desorption of tetracycline, oxytetracycline and chlortetracycline on pine bark, oak ash and mussel shell

Journal of Environmental Management 250 (2019) 109509

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Research article

Competitive adsorption/desorption of tetracycline, oxytetracycline and chlortetracycline on pine bark, oak ash and mussel shell

T

Manuel Conde-Cida, Gustavo Ferreira-Coelhob, Manuel Arias-Estéveza, Cristina Álvarez-Esmorísa, Juan Carlos Nóvoa-Muñoza, Avelino Núñez-Delgadob,∗, María J. Fernández-Sanjurjob, Esperanza Álvarez-Rodríguezb a b

Department of Plant Biology and Soil Science, Faculty of Sciences, Campus Ourense, Universidade de Vigo, 32004, Ourense, Spain Department of Soil Science and Agricultural Chemistry, Engineering Polytechnic School, Universidade de Santiago de Compostela, Lugo, 27002, Spain

A R T I C LE I N FO

A B S T R A C T

Keywords: Bio-adsorbents Chemical degradation Competitive adsorption Desorption Tetracycline antibiotics

We studied competitive adsorption for the tetracycline antibiotics (TCs) tetracycline (TC), oxytetracycline (OTC), and chlortetracycline (CTC) on three bio-adsorbents (mussel shell, oak wood ash, and pine bark). The results were compared for individual systems (with antibiotics added separately) and ternary systems (with all three antibiotics added simultaneously). In all cases batch-type experiments were carried out, with 24 h of contact time. In the individual systems, concentrations of 200 μmol L−1 were used for each of the three antibiotics, separately. In the ternary system, all three TCs were added simultaneously, using the following total concentrations: 50, 100, 200, 400, 600 μmol L−1, each antibiotic being 1/3 of the total. Taking into account that ionic strength of a solution is related to a measure of the concentration of ions in that solution, the use of individual and ternary systems allows to compare, for each antibiotic, systems having equal concentrations and similar ionic strength (concentrations of 200 μmol L−1), and systems having different concentrations and ionic strength (200 μmol L−1 in the individual systems, and 600 μmol L−1 in the ternary systems, resulting from the sum of 200 μmol L−1 corresponding to each of the three antibiotics). Adsorption/desorption results indicated that these processes were in all cases closely related to pH values, and to carbon and non-crystalline minerals contents in the bio-adsorbents. Both oak ash and pine bark adsorbed close to 100% of TCs in individual and ternary systems, with desorption < 4% for oak ash, and < 12% for pine bark. However, mussel shell gave clearly poorer results, only relatively acceptable for CTC, with adsorption < 56% and desorption even > 30% for TC and OTC. In view of the results, oak ash and pine bark can be recommended as effective bio-adsorbents for the three TCs studied, and could be useful to retain/inactive them in wastes, and soil or liquid media receiving these emerging pollutants, thus reducing risks of damage for public health and the environment.

1. Introduction Chemical pollution is one of the causes of soil degradation (Bridges and Oldeman, 1999), and, specifically, contamination due to the spreading of antibiotic residues can cause environmental degradation, affecting both soils and waters receiving these emerging pollutants (Bastos et al., 2018). In fact, antibiotics are widely used in human medicine, and also in animals, where they are also employed as growth promoters (Zhang et al., 2019). In China, approximately 162,000 t of antibiotics were consumed in 2013, with 52% of them used in veterinary, while in the United States 22,700 tons of antibiotics are consumed yearly, with near 50% of them directed to veterinary use (Kümmerer, 2009; Zhang et al., 2015, 2019). Spain is one the of the

∗

European Union countries with higher consumption of antibiotics, with 3000 t used yearly in animals, most of them tetracycline antibiotics (Conde-Cid et al., 2018). Currently, there are more than 2000 veterinary pharmaceutical products available on the market (Tasho and Cho, 2016), and an increase of 67% is expected in the use of veterinary antibiotics by 2030 (Van Boeckel et al., 2015). These antibiotics are incompletely metabolized in animals (El-Shafey et al., 2012), with sometimes more than 90% being excreted as original compound, which can cause its dispersion in the environment, directly with excreta, or indirectly when manures and slurries are spread as fertilizers. Recently, laboratory scale studies were performed on different soils in Galicia (NW Spain), focusing on the adsorption of several tetracycline antibiotics (Fernández-Calviño et al., 2015a, b). In addition, the

