Sorption and desorption of selected pharmaceuticals by polyethylene microplastics

Marine Pollution Bulletin 136 (2018) 516–523

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Sorption and desorption of selected pharmaceuticals by polyethylene microplastics Roger Mamitiana Razanajatovoa, Jiannan Dinga,b, Shanshan Zhanga, Hang Jianga, Hua Zoua,b, a b

T ⁎

School of Environmental and Civil Engineering, Jiangnan University, Wuxi 214122, China Jiangsu Collaborative Innovation Center of Technology and Material of Water Treatment, Suzhou 215009, China

ARTICLE INFO

ABSTRACT

Keywords: Microplastics Pharmaceuticals Sorption Desorption Model

The aim of the present study was to evaluate the sorption and desorption of sulfamethoxazole (SMX), propranolol (PRP) and sertraline (SER) by polyethylene (PE) microplastics in water. After the 96 h mixture, the sorption percentages of pharmaceuticals on PE microplastics decreased according to the following order: SER (28.61%) > PRP (21.61%) > SMX (15.31%). The sorption kinetics were fitted well with the pseudo-secondorder model. Both linear and Freundlich models were able to describe the sorption isotherm. The results suggest that the sorption process of the pharmaceuticals may be adequately described by their hydrophobicity and electrostatic interactions. The desorption results showed that 8% and 4% of PRP and SER, respectively, were released from the microplastics within 48 h, but the sorption of SMX was irreversible. The results indicate the potential risks of PRP and SER for bioaccumulation in aquatic organisms via ingestion of the microplastics in aquatic environments.

1. Introduction Due to excessive use and improper disposal, large quantities of plastics are accumulating in aquatic environments via surface runoff, wind dispersal, and other routes (Horton et al., 2017). It is estimated that there will be over 250 metric tons of plastics accumulated in the ocean by 2025 (Jambeck et al., 2015). Due to weathering processes (e.g., photo-oxidative and thermo-oxidative) (Alimi et al., 2018), plastics are broken down into smaller pieces with a size < 5 mm, which are also known as microplastics (Thompson et al., 2004). The presence of microplastics in marine and freshwater environments has been widely documented (Barboza and Gimenez, 2015; Eerkes-Medrano et al., 2015; Li et al., 2016; Shim and Thomposon, 2015). Several works have reported that microplastics are the primary sources of a number of additive chemicals such as plastizers, flame retardants, and antioxidants in the aquatic environment (Gouin et al., 2011; Hahladakis et al., 2018; Hammer et al., 2012; UNEP, 2015). In addition, because microplastics possess a size similar to that of planktons, microplastics may be ingested by aquatic organisms and distributed in their tissues (Cole et al., 2013; Ding et al., 2018). The ingested microplastics would release the additive chemicals and may have effects on aquatics organisms (Koelmans et al., 2013). Apart from the release of additive chemicals, recent studies have demonstrated the role of microplastics as a vector for other pollutants in ⁎

aquatic environments (Ziccardi et al., 2016; Teuten et al., 2009). Once the pollutant-sorbed microplastics are ingested by aquatic organisms, the pollutants may be desorbed from the microplastics and accumulate in the tissues (Paul-Pont et al., 2016; Qu et al., 2018). Hence, sorption and desorption by microplastics may play important roles in the fate of organic pollutants in aquatic ecosystems. To better understand the environmental and ecological impacts of microplastics, there is an urgent need to study the sorption and desorption behaviors of organic pollutants and microplastics in the aquatic environment (Lee et al., 2014). In the last few decades, the widespread accumulation of pharmaceuticals in aquatic environments has received growing attention (Boxall et al., 2012). Due to the extensive production and usage, pharmaceutical compounds are continuously being emitted into the aquatic environment (Kümmerer, 2009). Several pharmaceutical products, such as antibiotics, antidepressants, and beta-blockers, have been detected in surface waters (Khetan and Collins, 2007). Recently, a few studies have shown that some pharmaceutical agents present in water may be sorbed onto microplastics (Wu et al., 2016; Li et al., 2018; Xu et al., 2018). These results suggest that microplastics may affect the fate and transport of various pharmaceutical agents in aquatic environments. However, most of these studies only investigated the sorption of pharmaceuticals by microplastics. Information on the desorption behavior between pharmaceuticals and microplastics is limited.

