Occurrence and removal of pharmaceuticals and personal care products (PPCPs) in an advanced wastewater reclamation plant

w a t e r r e s e a r c h 4 5 ( 2 0 1 1 ) 5 2 1 8 e5 2 2 8

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Occurrence and removal of pharmaceuticals and personal care products (PPCPs) in an advanced wastewater reclamation plant Xin Yang a,*, Riley C. Flowers b, Howard S. Weinberg b, Philip C. Singer b a

School of Environmental Science and Engineering, Sun Yat-sen University, Guangzhou, China Department of Environmental Sciences and Engineering, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599-7431, United States b

article info

abstract

Article history:

The occurrence of nineteen pharmaceutically active compounds and personal care prod-

Received 7 May 2011

ucts was followed monthly for 12 months after various stages of treatment in an advanced

Received in revised form

wastewater reclamation plant in Gwinnett County, GA, U.S.A. Twenty-four hour composite

13 July 2011

samples were collected after primary clarification, activated sludge biological treatment,

Accepted 21 July 2011

membrane filtration, granular media filtration, granular activated carbon (GAC) adsorption,

Available online 29 July 2011

and ozonation in the wastewater reclamation plant. Compounds were identified and quantified using high performance liquid chromatography/tandem mass spectrometry (LC-

Keywords:

MS/MS) and gas chromatography/mass spectrometry (GCeMS) after solid-phase extraction.

Pharmaceuticals and personal care

Standard addition methods were employed to compensate for matrix effects. Sixteen of the

products (PPCPs)

targeted compounds were detected in the primary effluent; sulfadimethoxine, doxycycline,

Wastewater

and iopromide were not found. Caffeine and acetaminophen were found at the highest

Ozonation

concentrations (w105 ng/L), followed by ibuprofen (w104 ng/L), sulfamethoxazole and DEET

Activated sludge biological

(w103 ng/L). Most of the other compounds were found at concentrations on the order of

treatment

hundreds of ng/L. After activated sludge treatment and membrane filtration, the concen-

GAC adsorption

trations of caffeine, acetaminophen, ibuprofen, DEET, tetracycline, and 17a-ethynylestradiol (EE2) had decreased by more than 90%. Erythromycin and carbamazepine, which were resistant to biological treatment, were eliminated by 74 and 88%, on average, by GAC. Primidone, DEET, and caffeine were not amenable to adsorption by GAC. Ozonation oxidized most of the remaining compounds by >60%, except for primidone and DEET. Of the initial 16 compounds identified in the primary effluent, only sulfamethoxazole, primidone, caffeine and DEET were frequently detected in the final effluent, but at concentrations on the order of 10e100 ng/L. Removal of the different agents by the various treatment processes was related to the physicalechemical properties of the compounds. ª 2011 Elsevier Ltd. All rights reserved.

1.

Introduction

Pharmaceuticals and personal care products (PPCPs) are likely to be found in any body of water influenced by raw or treated

wastewater, including rivers, streams, lakes and impoundments, and ground waters, many of which are used as drinking water sources. Some PPCPs may cause ecological harm, such as endocrine disruption and development of

* Corresponding author. Tel.: þ86 2039332690. E-mail address: [email protected] (X. Yang). 0043-1354/$ e see front matter ª 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.watres.2011.07.026

w a t e r r e s e a r c h 4 5 ( 2 0 1 1 ) 5 2 1 8 e5 2 2 8

antimicrobial resistance. The health effects of small amounts of these agents on humans over a lifetime of exposure are unknown at this time. Municipal wastewater is a significant source of PPCPs in the environment because many of them are not removed completely in conventional wastewater treatment plants. The literature shows a wide range of many classes of PPCPs (e.g., antibiotics, betablockers, antiepileptics, liquid regulators) in wastewater effluents and receiving waters (Kasprzyk-Hordern et al., 2008; Kolpin et al., 2002; Lindberg et al., 2005; Ternes et al., 2003). Conventional wastewater treatment processes, such as activated sludge treatment and subsequent clarification, are not effective at completely eliminating all PPCPs from wastewater (Westerhoff et al., 2005). Activated carbon adsorption, ozonation or advanced oxidation, and membrane separation are promising advanced treatment processes that are capable of removing many of the PPCPs commonly found in wastewater (Ikehata et al., 2008; Snyder et al., 2007; Westerhoff et al., 2005). For example, addition of 5 mg/L of powder activated carbon (PAC) with a 4-h contact time removed 50%e>98% of the volatile PPCPs analyzed by GC/MS/MS and 10%e>95% of the polar PPCPs analyzed by LC/MS/MS (Westerhoff et al., 2005). Ozone is extremely reactive with some pharmaceuticals, such as carbamazepine, diclofenac, estradiol and estrogen (Ikehata et al., 2008; Westerhoff et al., 2005). These pharmaceuticals have functional groups and structures such as phenolic groups, amines, thioether sulfurs, and activated aromatic rings that are readily attacked by ozone. These advanced processes have mostly been evaluated using laboratory batch tests. Few studies have examined PPCP removal in full-scale treatment plants containing the advanced wastewater treatment processes listed above (Dickenson et al., 2009; Hollender et al., 2009; Reungoat et al., 2010). Furthermore, most of the full-scale studies that have been done have utilized intermittent grab samples. No study has been conducted to evaluate PPCP removal using composite samples over an extended period of time, e.g., one year. The F. Wayne Hill Water Resources Center, a wastewater reclamation plant in Gwinnett County, GA, employs both conventional biological treatment and advanced treatment processes, including membrane filtration, granular media filtration, granular activated carbon (GAC) adsorption, and ozonation, to treat its wastewater. The treated wastewater is currently discharged into the Chattahoochee River which ultimately serves as a drinking water supply for several downstream communities, including the City of Atlanta. Prior to this study, no information was available on the occurrence levels or effect of treatment on PPCPs at this plant. The primary aim of this work was to investigate the removal of 19 PPCPs by various wastewater treatment processes, including activated sludge treatment, membrane filtration, granular media filtration, GAC adsorption, and ozonation, in an advanced wastewater treatment plant and to relate the extent of removal to physicalechemical properties of the targeted PPCP compounds. The originality of this work derives from the long time span (over one year) of monthly sampling, utilization of composite sample collection instead of collection of grab samples, the investigation of different treatment processes in a full-scale advanced wastewater treatment plant, and a comparison of observations with wellknown physicalechemical properties of the analytes.

2.

Materials and methods

2.1.

