<<

UNIVERSITY OF CINCINNATI

Date: 13-Aug-2010

I, Ruth Marfil Vega , hereby submit this original work as part of the requirements for the degree of: Doctor of Philosophy in Environmental Science It is entitled: Abiotic Transformation of in Wastewater

Student Signature: Ruth Marfil Vega

This work and its defense approved by: Committee Chair: Makram Suidan, PhD Makram Suidan, PhD

George Sorial, PhD George Sorial, PhD

Margaret Kupferle, PhD, PE Margaret Kupferle, PhD, PE

Marc Mills, PhD Marc Mills, PhD

11/8/2010 1,041 Abiotic Transformation of Estrogens in

Wastewater

A Dissertation submitted to the

Graduate School

of the University of Cincinnati

in partial fulfillment of the

requirements for the degree of

Doctor of Philosophy

In the School of Energy, Environmental, Biological and Medical Engineering

By

Ruth Marfil-Vega

B.S. Chemistry, University of Valladolid, Spain, 2001

Committee Chair: Makram T. Suidan, Ph.D. ABSTRACT

The fate of seven : (E1), (E2), (E3), ethinylestradiol (EE2), (TEST), (AND), and

(PROG), in the presence of synthetic wastewater was studied in order to establish the role abiotic processes play in the elimination of these chemicals from the environment.

Comprehension of these mechanisms will foster the optimization of the existing technologies and the development of sustainable alternatives.

Distinctive behavior was encountered for the target compounds in accordance with their chemical structure, hence, different physico-chemical properties and reactivity.

Estrogenic compounds, comprising E1, E2, E3 and EE2, were found to undergo a catalytic transformation when contacted with a model vegetable material present in the synthetic wastewater. This transformation occurred in the absence of biological and enzymatic activity. On the other hand, the concentration of TEST, AND, and PROG stayed constant and in agreement with the spiked amount. The fastest transformation rate corresponded to E3, the least hydrophobic compound in the study. This may indicate that the catalytic reaction occurred in the aqueous phase. The contribution of steric and electronic factors, such as critical oxidation potential, in the reaction rate cannot be discarded; consequently, the hypothesis of a surface catalyzed reaction cannot be rejected.

14 14 The use of C4-estradiol ( C-E2) as model estrogenic compound corroborated the occurrence of a catalytic reaction, most likely through an oxidative coupling

ii mechanism. Under oxic conditions, the mass balance for radioactivity was closed after extended experimental periods (72 h), while the concentration of 14C-E2 measured by

Liquid Chromatography coupled with a Triple Quadrupole Mass Spectrometer

(LC/MS/MS) did not match the spiked one when analyzed independently in liquid and

solid phases. Furthermore, radioactivity was found to distribute in the aqueous phase as

well as extractable and non-extractable solids, suggesting that phenoxy radicals formed

on the phenolic ring of 14C-E2 could react among themselves (to form dimers), with the

functional groups present on the surface of the lignin-type vegetable model material

(resulting in covalent bonded matter), and with other chemicals species in the solution.

14 C4-estrone was also monitored in this study, but it was not detected in any sample.

Behavior encountered under anoxic conditions emphasized the role of molecular

oxygen in the catalytic process. In the absence of oxygen, the reaction was completely

halted; this was confirmed by the closure of the mass balance of 14C-E2, which was

performed by radioactivity and LC/MS/MS analyses. This indicated that estrogens were

transformed in an oxidation reaction catalyzed by some vegetable matter component and

in which the dissolved oxygen acted as oxidant. Preliminary investigations suggested that

manganese oxides could be acting as catalyst in this scenario.

iii

iv ACKNOWLEDGEMENTS

I would like to acknowledge my PhD advisor Dr. Makram T. Suidan, for his support and

guidance during these years. His mentorship has been really valuable, and I will never

forget any piece of advice he has given me.

I would also like to thank Dr. Margaret Kupferle, Dr. Marc Mills, and Dr. George Sorial

for serving in my committee. I am grateful for their suggestions to improve the quality of my research.

Many people have helped me conducting my research and also gave me advice whenever

I needed it; they are Dr. Campo Moreno, Dr. Brashear, Dr. Nakayama, and Dr.

Venkatapathy. I cannot forget Dr. Esperanza Quintana: she was my when I arrived in Cincinnati, and she has continued being great source of support and friendship.

Without the support of my friends, it would have been really difficult to complete this

dissertation; undoubtedly, a little piece of this work belongs to Cristina Jiménez

Betancourt. And there are many others that came to my mind while compiling the results

of my research… thank you to all the new friends I met in Cincinnati, and to the old ones

I left back home and around Europe.

And last, but not least, I would like to thank my family and my husband, for their love

and their unconditional support and encouragement. This work is dedicated to them:

Javier, Jesús, Dinesh, Mom… and Dad.

v TABLE OF CONTENTS

CHAPTER 1. OVERVIEW ______1

1.1 INTRODUCTION AND PROBLEM STATEMENT ______1 1.2 RESEARCH OBJECTIVES ______8 1.3 LAYOUT OF DISSERTATION ______9 1.4 REFERENCES ______10

CHAPTER 2. MATERIALS AND METHODS ______20

2.1 CHEMICALS ______20 2.2 SYNTHETIC FEED ______21 2.3 EXPERIMENTAL DESIGN ______21 2.4 ANALYTICAL METHODS ______21 2.4.1 SAMPLE PREPARATION OF AQUEOUS SAMPLES ______22 2.4.1.1 Extraction ______23 2.4.1.1.1 Initial extraction: SPE with C-18 (Chapter 3) ______23 2.4.1.1.2 Modified extraction: SPE with C-18 (Chapters 4 and 5) ______23 2.4.1.2 Clean-up: SPE with neutral Alumina (Chapters 3, 4 and 5) ______24 2.4.1.3 Derivatization procedure ______24 2.4.1.3.1 For GC/MS analysis (Chapter 3) ______24 2.4.1.3.2 For LC/MS/MS analysis (Chapters 4 and 5) ______26 2.4.2 SAMPLE PREPARATION OF SOLID SAMPLES ______26 2.4.2.1 Sample lyophilization (Chapter 3) ______27 2.4.2.2 Extraction ______27 2.4.2.2.1 Rotary tumbler extraction (Chapter 3) ______27 2.4.2.2.2 ASE extraction (Chapters 4 and 5) ______28 2.4.2.3 Clean-up ______29 2.4.2.3.1 Alumina clean-up followed by HPLC clean-up (Chapter 3) ______29 2.4.2.3.2 Alumina clean-up followed by C-18 clean-up (Chapters 4 and 5) ______31 2.4.2.4 Derivatization procedure ______32 2.4.2.4.1 For GC/MS analysis (Chapter 3) ______32 2.4.2.4.2 For LC/MS/MS analysis (Chapters 4 and 5) ______32 2.4.3 GC/MS ANALYSIS (CHAPTER 3) ______32 2.4.3.1 Method validation ______33 2.4.4 LC/MS/MS ANALYSIS (CHAPTERS 4 AND 5) ______34 2.4.4.1 Method validation ______35 2.4.5 RADIOACTIVITY ANALYSIS (CHAPTERS 4 AND 5) ______36 2.5 REFERENCES ______38

CHAPTER 3. ABIOTIC TRANSFORMATION OF ESTROGENS IN SYNTHETIC MUNICIPAL WASTEWATER: AN ALTERNATIVE FOR TREATMENT ______45

3.1 INTRODUCTION ______46

vii 3.2 MATERIALS AND METHODS ______49 3.2.1 REAGENTS AND CHEMICALS ______49 3.2.2 ANALYTICAL PROCEDURE ______50 3.2.3 EXPERIMENTAL DESIGN ______52 3.3 RESULTS AND DISCUSSION ______54 3.4 CONCLUSIONS ______62 3.5 REFERENCES ______64

CHAPTER 4. ASSESSMENT OF THE ABIOTIC TRANSFORMATION OF ESTROGENS IN A SYNTHETIC WASTEWATER MATRIX ______82

4.1 INTRODUCTION ______83 4.2 MATERIALS AND METHODS ______85 4.2.1 REAGENTS AND CHEMICALS ______85 4.2.2 ANALYTICAL PROCEDURE ______86 4.2.2.1 RADIOACTIVITY ANALYSIS ______87 4.2.2.2 LC/MS/ANALYSIS ______87 4.2.3 EXPERIMENTAL DESIGN ______88 4.3 RESULTS AND DISCUSSION ______89 4.4 CONCLUSIONS ______97 4.5 REFERENCES ______99

CHAPTER 5. ROLE OF MOLECULAR OXYGEN IN THE ABIOTIC TRANSFORMATIONS OF ESTROGENS IN ENGINEERED SYSTEMS ______110

5.1 INTRODUCTION ______111 5.2 MATERIALS AND METHODS ______113 5.2.1 REAGENTS AND CHEMICALS ______113 5.2.2 ANALYTICAL PROCEDURE ______114 5.2.3 EXPERIMENTAL DESIGN ______116 5.3 RESULTS AND DISCUSSION ______118 5.4 CONCLUSIONS ______124 5.5 REFERENCES ______126

CHAPTER 6. SUMMARY, CONCLUSIONS, AND FUTURE WORK ______138

viii LIST OF TABLES

CHAPTER 1 Table 1-1. Physico-chemical properties (Liu et al. 2009a; SRC PhysProp Database) ..... 18

CHAPTER 2 Table 2-1. Physico-chemical properties (Liu et al. 2009; SRC PhysProp Database) ...... 40 Table 2-2. Detailed composition of the concentrated synthetic feed...... 41

CHAPTER 3 Table 3-1. Detailed composition of the concentrated synthetic feed...... 69 Table 3-2. Physico-chemical properties (Liu et al. 2009; SRC PhysProp Database) ...... 70 Table 3-3. Experiments description. Model parameters for each ...... 71 Table 3-4. Percentage of concentration recovered from solids extraction ...... 72

CHAPTER 5 Table 5-1. Summary of batch experiments...... 130

ix LIST OF FIGURES

CHAPTER 1 Figure 1-1. Structure of the target compounds...... 19

CHAPTER 2 Figure 2-1. Structure of the target compounds...... 42 14 Figure 2-2. Structure of 17β- C4-estradiol...... 43 Figure 2-3. Structure of dansyl chloride...... 44

CHAPTER 3 Figure 3-1. Structure of the target compounds...... 73 Figure 3-2. Fractional recovery of E1, E2, E3, EE2 and TEST. Results from experiment 1 (black circles) and 2 (bar plot) (Table 3-3). Initial concentration: 4800 ng L-1 with -1 the addition of 20 mg L NaN3...... 74 Figure 3-3. Rate of disappearance of E2. Model obtained as combination of experimental results from experiments with initial concentration 1200 ng L-1 (black circles) and 4800 ng L-1 (grey circles) (experiments 2 and 3 in Table 3-3). Solid line: model fitting; black squares: results from experiment 4a (Table 3-3); white squares: results from experiment 4b (Table 3-3)...... 75 Figure 3-4. Rate of disappearance of E1. Model obtained as combination of experimental results from experiments with initial concentration 1200 ng L-1 (black circles) and 4800 ng L-1 (grey circles) (experiments 2 and 3 in Table 3-3). Solid line: model fitting; black squares: results from experiment 4a (Table 3-3); white squares: results from experiment 4b (Table 3-3)...... 76 Figure 3-5. Rate of disappearance of E3. Model obtained as combination of experimental results from experiments with initial concentration 1200 ng L-1 (black circles) and 4800 ng L-1 (grey circles) (experiments 2 and 3 in Table 3-3). Solid line: model fitting; black squares: results from experiment 4a (Table 3-3); white squares: results from experiment 4b (Table 3-3)...... 77 Figure 3-6. Rate of disappearance of EE2. Model obtained as combination of experimental results from experiments with initial concentration 1200 ng L-1 (black circles) and 4800 ng L-1 (grey circles) (experiments 2 and 3 in Table 3-3). Solid line: model fitting; black squares: results from experiment 4a (Table 3-3); white squares: results from experiment 4b (Table 3-3)...... 78 Figure 3-7. Percentage of concentration recovered from solid phase for each estrogen. . 79 Figure 3-8. Fractional recovery of E1, E2, E3 and EE2. Results from experiment 4a and 4b (Table 3-3). Total recovery (circle), recovery in liquid phase (triangle) and solid phase (square)...... 80 Figure 3-9. Fractional recovery of TEST, AND and PROG. Results from experiment 4a and 4b (Table 3-3). Total recovery (circle), recovery in liquid phase (triangle) and solid phase (square)...... 81

CHAPTER 4 14 Figure 4-1. Structure of 17β- C4-estradiol...... 104 Figure 4-2. Analytical protocol...... 105

x Figure 4-3. Percentage recovered of E2 vs time. Solid symbols: E2...... 106 14 Figure 4-4. Concentration of 17β- C4-estradiol vs time, from radioactivity measurement (left side of bar) and LC/MS/MS analysis (right side of bar), in liquid (L), extractable solid (ES) and non-extractable solid (NS) phases...... 107 Figure 4-5. Proposed scheme of the abiotic transformation of E2...... 108 14 Figure 4-6. Concentration of 17β- C4-estradiol and unidentified byproduct(s) vs time in liquid (L), extractable solid (ES) and non-extractable solid (NS) phases...... 109

CHAPTER 5 Figure 5-1. Structure of sterane and target estrogens...... 131 Figure 5-2. Analytical protocol...... 132 Figure 5-3. (a) Percentage of E2 recovered over time, (b) Percentage of TEST recovered over time...... 133 Figure 5-4. (a) Percentage of radioactivity over time under oxic and anoxic conditions (14C-E2), (b) Percentage of concentration over time under oxic and anoxic conditions, measured by LC/MS/MS, (14C-E2) (c) Percentage of concentration over time under anoxic conditions, measured by LC/MS/MS (E2)...... 134 Figure 5-5. Comparison of % concentration measured by LSC and LC/MS/MS over time under oxic and anoxic conditions (target compound 14C-E2)...... 135 Figure 5-6. Concentration of metals in raw rabbit food...... 136 Figure 5-7. Percentage of metal leached into solution over time...... 137

xi Chapter 1. OVERVIEW

1.1 INTRODUCTION AND PROBLEM STATEMENT

Endocrine Disrupting Chemicals (EDCs) comprise a diverse group of

heterogeneous contaminants, with the common effect of altering the normal functioning

of the endocrine system of living organisms. Different organizations such as the World

Health Organization, U.S. Environmental Protection Agency (US EPA), and the

European Commission have not yet provided consistent definitions or classifications for

these compounds (Hester and Harrison, 1999; Birkett and Lester, 2003), due to the vast

diversity of pollutants involved (e.hormone- Endocrine Disrupting Chemicals). The

definition adopted by the US EPA in 1997 states that an is "an

exogenous agent that interferes with the synthesis, , transport, binding, action, or

elimination of natural hormones in the body which are responsible for the maintenance or

homeostasis, reproduction, development, and/or behavior."

Silent Spring (1962) and Our Stolen Future (1996) introduced and spread the concept of endocrine disruption to the general public. Since the late 1970’s, a scientific

community comprised mainly by biologists and environmental chemists worked

toward the comprehension of the endocrine disruption phenomena (Sumpter and Johnson,

2008). Nevertheless, environmental engineers did not focused their efforts on the removal

of these contaminants from the environment until the publication of the surveys by

Daughton and Ternes (1999), and Kolpin et al. (2002), regarding the presence of EDCs in

the aquatic environment.

1

Impact of EDCs on wildlife encompasses disturbance of the immunological

system and fertility, reproductive failure due to thinning of eggshells, and

masculinization, and altered sexual development, among many others (Hester and

Harrison, 1999; e.hormone- Wildlife Effects). The effects these chemicals may induce in

humans are not completely known. Reductions in sperm count and quality, increased

incidence of certain types of cancer (mainly related to the reproductive system), and

congenital malformations, altered sex ratios and neurological effects have been

associated with exposure through diverse routes to EDCs (Hester and Harrison, 1999;

U.S. EPA, 2005).

Among the EDCs, steroidal hormones constitute one of the most significant

groups. These hormones include estrogens, , and progestins (Fig. 1-1). Their

importance lies on their high disrupting (Auriol et al., 2006) and their natural

occurrence in the of humans and animals (Liu et al., 2009b). But they also

originate from man-made sources like – products of the pharmaceutical industry. A

majority of contraceptive formulation uses ethinylestradiol as the active ingredient and its

consumption is expected to expand from the western countries to a global scale. Also, a

combination of estrogens and progestins is prescribed for the treatment of menopausal

symptoms (naturally occurring or surgically induced). Steroidal hormones are also used

as growth promoters in animals.

2 Water bodies used as source water for drinking represent the most significant

exposure route for humans and animals to estrogens and other steroidal hormones.

Although estrogens are typically found in water bodies in the low ng L-1 concentration

range, their disrupting effects on fish and other aquatic life are well documented (Auriol

et al., 2006; Joss et al., 2006; Bolong et al., 2009; Cooney, 2009). Recent surveys of

EDCs in drinking water suggest that the concentrations found are safe for human

consumption, but there are still concerns about long-term exposure to low-levels of these

chemicals (Benotti et al., 2009; Cooney, 2009). In an effort to address these concerns, US

EPA included in its Contaminant Candidate List 3, published in 2009, several estrogenic

compounds (α- and β-estradiol (E2), , , estriol (E3), estrone (E1),

ethinylestradiol (EE2), and ), as well as one progestin (norethindrone). An

immediate consequence of this regulatory decision would be that these compounds would

require regulation under the Safe Drinking Water Act; hence, a thorough understanding

of their fate and behavior in the environment is needed to reduce the risk of

contamination of the drinking water and its sources.

As result of their natural origin, steroidal hormones are released into the water

bodies via human and animal ; this fact minimizes the possibility of source

control as a remediation strategy (Joss et al., 2006) and places the entire responsibility for

their removal to wastewater treatment plants (WWTPs). Furthermore, their therapeutic

uses elevate and other healthcare facilities as well as Confined Animal Feeding

Operations to prominent point sources of these chemicals.

3 WWTPs are one of the most important sources of estrogens into the environment

(Bolong et al., 2009). Conventional WWTPs are designed for the elimination of nutrients and solids (Auriol et al., 2006); however, only partial removal of EDCs from the aqueous stream is achieved (Khanal et al., 2006). In 1999, Ternes et al. published the first study on the presence of estrogens in WWTPs in Germany and Canada. In this study E1, E2, and EE2 were found in several samples at concentrations between 15 to 70 ng L-1. More

recent studies showed concentrations of E2 at 6–14 ng L-1 in the influent and less than 5

ng L-1 in effluent samples from facilities in Canada (Lishman et al., 2006), while E1 was

found at slightly higher concentrations (influent: 16–49 ng L-1; effluent: 8 ng L-1 after

conventional activated sludge treatment). Similar results are reported in Sweden (Zorita

et al., 2009), with EE2 below 10 ng L-1 (limit of quantification), but only after tertiary

treatment. Also in agreement are values obtained in Australia (Braga et al., 2005), where

55, 22, and <5 ng L-1 of E1, E2, and EE2, respectively, were found in the influent of the

treatment plant. Janex-Habibi et al. (2009) published a survey of E1, E2, (isomers α and

β) and EE2 in thirteen wastewater treatment plants located in six countries. The concentrations measured in the raw water were in agreement with those reported in previous studies. While E2 was not found in effluents, E1 was found between 1 and 73 ng L-1, and EE2 was present in 4 out of 18 samples (maximum concentration was 2.8 ng

L-1). Although E3 is rarely targeted in surveys, it has also been found in sewage influents

in Italy at levels between 23 and 48 ng L-1 and <1 ng L-1 in the effluent (Laganà et al.,

2004). In Austrian utilities, the amount found in the influent varied from 23, 320, and 600

ng L-1 (Clara et al., 2005), with the first plant being the only one with a detectable concentration after water treatment (activated sludge + activated sludge). Even though the

4 concentrations reported are very low, endocrine disrupting effects have been found in fish

exposed to those levels, in the low ng L-1 range (Auriol et al., 2006; Joss et al., 2006;

Bolong et al., 2009; Cooney, 2009).

