Science of the Total Environment 473–474 (2014) 189–198

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Sorption, desorption and displacement of ibuprofen, estrone, and 17βestradiol in wastewater irrigated and rainfed agricultural soils

Juan C. Durán–Álvarez a, Blanca Prado b, Anouck Ferroud b, Narcedalia Juayerk b, Blanca Jiménez-Cisneros c,⁎a Centre of Applied Sciences and Technological Development, National Autonomous University of México, 3000 Avenida Universidad, Coyoacán, México City 04360, Mexicob Geology Institute, National Autonomous University of México, 3000 Avenida Universidad, Coyoacán, México City 04360, Mexicoc International Hydrological Programme (IHP), UNESCO, Paris, France

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• Sorption and transport of emergingpollutants were tested for two agri-cultural soils.

• Ibuprofen, estrone and estradiol weretested in wastewater irrigated andrainfed soils.

• Sorption of pollutants was higher forwastewater irrigated soil than forrainfed one.

• Transport of non-polar pollutants wasdelayed by soil.

• Wastewater irrigated soil was more effi-cient to retain pollutants than rainfedsoil.

⁎ Corresponding author. Tel.: +33 1 45 68 4002; fax: +E-mail address: bjimenezc@iingen.unam.mx (B. Jimén

0048-9697/$ – see front matter © 2013 Elsevier B.V. All rihttp://dx.doi.org/10.1016/j.scitotenv.2013.12.018

a b s t r a c t

a r t i c l e i n f o

Article history:Received 1 October 2013Received in revised form 6 December 2013Accepted 6 December 2013Available online 23 December 2013

Keywords:Agricultural soilsEnvironmental fateOrganic micropollutantsEndocrine disrupting chemicalsSorptionWastewater reuse

Sorption and leaching potential of ibuprofen, estrone and 17β estradiol were tested in two agricultural soils:one irrigated using municipal wastewater and the other used in rainfed agriculture. Batch sorption–desorptionexperiments and undisturbed soil column assays were carried out using both soils to which were addeda mixture of the target compounds. The three compounds were sorbed to a different extent by both soils:estrone N 17β estradiol N ibuprofen. Higher sorption was observed in the irrigated soil, which was attributedto the accumulation of organic matter caused by wastewater irrigation. Desorption of hormones was hystereticin the irrigated soil,while ibuprofen showed lowhysteresis in both soils. Retardation of the compounds' displace-ment was consistentwith the sorption pattern observed in the batch tests. Retardation factor (RF) was similar forthe three compounds in the two tested soils, indicating that the target compounds are much moremobile in thesoil columns thanwould be predicted based on their equilibrium sorption parameters. The results obtained in theexperiments clarify the role of wastewater irrigated soils as a filter and degradation media for the targetmicropollutants.

© 2013 Elsevier B.V. All rights reserved.

33 1 45 68 5811.ez-Cisneros).

ghts reserved.

190 J.C. Durán–Álvarez et al. / Science of the Total Environment 473–474 (2014) 189–198

1. Introduction

The reuse ofwastewater for agricultural purposes is a common prac-tice worldwide. An estimated 3.5 million hectares are globally irrigatedusing treated or untreated wastewater (Jiménez and Asano, 2008).Moreover, Hochstrat et al. (2005) foresee that a volume of reclaimedwastewater of the order of 2979 mm3/yr will be reused for differentpurposes in Europe by 2025. Irrigation using untreated municipalwastewater has notable benefits for agriculture such as: a) the increasein crop yields, attributable to the continuous supply of water andnutrients to the soil, leading to enhanced profits for farmers; b) theimprovement of soil quality, transforming barren soils into fertilecroplands; and in some cases, c) the recharge of the underlying aquiferwith potentially safe water due to the purification of wastewater as itinfiltrates through the soil (Bahri, 2008; Jiménez and Chávez, 2004).Conversely, wastewater irrigation poses real risks of pollution to soilsand crops, and is a potential source of contamination for water sourcesclose to the irrigated area (Toze, 2006). In this regard, increasing atten-tion is being paid to the so-called emerging pollutants. In recent years,pharmaceutically active substances such as the anti-inflammatorydrug ibuprofen ((RS)-2-(4-(2-methylpropyl)phenyl)propanoic acid),as well as the natural estrogenic hormones estrone (3-hydroxy-13-methyl-6,7,8,9,11,12,13,14,15,16-ecahydrocyclopenta[a]phenanthren-17-one) and 17β estradiol ((17β)-estra-1,3,5(10)-triene-3,17-diol)have been consistently detected in treated and untreated wastewaterat ng/L to μg/L levels, and inwastewater irrigated soils at concentrationsof μg/kg (Azzouz and Ballesteros, 2012; Santos et al., 2010).

Even at trace levels, these organic micropollutants may causeharmful effects to the exposed organisms. For example, ibuprofenmay cause genetic and systemic damage to some mussels and fishspecies (Ericson et al., 2010; Han et al., 2010), while estrone and17β estradiol are known to be potent endocrine disruptingchemicals capable of altering the reproductive health and genderratio of several aquatic species (Dammann et al., 2011; vonEngelhardt et al., 2004). Regarding terrestrial ecosystems, sex hor-mones can affect the vegetative cycle of alfalfa (Medicago sativa)(Shore et al., 1992), as well as lead to changes in the sex ratio offree life nematode communities in soil (Hu et al., 2011). Further-more, some crops, such as sweet corn, potatoes and sweet beans,can take up pharmaceuticals and hormones, and in some cases,these pollutants are able to translocate from roots to aerial tissues(Calderón-Preciado et al., 2012; Card et al., 2012). Due to the contin-uous occurrence of pharmaceuticals and hormones in wastewaterand wastewater irrigated soils as well as the potential effects theymay cause to exposed organisms, knowing the environmental fateof such pollutants is necessary in order to perform more accuraterisk assessments for ecosystems and human health.

