Removal of pharmaceutical compounds in tropical constructed wetlands

Ecological Engineering 37 (2011) 460–464

Contents lists available at ScienceDirect

Ecological Engineering journal homepage: www.elsevier.com/locate/ecoleng

Removal of pharmaceutical compounds in tropical constructed wetlands Dong Qing Zhang a,∗ , Soon Keat Tan b , Richard M. Gersberg c , Sara Sadreddini a , Junfei Zhu a , Nguyen Anh Tuan a a

DHI-NTU Centre, Nanyang Environment & Water Research Institute, Nanyang Technological University, N1.2-B1-02, 50 Nanyang Avenue, Singapore 639798, Singapore Maritime Research Centre, School of Civil and Environmental Engineering, Nanyang Technological University, N1-B1a-03, 50 Nanyang Avenue, Singapore 639798, Singapore c Graduate School of Public Health, San Diego State University, Hardy Tower 119, 5500 Campanile, San Diego, CA 92182-4162, USA b

a r t i c l e

i n f o

Article history: Received 23 August 2010 Received in revised form 26 October 2010 Accepted 7 November 2010 Available online 26 January 2011 Keywords: Constructed wetlands Pharmaceutical Removal Tropical region

a b s t r a c t The ability of tropical horizontal subsurface constructed wetlands (HSSF CWs) planted with Typha angustifolia to remove four widely used pharmaceutical compounds (carbamazepine, declofenac, ibuprofen and naproxen) at the relatively short hydraulic residence time of 2–4 days was documented. For both ibuprofen and naproxen, pharmaceutical compounds with low Dow values, the planted beds showed significant (p < 0.05) enhancement of removal efficiencies (80% and 91%, respectively, at the 4 day HRT), compared to unplanted beds (60% and 52%, respectively). The presence of plants resulted in the removal of these pharmaceutical compounds from artificial wastewater. The more oxidizing environment in the rhizosphere might have played an important role, but other rhizosphere effects, beside rhizosphere aeration, appeared to be important also. Carbamazepine, considered one of the most recalcitrant pharmaceuticals, and declofenac showed low removal efficiencies in our CW, and this is attributable to their higher hydrophobicity. The fact that the removal of these compounds could be explained by the sorption onto the available organic surfaces, explains why there was no significant difference (p > 0.05) in their removal efficiencies between planted as compared to unplanted beds. No statistical significant differences (p > 0.05) were observed for the removal efficiencies of any of the pharmaceuticals tested for the 2-day HRT as compared to that corresponding to 4-day HRT. The rather efficient removal shown by the wetlands in this study (with HRTs of 2–4 days), indicates that such a CW system may be more practically used (with less land requirements) in tropical regions for removing conventional pollutants and certain pharmaceutical compounds from wastewater effluents. © 2010 Elsevier B.V. All rights reserved.

1. Introduction Many pharmaceutical compounds are now considered as emerging contaminants of environmental concern because of their widespread use, continuous release, persistence, and increasing evidence for their ecotoxicological (if not human health) effects (Buser et al., 1999). Since some pharmaceutical compounds are not completely removed by conventional wastewater treatment, they are ubiquitous and persistent pollutants in receiving waters worldwide, especially where municipal wastewaters are discharged into waterways (Ellis, 2006). In certain urban centers, water concerns and supply issues have led to increasing attention on rainwater capture and indirect reuse of treated sewage discharge for augmentation of reservoirs, in order to increase potable water supplies. However, under these conditions, the potential for introduction of pharmaceuticals into

∗ Corresponding author. Tel.: +65 8165 6212; fax: +65 6790 6620. E-mail address: [email protected] (D.Q. Zhang). 0925-8574/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.ecoleng.2010.11.002

the drinking supply is of concern. Technologies do exist which can lower the level of pharmaceuticals discharged into receiving waters, e.g., ozonation, reverse osmosis, and advanced oxidation processes (Ternes et al., 2003). However, such treatment is extremely expensive (Heberer, 2002; Daughton and Ternes, 1999), and therefore the use of constructed wetlands (CWs) is growing in popularity as a low impact and economical alternative for purifying contaminated waters. Wetland ecosystems contain a rich biological diversity and contribute great benefits to society by recharging aquifers, retaining sediments and nutrients, controlling flood flows, and stabilizing the microclimate (Mitsch et al., 2008). Interest in wetland construction has been stimulated by the appreciation of the function and the values of wetland systems, especially their abilities to cleanse polluted water and provide habitat for a diversity of wildlife (Mitsch and Gosselink, 2007; Mitsch, 1995). Removal of contaminants in CWs occurs through a series of complex physical, chemical and microbial interactions (Gersberg et al., 1986; Kadlec and Knight, 1996), and involves a variety of processes including biodegradation, sorption to bed media, sedimentation, microbial and plant uptake,