Due to their moderate hydrophobic character (kow values reported in Table 1-1),

estrogens are expected to concentrate in sludges generated during wastewater treatment,

and in impacted soils and sediments (Jones-Lepp and Stevens, 2007; Heidler and Halden,

2008). Very limited data are reported in the literature on the effect of sludge stabilization on estrogens concentration because of the challenges faced in their analysis (Khanal et al., 2006). Under aerobic digestion, E2 seems to have similar degradation rates as under anaerobic digestions, while rates for E1 and EE2 were much higher aerobically (Auriol et al., 2006). After acclimation, however, removal efficiencies exceeding 80% can be obtained anaerobically (Carballa et al., 2007).

Researchers did not start routinely analyzing estrogens and other EDCs

independently in aqueous and solid phases. This was due to the analytical challenges

facing their determination at trace levels in the complex matrices under investigation.

Consequently, the presence of these chemicals in the sludge phase was indirectly

determined, or not considered at all in the majority of the studies ( Kinney et al., 2006;

Heidler and Halden, 2008). The lack of accurate information keeps unresolved the

question of whether physico-chemical properties (kow or koc and water solubility) are

sufficient to predict the fate of estrogens (Fürhacker et al., 1999; Kinney et al., 2006) in

solid matrices (Xia et al., 2005). Also, the possible contribution of abiotic processes to

5 the overall removal of these contaminants has been hindered by these indirect estimations. Furthermore, the role of sludge treatment on the re-introduction of estrogens to the environment is not fully understood (Harrison et al., 2006). Recent work (Carballa et al., 2007; Carballa et al.2008; Patureau et al., 2008) utilizing newer, more sensitive analytical instrumentation have provided insightful information regarding the fate of estrogens in sludge and biosolids.

Advanced technologies that include chlorination, ozonation, and other advanced oxidation processes, as well as those technologies utilizing catalytic (chemical or enzymatic) processes are under investigation with the goal to improve the effectiveness of conventional treatments. Preliminary data suggest these technologies are efficient for the removal of estrogens and could constitute a short-term solution (Joss et al., 2008).

Lack of feasibility studies of full-scale operations as well as lack of knowledge of the estrogenicity of the by-products generated (Auriol et al., 2006) are current drawbacks for the consideration of these technologies for the long-term management of estrogenic contamination. Additionally, it is economically prohibitive at the present time for implementation of advanced oxidation techniques in conventional wastewater treatment

(Liu et al., 2009a). Therefore, the necessity of optimizing existing wastewater treatment processes for the removal of these chemicals and the development of new cost- and energy-efficient processes is a priority.

Soil and sediments can also be impacted by wastewater discharges, agricultural run-off, and sludge and manure disposal (Fan et al., 2008; Stumpe and Marschner, 2009).

Similarly to the problems listed in the case of sludge and biosolids (analytical difficulties

6 and indirect characterization of adsorption), inaccurate estimations of adsorption and

underestimation of potential abiotic transformations (Sarmah et al., 2008) occurred in the

study of the fate of estrogens in these matrices. Consequently, erroneous results may be

generated for the estimation of the potential contamination of surface and groundwater

and, hence, for water recharge and reuse.

Unexpected decreases in concentration or increases in adsorption capacity of

estrogens in natural solid matrices have been reported (Shore et al., 1993; Lai et al., 2000;

Lee et al., 2003; Yu et al., 2004; Casey et al, 2005; Fan et al., 2007; Sarmah et al., 2008),

but with little or no justification and with most studies drawing conclusions based on

aqueous phase measurements, exclusively. Possible causes for the observed phenomena

are enhanced adsorption onto solid materials such as clays (Lee et al., 2003; Esperanza et

al., 2007), and/or abiotic reaction with any agent present, including some groups of (Lee et al., 2003; Hanselman et al., 2003; Gianfreda and Rao, 2004).

Although the abiotic transformations of phenolics have been extensively studied

in soils, sediments, and other engineered systems (Colarieti et al., 2002; Hanselman et al.,

2003; Lee et al., 2003; Yu et al., 2004; Sheng et al., 2009), to date, scarce references are found in the literature concerning estrogens (Sheng et al., 2009) in those scenarios. In

regard to the abiotic transformation of estrogens in wastewater, only studies under

laboratory conditions have been published, focusing more on the action of enzymes

(Auriol et al., 2007a; Auriol et al., 2007b; Blánquez and Guieysse, 2008) than on

chemical catalysts (Rudder et al., 2004; Forrez et al., 2009).

7 In summary, a thorough knowledge of the underlying mechanisms involved in the removal of estrogens during wastewater transport and treatment is still needed. Individual contribution of biodegradation, adsorption, and abiotic processes to the overall elimination has to be determined for the development of sustainable wastewater treatment technologies in order to help minimize health and environmental risks derived from exposure to EDCs. Elucidation of the abiotic processes and other biogeochemical redox transformations occurring in sewage will provide an alternative route for the advance in removal technologies (Young and T. Borch, 2009). Furthermore, the understanding of abiotic transformation of estrogens as representative compounds of phenolic EDCs can be extrapolated to other micropollutants with similar chemical structure (BPA and alkylphenol surfactants, for example).

1.2 RESEARCH OBJECTIVES

The objective of this study is to acquire a thorough understanding of the abiotic transformation of estrogens in wastewater and related matrices and apply it to the implementation of current wastewater treatment technologies. To fulfill this goal, experimentation was planned to accomplish the specific targets:

• Identify the potential abiotic and physico-chemical processes involved in

the elimination of estrogens from the environment.

• Characterize the abiotic conversion of estrogens in the presence of

synthetic wastewater.

• Establish the ultimate agent promoting the catalysis of estrogens.

8 • Determine the influence of environmental variables, such as presence of

molecular oxygen, in the occurrence of the catalytic reaction involved in

the transformation of estrogens.

1.3 LAYOUT OF DISSERTATION

Five chapters are included in this dissertation, in addition to the present Overview.

Chapter 2 comprises a summary of the experimental methods utilized. In Chapter 3, the initial work is oriented to identify the nature of the process depleting the estrogens in a synthetic wastewater. Moreover, a mathematical model to characterize the transformation of estrogens is developed. Chapter 4, by means of using radiolabeled estrogens, is devoted to the authentication of the catalytic reaction involved in the abiotic conversion of the estrogens. A comparison of the results obtained under oxic and anoxic conditions to establish the influence of the presence of molecular oxygen in the catalysis of estrogens, is the focus of Chapter 5. Finally, conclusions and recommendations for future work are integrated in Chapter 6.

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17 Table 1-1. Physico-chemical properties (Liu et al. 2009a; SRC PhysProp Database)

WATER SOLUBILITY, COMPOUND -1 pka mg L kOW E1 10.5 30 3.13 E2 10.7 3.6 4.01 E3 10.4 441 2.45 EE2 10.4 11 3.67 TEST NA 23 3.32 AND NA 58 2.75 PROG NA 8.8 3.87

18 Figure 1-1. Structure of the target compounds.

O OH

H H

H H H H

HO HO 17β-Estradiol (E2) Estrone (E1) OH OH

H OH H

H H H H

HO HO Estriol (E3) 17α-Ethinylestradiol (EE2)

OH O

H H

H H H H

O O

Testosterone (TEST) O Androstenedione (AND)

H

H H

O Progesterone (PROG)

19 Chapter 2. MATERIALS AND METHODS

2.1 CHEMICALS

The first part of this work focused on the study of the following seven

compounds: E1 (99%), E2 (> 98%), E3 (99%), EE2 (> 98%), TEST (99%), AND (98%),

and PROG (> 99%). These compounds were obtained from Sigma-Aldrich (Milwaukee,

WI). Their chemical structure and main physicochemical properties (water solubility,

octanol-water partition coefficient, and pKa) are provided in Fig. 2-1 and Table 2-1. To

13 determine efficiency of the analytical procedure, d4-estrone (d4-E1; Sigma-Aldrich), C2-

13 estradiol ( C2-E2; Cambridge Isotope Laboratories Inc., Andover, MA), d3-estriol (d3-

E3; C/D/N Isotopes Inc., Canada), d4-ethinylestradiol (d4-EE2; C/D/N Isotopes Inc.,

Canada), and d3-testosterone (d3-TEST; Sigma-Aldrich) were used as surrogates. For the

Gas Chromatography/Mass Spectrometry (GC/MS) analysis, 5α- (> 99%) and

5α-cholestane (98%), from Sigma-Aldrich, served as internal standards.

For the experiments in which E2 was used as model compound, the non-

14 radiolabeled standard was the same as stated above. The radiolabeled standard, 17β- C4-

14 -1 estradiol ( C4-E2) (Fig. 2-2), with an activity of 55 mCi mmol and 98% purity, was purchased from American Radiolabeled Chemicals Inc. (Saint Louis, MO). d4-EE2

(C/D/N Isotopes Inc., Canada) served as surrogate. Dansyl chloride (Fig. 2-3) (from

Sigma Aldrich, Milwaukee, WI) and sodium bicarbonate (NaHCO3) were used for the

derivatization of the analytes by Liquid Chromatography with tandem Mass Spectrometry

detection (LC/MS/MS).

20 2.2 SYNTHETIC FEED

A synthetic wastewater was used in this study. The detailed composition is presented in Table 2-2. Additional information about its preparation can be found in the work published by Esperanza et al. (2004; 2007). This medium-strength synthetic wastewater (Metcalf and Eddy, 2003) was created to mimic municipal wastewater influent by containing soluble and non-soluble organic materials. The use of a synthetic feed provides a reproducible composition of the influent and this allows a better control on the rest of the experimental variables.

For some of the experiments, only isolated components of the synthetic feed were employed as matrix. These components are in the same concentration as the listed in

Table 2-2.

2.3 EXPERIMENTAL DESIGN

A detailed description of the batch experiments that were performed to accomplish the goals of the present study is included in Chapters 3, 4, and 5.

2.4 ANALYTICAL METHODS

Liquid and solid phases of the synthetic wastewater matrix used in this study were separated in all experiments by filtration with 1.2 μm pore size glass fiber filters. This step was completed after the phases were acidified to pH= 2 with hydrochloric acid. Each matrix was analyzed independently in all sampling events in order to obtain an accurate

21 mass balance for each of the target compounds. To avoid losses due to adsorption to glass surfaces, all the glassware used was silanized (Sylon CT: 5% dimethyldichlorosilane in toluene, Supelco).

2.4.1 SAMPLE PREPARATION OF AQUEOUS SAMPLES

For the batch experiments described in Chapter 3, methods developed by

Esperanza et al. (2004; 2007) were used in the first three sets of experiments. The appropriate surrogate compounds were added after filtration and the samples were extracted by Solid Phase Extraction (SPE) using C-18 cartridges (Supelclean ENVI-18

SPE, volume 6 mL, bed weight 0.5 g, Supelco). The SPE extracts were subsequently cleaned with neutral alumina (LC-Alumina-N SPE, volume 3 mL, bed weight 1 g

Supelco), derivatized in two steps with methoxyamine hydrochloride (MOX) and 10% trimethylchlorosilane (TMCS) in N,O-Bis(trimethylsilyl)trifluoroacetamide (BSTFA), and finally analyzed by GC/MS (Agilent 6890 GC/5973 MS detector) in Single Ion

Monitoring (SIM) mode.

The work included in Chapters 4 and 5 was done using a modification of the method described above. A slight modification of the SPE with C-18 was implemented, and the final detection was done by LC/MS/MS. To improve the sensitivity of the detection method, the analytes were derivatized with dansyl chloride and NaHCO3.

22 2.4.1.1 Extraction

2.4.1.1.1 Initial extraction: SPE with C-18 (Chapter 3)

The C-18 cartridges were conditioned with 10 mL methanol and 20 mL Super Q water. For samples with a volume larger than 200 mL, 1% (v/v) of methanol was added prior extraction; then the samples were loaded at approximately 4 ml min-1. After loading the samples, the bottles were rinsed with 50 mL Super Q water and the rinse was loaded at the same rate. Next, the cartridges were dried under vacuum for 15 minutes. The cartridges were eluted with 10 mL of methanol. The final extracts were dried-up under a gentle nitrogen stream in a water bath (at 40 °C) and reconstituted in 0.2 mL dichloromethane (DCM) and 0.8 mL iso-octane for further clean-up with neutral alumina.

2.4.1.1.2 Modified extraction: SPE with C-18 (Chapters 4 and 5)

The C-18 cartridges were conditioned with 10 ml of each of the following solvents: acetone, methanol, and 20 ml Super Q water. Samples were then loaded at approximately 4 ml min-1 and the bottles were rinsed with 30 mL Super Q water. Before eluting the target compounds with 10 mL acetone, cartridges were washed with 5 mL of freshly prepared 35% methanol in Super Q water and dried under vacuum for 15 minutes.

The final extracts were dried-up under a gentle nitrogen stream in a water bath (at 40 °C) and reconstituted in 0.2 mL DCM and 0.8 mL iso-octane for further clean-up with neutral alumina.

23 2.4.1.2 Clean-up: SPE with neutral Alumina (Chapters 3, 4 and 5)

In this case, cartridges were conditioned with 9 mL of 30% methanol in acetone,

and 9 mL of 20% DCM in iso-octane. The 1 mL extract obtained after the SPE with C-18

were transferred to the cartridge, and the vials were rinsed three times with 0.5 mL each

of 20% DCM in iso-octane. The samples combined with the rinses were loaded by gravity, 9 mL hexane were used for washing the cartridges, and finally, the elution was done with 9 mL 30% methanol in acetone. The final extracts were dried down to approximately 1 mL under a gentle nitrogen stream in a water bath (at 40 °C) The samples were then transferred to 2 mL micro-reaction vessel. The vials were rinsed three times with 0.5 mL each of 30% methanol in acetone and the rinses were combined with the samples in the micro-reaction vessels.

2.4.1.3 Derivatization procedure

2.4.1.3.1 For GC/MS analysis (Chapter 3)

The derivatization consisted of two different reactions. The purpose of the first reaction (with MOX) was to protect the ketone group present in E1, TEST, AND, and

PROG to minimize the formation of two isomers in the latter reaction. The objective of the second reaction, with a mixture of TMCS and BSTFA, was to form the more volatile trimethylsilylated derivatives of the seven steroids.

The samples were dried-up under a gentle nitrogen stream in a water bath (at 40

°C). 50 µL of a solution of 15% (w/v) MOX in pyridine were added to reconstitute the residue. The combination was reacted for 4 h at 70 °C in a heating block. After the vials

24 cooled down to room temperature, the reaction mixture was dried-up under a gentle

nitrogen stream. 50 µL of dry pyridine were added to redissolve the extracts, and then and 100 µl of 10% TMCS in BSTFA were added. The silylation reaction took place for

15 h at 70 °C in a heating block.

Samples were kept in the reaction solution until injection in the GC/MS. Prior to injection, the samples were dried under a gentle nitrogen stream and reconstituted with

0.2 mL of 20% DCM in hexane plus 5% (v/v) BSTFA. 10 µL of the internal standards

(5α-androstane and 5α-cholestane) stock (with a concentration of 25 ng each µL) were

added, and finally the samples were transferred to the injection vials.

The pertinent calibration curve was done analogously to the methodology

described for the samples. Relevant amounts of surrogates and target compounds were

spiked into 1 mL of acetone to prepare a series of 6 standards with concentrations ranging

from 10 to 500 µg L-1. After this step, 4 µl of an in-house concentrated vegetable extract

were added to account for the matrix effect. After drying-up the solvent under a gentle

nitrogen stream in a water bath (at 40 °C), the standards were derivatized and prepared

for injection as described above. Finally, at least one standard check was derivatized

along with the samples in each heating block used to process all samples generated in

each experiment.

25 2.4.1.3.2 For LC/MS/MS analysis (Chapters 4 and 5)

For the LC/MS/MS analysis, the derivatization reagent selected was dansyl

chloride, which reacts with the phenol group of the estrogens to form a fluorescent

derivative. These derivatives are more easily fragmented in the electrospray than the

underivatized estrogens, hence, better sensitivity can be achieved.

The samples were dried under a gentle nitrogen stream in a water bath (at 40 °C).

Two reagents were added sequentially: first, 100 µL of NaHCO3 0.1 M were added to

reconstitute the samples to act as buffer of the dansylating reaction, and second, 200 µL

of dansyl chloride in acetone (1 mg mL-1) was added. The reaction took place for 15 min at 60 °C in a heating block. After the reaction mixture cooled down to room temperature,

0.4 mL of injection solvent (50% of methanol in water) were added.

The calibration curve and calibration checks standards were prepared analogously

to the samples for each batch experiment performed. The pertinent surrogates and target

analytes were spiked into 1 mL of acetone. After evaporating the solvent under a gentle

nitrogen stream in a water bath (at 40 °C), the standard procedure was followed. The

calibration standards covered a range of concentration from 7 to 700 µg L-1, and

calibration checks were prepared in each batch of samples.

2.4.2 SAMPLE PREPARATION OF SOLID SAMPLES

Similarly to the preparation of aqueous phase samples, in the case of solid

samples, the methodologies used to analyze the non-soluble components of the synthetic

26 feed, along with the filters, were modified over the course of the study. Initially, for all

the experiments (except the last one, included in Chapter 3), a traditional continuous

extraction in a tumbler were carried out. The solid samples collected in the last

experiment in Chapter 3 and all the later experiments described in Chapters 4 and 5 were extracted in an Accelerated Solvent Extractor (ASE). At the same time, the subsequent clean-up steps were modified: the original clean-up by High Performance Liquid

Chromatograph (HPLC) equipped with a fraction collector used by Esperanza et al.

(2007) was substituted with a SPE with C-18 clean-up. Another major modification of the sample preparation procedure is that in the experiments included in Chapter 3, the samples were lyophilized prior to extraction. After proper testing, it was concluded that

this step was not necessary when the samples were extracted in the ASE.

2.4.2.1 Sample lyophilization (Chapter 3)

After filtration, the solids along with the grass fiber filters were placed

individually in silanized glass vials. The samples were then frozen at -80 °C and kept

overnight at that temperature. Finally, the frozen samples were lyophilized using a freeze-

dryer (Labconco Freeze-dry system/Freezone 4.5). To ensure the complete dryness of the

samples, they were kept in the freeze-dryer for up to 72 h.