Sorption–desorption batch tests in tandem with displacementcolumn assays provide valuable information on the retention of targetpollutants by soil particles as well as their potential to leach into theaquifer. Displacement experiments using undisturbed soil columnsallow the evaluation of the effects of both the chemical properties andthe physical structure of the soil on the mobility of the contaminants.The accumulation of organic matter, the increase in the soil hydropho-bicity (Tarchitzky et al., 2007) and the gain of structure in the porousnetwork of the soil caused by the application of wastewater may delaythe transport of the pollutants by increasing their retention by the soil.

The aims of this work were both to determine the sorption andleaching potential of three organic micropollutants, namely ibuprofen,estrone and 17β estradiol, in agricultural soils by considering the chem-ical composition and the structure of the soil; and to elucidate the effectof long-term wastewater irrigation on the retention and transport ofthese pollutants through the soil. To accomplish such objectives,sorption–desorption batch tests and displacement experiments usingundisturbed soil columns were carried out by testing two agriculturalsoils from central Mexico: one that has been irrigated using Mexico

City's untreated wastewater for 85 years and another where rainfedagriculture is practiced.

2. Materials and methods

2.1. Chemicals

All of the target compounds as well as the surrogatestandard ketoprofen were purchased from Sigma-Aldrich (St. Louis,MO). The internal standard 2,3-dichlorophenoxyacetic acid (2,3-D)was available from Riedel-de Haën (Seelze, Germany). The deuteratedestrogens [2H4] estrone and [2H3] 17β estradiol, used as surrogateand internal standards, respectively, were obtained fromCambridge Isotopes (Andover, MA). The derivatizing agents N-tert-butyldimethylsilyl-N-methyltrifluoroacetamide (MTBSTFA) with 1% oft-butyldimethylsilylchlorane (TBDMSCI) and N,O-bis(trimethylsilyl)trifluoroacetamide (BSTFA) with 1% of trimethylsilylchlorane (TMSCI)were also obtained from Sigma-Aldrich. The solvents used for theanalysis were HPLC grade and purchased from Burdick and Jackson(Morristown, NJ). The Oasis HLB extraction cartridges (200 mg, 60 cc)were purchased from Waters (Milford, MA). Standard solutions of themixture of the target pollutants were prepared at concentrations of10, 1 and 0.1 ng/μL, using methanol as solvent. These solutions wereused for spiking the water used in the sorption–desorption anddisplacement experiments. For the analytical procedure, internal andsurrogate standards were prepared at 10 ng/μL in methanol. Table 1displays the relevant chemical properties of the target compounds aswell as the limits of detection of the analytical technique used forquantification.

2.2. Soils

Two mollisols were collected from the Mezquital Valley, a region incentral Mexico where untreated wastewater has been used inagricultural irrigation for several decades. These soils were selected toassess the influence of untreated wastewater irrigation time on theretention/displacement of the target contaminants. Detailed informa-tion on the quality of the wastewater used for irrigation has beencovered in other studies (Chávez et al., 2011), and can be found in theSupplementary information section. Flood irrigation is carried outonce amonth, which has resulted in the accumulation of organicmatterin the irrigated soils; furthermore, because the cropland has a slightslope, migration of clay by runoff has led to its accumulation in thelower part of the plots. Soil samples were collected at the lower partof the plots.

Two types of sampleswere taken: disturbed soil for the sorption anddesorption experiments and undisturbed soil columns for the transportexperiments. Collection of disturbed soil samples was carried out usinga stainless steel trowel. Before taking samples, the upper 3 cm layer oforganic material (plant and biota residues) was removed. Undisturbedsoil columns were obtained alongside the sampling point where dis-turbed samples were acquired. Sampling of undisturbed soil columnsconsisted of the following steps (Prado et al., 2006): a 40 cm deep pitwas dug; then, soil monoliths were carved with a stainless steel knifeto achieve the cylindrical shape, 15 cm in height and 9 cm in diameter.Soil monoliths were put into stainless steel cases and then liquidparaffin (chemically pure, at 60 °C) was poured in the free spacebetween the soil monolith and the stainless steel case to fix the mono-lith to the column and avoid the border effect during the displacementexperiments. Two columns were obtained from each site.

Both disturbed soil samples and undisturbed soil columns were putinto plastic bags and stored at 4 °C until characterization. For character-ization, disturbed soil samples were used as collected, while a smallsample (~50 g) was withdrawn from the top of each soil column. Soilsamples were air-dried for 12 h, slightly crushed in a mortar andhomogenized by sieving them using a 2 mm pore sized metallic mesh.

Table 1Relevant chemical and physical properties of the target compounds.

Compound Chemical structure Molecular weight(g mol−1)

pKaa Solubility in waterb

(mg L−1)Octanol/water partitioncoefficientb (Kow)

Vapor pressureb

(mm Hg)Limit of detectionc

(μg kg−1)

Ibuprofen 206.29 4.5 21 2.48 1.4 × 10−7 0.1

Estrone 270.37 10.7 30 3.13 3.8 × 10−10 1.0

17β estradiol 272.37 10.7 3.6 4.01 3.6 × 10−11 1.0

a pKa: acidic dissociation constant.b Determined at 25 °C.c From Durán-Álvarez et al. (2009).

