Unlike the discrepancies in seasonal variation in the WWTP
influents, all PPCPs except DEET showed similar seasonal varia-
tion patterns in the WWTP effluents: lower levels in summer
season and higher levels in winter season. (Figure 1e
h).
The PPCP concentrations in the WWTP effluents could be
affected by several factors. For some PPCPs, such as CP and BF,
the time-dependent influent load made a contribution to this
seasonal variation in the effluent. But as shown in Figure 1(a
b,
e
f), the seasonal trend was more significant in the effluent than
in the influent, which should be caused by the higher removal
efficiencies in summer season.
Temperature is likely the most important factor for the better
removal and in consequence the lower concentrations in the
effluents. In winter season, temperatures in the oxic tanks of two
WWTPs were 10
14 °C, which was unfavorable for activated
sludge. In summer season, the temperatures increased to
25
27 °C, and biodegradation efficiency increased conse-
quently. Clara et al. found that the temperature was of elementary
importance for the removal of BF.11 It was also suggested that a
lower rate of biodegradation during the wintertime led to the less
effective elimination and higher concentration of PPCPs in the
effluents.16,25,26
Rainfall was found to affect the concentrations of PPCPs in the
effluent in some cases.5 Increased flow caused by rainfall on one
hand might dilute the PPCP concentrations, but on the other
hand could result in lower removal efficiency due to reduced
HRT in the WWTPs. However, the WWTPs in this study are
connected with a sewage system that is separated from the
stormwater collection system. Thus the effects of rainfall varia-
bility can be excluded as a main influencing factor.
Removal Comparison for Three Treatment Processes. The
removal of each PPCP except CA and CP by different treatment
processes is compared in Figure 2. The low detection frequency
of CA and CP made it difficult to generate statistically sound
results for individual WWTPs, and thus, they were excluded in
this section.
3343
Nearly no removal of CBZ and SP was observed regardless of the
process utilized; in some cases, even negative removal efficiencies
were obtained. These results were consistent with previous
studies.5,8,13 The transformation of the conjugated forms into
the free form by microorganisms as well as the grab sampling
strategy adopted in this study might be the reason for the apparent
negative removal efficiencies.13,27
Previous studies reported that MBR was neither superior for
recalcitrant compounds nor for well degradable compounds.28,29
However, in this study, for some well degradable compounds,
MBR exhibited more stable performance than CAS and BNR.
CF could be well biodegraded by all the three treatment
processes. However, lower removal rates were found by CAS
(96%) and BNR (79%) in January and February, while the
elimination by MBR maintained >99% during the whole year.
The removal efficiencies of BF were 70
100% by MBR,
55
100% by CAS, and 13
76% by BNR process (Figure 2),
which is consistent with ref 13. The removal of BF by MBR was
very stable, while a minor fluctuation in removal by CAS was
observed (Figure 3). The performance of BNR was tempera-
ture-dependent, as the BF removal efficiencies decreased from
>60% to <30% with the temperature. The robustness of MBR
could be due to the quicker response to variable influent
concentrations, operational perturbations,30 and less suscept-
ibility to ambient temperatures.
Some PPCPs, namely DF, MTP, TP, and GF, could be
moderately removed by MBR; while their removal by CAS and
BNR was much lower or even negligible. The median removal rate
of DF was 61% by MBR, 37% by CAS, and 21% by BNR, which is
consistent with the comparison between MBR and CAS by
Radjenovic et al.13 Significant seasonal variation of DF removal
by MBR was observed, ranging from >60% during May to
September to <40% during December to March. In comparison,
low removal efficiency (<40%) was observed by CAS and BNR
during the whole year. For the MTP, both CAS and BNR
processes showed no elimination, or sometimes negative removal
efficiencies; while the removal efficiency by MBR achieved >70%
in July and August. Similarly, better removal performance of TP
dx.doi.org/10.1021/es200248d |Environ. Sci. Technol. 2011, 45, 3341–3348
Environmental Science & Technology ARTICLE

Figure 1. Seasonal variation in the concentrations of some PPCPs in the wastewater influents (a
d) and effluents (e
h). The symbols represent the
mean concentration, and error bars represent the maximum and minimum concentration in CAS, MBR, and BNR processes.