2.4.2.2 Extraction

2.4.2.2.1 Rotary tumbler extraction (Chapter 3)

Subsequent to collecting the vials from the freeze-dryer, the pertinent surrogates

were spiked to each of them. 7 mL of methanol were added to each sample and they

27 were placed in a rotary tumbler in a controlled temperature room at 35 °C. After 2 h of tumbling, the solvent was transferred to a silanized vial using a Pasteur pipette partially filled with glass wool and sodium sulfate. The combination of wool and sodium sulfate was used to avoid the presence of solids in the final extract. Methanol (7 mL) were added again to the samples that were extracted in the tumbler for another 4 h at 35 °C and the solvent was transferred as described before. This procedure was repeated one more time, resulting in a total extraction time of 10 h and an initial volume of methanol of 21 mL.

The final extracts were dried under gentle nitrogen stream in a water bath (at 40 °C) and reconstituted in 0.2 mL dichloromethane (DCM) and 0.8 mL iso-octane for further clean- up with neutral alumina.

2.4.2.2.2 ASE extraction (Chapters 4 and 5)

To assure that the maximum extractable mass of estrogens was being recovered from the solids, a new extraction methodology was developed and optimized using an

ASE (ASE 200, Dionex Corporation). The main parameters that were tested included: number of extraction cycles, temperature, pressure, and solvent (acetone, methanol, hexane, DCM, and mixtures of methanol and acetone: 50:50 (v/v), 25:75 (v/v), and 75:25

(v/v). The size of the extraction cells chosen was 11 mL in order to minimize the amount of solvent and because the small size of the samples.

The following conditions were found to provide the best results (considering the surrogate recoveries and the cleanliness of the correspondent chromatograms): 2

28 extraction cycles, 150 °C, 1500 psi, and methanol:acetone 25:75 (v/v). These extraction conditions were employed in the experiments included in Chapters 4 and 5.

Once the samples were vacuum-filtered, and the solids along with the filters were dried, they were wrapped and placed into the ASE cells. The correspondent surrogates were spiked into the filters and approximately 0.2 g of diatomaceous earth were added to remove the traces of water trapped in the solids. The samples were extracted with the conditions stated above and the final extracts were collected in silanized vials. The extracts were dried under a gentle nitrogen stream in a water bath (at 40 °C) and reconstituted in 0.2 mL dichloromethane (DCM) and 0.8 mL iso-octane for further clean- up with neutral alumina.

2.4.2.3 Clean-up

2.4.2.3.1 Alumina clean-up followed by HPLC clean-up (Chapter 3)

The alumina clean-up protocol was the same as the described above for the aqueous samples (Section 2.4.1.2). The cleaned extracts were taken to dryness under gentle nitrogen stream in a water bath (at 40 °C) and then reconstituted in 0.4 mL of 3% isopropyl alcohol (IPA) in hexanes. The samples were then filtered using 0.2 μm pore size PTFE filters into a reaction micro-vessel. The vial was rinsed with 0.5 mL 3% IPA in hexanes to fully recover the target compounds. This solvent was also filtered and collected in the same reaction vial.

29 The HPLC clean-up step was performed with an Agilent 1050 Series HPLC

equipped with a diode array detector and a fraction collector (Spectra-Chrom CF-1) using

a normal-phase silica column (Waters Spherisorb 5-μm silica 4.6 x 250 mm) as well as a

guard column (Waters Spherisorb 5-μm silica 4.6 × 10 mm), to extend the life of the

column.

The guard column had to be pre-conditioned before using it to avoid losses of the

compounds under study. This process was accomplished by pumping a solution of 0.5%

phosphoric acid in 10% IPA in hexanes through the guard column for 45 min. This was

completed with the cartridge holder detached from the column. The acid was then flushed

with 10% IPA in hexanes for 30 min.

The separation of the compounds as well as the purification of the extracts, was

done using an elution gradient. The initial composition of the mobile phase, 3% IPA in

hexanes, was maintained for 3 min. Next, the percentage of IPA was increased up to 4%

in 4 min, followed by another ramp at 1% IPA min-1 until 28% IPA was reached (total time 31 min). A re-equilibration time of 20 min finalized the run. The mobile phase flow was set up at 1 mL min-1. The wavelengths established to determine the retention time of

the compounds were 220 and 235 nm. A clean standard containing the target compounds

and surrogates was injected before any sample and thereafter every two samples to

confirm the retention times and avoid losses of the compounds since the dirtiness of the

extracts caused shifting of the peaks.

30 The samples (dissolved in 0.9 mL of 3% IPA in hexanes) were manually injected into a 1 mL injection loop, and three fractions were collected from the HPLC elution.

The first fraction contained EE2, E1, E2, and their surrogates (12.5–17 min). The second fraction, collected from 23 to 27 min contained E3, PROG, TEST, and d3-TEST. Finally,

AND was collected in the last fraction, from 28 to 29 min.

The HPLC-cleaned extracts were dried down to approximately 1 mL under a gentle nitrogen stream in a water bath (at 40 °C). The samples were then transferred to 2 mL micro-reaction vessel. The vials were rinsed three times with 0.5 mL each of 30%

IPA in hexanes and the rinses were combined with the samples in the micro-reaction vials.

2.4.2.3.2 Alumina clean-up followed by C-18 clean-up (Chapters 4 and 5)

The alumina clean-up protocol was the same as the described above for the aqueous samples (Section 2.4.1.2). For the last batch experiment included in Chapter 3, the initial SPE protocol with C-18 cartridges utilized for extracting the liquid samples

(2.4.1.1.1) was used for cleaning-up the extracts from the solid samples. In chapters 4 and

5, the clean-up was performed following the modified protocol described in the section for aqueous samples (Section 2.4.1.1.2).

31 2.4.2.4 Derivatization procedure

2.4.2.4.1 For GC/MS analysis (Chapter 3)

The same procedure as the one described for the liquid samples (Section

2.4.1.3.1) was followed—the only difference being that in the second reaction, 200 µL of

10% TMCS in BSTFA were added.

2.4.2.4.2 For LC/MS/MS analysis (Chapters 4 and 5)

The same procedure as the one described for the liquid samples (2.4.1.3.2) was

followed and prior to injection in the LC/MS/MS, the samples were filtered through 0.2

μm pore size PTFE filters.

2.4.3 GC/MS ANALYSIS (CHAPTER 3)

The final separation, detection, and quantification of the steroids in aqueous and

solid phases were conducted using a GC/MS (Agilent 6890 GC/5973 MS detector) in

SIM.

For separation, a DB-5MS column (J&W Scientific, 30 m, 0.25 mm ID x 0.25 µm

thickness) was utilized. A single taper direct connect liner (Agilent, 4 mm id) that was

silanized in-house and packed with 5 µg of glass wool, was used. A total volume of 1 µL

was injected in pulsed splitless mode at 310 °C. The carrier gas was ultra high purity

helium and its flow was 0.9 mL min-1. The GC oven temperature program was as

follows: initial temperature 50 °C (maintained for 0.75 min), first ramp at 25 °C min-1 (up to 200 °C), second ramp 4 °C min-1 (up to 300 °C); and the final temperature was hold for

32 16 min.

The detection was performed in SIM mode and the molecular ion of the

trimethylsilyl derivatives plus a confirmation ion were used for quantitation. The MS

parameters were set-up at 300 ºC, 230 ºC, and 150 ºC for interface, ion source, and

quadrupole temperatures, respectively. The ionization energy was 70 eV. The instrument

was tuned with the Autotune utility included in the software (Chemstation).

Finally, the quantification of the target compounds and the surrogates was

performed with an internal linear calibration, prepared as described in Section 2.4.1.3.1.

2.4.3.1 Method validation

13 d4-E1, C2-E2, d3-E3, and d4-EE2 were used as surrogates for the estrogens while d3-TEST was used as a surrogate for TEST, AND, and PROG. Surrogate solutions were spiked prior to extraction of the liquid and solid samples, with surrogate recovery QA/QC criteria set to 80 - 120% and 60 - 140% for liquid and solid matrices, respectively. For d3-

E3, recoveries above 60% were accepted in the liquid phase. Prior extensive testing did

not lead to improvements in this value. Quantification was performed using an internal

calibration with 5α-androstane and 5α-cholestane as the internal standards. Response

factor variability was limited to 20%.

33 The Method Detection Limit (Vogelgesang and Hädrich, 1998) was 1 ng L-1 in liquid samples and 5 ng g-1 in solids for E2, E3, and EE2, while it was 2 ng L-1 and 10 ng

g-1 in aqueous and solid phases, respectively, for E1, TEST, AND, and PROG.

2.4.4 LC/MS/MS ANALYSIS (CHAPTERS 4 AND 5)

An Agilent 1200 Series UPLC coupled with a 6410 Triple Quad and an

Electrospray Ionization (ESI) source was used for the quantification of the estrogens in

the experiments included in Chapters 4 and 5.

For separation, a C-18 column (Zorbax Eclipse XDB-C18, 2.1x50 mm, 3.5 μm,

Agilent) was used with a water (solvent A) and methanol (solvent B) gradient. Both

solvents were buffered with ammonium acetate (2 mM). The initial composition of the

mobile phase contained 60% of solvent B, and was increased up to 100% in 7.5 min. This

composition was maintained for 0.4 min and then the content of B was decreased to 60%

in 0.6 min. Re-equilibration of the system required 2 min. The column was maintained at

40 ºC and the flow during the run was 0.4 mL min-1. The injected volume was 1 µL.

The conditions in the ESI source were: gas (nitrogen) temperature and flow, 350

ºC and 10 L min-1, respectively; nebulizer, 50 psi; and capillary voltage, 4000 V. The equipment was tuned following the manufacturer’s specifications and using the standard

ESI tune mix from Agilent.

Two Multiple Reaction Monitoring (MRM) transitions in positive mode were

34 14 14 employed to quantify E1, E2, C-E2, and d4-EE2. The lack of a standard of C-E1 only

allowed a qualitative analysis of this compound. The MRM transitions selected corresponded to the precursor ion of the derivatized estrogen [M]+ (E1: 504, 14C-E1: 506,

14 E2: 506, C-E2: 508, d4-EE2: 534) and two characteristic fragments of the dansyl group

(m/z: 171 and 154). For all the ions monitored, the resolution was set up as wide in the

first quadrupole and unit in the second one, and the dwell was 200 ms. The voltages of the fragmentor and collision energy were optimized specifically for each of the ions

analyzed.

Finally, the quantification of the target compounds and the surrogates was

performed with an external linear calibration, prepared as described in Section 2.4.1.3.2.

The data was processed in the MassHunter Workstation (Agilent).

2.4.4.1 Method validation

For the LC/MS/MS analysis, only d4-EE2 was used as surrogate. This compound

was spiked prior to extraction of the liquid and solid samples, with surrogate recovery

QA/QC criteria set to 70 – 130% and 60 – 140% for liquid and solid matrices,

respectively. Quantification was performed using an external linear calibration with the calibration curve was accepted for quantitation if r2 was larger than 0.99 for the target

compounds and the surrogate.

The Instrument Detection Limit was calculated following the US EPA guidelines

(US EPA, 1992). The values calculated were 2.4 μg L-1, 1.1 μg L-1, and 1.1 μg L-1 for E1,

35 E2 and EE2 respectively.

2.4.5 RADIOACTIVITY ANALYSIS (CHAPTERS 4 AND 5)

In the experiments in which 14C-E2 was used as target compound, the

radioactivity was measured in liquid, extractable solid, and non-extractable solid phases.

The samples were counted in a Liquid Scintillation Counter (LSC, Packard Tri-Carb

2300TR, Packard Instrument Company, Meriden, CT) immediately after their collection.

A calibration curve, ranging from 100 to 5000 ng L-1, was prepared by spiking the

stock solution of 14C-E2 into LSC vials. The solvent was then evaporated and 3 mL of

liquid scintillation cocktail (Ultima Gold, Perkin Elmer) were added. The standards were

counted in the LSC cited above. A linear calibration curve was built to quantify the

radioactivity and equivalent concentration in the samples. The conversion of radioactivity

measured to equivalent concentration was based on the activity provided by the vendor of

the target compound.

In the case of liquid samples, 100 µL aliquots were collected from the sample filtrates before they underwent the SPE with C-18. The solid samples were extracted in the ASE and the collected solvent was then dried under a gentle nitrogen stream in a water batch (at 40 ºC). The residue was then redissolved in 5 mL of 25% methanol in acetone and 100 µL aliquots were collected. The aliquots from the aqueous samples and extracts from the solids were added to 3 mL of liquid scintillation cocktail, mixed, and then counted in the LSC.

36

In one experiment, described in Chapter 4, closed bottles with a potassium

14 hydroxide (KOH) trap were used in order to collect the carbon dioxide ( CO2 or CO2) that could have potentially evolved in the system due to biodegradation of the target compound. In this case, 300 µL were collected from the KOH traps employed to retain

14 the CO2 or CO2. The samples were added to 3 mL of liquid scintillation cocktail, mixed, and then counted in the LSC.

To determine the radioactivity that was irreversibly-bound to the solid material, the already extracted samples in the ASE were combusted in an oxidizer (Harvey Biological

14 Oxidizer OX700, R. Harvey, Hillsdale, NJ). The CO2 generated by the incineration of

the samples was collected automatically in liquid scintillation cocktail and then was measured in the same LSC mentioned above.

37 2.5 REFERENCES

Esperanza, M., Suidan, M.T., Marfil-Vega, R., Gonzalez, C., Sorial, G.A., McCauley, P.,

Brenner, R., 2007. Fate of sex hormones in two pilot-scale municipal wastewater

treatment plants: Conventional treatment. Chemosphere 66, 1535-1544.

Esperanza, M., Suidan, M.T., Nishimura, F., Wang, Z.-M., Sorial, G.A., Zaffiro, A.,

McCauley, P., Brenner, R., Sayles, G., 2004. Determination of sex hormones and ethoxylates in the aqueous matrixes of two pilot-scale municipal wastewater

treatment plants. Environmental Science & Technology 38, 3028-3035.

Liu, Z., Kanjo, Y., Mizutani, S., 2009. Removal mechanisms for endocrine disrupting

compounds (EDCs) in wastewater treatment — physical means, biodegradation, and

chemical advanced oxidation: A review. The Science of The Total Environment 407,

731-748.

Metcalf and Eddy, 2003. Wastewater Engineering: Treatment and Reuse. Fourth ed.

McGraw Hill, New York.

SRC PhysProp Database http://www.srcinc.com/what-we-do/databaseforms.aspx?id=386

Vogelgesang, J., Hädrich, J. 1998. Limits of detection, identification and determination: a

statistical approach for practitioners. Accreditation and Quality Assurance 3(6), 242-255.

US EPA, 1992. Guidelines establishing test procedures for the analysis of pollutants-

appendix B, part 136, Definition and procedures for the determination of the method

38 detection limit> US Code of Federal Regulations, Title 40, revised as July 1, 1992, 565-

567.

39 Table 2-1. Physico-chemical properties (Liu et al. 2009; SRC PhysProp Database)

WATER SOLUBILITY, COMPOUND -1 pka mg L kOW E1 10.5 30 3.13 E2 10.7 3.6 4.01 E3 10.4 441 2.45 EE2 10.4 11 3.67 TEST NA 23 3.32 AND NA 58 2.75 PROG NA 8.8 3.87

40 Table 2-2. Detailed composition of the concentrated synthetic feed.

Concentration Component (mg L-1) Substrates

Casein 564

Tryptone 564

Starch 1012

Kaolin clay 504

Rabbit food 1368

Sodium acetate 383

Glycerol 144

Caproic acid 139

Macronutrients

Ammonium sulfate 1392

Magnesium sulfate 835

Calcium chloride 270

Potassium phosphate 331

41 Figure 2-1. Structure of the target compounds.

O OH

H H

H H H H

HO HO 17β-Estradiol (E2) Estrone (E1) OH OH

H OH H

H H H H

HO HO Estriol (E3) 17α-Ethinylestradiol (EE2)

OH O

H H

H H H H

O O

Testosterone (TEST) O Androstenedione (AND)

H

H H

O Progesterone (PROG)

42 14 Figure 2-2. Structure of 17β- C4-estradiol.

OH

H

H H

HO * 14C

43 Figure 2-3. Structure of dansyl chloride.

O N S Cl O

44 Chapter 3. ABIOTIC TRANSFORMATION OF ESTROGENS IN

SYNTHETIC MUNICIPAL WASTEWATER: AN ALTERNATIVE

FOR TREATMENT

ABSTRACT

The abiotic transformation of estrogens, including estrone (E1), estradiol (E2), estriol

(E3) and ethinylestradiol (EE2), in the presence of model vegetable matter was confirmed in this study. Batch experiments were performed to model the catalytic conversion of E1,

E2, E3 and EE2 in synthetic wastewater. Greater than 80% reduction in the parent compounds was achieved for each target chemical after 72 h with the remaining concentration distributed between aqueous and solid phases as follows: 13% and 7% for

E1, 10% and 2% for E2, 6% and 2% for E3, and 8% and 3% for EE2, respectively.

Testosterone, androstenedione and progesterone were also monitored in this study, and their concentrations were found to be in agreement with initially spiked amount. Data collected under laboratory conditions provided the basis for implementing new abiotic

wastewater treatment technologies that use inexpensive materials.

† Portions of this chapter were published in Environmental Pollution (Marfil-Vega,

R., Suidan, M., Mills, M. 2010, 158, 3372-3377).

45 3.1 INTRODUCTION

Endocrine disrupting compounds (EDCs) have emerged as chemicals of concern in recent years (Sumpter and Johnson, 2008). Among EDCs, estrogens have received the most attention from various research disciplines. Discharges from wastewater treatment plants (WWTPs) represent a major source for entry of estrogens into the environment

(Khanal et al., 2006). Conventional WWTPs are designed for the elimination of nutrients

and solids (Auriol et al., 2006); nevertheless, these treatment systems are only partially

successful in removing estrogens from wastewater. The residual concentrations of the

estrogens in treated sewage are still at levels that cause adverse effects on aquatic life and

ecosystems (Auriol et al., 2006). Membrane bioreactors and advance oxidation

technologies are promising options to improve the elimination of estrogens (Hu et al.,

2007; Liu et al., 2009) from wastewater. However, the applicability of these technologies

is constrained by the lack of feasibility studies on their full-scale operation and the

prohibitive cost of their implementation in conventional wastewater treatment plants.

A majority of the studies in the literature on the fate of estrogens in WWTPs have

focused primarily on the role of biological transformation, and more recently, adsorption

processes (Khanal et al., 2006). Other removal processes such as enhanced adsorption of

the estrogens and catalytic transformations by chemical agents (metals, oxides, clays)

and/or enzymes have been identified in media such as soils and sediments (Hanselman et al., 2003; Lee et al., 2003; Yu et al., 2004; Sheng et al., 2009); however, there are scarce references in the literature about the occurrence of these processes in sewage (Carballa et al., 2008). Hence, understanding the mechanisms of adsorption and abiotic

46 transformation of estrogens and their exact role in their removal in WWTPs, may provide

potential insight into developing alternative wastewater treatment technologies and sludge management practices.

