Mathematical Model for Cyclodextrin Alteration of

Article pubs.acs.org/est

Mathematical Model for Cyclodextrin Alteration of Bioavailability of Organic Pollutants Huihui Liu, Xiyun Cai,* and Jingwen Chen Key Laboratory of Industrial Ecology and Environmental Engineering (Ministry of Education), School of Environmental Science and Technology, Dalian University of Technology, Dalian 116024, China S Supporting Information *

ABSTRACT: While many cyclodextrin-based applications have been developed to assess or enhance bioavailability of organic pollutants, the choice of cyclodextrin (CD) is largely empirical, with little consideration of pollutant diversity and environmental matrix effects. This study aimed at developing a mathematical model for quantifying CD alteration of bioavailability of organic pollutants. Cyclodextrin appears to have multiple effects, together contributing to its bioavailability-enhancing property. Cyclodextrin is adsorbed onto the adsorbent matrix to different extents. The adsorbed CD is capable of sequestrating organic pollutants, highlighting the role of a pseudophase similar to solid environmental matrix. Aqueous CD can reduce adsorption of organic pollutants via inclusion complexation. The two effects cancel each other to a certain degree, which determines the levels of organic pollutants dissolved (comprising freely dissolved and CD-included forms). Additionally, the CDincluded form is nearly identical in biological activity to the free form. A mathematical model of one variable (i.e., CD concentration) was derived to quantify effects of CD on the bioavailability of organic pollutants. Model analysis indicates that alteration of bioavailability of organic pollutants by CD depends on both CD (type and level) and environmental matrix. The selection of CD type and amendment level for a given application may be predicted by the model.

■

INTRODUCTION Organic compounds and their transformation products are common types of environmental contaminants and often occur in the form of complex mixture.1,2 Particularly, they are prone to adsorb and immobilize onto solid environmental matrices (e.g., soil and sediment), in which some fractions are unavailable for access by microbial degraders, or that the bioavailable level (i.e., bioavailability) decreases.3,4 The bioavailability of contaminants is known to influence the environmental persistence and risks of organic pollutants.5,6 In the context of bioremediation, decreased bioavailability is recognized as a limiting factor to contaminant removal.7,8 Many remediation practices do not completely remove the sequestered contaminants.5 Assessment of bioavailability of contaminants is a prerequisite for the management and evaluation of remediation sites, through which the contaminants of high risks are screened as the target to remove. Several analytical tools such as cyclodextrin (CD) extraction and solidphase microextraction have been developed for estimating bioavailability.3,9−11 Meanwhile, researchers have also explored options to enhance bioavailability and thus accelerate contaminant removal by using amendments of CD, surfactant, and organic acids.12,13 Cyclodextrin consists of a group of cyclic oligosaccharides and presents a doughnut-shaped structure. It has an axial open cavity of hydrophobic character that may include organics (or their moiety) in terms of geometric compatibility.14,15 The unique cavity that commonly increases the solubility and © XXXX American Chemical Society

diffusion of organics provides the fundamental mechanisms for CD to act as a drug delivery vector.16,17 It is also the basis for CD to enhance bioavailability of organic pollutants (e.g., pesticide and PCBs).18,19 Additionally, CD, being of a natural substance, is considered nontoxic14 and biodegradable without secondary environmental concerns.20,21 To date, a variety of CD-based approaches have been developed to assess bioavailability of pollutants (e.g., PAHs, hydrocarbons, and transformer oil)22,23 or to intensify their bioremediation efficiency.24,25 However, the selection of operational variables therein appears to be arbitrary and lacks optimization. These variables include CD types (i.e., β-CD, HPCD, and RMCD),26−28 the level of CD,19,29,30 and the ratio of CD solution to the solid matrix.19,31,32 Consequently, in some applications, these methods resulted in underestimation of bioavailability of organic pollutants,33−35 as evident from the parallel organism bioaccumulation and biodegradation assays. Such inconsistencies may be attributed to the absence of mathematical relationships correctly describing the interactions of CD with organic pollutants in environmental matrices. Multiple interactions may be involved in the tertiary CDcontaminant-sorbent matrix system, such as the concurrent adsorption of CD and contaminant onto the matrix,36−39 and Received: September 13, 2012 Revised: May 10, 2013 Accepted: May 13, 2013

A

dx.doi.org/10.1021/es303724b | Environ. Sci. Technol. XXXX, XXX, XXX−XXX

Environmental Science & Technology

Article

Scheme 1. Effects of Cyclodextrin on Distribution Behavior of Pesticide

the simultaneous inclusion of contaminant in CD.15,26 These interactions not only lead to the formation of CD-included organic pollutants but also alter phase distributions, due to potential inclusion of the adsorbed cyclodextrin and adsorption of the CD-included pollutants. The objective of this study was to develop a mathematical model to describe how coexistence of CD quantitatively alters bioavailability of organic pollutants in a solid matrix. To this end, we investigated adsorption of seven CDs onto three adsorbents and deduced a mathematical model that describes effects of CD on the adsorption of five pesticides as model pollutants. In addition, we assessed bioactivity and distribution of free and CD-included pollutants in simulated environmental matrices. The model may be used to guide the selection of variables for optimizing the use of CD in assessing or enhancing contaminant bioavailability.

respectively; and i refers to the species (i.e., CD, pesticide, or their complex). As CD adsorbed comprises free and included forms in the solution, mass conservation for CD is expressed as eq 3 C0,CDV = (Cs,CD + Cs,CD ‐ P)M + (Ce,CD + Ce,CD ‐ P)V

where V (L) is the volume of solution, M (kg) is the mass of solid matrix, and C0,CD (mg/L) is the initial concentration of CD. Integrating eqs 1−3, Ce,CD is deduced from eq 4, in which the term KcCe,p is equivalent to a ratio of Ce,CD‑P to Ce,CD (eq 5). The level (Cp) of pesticide encountered in the environment is generally below the level of μmol/L.40,41 As it is far lower than that of CD (in the mmol/L range), the ratio of Ce,CD‑P to Ce,CD may be approximated as zero. Then, the term KcCe,p may be neglected, leading to eq 6.