D.Q. Zhang et al. / Ecological Engineering 37 (2011) 460–464

Fig. 1. Layout of the horizontal subsurface flow constructed wetland (HFCW).

physical interaction with organic matter and volatilization (Brix, 1993; Kadlec and Knight, 1996; Vymazal and Kröpfelová, 2008; Matamoros and Bayona, 2007). The complexity of such processes makes it difficult to ascertain the primary removal mechanism for each class of contaminants. While there has been extensive research on CWs for removal of organic matter (Mitsch et al., 2005; Vymazal, 2005; Kadlek et al., 2000), relatively little work has been conducted to evaluate pharmaceutical removal efficiencies (Llorens et al., 2009) in engineered low impact systems such as CWs (Matamoros et al., 2005; Park et al., 2009; Matamoros and Bayona, 2006). In this paper, we focus on the removal efficiency of four pharmaceuticals: carbamazepine, diclofenac, ibuprofen and naproxen, in a batch loaded subsurface flow CWs in a tropical environment. These pharmaceuticals were chosen because they are widely used, and reported as present in the effluents of wastewater treatment plant (WWTP) effluents. The objectives of this study were to (i) compare the removal efficiency of selected pharmaceuticals in batch loaded subsurface flow CWs planted with Typha angustifolia and unplanted beds (sand filters), (ii) compare the removal efficiency of selected pharmaceuticals at relatively low hydraulic residence time (2 and 4 days), and (iii) determine the quantitative role that the aquatic plant plays in removal of the selected pharmaceuticals in a tropical CW. 2. Materials and methods Six wetland microcosmos were set up at the campus of Nanyang Technological University. The location is a typical tropical environment and is generally hot and humid year round. The average temperature ranges from 23 ◦ C to 32 ◦ C. There is no distinct wet/dry season and most rainfall occurs during the northeast monsoon (November–January) when the rainfalls are usually sudden and heavy. Fig. 1 shows the layout of the HSSF CW. The beds were fabricated with fiber glass (120 cm long, 60 cm wide and 60 cm deep). The gravel layer (diameter of 4–10 mm, D60 = 3.5 mm and porosity of 45%) was 0.3 m deep and the water level was kept 0.05 m below the gravel surface to give a water depth of 0.25 m. The porosity was