Clays and humic-like substances, which are present not only in soils and sediments, but also in wastewater (Matsui et al., 1998), are known to promote enhanced adsorption through different mechanisms (Huang et al., 1995). Clays are reactive solids

characterized by a large ion exchange capacity and surface area, hence, numerous active

sites for adsorption, while humic substances and phenolic compounds interact by

hydrogen or covalent bonding, resulting in an increase in apparent adsorption capacity

attributed solely to hydrophobic forces (Yu et al., 2004). This phenomenon could explain

the difficulties encountered in studying the presence of estrogens in primary sludge

(Ternes et al., 2002) and sewage (Carballa et al., 2008). However, discrepancies in the

theoretical versus the measured concentrations reported in those studies may also be caused by the occurrence of catalytic reactions mediated by metals, metal oxides and/or

enzymes that may be found in wastewater.

Several researchers have reported on possible catalytic reactions, mediated by

chemical agents such as metals or metal oxides (mainly manganese oxides), resulting in

abiotic transformation of estrogens (Hanselman et al., 2003; Lee et al., 2003; Sheng et al.,

2009) to chemicals with lesser estrogenic potency. However, to date the byproducts of these transformations have not been unequivocally identified. The use of manganese oxides has been proven efficient for the elimination of different estrogens from

47 wastewater under laboratory conditions (de Rudder et al., 2004; Forrez et al., 2009).

Enzymatic removal of microcontaminants is also being evaluated as a sustainable

alternative to conventional wastewater treatment. Ligninolytic enzymes are known to

catalyze the degradation of estrogenic compounds (Cabana et al., 2007). Peroxidases and

laccases are the main enzyme groups believed to affect these transformations (Gianfreda

et al., 1999). Their natural occurrence as extracellular enzymes in white rot fungi makes

them ubiquitous in the environment. Information on the elimination of estrogens by either

group of enzymes has been published in recent years (Auriol et al., 2007a; Auriol et al.,

2007b; Blánquez and Guieysse, 2008; Mao et al., 2009); however, scant information on

how these enzymes can be harnessed to achieve treatment in real scenarios is available in

the literature.

The occurrence of abiotic transformation of estrogens during wastewater

treatment was pointed out in our prior work (Esperanza et al., 2007). In that study,

difficulties were encountered in achieving closure of the mass balance in a synthetic feed

(composition detailed in Table 3-1) for estrone (E1), 17β-estradiol (E2), 17α-

ethinylestradiol (EE2) and especially, estriol (E3) after an aging period (24 h at 4 °C) for

feed to simulate interactions occurring during sewage transport in sewers. The four

estrogens, E1, E2, E3, and EE2 were recovered at 48%, 51%, 15% and 49% in the liquid

phase, and at 5%, 9%, 1% and 29% from the solids, respectively. The concentration of

the estrogens continued to decrease during the 24 h feeding cycle. The concentration of

the remaining three hormones, testosterone (TEST), androstenedione (AND) and progesterone (PROG), was in agreement with the amount initially fed. To further

48 investigate this phenomenon, a detailed study of the fate of the estrogens in the influent

was initiated.

The objective of the present study was to systematically investigate the

interactions between the estrogens (E1, E2, E3 and EE2), TEST, AND and PROG, and

the solid components of synthetic wastewater. Specifically, the goals were to confirm the

occurrence of abiotic transformation of estrogens in the presence of vegetable material,

and to model this process. The knowledge obtained here will establish the basis for the

optimization of wastewater treatment technologies based on the enhancement of this transformation mechanism.

3.2 MATERIALS AND METHODS

3.2.1 REAGENTS AND CHEMICALS

The target compounds for this study, E1 (99%), E2 (> 98%), E3 (99%), EE2 (>

98%), TEST (99%), AND (98%), and PROG (> 99%), were obtained from Sigma-

Aldrich (Milwaukee, WI). Their chemical structure and main physicochemical properties

(water solubility, octanol-water partition coefficient, pKa) are provided in Fig. 3-1 and

Table 3-2, respectively. To determine efficiency of the analytical procedure, d4-estrone

13 13 (d4-E1; Sigma-Aldrich), C2-estradiol ( C2-E2; Cambridge Isotope Laboratories Inc.,

Andover, MA), d3-estriol (d3-E3; C/D/N Isotopes Inc., Canada), d4-ethinylestradiol (d4-

EE2; C/D/N Isotopes Inc., Canada) and d3-testosterone (d3-TEST; Sigma-Aldrich) were

used as surrogates. For the Gas Chromatography/Mass Spectrometry (GC/MS) analysis,

49 5α-androstane (> 99%) and 5α-cholestane (98%), from Sigma-Aldrich, served as internal

standards.

In the present study, a medium-strength wastewater was synthesized in an attempt

to mimic a municipal wastewater influent by introducing some insoluble organic

materials. The complete list of chemicals added is included in Table 3-1; briefly, casein,

tryptone and starch were added to simulate human excretions and kitchen waste, and

kaolin was introduced as a surrogate of inorganic material from run-off. The rabbit food

was added to represent organic and vegetable wastes discharged into sewers; this

compound, a vegetable and lignin based material with a fiber content of up to 15%, was

selected to aid in comprehending the fate of estrogens in wastewater and less studied

scenarios such as waste discharges and run-off while providing the advantages of

working with a well-controlled matrix.

3.2.2 ANALYTICAL PROCEDURE

Liquid and solid phases of the synthetic wastewater matrix used in this study were

separated in all experiments by filtration with 1.2 μm pore size glass fiber filters. Each matrix was analyzed independently in all sampling events to obtain an accurate mass balance for each of the target compounds. To avoid losses due to adsorption to glass surfaces, all the glassware used was silanized (Sylon CT: 5% dimethyldichlorosilane in toluene, Supelco).

50 Four sets of experiments were conducted in this study. Methods developed by

Esperanza et al. (2004, 2007) were used in the first three sets of experiments. Briefly, for the liquid phase, the appropriate surrogate compounds were added after filtration and the samples were extracted by Solid Phase Extraction (SPE) using C-18 cartridges

(Supelclean ENVI-18 SPE, Supelco). The SPE extracts were subsequently cleaned with neutral alumina (LC-Alumina-N SPE, Supelco), derivatized in two steps with methoxyamine hydrochloride and 5% trimethylchlorosilane in N,O-

Bis(trimethylsilyl)trifluoroacetamide, and finally analyzed by GC/MS (Agilent 6890

GC/5973 MS detector) in Single Ion Monitoring mode.

In the case of solid samples, the methodologies used to analyze the non-soluble components of the synthetic feed, along with the filters, were modified over the course of the study. Lyophilized samples spiked with the surrogate cocktail were extracted in a tumbler at 35 °C using methanol as solvent. The extracts underwent two clean-up steps, first with neutral alumina cartridges and second with an Agilent 1050 Series High

Performance Liquid Chromatograph (HPLC) equipped with a fraction collector using a silica column (Waters Spherisorb 5-μm silica 4.6 x 250 mm). Finally, procedures for derivatization and GC/MS analysis were the same as those described earlier for the liquid samples. In the last experiment, the analysis of solid samples was improved by using pressurized solvent extraction (ASE 200, Dionex Corporation), with a mixture of 25% methanol in acetone. The HPLC clean-up step was substituted, after proper testing, by a

C-18 clean-up process analogous to the initial extraction of the liquid fraction. A detailed description of the analytical methods followed can be found in Chapter 2.

51

3.2.3 EXPERIMENTAL DESIGN

To establish that the previously observed loss of estrogens (Esperanza et al.,

2007) was not due to volatilization or adsorption to the walls of the reservoirs and pipes

used in the experimental set up, a completely mixed stainless steel tank was filled with

-1 dechlorinated water, buffer (dipotassium phosphate: K2HPO4, 0.33 g L ) and microbial

-1 growth inhibiting agent (sodium azide: NaN3, 20 mg L ), and the resulting solution was

spiked with 4800 ng L-1 of each target compound. The tank was placed in a 4 °C constant

temperature room to minimize any potential biological activity, and samples were

collected over 120 h.

To determine the constituent of synthetic wastewater that was responsible for the

loss of estrogens, a series of serum bottles were set up for each of the major chemicals

present in the synthetic wastewater concentrate. The components tested were casein,

starch, kaolinite clay and commercial rabbit food. Samples were tumbled for 72 h at 4 °C

and sacrificed for analysis at times 1 and 72 h. The amount of added to each

bottle was proportional to its corresponding concentration in the synthetic feed (Table 3-

-1 1). Bottles were filled with 80 mL of dechlorinated tap water to which NaN3 (20 mg L )

-1 and K2HPO4 (0.33 g L ) were added. The seven target compounds were spiked into each

bottle at 5000 ng L-1 each. Liquid and solid phases were analyzed independently, as

described in Section 3.2.2.

52 To estimate the estrogens disappearance rate and model their behavior in the

synthetic feed, different concentrations of the target chemicals were spiked and

monitored over time. For this purpose, two batch experiments using completely mixed 48

L stainless steel tanks were run. These tanks were placed in a constant temperature room

maintained at 4 °C to minimize any potential biological activity. Briefly, the concentrated

waste was prepared in dechlorinated tap water, with a final pH of 6.7. The initial

concentrations of the seven target compounds (E1, E2, E3, EE2, TEST, AND, PROG)

were 1200 and 4800 ng L-1 in each experiment. Detailed conditions of each of the runs are included in Table 3-3. Samples were collected at several preset times during the

experiments in order to obtain a time-varying concentration profile of the EDCs. Liquid

and solid phases were analyzed separately as described in Section 3.2.2.

Finally, confirmation of the catalytic transformation of estrogens in the sole presence of rabbit food and the validity of the model developed with the whole synthetic

influent were examined. Two 5 L bottles containing the relevant amounts of rabbit food,

-1 -1 K2HPO4, (0.33 g L ) and NaN3 (20 mg L ) were prepared and placed in a controlled

temperature room at 4 °C. The steroids were initially spiked in both bottles at a

concentration of 5000 ng L-1 for each compound. The mixture was continually stirred,

and samples were collected in triplicates periodically, starting at 1 h and up to 72 h, from

the first bottle. At time 72 h, the second 5 L bottle was spiked again with the same

concentration, 5000 ng L-1, and samples were collected in triplicates periodically from 73

up to 144 h. Throughout the experiment, liquid and solid phases were analyzed

independently at each sampling time following the methodology described earlier.

53

3.3 RESULTS AND DISCUSSION

A series of experiments (described in Section 3.2.3) were performed to

characterize the observed loss in estrogen mass in the concentrated feed, and determine if

the losses were due to chemical transformations or adsorption. The following two

hypotheses were considered. First, enhanced adsorption of the estrogens caused their apparent elimination from the synthetic wastewater matrix; the process most likely involved interactions between clay and/or rabbit food present in the influent and the phenolic group in the estrogen skeleton, which does not exist in TEST, AND and PROG.

Second, an abiotic reaction was transforming the estrogens into up-to-date unidentified products; potential catalysts could have been metals, oxides, clays and enzymes. The two aforementioned mechanisms are not mutually exclusive.

Enzymatic transformation of estrogens through exposure to the synthetic wastewater was rejected based on information available in the literature. First, the potential for a peroxidase catalytic reaction between the estrogens and the non-soluble components of the feed was discarded outright because of the absence of a reaction activator required by these enzymes (Mester and Tien, 2000). Second, laccases activity was considered very unlikely to occur at the low temperature of our experiments, 4 °C, and in the presence of NaN3 (Johannes and Majcherczyk, 2000).

Biodegradation was never considered to be the main culprit for the disappearance

of the estrogens in our experiments. The experiments were always conducted in a

54 temperature-controlled room set to 4 °C (a widely used preservation technique) to

minimize biological activity. Even though all experiments were conducted at 4 °C, NaN3

was added in most of the experiments to ensure suppression of aerobic biological

transformations.

Table 3-3 summarizes the conditions for the experiments performed to

characterize the depletion of estrogens in the concentrated feed. The first experiment was

designed to assess losses of hormones attributable to volatilization or adsorption onto the

stainless steel reservoirs. Results from this experiment, shown in Fig. 3-2 (black circles), affirm that no such losses occur in the absence of wastewater constituents; results included in Fig. 3-2 correspond only to E1, E2, E3, EE2, with TEST as an example of the behavior of non-estrogenic compounds. All seven hormones were fully recovered after

120 h of exposure in the feed reservoirs.

The various constituents of the synthetic wastewater (Table 3-1) were tested individually to ascertain their potential to affect the observed transformation of the estrogens. Results from these experiments led to the conclusion that rabbit food was the agent causing the increased adsorption/abiotic transformation of the estrogens (results not shown). Concentrations recovered from liquid phase after 72 h were above 90% for the four estrogenic compounds in the bottles containing kaolin, casein and starch; on the other hand, concentrations ranging 15-20% were found in the aqueous samples that were in contact with the rabbit food. No variation in the concentration of TEST, AND and

PROG was found in any of the bottles containing the four tested substrates, which was

55 consistent with what was observed in our first experiment included in this manuscript and

the work published by Esperanza et al. (2007). Kaolin was initially believed to be

involved in a surface reaction that could cause estrogen loss (Lee et al., 2003); however,

this hypothesis was discarded because the total mass spiked was recovered in the bottles

containing kaolin, which is in agreement with other studies focused on adsorption onto

minerals (Shareef et al., 2006).

The identification of rabbit food as the culprit of the estrogens depletion is very

significant since the constituents of rabbit food have a strong resemblance to vegetable

waste entering sewer systems (ratio Chemical Oxygen Demand/Volatile Suspended

Solids (COD/VSS) equal to 1.2, close to the typical value of 1.45 for biomass (Mercer et

al., 2003)). Additionally, in light of our initial findings, organic vegetable wastes may

constitute inexpensive materials for promoting the removal of estrogens via enhanced

adsorption and/or catalytic reaction.

Experiments 2 and 3 (Table 3-3) were performed to identify a mathematical

model that fitted and explained the reduction in the concentration of estrogens, and to

determine the effects, if any, of the presence of biological inhibitors on the disappearance

rate. The bar plot in Fig. 3-2 show the fractional recovery with time for five of the target

compounds (E1, E2, E3, EE2 and TEST) in the liquid (white portion of the bars) and

solid phases (grey portion of the bars) when the solution was spiked with an initial

-1 -1 concentration of 4800 ng L of each hormone and with the addition of 20 mg L NaN3

(Experiment 2 in Table 3-3). A similar profile was obtained when the spiked

56 concentration of each hormone was 1200 ng L-1 (Experiment 3 in Table 3-3, Data not

shown). As can be observed from Fig. 3-2, the total concentration of estrogens decreased

steadily over time, while TEST was recovered fully (> 80%) after extended periods of interaction (up to 120 h); AND and PROG showed the same behavior as TEST (results not included), confirming that biodegradation was not occurring in our system.

Figure 3-3 shows the rate of disappearance of E2 obtained from experiments 2 and 3 against the log-mean concentration of E2 in liquid phase at each 1 h interval; black and grey circles correspond to the results from experiment 2 and 3, respectively. Similar results were observed for E1, E3 and EE2 (Fig. 3-4, 3-5 and 3-6, correspondingly).

The rate of disappearance for each estrogen was computed as follows: the total concentration (sum of concentration measured in liquid and solid phases independently) was represented against time, and the resulting plot was fitted to a negative exponential equation to predict the total concentration in 1 h intervals. The average rate of disappearance of an estrogen, r, for each 1 h interval was computed as the difference between the predicted total mass of estrogen recovered at two consecutive time events divided by the product of time interval (1 h) and the mass of rabbit food. To simplify the calculations, the initial mass of rabbit food was used (1.37 g L-1) for all calculations given

that the solids concentration fluctuated ± 5% in a 120 h period (Total Suspended Solids:

757 mg L-1, VSS: 725 mg L-1), and other parameters such as Total Organic Carbon

(TOC) and Total and Soluble COD (CODt and CODs) also remained constant (TOC: 114

ppm ± 10%; CODt: 1305 ppm ± 4 %; CODs: 332 ppm ± 6 %). Finally, the calculated rate

57 was plotted against the concentration of estrogens predicted in aqueous phase (from the fitting of concentration analyzed in aqueous phase against time) or against the predicted total measured concentration (as explained to compute the rate). The data were fitted using a saturation type equation (Eq. 1), characteristic of a catalytic process:

k[S] r = − (1) + KS [S] where r is the average rate of disappearance of an estrogen, k (ng h-1 g-1) is the maximum specific estrogen disappearance rate, [S] (ng L-1) is the concentration of an estrogen in the

-1 liquid phase, and Ks (ng L ) is the half-saturation constant (estrogen concentration in liquid phase corresponding to a rate equal to at one-half k). In the last columns of Table

3-3 the values of k and Ks are listed along with the associated errors for each estrogen as well as the correlation coefficient, r2. The same data analysis was performed fitting the rate and the predicted total concentration, but the r2 obtained was lower and the residuals were bigger than in the case with the concentration in liquid phase. Therefore, the subsequent discussion of our results is done based on the results reported in Table 3-3, from the concentrations in liquid phase.

As can be observed from Fig. 3-3 and the r2 values in Table 3-3, the rate data for

E2 corresponding to Experiments 2 and 3 agree rather well with the saturation function expressed by Eq. 1. In addition, the data in Fig. 3-3, 3-4, 3-5, and 3-6 suggest that addition of NaN3 does not affect the overall rate of the reaction, at least in the concentration used in these experiments (20 mg L-1 or 0.3 mM). Hence, the addition of sodium azide along with maintaining the temperature at 4 °C was considered to be

58 sufficient to eliminate biotic transformation as the source of elimination of estrogens from the matrix.

Since biotic transformations were eliminated, the observed decrease in estrogens in the matrix is either due to an abiotic transformation or a combination of abiotic and adsorption process. The data in Fig. 3-7 represents the time-varying fractional recovery of each of the four estrogens (circles, inverted triangles, squares and diamonds for E1, E2,

E3 and EE2, respectively) from the solid phase as obtained from Experiment 2. The data in Fig. 3-7 show that the concentration of the estrogens in the solid phase increased initially with time until a maximum is reached. The solid-phase concentration subsequently decreases steadily during the remaining duration of the experiment.

However, the data in Fig. 3-2, 3-3, 3-4, 3-5, 3-6, and 3-7 also indicate that there is some estrogen that is being recovered from the solid phase even after 120 h of contact. This seems to indicate that adsorption onto the surface does play a role in the elimination of estrogens from the matrix. The initial increase in estrogen concentration in the solid phase is indicative of adsorption onto the surface, while the subsequent decrease in estrogen concentration in both the solid and liquid phases with time is indicative of abiotic transformation in the liquid and/or solid phases. E1, E2 and EE2 exhibit the expected behavior where transformation in the aqueous and/or solid phase and adsorption onto the solids are simultaneously competing for the estrogen. These data suggest that the adsorption of estrogens and/or its transformation product was reversible as the concentration of the estrogen in the aqueous and solid phases were observed to decrease with time. In the case of E3, however, the concentration recovered from the solids was

59 very small at all time points, which is in agreement with its lower kow (and higher Ks).

Consequently, the rate of disappearance of E3 (Fig. 3-5) appears to be more due to the abiotic transformation in the aqueous phase than adsorption and/or abiotic transformation in the solid phase.

The results from this experiment seem to indicate that a catalytic process is governing the estrogens depletion, modeled by Eq. 1. Although there is a contribution of adsorption to the overall reduction, the compounds appear to bind reversibly to rabbit food. Extensive testing of extraction conditions to optimize the use of an ASE for the analysis of solid samples (representative results included in Table 3-4) did not provide a representative increase in the recovery of estrogens from that phase, when compared with the traditional extraction method that uses milder extraction conditions. Furthermore, the rapid decrease in the concentration of E3, the least hydrophobic compound among the targeted estrogens, suggests that adsorption is not the rate-limiting step and unlikely to be the driving process of the phenomenon under study.