191J.C. Durán–Álvarez et al. / Science of the Total Environment 473–474 (2014) 189–198

The physical and chemical properties shown in Table 2 were deter-mined to soils using standard procedures (Soon and Hendershot,2008). The pH and electrical conductivity were measured in a 1:1 soil:CaCl2 10 mM suspension using a sensION156 HACH pH/conductivitymeter. The soil organic carbon content was determined using a PerkinElmer 2400 CHNS/O elemental analyzer. The bulk density was obtainedusing intact soil cores, which were taken directly in the field. Soilparticle size distribution and soil texture were determined using theBouyoucos hydrometer method. The specific surface area of the soilparticles was obtained using the nitrogen-adsorption BET method. Inaddition, the net charge of the soils was determined by the calculationof the ΔpH (i.e. the difference between pHKCl − pHH2O).

According to Uehara and Gillman (1980), zero and positive values ofΔpH are indicative of the variable charge of soil, while values of ΔpHlower than −0.35 are evidence of negative net charge in the soil. Thebackground concentration of the target pollutants was also determinedin the tested soils prior to the experiments.

2.3. Sorption–desorption tests

For the sorption–desorption experiments, 3 g (dry mass) of eachdisturbed soil sample was accurately weighed into 50 mL amber glasstubes; then, 15 mL of 0.01 M CaCl2 solution were added (the soil tosolution ratio was 1:5). The tubes were capped using Teflon lids andagitated in an orbital shaker at 80 rpm and 25 °C for 24 h. Next, analiquot of the standard solution containing the mixture of the target

Table 2Relevant physical and chemical properties of the studied soils.

Parameter Irrigated soil Rainfed soil

pH 8.0 ± 0.1 7.2 ± 0.1Electrical conductivity (μS/cm) 1792 ± 7 711 ± 2Organic carbon (%) 2.6 ± 0.08 0.8 ± 0.03Sand (%) 13 26.5Silt (%) 39 48.5Clay (%) 48 25CEC (cmol/kg) 37.9 ± 2 12.1 ± 2Specific surface area (m2/g) 66 ± 1 18 ± 0.8Net charge (ΔpH value) Negative (−0.98) Negative (−0.88)

Organic micropollutants background concentration (μg/kg)Ibuprofen 1.8 ± 0.3 bLODEstrone 0.9 ± 0.05 bLOD17β estradiol bLOD bLOD

bLOD: below of the limit of detection.

compounds was added to achieve concentrations of 0.01, 0.05, 0.1, 1.0,5.0 and 10.0 μg/L; each concentration was tested in triplicate. Thefraction of methanol in suspensions was maintained below 0.1% of thetotal volume to avoid the co-solvent effect. The selection of the testedconcentrations was based on the occurrence of the target pollutants inthe wastewater used for irrigation in the study zone (Chávez et al.,2011). The tubes containing the fortified suspension were then agitatedat 80 rpm and 25 °C for another 24 h. Sorption equilibrium time for thisexperiment was selected based on values reported in literature for sim-ilar compounds in soils of the irrigated area (Durán-Álvarez et al., 2012).After agitation, the tubes were centrifuged at 5000 rpm for 60 min toseparate the liquid phase and soil; then, the supernatants (~15 mL)were recovered.

A volume of fresh CaCl2 solution identical to the amount of superna-tant removed in the last step was added to each tube and the two-stagedesorption step was carried out using the same agitation and centrifu-gation conditions established for the sorption test. After each desorptionstage, the complete liquid phase (~15 mL) was recovered in glass vials.At the end of the experiment, the soil was also recovered, and both thesupernatants and soil were stored at −10 °C until chromatographicanalysis was carried out.

2.4. Displacement experiments

The mobility of the target pollutants was evaluated in the soil col-umns under steady-state conditions. The undisturbed soil columnswere placed on a rain simulator device consisting of a reservoir of500 mL equipped with 9 needles of 0.5 mm diameter to apply the de-siredwaterflow. The reservoirwasplaced at the top of each soil column.Water was supplied to the simulator from a bottle with a peristalticpump,which also pumped the leachate from thebottomof the columns.At the base of the column, the leachate was conducted to an online pH/conductivity meter and lastly divided into 7.5 mL sub-samples by afraction collector. Details of the rain simulator apparatus are providedin the Supplementary information section. Irrigation was carried outusing the 0.01 M CaCl2 solution. The solution was passed through thesoil column at a constant flow rate of 7.5 mL h−1. Care was taken toavoid water saturation of the soil. Table 3 shows the relevant parame-ters of the steady-state transport assays.

The experiment was divided into three stages. In the first stage theCaCl2 solution was applied to the soil columns to achieve the steady-state condition; steady-state was considered to be achieved whenequal flow rate, pH and EC values were observed for both the injectionsolution and the leachate. During the second stage, the pulse containingthe mixture of the target pollutants (ibuprofen at 10 μg/L and the

Table 3Experimental parameters of the soil column experiments.

Soil type Depth Bulk density θ v Darcy velocity Pulse duration(cm) (g cm−3) (cm3 cm−3) (cm h−1) (cm h−1) (cm3 cm−3)

Irrigated soil 0–15 1.0 0.41 0.284 0.0019 0.45Rainfed soil 0–15 1.1 0.40 0.267 0.0020 0.69

θ: soil water content; v: pore water velocity.

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hormones at 1 μg/L) and bromide as a conservative water tracer, in theform of KBr salt at 0.1 M, were applied to the soil columns for 0.5 porevolumes. A pore volume is the amount of water within the soil column,which is calculated bymultiplying the total volumeof the columnby thevolumetric water content of the soil at the equilibrium; for these soilcolumns, pore volume was ~300 mL. In the third and final stage, CaCl2solution with no compounds added was applied with the aim ofdisplacing the pollutants within the soil columns; this stage was carriedout for 13 pore volumes. In order to test the suitability of the Br− ion as aconservative water tracer for the tested soils, an additional columnexperiment was performed using the H2

18O isotope as water tracer.The experiment testing the two tracers was carried out in two separatecolumns by following the procedure described above. Leachate sampleswere stored at−10 °C prior to analysis to determine the concentrationof both the tracers and the target pollutants.