Corresponding author. E-mail address: [email protected] (A. Núñez-Delgado).

https://doi.org/10.1016/j.jenvman.2019.109509 Received 13 April 2019; Received in revised form 13 August 2019; Accepted 1 September 2019 0301-4797/ © 2019 Elsevier Ltd. All rights reserved.

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2. Materials and methods

presence of tetracycline antibiotics has also been verified for Galician soils, manures, slurries, and crops (Conde-Cid et al., 2018), although in a limited number of samples. Specifically, Tetracycline (TC) was found in 5 soils, in many cases together with other tetracyclines, Oxytetracycline (OTC) was found in 2 soils, and Chlortetracycline (CTC) was not found in the set of soils analyzed, taking into account that this was a limited set of samples, and the first time that soils were analyzed for antibiotics in that geographic area. In fact, at a global scale, the presence of antibiotics in fertilizers and slurries has become an important environmental issue, related to bacterial resistance, entry into soils, surface and ground-waters, and the food chain, supposing a relevant risk for human and animal health (Bengtsson-Palme and Larsson, 2016; Charuaud et al., 2019; Conde-Cid et al., 2018; Cycoń et al., 2019; Grenni et al., 2018; Kivits et al., 2018). The behavior and fate of antibiotics depend on its characteristics, but also on those of soils, as well as on weather and climatic conditions. In this regard, the most important characteristics of antibiotics are photo-stability, binding and adsorption to different soil components, biodegradation potential, and water solubility. Some antibiotics are hydrophobic or non-polar, while other have high water solubility, depending on pH. Among antibiotics, some of them contain several ionic functional groups, and several acid dissociation constants (pKa), and in some cases they may have a pH-dependent charge (Wang and Wang, 2015). Regarding soil characteristics, Sibley and Pedersen (2008) indicate that the amount and composition of organic matter (OM) strongly affects antibiotics adsorption, due to the presence in OM of a large number of functional groups that dissociate at different pH, providing a wide variety of adsorption sites. Other soil characteristics strongly affecting adsorption processes are clay content, pH, and competitive interactions between some antibiotics (Parolo et al., 2008). Although an initial partial mitigation of antibiotics toxicity can be reached through soil retention, in the long term this capacity can be saturated, increasing risks of passage to plants and water bodies. In view of that, the use of bio-adsorbent materials is of growing interest, as efficient and low-cost alternative to remove/retain these pollutants from soils and waters. Bio-adsorbents include natural raw materials, as well as some waste and by-products. Also clearly interesting, new types of materials, such as metal organic frameworks and activated carbon fibers, have been used to retain antibiotics (Xiong et al., 2018a, b) or other pollutants (Xiong et al., 2017). Generally, materials locally available in large quantities, which are effective and low-cost sorbents, are considered best choices (Coelho et al., 2014; Cutillas-Barreiro et al., 2014). The use of these materials as adsorbents can, therefore, be considered an appropriate approach for both improving waste management and protecting the environment (Silva et al., 2018). These authors compiled different works carried out in recent years on the use of waste and by-products as adsorbents for pharmaceutical compounds, and pointed out the scarcity of multicomponent studies (those including various antibiotics simultaneously). In fact, multi-component studies are especially relevant for veterinary antibiotics, as the simultaneous presence of several different antibiotic compounds is frequent in animal manures or slurries, most of which are spread on soils (Conde-Cid et al., 2018). In view of that background, the main objective of this work is to shed light on competitive adsorption/desorption processes for three tetracycline antibiotics (tetracycline, oxytetracycline and chlortetracycline), using two forest by-products (oak ash and pine bark), and a byproduct from the food industry (mussel shell). In addition, adsorption/ desorption results are compared for individual and ternary (multicomponent) systems, varying the molar concentrations of the antibiotics and the resulting ionic strength. The results of this work could be of relevance in order to elucidate the capacity of these by-products to retain the studied antibiotics in multi-component systems, and thus their potential to reduce risks of pollution and damage for the affected environmental compartments.