461

0.45. The emergent macrophyte, T. angustifolia, with 3-year maturity before purchase was established in the three HSSF CWs, and plants achieved a uniform density of approximately 14 plants/m2 . Three beds without plants were used as “unplanted” control beds. All the containers had a drainage pipe (0.4 m long and 50 mm in diameter) located on the flat bottom for effluent discharge. A standpipe on the outside of the container was used to maintain the water level at 5 cm below the gravel surface. Batch-load HSSF CWs and SFs were fed with synthetic wastewater with the same organic load and operated for 4 weeks before experimental data were collected. Hydraulic retention times (HRTs) were 2 and 4 days. Experiments started in April 2010 and lasted 2 months. The composition of influent was: 300 mg l−1 COD, 27 mg l−1 NH4 –N, 7 mg l−1 PO4 –P, and 4 mg l−1 Fe, 7 mg l−1 Mg, and 6 mg l−1 Ca. General parameters monitored were COD, ammonia–N (NH4 –N), nitrate (NO3 –N) and total phosphorus (TP), all in accordance with conventional methods (Standard Methods for Examination of Water and Wastewater – APHA, 1989). Carbamazepine, declofenac, ibuprofen, and naproxen (97–100% purity) were obtained from Sigma–Aldrich. The cartridges for solid phase extraction (SPE) were GracePureTM C18 – Max SPE columns. The 0.45 ␮m glass fiber filters of 47 mm (Whatman) were purchased from Schleicher & Schuell (Germany). Standard stock solution of 500 ␮g/ml was prepared in methanol and stored at 4 ◦ C. With respect to the pharmaceutical injection, 50 l of synthetic wastewater was spiked with 1.25 mg of each pharmaceutical compound to obtain a final concentration of 25 ␮g l−1 . Prior to extraction, 500 ml of effluent wastewater was filtered through a 0.45 ␮m glass fiber membrane filter (Millipore, USA) and then acidified to pH 2 with hydrochloric acid. The SPE cartridges were conditioned using 5 ml n-hexane, 5 ml ethyl acetate, 10 ml methanol and 10 ml of Milli-Q water (pH 2) at a flow-rate of approximately 3 ml/min. Samples were percolated to the SPE cartridges through a Teflon tube at a flow-rate of approximately 10 ml/min. The cartridge filter was then rinsed with methanol:Milli-Q water (pH 2) = 10:90, followed by 20 ml of Milli-Q water (pH 2). Thereafter the cartridges were allowed to dry for 30 min and then eluted with 5 ml ethyl acetate with elution solutions collected in 15 ml calibrated centrifuge tubes. The extracted solution was then concentrated to ca. 400 ␮l under a gentle nitrogen stream and was then reconstituted to 500 ␮l with methanol. Chromatographic analysis was performed on a Shimadzu Ultra Fast Liquid Chromatograph (UFLC) (Shimadzu, Japan) equipped with a quaternary LC-20AD pump, a CTO-20A oven, and a SPDM20A Diode Array Detector (DAD). The injector was SIL-20A HT fitted to a Shimadzu autosampler with a 20 ␮l sample loop. Chromatographic separation was carried out using an Inertsil ODS-3 column (4.6 mm × 150 mm, 5 ␮m) (Alpha Analytical). Chromatograms were processed using a “Shimadzu LCSolution program”. 3. Results Table 1 shows the basic water quality parameters of the wetland effluent in the planted and unplanted beds, respectively. There

Table 1 Basic physical and chemical parameters of effluent in the planted and unplanted beds. HRT 2-Day Planted Unplanted 4-day Planted Unplanted

Temperature (◦ C)

pH

DO (mg l−1 )

Conductivity (S m−1 )

TOC (mg l−1 )

25.8 ± 1.3 26.0 ± 1.0

6.5 ± 0.3 6.9 ± 0.2

3.7 ± 2.2 4.5 ± 1.6

402 ± 73.8 552 ± 96.3

3.9 ± 1.1 5.6 ± 3.4

26.0 ± 0.8 25.8 ± 0.5

6.6 ± 0.1 6.5 ± 0.3

3.3 ± 0.6 2.9 ± 0.9

415 ± 37.8 398 ± 74.9

3.2 ± 1.4 5.0 ± 2.7

462

D.Q. Zhang et al. / Ecological Engineering 37 (2011) 460–464

Table 2 Removal of COD, NH4 –N, TN and TP at 2-day and 4-day retention times in the planted and unplanted beds. HRT

COD (mg l−1 )

NH4 (mg l−1 )

NO3 (mg l−1 )

TP (mg l−1 )

Inflow Outflow 2-Day Planted Removal (%) Unplanted Removal (%) 4-Day Planted Removal (%) Unplanted Removal (%)