■

⎡ Ce,CD = C0,CD/⎢(1 + KcCe,P) ⎢⎣

THEORETICAL SECTION In the sorbent-sorbate system, inclusion complexation and adsorption of CD and organic pollutants may occur concurrently. Pesticide (as a model organic pollutant), CD, and their complex may be all adsorbed onto the solid matrix (Scheme 1). The fractions of these three species in the solution can be calculated on the basis of inclusion complexation (eq 1) and mass conservation. Cyclodextrin adsorbed is potentially capable of including the pesticide because of the unique doughnut-shaped structure. Once inclusion and adsorption processes reach equilibrium, adsorption coefficient (Kd,i) of pesticide, CD, and their complex is represented by eq 2 C Kc = CD ‐ P CCDC P Kd, i =

⎛ Kd,CD ⎞⎤ + Kd,CD ‐ P M/V ⎜⎜ + KcCe,P⎟⎟⎥ ⎝ Kd,CD ‐ P ⎠⎥⎦ KcCe,P =

Ce,CD ‐ P Ce,CDCe,P

Ce,P =

Ce,CD ‐ P Ce,CD

Ce,CD = C0,CD/(1 + Kd,CD M /V )

≤

CP Ce,CD

(4)

(5) (6)

Apparent adsorption coefficient (Kd,P(apparent)) of pesticide (comprising free and CD-included forms) is given in eq 7, which is further transformed to eq 8 by integrating eqs 1 and 2. Substituting the term Ce,CD from eq 6 into eq 8 yields eq 9 that describes the effect of CD on apparent adsorption of pesticide. The term C0,CD is the sole variable in eq 9, as the terms Kd,P, Kd,CD, and Kd,CD‑P may be considered as constants in a limited range of concentrations. Theoretically, the term Kd,P(apparent) should correlate linearly with the term (1+Kd,CDM/V)/ (1+Kd,CDM/V+KcC0,CD). The intercept and slope of the linear equation correspond to the term Kd,CD‑P and the difference of Kd,P and Kd,CD‑P, respectively. Additionally, the term Kd,CDM/V

(1)

Cs, i Ce, i

(3)

(2)

where CCD (mg/L), CP (mg/L), and CCD‑P (mg/L) are the concentrations of CD, pesticide, and their complex, respectively; Ce,i (mg/L) and Cs,i (mg/kg) are the concentrations of pesticide in the solution and adsorbed onto the matrix, B



Article

S1). The isothermal adsorption data were fitted to Freundlich equation. Moreover, the adsorbents separated were rinsed with 10 mL of purified water to remove the adherent solution at the surface and lyophilized for FTIR, XPS, and SEM characterization (Text S2). Adsorption of Pesticide in the Presence of Cyclodextrin. Adsorption of pesticide was also measured through batch adsorption experiments. Cyclodextrin amendment levels were set at 0, 2, 4, 6, 8, and 10 mmol/L. At each level of CD, a series of levels of pesticide were evaluated. The samples of pesticide-CD mixture prepared in 25-mL glass centrifuge tubes were shaken at 180 rpm and 25 °C for 3 d to ensure inclusion equilibrium. Appropriate amounts of adsorbent were added to obtain solid−liquid ratios of 1:5 for soil, 1:25 for kaolin, and 1:25 for active carbon. The samples were further shaken for 24 h to reach adsorption equilibrium. Finally, the samples were separated by centrifugation, and the supernatant was filtered through a 0.45-μm Millipore membrane. Pesticide in the filtrate was measured on a Hitachi L-2000 HPLC (Text S3), and data were fitted to Freundlich model. Bioassay of Pesticide in the Presence of Cyclodextrin. Biological activity of free and CD-included forms was measured using green algal growth-inhibition and zebra fish acute toxicity tests. In the former, two herbicides (i.e., atrazine and butachlor) and three CDs (i.e., β-CD, HPCD, and RMCD) were measured; and in the latter, the insecticide fipronil and three CDs were used. The algal growth-inhibition test was carried out according to the updated OECD guideline for freshwater algal and cyanobacterial growth inhibition test.42 The algae Chlorella vulgaris was obtained from the Institute of Hydrobiology of Chinese Academy of Sciences (Wuhan, China). The algae was maintained in algal growth medium HB IV at 24 ± 0.5 °C in an incubator under continuous illumination of 3000−4000 lx per day. Prior to the inoculation, the test solutions containing CD (0−10 mmol/L for β-CD and HPCD and 0−20 mmol/L for RMCD) and pesticide (0−18.54 μmol/L for atrazine and 0− 55.80 μmol/L for butachlor) were mixed for 3 d to achieve inclusion equilibrium. The algae was inoculated into the test solutions to obtain a density of 4.00 × 105 cells/mL. According to the linear equation between cell counts and optical density at 680 nm (OD680), algal growth inhibition was determined by measuring OD680 using an UV-2300 spectrophotometer (Techcomp Limited, Shanghai, China). The effect concentration of pesticide inhibiting 50% of algal growth (EC50) was calculated in terms of inhibition rate of algal cells using LD50 Data Processing Program V1.01 (Blue Cosmos Studio, Guangzhou, China). The zebra fish acute toxicity test was carried out according to the updated OECD guideline for the fish acute toxicity test.43 The zebra fish (Danio rerio) (age 2 months) was purchased from a local pet store. The fish was incubated in the laboratory, and the mortality was less than 10%. The water was maintained at 25 ± 1 °C and renewed every 24 h, in which dissolved oxygen concentration was at least 60% of air saturation. Prior to the test, the fish was starved for 24 h to clean the gut. Similarly, the test solutions containing CD (i.e., β-CD, HPCD, and RMCD) and fipronil were mixed for 3 d to achieve inclusion equilibrium. Eight fish was transferred to each 2-L test vessel. The fish was kept without feeding during the exposure. Mortality was recorded at 48 h to calculate LC50 value using the same program.