was obtained by MBR (53
98%) than CAS (
53%
77%) and
BNR (
67
32%). GF was removed 96% by MBR, whereas the
median removal rates by CAS and BNR treatment were 52% and
4%, respectively. In a previous study, GF was found not removed
by CAS and slightly removed by MBR (30
40%, ref 13). Besides,
the performance of MBR was also very stable. In spite of January,
February, and May (60
72%), the removal efficiencies in other
months were maintained >90%. During CAS treatment, the same
high removal was achieved in July and August (96
99%). However,
it decreased dramatically with the decrease of temperature.
In summary, the higher biomass and the longer SRT could be
the reason for the better performances of MBR over CAS and
3344
BNR. Higher biomass in MBR led to a lower food to micro-
organisms (F/M) ratio. Under these conditions, the relative
shortage of biodegradable organic matter may force microor-
ganisms to metabolize more recalcitrant compounds.29,30
Longer SRT would allow the enrichment of slow-growing
bacteria and the establishment of a more diverse bacterial
population.12,31 The nature of microbial population has been
shown to have a significant impact on the biodegradation of
some PPCPs.31
Removal Contribution of MBR Tanks. To further study the
performance of MBR, concentrations of four biodegradable
PPCPs (BF, CF, DEET, and TP) in different tanks of MBR
dx.doi.org/10.1021/es200248d |Environ. Sci. Technol. 2011, 45, 3341–3348
Environmental Science & Technology ARTICLE

Figure 2. Comparison of the overall removal efficiencies by CAS, BNR, and MBR processes.

Figure 3. Seasonal variation in the removal efficiencies of PPCPs during the whole year: comparison among MBR and other two biological treatment
processes.

processes were analyzed twice to determine their removal tank (Figure S2), to exclude the concentration reduction due to
contributions. As a portion of the wastewater was recycled from dilution, the load based on the amount, rather than the concen-
the anoxic to the anaerobic tank and from the oxic to the anoxic tration, of PPCP was used to calculate the removal efficiency in
3345 dx.doi.org/10.1021/es200248d |Environ. Sci. Technol. 2011, 45, 3341–3348
Environmental Science & Technology
Figure 4. Removal efficiencies of PPCPs in each tank of A/A/O-MBR process: (a) BF, (b) CF, (c) DEET, (d) TP. *** means that the removal efficiency
of aerobic tank and membrane filtration could not be calculated because the CF concentrations were <LOQ after anoxic tank in the first sampling.
each tank (eq 1).
Min
Mout
Removal efficiency ¼  100% ð1Þ
Min
where Min and Mout are the amounts of individual PPCP entering
and leaving the investigated tank, respectively (mg/d).
As shown in Figure 4, the oxic tank appeared to be the most
important tank for PPCP biodegradation. The removals of BF
and CF in the oxic tank were >72% and 98%, respectively. In the
first trial, 54% of TP was removed in the oxic tank, while in the
second trial the removal was negligible. For DEET, lower but still
notable reduction (21
24%) was observed. The oxic tank was
also considered to be crucial for the biodegradation of some
PPCPs in previous studies.32 The first-order biodegradation rate
constant k1 of CF was found to be 0.38 h
1 under aerobic
conditions, much higher than those under anaerobic (0.05 h
1)
and anoxic conditions (0.08 h
1).32
The anaerobic tank showed different performances for each
PPCP. High removal efficiencies (57
78%) were observed for
CF. TP and DEET were moderately reduced (14
39%), while
less than 20% reduction of BF was achieved in the anaerobic tank.
The reduction after the anaerobic tank may be ascribed to the
rapid sludge-adsorption rate, which was confirmed by batch
experiments.32 The adsorption of PPCPs might occur despite the
redox conditions. When a full-scale anoxic
anaerobic
oxic pro-
cess was investigated, a significant decrease of sulfonamide anti-
biotics was also found in the first tank.33 Biodegradation by
microorganisms might be another influence on this phenomenon.