At the end of the experiment, the soil columnswereweighed and cutinto three segments of similar length. The soil of each section was ho-mogenized by sieving through a 2 mm metallic mesh and analyzed todetermine both the volumetric water content and the residual concen-tration of the target pollutants. The soil water content at steady statewas determined gravimetrically, for this, small soil samples (~20 g)were taken at the upper and lower part of the columns. The bulk densityof the soil was estimated by dividing the total mass of the soil monolithby its volume, considering the content of water.

2.5. Analytical methods

The concentration of bromide in the leachate samples wasdetermined using a ThermoScientific ion selective electrode, while con-centration of the 18O–water isotope was determined in a ThermoFinnigan MAT 253 stable isotope ratio mass spectrometer followingthe method proposed by Epstein and Mayeda (1953).

The concentration of the target compounds in the liquid samples(supernatants of the sorption–desorption tests and leachates from thecolumn experiments) was determined following the procedure devel-oped and validated by Gibson et al. (2007). The pH in the liquid sampleswas adjusted to 2 using sulfuric acid (98%); then, the surrogate stan-dards ketoprofen and [2H4] estrone were added. Samples were passedthrough Oasis HLB cartridges previously conditioned twice with 5 mLof acetone and once with 5 mL of 5% acetic acid. Samples were passedthrough the cartridges using a vacuum flow of 5 mL/min. Ibuprofenwas eluted from the cartridges with 5.5 mL of a mixture 40:60 ofacetone:sodium bicarbonate 0.1 M (adjusted to pH 10); then, thecartridges were dried using a vacuum at a flow rate of 10 mL/min for1 h. Following the drying step, the hormones were eluted with 5 mLof acetone. Both phases were concentrated using a gentle atmosphereof ultra-high purity nitrogen and the remaining water was removedfrom the samples by adding anhydrous sodium sulfate. Lastly, the inter-nal standards 2,3-D and [3H2] 17β estradiol were added and derivatiza-tion was carried out through the production of methylsilyl derivatesusing the agents MTBSTFA for ibuprofen and BSTFA for hormones.

Analysis of soils was performed using the method proposed andvalidated by Durán-Álvarez et al. (2009). Extraction of the targetcompounds was carried out through the pressurized liquid extractiontechnique, using a Dionex ASE® 200 device. 5 g of soil and 2 g of diato-maceous earth, the latter used as dispersing agent, were accuratelyweighed in 22 mL-ASE stainless steel cells and extracted using a

hexane:acetone:acetic acid (49:49:2 v/v/v) mixture. The extractionconditions were as follows: two cycles, 100 °C, 10.34 MPa, 0 min ofpre-heating, 5 min of heating time, 5 min of static time and flushingat 60%. The surrogate standards were added to the obtained extractsand the spiked extracts were evaporated down to a volume of ~3 mL.After evaporation, 20 mL of HPLC-grade water were added. Theresulting solutionswere passed through Oasis HLB cartridges, previous-ly conditioned as described above. Ibuprofenwas eluted from cartridgesusing a 40:60 acetone:sodium bicarbonate 0.1 M mixture, while hor-moneswere eluted using 5 mL of a 50:50 acetone:dichloromethane sol-vent mixture. After elution, the same sample preparation proceduredescribed for liquid samples was used. Recoveries achieved in the ex-traction of soils using the ASEmethodwere determined as 102% for ibu-profen, 93% for estrone and 99% for 17β estradiol.

Separation and quantification was carried out using a HP 6890 gaschromatograph in tandem with a HP 5397 mass selective detector.The chromatographic column was an Agilent HP-5MS capillary column(30 m × 0.25 mm, 0.25 μmof film thickness)with a stationary phase of5% phenyl–95%methylsiloxane. The carrier gaswasheliumat a constantflow of 1 mL/min, and 1 μL of samplewas injected in the splitlessmode.The oven temperature programwas as follows: 100 °C for 1 min, rampof 20 °C/min to 280 °C, and 280 °C for 10 min. The detector was used inthe selected ion monitoring (SIM) mode. The electron impact sourcetemperature was 230 °C with electron energy of 70 eV. Calculation ofthe analytes' concentration was done using the internal standardmeth-od. Quality assurancewas guaranteed by the use of surrogate standards.The recoveries obtained for surrogate standards were between 90% and96% for ketoprofen and 88 to 91% for [2H4] estrone. Laboratory blankswere also processed to determine the background concentration ofthe target compounds in the reagents and materials used during thesample processing and analysis. Concentrations of the target com-pounds in blanks, when detected, were in the range of 0.2 to 0.6 ng/L;such concentrations were subtracted from those found in samples.

2.6. Data analysis

Data obtained in the sorption–desorption experiments were fittedto the Freundlich model, which is described by the expression qe =KFCe

1/n. Where qe represents the target compound's concentrationin the soil when equilibrium is reached (μg kg−1); Ce is the concentra-tion of the target compounds in the liquid phase after sorption equilib-rium is reached (μg L−1); KF is the Freundlich sorption constant(μg1 − 1/n L1/n g−1); and 1/n indicates the non-linearity of the isotherm(dimensionless). The apparent hysteresis index was calculated usingthe expression HI = (qed − qe

s) / qes. Where qed and qe

s are the solid-phase concentration of the target compounds for the sorption anddesorption experiments, respectively.