may be neglected, as in some cases CD is poorly adsorbed. Equation 9 can be further transformed to eq 10 that only relates to the term C0,CD. Finally, a fraction (α) of pesticide dissolved in the solution is quantified in eq 11 on the basis of mass conservation. Kd,P(apparent) =

Kd,P(apparent) =

Cs,P + Cs,CD ‐ P Ce,P + Ce,CD ‐ P

(7)

Kd,PCe,P + Kd,CD ‐ PKcCe,CDCe,P

Ce,P + KcCe,CDCe,P Kd,P − Kd,CD ‐ P = + Kd,CD ‐ P 1 + KcCe,CD

Kd,P(apparent) =

(Kd,P − Kd,CD ‐ P)(1 + Kd,CD M/V ) 1 + Kd,CD M/V + KcC0,CD + Kd,CD ‐ P

Kd,P(apparent) =

α=

■

(8)

(9)

Kd,P − Kd,CD ‐ P 1 + KcC0,CD

+ Kd,CD ‐ P

(10)

(Ce,P + Ce,CD ‐ P)V

(Cs,P + Cs,CD ‐ P)M + (Ce,P + Ce,CD ‐ P)V 1 = Kd,P(apparent) M /V + 1

(11)

EXPERIMENTAL SECTION Materials and Materials Characterization. Information on β-cyclodextrin (β-CD) and five derivatives (i.e., RMCD, 2MCD, 3MCD, 6MCD, and HPCD) was listed in Table S1. Five pesticides (i.e., butachlor, metolachlor, atrazine, fipronil, and diclofop) with distinct properties were selected as model organic pollutants (Table S2). Three adsorbents (i.e., soil, kaolin, and active carbon) were used as model environmental matrices (Table 1). Their surface area and porosity were Table 1. Physicochemical Properties of Three Adsorbents adsorbent

surface area (m2/g)

pore volume (cc/kg)

pore size (nm)

particle size (μm)

soil kaolin active carbon

29.41 22.00 774.40

43.58 84.61 506.10

5.98 15.38 2.61

179.06 31.13 973.06

measured by Quadrasorb-SI (Quantachrome Instruments, Boynton Beach, USA), and particle size was measured by a Mastersize 2000 Particle Analyzer (Malvern Instruments Limited, Worcestershire, England). Adsorption of Cyclodextrin and Adsorbent Characterization. Batch adsorption experiments were conducted in 25mL glass centrifuge tubes with solid−liquid ratios of 1:5 for soil, 1:25 for kaolin, and 1:25 for active carbon. A series of concentrations of CD were prepared in 10-mmol/L CaCl2. After appropriate amounts of adsorbent were added, all samples were shaken at 180 rpm and 25 °C for 24 h to reach adsorption equilibrium. The slurry was separated by centrifugation at 4000 rpm for 10 min. The supernatant was filtered through a 0.45μm Millipore membrane. Cyclodextrin in the filtrate was measured by the phenolphthalein colorimetric method (Text C



Article

Data Analysis. All experiments were performed in triplicate. Data for inclusion constant and distribution coefficient were represented by mean values (n = 3). Data for EC50 and LC50 values were represented by 95% confidence interval. Statistical analysis for the significance was performed using one-way ANOVA in Origin 8.0 (Microcal Software, New Jersey, USA). The values without overlapping 95% confidence interval were considered to be significantly different.