Some inorganic ions, such as Fe3þ, and various organic oxidative
compounds may have acted as electron acceptors.34 In addition,
3346
ARTICLE
some microorganisms, for instance the phosphate accumulating
organisms, might use PPCPs as carbon sources during the phos-
phorus release process, converting them into polyhydroxyalkanoates,
and then storing them in the cells in the anaerobic tank.32
The anoxic tank showed negative removal for all the 4 PPCPs.
The increased load in the anoxic tank might be explained by the
presence of PPCP conjugates. PPCPs can be excreted as un-
changed parent compounds or as conjugates of glucuronic and
sulphuric acid,33 so deconjugation during contact with activated
sludge may occur, leading to an increased PPCP load. Mean-
while, as most PPCPs are mainly excreted with bile and feces,
they could be enclosed in feces particles and released during
biological treatment,29 therefore leading to apparent concentra-
tion increases.14
It should be noted that because the concentrations of PPCPs
in the sludge were not determined, the contribution of sludge
adsorption could not be distinguished, and may lead to some
uncertainty when calculating aqueous phase removal.
Differences between the two trials in the removal of PPCPs
achieved by membrane filtration were observed. As the concentra-
tions of the biodegradable PPCPs were very low in the oxic tank, a
reasonable analytical error may lead to false apparent removal
efficiency by comparing the load before and after membrane
filtration. In fact, the contribution of membrane filtration was very
small compared to the total removal (Figure S4).
’ ASSOCIATED CONTENT
bS Supporting Information. This material is available free
of charge via the Internet at http://pubs.acs.org.
dx.doi.org/10.1021/es200248d |Environ. Sci. Technol. 2011, 45, 3341–3348
Environmental Science & Technology
’ AUTHOR INFORMATION
Corresponding Author
*Tel.: þ86 10 6278 7137; fax: þ86 10 62794006; e-mail:
yg-den@tsinghua.edu.cn.
’ ACKNOWLEDGMENT
This work was financially supported by the National Science
Fund for Distinguished Young Scholars (50625823). The assis-
tance provided by the operators of investigated WWTPs is also
appreciated.
’ REFERENCES
(1) Daughton, C. G.; Ternes, T. A. Pharmaceuticals and personal
care products in the environment: Agents of subtle change?. Environ.
Health Perspect. 1999, 107, 907–938.
(2) Snyder, S. A.; Westerhoff, P.; Yoon, Y.; Sedlak, D. L. Pharma-
ceuticals, personal care products, and endocrine disruptors in water:
Implications for the water industry. Environ. Eng. Sci. 2003, 20, 449–469.
(3) Fent, K.; Weston, A. A.; Caminada, D. Ecotoxicology of human
pharmaceuticals. Aquat. Toxicol. 2006, 76, 122–159.
(4) Loraine, G. A.; Pettigrove, M. E. Seasonal variations in concen-
trations of pharmaceuticals and personal care products in drinking water
and reclaimed wastewater in southern California. Environ. Sci. Technol.
2006, 40, 687–695.
(5) Ternes, T. A. Occurrence of drugs in German sewage treatment
plants and rivers. Water Res. 1998, 32, 3245–3260.
(6) Nakada, N.; Tanishima, T.; Shinohara, H.; Kiri, K.; Takada, H.
Pharmaceutical chemicals and endocrine disrupters in municipal waste-
water in Tokyo and their removal during activated sludge treatment.
Water Res. 2006, 40, 3297–3303.
(7) Kim, S. D.; Cho, J.; Kim, I. S.; Vanderford, B. J.; Snyder, S. A.
Occurrence and removal of pharmaceuticals and endocrine disruptors in
South Korean surface, drinking, and waste waters. Water Res. 2007,
41, 1013–1021.