294

27.36

–

22

21.7 ± 14.3 92.6 30.5 ± 21.2 89.6

1.7 ± 0.9 93.7 11.5 ± 4.6 57.9

0.3 ± 0.2 – 0.3 ± 0.2 –

9.2 ± 3.2 58.0 13.9 ± 4.8 37.0

12.4 ± 12.2 95.8 20.8 ± 15.6 92.9

1.3 ± 1.1 95.3 10.9 ± 3.0 60.3

0.2 ± 0.1 – 0.2 ± 0.1 –

6.7 ± 2.3 69.6 12.1 ± 3.4 41.2

were no significant differences for DO, pH, temperature, conductivity, and TOC between treatments (planted vs unplanted beds) or as a function of hydraulic retention time (HRT). Table 2 shows the removal of COD, NH4 –N, and TP at the 2day and 4-day HRTs. Removal efficiencies for all parameters were good, even at the 2-day HRT, with removals of 92.6% (planted) and 89.6% (unplanted) for COD, 93.7% (planted) and 57.9% (unplanted) for NH4 , and 58.0% (planted) and 37.0% (unplanted) for TP at the 2-day HRT. Removal efficiencies for these same parameters were marginally higher at the 4-day HRT. There was no significant difference for COD and TP at either 2-day HRT or 4-day HRT (p > 0.05). There was also no significant difference when the effluent values for COD and TP in the planted beds were compared to unplanted beds. On the other hand, NH4 –N removal was significantly enhanced (p < 0.05) in the planted beds, compared to the unplanted beds. Removal efficiencies were 93.7% (2-day HRT) and 95.3% (4-day HRT) for NH4 in the planted beds, compared to 57.9% (2-day HRT) and 60.3% (4-day HRT) for NH4 in the unplanted beds. The removal efficiencies of pharmaceutical compounds in the planted and unplanted beds at both the 2-day and 4-day HRTs are shown in Table 3. The removal efficiency of ibuprofen in our experiment was higher in the planted beds (71.0% for 2-day HRT and 79.7% for 4-day HRT) than that for the unplanted beds (56.7% for 2day HRT and 60.0% for 4-day HRT) (Table 3), but the enhancement by plants was only significant (p < 0.05) at the 4-day HRT.

A significant difference (p < 0.05) was observed for naproxen removal efficiency between the planted HSSF beds (82.8% for 2day HRT and 91.3% for 4-day HRT) and the unplanted beds (49.5% for 2-day HRT and 51.8% for 4-day HRT) at both HRTs (Table 3). As for carbamazepine, no significant differences in carbamazepine removal efficiency between planted beds (28.4% for 2-day HRT and 26.7% for 4-day HRT) and unplanted beds (28.8% for 2-day and 28.3% for 4-day HRT) were observed in our study (Table 3). Another pharmaceutical compound, diclofenac, has also been reported as a recalcitrant compound in microcosm experiments, membrane bioreactor systems, and activated sludge STP (Heberer, 2002; Beausse, 2004; Quintana et al., 2005), and in our study the removal efficiency of diclofenac in the planted beds ranged from 47.5 to 55.4%, compared to that of unplanted bed of 41.1–46.7% (Table 3). Based on the findings of our study, we found that CWs in a tropical environment could exhibit relatively good treatment performance (93% for COD, 92% for NH4 , and 58% for TP) for the traditional parameters at HRTs as low as 2 days. Both naproxen and ibuprofen were removed with high efficiency at HRT of 4 days (91.3% and 79.7%, respectively) as well as an HRT of 2 days (82.8% and 71.0%). Similarly, although in a lower range of removal efficiencies, there were no significant differences (p > 0.05) between the 2-day HRT and 4-day HRT for carbamazepine (planted beds: 28.4% vs 26.7%; unplanted beds: 28.8% vs 28.3%) and diclofenac (planted beds: 47.5% vs 55.4%; unplanted beds: 46.7% vs 41.1%).

4. Discussion For the conventional parameters, our findings showed no significant differences when the effluent values for COD and TP in the planted beds were compared to the unplanted beds. On the other hand, NH4 –N removal was significantly (p < 0.05) enhanced in the planted beds, compared to the unplanted beds. Removal efficiencies were 93.7% (2-day HRT) and 95.3% (4-day HRT) for NH4 in the planted beds, compared to 57.9% (2-day HRT) and 60.3% (4day HRT) for NH4 in the unplanted beds. These results are in good agreement with Jing et al. (2008), who found that at the HRTs of 2–4 days, a tropical CW system in southern Taiwan maintained greater than 72%, 80% and 46% removal for COD, NH4 , and TP,

Table 3 Mean levels of pharmaceutical compounds, and their removal efficiencies in the CWs.

2-Day HRT Planted Removal (%) Unplanted Removal (%) 4-Day HRT Planted Removal (%) Unplanted beds Removal (%) Other removal (%) SFa HSSFCWb HSSFCWd VSSFCWa WWTP a b c d e f *

Carbamazepine (␮g l−1 )

Naproxen (␮g l−1 )

Diclofenac (␮g l−1 )

Ibuprofen (␮g l−1 )