Therefore, the dimensionless Kd was used, which was calculated as the mean of Kd at all CD levels. Comparison of mean Kd values indicated that active carbon had high affinity to CD with Kd values of 35 (HPCD) to 189 (β-CD). This was likely due to the large surface area (774.40 m2/g) and optimum pore size (2.61 nm) of activated carbon as an adsorbent, consistent with the findings of Abe et al.36 Kaolin exhibited moderate affinity to CD, as Kd varied from 5.76 (3MCD) to 13.32 (6MCD). In contrast, soil was relatively a weak adsorbent, with the exception of β-CD that had a Kd value of 27.01. Similar findings have been obtained in previous studies suggesting that adsorption of CD depended on soil types and that adsorption of CD was negligible in some soils.39,44 Chemical modifications significantly influenced the adsorption potential of natural β-cyclodextrin (Table 2). β-Cyclodextrin and its methylated derivatives (e.g., RMCD) showed stronger adsorption. It is likely due to the low solubility (i.e., 16 mmol/L at 20 °C) of β-CD.39 The methylated analogues are readily soluble in weakly polar organic solvents (e.g., dichloromethane45), which may have contributed to the enhanced sorption.27,38 The hydroxypropylated derivative (i.e., HPCD) showed decreased sorption, which was in agreement with the finding that HPCD was weakly adsorbed by iron surface, kaolin, and Illite.37,46,47 Adsorption of Pesticide in the Presence of Cyclodextrin. The pesticides used in this study exhibited distinct adsorption behavior, highlighted by the varying heterogeneity factors (Figure S5). The fitting of eq 9 indicated good linear correlation of Kd,P(apparent) with the term (1+Kd,CDM/V)/ (1+Kd,CDM/V+KcC0,CD), in which the terms Kd,CD and Kc were derived from batch adsorption experiments and phase solubility measurement (Text S4), respectively. For example, in soil, Kd,P(apparent) of five pesticides at 8.00 mg/L was plotted as a linear function of (1+Kd,CDM/V)/(1+Kd,CDM/V+KcC0,CD) with R2 ≥ 0.91 and P < 0.05, when the CD concentration was varied from 0 to 10 mmol/L (Figure S6). The terms Kd,P and Kd,CD‑P were calculated from the intercept and slope of the linear relationship, respectively. The values of Kd,P calculated were in close agreement with those derived from the batch adsorption experiments (Table 3), and they showed good linear correlation with slope close to 1 (y = 0.9844x, R2 > 0.96 and P < 0.01). Similarly, good agreement between the Kd,P(apparent) values calculated and observed was yielded for all the adsorbents (Figure S7). Moreover, the fitting degrees of eq 10 (Figure S8) were nearly identical to those of eq 9 (Figure S7), even though the adsorption of CD itself was neglected. Only one term (i.e., Kc) is required for eq 10, while four terms (i.e., Kd,CD, M, V, and Kc) are necessary for eq 9. This fact shows that the model given by eq 10 may be simple and feasible. The calculation of the term Kd,CD‑P indicated that CD adsorbed onto adsorbent was capable of adsorbing organic molecules (Tables 2 and 3), implying the role of a pseudophase of CD similar to the solid matrix. Accordingly, CD adsorbed and the adsorbent matrix may be considered as a composite adsorbent. This interaction has been implicated in various studies showing that adsorption of CD modified soil properties as well as the environmental behavior of organic pollutants,38,45,48 and this interaction provides theoretical validation to eqs 9 and 10. Overall, the adsorption of CD onto the solid environmental matrix may not only affect adsorption behavior and extraction efficiency of organic contaminants but also cause CD loss.

■

RESULTS AND DISCUSSION Adsorption of Cyclodextrin onto Three Adsorbents. Characterization of the lyophilized adsorbents (Figures S1−S3) clearly demonstrated adsorption of CD onto adsorbent. Figure S1 shows FTIR spectra of the adsorbents. Characteristic peaks of CD, i.e., O−H at 3430 cm−1 and 1630 cm−1, C−H at 2920 cm−1, and pyranoid sugar ring at 1500−400 cm−1, were identified in the active carbon samples. Though these peaks were not detected in the other two adsorbent samples, new absorption bands (e.g., 2930 cm−1) appeared in the kaolin samples, suggesting the loading of CD. The XPS spectra also exhibited changes in position and/or intensity of O 1s (Figure S2). For example, for the soil-CD treatment, the O 1s position shifted from 529.23 to 531.65 eV that approximated the intrinsic value (ca. 531.79 eV) of β-CD, while the intensity did not change. The presence of other CDs induced upward shifts of O 1s as well as variations of the intensity. Amendments of HPCD and 6MCD increased the intensity of O 1s, while treatments of RMCD and 2MCD had an opposite impact. In addition, SEM images (Figure S3) showed obvious alterations of the morphology of the adsorbents, e.g., CD-initiated porefilling on active carbon. Adsorption isotherms of CD onto these three adsorbents were well fitted to the Freundlich model (Figure S4 and Table 2). The values of heterogeneity factor n ranged from 0.10 to 1.77. The deviation from unity indicated that CD adsorption proceeded via complicated interactions other than partition process. The resulting Kf value was of dimension, so that it would be a poor indicator for adsorption potential of CD. Table 2. Freundlich Isothermal Constants of CD onto Three Adsorbents adsorbent soil

kaolin

active carbon

a

cyclodextrin

Kfa

nb

R2

Kd,CD

β-CD HPCD RMCD 2-di-o-MCD 3-di-o-MCD 6-di-o-MCD β-CD HPCD RMCD 2-di-o-MCD 3-di-o-MCD 6-di-o-MCD β-CD HPCD RMCD 2-di-o-MCD 3-di-o-MCD 6-di-o-MCD

281.36 0.23 12.60 152.86 16.37 14.74 0.45 0.04 15.95 86.49 20.84 95.03 1219.52 19665.37 32677.10 26632.26 23959.35 15712.50

0.46 1.05 0.60 0.26 0.63 0.59 1.41 1.77 0.97 0.74 0.84 0.75 0.70 0.17 0.10 0.14 0.17 0.23

0.90 0.97 0.98 0.97 0.92 0.93 0.98 0.93 0.95 0.98 0.98 0.99 0.97 0.98 0.97 0.99 0.98 0.98

27.01 0.31 1.40 2.42 2.17 1.53 10.81 13.09 11.70 11.12 5.72 13.36 189.04 34.97 186.15 116.43 122.29 125.91