Corresponding author at: School of Environmental and Civil Engineering, Jiangnan University, Wuxi 214122, China. E-mail address: [email protected] (H. Zou).

https://doi.org/10.1016/j.marpolbul.2018.09.048 Received 13 August 2018; Received in revised form 26 September 2018; Accepted 26 September 2018 0025-326X/ © 2018 Published by Elsevier Ltd.

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The aim of this study was to examine the sorption and desorption processes of pharmaceutical compounds relative to microplastics in water. In the present study, the antibiotic sulfamethoxazole (SMX), the beta-blocker propranolol (PRP), and the antidepressant sertraline (SER) were selected as the sorbates. Ultra-high molecular weight polyethylene (UHMW-PE) microplastics were selected as sorbents. The three target pharmaceuticals and PE microplastics were chosen due to their widespread presence in aquatic environments, as reported by previous studies (Yan et al., 2018; Xie et al., 2017; Aus Der Beek et al., 2016; Godoy et al., 2015; Schultz et al., 2010; Duis and Coors, 2016). Batch experiments were conducted to study the sorption and desorption behaviors of SMX, PRP, and SER by PE microplastics. The sorption/desorption kinetics and sorption isotherms for the three different pharmaceutical compounds were determined. Through these experiments, we hope to broaden our understanding of the environmental behavior of pharmaceuticals affected by microplastics.

experiment, a microplastics to solution ratio of 1:5 (w:v) was used. The experiment duration was 96 h in the kinetics study (Fig. S2). The sample was withdrawn at specific time intervals (3, 6, 12, 24, 48, 72, and 96 h). All of the other procedures were the same as those used in the preliminary experiment and each test was conducted in triplicate. The sorption isotherm study also followed the procedures mentioned above, but five different concentrations (1, 10, 20, 50, and 100 μg L−1) were used for each pharmaceutical agent. The samples were taken at 96 h when the equilibrium was reached for the three pharmaceutical agents as determined by the sorption kinetic studies. 2.2.2. Desorption experiment After the sorption isotherm experiment, the suspension was filtered through a 2 μm glass fiber filter. The filters containing the PE microplastics were then dried in a vacuum desiccator for 2 d. The vacuum desiccator was wrapped with aluminum foil to avoid any possible photodegradation of the pharmaceutical agents. Then, the dried glass fiber filter with PE microplastics was added to a 50 mL centrifuge tube. The tube was filled with 40 mL of ultrapure water containing 0.01 M CaCl2, 0.02% (w/v) NaN3, and 15.5 mM sodium taurocholate to simulate the internal environment of the digestive tract for some aquatic organisms, to determine the role of gut surfactant in desorption of pharmaceuticals from microplastics (Bakir et al., 2014a; Bakir et al., 2016). Afterward, the tube was wrapped with aluminum foil and shaken at 24 °C in the dark. Each test was conducted in triplicate. Then, 1 mL of the sample was withdrawn at each given time interval (3, 6, 12, 24, and 48 h) and filtered through a 2 μm glass fiber filter. All of the obtained samples were stored at −20 °C until the following analyses.

2. Materials and methods 2.1. Materials and chemicals Three target pharmaceuticals (SMX, PRP, and SER) were obtained from Shanghai Send Pharm Co., Ltd. (Shanghai, China) and had a declared purity > 98%. The different physicochemical properties of the three pharmaceuticals are presented in Table S1. A stock solution of each pharmaceutical agent was obtained by dissolving 0.01 g of each pharmaceutical in 1 mL of methanol (HPLC Grade). Working standard solutions of SMX, PRP, and SER (60 μg L−1) were prepared from the stock solutions by serial dilution. This initial concentration was chosen based on the solubility of each pharmaceutical compound (OECD, 2000). UHMW-PE powder with a size ranging from 45 to 48 μm was purchased from Sigma Aldrich (St. Louis, MO, USA) as a representative of PE microplastics. The shape and surface characteristics of the used PE microplastics are shown in Fig. 2. Sodium taurocholate was purchased from Shanghai Macklin Biochemical Co., Ltd. (Shanghai, China). Ultrapure water (DI water, 18.2 MΩ-cm) was taken from a laboratory water purification system (Master - Q15). GF/D glass fiber filters were purchased from Whatman (Maidstone, UK).