17.9 ± 2.5 28.4 ± 10.3 17.8 ± 2.8 28.8 ± 11.3

4.3 ± 1.8 82.8 ± 7.1* 13.1 ± 3.7 49.5 ± 13.0*

12.8 ± 2.8 47.5 ± 8.1 14.2 ± 3.8 46.7 ± 12.3

7.3 ± 3.4 71.0 ± 15.5 11.9 ± 6.6 56.6 ± 24.6

17.0 ± 4.7 26.7 ± 7.0 17.9 ± 2.0 28.3 ± 8.1

2.6 ± 2.4 91.3 ± 5.7* 12.0 ± 4.2 52.0 ± 17.3*

11.3 ± 2.8 55.4 ± 11.1* 14.6 ± 2.8 41.1 ± 11.3*

4.3 ± 2.1 79.7 ± 11.1* 10.1 ± 5.7 59.8 ± 22.7*

8–11 16c 16 20–26 8e /7f

66–80 0–47 80–90 62–89 40–55c /66f

39–76 0–11 0–45 53–73 9–75f /17e

49–90 17–52 62–80 55–99 60–70c /90f

Matamoros et al. (2007). Matamoros and Bayona (2006): sand depth 0.5 m. Garballa et al. (2004). Matamoros and Bayona (2006): sand depth 0.27 m. Heberer (2002). Daughton and Ternes (1999). Statistically significant differences at a significance level of <0.05 (planted vs unplanted beds).

D.Q. Zhang et al. / Ecological Engineering 37 (2011) 460–464

respectively. In the same report and for planted beds, mean ammonium removal efficiencies were 91% over the period of the study, while in the unplanted beds, the removal efficiencies were much lower, at less than 35%. These authors concluded that the efficient removals of these constituents obtained with HRTs between 2 and 4 days indicated the possibility of using a CW system for wastewater treatment with less footprint requirements, and our results confirm this finding. In the present study, ibuprofen and naproxen, both pharmaceutical compounds with low Dow values, which is the overall octanol–water partition coefficient of a mixture of related chemical species (Turner and Williamson, 2005), showed significantly (p < 0.05) higher removal efficiencies in the planted beds, compared to the unplanted beds. This finding is also consistent with other research, which indicated that the removal efficiency in a planted HSSF system (with sand depth of 0.27 m) ranged from 71 to 80% for ibuprofen and 80 to 90% for naproxen (Matamoros and Bayona, 2006), but was only 49–90% for ibuprofen and 66–80% for naproxen in unplanted beds (Matamoros et al., 2007). This may be well attributed to the rhizosphere effect, since it has been extensively shown that rhizosphere aeration plays an important role part in the establishment of an oxidizing environment to support high microbial activity (Reddy et al., 1989; Brix, 1994; Gersberg et al., 1983). However, surprisingly, levels of DO, COD and TOC in the planted beds compared to those in the unplanted beds were found to be not statistically different (p > 0.05), indicative of some rhizosphere effect aside from rhizosphere aeration alone, as playing a significant role in the efficient pharmaceutical removal in tropical CWs we observed. The relatively efficient removal value for ibuprofen and naproxen observed in planted beds was also reported by HijosaValsero et al. (2010b). These authors also indicated that ibuprofen does not to bind significantly to organic matter retained in the gravel beds or pond sediment, and an HFCW planted with T. latifolia played a significant role in the removal of ibuprofen. This was attributed to the effect of active plant take-up. It is also known that plants considerably increase the amount of aerobic/anaerobic interface present in the soil, and as the surface water flows through the plant stands, the stems and associated biofilms can potentially remove and degrade a number of compounds (Brix, 1997). Also, the stems of the plants provide a substrate for colonization of biofilms, which have been shown in the lab studies to be effective in removing some pharmaceutical compounds (White et al., 2006). Herklotz et al. (2010) also demonstrated that selected pharmaceuticals commonly present in treated wastewater can be actively taken up by various species of plants. In addition, root exudates released by the plant in the rhizosphere, are known to result in intense microbial activity in the vicinity of roots (Brimecombe et al., 2001). The establishment of large numbers of metabolically active populations of soil microbes in the rhizosphere is certainly important (Brix, 1997; Veen et al., 1997; Dunbabin et al., 1988), as the microbial population found in the soil is associated with the plant roots, can reach up to 109 –1012 per gram of soil (Whipps, 1990). The possibility that root exudates also may play a role in induction of specific metabolic activities conferring the ability to degrade certain pharmaceuticals, or increase bioavailability of pharmaceuticals by acting as surfactants or transporters, should not be overlooked. Carbamazepine is considered to be one of the most recalcitrant pharmaceuticals and the removal behavior of such compounds is completely different from the others above. The recalcitrant nature of this substance has also been previously reported at other WWTPS (Ternes et al., 2007; Bendz et al., 2005; Hijosa-Valsero et al., 2010a). Its low removal efficiency can be attributed to its higher hydrophobicity, and the major fraction of removal of this compound could be explained by the sorption onto the available organic