The isotherm constant. bThe heterogeneity factor. D



Article

Table 3. Adsorption Coefficient of Free and CD-Included Pesticides adsorbent soil

kaolin

active carbon

adsorbate

Kca

Kd,P obsd

Kd,P calcd

Kd,CD‑P calcd

Qb

butachlor-β-CD butachlor-RMCD butachlor-HPCD metolachlor-HPCD atrazine-HPCD diclofop-HPCD butachlor-HPCD metolachlor-HPCD diclofop-HPCD fipronil-β-CD fipronil-RMCD fipronil-HPCD metolachlor-β-CD metolachlor-RMCD metolachlor-HPCD

454.32 2537.23 125.33 30.83 40.81 750.51 125.33 30.83 750.51 58.85 200.08 125.08 86.33 96.63 30.83

34.39 40.68 75.79 5.15 11.14 15.39 109.79 23.35 544.37 592.65 515.67 591.17 37245.42 38539.38 38159.16

33.06 41.33 76.11 5.33 11.16 15.22 107.27 23.70 530.08 591.75 512.08 588.12 36793.16 37860.29 37514.25

0.11 5.15 8.42 10.79 7.42 7.90 0.25 42.16 64.72 6.95 2.05 6.87 7391.05 3361.12 283.01

300.55 8.03 9.04 0.49 1.50 1.93 429.08 0.56 8.19 85.14 249.80 85.61 4.98 11.26 132.55

The values of atrazine, butachlor and fipronil were based on phase solubility measurement.15 bQ (efficiency-enhancing coefficient) was defined as a ratio of Kd,p calculated to Kd,CD‑P calculated. a

Comparison of the calculated values of Kd,CD‑P and Kd,P suggested that CD adsorbed generally had less affinity to pesticide than the adsorbent itself, highlighted by the term Q (i.e., efficiency-enhancing coefficient) being greater than 1 (Table 3). The exception was HPCD-metolachlor treatment where Q was 0.49 for soil and 0.56 for kaolin. This observation indicated that the presence of HPCD would increase the overall sorption of pesticides onto adsorbent. Furthermore, the enhancing potential of CD varied with pesticide and adsorbent (Table 3). For butachlor, β-CD exhibited the highest enhancing potential in soil, followed by HPCD (Q = 9.04) and RMCD (Q = 8.03). For fipronil, RMCD (Q = 249.80) was more efficient for kaolin than HPCD (Q = 85.61) or β-CD (Q = 85.14). In the active carbon system, HPCD displayed a large Q (132.55) for metolachlor. Such a variation does not support the fact that HPCD has been used widely as an effective additive to remove organic pollutants.8,47 Biological Activity of Pesticide in the Presence of Cyclodextrin. In preliminary experiments, CD did not show any adverse effects to the test organisms (data not shown). Moreover, CD universally acts as a delivery vector in pharmaceutical chemistry by increasing solubility and availability of drugs at the barrier surfaces,16 where drug release from CD-included complex is rapid and quantitative.49 Generally, the complex is more water-soluble than the guest and thus has higher diffusive potential than the free form. At the surfaces of target, the complex dissociates to the free form that is actually the active form. Therefore, it is reasonable to assume that free and CD-included forms have the same biological mechanism but probably different potency. In theory, the dose addition model (eq 12) may illustrate the joint bioactivity of free and included forms yi xi 1 = + EC50(mix, i) EC50,P EC50,CD ‐ P (12)

ments, presenting the slope of close 1 (Figure S9). The similarity in EC50 (or LC50) values supports the application of dose addition model. Subsequently, the EC50 (or LC50) values of inclusion complexes were calculated from the model. For example, atrazine-β-CD and butachlor-RMCD complexes had EC50 values of 2.80 to 4.17 μM and 27.27 to 33.33 μM against the algae. The LC50 of fipronil-HPCD for fish was 0.63 to 0.92 μM. The EC50 (or LC50) values of the complexes appeared to overlap or be similar to the 95% confidence interval of the corresponding values of the free forms. Therefore, the free and CD-included pesticides exhibited nearly identical activity to the test organisms, which is attributable to rapid dissociation of the complex to the free form biologically active. This observation was in agreement with the finding of similar biological activity of the pesticides in the absence or in the presence of CD (Table S3). This may be due to the fact that EC50 (or LC50) values are less than their water solubility for these treatments.16 The enhancement of bioactivity by CD is expected to be more pronounced for poorly soluble compounds, due to increases in water solubility, mass diffusion, and bioavailability.7,16,17 However, in some cases, it was observed that CD at high levels resulted in reduced bioactivity by decreasing mass transfer.35,50 Use of Cyclodextrin To Improve Bioavailability of Pesticides. It is well accepted that only the freely dissolved fraction of a chemical is potentially bioavailable.6,51 The existence of CD increases aqueous phase levels of organic pollutants via multiple effects, such as increased water solubility and decreased adsorption. Furthermore, CD is demonstrated to promote mass transfer of organic compounds in the liquid phase.52−54 Specifically, CD enhances convective mass transfer and thus rapidly rewashes organic compounds from solid to liquid phases, and diffusive mass transfer of organic pollutants (i.e., PAHs) is significantly enhanced in the soil with CD treatment.53 The two improvements commonly speed up distribution processes of organic compounds, thereby facilitating an improvement in bioavailability. In the environmental matrices with CD addition, the fraction of pesticide dissolved consists of free and included forms (eq 11). As both forms had similar bioactivity, the total fraction of pesticide dissolved would indicate pesticide bioavailability. This conclusion is clearly consistent with the wide application of CD

where EC50(mix,i) is the apparent medium effect concentration of pesticide in the presence of CD at concentration i (mM); EC50,P and EC50,CD‑P are the medium effect concentrations of free and included pesticides, respectively; and xi and yi are the fractions of free and included pesticides, respectively. The apparent EC50 (or LC50) values calculated from eq 12 correlated closely with the values observed from the experiE