Ultimately, the catalytic transformation of estrogens in the sole presence of rabbit food and the validity of the model developed (Eq. 1) with the whole synthetic influent were examined in the respiking experiment, denoted as 4a and 4b in Table 3-3. If identical disappearance rates were observed upon respiking, then it would corroborate the occurrence of catalytic reaction. However, catalyst poisoning and/or exhaustion can easily lead to variation in the rates. The time-varying fractional recovery of each of the seven steroids can be seen in Fig. 3-8 and 3-9; the concentration of TEST, AND and

60 PROG matched the total amount spiked at time 0 and at 72 h. As for the estrogens, the concentrations measured after the first 72 h experimental period were in agreement with the results from previous experiments. Respiking the compounds resulted in similar behavior with the four estrogens continuing to be depleted at a rapid rate, thus confirming the large capacity of rabbit food (ground to less than 200 U.S. Mesh size using a ball mill) for attenuating estrogens.

Figure 3-3 shows the rate of disappearance of E2, computed as explained above, as a function of its log-mean concentration in liquid phase for experiment 4a (black squares) and the subsequent respiking experiment, 4b (white squares) (see Fig. 3-4, 3-5, and 3-6 for other estrogens). The data obtained during the initial 72 h (black squares in

Fig. 3-3) observation period are in agreement with the model fitted to data from experiments 2 and 3, with slight deviations that may be attributed to changes in the solid phase since rabbit food was the only non-soluble component of the synthetic feed in this experiment. Results from the respiking experiment showed that while the concentrations of the estrogens in aqueous phase were higher after respiking the solution, the recovered amounts from the solid phase during the second 72 h experimental period were similar to those obtained during the initial one. However, the overall disappearance rates appear to be slightly lower in the second part of the experiment than in the initial 72 h. This is most likely due to the consumption of the catalytic agent (either metals/metal oxides leached out from the rabbit food or reactive sites on the surface of the solid phase). Also it may be an indication of substrate self-inhibition at high concentrations. Additional research would be necessary to confirm any of these hypotheses.

61

Summarizing, this last experiment confirms the occurrence of a catalytic transformation of E1, E2, E3 and EE2 coupled to a reversible adsportion process, which has a bigger influence on the overall reaction rates of the more hydrophobic chemicals

(E1, E2 and EE2); the slightly different behavior showed by E3 may indicate that the abiotic reaction is taking place in the liquid phase, although its occurrence at the aqueous- solid interphase cannot be rejected with the results available up to date.

3.4 CONCLUSIONS

Four estrogens, E1, E2, E3, and EE2 were found to undergo an abiotic transformation in the presence of a model vegetable matter (rabbit food) in aqueous solutions. An independent analysis of aqueous and solid phases in all experiments to accurately quantify the adsorption contribution provides some evidence that sorption plays a role, but abiotic transformations in the aqueous and/or solid phase are responsible for the elimination of estrogens from the matrix.

The ultimate mechanism for this process is still unclear. The catalytic polymerization of phenolic compounds through an oxidative coupling mechanism is well documented in soils (Huang et al., 1995; Hanselman et al., 2003), as well as in engineered systems (Vidic et al., 1990). Because of the structural similarity of the rabbit food with some soil components, such as humic substances, it could be hypothesized that an analogous process is occurring in the system under study.

62 Further research, using 14C-estrogens, is planned to provide more thorough understanding of the fate of these compounds in sewage and during wastewater treatment. Emphasis is also placed on characterizing the substrate (rabbit food) in order to develop novel technologies that harness abiotic processes for control of estrogens in wastewater.

63 3.5 REFERENCES

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Auriol, M., Filali-Meknassi, Y., Tyagi, R.D., Adams, C.D., 2007b. Oxidation of natural and synthetic hormones by the horseradish peroxidase enzyme in wastewater.

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Auriol, M., Filali-Meknassi, Y., Tyagi, R.D., Adams, C.D., Surampalli R.Y., 2006.

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Biochemistry 41, 525-539.

Blánquez, P., Guieysse, B., 2008. Continuous biodegradation of 17β-estradiol and 17α- ethynylestradiol by Trametes versicolor. Journal of Hazardous Materials 150, 459-462.

Cabana, H., Jones, J., Agathos, S., 2007. Elimination of endocrine disrupting chemicals using white rot fungi and their lignin modifying enzymes: A review. Engineering in Life

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Carballa, M., Omil, F., Lema, J.M., 2008. Comparison of predicted and measured concentrations of selected pharmaceuticals, fragrances and hormones in Spanish sewage.

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64 De Rudder, J., Van de Wiele, T., Dhooge, W., Comhaire, F., Verstraete, W., 2004.

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(EE2). Water Research 38, 184-192.

Esperanza, M., Suidan, M.T., Marfil-Vega, R., Gonzalez, C., Sorial, G.A., McCauley, P.,

Brenner, R., 2007. Fate of sex hormones in two pilot-scale municipal wastewater treatment plants: Conventional treatment. Chemosphere 66, 1535-1544.

Esperanza, M., Suidan, M.T., Nishimura, F., Wang, Z.-M., Sorial, G.A., Zaffiro, A.,

McCauley, P., Brenner, R., Sayles, G., 2004. Determination of sex hormones and nonylphenol ethoxylates in the aqueous matrixes of two pilot-scale municipal wastewater treatment plants. Environmental Science & Technology 38, 3028-3035.

Forrez, I., Carballa, M., Noppe, H., De Brabander, H., Boon, N., Verstraete, W., 2009.

Influence of manganese and ammonium oxidation on the removal of 17α- ethynylestradiol (EE2). Water Research 43, 77-86.

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Hanselman, T.A., Graetz, D.A., Wilkie, A.C., 2003. Manure-borne estrogens as potential environmental contaminants: A review. Environmental Science & Technology 37, 5471-

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Hu, J., Chen, X., Tao, G., Kekred, K., 2007. Fate of endocrine disrupting compounds in membrane bioreactor systems. Environmental Science & Technology 41, 4097-4102.

65 Huang, P.M., Berthelin, J., Bollag, J.M., McGill, W.B., Page, A.L., 1995. Environmental

Impact of Soil Component Interactions. Natural and Anthropogenic Organics. Vol. 1,

CRC Press, Boca Raton.

Johannes, C., Majcherczyk, A., 2000. Laccase activity tests and laccase inhibitors.

Journal of Biotechnology 78, 193-199.

Khanal, S.K., Xie, B., Thompson, M.L., Sung, S., Ong, S., van Leeuwen, J., 2006. Fate, transport, and biodegradation of natural estrogens in the environment and engineered systems. Environmental Science & Technology 40, 6537-6546.

Lee, L.S., Strock, T.J., Sarmah, A.K., Rao, P.S.C., 2003. Sorption and dissipation of testosterone, estrogens and their primary transformation products in soils and sediment.

Environmental Science & Technology 37, 4098-4105.

Liu, Z., Kanjo, Y., Mizutani, S., 2009. Removal mechanisms for endocrine disrupting compounds (EDCs) in wastewater treatment — physical means, biodegradation, and chemical advanced oxidation: A review. The Science of The Total Environment 407,

731-748.

Mao, L., Huang, Q., Lu, J., Gao, S., 2009.Ligninase-mediated removal of natural and synthetic estrogens from water: I. reaction behaviors. Environmental Science &

Technology 43, 374-379.

Matsui, S., Yamamoto, H., Shimizu, Y., Harada, J., Einaga, D., 1998. Humic substances affecting the limitation of the activated sludge process for removal of micropollutants.

Water Science and Technology 38, 7, 217-225.

66 Melcer, H., Dold, P.L., Jones, R.M., Bye, C.M., Takacs, I., Stensel, H.D., Wilson, A.W.,

Sun, P., Bury, S., 2003. Methods for Wastewater Characterization in Activated Sludge

Modelling, Water Environment Research Foundation, Alexandria.

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46, 51-59.

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17α-ethynylestradiol and estrone to mineral surfaces. Journal of Colloid and Interface

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Sheng, G.D., Xu, C., Xu, L., Qiu, Y.P., Zhou, H.Y., 2009. Abiotic oxidation of 17β- estradiol by soil manganese oxides. Environmental Pollution 157, 2710-2715.

SRC PhysProp Database http://www.srcinc.com/what-we-do/databaseforms.aspx?id=386

Sumpter, J., Johnson, A., 2008. 10th Anniversary perspective: Reflections on endocrine disruption in the aquatic environment: from known knowns to unknown unknowns (and many things in between). Journal of Environmental Monitoring 10, 1476-1485.

Ternes, T.A., Andersen, H., Gilberg, D., Bonerz, M., 2002. Determination of estrogens in sludge and sediments by liquid extraction and GC/MS/MS. Analytical Chemistry 74,

3498-3504.

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67 Yu, Z., Xiao, B., Huang, W., Peng, P., 2004. Sorption of steroid estrogens to soils and sediments. Environmental Toxicology and Chemistry 23, 531-539.

68 Table 3-1. Detailed composition of the concentrated synthetic feed.

Concentration Component (mg L-1) Substrates

Casein 564

Tryptone 564

Starch 1012

Kaolin clay 504

Rabbit food 1368

Sodium acetate 383

Glycerol 144

Caproic acid 139

Macronutrients

Ammonium sulfate 1392

Magnesium sulfate 835

Calcium chloride 270

Potassium phosphate 331

69 Table 3-2. Physico-chemical properties (Liu et al. 2009; SRC PhysProp Database)

WATER SOLUBILITY, COMPOUND -1 pka mg L kOW E1 10.5 30 3.13 E2 10.7 3.6 4.01 E3 10.4 441 2.45 EE2 10.4 11 3.67 TEST NA 23 3.32 AND NA 58 2.75 PROG NA 8.8 3.87

70 Table 3-3. Experiments description. Model parameters for each estrogen.

SAMPLING BIOLOGICAL EXP# CONCENTRATION MATRIX SAMPLES# TIMES, h INHIBITOR

Yes: 1, 12, 24, 36, 48, 60, 1 4800 ng L-1 each Water Duplicates 20 mg L-1 72, 84, 96, 108, 120 -1 -1 -1 2 NaN3 COMPOUND k, ng h g KS, ng L r

Yes: E1 133 (±8) 4072 (±387) 0.967 Synthetic 1, 12, 24, 36, 48, 60, 2 4800 ng L-1 each Duplicates 20 mg L-1 influent 72, 84, 96, 108, 120 NaN3 E2 90 (±3) 1938 (±134) 0.970

2 tanks 1 E3 270 (±14) 6872 (±496) 0.992 Synthetic 3 1200 ng L-1 each 1, 24, 30, 36, 42, 48 sample from NO influent each EE2 134 (±6) 2965 (±244) 0.974

Yes: Rabbit 4a 5000 ng L-1 each 1, 24, 48, 72 Triplicates 20 mg L-1 Food NaN3

Yes: 5000 ng L-1 each Rabbit 4b 73, 96, 120, 144 Triplicates 20 mg L-1 (Respike) Food NaN3

71 Table 3-4. Percentage of concentration recovered from solids extraction

using a rotary tumbler or ASE.

Tumbler ASE ASE % ASE Mix MeOH MeOH Acetone 13C-E2 77±15 80±10 84±14 74±2 E2 2±0 2±0 2±0 4±0

d3-TEST 97±7 94±15 117±9 127±9 TEST 12±1 10±1 9±0 18±4 % Recovery ± error (triplicates) 13 C-E2 and d3-TEST: Surrogate recovery E2 and TEST: Amount recovered after 72 h of contact with rabbit food; initial spiked concentration 5000 ng L-1.

Extraction conditions:

Tumbler MeOH: Rotary tumbler in a controlled temperature room at 35 °C; 100% methanol, 21 mL total during 10 h (7 mL x 2 h, 7 mL x 4 h, 7 mL x 4 h). ASE MeOH: ASE; 100% methanol, 4 cycles, 100 °C, 2000 psi. ASE Acetone: ASE; 100% acetone, 4 cycles, 100 °C, 2000 psi. ASE Mix: ASE; 25:75 methanol:acetone, 4 cycles, 100 °C, 2000 psi.

72 Figure 3-1. Structure of the target compounds.

O OH

H H

H H H H

HO HO 17β-Estradiol (E2) Estrone (E1) OH OH

H OH H

H H H H

HO HO Estriol (E3) 17α-Ethinylestradiol (EE2)

OH O

H H

H H H H

O O

Testosterone (TEST) O Androstenedione (AND)

H

H H

O Progesterone (PROG)

73 Figure 3-2. Fractional recovery of E1, E2, E3, EE2 and TEST. Results from experiment

1 (black circles) and 2 (bar plot) (Table 3-3). Initial concentration: 4800 ng

-1 -1 L with the addition of 20 mg L NaN3.

-1 -1 INITIAL CONCENTRATION 4800 ng L + 20 mg L NaN3

140 SOLID (Experiment 2) LIQUID (Experiment 2) WATER (Experiment 1)

120

100

80

60 % RECOVERED%

40

20

0 E1 E2 E3 EE2 TEST SAMPLING TIMES: 1, 12, 24, 36, 48, 60, 72, 84, 96, 108,& 120 h.

74 Figure 3-3. Rate of disappearance of E2. Model obtained as combination of experimental

results from experiments with initial concentration 1200 ng L-1 (black

circles) and 4800 ng L-1 (grey circles) (experiments 2 and 3 in Table 3-3).

Solid line: model fitting; black squares: results from experiment 4a (Table

3-3); white squares: results from experiment 4b (Table 3-3).

ESTRADIOL

120 1200 ng L-1 4800 ng L-1 Respike I 100 Respike II -1

80 rabbit food g -1 60

40 - RATE, ng h 20

0 0 1000 2000 3000 4000 5000 CONCENTRATION, ng L-1

75 Figure 3-4. Rate of disappearance of E1. Model obtained as combination of experimental

results from experiments with initial concentration 1200 ng L-1 (black

circles) and 4800 ng L-1 (grey circles) (experiments 2 and 3 in Table 3-3).

Solid line: model fitting; black squares: results from experiment 4a (Table 3-

3); white squares: results from experiment 4b (Table 3-3).

ESTRONE

120 1200 ng L-1 4800 ng L-1 Respike I 100 Respike II -1

80 rabbit food g -1 60

40 - RATE, ng h 20

0 0 1000 2000 3000 4000 5000 CONCENTRATION, ng L-1

76 Figure 3-5. Rate of disappearance of E3. Model obtained as combination of experimental

results from experiments with initial concentration 1200 ng L-1 (black

circles) and 4800 ng L-1 (grey circles) (experiments 2 and 3 in Table 3-3).

Solid line: model fitting; black squares: results from experiment 4a (Table 3-

3); white squares: results from experiment 4b (Table 3-3).

ESTRIOL

120 1200 ng L-1 4800 ng L-1 Respike I 100 Respike II -1

80 rabbit food g -1 60

40 - RATE, ng h 20

0 0 1000 2000 3000 4000 5000 CONCENTRATION, ng L-1

77 Figure 3-6. Rate of disappearance of EE2. Model obtained as combination of

experimental results from experiments with initial concentration 1200 ng L-1

(black circles) and 4800 ng L-1 (grey circles) (experiments 2 and 3 in Table

3-3). Solid line: model fitting; black squares: results from experiment 4a

(Table 3-3); white squares: results from experiment 4b (Table 3-3).

ETHINYLESTRADIOL

120 1200 ng L-1 4800 ng L-1 Respike I 100 Respike II -1

80 rabbit food g -1 60

40 - RATE, ng h 20

0 0 1000 2000 3000 4000 5000 CONCENTRATION, ng L-1

78 Figure 3-7. Percentage of concentration recovered from solid phase for each estrogen.

-1 -1 Initial concentration: 4800 ng L with the addition of 20 mg L NaN3

(experiment 2 in Table 3-3).

% RECOVERED FROM SOLID PHASE 25 E1 E2 E3 EE2 20

15

% RECOVERED % 10

5

0 20 40 60 80 100 120 TIME, h

79 Figure 3-8. Fractional recovery of E1, E2, E3 and EE2. Results from experiment 4a and

4b (Table 3-3). Total recovery (circle), recovery in liquid phase (triangle)

and solid phase (square).

ESTRONE ESTRADIOL 160 160

140 140

120 120

100 100

80 80

60 60 % RECOVERED RECOVERED % RECOVERED %

40 40

20 20

0 0 0 20 40 60 80 100 120 140 0 20 40 60 80 100 120 140 TIME (h) TIME (h) ESTRIOL ETHINYLESTRADIOL 160 160

140 140

120 120

100 100

80 80

60

60 RECOVERED % % RECOVERED RECOVERED %

40 40

20 20

0 0 0 20406080100120140 0 20 40 60 80 100 120 140 TIME (h) TIME (h)

80 Figure 3-9. Fractional recovery of TEST, AND and PROG. Results from experiment 4a

and 4b (Table 3-3). Total recovery (circle), recovery in liquid phase

(triangle) and solid phase (square).

TESTOSTERONE ANDROSTENEDIONE 250 250

200 200

150 150

100 100 % RECOVERED % % RECOVERED%

50 50

0 0 0 20 40 60 80 100 120 140 0 20 40 60 80 100 120 140 TIME (h) TIME (h) PROGESTERONE 250

200

150

100 % RECOVERED RECOVERED %

50

0 0 20 40 60 80 100 120 140 TIME (h)

81 Chapter 4. ASSESSMENT OF THE ABIOTIC TRANSFORMATION

OF ESTROGENS IN THE PRESENCE OF VEGETABLE MATTER

ABSTRACT

14 14 A study using 17β- C4-estradiol ( C-E2) was performed to confirm and characterize the catalytic transformation of estrogens in the presence of a model vegetable matter (namely rabbit food) as a surrogate material for vegetable wastes found in sewage. Results corroborated the occurrence of an abiotic transformation. Unknown transformation byproduct(s) accounted, respectively, for 38 and 9% of the initial radioactivity in liquid and extractable solid phases after 72 h; on the other hand, only 15 and 7% of this radioactivity corresponded to 14C-E2 in those same matrices. Mass balance was closed including the radioactivity irreversibly bounded to the solid phase.

14 Formation of C4-estrone was monitored by Liquid Chromatography with tandem Mass

Spectrometry detection; negative results were found in all sampling events. This process could be harnessed to optimize sustainable technologies for the removal of phenolic microcontaminants from wastewater.

82 4.1 INTRODUCTION

17β-estradiol (E2) is the predominant estrogen in humans, found at elevated concentrations in females and at lower levels in males. Urinary excretion rates in females vary from 2.78 to 347 μg d-1, and the average in males is 1.5 μg d-1 (Liu et al., 2009). E2 has become the representative compound of the Endocrine Disrupting Chemicals (EDCs) during the past decade, due mainly to its natural origin and its high estrogenic potency

(Liu et al., 2009). Numerous research articles have been addressed its fate in the environment (Kolpin et al., 2002; D'Ascenzo et al., 2003; Hanselman et al., 2003; Casey et al., 2005; Khanal et al., 2006; Esperanza et al., 2007).