2.1. Materials 2.1.1. Bio-adsorbent materials Two of the bio-adsorbents were by-products from the forest industry, specifically oak wood ash from a combustion boiler in Lugo (Spain), and pine bark (a commercial product from Geolia, Madrid). The third bio-adsorbent was finely ground (< 1 mm) mussel shell from the Abonomar S.L. factory (A Illa de Arousa, Pontevedra Province, Spain). 2.1.2. Antibiotics Three different HPLC-grade tetracycline antibiotics were used, all of them supplied by Sigma-Aldrich (Barcelona, Spain): tetracycline (TC) (95%, CAS number: 0 000 064 755); oxytetracycline (OTC) (95%, CAS number: 0 002 058 460); and chlortetracycline (CTC) (76%, CAS number: 0 000 064 722), all three as hydrochloride. More general details on these antibiotics are provided in Fernández-Calviño et al. (2015a, b). 2.2. Methods 2.2.1. Characterization of the bio-adsorbent materials All three bio-adsorbent materials were previously characterized (Romar-Gasalla et al., 2018), with analytical results shown in Table S1 and Figs. S1–S4 (Supplementary Material). 2.2.2. Adsorption and desorption experiments To study adsorption, batch-type experiments were carried out, stirring for 24 h 1 g of each bio-adsorbent material with 40 mL of 0.005 M CaCl2, which also contained a specific concentration of the antibiotics under study. Specifically, for the individual adsorption test, a concentration of 200 μmol L−1 was used for each antibiotic (separately). In the ternary (multi-component) test (competition among the three tetracycline antibiotics), the total concentrations used for the three antibiotics together were: 50, 100, 200, 400, 600 μmol L−1, each antibiotic corresponding to 1/3 of the total concentration in each case. After contacting each bio-adsorbent with the CaCl2 solution containing the corresponding concentration of antibiotic, and performed the subsequent agitation for 24 h, all samples were centrifuged at 4000 rpm (6167×g) for 15 min. In the equilibrium solution, the concentration of each of the three tetracycline antibiotics was quantified by HPLC (see details below). The amount of antibiotic adsorbed was calculated by the difference between the added concentration and that remaining in the equilibrium solution. In addition, in the same equilibrium solutions pH was determined using a glass electrode (Crison, Barcelona, Spain). The results allow to compare each antibiotic for the following: a) on the one hand, adsorption at equal total molar concentration of antibiotics (i.e., similar or equivalent ionic strength), for an antibiotic in an individual system (concentration of 200 μmol L−1 for one antibiotic) with the same antibiotic in a ternary system in which total concentration is 200 μmol L−1 for the sum of the three antibiotics, thus being 66.67 μmol L−1 for each; b) on the other hand, adsorption at different total molar concentration of antibiotics (i.e., with different ionic strength), for an antibiotic in an individual system (concentration of 200 μmol L−1 for one antibiotic) with the same antibiotic in a ternary system in which total concentration is 600 μmol L−1 for the sum of the three antibiotics, thus being 200 μmol L−1 for each. In all cases, determinations were made in triplicate. Regarding desorption, each solid precipitate remaining from the adsorption phase was added with 40 mL of 0.005 M CaCl2. Then, each sample was stirred for 24 h, and centrifuged at 4000 rpm (6167×g) for 15 min. In the equilibrium solution, pH was determined as indicated above. All determinations were made in triplicate. 2

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Table 1 Fitting of antibiotics (TC, OTC and CTC) adsorption data to the Langmuir and Freundlich models, for the three bio-adsorbents used. Cases where fitting was not good due to high error values are indicated by means of cursive and lower size fonts. Bio-adsorbent