Article

Findings and mechanistic analysis in this study indicated that the presence of CD alters the bioavailability of organic pollutants through multiple concurrent interactions (e.g., inclusion complexation and adsorption of a pseudophase). The modification of contaminant bioavailability by CD may be conveniently described by the one-variable (i.e., CD concentration) mathematical model. This model provides theoretical guideline for the selection of CD type and application rates when CDs are used to either assess or enhance the bioavailability of contaminants. An important finding from the modeling and experiments suggests that β-CD is likely superior to HPCD that is currently widely used, with the advantages of high efficiency (Figure 1), low cost, and moderate persistence in the environment.20,21 The selection of β-CD over HPCD will likely reduce the overall cost of CDbased remediation treatments. Observations from this study form the basis for more detailed studies involving more organic pollutants and other types of environmental matrices and addressing different objectives.

in bioavailability assessment and bioremediation enhancement.30,39 Thus, eq 11 illustrates the profile of bioavailable fraction of pesticide as a function CD level (Figure 1). The

■

ASSOCIATED CONTENT

S Supporting Information *

Additional text, tables, and figures. This material is available free of charge via the Internet at http://pubs.acs.org.

■

AUTHOR INFORMATION

Corresponding Author

*Phone/Fax: +86-411-8470 7844. E-mail: [email protected]. cn. Notes

The authors declare no competing financial interest.

■

ACKNOWLEDGMENTS This study was supported by the National Natural Science Foundation of China (Nos. 21077020, 41171382, and 21137001), the Fok Ying Tung Education Foundation (No. 114042), the Fundamental Research Funds for the Central Universities, and the Program for New Century Excellent Talents in University (No. NCET-11-0047). The artificial climate incubator used in algal growth inhibition tests was donated by the International Foundation for Science (No. F/ 4580-1). We would like to thank the anonymous referees for their constructive comments and suggestions.

Figure 1. Profile of bioavailable fraction (α) of pesticide over CD levels.

presence of CD commonly enhanced the bioavailability of all test pesticides, except for metolachlor in the soil and kaolin systems. In most cases, an apparent increase in bioavailability of pesticide was observed at a relatively low and moderate level of CD, followed by a plateau at the high level. In addition, HPCD was not the optimal bioavailability-enhancing reagent under the conditions considered in this study, even though HPCD has been widely employed in various applications. For example, bioavailability-enhancement followed an order β-CD > RMCD > HPCD for butachlor in soil and RMCD > HPCD > β-CD for fipronil in kaolin. On the other hand, CDs are commercially available at distinct prices, with HPCD and MCD (50−80 USD/kg) typically many times more expensive than β-CD (3−4 USD/ kg). Whether single or a mixture of pollutants is targeted for remediation, the remediation end-points may be achieved with CDs at different application rates (Figure 1). Accordingly, the cost of CDs used in the remediation treatment varies with both the price and application rates. The selection of the inexpensive β-CD is likely more cost-effective than HPCD, because the former has similar or higher bioavailability-enhancing capability for certain organic pollutants (Figure 1).

■

REFERENCES

(1) Schwarzenbach, R. P.; Escher, B. I.; Fenner, K.; Hofstetter, T. B.; Johnson, C. A.; von Gunten, U.; Wehrli, B. The challenge of micropollutants in aquatic systems. Science 2006, 313 (5790), 1072− 1077. (2) Relyea, R. A. A cocktail of contaminants: how mixtures of pesticides at low concentrations affect aquatic communities. Oecologia 2009, 159 (2), 363−376. (3) Bondarenko, S.; Gan, J. Simultaneous measurement of free and total concentrations of hydrophobic compounds. Environ. Sci. Technol. 2009, 43 (10), 3772−3777. (4) Barriuso, E.; Benoit, P.; Dubus, I. G. Formation of pesticide nonextractable (bound) residues in soil: magnitude, controlling factors and reversibility. Environ. Sci. Technol. 2008, 42 (6), 1845−1854. (5) Alexander, M. Aging, bioavailability, and overestimation of risk from environmental pollutants. Environ. Sci. Technol. 2000, 34 (20), 4259−4265. (6) Escher, B. I.; Hermens, J. L. Internal exposure: linking bioavailability to effects. Environ. Sci. Technol. 2004, 38 (23), 455A− 462A.