463

surfaces (Matamoros et al., 2005, 2008a). Surprisingly, comparing with other unplanted beds, HSSF CWs, VSSF CWs, or even WWTPs, the removal efficiencies of cabamazepine in our study show much better outcome. However, Hijosa-Valsero et al. (2010b) reported that carbamazepine removal was favored by plant presence, which is not consistent with our results. As for diclofenac removal, the sorption of these compounds onto organic matter retained in the gravel bed is an important removal mechanism due to their hydrophobic structure, which could be ascribed to specific structural characteristics. Surprisingly, a significant difference between planted and unplanted bed was observed for planted beds compared to the unplanted beds, but only at a 4-day HRT (Table 3). Further investigation of its removal pathway and mechanisms is needed to be carried out in future experiments. The higher temperatures of wetlands in the tropics would be expected to increase plant productivity, biodegradation kinetics, and decrease the time necessary for biodegradation. Tropical conditions (e.g., warmth, plant activity and sunlight) can enhance the removal of pharmaceuticals (Hijosa-Valsero et al., 2010b), as microorganisms living in the CWs usually reach their optimal activity at warm temperatures (15–25 ◦ C) (Truu et al., 2009). Dordio et al. (2009) indicated that the removal of ibuprofen, cabamazepine and clofibric acid in planted microcosm CWs in summer (96%, 97% and 75%, respectively) was higher than in winter (82%, 88% and 48%, respectively). Similarly, Matamoros et al. (2008b) studying a full-scale surface flow constructed wetland found mean removal efficiencies of 92% and 52% for naproxen in the summer and winter, respectively, but this was at a much longer retention time (1 month) than the 2–4 day HRT used in our study. The rather efficient removal shown by the tropical wetlands with HRTs of 2–4 days indicates that such a CW system may be practically used with less land requirements in tropical regions for removing conventional pollutants and certain pharmaceuticals from wastewater effluents. 5. Conclusion This study demonstrated that CWs can be a cost-effective and sustainable alternative for removing selected emerging contaminants. Since artificial wastewater was used in this study, it is possible that the pollutant removal observed for treatment of actual wastewaters may be somewhat different than what we observed. The key results can be reported as follows: (1) CWs can offer comparable or even better pharmaceutical removal efficiencies compared to conventional WWTPs. Both ibuprofen and naproxen, pharmaceutical compounds both with low Dow values showed significant (p < 0.05) enhancement of removal in planted beds compared to unplanted ones. The presence of plants seems to favor the removal of certain pharmaceuticals from wastewater. Rhizosphere aeration may play an important role part in the establishment of an oxidizing environment, leading to higher degree of biodegradation and removal efficiency, but direct plant uptake of pharmaceutical compound may also be occurring. (2) Carbamazepine, considered as the most recalcitrant pharmaceuticals, and diclofenac showed low removal efficiencies in our CW, attributed to their higher hydrophobicity. The fact that the removal of these compounds could be explained by the sorption onto the available organic surfaces, explains why there was no significant difference (p > 0.05) in their removal efficiencies between planted and unplanted beds. (3) No statistical significant differences (p > 0.05) were observed for the removal efficiencies of any of the pharmaceuticals tested for a 2-day HRT compared to a 4-day HRT.