2.3. Analysis of the pharmaceutical agents and microplasics surface properties All samples of the pharmaceutical agents were analyzed with an ultra-high-performance liquid chromatography-tandem mass spectrometer (UPLC/MS/MS). The UPLC/MS/MS instrument was Waters ACQUITY UPLC Xevo TQ with electrospray source (Milford, OH, USA) containing an Acquity BEH C18 column (100 mm × 2.1 mm, 1.7 μm). Chromatographic separation was performed with acetonitrile and 0.1% formic acid. During the mass spectrometric detection, the electrospray ionization source (ESI) for the three pharmaceuticals was set to the positive mode. Detailed protocols of the analysis are available in the Supplemental Material (Table S2 and S3). The areas of the peaks of the target compounds were plotted against the standard concentrations resulting in a linear correlation with R2 > 0.99 (Fig. S1). The microplastics surface properties were analyzed with Scanning Electron Microscope (SEM, FEI Quanta 200, Eindhoven, Netherlands).

2.2. Batch experiments 2.2.1. Sorption kinetics and isotherm experiments The kinetic studies involved two steps. First, a preliminary experiment was performed to identify the equilibrium time and relevant sorbent:solution ratio (OECD, 2000). A definitive study was then conducted to develop the sorption kinetics and isotherms of the three pharmaceutical compounds to PE microplastics. In the preliminary experiment, different amounts of PE microplastics were added to 50 mL glass centrifuge tubes containing 40 mL of ultra-pure water. The obtained concentrations of PE microplastics were 50, 200, and 500 mg L−1. In addition, 0.01 M CaCl2 and 0.02% (w/v) NaN3 were added to the tubes to maintain the ionic strength of the suspension and to prevent microbial degradation, respectively. Then, PRP was spiked at an initial concentration of 100 μg L−1. Each test was conducted in triplicate. Tubes were capped and wrapped with aluminum foil to prevent potential photochemical reactions during mixing and were agitated horizontally at 150 rpm at 24 °C for 144 h. The samples were then withdrawn with glass syringes at specific time intervals (3, 6, 12, 24, 32, 48, 72, 96, 120, and 144 h) and filtered through glass fiber filters with a pore size of 2 μm to remove the microplastic particles. Finally, the filtering mediums were stored in the dark at −20 °C until further analysis. Control samples without microplastics were set up under the same testing conditions to determine the possible degradation or the sorption of PRP to the glass receptacle. In the kinetics study, all of the initial concentrations of PRP, SER, and SMX were 60 μg L−1. Based on the results of the preliminary

2.4. Statistical analyses The statistical analysis and data fitting were performed with Microsoft Office Excel 2016 and Sigma Plot 12.5. The mass difference between the initial and residual concentration was used to determine the amount of pharmaceuticals sorbed to the PE microplastics at a given time (t).

qt =

(C0

Ct ) × VW mPE

(1)

−1

where qt (μg g ) is the concentration of pharmaceuticals sorbed to the microplastics at a given time; C0 and Ct (μg L−1) are the initial concentration and residual concentration of a pharmaceutical at given time (t) in liquid phase, respectively; Vw (L) is the solute volume; and mPE (g) is the mass of PE microplastics. The percentage sorbed was calculated according to Eq. (2):

%Sorbed = 517

C0

Ct C0

× 100

(2)

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Fig. 1. Scanning electron microscopic images of PE microplastics used in this study.

The reaction-based sorption kinetics were described by the pseudofirst-order model (PFOM) and the pseudo-second-order model (PSOM). The nonlinear form of Lagergren's first order rate equation is as follows:

qt = qe (1

e

3. Results and discussion 3.1. Morphology of PE microplastics

(3)

K1 t )

The sorption of SMX, PRP, and SER may be related to the properties of the used microplastics. Zhan et al. (2016) state that the surface area of the microplastics may play an important part in the sorption behavior of hydrophobic contaminants. The surface and the morphology of the PE microplastics are shown in Fig. 1. The SEM images evidently show that the shape of the PE microplastics was pellet-like. In addition, the surface of the PE microplastics was rough and several pores could be seen. Previous studies have classified the PE microplastics used in this study as rubbery microplastics (Bakir et al., 2012). The microplastics used in this study have the potential to sorb pollutants, especially hydrophobic compounds (Li et al., 2018; Guo et al., 2012). Due to the various physicochemical properties of the pharmaceutical compounds, the sorption behavior and process were also significantly different. Therefore, the sorption kinetics and isotherm of the pharmaceuticals to the PE microplastics should be studied.