F



Article

(7) Heitzer, A.; Webb, O. F.; Thonnard, J. E.; Sayler, G. S. Specific and quantitative assessment of naphthalene and salicylate bioavailability by using a bioluminescent catabolic reporter bacterium. Appl. Environ. Microb. 1992, 58 (6), 1839−1846. (8) Allan, I. J.; Semple, K. T.; Hare, R.; Reid, B. J. Cyclodextrin enhanced biodegradation of polycyclic aromatic hydrocarbons and phenols in contaminated soil slurries. Environ. Sci. Technol. 2007, 41 (15), 5498−5504. (9) van der Heijden, S. A.; Jonker, M. T. O. PAH bioavailability in field sediments: comparing different methods for predicting in situ bioaccumulation. Environ. Sci. Technol. 2009, 43 (10), 3757−3763. (10) Jia, F.; Cui, X.; Wang, W.; Delgado-Moreno, L.; Gan, J. Using disposable solid-phase microextraction (SPME) to determine the freely dissolved concentration of polybrominated diphenyl ethers (PBDEs) in sediments. Environ. Pollut. 2012, 167, 34−40. (11) Cui, X. Y.; Mayer, P.; Gan, J. Methods to assess bioavailability of hydrophobic organic contaminants: principles, operations, and limitations. Environ. Pollut. 2013, 172, 223−234. (12) Brusseau, M. L.; Wang, X. J.; Wang, W. Z. Simultaneous elution of heavy metals and organic compounds from soil by cyclodextrin. Environ. Sci. Technol. 1997, 31 (4), 1087−1092. (13) Mitton, F. M.; Gonzalez, M.; Pena, A.; Miglioranza, K. S. B. Effects of amendments on soil availability and phytoremediation potential of aged p,p′-DDT, p,p′-DDE and p,p′-DDD residues by willow plants (Salix sp.). J. Hazard. Mater. 2012, 203−204, 62−68. (14) Szejtli, J. Past, present, and future of cyclodextrin research. Pure Appl. Chem. 2004, 76 (10), 1825−1845. (15) Liu, H. H.; Cai, X. Y.; Wang, Y.; Chen, J. W. Adsorption mechanism-based screening of cyclodextrin polymers for adsorption and separation of pesticides from water. Water Res. 2011, 45 (11), 3499−3511. (16) Loftsson, T.; Masson, M. Cyclodextrins in topical drug formulations: theory and practice. Int. J. Pharm. 2001, 225 (1−2), 15−30. (17) Jessel, N.; Oulad-Abdelghani, M.; Meyer, F.; Lavalle, P.; Haîkel, Y.; Schaaf, P.; Voegel, J. C. Multiple and time-scheduled in situ DNA delivery mediated by β-cyclodextrin embedded in a polyelectrolyte multilayer. Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 8618−8621. (18) Hartnik, T.; Styrishave, B. Impact of biotransformation and bioavailability on the boxicity of the insecticides alpha-cypermethrin and chlorfenvinphos in carthworm. J. Agric. Food. Chem. 2008, 56 (22), 11057−11064. (19) Wong, F.; Bidleman, T. F. Hydroxypropyl-beta-cyclodextrin as non-exhaustive extractant for organochlorine pesticides and polychlorinated biphenyls in muck soil. Environ. Pollut. 2010, 158 (5), 1303−1310. (20) Fava, F.; Berlin, L.; Fedi, S.; Zannoni, D. Methyl-β-cyclodextrinenhanced solubilization and aerobic biodegradation of polychlorinated biphenyls in two aged contaminated soils. Biotechnol. Bioeng. 2003, 81 (4), 381−390. (21) Fenyvesi, E.; Gruiz, K.; Verstichel, S.; De Wilde, B.; Leitgib, L.; Csabai, K.; Szaniszlo, N. Biodegradation of cyclodextrins in soil. Chemosphere 2005, 60 (8), 1001−1008. (22) Cuypers, C.; Pancras, T.; Grotenhuis, T.; Rulkens, W. The estimation of PAH bioavailability in contaminated sediments using hydroxypropyl-beta-cyclodextrin and Triton X-100 extraction techniques. Chemosphere 2002, 46 (8), 1235−1245. (23) Papadopoulos, A.; Paton, G. I.; Reid, B. J.; Semple, K. T. Prediction of PAH biodegradation in field contaminated soils using a cyclodextrin extraction technique. J. Environ. Monit. 2007, 9 (6), 516− 522. (24) Bardi, L.; Ricci, R.; Marzona, M. In situ bioremediation of a hydrocarbon polluted site with cyclodextrin as a coadjuvant to increase bioavailability. Water, Air, Soil Pollut. 2003, 3 (3), 15−23. (25) Molnár, M.; Leitgib, L.; Gruiz, K.; Fenyvesi, É.; Szaniszló, N.; Szejtli, J. Enhanced biodegradation of transformer oil in soils with cyclodextrin–from the laboratory to the field. Biodegradation 2005, 16 (2), 159−168.