Selected PPCPs

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A diverse group of PPCPs widely reported to occur in aquatic systems was chosen for study (see Table 1). Compounds were chosen to represent different groups of PPCPs, such as antibiotics, antiepileptics, analgesic drugs, X-ray contrast agents, and personal care products such as insect repellants. One or two compounds representing different classes of antibiotics were selected, such as quinolones, tetracyclines, sulfonamides, diaminopyrimidines, and lincosamides. In each class, compounds that are frequently reported in wastewater were considered. Differences in structures and physicalechemical properties were also considered. As noted in Table 1, sulfamethoxazole, erythromycin, trimethoprim, lincomycin, caffeine, DEET, acetaminophen, and triclosan were among the 30 most frequently detected organic wastewater contaminants as reported by the US Geological Survey (Kolpin et al., 2002). Six of the compounds selected e ciprofloxacin, erythromycin, sulfamethoxazole, carbamazepine, ibuprofen, and diclofenac e were among the top 10 high priority pharmaceuticals identified in a European assessment of PPCPs (Voogt et al., 2008). Physical, chemical, and biological properties of the targeted PPCPs are listed in Table 1 and the structures of the PPCPs are given in Table S1.

2.2.

Description of treatment plant

The F. Wayne Hill Water Resources Center treats 227 thousands of cubic meters per day of wastewater from Gwinnett County, GA. The facility consists of primary clarification for removal of settleable solids; activated sludge treatment (sludge age of 12 days and mixed liquor suspended solids concentration of 3200 mg/L) to achieve removal of biochemical oxygendemanding organic compounds (BOD), nitrogen, and phosphorus; and secondary clarification. Flow then splits, with about 5% going to a second clarification tank after ferric chloride addition, followed by granular media filtration. The remaining 95% of the flow goes to submerged membrane microfiltration units. The flow is then combined and passes on to GAC adsorption beds (Calgon F-400) with an empty bed contact time of 15 min. The beds were in place for about three years at the time this study began. It was assumed that they were essentially exhausted with respect to adsorption capacity other than capacity produced by bio-regeneration. The final effluent passes through ozone contact chambers; ozone doses range from 0.75 to 2 mg/L, with an average of 1 mg/L. A schematic diagram of the facility is shown in Fig. 1. General wastewater quality parameters, e.g., COD (chemical oxygen demand), TSS (total suspended solids), ammonia-nitrogen, etc., are listed in Table S2 in the Supporting Information.

2.3.

Sample collection

Composite samples at the wastewater reclamation treatment plant were collected by plant personnel once each month over a 24-h period using an Isco (Teledyne Isco, Lincoln NE)

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Table 1 e Targeted PPCPs in this study and their properties. Class Sulfonamide antibiotic Macrolide antibiotic Quinolone antibiotic Tetracycline antibiotic Other antibiotic Antiepileptic X-ray contrast agent Anti-inflammatory

Antiseptic Hormone Others

Log K[2] ow

Compound

pKa[1]

Sulfadimethoxine Sulfamethoxazolea,b Erythromycina,b Lincomycina Ciprofloxacinb Levofloxacin Doxycycline Tetracycline Trimethoprima Carbamazepineb Primidone Iopromide Ibuprofenb Acetaminophena Diclofenacb Triclosana 17a-Ethynylestradiol (EE2) Caffeinea DEETa

N/A 1.69, 5.57 8.88 7.60 6.43, 8.49 6.05, 8.22 N/A 3.30, 7.68, 9.69 7.12 13.90 N/A N/A 4.91 9.38 4.15 7.9 10.4 10.40 0.67

kOH (109 M1s1)

Log Kd

Kbiol

kO3 (M1s1)

N/A 0.89 3.06 0.56 0.28 0.39 N/A 1.3 0.91 2.45 0.91 2.05 3.97 0.46 4.51 4.76 3.67

N/A 2.4[3] N/A N/A 4.3[7] N/A N/A N/A 2.3[3] 0.1[9] N/A 1.0[9] 0.9[9] 2.6[12] N/A 1.2[9] N/A 2.5[9]

N/A <0.1[4] 0.5e1[4] N/A N/A N/A N/A N/A N/A <0.01[10] N/A 1e2.5[10] 21e35[10] N/A <0.1[10] N/A 7e9[4]

N/A 2.5  106 [5] N/A 3.3  105 [6] 1.9  104 [8] N/A N/A 1.9  106 [8] 2.7  105 [8] 3.0  105 [5] 1.04[11] <0.8[5] 9.1  1[5] 1.41  103 [13] 1.0  106 [5] 3.8  107 [14] 3.0  106 [5]

N/A 5.5  0.7[5] N/A N/A 4.1[8] N/A N/A 7.7[8] 6.9[8] 8.8  1.2[5] 6.7[11] 3.3  0.6[5] 7.4  1.2[5] 2.2 7.5  1.5[5] N/A 9.8  1.2[5]

0.07 2.18

N/A N/A

N/A N/A

0.82[15] N/A

6.9[16] 4.95[17]

pKa, negative log of acidity constant(s); Kow, octanol-water partition coefficient; Kd, sorption constant on activated sludge; Kbio, pseudo firstorder degradation rate constant (1 g SS1 day1); KO3, second-order rate constant with O3; KOH, second-order rate constant with OH radicals. References : [1] Howard and Meylan, 1997 [2] http://logkow.cisti.nrc.ca/logkow/search.html. [3] Gobel et al., 2005 [4] Suarez et al., 2008 [5] Huber et al., 2003 [6] Qiang et al., 2004 [7] Golet et al., 2003 [8] Dodd et al., 2006 [9] Ternes et al., 2004 [10] Joss et al., 2006 [11] Benitez et al., 2008 [12] Carballa et al., 2007 [13] Andreozzi et al., 2005 [14] Suarez et al., 2007 [15] Rosal et al., 2009 [16] Kesavan and Powers, 1985 [17] Song et al., 2009. a Among the 30 most frequently detected organic wastewater chemicals reported by US Geological Survey (Kolpin et al., 2002) b Among the top 10 high priority pharmaceuticals identified in a European assessment of PPCPs (Voogt et al., 2008).

automated refrigerated sampler on a flow-weighted basis from each of the sampling locations shown in Fig. 1. Samples of primary clarifier, membrane filtration, GAC adsorption, and final effluent were collected monthly from January to December 2008. Secondary clarifier effluent following activated sludge treatment, and granular media filtration effluent were collected from September to December 2008. Raw wastewater influent was not collected and analyzed due to complexity introduced by the high suspended solids content of these samples and difficulties associated with analysis of such samples. After collection, samples were transferred to 2.5 L amber glass bottles, packed with “blue ice” in an insulated cooler chest, and transported to the University of North Carolina at Chapel Hill (UNC) for overnight delivery. The bottles had

been previously treated with 5% dimethyldichlorosilane in toluene to minimize adsorption of analytes to the walls of the bottles. The treated bottles were rinsed with toluene, methanol and laboratory-grade water (LGW), and dried prior to use (Ye et al., 2007). Upon receipt at UNC, samples were filtered immediately through 0.45 mm nylon filters (Millipore, Billerica, MA) and the pH was adjusted to 2.5 with concentrated sulfuric acid. Samples were then stored at 4  C in the dark. The extracts were analyzed within one week of receipt.

2.4.