The determination of the transport parameters was carried outby the solution of the classic convection–dispersion equation for bothtracer and target pollutants using the CXTFIT 2.1 code (Toride et al.,1995). This model estimates the transport parameters duringsteady one-dimensional flow by fitting data obtained from solute dis-placement experiments to the parameters of the convection–dispersionequation. The code was used in the inverse mode for either equilibriumor non-equilibrium conditions. The solution of the equation was fittedto the experimental data by the least-squares optimization method.The model was fitted to the breakthrough curve (BTC) of both Br−

193J.C. Durán–Álvarez et al. / Science of the Total Environment 473–474 (2014) 189–198

and H218O tracers, using a retardation factor (RF) of 1 (a non-sorbed

solute) to get the dispersion coefficient (D, cm2 min−1). The parameterDwas then kept constant to fit the samemodel to the BTCs obtained fortracers and the target compounds in order to calculate RF. The averagepore water velocity (υ, cm min−1) was calculated using the followingrelation: υ = q / θ. Where q is the Darcy velocity (cm min−1) and θis the volumetric water content (cm3 cm−3). The dispersivity length(λ, cm) was estimated using the equation: λ = D / υ.

3. Results and discussion

3.1. Sorption and desorption tests

Figs. 1 and 2 show the sorption–desorption isotherms of the threetarget pollutants in the irrigated and the rainfed soil, respectively.Data was fitted adequately to the Freundlich kinetic model, as evi-denced by the values of the coefficient of determination (R2) from0.94 to 0.99 (Table 4). Values of the parameter 1/n below unity indicatethe non-linearity of sorption, except for ibuprofen in the rainfed soil.This non-linearity implies that the intensity of the sorption was notthe same throughout the range of concentrations tested; being slightlylower at concentration levels higher than 1 μg/L. Because of this non-

0

1

2

3

4

5

0 1 2 3 4 5

log Ce

Sorption

Desorption 1

Desorption 2

0

1

2

3

4

5

0 1 2 3 4 5log Ce

Sorption

Desorption 1

Desorption 2

0

1

2

3

4

5

0 1 2 3 4 5log Ce

Sorption

Desorption 1

Desorption 2

a

b

c

Fig. 1. Freundlich sorption–desorption isotherms of (a) ibuprofen, (b) estrone and (c) 17βestradiol corresponding to the irrigated soil (bars show standard deviation).

linearity, the organic matter-normalized distribution coefficient (Koc)was not used for comparison of the isotherms; furthermore, the hyster-esis index was determined at three points on the isotherms rather thanone single value for each isotherm.

Using the Freundlich sorption coefficients (KF) obtained in the batchsorption experiments, the order at which the target compounds weresorbed by soil was: estrone N 17β estradiol N ibuprofen, for both soils(Table 4). Sorption of the three pollutants was higher in the irrigatedsoil than in the rainfed one, whichmay be attributed to the high contentof organicmatter in the former as a consequence of the long-term appli-cation of untreated wastewater. Ibuprofen showed lower values of KF

compared with hormones in both soils; sorption was the lowest in thesoil displaying the poorest organic matter content. Such behavior issimilar to that reported by Xu et al. (2009) who observed a decreasein the sorption of the pharmaceutical compound as the content of soilorganic matter decreases and sandy texture prevails in soil. On theother hand, Lin and Gan (2011) report lower sorption coefficients ofanti-inflammatory drugs in non-irrigated soils with different texturalcharacteristics compared with the observed in this study for the waste-water irrigated soil. These comparisons support the hypothesis of theincrease in the sorption capacity of soil due to the accumulation of or-ganic matter in wastewater irrigated soils. It is known that sorption of

Sorption

Desorption 1

Desorption 2

Sorption

Desorption 1

Desorption 2

Sorption

Desorption 1

Desorption 2

a

b

c

0 1 2 3 4 5log Ce

0 1 2 3 4 5log Ce

0 1 2 3 4 5log Ce

0

1

2

3

4

5

0

1

2

3

4

5

0

1

2

3

4

5

Fig. 2. Freundlich sorption–desorption isotherms of (a) ibuprofen, (b) estrone and (c) 17βestradiol corresponding to the rainfed soil (bars show standard deviation).

194 J.C. Durán–Álvarez et al. / Science of the Total Environment 473–474 (2014) 189–198

organic compounds onto the soil is attributable not only to the organicmatter and clay contents but also to the pH values of the soil solution.In the case of ibuprofen, the low retention on the tested soils may becaused by its dissociation into the anionic form at the pH values of thetested soils (Table 2). The organic anions derived from dissociation ofibuprofen are more soluble than the protonated form of the molecule,which leads to a reduction of the sorption by hydrophobic partitiononto the soil organic matter. Additionally, the carboxylate moiety with-in the ibuprofen ionized molecule may be repelled by the negativelycharged particles within the soil (i.e. organic matter and clay) (Hylandet al., 2012). Negative net charge was determined in both soils(Table 2), which enforces the hypothesis of the anion exclusion of theionized ibuprofen molecules. The opposite effect could be observed forpositively charged (cations) organic molecules in soils displaying highcationic exchange capacity, as reported by Pateiro-Moure et al. (2010).Compared with other pharmaceutical compounds with carboxylicacid–carboxylate moieties, ibuprofen has shown the lowest sorptionpotential in soil (Xu et al., 2009; Yamamoto et al., 2009). This may beexplained by the simple chemical structure of the ibuprofen molecule,which is made up of one aromatic moiety and two branched smallhydrocarbon chains. In spite of both the increase in the solubility ofibuprofen and the anion exclusion phenomenon, ibuprofen was indeedsorbed onto the two tested soils. This may be explained by the forma-tion of non-specific hydrophobic interactions between the non-polarfraction of the ibuprofen molecules and the soil organic matter. One ex-ample of such a bond is the π–π electron donor–acceptor interactions;these bonds occur between the aromatic moiety within the solute mol-ecules and the aromatic compounds making up the soil organic matter(Chefetz et al., 2008). Such π–π interactions are expected to be strongeras the hydrophobicity of soil organic matter increases (Zhu et al., 2004).