−1

where qt and qe (μg g ) are the concentrations of pharmaceuticals sorbed to the PE-microplastics at a given time (t) and at equilibrium state, respectively. K1 (h−1) is the constant rate of the pseudo-firstorder kinetics. The nonlinear form of the pseudo-second-order equation is as follows:

qt =

qe 2K2 t

(4)

1 + qe K2 t −1

−1

where K2 (g μg h ) is the constant rate of the pseudo-second-order kinetics. Linear and Freundlich sorption models were used to fit the sorption isotherms of the three pharmaceuticals. Briefly, the linear model can be described as: (5)

qe = K d Ce −1

3.2. Sorption kinetics of SMX, PRP, and SER to PE microplastics

−1

where qe (μg g ) and Ce (μg L ) are the sorbed amounts of pharmaceuticals in a solid phase and in the aqueous phase at equilibrium state, respectively; and Kd (L g−1) is the partition coefficient. The Freundlich model is given by: 1

The sorption percentage of the three pharmaceuticals onto the PE microplastics are illustrated in Fig. 2. For SER, PRP, and SMX, the maximum sorption percentages were 28.61%, 21.61%, and 15.31%, respectively. The results indicated that all sorbates used in this study could be sorbed to the PE microplastics. The sorption kinetics data of SMX, PRP, and SER onto the microplastics are presented in Fig. 3. Two common nonlinear sorption kinetics models, i.e., PFOM and PSOM, were used to fit the data and the fitting parameters are shown in Table 1. Compared to PFOM, PSOM is much better at describing the sorption kinetics of the three pharmaceutical compounds, as shown by the relatively higher R2 (Table 1). These findings are consistent with previous studies, where compared to PFOM, the sorption kinetics of SMX onto PE microplastics (Xu et al., 2018) and PRP onto modified attapulgite (Deng et al., 2011) were better described by the PSOM. Based on our knowledge, this is the first study to report the sorption of SER onto microplastics. Our results showed that in PSOM, SER had a relatively higher R2 than in PFOM. The good fitting of PSOM indicates

(6)

qe = Kf Cen

where Kf is the Freundlich sorption coefficient, which indicates sorption capacity; n is the Freundlich isotherm exponent, which determines the nonlinearity. The percentage of desorbed pharmaceuticals was calculated using:

%D =

Cdes × 100 CSorb −1

(7) −1

where Cdes (μg L ) and Csorb (μg L ) are the concentrations of pharmaceuticals desorbed at a given time and the sorbed concentration of pharmaceuticals on the PE microplastics at the beginning of the desorption experiment.

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Fig. 3. The PFOM and PSOM kinetics fitting curve of SER, PRP, and SMX to PE microplastics. Experimental conditions: Cinitial = 60 μg L−1, temperature = 24 °C, pH = 6.85, shaker speed = 150 rpm, contact time = 96 h.