Standards were obtained from the following suppliers: iopromide (U.S. Pharmacopeia, Rockville, MD), primidone (MP

Membrane filtration

Chemical Addition

Grit chamber

Standards and reagents

95%

screen

Primary clarifier

Aeration tanks Secondary clarifier

5%

Chemical Addition

GAC

Ozone contactor

Chemical clarifier Composite sampling location – Monthly sampling for 12 months

Granular media filter

Composite sampling location – Monthly sampling for 4 months

Fig. 1 e Schematic diagram of the wastewater reclamation plant, showing sampling locations.

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Biomedicals, LLC, Solon, OH), ciprofloxacin (ICN Biochemicals, Irvine, CA), levofloxacin, caffeine, and triclosan (Fluka, Buchs, Switzerland). Surrogate standards 13C6-sulfamethoxazole and 13 C2-erythromycin were obtained from Cambridge Isotope Laboratories (Andover, MA) and d3-caffeine was obtained from C/D/N Isotopes (Quebec, Canada). Internal standards simatone and fenoprop were purchased from Accustandard (New Haven, CT) and SigmaeAldrich (St. Louis, MO), respectively. All other standards were obtained from SigmaeAldrich (St. Louis, MO). LGW was prepared in a water purification system (Pure Water Solutions, Hillsborough, NC) which prefilters fines (1 mm), removes chlorine, reduces total organic carbon to less than 0.2 ppm with activated carbon, and removes ions to 18 MU with mixed-bed ion-exchange resins. Stock solutions of the standards were prepared by dissolving each compound in methanol or LGW.

2.5.

Analytical methods

Solid-phase extraction (SPE) methods were employed to concentrate the analytes from the aqueous samples. Triclosan and EE2 were extracted, derivatized and analyzed by gas chromatography/mass spectrometry (GC/MS) based on a previously published method by Stanford and Weinberg (Stanford and Weinberg, 2007). Other compounds were analyzed by liquid chromatography/tandem mass spectrometry (LC/MS/MS) using the method of Ye et al. (Ye et al., 2007) with the following modifications; 13C6-sulfamethoxazole, 13 C2-erythromycin and d3-caffeine were used as surrogate standards and simatone and fenoprop were used as internal standards. The detailed SPE methods for all PPCPs are described in the Supporting Information (Text S1). The method of standard additions was used to compensate for matrix effects. Each sample was split into seven aliquots, five of which were spiked with standard solutions of the target

PPCPs; the remaining two were not spiked. The spike levels were selected so that the calculated concentrations of the compounds fell into the ranges of the spiked additions. Spike levels of 10, 20, 50, 100, and 200 ng/L were employed for the final effluent from the wastewater plant. The spike levels for the other samples varied. The LC/MS/MS system consisted of a ProStar 210 solvent delivery module, a ProStar 430 autosampler, and a Varian 1200L triple quadrupole mass spectrometer (Varian Inc., Walnut Creek, CA). Chromatographic separation was achieved using a Pursuit C-18 column (15 cm  2 mm, 3 mm) and a C-18 guard column (3 cm  2 mm, 3 mm) supplied by Varian Inc. The optimal collision voltage for each of the precursor to product ion transitions of each compound is listed in Table S3 in the Supporting Information. The derivatized triclosan and EE2 were analyzed on an HP 5890 bench-top GC/MS (HewlettePackard) containing an HP 5972 mass selective detector (MSD) equipped with electron ionization (70 eV). The column was a DB-5MS fused silica capillary column (30 m  0.25 mm I.D. with 0.25 mm film thickness, J&W Scientific). Detailed information about the chromatographic and mass spectrometric methods, detection limits, quality assurance and control protocols are described in the Supporting Information (Text S2). Minimum reporting limits (MRLs) and recovery data are listed in Tables S4 and S5 in the Supporting Information, respectively.

3.

Results and discussion

3.1. PPCP concentration profiles across the wastewater reclamation plant Table 2 summarizes the monthly average, minimum and maximum concentrations of the targeted PPCPs in the primary, membrane filter, GAC and final effluent for the 12-

Table 2 e Summary of monthly average, minimum, and maximum concentrations of targeted PPCPs measured in 24-h composite samples of primary, membrane filter, GAC and final effluent (January to December, 2008). Compounds

Sulfamethoxazole Erythromycin Trimethoprim Lincomycin Ciprofloxacin Levofloxacin Tetracycline Carbamazepine DEET Primidone Diclofenac Triclosan EE2 Caffeine Acetaminophen Ibuprofen

Primary effluent

Membrane effluent

Average ng/L

Min ng/L

Max ng/L

Average ng/L

2600 340 610 21 620 460 160 230 1500 100 220 470 140 80000 80000 11000

1200 (140) 390 11 430 250 68 130 220 (60) 140 170 (24) 54000 37000 (3900)

3400 480 770 36 1100 900 310 440 4000 180 280 820 242 120000 130000 15000

420 270 280 14 130 140 <50 250 29 120 99 15 <20 65 <50 64

() Values are below MRLs, but meet quality control criteria. a Detected in a single sample.

GAC effluent

Final effluent

Min ng/L

Max ng/L

Average ng/L

Min ng/L

Max ng/L

Average ng/L

Min ng/L

Max ng/L

130 140 (69) 10 70 63

1600 410 530 20 240 250

210 13 11

1200 50 32

140 15

19

30

550 100 190 130 19

25 13 33

140 48 96

14

57

80 2 <10 <10 1 1 <10 1 18 46 <10 <10 <10 17 <50 <10

35 <10

100 13 90 (27) 13

670 28 21 <10 23 <10 <10 67 24 72 <10 <10 <10 36 <50 <10

38

98

(49)