Regarding sex hormones, both estrone and 17β estradiol weresorbed onto the tested soils more efficiently than ibuprofen, as demon-strated by the KF values shown in Table 4. Sorption coefficients of bothhormones were slightly lower than those reported by Sarmah et al.(2008) and Stumpe and Marscher (2007) using similar wastewaterand freshwater irrigated soils, respectively. Sorption isotherms ofhormones showed non-linearity in both soils, although this was moreevident for non-irrigated soil. Non-linearity in isotherms implies thatcompound is sorbed by soil as successive equilibrium steps ratherthan instantaneously. Such behavior increases as concentration ofhormones in the liquid phase decreases, as has been reported by Yuet al. (2004) for estrogenic hormones in natural soils. Similarly to the re-ported in this study, higher sorption of estrogenic hormones comparedwith that of the ionized form of ibuprofen has been reported by others(Martín et al., 2012). This may be in part because the protonated stateof hormones prevails at the pH of the soils (see pKa values in Table 1).Retention of hormones by soil may occur via the formation of hydrogenbonds between the hydroxyl and keto radicals (the latter in the case ofestrone) and the hydrogenated radicals within the organic domain ofthe soil (Neale et al., 2008). Previous studies in our research group onthe characterization of the soils in the study area have found the preva-lence of carboxylic and phenol functionalities within the organic matter

Table 4Sorption and desorption parameters of the three target pollutants for the two tested soils.

Compound KF 1/n R2 HIdes1

C0: 0.05 μg/L

Wastewater irrigated soilIbuprofen 3.05 ± 0.06 0.82 ± 0.01 0.98 −0.02Estrone 13.1 ± 0.7 0.93 ± 0.01 0.99 0.0617β estradiol 9.5 ± 0.3 0.88 ± 0.01 0.98 0.07

Rainfed soilIbuprofen 1.18 ± 0.1 0.99 ± 0.02 0.98 −0.01Estrone 7.1 ± 0.5 0.81 ± 0.02 0.98 0.0517β estradiol 5.1 ± 0.4 0.73 ± 0.01 0.95 0.02

of wastewater irrigated soils; which may favor the formation of hydro-gen bonds between soil organic matter and hormones (unpublisheddata). Partition of hormones onto the non-polar organic matter of thesoil may have occurred in parallel to the formation of hydrogen bonds(Neale et al., 2008) since hormones have low water solubility as wellas high octanol–water partition coefficients (Table 1).

Regarding the role of clay in the retention of target pollutants ontosoil, sorption of ibuprofen and hormones has been shown to be lowerthan that observed by soil organic matter (Casey et al., 2005; vanEmmerik et al., 2003). The main hindrance for the sorption of thesecompounds by clay under field conditions is that sorption equilibriumis most efficiently achieved under acidic conditions (Behera et al.,2012) after long periods of time (up to 3 d) (Casey et al., 2005), whichis significantly higher than the limited time that water is in contactwith soil in the field.

Regarding desorption, ibuprofen exhibited higher desorption thanhormones, as can be inferred by the values of the hysteresis indexobtained for both soils (Table 4). The overlapping of the sorption anddesorption isotherms of ibuprofen in the irrigated soil indicated thatboth phenomena occurred with the same intensity for this soil. Suchbehavior indicated that linkages established by the compound withthe solid matrix in the sorption step are readily reversible upon thewashing of soil. As applied in the field, this implies that once sorbed,the compound may be released from soil during further irrigation orrain events. Desorption of ibuprofen in the rainfed soil was less intensethan that observed for the irrigated soil, notably in the second desorp-tion step, indicating that the bonds established between ibuprofenand the rainfed soil were stronger than those formed with the irrigatedone. π–π interactions between the aromaticmoieties of both soil organ-icmatter and solutemolecules are expected to be stronger in hydropho-bic environments, thus these interactions are broken in a lower extentin the soil with higher content of humified organic matter, which is dis-tinguished by its high aromaticity. Drori et al. (2006) have observed agreater content of humified organic matter in freshwater irrigated andnon-irrigated soils than in wastewater irrigated soils, which could ex-plain the higher hysteresis index of ibuprofen in the rainfed soil. In con-trast with ibuprofen, the hysteresis index obtained for hormones washigher in the irrigated soil than in the rainfed one (Table 4). In thiscase, hysteresis is attributed to the quantity of organic matter in thesoil rather than its quality. Similarly, low desorption coefficients havebeen observed for other non-polar compounds in agricultural irrigatedand non-irrigated soils (Bermúdez-Couso et al., 2011). Estrone wasthe most resistant to desorption; this may have been a result of thehigh hydrophobicity of the molecule and the potential of the keto radi-cal to establish covalent bonds with metals within the mineral domainof soil, as has been observed for other organic micropollutants(Carrasquillo et al., 2008). Similarly to ibuprofen, the target hormoneshave aromatic moieties within their molecules (Table 1), thus the for-mation of π–π interactions between the molecules and the soil organicmatter is plausible. However, given the chemical configuration of thetarget hormones, it is likely that some steric impediment occurs,diminishing the potential for such bonds to form. Values of the

HIdes2

C0: 1 μg/L C0: 10 μg/L C0: 0.01 μg/L C0: 1 μg/L C0: 10 μg/L

−0.03 −0.06 0.01 0.01 −0.030.08 0.09 0.13 0.17 0.120.07 0.08 0.09 0.08 0.11

0.01 −0.02 0.05 0.05 0.070.05 0.07 0.09 0.06 0.10.04 0.05 0.04 0.06 0.7

0

0.2

0.4

0.6

0 2 4 6 8 10 12

C/C

o

Pore volume

Ibuprofen observed

Ibuprofen modeled

Estradiol observed

Estradiol modeled

Estrone observed

Estrone modeled

Bromide observed

Ibuprofen observed

Ibuprofen modeled

Estradiol observed

Estradiol modeled

Estrone observed

Estrone modeled

Bromide observed

a

0

0.2

0.4

0.6

C/C

o

b

0 2 4 6 8 10 12

Pore volume

Fig. 3. Breakthrough curves of bromide and the target pollutants for (a) the wastewater irrigated soil and (b) the rainfed soil.