The natural estrogen E2, along with others such as estrone (E1), estriol (E3), and the synthetic one ethinylestradiol (EE2), wastewater treatment plants (WWTPs) primarily in their deconjugated form (Desbrow et al., 1998) through sanitary sewers.

Although the levels of estrogens normally reported in sewage are in the low ng L-1 range, these concentrations have been found to cause adverse effects in aquatic life (Bolong et al., 2009). Extensive research has proved that conventional WWTPs are, in general, not efficient in removing these chemicals down to safe levels for aquatic ecosystems (Bolong et al., 2009). Recent evaluations indicated that advanced treatment systems may be required for the elimination of estrogens from WWTPs discharges (Joss et al., 2008).

Nevertheless, the implementation of sustainable and globally applicable treatment technologies is still needed for the long-term management of estrogenic contaminants in the environment.

83 Research efforts to date have focused primarily on biodegradation and, more recently, adsorption processes (Khanal et al., 2006) for the removal of estrogens in wastewater. However, while the occurrence of additional transformation mechanisms other than the aforementioned has been reported in natural aquatic systems (Carballa et al., 2008), little attention has been devoted to gaining a thorough understanding of them.

The abiotic transformation of phenolic compounds, including E2, has been documented in soil and sediment systems (Colarieti et al., 2002; Hanselman et al., 2003;

Lee et al., 2003; Yu et al., 2004; Sheng et al., 2009). Most important reaction pathways involve either the oxidative and/or catalytic action of metal oxides, primarily manganous or ferrous metals, or the mediation of ligninolytic enzymes (Auriol et al., 2006; Gianfreda and Rao, 2004; Blánquez and Guieysse, 2008). In general, these reactions lead to the formation of polymers or the incorporation of phenolic compounds within humic substances (Huang et al., 1995), which are also a major component of wastewater (Matsui et al., 1998), through an oxidative coupling mechanism. Some studies have reported other transformation products such as E1 and quinone-type compounds, resulting also from oxidative reactions (Casey et al, 2005; Sheng et al., 2009).

A thorough understanding of the mechanisms underlying these abiotic processes and other biogeochemical redox transformations in sewage and in WWTPs is needed for the improvement of treatment technologies and management practices of natural and engineered systems impacted by estrogens and other EDCs (Young and Borch, 2009).

84 Abiotic transformation of estrogens in the presence of vegetable matter from simulated sewage has been identified previously in our research group (Chapter 3). Our initial investigation suggested that a catalytic process is responsible for the apparent disappearance of E1, E2, E3, and EE2 in a simulated wastewater.

The objective of the current study was to authenticate the occurrence of the abiotic transformation of estrogens in the presence of a model vegetable matter (namely,

14 14 rabbit food). The use of 17β- C4-estradiol ( C-E2) provided two major advantages.

First, a precise mass balance could be performed by the simultaneous measurement of radioactivity and concentration by Liquid Chromatography with tandem Mass

14 14 Spectrometry detection (LC/MS/MS). And second, the formation of C4-estrone ( C-

E1) as a result of biological activity or other chemical transformation could be monitored as well. The model vegetable material was selected to represent the organic matter that can be discharged in wastewater streams; the rabbit food is a vegetable based material with 15% fiber.

4.2 MATERIALS AND METHODS

4.2.1 REAGENTS AND CHEMICALS

14 14 -1 17β- C4-estradiol ( C-E2) (Fig. 4-1) with an activity of 55 mCi mmol was purchased from American Radiolabeled Chemicals Inc. (Saint Louis, MO). d4-

Ethynilestradiol (C/D/N Isotopes Inc., Canada) served as surrogate to determine the extraction efficiency of the analytical method. Dansyl chloride (from Sigma Aldrich,

85 Milwaukee, WI) and sodium bicarbonate (NaHCO3) were used for the derivatization of the analytes.

4.2.2 ANALYTICAL PROCEDURE

In order to accurately determine the mass balance on 14C-E2, the liquid and solid phases were analyzed individually for the estrogen by means of radioactivity measurement and LC/MS/MS quantification. At the preselected sampling times, samples

(prepared as explained in section 4.2.3) were collected in triplicates. They were acidified and filtered through 1.2 μm pore size glass fiber filters. Figure 4-2 shows a schematic of the analytical protocol.

From each samples, 100 μL aliquots of the aqueous phase and the solvent from the solids extraction were collected for radioactivity counting. The remaining extracted solids and the filters, were combusted in an oxidizer (Harvey Biological Oxidizer OX700,

R. Harvey, Hillsdale, NJ) to quantify any radioactivity that was irreversibly adsorbed on the rabbit food.

The sample preparation for the LC/MS/MS analysis of the aqueous phase included an initial Solid Phase Extraction with C-18 cartridges followed by clean-up with neutral alumina. The solid samples underwent an extraction in an Accelerated Solvent

Extractor with a mixture of acetone and methanol, followed by two clean-up steps with neutral alumina and C-18. A more detailed description of the extraction of liquid and solid samples for the LC/MS/MS analysis is included in Chapter 2.

86

4.2.2.1 RADIOACTIVITY ANALYSIS

The aliquots from the aqueous samples and extracts from solids were added to 3 mL of a liquid scintillation cocktail. Samples were counted in a Liquid Scintillation

Counter (LSC, Packard Tri-Carb 2300TR, Packard Instrument Company, Meriden, CT) immediately after their collection. A calibration curve was prepared in the same way to quantify the radioactivity and equivalent concentration. The conversion of radioactivity measured to equivalent concentration was based on the activity provided by the vendor of the target compound. The radioactivity irreversibly bound to the solids was quantified by

14 collecting in scintillation liquid the CO2 generated by the incineration of the solids after their extraction in the ASE.

4.2.2.2 LC/MS/ANALYSIS

Quantification of estrogens was conducted by LC/MS/MS. An Agilent 1200

Series UPLC coupled with a 6410 Triple Quad and an Electrospray Ionization source was used for this purpose. A C-18 column (Zorbax Eclipse XDB-C18, 2.1x50 mm, 3.5 μm,

Agilent) was used for separation, with a methanol/water gradient buffered with ammonium acetate (2 mM). The calibration standards, liquid samples and solid extracts were derivatized with NaHCO3 and dansyl chloride (100 μL and 200 μL, respectively) for 15 min and 60 °C. This derivatization reaction was used to improve the fragmentation of the estrogens (Lien et al., 2009). After the mix cooled down, the injection solvent

(50% of methanol in water) was added and samples were subsequently filtered through

0.2 μm pore size PTFE filters and injected in the LC/MS/MS (injection volume: 1 μL).

87 Two Multiple Reaction Monitoring (MRM) transitions in positive mode were employed

14 14 to quantify C-E2 and d4-EE2. The lack of a standard of C-E1 only allowed a qualitative analysis of this compound. The MRM transitions selected corresponded to the

+ 14 14 precursor ion of the derivatized estrogen [M] ( C-E2: 508, C-E1: 506, d4-EE2: 534) and two characteristic fragments of the dansyl group (m/z: 171 and 154).

4.2.3 EXPERIMENTAL DESIGN

A series of serum bottles were set up in triplicates in the dark in an environmental chamber set at 4 °C. The bottles were sacrificed at predetermined sampling times. Each bottle was filled with 100 mL of Super Q water containing 1.4 g L-1 of the model

-1 vegetable material (rabbit food), 20 mg L of sodium azide (NaN3) as a biological inhibitor (Johannes and Majcherczyk, 2000), 0.33 g L-1 of dipotassium phosphate as

-1 14 buffer (KH2PO4), and 5000 ng L of the target compound, C-E2. The solution was mixed in a rotating tumbler for the duration of the experiment. Time 0 h measurements were taken from the aqueous solution containing biological inhibitor, buffer, and the target compound without the addition of rabbit food. Additional samples with same composition as the time 0 h samples were set up as controls, and sacrificed at the initial and last sampling events of the experiment.

14 To assess any potential formation of carbon dioxide (CO2 and/or CO2) resulting from biotic activity, the serum bottles were replaced with respirometry flasks in one of the experiments. The flasks were closed and contained a CO2 trap charged with potassium hydroxide and the indicator Alizarin Red. At the end of the experiment, the

88 contents of the flasks were acidified with hydrochloric acid to facilitate in the transfer of

14 CO2 and/or CO2 from the bulk solution to the trap. After acidification, the sacrificed flasks were stirred for an additional 24 h period prior to opening.

Additional batch experiments were performed to optimize sampling times and analytical method. Non-radiollabeled E2 was used in these experiments because of cost considerations when compared to 14C-E2, and to minimize the use of and exposure to radioactive material, as well as to reduce waste generation.

4.3 RESULTS AND DISCUSSION

Prior studies in our research group (Chapter 3; Esperanza et al., 2007) evaluated the fate of steroid hormones in WWTPs. Unexpected behavior exhibited by the estrogens

(E1, E2, E3, and EE2) in the refrigerated feed reservoirs provided the motivation to further investigate the potential abiotic transformation of these chemicals. In summary, the total concentration of estrogens (analyzed independently in aqueous and solid phases) was found to decrease over time when placed in a chamber maintained at 4 °C and in the absence of biological activity. The culprit of this behavior was determined to be a model vegetable material (rabbit food). This substance was added to a medium strength synthetic wastewater (Metcalf and Eddy, 2003) to simulate organic and vegetable wastes discharged into sewer systems.

Figure 4-3 shows the data for the time varying concentration of E2 in the simulated wastewater. This figure reveals that after 72 h of contact, only 17% of the

89 initial concentration of E2 (5000 ng L-1) was accounted for (12% in the aqueous phase and 5% in the solid phase). The remaining 83% of the E2 was hypothesized to have been either irreversibly adsorbed on the rabbit food or abiotically transformed to a different compound. The experiment examining the time-varying concentration of E2 when exposed to rabbit food was repeated using 98% labeled 14C-E2. Results from LC/MS/MS analysis of samples from this experiment are also shown in Fig. 4-3. The concentration of 14C-E2 in the liquid phase is represented by an open triangle, while open squares represent the concentrations extracted from the solids and the sum of the two is expressed as open circles. The amount of 14C-E2 recovered after 72 h was 15 and 7% in liquid and extractable solid phases, respectively. This set of data exhibits a strong agreement with the data from the earlier experiment.

Monitoring for 14C-E2 in this study allows for separation between contributions of abiotic transformations and irreversible adsorption of the parent compound and/or transformation products on the rabbit food solids. Figure 4-4 presents the results from one of the batch experiments carried out in serum bottles. In Fig. 4-4, the equivalent concentration of 14C-E2 at each sampling event, calculated from the radioactivity measurement, is shown on the left side of each data bar. The white, grey and dark grey portions correspond to the concentration measured in the liquid phase, extractable solids, and non-extractable solids, respectively. The sampling events from time 0 to 72 h correspond to the samples in which the vegetable material was added; on the other hand, the bars labeled as C0 and C72 show the data for the control samples (without addition of rabbit food) at 0 and 72 h, respectively. These three different fractions were obtained as

90 shown in Fig. 4-2. The radioactivity measured in the extractable solid phase was that measured in the solvent extract, while the radioactivity analyzed in the non-extractable solid phase represents the amount measured after the oxidation of the residue of the

14 extracted solids. CO2 and/or CO2 evolved in the system was not monitored in this specific run. As can be seen from the left side of the data bar on Fig. 4-4, a mass balance on radioactivity was closed by adding the concentrations measured in the three phases mentioned above. Additionally, in the control samples, the equivalent concentration of

14C-E2 stays constant and in agreement with the initial amount spiked for the duration of

14 the experiment. The absence of formation of CO2 and/or CO2 as a result of any biotic activity was confirmed in a batch test performed using respirometry flasks. In the run where the samples were prepared in respirometry flasks, quantitative recovery of radioactivity (>90%) was also achieved through the summation of the amounts measured in aqueous and solid phases (extractable plus non-extractable).

In Fig. 4-4, the right side of each data bar represents the concentration of 14C-E2 measured by LC/MS/MS. The dotted white and dotted grey bars correspond to the absolute concentration measured in liquid and extractable solid phases, respectively. The differences between the values determined by the two analytical methods (LSC and

LC/MS/MS) in aqueous and extractable solid phases confirm the occurrence of an abiotic reaction that is responsible for transforming 14C-E2 to an unidentified product and explains the reduction in the measured 14C-E2 concentrations. Even though radioactivity was measured by LSC in liquid and extractable solid phases, the signal was emitted by a chemical other than 14C-E2 as the concentration of this compound, analyzed by

91 LC/MS/MS, was lower than that computed as the equivalent radioactivity. The maximum divergence in the concentration values measured by LSC and LC/MS/MS occurred at 72 h; these were 38 and 9% in liquid and extractable solid phase, respectively. At 12 h and

24 h, the differences measured in the extractable solid phase was constant (7%), and slightly increased over time in the liquid phase (from 17 to 23%). These concentrations can most likely be assigned to unknown byproducts formed during the experiment as a consequence of catalytic transformation. On the other hand, the concentration measured by LC/MS/MS analysis in the control samples (C0 and C72) matches the equivalent concentration calculated form the radioactivity measurement, confirming that the transformation of estrogens was abiotic and occurring exclusively in the presence of rabbit food.

Formation of 14C-E1 was qualitatively monitored throughout the duration of the experiment to assess whether any of the 14C-E2 was converted to 14C-E1 as is reported to occur under aerobic biotic conditions, or through any other chemical process. No peak, corresponding to the characteristics MRM transitions of 14C-E1, was identified at a retention time similar to that corresponding to non-labeled E1 for any of the sampling events. Furthermore, E1 was always monitored quantitatively in all the tests performed with E2 for optimizing the experimental methodology. As in the case of 14C-E1, the non- labeled E1 was not detected in any run. Consequently, a catalytic reaction following an oxidative coupling mechanism appears to be the principal mechanism for the observed transformations.

92 In Fig. 4-5 a mechanism is proposed for the disappearance of estrogens in the presence of rabbit food. This mechanism is based on the oxidative coupling of phenolic compounds, thoroughly studied in soils (Huang et al., 1995) and activated carbon (Vidic et al, 1993a). Initially, the target compound E2 is present in solution. After coming in contact with the rabbit food, E2 can partition reversibly to the surface of the solid material (depending upon its hydrophobicity) and, simultaneously, a semiquinone radical can be formed. This radical will either follow a cross-coupling reaction with another radical present in the aqueous phase or react with the superficial functional groups in order to be incorporated into the material (referred in the figure as irreversible adsorption). Similarly, the first reaction product of the oxidative coupling of E2

(potentially a dimer) can undergo the same transformation: reversible sorption and radical formation with subsequent reaction with other radical or superficial groups. This proposed mechanism would explain the distribution of 14C-E2 and the byproduct(s) in the different phases analyzed: aqueous, extractable solid and non-extractable solid. As mentioned before, the concentration of 14C-E2 was measured by LC/MS/MS, while the byproduct(s) were quantified as the difference between the equivalent concentrations measured by LSC and LC/MS/MS.

At 12 h, the percent of radioactivity in liquid phase was reduced to 64% and decreased an additional 12% in the next 48 h. The measurement of extractable radioactivity was more stable during the experiment, with measured values of 21, 20, and

16% at 12, 24, and 72 h. On the other hand, the non-extractable fraction increased over time from 17 to 25%. Variations with time of the 14C-E2 concentration determined by

93 LC/MS/MS follow a similar pattern to the changes measured by LSC. However, the drop in liquid phase was more pronounced: 33% within 48 h (from 48 to 15%). To better picture the overall kinetics of the various processes occurring simultaneously in the reaction mixture, the concentrations of 14C-E2 and byproducts are represented individually over time in liquid and extractable solid phases in Fig. 4-6. An additional bar shows the concentration of both compounds irreversibly bound to the solids. The abiotic reaction appeared to be the fastest mechanism in the disappearance of 14C-E2, since the slope of the decrease in the concentration of 14C-E2 in liquid phase (white bars in Fig. 4-6) is higher than that corresponding to the generation of byproduct(s) staying in liquid phase (concentration represented in Fig. 4-6 by grey patterned bars). And the adsorption process appears to force the accumulation of the byproduct(s) in solution.

What posed a bigger challenge was our attempt to characterize how the parent compound and the products of the reaction distribute between reversible and irreversible adsorption because only total radioactivity could be measured. In addition, the direct reaction of 14C-

E2 and/or its byproduct(s) with the surface chemical groups looked less favorable than catalytic reaction in liquid phase since the radioactivity values in the solid residues remained very similar during the experiment.

Additional experimentation employing Liquid Chromatography coupled with

Quadrupole Time of Flight Mass Spectrometry and Ion Trap Mass Spectrometry is required to accurately identify the reaction products. The analysis of the samples using the LC/MS/MS in scan mode did not provide any meaningful information when trying to identify the byproducts because any potential peak was hidden under the spectra of the

94 matrix. Due to the complexity of the mechanism involved in the transformation of estrogens (Fig. 4-5) and the variety of experimental conditions employed in related studies, it is difficult to predict and compare the yield of the reaction in the different scenarios. Singular experimental conditions may shift the oxidative coupling reaction or other oxidative transformation toward either kinetically or thermodynamically favored end-products (polymers or quinone-derivatives and E1, respectively).

Based on the data currently available, we can hypothesize the formation of transformation products more hydrophobic than E2, such as polymers, which could result from an oxidative coupling reaction. Our previous work suggests that at 12 h, the partition equilibrium of estrogens between the aqueous and solid phases is reached

(Chapter 3). Furthermore, at this sampling time it can be first assumed that leaching to the water of reversibly-bound 14C-E2 to undergo the abiotic transformation is minimal; and second, that there is not accumulation of byproduct(s) in solution yet because of the faster kinetics of the abiotic reaction when compared to the adsorption process. Hence, a partition coefficient can be computed, as concentration in solid phase divided by the concentration in the liquid phase, for 14C-E2 and the byproduct(s). The partition coefficients were 0.23 and 0.30 L (g solids)-1 for the parent compound and byproduct(s), respectively, suggesting that the later is a more hydrophobic chemical. This would be in agreement with the general mechanism of the oxidative coupling process, with dimers and to a lesser extent trimers, of E2 being the expected byproducts, as described by previous research (Cajthaml et al., 2009; Mao et al., 2010). Higher chain polymers are very unlikely to occur because of the steric hindrance due to the large size of the

95 molecule. Other studies have reported the formation of E1 and/or more polar unidentified quinone-type compounds under abiotic conditions (Casey et al., 2005; Sheng et al.,

2009), mainly in soils and sediments. As mentioned earlier, our present work has confirmed the absence of E1.

To investigate the possibility of an enzyme catalyzing the transformation of estrogens, the activity of lignolytic enzymes was monitored. Peroxidases, a class of the aforementioned enzymes, require the presence of a reaction activator (such as hydrogen peroxide) to act as catalyst. Since there were no chemicals that could act as activator in our system, the activity of this type of enzyme was not quantified. Monitoring of laccases’ activity in rabbit food was done utilizing 2, 6-dimethoxyphenol, a known substrate that undergoes oxidation in the presence of these enzymes (Blánquez and

Guieysse, 2008; Johannes and Majcherczyk, 2000). To correct for the presence of solids in our system, a modification of a published method (Johannes and Majcherczyk, 2000) was utilized. Measurements provided negligible values for the activity at the experimental conditions (pH 5, room temperature and without addition of inhibitors).