78

<10 <10

16a 10a

<10 <10 25

12a 30 120

<10

50

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month period from January to December, 2008. Figure S1(a)e(d) in the Supporting Information show PPCP concentrations in the primary, membrane, GAC and final effluent composite samples collected each month, respectively; the error bars shown represent the difference in concentration of the two duplicate unspiked samples. Sixteen of the nineteen target compounds were detected in the primary effluent. Doxycycline, sulfadimethoxine, and iopromide were below their MRL values in each sample. The compounds with the highest concentrations were caffeine, acetaminophen and ibuprofen which were found at levels of tens of mg/L. (See Table 2 and right side of Figure S1(a) and note change in scale.) Acetaminophen and ibuprofen are pain killers and are among the most widely used PhACs in the US. Caffeine is a stimulant and is also commonly used in beverages and foods. Similar levels of these compounds have been reported in the raw wastewater of other municipal wastewater treatment plants (Benotti and Brownawell, 2007; Buerge et al., 2003; Vieno et al., 2005). Sulfamethoxazole concentrations varied from about 1200 to 3400 ng/L, with an average concentration of 2570 ng/L. Previous reported levels of sulfamethoxazole in raw wastewater range from 520 to 9000 ng/L (Gobel et al., 2005; Hartig et al., 1999; Lindberg et al., 2005). The high concentrations of sulfamethoxazole could be due to its high rate of consumption for medical treatment purposes. Trimethoprim is always prescribed with sulfamethoxazole at a dose weight ratio of 0.2, and a trimethoprim/ sulfamethoxazole ratio of 0.23 by weight was found for most of the samples in this study. Concentrations of DEET, a widely used insect repellant, ranged from about 220 to 4000 ng/L, with an average level of 1500 ng/L. The measured concentrations of DEET in the primary effluent show a noticeable seasonal pattern, with concentrations being lowest in the winter months and peaking in the summer months, consistent with expected usage patterns for this insect repellant. (Values are not shown for July and August because the observed concentrations were above the highest spike levels (2000 ng/L) used to construct the calibration curve.) The other eleven PPCPs were found at concentrations below 1000 ng/L (1 mg/L). After activated sludge treatment and membrane filtration, most compounds were measured at concentrations below 1000 ng/L (see Figure S1(b) and Table 2). Tetracycline, EE2 and acetaminophen were below their respective MRLs of 50, 20 and 50 ng/L. Caffeine, ibuprofen and acetaminophen, which were found at the highest concentrations in the primary effluent, were all reduced to below 100 ng/L. A comparison of PPCP concentrations in the effluent from the secondary clarifiers, membrane filters, and granular media filters (GMF) for the 4 months in which composite samples were collected at all three of these locations (see Fig. 1) is shown in Figure S2 in the Supporting Information. In general, similar concentrations were found for all of the PPCPs in the clarifier and membrane filter effluents, implying that the PPCP removal shown in Figure S1(b) and Table 2 was due to biological treatment and subsequent solideliquid separation of the biological floc, not due to removal by membrane treatment. Microfiltration membranes are essentially a particle removal technology and, accordingly, do not reject soluble PPCPs. Since the analytical methods used in this study only

capture PPCPs in the aqueous phase, this is hardly surprising. Snyder et al. also found that microfiltration and ultrafiltration did not reject PPCPs to any appreciable degree (Snyder et al., 2007). Concentrations of PPCPs in GMF effluent were similar to those in secondary clarifier and membrane effluent, except for ciprofloxacin and levofloxacin, which were lower in the GMF effluent. For the GAC effluent, the compound with the highest levels was sulfamethoxazole, with concentrations ranging from 210 to 1200 ng/L. All other PPCPs were found at concentrations below 100 ng/L (except for one case of carbamazepine), as shown in Figure S1(c) and Table 2. Table 2 and Figure S1(d) show the PPCP concentrations in the final effluent, after ozonation. Sulfamethoxazole and primidone were detected in all of the monthly samples. Caffeine and DEET were detected frequently. The concentrations of sulfamethoxazole, primidone, DEET, and caffeine were in the range of 35e140, 25e120, <10e30, and <10e50 ng/L, respectively, and the average concentrations were respectively 78, 46, 21, and 20 ng/L. Erythromycin, ciprofloxacin, ibuprofen, and carbamazepine were found only occasionally in the final effluent. All of the other targeted PPCP compounds were below their MRLs.

3.2. Removal of targeted PPCPs by various unit processes Fig. 2 shows the concentrations of selected PPCPs across the treatment plant for illustrative purposes: (a) DEET; (b) sulfamethoxazole; and (c) primidone. Figure S3 in the Supporting Information shows concentrations of the other PPCPs across the treatment plant. Activated sludge treatment and microfiltration reduced the concentrations of DEET by several orders of magnitude (Fig. 2(a)). DEET appears to be relatively resistant to removal by GAC adsorption and ozonation. Significant removal of sulfamethoxazole (Fig. 2(b)) was achieved by biological treatment, but GAC treatment for sulfamethoxazole removal appeared to be limited. In fact, for a number of months, the concentration of sulfamethoxazole in the GAC effluent appeared to be higher than in the GAC influent. This is the only PPCP for which this pattern was observed. The cause of this apparent anomaly is not clear, but may be related to the anionic nature of sulfamethoxazole or to the presence and transformation of sulfamethoxazole metabolites. Table 1 indicates that, because of the low acidity constants for sulfamethoxazole, it is most likely present in anionic form. Anionic species tend to be poorly adsorbed by GAC, and it is possible that any sorbed sulfamethoxazole might have been displaced by other adsorbates. This pattern of adsorption and displacement may vary over time, depending on variations in influent water quality to the GAC bed and the extent of biodegradation reactions within the bed. Additionally, various human metabolites of sulfamethoxazole, such as N4-acetylsulfamethoxazole, are known to be present in municipal wastewater. N4-acetylsulfamethoxazole was measured using the same method as for sulfamethoxazole and analyzed by LC/MS/MS for two months during the latter phases of the study; the results are shown in Figure S4. Concentrations of N4-acetylsulfamethoxazole were greatly

w a t e r r e s e a r c h 4 5 ( 2 0 1 1 ) 5 2 1 8 e5 2 2 8

5000

a

DEET

Concentration (ng/L)

4000

90th percentile

2000

75th percentile

3.3.1.

Median

The percentage removal of each PPCP by activated sludge treatment and microfiltration is shown in Fig. 3. The removal is presented using box and whiskers plots which give the 10th, 25th, 50th (median), 75th, and 90th percentile values of the monthly composite analyses, as well as any outliers. Removal here refers to a reduction in concentration due to biodegradation and sorption (see below) since only measurements in the liquid phase were made. Also, it is recognized that the compound may be transformed to various products that may persist in the treated water so that the compound may not be completely removed; no analyses were performed for possible degradation products. Because, as noted above, membrane microfiltration is essentially a particle removal process, the values shown in Fig. 3 are attributed to removal by the microorganisms in the activated sludge process. PPCP removal in the activated sludge process is attributed to two mechanisms: sorption onto biological floc and biodegradation. Kd, the sorption constant which describes the partitioning of a compound between solid and aqueous phases, Kow, the widely used octanol-water partition coefficient which describes partitioning between lipophilic and hydrophilic phases, and Kbiol, the pseudo first-order biodegradation rate constant obtained from batch biodegradation tests, are listed in Table 1 for the various PPCPs examined, along with reference citations from which the values were obtained. The Kd values vary for sludges with different sludge ages and properties, and biodegradation rates for each of the compounds may differ due to different operating conditions at the treatment plant. The different PPCPs investigated in this study exhibited very different removal percentages. Acetaminophen, caffeine and ibuprofen, which were present at the highest concentrations in the primary effluent, were removed by more than 99%. Consistently high removal efficiencies for these compounds have also been reported by other researchers (Buerge et al., 2003; Miao et al., 2005; Vieno et al., 2005; Yu et al., 2006), attributable primarily to microbial degradation (Joss et al., 2006). No detectable tetracycline was found after activated sludge treatment. Though tetracycline has a high aqueous solubility and a low Kow, it has been shown to sorb readily onto various solids, such as soil particles (Lindsey et al., 2001; Sithole and Guy, 1987), and exhibited a high adsorption affinity for activated sludge biosolids (Kim et al., 2005). Significant removal of fluoroquinolone antibiotics was observed, an average of 80% for ciprofloxacin and 71% for levofloxacin. Sorption onto sludge floc has been found to be significant for ciprofloxacin, consistent with its high log Kd value of 4.3 reported by Golet et al. (2003). Although a Kd value for levofloxacin was not reported, the high Kd values for other fluoroquinolone antibiotics, such as norfloxacin, trovafloxacin, and gemifloxacin, suggest that levofloxacin is also strongly adsorbed. Due to the higher polarity of levofloxacin, its removal by adsorption was expected to be less than that of ciprofloxacin.