microplastics may be positively related to the hydrophobicity of the target pharmaceuticals. The logKow values of the pharmaceuticals in this study ranged from 0.89 to 5.29 (Table S1). According to Nam et al. (2014), we classified the degree of hydrophobicity of the three pharmaceutical compounds by their logKow, with SMX having a logKow < 2 as low hydrophobicity, PRP with a logKow < 3.5 as medium hydrophobicity, and SER with a logKow > 3.5 as high hydrophobicity. Thus, in this study, SER was expected to be more readily sorbed than SMX and PRP. Recent studies have demonstrated that the logKow of the sorbate plays an important role in determining the sorption extent of hydrophobic organic compounds on microplastics, including non-polar organic compounds, and pharmaceuticals and personal care products (PPCPs) (Hüffer and Hofmann, 2016; Wu et al., 2016; Li et al., 2018). Apart from the hydrophobicity, the sorption process of the three pharmaceuticals on PE microplastics may also be affected by other factors, such as electrostatic interactions. The different pKa values of the target compounds may explain their possible sorption processes. The pKa of SMX, PRP, and SER were 1.90, 9.42, and 9.85, respectively (Table S1), and the pH of the solution in this study was approximately 6.85 ± 0.04. Based on our knowledge, the pKa and pH of the solution may determine the isoelectric charge of the compounds (Mrozik and Stefańska, 2014). Thus, each pharmaceutical has different charges under experimental pH. The different charges of the pharmaceutical compounds under the experimental pH is summarized in Table 3. Moreover, the pH point zero charge (pHpzc) of the PE microplastics is 4.30 (Xu et al., 2018). In this study, the pHpzc of the PE microplastics was lower than the pH of the solution and therefore carried a negative surface charge under the experimental pH. The attraction of the negative charge on the surface of the PE microplastics and the positive charge of the SER and PRP enhanced their sorption to the PE microplastics. On the other hand, the lower sorption capacity of SMX might be due to the repulsion between the negative charges of the PE microplastics. Collectively, the relation between the pKa of the pharmaceuticals, the pH of the solution, and the pHpzc of the microplastics determines the electrostatic attraction/repulsion interactions and may consequently affect the sorption process between pharmaceuticals and microplastics. Further studies are necessary to investigate the sorption of these compounds to PE microplastics under different pH values. Moreover, some other water quality parameters, such as salinity, may also influence the sorption process of pharmaceuticals to microplastics (Wu et al., 2016). Hence, it is necessary to use seawater and/or freshwater in nature as the medium of sorption process in our future lab works.

Fig. 2. Percentage sorbed of SER (A), PRP (B), and SMX (C) to PE microplastics. Error bars indicate ± SD (n = 3). Experimental conditions: Cinitial = 60 μg L−1, temperature = 24 °C, pH = 6.85, shaker speed = 150 rpm, contact time = 96 h. Values not sharing common letters (a-c) are significantly different from each other (p < 0.05).

that the three pharmaceuticals were sorbed to different binding sites on the microplastics (Wang et al., 2015). Therefore, the following discussion is based on the sorption parameters calculated from the PSOM fitting results. As seen in Table 1, at an initial concentration of 60 μg L−1, the maximum sorbed concentrations of SMX, PRP, and SER were respectively 46.09, 64.38, and 88.80 μg g−1; and the sorption equilibrium was achieved at 96 h for the three pharmaceuticals. The equilibrium time was determined during the preliminary experiment (Supplementary material, Fig. S2). In addition, the PSOM rate constant (k2) followed the order: SER > PRP > SMX (Table 1) and was positively correlated with the logKow of the three pharmaceuticals. These results suggest that the adsorption rate and sorption capacity of the pharmaceuticals on PE 519

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Table 1 Estimated PFOM and PSOM parameters for SER, PRP and SMX on PE microplastics. Compound

Pseudo First Order Model −1

Qe (μg g SMX PRP SER

)

Pseudo Second Order Model K1 (h

45.37 60.37 81.58

−1

2

)

0.86 0.26 0.05

R

Qe (μg g−1)

K2 (μg g−1 h−1)

R2

0.996 0.980 0.960

46.09 64.38 88.80

0.01 0.03 0.17

0.999 0.988 0.980

Fig. 4. Linear and Freundlich isotherm model fitting curve of SER, PRP, and SMX to PE microplastics Experimental conditions: Cinitial = 1–100 μg L−1, temperature = 24 °C, pH = 6.85, shaker speed = 150 rpm, contact time = 96 h. Table 2 Estimated Linear and Freundlich parameters for SER, PRP, and SMX on PE microplastics. Compound

SMX PRP SER

Isotherm Linear Model

Freundlich Isotherm

Kd (L g−1)

R2

Kf

1/n

R2

0.70 ± 0.35 2.30 ± 2.79 3.33 ± 0.80

0.912 0.986 0.989

3.09 ± 0.66 2.24 ± 1.09 4.36 ± 0.88

0.54 ± 0.05 0.74 ± 0.20 0.89 ± 0.05

0.977 0.976 0.995

Table 3 Possible interaction between three pharmaceuticals compound and PE microplastics. Compound