195J.C. Durán–Álvarez et al. / Science of the Total Environment 473–474 (2014) 189–198

hysteresis index shown in Table 4 are evidence of higher impedance forthe three compounds to desorb in the secondwashing step compared tothe former. The mass of compound remaining in the soil after the sec-ond desorption step was extracted from the solid matrix using organicsolvents through the pressurized liquid extraction method (as ex-plained in the Materials and methods section). This mass remaining insoil after the two stage desorption step was cataloged as the massnon-extractable with water.

3.2. Displacement experiments

Bromide breakthrough curves (BTC) obtained for both soils did notshow a perfect symmetrical Gaussian shape (Fig. 3); however, datawas fitted better with the physical equilibrium model than with thenon-equilibrium model. Physical equilibrium can be interpreted as theabsence of preferential paths through the soil column; such preferentialpaths promote the rapid leaching of solutes through the soil. In thewastewater irrigated soil, the physical equilibrium state could beachieved by the swelling of expandable clay upon soil humidification(Friedel et al., 2000). For the rainfed soil, the prevalence of fine particles(silt and clay), in addition to the lack of organic matter, stones and roots

Table 5Transport parameters of the target pollutants for the two tested soils.

Solute Rainfed soil Wastewater irrigated soil

RF R2 Model λ (cm) RF R2 Model λ (cm)

Bromide 1.0 0.81 Ph-Eq 3.07 0.92 0.81 Ph-Eq 0.33Ibuprofen 1.4 0.83 Ch-Eq 1.6 0.96 Ch-Eq17β estradiol 6.5 0.95 Ch-Eq 6.4 0.96 Ch-EqEstrone 7.7 0.80 Ch-Eq 8.4 0.82 Ch-Eq

RF: retardation factor; λ: dispersivity; R2: coefficient of determination; Ph-Eq: model atphysical equilibrium; Ch-Eq: model at chemical equilibrium.

could limit the occurrence of preferential paths. The physical equilibri-um condition implies that the transport of solutes is only influencedby the chemical properties of the soil, as occurs in the batch sorption–desorption tests. As shown in Fig. 3, the centroid of the bromide BTCcorresponding to the irrigated soil is nearly one pore volume after thepulse application. The retardation factor (RF) of bromide in the irrigatedsoil, obtained by inverse modeling using the CXTFIT code, was 0.92(Table 5). This behavior is unexpected for a conservative tracer becauseit should be inert to the soil components, leaving the soil column at thesame time as the volume of water corresponding to the pulse, and thusresulting in a RF value of 1. The rapid exit of bromide from the columncan be explained by the anion exclusion of the ion caused by some ofthe negatively charged soil components, e.g. montmorillonite typeclays, oxides and organic matter (Korom and Seaman, 2012). Anion ex-clusion was not observed in the rainfed soil, whichmay be attributed toits lower content of organic matter and clay. The anion exclusion phe-nomenon in the wastewater irrigated soil was proven by comparingthe BTC of bromide tracer vis á vis that obtained for a water isotope(H2

18O). The BTCs of both tracers in the irrigated soil columnwere slight-ly asymmetrical (Fig. 4); however, data fitted well to the code used inthe inverse mode for deterministic equilibrium. The fit of the experi-mental data to the model resulted in a coefficient of determination of0.98 for each tracer. The use of the two-site/two-region model (non-equilibrium mode) did not improve the fitting. The dispersivity wasthe same for both tracers, while the RF of the water isotope was 1 com-pared with 0.92 for bromide. Anion exclusion may be experienced byother negatively charged organic solutes, such as ibuprofen. Dispersivityof bromide varied for each soil type; dispersivity obtained for therainfed soil was ten times higher than that of the irrigated one. This re-sult was contrary towhat was expected, as dispersivity tends to be highin clayey soils and decreases moving from fine to coarse texture(Bromly et al., 2007; Perfect et al., 2002). Values of the dispersivity coef-ficient obtained for the irrigated soil were of the same order as that re-ported for loam clayey soils from the same region (Müller et al., 2012).

0.0

0.2

0.4

0.6

0.8

1.0

0 1 2 3 4

C/C

o

Pore Volume

Modeled bromide

Observed Bromide

Modeled 18-O

Observed 18-O

Pulse

Fig. 4. Observed and modeled breakthrough curves for bromide and H218O tracers obtained for the irrigated soil.

196 J.C. Durán–Álvarez et al. / Science of the Total Environment 473–474 (2014) 189–198

For the target pollutants, dispersivity of hormones was higher in the ir-rigated soil than in the rainfed one, while for ibuprofen this parameterwas quite similar in both soils.