25th percentile 10th percentile 1000

b

Sulfamethxoazole

Concentration (ng/L)

3000

2000

1000

c Primidone 200

Concentration (ng/L)

PPCPs were apparent, other than the observation for DEET noted above.

3.3. Integrated assessment of removal of PPCPs by various processes

outlier 3000

5223

150

100

50

0

Primary effluent

Membrane GAC effluent effluent

Final effluent

Fig. 2 e Concentrations of (a) DEET; (b) sulfamethoxazole; and (c) primidone in primary, membrane filtration, GAC, and final effluent.

reduced during activated sludge treatment, and GAC treatment provided additional removal. It is possible that some of the N4-acetylsulfamethoxazole was transformed to sulfamethoxazole during GAC treatment. Transformations of other sulfamethoxazole metabolites confound the interpretation of sulfamethoxazole behavior during treatment. The results for primidone (Fig. 2(c)) show that it is essentially resistant to activated sludge treatment, GAC adsorption, and ozonation. Primidone was frequently detected in the final effluent of the treatment facility. An attempt was made to examine seasonal variations in the occurrence and removal of the PPCPs and also to see if there were any relationships with wastewater quality or operational parameters at the treatment plant. However, no seasonal variations in the occurrence and removal of the

Activated sludge treatment and microfiltration

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100%

Removal efficiency

80% outlier

60%

90th percentile 75th percentile

40%

Median 25th percentile

20%

10th percentile

0% -20%

9

4

7

4

9

4

9

8

9

4

11

8

6

9

Caffeine

ibuprofen

Tetracycline

EE2

DEET

triclosan

Sulfamethoxazole

Ciprofloxacin

Levofloxacin

diclofenac

Trimethoprim

Lincomycin

Erythromycin

Primidone

10 Carbamazepine

N 9 Acetaminophen

N: number of samples

Fig. 3 e Removal efficiency of targeted PPCPs by activated sludge biological treatment and membrane filtration. (The number above the X-axis refers to the number of samples that were analyzed and met the quality assurance criteria.)

Removal of trimethoprim varied from 21% to 91%, with a median value of 58%, and removal of erythromycin varied from 41% to 72% with a median value of 4%. Values from the literature also show a large variation, from 40% to 70% removal for trimethoprim (Batt et al., 2006; Gobel et al., 2007; Lindberg et al., 2005; Kasprzyk-Hordern et al., 2009) and 14 to 49% removal for erythromycin (Gobel et al., 2007; KasprzykHordern et al., 2009). Higher removals have been reported for trimethoprim in nitrifying sludge, with longer sludge ages, than in conventional activated sludge (Batt et al., 2006). For sulfamethoxazole, the mean removal in this study was 92%, which is inconsistent with the findings by Joss et al. (2006) who reported a Kbiol value of less than 0.1 for sulfamethoxazole, suggesting it is minimally biodegradable. Different operating conditions in full-scale, continuous-flow treatment plants compared to the batch biodegradation tests conducted by Joss et al. (2006), such as differing dissolved oxygen levels, sludge ages, and wastewater characteristics, may be responsible for the observed differences in the two studies. N4-acetylsulfamethoxazole, a metabolite of sulfamethoxazole, was also reduced in concentration by 80e90%, presumably via biodegradation. Diclofenac was removed by 51e80% by activated sludge treatment. Removal percentages reported in the literature vary significantly. Some studies showed resistance of diclofenac to activated sludge treatment (Kasprzyk-Hordern et al., 2009), while other researchers reported a range of 9e80% removal (Kimura et al., 2007; Lindqvist et al., 2005; Yu et al., 2006). The sorption coefficient of 16 L/kg SS (log Kd ¼ 1.2) is

too low to expect significant attachment to sludge floc (Ternes et al., 2004). Poor biodegradation was also found in the batch tests by Joss et al. (2006). Zwiener and Frimmel (2003) reported that the anoxic-oxic ratios in microbial reactors may influence the efficiency of diclofenac removal, with better diclofenac degradation under anoxic conditions. The activated sludge process in the Gwinnett plant employs anoxic cells along with aeration cells to facilitate nitrogen and phosphorus removal. This may explain the high removal observed for diclofenac. Triclosan was eliminated by 96% due to biological treatment. Triclosan is relatively hydrophobic (log Kow ¼ 4.76), and the high sorption constant (log Kd ¼ 4.3) suggests that triclosan will be strongly sorbed onto sludge floc (Singer et al., 2002). Triclosan was also reported to undergo complete mineralization to CO2 as a result of biodegradation, with some incorporation into biomass (Federle et al., 2002). Therefore, it appears that both biodegradation and sorption contribute to triclosan removal. Good removal of DEET and EE2 were found in this study as a result of activated sludge treatment. DEET and EE2 have both been reported to be readily biodegradable (Joss et al., 2006; Rivera-Cancel et al., 2007). No significant removal of carbamazepine was found by activated sludge treatment, which is consistent with literature reports (Clara et al., 2004; Joss et al., 2005; Miao et al., 2005). The low Kd and Kbio values suggest that carbamazepine does not adsorb onto sludge biosolids and is not readily biodegradable. Although corresponding properties for primidone were not found in the literature, the results indicate that primidone is recalcitrant to activated sludge treatment.

w a t e r r e s e a r c h 4 5 ( 2 0 1 1 ) 5 2 1 8 e5 2 2 8

In summary, sorption, biodegradation, or both could be the dominant pathway for the removal of PPCPs during activated sludge treatment, dependent on the physical, chemical, and biological properties of the specific PPCP.

applied to predict the adsorbability of an acidic or basic PPCP using the following equation, which takes into account the speciation of the compound at the pH of the wastewater: 0

KOW ¼

3.3.2.