Charge

Sorbent surface charge

Force

Sulfamethoxazole(SMX) Propranolol(PRP) Sertraline(SER)

− + +

− − −

Repulsion Attraction Attraction

3.3. Sorption isotherms of SMX, PRP, and SER to PE microplastics The fitting curves of the sorption isotherms based on a linear model and a Freundlich model are presented in Fig. 4. The isotherm parameters obtained by linear and Freundlich nonlinear fitting of Eqs. (5) and (6) are listed in Table 2, respectively. The R2 values of the linear model followed the order SER (0.989) > PRP (0.986) > SMX (0.912). Based on the R2 value, the sorption isotherm of the three pharmaceuticals fit well with the linear model. The highest R2 value of SER and PRP might be due to their high hydrophobicity. Several studies have reported that the sorption of hydrophobic compounds on particles fit well with a linear model (Guo et al., 2012; Nam et al., 2014). However, SMX is known as a hydrophilic compound, and in the present study, the sorption isotherm of SMX still

Fig. 5. The relationship between initial concentration and sorption percentage of SER (A), PRP (B), and SMX (C) to PE microplastics after 96 h mixture. Error bars indicate ± SD (n = 3). Values not sharing common letters (a–c) are significantly different from each other (p < 0.05).

fit a linear model (R2 > 0.91). Previous studies have found that the sorption of SMX on sediments (Le Guet et al., 2018; Wang et al., 2017) and PE microplastics (Xu et al., 2018) fit a linear model as confirmed by the high R2 value. The good fitting of the linear isotherm suggests that 520

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sorption capacity of SMX did not vary significantly by increasing the initial concentration from 1 to 100 μg L−1. We believe that the effect on the sorption of SMX may be masked by the electrostatic repulsion between the negative charge of the microplastics surface and the negative isoelectric point of SMX. These results indicate that the sorption of SER and PRP to microplastics were higher at a lower concentration. It should be noted that environmentally relevant concentrations of the pharmaceuticals in surface water, groundwater and drinking water are ng L−1 to low μg L−1 (Miller et al., 2018). Considering that the low treatment concentrations used in this study (1 μg L−1) were of the same magnitude as the environmentally relevant concentrations of SER and PRP, the sorption of these pharmaceuticals onto microplastics should be carefully considered when tracing their fate in aquatic environments. 3.4. Desorption of pharmaceutical compounds from PE microplastics Fig. 6. Percentage desorbed of SER and PRP from PE Microplastics. Error bars indicate ± SD (n = 3). Experimental condition: QSER initial = 329.97 μg g−1, QPRP initial = 133.49 μg g−1, temperature = 24 °C, contact time = 48 h.

After the isotherm experiment, the sum of the final concentrations of SMX, PRP, and SER sorbed onto the PE microplastics for all the replicates were 86.78, 133.49, and 329.97 μg g−1, respectively. The desorption percentage of the two hydrophobic pharmaceuticals from the PE microplastics are illustrated in Fig. 6. As shown in Figs. 6, 8% and 4% of PRP and SER were desorbed from the PE microplastics after the first 3 h, respectively. Afterward, no significant desorption occurred until 48 h when the desorption equilibrium was reached. The release of PRP and SER from the microplastics might be due to the hydrophobic interactions between the two hydrophobic pharmaceuticals and the PE microplastics. Bui et al. (2013) observed that the highest desorption rates of the hydrophobic pharmaceutical compounds (i.e., diclofenac and ibuprofen) were due to hydrophobic interactions with trimethylsilylated mesoporous SBA-15. Hence, the logKow of the pharmaceuticals not only determined their sorption to microplastics but also had an important role in their release from microplastics. Moreover, as mentioned above, the pharmaceuticals first occupied the high energy sites on the surface of the microplastics and later occupied the low energy sites. Oleszczuk et al. (2009) reported that the desorption of pharmaceuticals from high energy adsorption sites of nanotubes is very difficult. Thus, the release of SER and PRP might be from the surface and/or the low energy sorption sites present on PE microplastics. This hypothesis is similar to that proposed by Hartmann et al. (2017), who reported that HOCs could be easily desorbed from microplastics when sorbed to the surface of microplastics. In the desorption study, SMX was not measurable in the surrounding solution, indicating that the sorption of SMX on PE microplastics was irreversible. This might be due to the hydrophilicity and the low sorption on PE microplastics. Bakir et al. (2014a) have shown that desorption of hydrophilic PFOA from PE microplastics was not measurable since PFOA showed very little affinity for PE microplastics. The irreversible sorption of SMX enlightened that the presence of microplastics would decrease the bioaccumulation potential of hydrophilic pharmaceuticals in aquatic organism tissues. In the desorption experiment, we did not analyze the effect of glass fiber filter. Thus, in our future work it is necessary to use other method to separate the liquid and solid phase instead of filtration using glass fiber filter to confirm the possible effect of glass fiber filter. This study revealed that when aquatic organisms ingest microplastics contaminated by hydrophobic pharmaceuticals, they may act as transporters of these pharmaceuticals into the tissues via desorption. However, the desorption rate of the sorbed contaminants is likely to vary considerably according to the physiological conditions (pH and temperature) of the organisms involved (Bakir et al., 2014a). Previous research has found that a lower pH and higher temperature may enhance the desorption of HOCs from microplastics (Bakir et al., 2014b). However, this effect was not investigated in this study; further studies are necessary to examine the desorption of pharmaceuticals under different physiological conditions.