Furthermore, the potential catalytic activity of laccases would have been more suppressed

-1 at temperature of our experiments, 4 °C, and in the presence of 20 mg L of NaN3,

(Johannes and Majcherczyk, 2000; Gianfreda et al., 1999).

Although the ultimate catalyst is still unknown, but it is hypothesized that metallic oxides in the rabbit food are the potential candidates. Some of these oxides, like the ones with manganese, are known to act as a true catalyst or as an oxidant, being consumed

96 during the course of the reaction (Huang et al., 1995). Also molecular oxygen could be the mediator in this catalytic process. In fact, prior studies carried out in our research group (Vidic et al., 1990; Vidic et al., 1993b; Lu and Sorial, 2007) established that phenolic compounds, when exposed to activated carbon and dissolved oxygen, polymerize through the oxidative coupling mechanism. The same authors reported that the relative affinity of different phenolic compounds toward oxidative coupling on the surface of activated carbon was related to the critical oxidation potential of the phenolic compounds and the presence of specific surface functional groups and metallic oxides in the activated carbon. Analogous conclusions were established regarding the polymerization of phenolic compounds by soils, for their removal from groundwater

(Colarieti et al., 2002). Enzymatic activity does not appear to be the likely cause of the transformation of E2 in our system; a more detailed discussion is included in the

Supplementary Material.

4.4 CONCLUSIONS

In summary, the abiotic transformation of E2 in the presence of vegetable matter has been confirmed by the difference in the equivalent concentration measured by LSC and LC/MS/MS in both liquid and solid phases. Most likely, oxidative coupling of the estrogens is catalyzed by a still unidentified chemical. Simultaneously with abiotic transformation, irreversible adsorption also occurs. We hypothesize that adsorption can mediate this transformation by either of two processes (as shown in Fig. 4-5). In the first one, E2 and its byproducts partitioned irreversibly to the solid phase, and in the second, the phenoxy radicals formed in the E2 molecule incorporated into the matrix through

97 covalent bonding with the functional groups on the surface. However, the individual contributions of E2, byproduct and/or covalent bonded material to the non-extractable radioactivity cannot be estimated due to the destructive nature of the analysis.

Very little is known about the underlying mechanisms responsible for the removal of estrogens from the environment. The exact role of the abiotic processes involved in their elimination, especially in WWTPs, needs to be elucidated. To the best of our knowledge, this is the first work focused on providing a preliminary characterization and confirmation of the catalytic transformation of estrogens in the presence of a model vegetable waste similar to the residues found in sewer. These insights will be extremely helpful in the optimization of sustainable technologies for wastewater treatment because it will help to minimize health and environmental risks derived from exposure to EDCs.

Furthermore, the understanding of the abiotic transformation of estrogens may be extrapolated to other EDCs and micropollutants with similar chemical structure, such as bisphenol A and alkylphenolic surfactants.

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103 14 Figure 4-1. Structure of 17β- C4-estradiol.

OH

H

H H

HO * 14C

104 Figure 4-2. Analytical protocol.

SAMPLE

Filtration

LIQUID SOLID+FILTER

SPE C-18 ASE Alumina Clean-up LSC Derivatization Residue Solvent Extract

Oxidation Alumina Clean-up LC/MS/MS C-18 clean-up

Derivatization 14 CO2

LSC

105 Figure 4-3. Percentage recovered of E2 vs time. Solid symbols: E2.

14 Open symbols: C4-E2.

100 Liquid phase - E2 Solid phase - E2 Total - E2 14 Liquid- C4-E2 14 80 Solid - C4-E2 14 Total - C4-E2

60

% Recovered 40

20

0 0204060 Time, h

106 14 Figure 4-4. Percentage of concentration recovered of 17β- C4-estradiol vs time, from

radioactivity measurement (left side of bar) and LC/MS/MS analysis (right

side of bar), in liquid (L), extractable solid (ES) and non-extractable solid

(NS) phases.

* C0 and C72 are the control samples sacrificed at 0 and 72 h, respectively.

RADIOACTIVITY LC/MS/MS MEASUREMENT ANALYSIS Non-extractable Solids Byproducts Extractable Solids Extractable Solids 14C-E2 Extractable Solids Byproducts Liquid 120 Liquid 14C-E2 Liquid

100

80

60

40 % Concentration

20

0 0 122472C 0C 72 Time, h

107 Figure 4-5. Proposed scheme of the abiotic transformation of E2.

Irreversible adsorption Solid phase Reversible adsorption

Water kow kow E2 E2● Byproducts Byproducts● Byproducts’… (dimer) (trimer) Longer chain compound unlikely to occur because of steric hindrance

108 14 Figure 4-6. Concentration of 17β- C4-estradiol and unidentified byproduct(s) vs time in

liquid (L), extractable solid (ES) and non-extractable solid (NS) phases.

5000 E2-ES BYPRODUCT-ES E2-L 4000 BYPRODUCT-L E2+BYPRODUCT NS -1

3000

2000 Concentration, ng L ng Concentration,

1000

0 0 122436486072 Time, h

109 Chapter 5. ROLE OF MOLECULAR OXYGEN IN THE ABIOTIC

TRANSFORMATIONS OF ESTROGENS IN THE PRESENCE OF

VEGETABLE MATTER

ABSTRACT

This study characterizes the abiotic transformation of estrogens during wastewater transport and treatment. The effect of oxygen in the catalytic transformation of the

14 estrogens in synthetic wastewater was evaluated using 17β-estradiol (E2) and 17β- C4- estradiol (14C-E2) as model compounds. Batch experiments were run under both oxic and anoxic conditions. In order to accomplish an accurate mass balance of the target estrogen, two analyses were performed simultaneously: first, radioactivity counting, and second,

14 14 quantitation of E2 and C-E2, as well as their transformation product estrone and C4- estrone, by Liquid Chromatography tandem Mass Spectrometry. Under oxic conditions, the concentration of 14C-E2 was found to decrease 78% in 72 h. The amount measured at that time was 15% and 7% of the initial concentration in aqueous and solid phases, respectively. Conversely, when the estrogens were contacted with the synthetic influent under anoxic conditions, E2 was quantitatively recovered after 72 h (70% and 22% in aqueous and solid matrices, correspondingly). These results suggest that when the concentration of dissolved oxygen is null or limited, catalysis through an oxidative coupling mechanism is halted. Therefore, wastewater treatment technologies and other processes involving anoxic stages may show a reduced overall removal efficiency for the elimination of estrogens from the environment.

110 5.1 INTRODUCTION

Endocrine Disrupting Chemicals (EDCs), along with pharmaceuticals and personal care products, have become a major concern in the past decade and still constitute an emerging topic for the scientific community and the general public.

Estrogens are among the most studied EDCs due to their potent disrupting effect and, in most cases, their natural origin in animal and human excretions. The significance of understanding the fate of estrogens in the environment is not limited to the necessity of their attenuation in the environment, it also resides in their chemical structure, which is commonly found in steroidal natural products, consumer products, and pharmaceuticals.

The structure of estrogens consists of a sterane-type backbone and a phenolic group in ring A (Fig. 5-1); the presence of this phenolic group makes estrogens an ideal surrogate for predicting how other micropollutants will behave in the environment.

In recent years, extensive research has been performed to determine the fate of estrogens in different environmental matrices (Kolpin et al., 2002; D'Ascenzo et al.,

2003; Hanselman et al., 2003; Casey et al., 2005; Khanal et al., 2006). Additionally, several studies have been conducted to assess the efficiency of wastewater treatment technologies in attenuating estrogens in wastewater streams (Joss et al., 2004; Esperanza et al., 2007; Bolong et al., 2009; Janex-Habibi et al., 2009). Overall, conventional wastewater treatment plants have not been found to adequately attenuate these compounds (Khanal et al., 2006) and advanced treatment systems seem to only provide short-term solutions (Joss et al., 2008). Furthermore, the economic and energy requirements of these processes need to be carefully assessed (Lundstrom et al., 2010) to

111 determine the sustainability of these solutions, as well as their application at a global scale.

A common flaw in the early work in this field is the assumption that only biodegradation and adsorption processes were involved in the elimination and transportation of estrogens in the environment. This was partially caused by the lack of sensitive analytical instrumentation as well as the exclusive application of indirect mass balances, where only liquid phases were considered.

The occurrence of catalytic reactions, mediated by metals or their oxides, which eliminate phenolic chemicals, such as estrogens, and anilines from the environment is well documented in soils and aquifer materials (Huang et al., 1995; Li and Lee, 1999; Lee et al., 2003; Colarieti et al., 2002; Hanselman et al., 2003; Sheng et al., 2009). However, little attention has been devoted to these reactions in wastewater transport and treatment.

These abiotic processes may play a key role in the elimination of estrogens from the environment, but only a few studies (on their role during wastewater treatment) have been published to date under laboratory conditions (Rudder et al., 2004; Forrez et al.,

2009; Sheng et al., 2009). Moreover, the use of biogenic manganese and other metals has recently been proposed as a potential alternative for wastewater treatment (Hennebel et al., 2009). The implementation of these reactions in engineered systems or their enhancement in natural scenarios will possibly be an aid in the minimization of economic and energy costs of the different treatments. Assessment of the impact of environmental variables on these catalytic reactions is required for a more comprehensive understanding

112 of the fate of estrogens in natural and engineered systems. The outcomes from this study could aid in the development of novel technologies for control of these compounds during wastewater treatment.

Previous work in our research group (Chapter 3) identified the occurrence of an abiotic transformation of estrogens in the presence of a model vegetable material that is similar to vegetable residues discharged to the sewer from domestic and natural sources

(e.g., humic substances). In the present study, the influence of molecular oxygen on the rate of the abiotic transformation of estradiol (E2) was studied using 17β-E2 and 17β-

14 14 14 C4-estradiol ( C-E2) as estrogenic model compounds. The use of C-E2 provided the opportunity of detecting and monitoring the presence of estrone (as 14C-E1) and other unidentified byproducts.

5.2 MATERIALS AND METHODS

5.2.1 REAGENTS AND CHEMICALS

Two estrogens, E2 and 14C-E2, were examined in this study. E2 (>98%) was obtained from Sigma-Aldrich (Milwaukee, WI) and 14C-E2 was purchased from

American Radiolabeled Chemicals Inc. (Saint Louis, MO). 14C-E2 had an activity of 55

-1 mCi mmol and 98% of it radiolabelled. d4-Ethinylestradiol (C/D/N Isotopes Inc.,

Canada) was utilized as a surrogate. Dansyl chloride (from Sigma Aldrich, Milwaukee,

WI) and sodium bicarbonate (NaHCO3) served as derivatization reagents for the Liquid

Chromatography/Mass Spectrometry analysis (LC/MS/MS).

113 5.2.2 ANALYTICAL PROCEDURE

Figure 5-2 represents the different analytical protocols followed in each of the batch experiments. Common to all of the protocols was the individual analysis of aqueous and solid phases, which were performed to accurately estimate the fate of the target compound. At each sampling event, triplicate serum bottles were sacrificed.

The solid line in Fig. 5-2 represents the standard procedure followed in the batches that were run under oxic conditions and used non-radiolabelled E2. After filtration with glass fiber filters, liquid and solid samples were extracted, cleaned-up, and derivatized prior to LC/MS/MS analysis. A detailed description of the analytical method can be found in Chapter 2.

To prevent exposure of samples to molecular oxygen in the anoxic experiments, the filtration of the samples and the solid phase extraction of the aqueous samples were performed inside an anaerobic hood. Additionally, before opening the bottles, the head- space composition was analyzed by Gas Chromatography with Thermal Conductivity

Detection (GC/TCD) to confirm the absence of molecular oxygen. The steps completed inside the anaerobic hood are represented by the squares with the dotted line in Fig. 5-2.

When 14C-E2 was used as the target compound, supplementary analyses were carried-out and are designated using a dashed line in Fig. 5-2. Radioactivity was counted in a Liquid Scintillation Counter (LSC, Packard Tri-Carb 2300TR, Packard Instrument

Company, Meriden, CT), using aliquots collected from the liquid samples immediately

114 after filtration as well as aliquots from the solids extracts after the extraction (using an

Accelerated Solvent Extractor (ASE)). The remaining solids, along with the filters, were combusted in an oxidizer (Harvey Biological Oxidizer OX700, R. Harvey, Hillsdale, NJ) to quantify the radioactivity irreversibly adsorbed on the extracted rabbit food.

A more comprehensive description of the radioactivity measurement protocol as well as the LC/MS/MS analysis can be found in Chapter 2. To quantify the target

14 compounds (E2 or C-E2, as well as the surrogate d4-EE2) in the LC/MS/MS, two

Multiple Reaction Monitoring (MRM) transitions in positive mode were employed.

These transitions corresponded to the pertinent precursor ion of the dansylated estrogen

14 (E2: 506, C-E2: 508, d4-EE2: 534) and two characteristic fragments of the dansyl group

(m/z: 171 and 154). In all of the experiments, E1 (or 14C-E1, depending upon the chemical initially spiked) was monitored. Due to the lack of standards of 14C-E1, this compound could only be qualitatively determined by monitoring the MRMs 506 171 and 506154. In the case of E1, standards were available; hence, calibration and quantitation of the analyte were possible (MRMs used: 504 171 and 504154).

Initial characterization of the metal content of the model vegetable material

(rabbit food) was also performed during this study. To determine the presence of metals, the raw rabbit food was analyzed by Inductively Coupled Plasma (ICP) (EPA method

6010c) after microwave digestion (EPA method 3051a). To study the concentration of metals leaching into the solution during the course of the experiments, the aqueous phase

115 of the solution containing the rabbit food was also analyzed following EPA method

6010c.

5.2.3 EXPERIMENTAL DESIGN

The experiment was designed so that sets of batch experiments were performed under both oxic and anoxic conditions (see Table 5-1 for description). In both cases, series of serum bottles were set up in triplicates in a controlled temperature room (at 4

°C). E2 or 14C-E2 was spiked into a synthetic wastewater and the samples were sacrificed at predetermined sampling times. Although the absence of biological activity in our experimental set-up (Chapter 3) was confirmed, samples were kept at 4 °C as a precaution. E2 and 14C-E2 were selected as model compounds because of the known transformation to E1 (or 14C-E1) as a result of biodegradation (Johnson and Sumpter,

2001) as well as other possible chemical transformations (Sheng et al., 2009). The use of

14C-E2 provided another major advantage; it allowed the simultaneous monitoring of radioactivity (that originated from the parent compound and any other potential byproducts) and the actual concentration of the estrogen measured by LC/MS/MS.

Consequently, the fate of E2, as a result of adsorption and chemical transformations, could be accurately determined.

For the oxic experiments, the working solution contained sodium azide (NaN3, 20

-1 -1 mg L ), as a biological inhibitor, and dipotassium phosphate (K2HPO4, 0.33 g L ) as buffer in Super Q water. The selected target compound (5000 ng L-1) was spiked into this solution. The corresponding amount of model vegetable material (rabbit food) was

116 weighed into each serum bottle to provide a final concentration of 1.4 g L-1, and 100 mL of the solution prepared as described above were added (the same solution used for time

0 h samples but without rabbit food) inside a fume hood. The bottles were then capped with polytetrafluoroethylene (PTFE) septa and placed in a tumbler for mixing at 4 °C and in the dark until the preselected sampling time.

Sample preparation for the anoxic experiments was performed inside an anaerobic hood. The composition of the gas inside the hood was monitored periodically by

GC/TCD to confirm the absence of molecular oxygen. Serum bottles with the adequate amount of rabbit food (to provide a final concentration of 1.4 g L-1) were introduced into the anaerobic hood five days prior the start of the experimentation in order to eliminate any residual molecular oxygen in the solids pores. A solution with the same composition

-1 -1 as the one used in the oxic experiments (20 mg L of NaN3 and 0.33 g L of K2HPO4) was purged with nitrogen and then immediately placed into the anaerobic hood for three days. Immediately before filling the serum bottles with 100 mL of the solution, the

14 -1 selected target compound (E2 or C4-E2) was spiked at 5000 ng L . Although NaN3 is ineffective in arresting biological activity under anaerobic conditions, it was added to the anoxic solution to mimic the chemical composition of the oxic solution. To assure the absence of molecular oxygen in the anoxic serum bottles, sodium sulfite (Na2SO3) was spiked into each bottle before capping them. The final concentration of the Na2SO3 was

200 mg L-1. Once the serum bottles were closed, they were taken out of the anaerobic hood and placed in a tumbler in a controlled temperature room at 4 °C and in the dark until they were sacrificed.

117

5.3 RESULTS AND DISCUSSION

The catalytic transformation of estrogens (E1, E2, estriol, and ethinylestradiol) in the presence of a vegetable model material, most likely through an oxidative coupling mechanism, was previously identified in our research (Chapter 3 and 4). The combination of biological degradation, enzymatic catalysis, and/or irreversible adsorption proved to be inadequate when it came to achieving closure in the mass balance for the estrogens.

Figure 5-3 (a) shows the decrease in concentration with time for E2. In contrast, the concentration of testosterone was found to remain constant and in agreement with the amount initially spiked under the same conditions (Fig. 5-3 (b)).

Figure 5-4 (a, b, c) summarizes the results from different batch experiments, which were run under oxic and anoxic conditions, using 14C-E2 or E2 as model compounds. Figure 5-4 (a) shows the percent of radioactivity measured over time in a batch experiment in which 14C-E2 was spiked. Void bars correspond to the results under oxic conditions and dashed ones correspond to the anoxic samples. In both cases, the white, light grey, and dark grey portions correspond to the amount of radioactivity measured in the liquid phase, in the extracts collected from the ASE, and in the irreversibly bound fraction of the extracted solids, respectively. As it can be observed in

Fig. 5-4 (a), the radioactivity mass balance was closed over the 72 h experimental period for both oxic and anoxic conditions. Additionally, while the amount of radioactivity irreversibly bound to the solids under oxic conditions increased over time (8% from 12 h to 72 h of exposure), the amount of radioactivity measured in the oxidized solids was

118 negligible at the end of the experimental time (72 h) for the samples kept under anoxic conditions. This indicates that the incorporation of 14C-E2 to the solids, either by irreversible adsorption or covalent bonding (as result of the oxidative coupling reaction with the functional groups on the surface of rabbit food), is not taking place. In the samples prepared without limitation of molecular oxygen, simultaneous to the increase of radioactivity in the non-extractable solid phase, radioactivity declined in liquid and extractable solid phases. In the liquid phase, the drop in radioactivity was more pronounced between 0 and 12 h, thereafter steadily decreasing throughout the duration of the experiment. On the other hand, in the extractable solids, the decrease was more pronounced at the end of the experiment, probably because of the lesser impact of the partition equilibrium of 14C-E2 to solid phase at longer exposure times.