464

D.Q. Zhang et al. / Ecological Engineering 37 (2011) 460–464

References APHA, 1989. In: Clesceri, L.S., Greenberg, A.F., Trussell, R.R. (Eds.), Standard Methods for the Examination of Water and Wastewater. American Public Health Association. Beausse, J., 2004. Selected drugs in solid matrices – a review of environmental determination, occurrence and properties of principal substances. Trends Anal. Chem. 23, 753–761. Bendz, D., Paxéus, N.A., Ginn, T.T., Loge, F.J., 2005. Occurrence and fate of pharmaceutically active compounds in the environment: a case study: Höje River in Sweden. J. Hazard. Mater. 122, 195–204. Brimecombe, M.J., Leij, F.A.A.M., Lynch, J.M., 2001. Rhizodeposition and microbial populations. In: Pinton, R., Varanini, Z., Nannipieri, P. (Eds.), The Rhizosphere: Biochemistry and Organic Substances at the Soil–Plant Interface. Marcel Dekker, New York, pp. 74–98. Brix, H., 1994. Use of constructed wetlands in water pollution control: historical development, present status, and future perspectives. Water Sci. Technol. 30 (8), 209–223. Brix, H., 1993. In: Moshiri, G.A. (Ed.), Constructed Wetlands for Water Quality Improvement. CRC Press, Inc.. Brix, H., 1997. Do macrophytes play a role in constructed treatment wetlands? Water Sci. Technol. 35 (5), 11–17. Buser, H., Poiger, T., Mueller, M.D., 1999. Occurrence and environmental behaviour of the chiral pharmaceutical drug ibuprofen in surface waters and in wastewater. Environ. Sci. Technol. 33, 2529–2535. Daughton, C.G., Ternes, T.A., 1999. Pharmaceuticals and personal care products in the environment: agents of subtle change. Environ. Health Perspect. 107, 907–938. Dordio, A.V., Candeias, A.J.E., Pinto, A.P., Costa, C.T.D., Carvalho, A.J.P., 2009. Preliminary media screening for application in the removal of clofibric acid, carbamazepine and ibuprofen by SSF-constructed wetlands. Ecol. Eng. 35, 290–302. Dunbabin, J.S., Pokorny, J., Bowmer, K.H., 1988. Rhizosphere oxygenation by Typha domingensis in miniature artificial wetland filters used for metal removal from wastewaters. Aquat. Bot. 29, 303–317. Ellis, J.B., 2006. Pharmaceutical and personal care products (PPCPs) in urban receiving waters. Environ. Pollut. 144, 184–189. Garballa, M., Omil, F., Lema, J.M., Llompart, M., García-Jares, C., Rodríguez, I., Gómez, M., Ternes, T., 2004. Behavior of pharmaceuticals, consmetics and hormones in a sewage treatment plant. Water. Res. 38, 2918–2926. Gersberg, R.M., Elkins, B.V., Goldman, C.R., 1983. Nitrogen removal in artificial wetlands. Water Res. 17 (9), 1009–1014. Gersberg, R.M., Elkins, B.V., Lyon, S.R., Goldman, C.R., 1986. Role of aquatic plants in wastewater treatment by artificial wetlands. Water Res. 20 (3), 363–368. Heberer, T., 2002. Occurrence, fate and removal of pharmaceutical residues in the aquatic environment: a review of recent research data. Toxicol. Lett. 131, 5–17. Herklotz, P.A., Gurung, P., Heuvel, B.V., Kinney, C.A., 2010. Uptake of human pharmaceuticals by plants grown under hydroponic conditions. Chemosphere 78 (2010), 1416–1421. Hijosa-Valsero, M., Matamoros, V., Martín-Villacorta, J., Bécares, E., Bayona, J.M., 2010a. Assessment of full-scale natural systems for the removal of PPCPs from wastewater in small communities. Water Res. 44 (2010), 1429–1439. Hijosa-Valsero, M., Matamoros, V., Sidrach-Cardona, R., Martín-Villacorta, J., Bécares, E., Bayona, J.M., 2010b. Comprehensive assessment of the design configuration of constructed wetlands for the removal of pharmaceuticals and personal care products from urban wastewaters. Water Res. 44 (2010), 3669–3678. Jing, S.R., Lin, Y.F., Shih, K.C., Lu, H.W., 2008. Applications of constructed wetlands for water pollution control in Taiwan: review. Pract. Periodical Hazard. Toxic Radioactive Waste Manage. 12 (4), 249–259. Kadlec, R.H., Knight, R.L., 1996. Wetland soils. In: Kadlec, R.H., Knight, R.L. (Eds.), Treatment Wetlands. Lewis Publishers, Boca Raton, New York, pp. 63–118. Kadlek, R.H., Knight, L.R., Vymazal, J., Brix, H., 2000. Constructed wetlands for pollution control. Scientific and Technical Report, no. 8, p. 156. Llorens, E., Matamoros, V., Domingo, V., Bayona, J.M., García, J., 2009. Water quality improvement in a full-scale tertiary constructed wetland: effects on con-