(26) Szejtli, J. Introduction and general overview of cyclodextrin chemistry. Chem. Rev. 1998, 98 (5), 1743−1753. (27) Józefaciuk, G.; Muranyi, A.; Fenyvesi, E. Effect of cyclodextrins on surface and pore properties of soil clay minerals. Environ. Sci. Technol. 2001, 35 (24), 4947−4952. (28) Stroud, J. L.; Paton, G. I.; Semple, K. T. Linking chemical extraction to microbial degradation of C-14-hexadecane in soil. Environ. Pollut. 2008, 156 (2), 474−481. (29) Villaverde, J.; Maqueda, C.; Morillo, E. Improvement of the desorption of the herbicide norflurazon from soils via complexation with beta-cyclodextrin. J. Agric. Food. Chem. 2005, 53 (13), 5366− 5372. (30) Reid, B. J.; Stokes, J. D.; Jones, K. C.; Semple, K. T. Nonexhaustive cyclodextrin-based extraction technique for the evaluation of PAH bioavailability. Environ. Sci. Technol. 2000, 34 (15), 3174−3179. (31) Hickman, Z. A.; Swindell, A. L.; Allan, I. J.; Rhodes, A. H.; Hare, R.; Semple, K. T.; Reid, B. J. Assessing biodegradation potential of PAHs in complex multi-contaminant matrices. Environ. Pollut. 2008, 156 (3), 1041−1045. (32) Hartnik, T.; Jensen, J.; Hermens, J. L. M. Nonexhaustive betacyclodextrin extraction as a chemical tool to estimate bioavailability of hydrophobic pesticides for earthworms. Environ. Sci. Technol. 2008, 42 (22), 8419−8425. (33) Gould, S.; Scott, R. C. 2-Hydroxypropyl-beta-cyclodextrin (HPbeta-CD): a toxicology review. Food Chem. Toxicol. 2005, 43 (10), 1451−1459. (34) Gomez-Eyles, J. L.; Collins, C. D.; Hodson, M. E. Using deuterated PAH amendments to validate chemical extraction methods to predict PAH bioavailability in soils. Environ. Pollut. 2011, 159 (4), 918−923. (35) Fai, P. B.; Grant, A.; Reid, B. J. Compatibility of hydroxypropylbeta-cyclodextrin with algal toxicity bioassays. Environ. Pollut. 2009, 157 (1), 135−140. (36) Abe, I.; Fukuhara, T.; Kawasaki, N.; Hitomi, M.; Kera, Y. Characteristics of cyclodextrin adsorption onto activated carbons. J. Colloid Interface Sci. 2000, 229 (2), 615−619. (37) Sheremata, T. W.; Hawari, J. Cyclodextrins for desorption and solubilization of 2,4,6-trinitrotoluene and its metabolites from soil. Environ. Sci. Technol. 2000, 34 (16), 3462−3468. (38) Józefaciuk, G.; Muranyi, A.; Fenyvesi, E. Effect of randomly methylated beta-cyclodextrin on physical properties of soils. Environ. Sci. Technol. 2003, 37 (13), 3012−3017. (39) Villaverde, J. Time-dependent sorption of norflurazon in four different soils: use of beta-cyclodextrin solutions for remediation of pesticide-contaminated soils. J. Hazard. Mater. 2007, 142 (1−2), 184− 190. (40) Kishimba, M. A.; Henry, L.; Mwevura, H.; Mmochi, A. J.; Mihale, M.; Hellar, H. The status of pesticide pollution in Tanzania. Talanta 2004, 64 (1), 48−53. (41) Konstantinou, I. K.; Hela, D. G.; Albanis, T. A. The status of pesticide pollution in surface waters (rivers and lakes) of Greece. Part I. review on occurrence and levels. Environ. Pollut. 2006, 141 (3), 555−570. (42) OECD guideline for testing of chemicals, 2002. Fresh water alga and cyanobacteria growth inhibition test. Draft Rev Sed Guideline 201, OECD, Paris. (43) OECD guideline for testing of chemicals, 1992. Fish acute toxicity test. Draf t Rev Sed Guideline 203, OECD, Paris. (44) Guo, H. Q.; Zhang, J.; Liu, Z. Y.; Yang, S. G.; Sun, C. Effect of Tween80 and beta-cyclodextrin on the distribution of herbicide mefenacet in soil-water system. J. Hazard. Mater. 2010, 177 (1−3), 1039−1045. (45) Cai, X. Y.; Liu, W. P.; Chen, S. W. Environmental effects of inclusion complexation between methylated beta-cyclodextrin and diclofop-methyl. J. Agric. Food. Chem. 2005, 53 (17), 6744−6749. (46) Bizzigotti, G. O.; Reynolds, D. A.; Kueper, B. H. Enhanced solubilization and destruction of tetrachloroethylene by hydroxypropG



Article

yl-beta-cyclodextrin and iron. Environ. Sci. Technol. 1997, 31 (2), 472− 478. (47) Ko, S. O.; Schlautman, M. A.; Carraway, E. R. Partitioning of hydrophobic organic compounds to hydroxypropyl-beta-cyclodextrin: experimental studies and model predictions for surfactant-enhanced remediation applications. Environ. Sci. Technol. 1999, 33 (16), 2765− 2770. (48) Pérez-Martínez, J. I.; Gines, J. M.; Morillo, E.; GonzalezRodriguez, M. L.; Mendez, J. R. M. Improvement of the desorption of the pesticide 2,4-D via complexation with HP-beta-cyclodextrin. Pest Manage. Sci. 2000, 56 (5), 425−430. (49) Stella, V. J.; Rao, V. M.; Zannou, E. A.; Zia, V. V. Mechanisms of drug release from cyclodextrin complexes. Adv. Drug Delivery Rev. 1999, 36 (1), 3−16. (50) Kilsdonk, E. P.; Yancey, P. G.; Stoudt, G. W.; Bangerter, F. W.; Johnson, W. J.; Phillips, M. C.; Rothblat, G. H. Cellular cholesterol efflux mediated by cyclodextrins. J. Biol. Chem. 1995, 270 (29), 17250−17256. (51) Hu, X. L.; J.F., L.; Lu, S. Y.; Jiang, G. B. Freely dissolved concentration and bioavailability of environmental pollutants. Prog. Chem. 2009, 21 (15), 514−523. (52) Bosma, T. N. P.; Middeldorp, P. J. M.; Schraa, G.; Zehnder, A. J. B. Mass transfer limitation of biotransformation: quantifying bioavailability. Environ. Sci. Technol. 1997, 31 (1), 248−252. (53) Mayer, P.; Fernqvist, M. M.; Christensen, P. S.; Karlson, U.; Trapp, S. Enhanced diffusion of polycyclic aromatic hydrocarbons in artificial and natural aqueous solutions. Environ. Sci. Technol. 2007, 41 (17), 6148−6155. (54) Gouliarmou, V.; Mayer, P. Sorptive bioaccessibility extraction (SBE) of soils: combining a mobilization medium with an absorption sink. Environ. Sci. Technol. 2012, 46 (19), 10682−10689.

H


Mathematical Model for Cyclodextrin Alteration of

Recommend Documents