the sorption process of the pharmaceuticals on PE microplastics was dominated by partition interactions. In addition, the Kd of the three pharmaceuticals were 0.70, 2.30, and 3.33 L g−1 for SMX, PRP, and SER, respectively. These results indicate that compounds with a high hydrophobicity are prone to be sorbed onto microplastics. Bui et al. (2013) investigated the sorption isotherms of 12 selected pharmaceuticals onto trimethylsilylated mesoporous SBA-15 (TMS-SBA-15) and found that the Kd of those pharmaceuticals was positively correlated with their hydrophobicity. The results corroborate that the hydrophobicity of the pharmaceuticals is an important factor in controlling their sorption mechanism onto microplastics. However, further study need to confirm the main force controlling the interaction between the pharmaceuticals and microplastics. The Freundlich model is a nonlinear sorption model and involves the heterogeneity of the microplastics surface. As seen in Table 2, the three pharmaceuticals were well fitted to the Freundlich model, judging from their high R2 between 0.97 and 0.99. These findings are similar to those of previous studies that have found that the Freundlich model could fit the sorption isotherms of persistent organic pollutants such as dichlorodiphenyltrichloroethane, phenanthrene and perfluorooctanoic acide (PFOA) to microplastics (Bakir et al., 2014a) and the sorption isotherms of PPCPs such as bisphenol A, carbamazepine, gemfibrozil, octylphenol and triclosan onto three different soils (Yu et al., 2013). For the three sorbates, all of the 1/n values were < 1, suggesting a decrease in sorption capacity with increasing initial concentrations (Yu et al., 2013), especially for SER and PRP. As shown in Fig. 5A and B, the sorbed percentages of the two hydrophobic compounds (i.e., SER and PRP) with an initial concentration of 1 μg L−1 were higher than those with 100 μg L−1. For PRP and SER, there was a significantly difference in the sorption percentage between treatments of 1 and 100 μg L−1 (p < 0.05). Wang and Wang (2018) revealed that PE microplastics showed a decrease in their sorption efficiencies as the initial pyrene concentration increased. The reason for this phenomenon may be the selective adsorption site of the pharmaceuticals molecules present on the surface of the microplastics. Since the microplastics surface is heterogeneous and porous (Fig. 1), the pharmaceutical molecules may first occupy the high energy sites and later occupy the lower energy sites on the surface of the PE microplastics. In addition, the surface area of PE microplastics may not be large enough. Since hydrophobic interactions might be the dominant interactions in the sorption process of pharmaceuticals onto PE microplastics, in cases of higher initial concentrations, the binding sites (high energy sites and lower energy sites) on the surface of PE microplastics may become rapidly occupied by pharmaceutical molecules. Abdullah et al. (2009) found that a larger surface area can increase the availability of sorption sites. However, the 521