Similarly to those obtained for tracers, BTCs of the three targetcompounds were not symmetrical, although experimental data fittedbetter to the physical equilibrium model. The CXTFIT code indicatedthat transport of the pollutants took place under chemical equilibriumconditions. The chemical equilibriumdisplacement indicates the instan-taneous sorption of the compounds onto the soil. Instantaneous sorp-tion can be attributed to the hydrophobic partition of the solutes ontothe organic domain of the soil. Hydrophobic partition tends to bemore rapid than the formation of hydrogen bonds or π–π interactions(Voice and Weber, 1983). Table 5 shows the results obtained from theBTCs modeling. The values of the coefficient of determination (R2) ob-tained for the regression between observed data and the equilibriummodel ranged from 0.80 to 0.95. The transport of the target pollutantswas delayed by the tested soils by the same order as in the batchexperiment, with the transport of estrone being the most delayedwhile ibuprofen was the most mobile compound. The RF of the threecompounds was similar for both soils (Table 5). This was unexpectedas the irrigated soil showed a higher capacity for sorbing the targetpollutants than the rainfed one in the batch tests and thus a higherretardation in the compounds'mobilizationwas expected in the former.Since physical equilibrium conditions were present in both soils, suchbehavior is related to the chemical properties of the soil rather than itsphysical structure, and may be explained by three phenomena whichmay be occurring either separately or together. The first phenomenonis the migration of the sorbed compounds from the soil to the liquidphase because of the gradient of polarity between the two phases. Thehigh electrical conductivity of the irrigated soil may enhance desorptionof the non-polar compounds (i.e. the hormones) after sorption equilib-rium is achieved. The enhancement in the sorption rate of non-polarorganic compounds using liquid phase with high electrical conductivitylevels has been observed in previous studies (Durán-Álvarez et al.,2012; Williams et al., 2006), suggesting that the opposite effect mayoccur with a saline soil (e.g. the wastewater irrigated soil, Table 2).The second possible mechanism causing the rapid mobilization of thetarget compounds in the irrigated soil is the facilitated desorption ofthe sorbed molecules by the formation of complexes with the dissolved

Table 6Residual mass of the target compounds in the soil at the end of the batch sorption–desorption and displacement columns assays.

Soil type % of the mass initially added

Ibuprofen Estrone 17β estradiol

Irrigated-batch 11.2 ± 0.2 31 ± 1.1 18.1 ± 0.9Rainfed-batch 10.8 ± 0.7 17.3 ± 0.5 13.9 ± 0.1Irrigated-columns 19.7 ± 0.4 77.5 ± 3 27.5 ± 0.8Rainfed-columns 18.3 ± 1 66.7 ± 5 32.6 ± 1.2

organic matter released by the soil. It is known that estrogenic hor-mones can establish interactionswith the hydrophobic dissolved organ-ic matter of the soil (Jin et al., 2007; Stumpe andMarscher, 2007), whileibuprofen is able to establish electrostatic interactions with the basicpositive-charged hydrophilic dissolved organic matter (Maoz andChefetz, 2010). Moreover, hydrophobic compounds are more suscepti-ble to desorption from soil by the formation of this type of complexesthan hydrophilic molecules (Johnson and Amy, 1995). This would ex-plain the notable increase in the mobilization of hormones comparedto ibuprofen (Table 5). The third mechanism is the exchange of thesorbed pollutants by the dissolved organic matter released by the soil,as has been reported for other organic pollutants (Flores-Céspedeset al., 2002).

As occurred with batch tests, mass balances carried out on the col-umns evidenced the presence of mass that was non-extractable withwater. Table 6 shows the fraction of residual mass of the target pollut-ants in soil at the end of batch and column tests. Less residual masswas found in the soil columns than in the remaining soil in batchtests. This result is attributable to the extended desorption step in thecolumn experiments (13 pore volumes). The mass of the compoundsthat were not detected either in leachate or soil at the end of the dis-placement assayswas considered to bedegraded by non-specific routes,most likely biodegradation. These values were determined taking intoaccount the recoveries of the target compounds during soil extractionand analysis (see Section 2.5). Degradation efficiency was higher inthe irrigated soil (24.5% for ibuprofen, −2.84% for estrone and 30.8%for 17β estradiol), than in the rainfed one (12% for ibuprofen, 1% for es-trone and 16.8% for 17β estradiol). In the irrigated soil, negative valuesof degradation yield for estrone were attributed to its productionthrough the aerobic biodegradation of 17β estradiol (Xuan et al.,2008). The results obtained in mass balances highlight the need of con-duct comparative batch and column studies using both sterile and non-sterile soils in order to obtain the biodegradation of the target com-pounds under static and dynamic water flow conditions.

4. Conclusions

The results obtained in these experiments clarify the role of waste-water irrigated soils as a filter and degradation media for the targetmicropollutants contained in untreated wastewater used in irrigation.Sorption of the target compounds was grater in the wastewater irrigat-ed soil compared to that observed for non-irrigated soil due to the accu-mulation of organic matter in the former. The concentration of organicmatter in soil was determinant in desorption of non-polar compounds,whereas for ibuprofen the quality of soil organic matter, i.e. humifica-tion level, influenced more significantly in desorption. The mobility ofthe compounds through the soil columns was shown to be similar forboth soils; because of this, the biodegradation of the pollutants withinthe soil matrix, which was higher in the irrigated soil, may be thedetermining factor in preventing groundwater pollution. Given that

197J.C. Durán–Álvarez et al. / Science of the Total Environment 473–474 (2014) 189–198

the irrigated soil was shown to bemore effective at removing the targetpollutants, settingup irrigation of rainfed soilswith untreatedwastewa-ter is not advisable; instead, treated wastewater should be used topromote the accumulation of organic matter in this type of soil inorder to acclimate soil to retain/degrade pollutants in cases in whichuntreated wastewater is to be used for irrigation in the future.

Conflict of interest

With regard to the submission and revision of this manuscript to thejournal Science of the Total Environment, we, the authors, state that wedo not have any conflict of interest to report.

Acknowledgments

The authors would like to express gratitude to Professor René Alcaláfrom the Laboratorio de Fisica de Suelos del Instituto deGeología, UNAMfor the support in the analysis of soil samples, aswell as to the DirecciónGeneral de Asuntos del Personal Académico de la UNAM (DGAPA)and to the Mexican Council of Science and Technology (CONACyT) byfunding this work in the framework of projects IN101610 and 99964,respectively.

Appendix A. Supplementary data

Supplementary data to this article can be found online at http://dx.doi.org/10.1016/j.scitotenv.2013.12.018.

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