ventional and specific organic contaminants. Sci. Total Environ. 407 (2009), 2517–2524. Matamoros, V., García, J., Bayona, J.M., 2005. Behavior of selected pharmaceuticals in subsurface flow constructed wetlands: a pilot-scale study. Environ. Sci. Technol. 39, 5449–5454. Matamoros, V., Bayona, J.M., 2006. Elimination of pharmaceuticals and personal care products in subsurface flow constructed wetlands. Environ. Sci. Technol. 40, 5811–5816. Matamoros, V., Arias, C., Brix, H., Bayona, J.M., 2007. Removal of pharmaceuticals and personal care products (PPCPs) from urban wastewater in a pilot vertical flow constructed wetland and a sand filter. Environ. Sci. Technol. 41, 8171–8177. Matamoros, V., Osorio-Casellees, A., García, J., Bayona, J.M., 2008a. Behaviour of pharmaceutical products and biodegradation intermediates in horizontal subsurface flow constructed wetland. A microcosm experiment. Sci. Total Environ. 394 (2008), 171–176. Matamoros, V., García, J., Bayona, J.M., 2008b. Organic micropollutant removal in a full-scale surface flow constructed wetland fed with secondary effluent. Water Res. 42 (2008), 653–660. Matamoros, V., Bayona, J.M., 2007. Behavior of Emerging Pollutants in Constructed Wetlands, vol. 3, Part S/2 (2008). Handb. Environ. Chem, pp. 199–217. Mitsch, W.J., Day, J.W., Zhang, J.L., Lane, R., 2005. Nitrate–nitrogen retention by wetlands in the Mississippi River Basin. Ecol. Eng. 24, 267–278. Mitsch, W.J., Tejada, J., Nahlik, A., Kohlmann, B., Bernal, B., Hernández, C.E., 2008. Tropical wetlands for climate change research, water quality management and conservation education on a university campus in Gosta Rica. Ecol. Eng. 34 (2008), 276–288. Mitsch, W.J., Gosselink, J.G., 2007. Wetlands, 4th ed. John Wiley & Sons, Inc., New York. Mitsch, W.J., 1995. Restoration and creation of wetlands – providing the science and engineering basis and measuring success. Ecol. Eng. 4 (1995), 61–64. Park, N., Vanderford, B.J., Snyder, S.A., Sarp, S., Kim, S.D., Cho, J., 2009. Effective controls of micropollutants in wastewater effluent using constructed wetlands under anoxic condition. Ecol. Eng. 35 (2009), 418–423. Quintana, J.G., Weiss, S., Reemtsma, T., 2005. Pathways and metabolites of microbial degradation of selected acidic pharmaceuticals and their occurrence in municipal wastewater treated by a membrane bioreactor. Water Res. 39, 2654–2664. Reddy, K.R., Patrick, W.H., Lindau, C.W., 1989. Nitrification–denitrification at the plant root–sediment interface in wetlands. Ecol. Eng. 34, 1004–1013. Ternes, T.A., Stüber, J., Herrmann, N., McDowell, D., Ried, A., Kampmann, M., 2003. Ozonation: a tool for removal of pharmaceuticals, contrast media and musk fragrances from wastewater? Water Res. 37 (8), 1976–1982. Ternes, T.A., Bounerz, M., Herrmann, N., Teiser, B., Andersen, H.R., 2007. Irrigation of treated wastewater in Braunschweig, Germany, an option to remove pharmaceuticals and musk fragrances. Chemosphere 66, 894–904. Truu, M., Juhanson, J., Truu, J., 2009. Microbial biomass, activity and community composition in constructed wetlands. Sci. Total Environ. 407 (13), 3958–3971. Turner, A., Williamson, I., 2005. On the relationship between Dow and Kow in natural waters. Environ. Sci. Technol. 39, 8719–8727. Veen, J.A., Overbeek, L.S., Elsas, J.D., 1997. Fate and activity of microorganisms introduced into soil. Microbiol. Mol. Biol. Rev. 61 (2), 121–135. Vymazal, J.K., Kröpfelová, L., 2008. Natural and constructed wetlands for wastewater treatment. In: Wastewater treatment in constructed wetlands with horizontal sub-surface flow. Environ. Pollut. 14, 3. Vymazal, J., 2005. Horizontal sub-surface flow and hybrid constructed wetlands systems for wastewater treatment. Ecol. Eng. 25, 478–490. Whipps, J.M., 1990. Carbon economy. In: Lynch, J.M. (Ed.), The Rhizosphere. Wiley, New York, pp. 59–97. White, J.R., Belmont, M.A., Metcalfe, C.D., 2006. Pharmaceutical compounds in wastewater: wetlands treatment as a potential solution. Sci. World J. 6, 1713–1736.