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4. Conclusions

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The obtained results showed that the sorption capacity, behavior and process varied among the pharmaceuticals physico-chemicals properties (e.g. logKow and pKa) and the specific surface area of the PE microplastics (degree of crystalline). The maximum sorption capacities of SER, PRP, and SMX in the sorption processes did not reach up to 50%. This may be due to the fewer availability of sorption sites on the microplastics and electrostatic repulsion interaction. We suggest that in the present study, the sorption processes of SMX, PRP, and SER were primarily dominated by hydrophobic interactions and electrostatic effects. Moreover, PRP and SER desorbed from PE microplastics since they are hydrophobic pharmaceuticals, indicating the potential risks of the two pharmaceuticals for bioaccumulation in aquatic organisms via ingestion of the microplastics in the aquatic environment. In the future studies, due to the mixture of the different pharmaceuticals and various microplastics in the environment, it will be important for future research to investigate the competitive sorption/desorption of pharmaceuticals to microplastics of different kinds and sizes under different surrounding environmental conditions. Acknowledgements This study was supported by the National Natural Science Foundation of China (Grant No. 51809118), the Natural Science Foundation of Jiangsu Province, China (Grant No. BK20170188), the National Key Research and Development Program of China (Grant No. 2016YFE0123600), and the Fundamental Research Funds for the Central Universities (Grant No. JUSRP11714). Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.marpolbul.2018.09.048. References Abdullah, M.A., Chiang, L., Nadeem, M., 2009. Comparative evaluation of adsorption kinetics and isotherms of a natural product removal by Amberlite polymeric adsorbents. Chem. Eng. J. 146 (3), 370–376. Alimi, O.S., Farner Budarz, J., Hernandez, L.M., Tufenkji, N., 2018. Microplastics and nanoplastics in aquatic environments: aggregation, deposition, and enhanced contaminant transport. Environ. Sci. Technol. 52 (4), 1704–1724. Aus Der Beek, T., Weber, F.A., Bergmann, A., Hickmann, S., Ebert, I., Hein, A., et al., 2016. Pharmaceuticals in the environment-global occurrences and perspectives. Environ. Toxicol. Chem. 35 (4), 823–835. Bakir, A., Rowland, S.J., Thompson, R.C., 2012. Competitive sorption of persistent organic pollutants onto microplastics in the marine environment. Mar. Pollut. Bull. 64 (12), 2782–2789. Bakir, A., Rowland, S.J., Thompson, R.C., 2014a. Enhanced desorption of persistent organic pollutants from microplastics under simulated physiological conditions. Environ. Pollut. 185, 16–23. Bakir, A., Rowland, S.J., Thompson, R.C., 2014b. Transport of persistent organic pollutants by microplastics in estuarine conditions. Estuar. Coast. Shelf Sci. 140, 14–21. Bakir, A., O'Connor, I.A., Rowland, S.J., Hendriks, A.J., Thompson, R.C., 2016. Relative importance of microplastics as a pathway for the transfer of hydrophobic organic chemicals to marine life. Environ. Pollut. 219, 56–65. Barboza, L.G.A., Gimenez, B.C.G., 2015. Microplastics in the marine environment: current trends and future perspectives. Mar. Pollut. Bull. 97 (1–2), 5–12. Boxall, A.B.A., Rudd, M.A., Brooks, B.W., Caldwell, D.J., Choi, K., Hickmann, S., et al., 2012. Pharmaceuticals and personal care products in the environment: what are the big questions? Environ. Health Perspect. 120 (9), 1221. Bui, T.X., Pham, V.H., Le, S.T., Choi, H., 2013. Adsorption of pharmaceuticals onto trimethylsilylated mesoporous SBA-15. J. Hazard. Mater. 254, 345–353. Cole, M., Lindeque, P., Fileman, E., Halsband, C., Goodhead, R., Moger, J., et al., 2013. Microplastic ingestion by zooplankton. Environ. Sci. Technol. 47 (12), 6646–6655. Deng, Y., Wu, F., Liu, B., Hu, X., Sun, C., 2011. Sorptive removal of β-blocker propranolol from aqueous solution by modified attapulgite: effect factors and sorption mechanisms. Chem. Eng. J. 174 (2–3), 571–578.

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