GAC adsorption

Fig. 4 summarizes the PPCP removal results by GAC treatment. GAC effectively removed many of the PPCPs, with concentrations of some compounds decreasing by over 60% after GAC treatment. DEET, caffeine and primidone were relatively resistant to GAC treatment. As noted earlier, the GAC beds were in place for about three years at the time this study began. It was assumed that they were essentially exhausted with respect to adsorption capacity other than capacity produced by bio-regeneration. Biodegradation is known to occur in GAC beds (American Water Works Association, 1981), and the fact that the measured dissolved oxygen concentration in the effluent from the GAC beds was close to zero supports the presence of biological activity within the beds. Hence the GAC beds provide opportunities both for adsorption of the target compounds and biodegradation. Lincomycin, levofloxacin, trimethoprim, and ciprofloxacin, all of which exhibited high degrees of removal by GAC, were also readily removed by activated sludge treatment (see Fig. 3 and Table 1). Interestingly, some compounds, e.g. carbamazepine and erythromycin, which were not eliminated to any appreciable degree during activated sludge treatment, were eliminated quite well by the GAC, suggesting that there was still some sorption capability available in the beds, perhaps as a result of bio-regeneration. Adsorption of specific PPCPs onto GAC is dependent on the physical-chemical properties of the individual PPCPs. GAC tends to adsorb hydrophobic organic compounds; hydrophobicity is often characterized by the log of the octanol-water partition coefficient, Kow. A modified log Kow value (Kow0 ) was

Removal efficiency

100% 80%

-0.46 -1.39 1.66 1.88 0.66 -0.39

5225

KOW
1 þ 10^ ðpH  pKaÞ

Fig. 4 shows the percent removal of the targeted PPCPs that were detectable in the GAC influent and their corresponding log Kow0 values. Carbamazepine and erythromycin, with log Kow0 s of 3.05 and 2.45 respectively, exhibited high removal efficiencies while primidone and DEET, with respective log Kow0 s of 6.09 and 4.15, exhibited low removal efficiencies. Overall, however, no consistent pattern between log Kow0 and percent removal is apparent. Hence, it would appear that both adsorption and biodegradation contribute to the observed removal of PPCPs in the GAC beds. To assist in understanding the GAC removal results, supplementary batch adsorption tests were conducted using membrane effluent from the wastewater reclamation plant. 25 mg/L of pulverized F-400 GAC (the same carbon used in the full-scale plant) was added to the membrane effluent and mixed for 24 h, after which the pulverized carbon was separated from the suspension by filtration through 0.45 mm filters. The results are shown in Figure S5 in the Supporting Information by overlaying the removals during a single batch test with those obtained from the 12-month plant survey. The results confirm that primidone and DEET are the least readily removed by adsorption on activated carbon.

3.3.3.

Ozonation

Fig. 5 summarizes the removal efficiency of the PPCPs remaining in the GAC effluent by ozonation in the form of a series of box and whiskers plots. Also shown are the molecular structures for the PPCPs and their second-order rate constants with molecular ozone. As illustrated, ozonation effectively removed most of the remaining PPCPs in the GAC

-0.07

Log Kow '

60%

3.05 2.45

40% 20% 0%

9

10

3

7

8

9

11

10

9

Levofloxacin

diclofenac

ibuprofen

Trimethoprim

Ciprofloxacin

Erythromycin

Carbamazepine

Caffeine

Primidone

Lincomycin

N 8

-4.15 10 DEET

-6.09 -20%

Fig. 4 e Removal efficiency of targeted PPCPs by GAC. The number above the X-axis (N) refers to the number of samples that were analyzed and met the quality assurance criteria for reporting data. The values associated with each box or bar are the log of the modified octanol-water partition coefficients (log Kow0 ).

Fig. 5 e Removal of PPCPs by ozonation with their corresponding structures and second-order rate constants with molecular ozone.

5226

w a t e r r e s e a r c h 4 5 ( 2 0 1 1 ) 5 2 1 8 e5 2 2 8

effluent, although it is expected that most were transformed to other compounds. Sulfamethoxazole, primidone, caffeine and DEET were the only compounds routinely detected after ozonation; ciprofloxacin was detected on only two occasions. The removal of trimethoprim and carbamazepine was over 80%, and removal of sulfamethoxazole ranged from 67 to 94%. Rapid conversion of carbamazepine, trimethoprim, and sulfamethoxazole during ozonation has been reported by several groups of researchers (Nakada et al., 2007; Ternes et al., 2002). Nakada et al. (2007) demonstrated that 96% trimethoprim and 87% sulfamethoxazole were converted at an applied ozone dose of 3 mg/L and 27 min of contact in a secondary wastewater effluent after sand filtration (DOC ¼ 3.3 mg/L) at pH 7. An applied ozone dose of 0.5 mg/L was sufficient to convert 1 mg/ L carbamazepine spiked in surface water after flocculation (DOC ¼ 1.3 mg/L) at pH 7.8 (Ternes et al., 2002). This is consistent with our findings for an ozone dose of 1 mg/L and a DOC concentration of 4.5 mg/L. The removal of caffeine, primidone, and DEET exhibited a high degree of variation, ranging from no removal to 100% removal. This may be attributable to variations in the ozone dose, which ranged from 0.75 to 2.0 mg/L with an average value of 1 mg/L, or to variations in the influent water quality to the ozonation chamber. Trimethoprim, sulfamethoxazole, and carbamazepine all have amino groups, which are susceptible to chemical attack by ozone. The rate constants for the reaction of molecular O3 with these PhACs are 2.7  105, 2.5  106, and 3  105 M1s1, respectively (Dodd et al., 2006; Huber et al., 2003), as shown in Table 1 and Fig. 5. The rate constants of primidone and caffeine toward molecular O3 are low (1.0 and 0.8 M1s1, respectively) (Benitez et al., 2008; Rosal et al., 2009). The NH functional groups in primidone and the NeC double bonds in caffeine are the likely sites of ozone attack. Dodd et al. (2006) suggest that compounds with kO3/kOH (see Table 1) ratios less than 105 will generally be transformed to a large extent by OH radicals rather than by molecular ozone during wastewater ozonation. This corresponds to a rate constant for molecular ozone (kO3) of less than 104 M1s1, since kOH values tend to be on the order of 109 M1s1. While reactions with OH radicals could be a major mechanism contributing to the removal of primidone, DEET and caffeine by ozone, there are a large number of competing reactants for the OH radical in treated wastewater.

4.

Conclusions

Sixteen out of the nineteen targeted compounds were detected in the primary effluent in the wastewater reclamation plant. Most of compounds were found at concentrations on the order of hundreds of ng/L except caffeine and acetaminophen (w105 ng/L), ibuprofen (w104 ng/L), sulfamethoxazole and DEET (w103 ng/L). Only sulfamethoxazole, primidone, caffeine and DEET were frequently detected in the final effluent, but at concentrations on the order of 10e100 ng/L. After activated sludge treatment and membrane filtration, the concentrations of caffeine, acetaminophen, ibuprofen, DEET, tetracycline, and 17a-ethynylestradiol (EE2) had decreased by more than 90%. Erythromycin and carbamazepine, which

were resistant to biological treatment, were eliminated by 74 and 88%, on average, by GAC. Ozonation oxidized most of the remaining compounds by >60%. Primidone, DEET, and caffeine were not amenable to adsorption by GAC and ozonation. The results obtained in this full-scale plant assessment were generally consistent with previous findings from laboratory studies or in grab samples taken from full-scale wastewater treatment facilities, and with expectations based on physical-chemical characteristics of the compounds.