(8) Sui, Q.; Huang, J.; Deng, S. B.; Yu, G.; Fan, Q. Occurrence and
removal of pharmaceuticals, caffeine and DEET in wastewater treatment
plants of Beijing, China. Water Res. 2010, 44, 417–426.
(9) Schultz, M. M.; Furlong, E. T.; Kolpin, D. W.; Werner, S. L.;
Schoenfuss, H. L.; Barber, L. B.; Blazer, V. S.; Norri, D. O.; Vajda, A. M.
Antidepressant pharmaceuticals in two US effluent-impacted streams:
Occurrence and fate in water and sediment, and selective uptake in fish
neural tissue. Environ. Sci. Technol. 2010, 44, 1918–1925.
(10) Melin, T.; Jefferson, B.; Bixio, D.; Thoeye, C.; De Wilde, W.; De
Koning, J.; van der Graaf, J.; Wintgens, T. Membrane bioreactor
technology for wastewater treatment and reuse. Desalination 2006,
187, 271–282.
(11) Clara, M.; Strenn, B.; Ausserleitner, M.; Kreuzinger, N. Com-
parison of the behavior of selected micropollutants in a membrane
bioreactor and a conventional wastewater treatment plant. Water Sci.
Technol. 2004, 50, 29–36.
(12) Kimura, K.; Hara, H.; Watanabe, Y. Elimination of selected
acidic pharmaceuticals from municipal wastewater by an activated sludge
system and membrane bioreactors. Environ. Sci. Technol. 2007,
41, 3708–3714.
(13) Radjenovic, J.; Petrovic, M.; Barcelo, D. Fate and distribution of
pharmaceuticals in wastewater and sewage sludge of the conventional
activated sludge (CAS) and advanced membrane bioreactor (MBR)
treatment. Water Res. 2009, 43, 831–841.
(14) Gobel, A.; McArdell, C. S.; Joss, A.; Siegrist, H.; Giger, W. Fate
of sulfonamides, macrolides, and trimethoprim in different wastewater
treatment technologies. Sci. Total Environ. 2007, 372, 361–371.
(15) Smook, T. M.; Zho, H.; Zytner, R. G. Removal of ibuprofen
from wastewater: Comparing biodegradation in conventional,
3347
ARTICLE
membrane bioreactor, and biological nutrient removal treatment sys-
tem. Water Sci. Technol. 2008, 57, 1–8.
(16) Zuehlke, S.; Duennbier, U.; Lesjean, B.; Gnirss, R.; Buisson, H.
Long-term comparison of trace organics removal performances between
conventional and membrane activated sludge processes. Water Environ.
Res. 2006, 78, 2480–2486.
(17) Sui, Q.; Huang, J.; Deng, S. B.; Yu, G. Rapid determination of
pharmaceuticals from multiple therapeutic classes in wastewater by
solid-phase extraction and ultra-performance liquid chromatography
tandem mass spectrometry. Chin. Sci. Bull. 2009, 54, 4633–4643.
(18) Watkinson, A. J.; Murby, E. J.; Costanzo, S. D. Removal of
antibiotics in conventional and advanced wastewater treatment: Im-
plications for environmental discharge and wastewater recycling. Water
Res. 2007, 41, 4164–4176.
(19) Glelt, A. Estimation for small normal data sets with detection
limits. Environ. Sci. Technol. 1985, 19, 1201–1208.
(20) Reemtsma, T.; Weiss, S.; Mueller, J.; Petrovic, M.; Gonzalez, S.;
Barcelo, D.; Ventura, F.; Knepper, T. P. Polar pollutants entry into the
water cycle by municipal wastewater: A European perspective. Environ.
Sci. Technol. 2006, 40, 5451–5458.
(21) Davey, P.; Ferech, M.; Ansari, F.; Muller, A.; Goossens, H.
Outpatient antibiotic use in the four administrations of the UK: cross-
sectional and longitudinal analysis. J. Antimicrob. Chemother. 2008,
62, 1441–1447.