Figure 5-4 (b) shows the concentrations measured by LC/MS/MS, in the same set of experiments as in Fig. 5-4 (a) (same color code followed in both figures). In the oxic batch, a continuous decrease in the concentration of 14C-E2 in aqueous and extractable solid phases was observed, with the total amount measured at 72 h of only 23% of the spiked concentration. In contrast, at 72 h under anoxic conditions, 100% of the initial concentration spiked in the samples was measured as 14C-E2 (73% in the liquid and 27% in the extracted solids, respectively). After 72 h of the reaction, maximum differences in the concentrations (measured by LC/MS/MS) of the samples under oxic and anoxic conditions were encountered and corresponded to 53% in the aqueous phase and 20% in the extractable solids. The main conclusion that could be drawn from these results was that the presence of oxygen was essential for the occurrence of the catalytic

119 transformation through oxidative coupling of the estrogens when in contact with the rabbit food (Vidic et al., 1990; Colarieti et al., 2002). It is worth mentioning that the same batch of initial solution was used for the experiments (oxic and anoxic) included in Fig.

5-4 (a) and 5-4 (b). Also, the gas composition of the head-space of the bottles maintained in an anoxic environment was analyzed prior to processing the samples for radioactivity and LC/MS/MS analysis. This analysis showed that molecular oxygen content was found to be below detection in each bottle. 14C-E1 was monitored in all samples, oxic and anoxic, with negative results in all cases.

To better compare the differences between the equivalent concentration

(calculated based on the radioactivity measurements and the activity of 14C-E2 provided by the supplier) and the concentration detected in the LC/MS/MS analysis, both quantities were combined in Fig. 5-5. The absolute value of these differences could be attributed to the concentration of yet unidentified byproducts (different from 14C-E1). The columns on the left side show the results from the oxic batch and the columns on the right belong to the samples kept under anoxic conditions. White, light grey, and dark grey correspond to the equivalent concentration from radioactivity in aqueous, extractable solids and non-extractable solids, respectively. The dashed fraction within each bar represents the concentration measured in the LC/MS/MS (this value was not available for the non-extractable solids due to the destructive nature of the radioactivity analysis). The divergence in the values increased with time under oxic conditions in both liquid and extractable solid phases. A detailed discussion of this behavior can be found in Chapter 4.

On the other hand, the differences encountered in the anoxic samples fall within the

120 experimental error, as can be observed in Fig. 5-5. This corroborates the assumption that catalytic transformation was completely halted in the absence of molecular oxygen in the system.

Assuming that the mechanism followed in the catalytic transformation of E2 is oxidative coupling, the lack of oxygen does not allow the formation of the phenoxy radical in the structure of E2; consequently, the reaction with other radicals to form a dimer or with the functional groups on the surface of rabbit food does not occur. Both facts are confirmed experimentally by the matching concentrations from LSC and

LC/MS/MS analysis in aqueous samples and extractable solids and the absence of radioactivity in the non-extractable solids in the anoxic experiment.

To corroborate the results found using 14C-E2, another batch experiment was run with E2 under anoxic conditions where samples were collected at the same times as the oxic experiments. Results of the concentration measured by LC/MS/MS are included in

Fig. 5-4 (c). White bars correspond to aqueous sample and light grey bars to the extracted solids. The total concentration recovered in all sampling events remained constant and over 90%, confirming that in the absence of molecular oxygen, the only process occurring is the partition to solid phase. Moreover, the ratio between the concentrations found in liquid and solid phases also stayed constant (0.31±1), indicating that the partition equilibrium was reached before 12 h. This result is in agreement with our previous results (Chapter 3).

121 Oxidative coupling of phenolic chemicals has been widely studied in different environmental matrices and systems (Vidic et al., 1993; Huang et al., 1995; Li and Lee

L., 1999; Colarieti et al., 2002). Although this reaction may occur spontaneously in soils in the presence of oxygen at neutral and alkaline pH, the presence of a catalyst is normally required (Sorial et al., 1993; Huang et al., 1995). These catalysts can be separated into two groups: biotic and abiotic. The action of biotic catalysts, such as enzymes, in our system was previously eliminated (Chapters 3 and 4). Abiotic catalysts include metal oxides, clays, and organomineral complexes (Huang et al., 1995). Clays were proven not to act as a catalyst in the matrix under investigation (Chapter 3). Figure

5-6 shows the metals content in the rabbit food, as mg L-1 (concentration calculated taking into consideration the amount of rabbit food added in the synthetic wastewater, 1.4 g L-1), measured by ICP analysis. Copper, manganese, and iron oxides or complexes are reported as major species involved in the polymerization of phenolic compounds (Huang et al., 1995; Liyanapatirana et al., 2010) in environmental samples. These three metals were measured in the rabbit food (copper: 0.019±0.002 mg L-1; manganese: 0.193±0.004 mg L-1; iron: 0.466±0.033 mg L-1). To better understand the role these metals may play along with molecular oxygen in the transformation of estrogens, their concentration leached into the aqueous phase of the synthetic feed was quantified over time, by ICP analysis. The percent of the initial concentration for each of the metals measured in solution at each sampling event is shown in Fig. 5-7. While iron was not found to leach, the concentrations of manganese and copper increased over time, rising steadily to 37% for manganese and randomly in the case of copper. The rise in the concentration of the metals in the aqueous phase could be a consequence of the dissolution of their reduced

122 form (Mn2+ or Cu+), after its corresponding oxides, sparingly soluble in water, acted as electron transfer mediators between the estrogens and molecular oxygen. The kinetics of the reoxidation of Mn2+ under normal conditions in the presence of oxygen is much slower than Cu+; this would explain the steady increase of the concentration of manganese in the solution and its apparent action as an oxidant instead of a true catalyst.

On the other hand, copper is reported to act as a true catalyst when associated with (Huang et al., 1995), thus, other processes might be involved in its leaching into solution. There is no agreement on the fundamental mechanism of the reaction (Stone and

Morgan, 1984; Laha and Luthy, 1990); hence, without more experimental evidence of the oxidation state of the metals in the solid phase, it is difficult to hypothesize their exact role.

Nevertheless, the presence of oxygen was proven essential for the reaction to occur. It has been reported in the literature that manganese oxides could participate in the oxidative coupling of phenolic compounds and anilines under anoxic conditions (Stone,

1987; Laha and Luthy, 1990); however, in those studies, pure suspensions of Mn (III/IV) at high concentrations were employed, in contrast to the trace amounts found in natural environments. Colarieti et al. (2002) confirmed that in polluted waters, the polymerization initially proceeded in the absence of oxygen but the reaction later stopped. Instead, complete removal of the target chemicals was achieved when oxygen was present in the reaction media. In our current study, it is possible that the oxidation capacity of manganese present in the rabbit food was neutralized by the addition of

Na2SO3 to the anoxic solutions because of its high reducing potential.

123

5.4 CONCLUSIONS

In summary, the influence of molecular oxygen on the catalytic transformation of estrogens was determined in this study. It was confirmed that under anoxic conditions, the oxidative coupling was halted since the main oxidant was eliminated from the system.

Therefore, wastewater treatment technologies that rely on anaerobic/anoxic stages may present poorer removal efficiencies, since the enhanced elimination of estrogens via catalytic transformation would be halted when the amount of molecular oxygen is limited. Initial investigations suggested that the manganese present in the rabbit food played a key role in catalyzing the reaction under oxic conditions but additional research is needed to confirm this.

The extent of the occurrence of abiotic transformations also needs to be considered. In addition, further assessment of biological and physical processes utilized by treatment technologies for the elimination of estrogens and other micropollutants from the environment must be completed. Although work is still needed to optimize the yield of these reactions, as well as to identify the byproducts formed and their estrogenicity (in the case of EDCs) and other toxicological effects, the catalytic transformations of micropollutants offers a promising mechanism for the removal of estrogens during wastewater treatment.

Our findings regarding the catalytic transformation of estrogens, and the negative impact of the absence of oxygen, raise interesting possibilities for the future of

124 wastewater treatment technologies as well as the infiltration and transportation of estrogens to subsurface waters.

125 5.5 REFERENCES

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Colarieti, M.L., Toscano, G., Greco Jr, G., 2002. Soil-catalyzed polymerization of phenolics in polluted waters. Water Research 36, 3015-3022.

D'Ascenzo, G., Di Corcia, A., Gentili, A., Mancini, R., Mastropasqua, R., Nazzari, M.,

Samperi., R., 2003. Fate of natural estrogen conjugates in municipal sewage transport and treatment facilities. The Science of The Total Environment 302, 199-209.

Esperanza, M., Suidan, M.T., Marfil-Vega, R., Gonzalez, C., Sorial, G.A., McCauley, P.,

Brenner, R., 2007. Fate of sex hormones in two pilot-scale municipal wastewater treatment plants: Conventional treatment. Chemosphere 66, 1535-1544.

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Hanselman, T.A., Graetz, D.A., Wilkie, A.C., 2003. Manure-Borne Estrogens as

Potential Environmental Contaminants: A Review. Environmental Science and

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126 Hennebel, T., De Gusseme, B., Boon, N., Verstraete, W., 2009. Biogenic metals in advanced water treatment. Trends in Biotechnology 27, 90-98.

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Impact of Soil Component Interactions. Natural and Anthropogenic Organics. Vol. 1,

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Janex-Habibi, M., Huyard, A., Esperanza, M., Bruchet, A., 2009. Reduction of endocrine disruptor emissions in the environment: the benefit of wastewater treatment. Water

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Johnson, A., Sumpter, J., 2001. Removal of endocrine-disrupting chemicals in activated sludge treatment works. Environmental Science & Technology 35, 4697-4703.

Joss, A., Siegrist, H., Ternes, T.A., 2008. Are we about to upgrade wastewater treatment for removing organic micropollutants? Water Science and Technology 57, 251-255.

Joss, A., Andersen, H., Ternes, T., Richle, P.R., Siegrist, H., 2004. Removal of estrogens in municipal wastewater treatment under aerobic and anaerobic conditions: consequences for plant optimization. Environmental Science & Technology 38, 3047-3055.

Khanal, S.K., Xie, B., Thompson, M.L., Sung, S., Ong, S., van Leeuwen, J., 2006. Fate, transport, and biodegradation of natural estrogens in the environment and engineered systems. Environmental Science & Technology 40, 6537-6546.

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

127 contaminants in U.S. streams, 1999-2000: A national reconnaissance. Environmental

Science & Technology 36, 1202-1211.

Laha, S., Luthy, R.G., 1990. Oxidation of aniline and other primary aromatic amines by manganese dioxide. Environmental Science & Technology 24, 363-373.

Lee, L.S., Strock, T.J., Sarmah, A.K., Rao, P.S.C., 2003. Sorption and dissipation of testosterone, estrogens, and their primary transformation products in soils and sediment.

Environmental Science & Technology 37, 4098-4105.

Li H., Lee L.S., 1999. Sorption and abiotic transformation of aniline and alpha- naphthylamine by surface soils. Environmental Science & Technology 33, 1864-1870.

Liyanapatirana, C., Gwaltney, S.R., Xia, K., 2010. Transformation of by

Fe(III)-Saturated Montmorillonite. Environmental Science & Technology 44, 668-674.

Lundstrom, E., Bjorlenius, B., Brinkmann, M., Hollert, H., Persson, J.O., Breitholtz, M.,

2010. Comparison of six sewage effluents treated with different treatment technologies—

Population level responses in the harpacticoid copepod Nitocra spinipes. Aquatic

Toxicology 96, 298-307.

Rudder, J.d., Wiele, T.V.d., Dhooge, W., Comhaire, F., Verstraete, W., 2004. Advanced water treatment with manganese oxide for the removal of 17α-ethynylestradiol (EE2).

Water Research 38, 184-192.

Sheng, G.D., Xu, C., Xu, L., Qiu, Y.P., Zhou, H.Y., 2009. Abiotic oxidation of 17β- estradiol by soil manganese oxides. Environmental Pollution 157, 2710-2715.

128 Sorial, G.A., Suidan, M.T., Vidic, R.D., Brenner, R.C., 1993. Effect of GAC

Characteristics on adsorption of organic pollutants. Water Environment Research 65, 53-

56.

Stone, A.T., 1987. Reductive Dissolution of manganese (III/IV) oxides by substituted phenols. Environmental Science & Technology 21, 979-988.

Stone, A.T., Morgan, J.J., 1984. Reduction and dissolution of manganese (III) and manganese (IV) oxides by organics. 1. Reaction with hydroquinone. Environmental

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Vidic, R.D., Suidan, M.T., Brenner, R.C., 1993. Oxidative coupling of phenols on activated carbon: impact on adsorption equilibrium. Environmental Science &

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Vidic, R., Suidan, M., Traegner, U., Nakhla, G., 1990. Adsorption isotherms – Illusive capacity and role of oxygen. Water Research 24, 1187-1195.

129 Table 5-1. Summary of batch experiments.

Target compound E2 (*) 14C-E2 0 h A O A Sampling 12 h A O time 24 h A O 72 h A O A O: oxic conditions. A: anoxic conditions. (*) Majority of the previous work was performed with E2 under oxic conditions

130 Figure 5-1. Structure of sterane and target estrogens.

12 17 11 13

CD16 1 9 10 8 2 14 15 AB 3 5 7

4 6 Core Sterane Structure

OH OH

H H

H H H H

HO HO * 14C β β 14 17 -Estradiol 17 - C4-Estradiol

131 Figure 5-2. Analytical protocol.

Head-space gas analysis

SAMPLE

Filtration

LIQUID SOLID+FILTER

SPE C-18 ASE Alumina Clean-up LSC Derivatization Residue Solvent Extract

Oxidation Alumina Clean-up LC/MS/MS C-18 clean-up

Derivatization 14 CO2

LSC

132 Figure 5-3. (a) Percentage of E2 recovered over time, (b) Percentage of TEST recovered

over time.

(a) E2 INITIAL CONCENTRATION 4800 ng L-1

140

SOLID LIQUID 120

100

80

60 % RECOVERED %

40

20

0

SAMPLING TIMES: 1, 12, 24, 36, 48, 60, 72, 84, 96, 108,& 120 h.

(b) TEST INITIAL CONCENTRATION 4800 ng L-1

140 SOLID LIQUID

120

100

80

60 % RECOVERED%

40

20

0

SAMPLING TIMES: 1, 12, 24, 36, 48, 60, 72, 84, 96, 108,& 120 h.

133 Figure 5-4. (a) Percentage of radioactivity over time under oxic and anoxic conditions

(14C-E2), (b) Percentage of concentration over time under oxic and anoxic

conditions, measured by LC/MS/MS, (14C-E2) (c) Percentage of

concentration over time under anoxic conditions, measured by LC/MS/MS

(E2). (a) % RADIOACTIVITY 120

Oxic-Non Extractable 100 Anoxic-Non Extractable Oxic-Extractable Anoxic-Extractable Oxic-Liquid 80 Anoxic-Liquid

60

% Radioactivity % 40

20

0 0 122436486072 Time, h (b) % CONCENTRATION BY LC/MS/MS 120

Oxic-Extractable 100 Anoxic-Extractable Oxic-Liquid Anoxic-Liquid 80

60

% Concentration % 40

20

0 0 122436486072 Time, h (c) % CONCENTRATION BY LC/MS/MS 120

Anoxic-Extractable 100 Anoxic-Liquid

80

60

% Concentration % 40

20

0 0 122436486072134 Time, h Figure 5-5. Comparison of % concentration measured by LSC and LC/MS/MS over time

under oxic and anoxic conditions (target compound 14C-E2).

120 OXIC ANOXIC

100

NS-LSC 80 ES-LSC ES-LC L-LSC 60 L-LC % Recovered 40

20

0 0 12 24 72 072 Time, h

135 Figure 5-6. Concentration of metals in raw rabbit food.

20

0.5

0.4

0.3 15 0.2 -1

10

0.0 Al As Ba Cd Co Cr Cu Fe Mn Mo Ni Pb Sb Se Sr Ti V Zn Concentration, mg L Concentration, mg 5

0 Al AsBaCaCdCoCrCuFe K MgMnMoNa Ni Pb S SbSe Sr Ti V Zn Metal

136 Figure 5-7. Percentage of metal leached into solution over time.

120

100

80

n

o

i

t

u l

60

so

n

i

% 40

20

0 0 S Ti 1 MoPb Tim 12 Cr Fe e BaAl , h 24 Zn Ni NaCu 72 MgK Sr Ca tal Mn Me

Potassium (K) and sodium (Na) were added in the synthetic water mixture. Sample contamination with barium (Ba) occurred during the analysis of metals.

137 Chapter 6. SUMMARY, CONCLUSIONS, AND FUTURE WORK

The data reported in this work confirmed the occurrence of the catalytic transformation of estrogens (E1, E2, E3, and EE2), most likely through an oxidative coupling mechanism, in the presence of a model vegetable material (a surrogate of vegetable wastes found in sewers). The other targeted compounds in the study (TEST,

AND, and PROG) did not undergo this transformation because of the lack of a phenolic ring in their structure.

The phenomenon was modeled following a saturation type equation that is characteristic of catalytic processes. The values of the constants, maximum specific disappearance rate and the half-saturation constant, for the estrogens monitored (E1, E2,

E3, and EE2) suggested that the catalysis occurred in the aqueous phase, but this fact could not be confirmed in the present study. Depending on the focus of the investigations and the matrices used for promoting the catalysis, different mechanisms are proposed in the literature without agreement on whether the reaction occurs in the solid or liquid phase.

The combined use of a model vegetable material and radiolabeled estrogens (14C-

E2) provided fundamental information on the mechanism of the abiotic reaction. First, it was corroborated that E2 was transformed catalytically to, as yet, unidentified byproduct(s). Second, both, parent and transformation compounds, were found to partition between aqueous and solid phases. And third, the incorporation of the estrogens into the solid material was confirmed. This information could explain, in combination

138 with the specifics of biodegradation processes, the enhanced efficiency of treatment technologies for the removal of estrogens in which elongated retention times are employed.

The findings regarding the impact of molecular oxygen on the reaction rate was the final confirmation of the mechanism of the transformation of the estrogens, an oxidative coupling reaction. In environmental samples and engineered systems, it is broadly accepted that the presence of oxygen is essential for the occurrence of this reaction, and the presence of a catalyst is also normally required. Among the metals present in the model vegetable material, manganese was hypothesized to be the main candidate to catalyze the reaction, and preliminary results confirm this hypothesis. The main environmental implication of the effect of anoxic conditions on the oxidative coupling reaction rate is the lack of elimination of estrogens through the incorporation reaction with the lignin-type surfaces. This is relevant for situations such as sewage transport and other phenomena that involve the movement of estrogens through environmental matrices.

In order to be able to develop practical, economical, and measurable solutions for the removal of estrogens from wastewater while maximizing the yield of the catalytic transformation through an oxidative coupling mechanism, there is still the necessity for fundamental research. These should be designed to address the following unknowns:

• Identification of the byproducts generated by the catalytic reaction, their

estrogenicity and toxicity, and the potential reversibility of the reaction.

139 • Elemental characterization of the vegetable model material to discern the

specific role of metals and superficial chemical groups in the reaction

progression.

• Depiction of the ultimate mechanism involved in this catalytic

transformation, including its kinetics at relevant environmental conditions

and the effects of competing processes, such as biodegradation, in the

reacting medium.

• Assessment of the catalytic transformation of other priority pollutants,

such as bisphenols, alkylphenolic surfactants, triclosan, and other

phenolics and anilines and derivatives.

After the elucidation of these critical concepts, research efforts should focus on determining the biotic and abiotic mechanisms that are responsible for removal of estrogens and other phenolic contaminants in the various unit processes of wastewater treatment, including sludge treatment and disposal, at a pilot-scale operation. Also, the design of technologies that maximize the rate of this abiotic transformation should be evaluated.

140