Acknowledgments We thank the management and operations personnel at the F. Wayne Hill Water Resources Center and the Gwinnett County Department of Public Utilities for financial support of this project and for their assistance with sample collection. We extend appreciation to Kate Bronstein and Shannon Weston who helped with the analytical methodology at the beginning of the project.

Appendix. Supplementary data Supplementary data associated with this article can be found, in the online version, at doi:10.1016/j.watres.2011.07.026.

references

American Water Works Association, 1981. An assessment of microbial activity on GAC. Journal of American Water Works Association 73, 447e454. Andreozzi, R., Canterino, M., Marotta, R., Paxeus, N., 2005. Antibiotic removal from wastewaters: the ozonation of amoxicillin. Journal of Hazardous Materials 122, 243e250. Batt, A.L., Kim, S., Aga, D.S., 2006. Enhanced biodegradation of iopromide and trimethoprim in nitrifying activated sludge. Environmental Science & Technology 40, 7367e7373. Benitez, F.J., Real, F.J., Acero, J.L., Sagasti, J.J., 2008. Oxidation of the Pharmaceutical Primidone by Single Oxidants (UV radiation and ozone) and Advanced Oxidation Processes. 236th ACS National Meeting, Philadelphia, PA. Benotti, M.J., Brownawell, B.J., 2007. Distributions of Pharmaceuticals in an Urban Estuary During both Dry- and Wet-Weather Conditions, pp. 5795e5802. Buerge, I.J., Poiger, T., Muller, M.D., Buser, H.R., 2003. Caffeine, an anthropogenic marker for wastewater contamination of surface waters. Environmental Science & Technology 37, 691e700. Carballa, M., Omil, F., Lema, J.M., 2007. Calculation methods to Perform mass Balances of micropollutants in sewage treatment plants. Application to pharmaceutical and personal care products (PPCPs). Environmental Science & Technology 41, 884e890. Clara, M., Strenn, B., Ausserleitner, M., Kreuzinger, N., 2004. Comparison of the behaviour of selected micropollutants in a membrane bioreactor and a conventional wastewater treatment plant. Water Science & Technology 50, 29e36. Dickenson, E.R.V., Drewes, J.E., Sedlak, D.L., Wert, E.C., Snyder, S. A., 2009. Applying surrogates and Indicators to Assess removal efficiency of Trace organic chemicals during chemical

w a t e r r e s e a r c h 4 5 ( 2 0 1 1 ) 5 2 1 8 e5 2 2 8

oxidation of wastewaters. Environmental Science & Technology 43, 6242e6247. Dodd, M.C., Buffle, M.O., vonGunten, U., 2006. Oxidation of antibacterial Molecules by aqueous ozone: moiety-specific reaction kinetics and application to ozone-based wastewater treatment. Environmental Science & Technology 40, 1969e1977. Federle, T.W., Kaiser, S.K., Nuck, B.A., 2002. Fate and effects of triclosan in activated sludge. Environmental Toxicology and Chemistry 21, 1330e1337. Gobel, A., McArdell, C.S., Joss, A., Siegrist, H., Giger, W., 2007. Fate of sulfonamides, macrolides, and trimethoprim in different wastewater treatment technologies. Science of the Total Environment 372, 361e371. Gobel, A., Thomsen, A., McArdell, C.S., Joss, A., Giger, W., 2005. Occurrence and sorption behavior of sulfonamides, macrolides, and trimethoprim in activated sludge treatment. Environmental Science & Technology 39, 3981e3989. Golet, E.M., Xifra, I., Siegrist, H., Alder, A.C., Giger, W., 2003. Environmental exposure assessment of fluoroquinolone antibacterial agents from sewage to soil. Environmental Science & Technology 37, 3243e3249. Hartig, C., Storm, T., Jekel, M., 1999. Detection and identification of sulphonamide drugs in municipal waste water by liquid chromatography coupled with electrospray ionisation tandem mass spectrometry. Journal of Chromatography A 854, 163e173. Hollender, J., Zimmermann, S.G., Koepke, S., Krauss, M., McArdell, C.S., Ort, C., Singer, H., von Gunten, U., Siegrist, H., 2009. Elimination of organic micropollutants in a municipal wastewater treatment plant Upgraded with a full-scale Postozonation followed by sand filtration. Environmental Science & Technology 43, 7862e7869. Howard, P.H., Meylan, W.M., 1997. Handbook of Physical Properties of Orgnanic Chemicals. Lewis Publishers. Huber, M.M., Canonica, S., Park, G.Y., von Gunten, U., 2003. Oxidation of pharmaceuticals during ozonation and advanced oxidation processes. Environmental Science & Technology 37, 1016e1024. Ikehata, K., El-Din, M.G., Snyder, S.A., 2008. Ozonation and advanced oxidation treatment of Emerging organic Pollutants in water and wastewater. Ozone: Science & Engineering 30, 21e26. Joss, A., Keller, E., Alder, A.C., Gobel, A., McArdell, C.S., Ternes, T., Siegrist, H., 2005. Removal of pharmaceuticals and fragrances in biological wastewater treatment. Water Research 39, 3139e3152. Joss, A., Zabczynski, S., Gobel, A., Hoffmann, B., Loffler, D., McArdell, C.S., Ternes, T.A., Thomsen, A., Siegrist, H., 2006. Biological degradation of pharmaceuticals in municipal wastewater treatment: proposing a classification scheme. Water Research 40, 1686e1696. Kasprzyk-Hordern, B., Dinsdale, R.M., Guwy, A.J., 2008. The occurrence of pharmaceuticals, personal care products, endocrine disruptors and illicit drugs in surface water in South Wales, UK. Water Research 42, 3498e3518. Kasprzyk-Hordern, B., Dinsdale, R.M., Guwy, A.J., 2009. The removal of pharmaceuticals, personal care products, endocrine disruptors and illicit drugs during wastewater treatment and its impact on the quality of receiving waters. Water Research 43, 363e380. Kesavan, P.C., Powers, E.L., 1985. Differential modification of oxic and anoxic components of radiation damage in Bacillus megaterium spores by caffeine. International Journal of Radiation Biology 48, 223e233. Kim, S., Eichhorn, P., Jensen, J.N., Weber, S., Aga, D.S., 2005. Removal of antibiotics in wastewater: effect of Hydraulic and solid Retention times on the Fate of tetracycline in the