(22) Ockene, I. S.; Chiriboga, D. E.; Stanek, E. J., 3rd; Harmatz,
M. G.; Nicolosi, R.; Saperia, G.; Well, A. D.; Freedson, P.; Merriam, P. A.;
Reed, G.; Ma, Y.; Matthews, C. E.; Hebert, J. R. Seasonal variation in
serum cholesterol levels: Treatment implications and possible mechan-
isms. Arch. Intern. Med. 2004, 164, 863–870.
(23) Marketing Research Report on Antilipidemic in 2005; China
Medicine Economic Information Net (CMEIN): Guangzhou, China,
2005.
(24) Brennan, P. J.; Greenberg, G.; Miall, W. E.; Thompson, S. G.
Seasonal variation in arterial blood pressure. Br. Med. J. (Clin. Res. Ed.)
1982, 285, 919–923.
(25) Vieno, N. M.; Tuhkanen, T.; Kronberg, L. Seasonal variation in
the occurrence of pharmaceuticals in effluents from a sewage treatment
plant and in the recipient water. Environ. Sci. Technol. 2005,
39, 8220–8226.
(26) Castiglioni, S.; Bagnati, R.; Fanelli, R.; Pomati, F.; Calamari, D.;
Zuccato, E. Removal of pharmaceuticals in sewage treatment plants in
Italy. Environ. Sci. Technol. 2006, 40, 357–363.
(27) Vieno, N.; Tuhkanen, T.; Kronberg, L. Elimination of pharma-
ceuticals in sewage treatment plants in Finland. Water Res. 2007,
41, 1001–1012.
(28) Weiss, S.; Reemtsma, T. Membrane bioreactors for municipal
wastewater treatment
A viable option to reduce the amount of polar
pollutants discharged into surface waters?. Water Res. 2008,
42, 3837–3747.
(29) Sipma, J.; Osuna, B.; Collado, N.; Monclus, H.; Giuliana, F.;
Comas, J.; Rodriguez-Roda, I. Comparison of removal of pharmaceu-
ticals in MBR and activated sludge system. Desalination 2010,
250, 653–569.
(30) De Wever, H.; Weiss, S.; Reemtsma, T.; Vereecken, J.; Muller,
J.; Knepper, T.; Roden, O.; Gonzalez, S.; Barcelo, D.; Hernando, M. D.
Comparison of sulfonated and other micropolluants removal in mem-
brane bioreactor and conventional wastewater treatment. Water Res.
2007, 41, 935–945.
(31) Petrovic, M.; de Alda, M. J. L.; Diaz-Cruz, S.; Postigo, C.;
Radjenovic, J.; Gros, M.; Barcelo, D. Fate and removal of pharmaceu-
ticals and illicit drugs in conventional and membrane bioreactor waste-
water treatment plants and by riverbank filtration. Philos. Trans. R. Soc.
London, Ser. A. 2009, 367, 3979–4003.
(32) Xue, W. C.; Wu, C. Y.; Xiao, K.; Huang, X.; Zhou, H. D.; Tsuno,
H.; Tanaka, H. Elimination and fate of selected micro-organic pollutants
in a full-scale anaerobic/anoxic/aerobic process combined with mem-
brane bioreactor for municipal wastewater reclamation. Water Res. 2010,
44, 5999–6010.
dx.doi.org/10.1021/es200248d |Environ. Sci. Technol. 2011, 45, 3341–3348
Environmental Science & Technology ARTICLE

(33) Chang, H.; Hu, J. Y.; Wang, L. Z.; Shao, B. Occurrence of

sulfonamide antibiotics in sewage treatment plants. Chin. Sci. Bull. 2008,
53, 514–520.
(34) Joss, A.; Andersen, H.; Ternes, T.; Richle, P. R.; Siegrist, H.
Removal of estrogens in municipal wastewater treatment under aerobic
and anaerobic conditions: Consequences for plant optimization. Envir-
on. Sci. Technol. 2004, 38, 3047–3055.

3348 dx.doi.org/10.1021/es200248d |Environ. Sci. Technol. 2011, 45, 3341–3348