5227

activated sludge process. Environmental Science & Technology 39, 5816e5823. Kimura, K., Hara, H., Watanabe, Y., 2007. Elimination of selected acidic pharmaceuticals from municipal wastewater by an activated sludge system and membrane Bioreactors. Environmental Science & Technology 41, 3708e3714. Kolpin, D.W., Furlong, E.T., Meyer, M.T., Thurman, E.M., Zaugg, S. D., Barber, L.B., Buxton, H.T., 2002. Pharmaceuticals, Hormones, and other organic wastewater contaminants in U. S. Streams, 1999e2000: a National Reconnaissance. Environmental Science & Technology 36, 1202e1211. Lindberg, R.H., Wennberg, P., Johansson, M.I., Tysklind, Mats, Andersson, B.A.V., 2005. Screening of human antibiotic Substances and Determination of Weekly mass flows in five sewage treatment plants in Sweden. Environmental Science & Technology 39, 3421e3429. Lindqvist, N., Tuhkanen, T., Kronberg, L., 2005. Occurrence of acidic pharmaceuticals in raw and treated sewages and in receiving waters. Water Research 39, 2219e2228. Lindsey, M.E., Meyer, M., Thurman, E.M., 2001. Analysis of Trace levels of sulfonamide and tetracycline antimicrobials in groundwater and surface water using solid-phase extraction and liquid Chromatography/Mass spectrometry. Analytical Chemistry 73, 4640e4646. Miao, X.S., Yang, J.J., Metcalfe, C.D., 2005. Carbamazepine and its metabolites in wastewater and in biosolids in a municipal wastewater treatment plant. Environmental Science & Technology 39, 7469e7475. Nakada, N., Shinohara, H., Murata, A., Kiri, K., Managaki, S., Sato, N., Takada, H., 2007. Removal of selected pharmaceuticals and personal care products (PPCPs) and endocrine-disrupting chemicals (EDCs) during sand filtration and ozonation at a municipal sewage treatment plant. Water Research 41, 4373e4382. Qiang, Z., Adams, C., Surampalli, R., 2004. Determination of ozonation rate constants for lincomycin and Spectinomycin. Ozone: Science & Engineering 26, 525e537. Reungoat, J., Macova, M., Escher, B.I., Carswell, S., Mueller, J.F., Keller, J., 2010. Removal of micropollutants and reduction of biological activity in a full scale reclamation plant using ozonation and activated carbon filtration. Water Research 44, 625e637. Rivera-Cancel, G., Bocioaga, D., Hay, A.G., 2007. Bacterial degradation of N, N-Diethyl-m-Toluamide (DEET): cloning and Heterologous Expression of DEET Hydrolase. Applied Environmental Microbiology 73, 3105e3108. Rosal, R., Rodrı´guez, A., Perdigo´n-Melo´n, J.A., Petre, A., Garcı´aCalvo, E., Gomez, M.J., Agu¨era, A., Ferna´ndez-Alba, A.R., 2009. Degradation of caffeine and identification of the transformation products generated by ozonation. Chemosphere 74, 825e831. Singer, H., Mu¨ller, S., Tixier, C., Pillonel, L., 2002. Triclosan: occurrence and Fate of a widely used Biocide in the aquatic environment: field measurements in wastewater treatment plants, surface waters, and lake sediments. Environmental Science & Technology 36, 4998e5004. Sithole, B.B., Guy, R.D., 1987. Models for tetracycline in aquatic environments. Water, Air, & Soil Pollution 32, 303e314. Snyder, S.A., Adham, S., Redding, A.M., Cannon, F.S., DeCarolis, J., Oppenheimer, J., Wert, E.C., Yoon, Y., 2007. Role of membranes and activated carbon in the removal of endocrine disruptors and pharmaceuticals. Desalination 202, 156e181. Song, W., Cooper, W.J., Peake, B.M., Mezyk, S.P., Nickelsen, M.G., O’Shea, K.E., 2009. Free-radical-induced oxidative and reductive degradation of N, N’-diethyl-m-toluamide (DEET): kinetic studies and degradation pathway. Water Research 43, 635e642.

5228

w a t e r r e s e a r c h 4 5 ( 2 0 1 1 ) 5 2 1 8 e5 2 2 8

Stanford, B.D., Weinberg, H.S., 2007. Isotope dilution for quantitation of steroid estrogens and nonylphenols by gas chromatography with tandem mass spectrometry in septic, soil, and groundwater matrices. Journal of Chromatography A 1176, 26e36. Suarez, S., Carballa, M., Omil, F., Lema, J.M., 2008. How are pharmaceutical and personal care products (PPCPs) removed from urban wastewaters? Reviews in Environmental Science and Biotechnology 7, 125e138. Suarez, S., Dodd, M.C., Omil, F., von Gunten, U., 2007. Kinetics of triclosan oxidation by aqueous ozone and consequent loss of antibacterial activity: relevance to municipal wastewater ozonation. Water Research 41, 2481e2490. Ternes, T.A., Herrmann, N., Bonerz, M., Knacker, T., Siegrist, H., Joss, A., 2004. A rapid method to measure the solid-water distribution coefficient (Kd) for pharmaceuticals and musk fragrances in sewage sludge. Water Research 38, 4075e4084. Ternes, T.A., Meisenheimer, M., McDowell, D., Sacher, F., Brauch, H.J., Gulde, B.H., Preuss, G., Wilme, U., Seibert, N.Z., 2002. Removal of pharmaceuticals during drinking water treatment. Environmental Science & Technology 36, 3855e3863. Ternes, T.A., Stuber, J., Herrmann, N., McDowell, D., Ried, A., Kampmann, M., Teiser, B., 2003. Ozonation: a tool for removal of pharmaceuticals, contrast media and musk fragrances from wastewater? Water Research 37, 1976e1982.

Vieno, N.M., Tuhkanen, T., Kronberg, L., 2005. Seasonal variation in the occurrence of pharmaceuticals in effluents from a sewage treatment plant and in the Recipient water. Environmental Science & Technology 39, 8220e8226. Voogt, P., Janex-Habibi, M.L., Sacher, F., Puijker, L., Mons, M., 2008. Development of a Common Priority List of Pharmaceuticals Relevant for the Water Cycle. IWA World Water Congress and Exhibition, Vienna, Austria. Westerhoff, P., Yoon, Y., Snyder, S., Wert, E., 2005. Fate of endocrine-Disruptor, pharmaceutical, and personal care product chemicals during Simulated drinking water treatment processes. Environmental Science & Technology 39, 6649e6663. Ye, Z., Weinberg, H.S., Meyer, M.T., 2007. Trace analysis of trimethoprim and sulfonamide, macrolide, quinolone, and tetracycline antibiotics in chlorinated drinking water using liquid chromatography electrospray tandem mass spectrometry. Analytical Chemistry 79, 1135e1144. Yu, J.T., Bouwer, E.J., Coelhan, M., 2006. Occurrence and biodegradability studies of selected pharmaceuticals and personal care products in sewage effluent. Agricultural Water Management 86, 72e80. Zwiener, C., Frimmel, F.H., 2003. Short-term tests with a pilot sewage plant and biofilm reactors for the biological degradation of the pharmaceutical compounds clofibric acid, ibuprofen, and diclofenac. The Science of the Total Environment 309, 201e211.