Oak ash

Pine bark

Mussel shell

Antibiotic

TC OTC CTC TC OTC CTC TC OTC CTC

Langmuir Qm (μmol kg−1)

Error

KL (L μmol−1)

Error

R2

R2adj

RSS

RMSE

58825.87 20086.48 8749.75 2.6040 e5 2.4322 e8 6.0183 e4 2.5602 e7 4.0310 e6 1.6545 e8

97245.23 15055.02 563.997 6.5843 e5 1.87379 e12 4.5849 e4 1.2004 e11 4.9058 e9 2.8835 e12

0.0064 0.0251 1.6823 0.00418 2.046 e−6 0.03501 7.4383 e−7 2.6848 e−5 5.3191 e−7

0.0118 0.0276 0.3885 0.0108 0.0157 0.0302 0.0034 0.0043 0.0092

0.985 0.965 0.988 0,998 0.985 0.996 0.944 0.900 0.981

0.981 0.953 0.984 0.997 0.980 0.995 0.925 0.866 0.975

440711.73 1082790 426496.08 61818.33 507793.10 132456.98 315343.14 399910.92 429579.87

383.281 600.775 377.048 143.548 411.417 210.124 324.213 365.107 378.408

KF (μmol kg−1)

Error

n

Error

R2

R2adj

RSS

RMSE

398.72 732.17 4151.33 1544.50 1114.77 399.2011 2080.1883 989.05 7.6115 7.6077 28.9161 13.07

133.14 290.32 310.93 704.04 75.9620 135.1152 125.2232 419.44 11.0324 15.2521 16.3411 15.52

0.9389 0.7359 0.4268 0.69 0.9715 1.0878 0.9116 0.96 1.1940 1.1296 1.3079 1.14

0.1131 0.1355 0.0504 0.12 0.0362 0.1312 0.0442 0.13 0.2994 0.4074 0.1423 0.20

0.985 0.973 0.986 0.950 0.998 0.987 0.997 0.986 0.953 0.904 0.993 0.978

0.982 0.964 0.981 0.934 0.998 0.982 0.996 0.964 0.938 0.873 0.990 0.968

447217.00 840751.63 513338.53 1.31 e7 54478.99 446292.08 92173.55 7.77 e6 262488.61 380335.70 159974.20 1.39 e6

386.098 529.386 413.657 2093.55 134.757 385.699 175.284 1609.04 295.797 356.059 230.921 834.254

Freundlich

Oak ash

Pine bark

Mussel shell

TC OTC CTC TC+OTC+CTC TC OTC CTC TC+OTC+CTC TC OTC CTC TC+OTC+CTC

Qm: Langmuir's maximum adsorption capacity; KL: Langmuir's parameter related to the strength of interaction adsorbent/adsorbate; KF: Freundlich's parameter related to the adsorption capacity; n: Freundlich's parameter related to the solid heterogeneity; R2: coefficient of determination; R2adj: adjusted coefficient of determination; RSS: residual sum of squares; RMSE: root mean squared error; * Obtained from Eq. (4).

of Cu and Cd competition on kaolin; and Arias et al. (2006) included additional parameters to account for competition between Cu and Zn in Murali–Aylmore equations (a model used to describe adsorption of individual adsorbates from multiadsorbate solutions when all these adsorbates comply with Freundlich equations in the absence of competitors), whereas Oladipo and Gazi (2015) used a competitive, multicomponent Langmuir isotherm to express the adsorption process, and Oladipo et al. (2015) included a selectivity factor into the extended Langmuir model to get better modeling of binary competitive adsorption of dyes on a chitosan-based hydrogel. In this way, in the current work an initial approach can be done taking into account the total amount of antibiotics adsorbed (Eq. (4))

2.2.3. Quantification of the tetracycline antibiotics A previously described procedure (López-Peñalver et al., 2010; Fernández-Calviño et al., 2015a, b), subjected to just slight modifications, was followed to determine each of the three tetracycline antibiotics. Details are included in Supplementary Material. 2.2.4. Data analyses and statistical treatment The Freundlich (Eq. (1)) and Langmuir (Eq. (2)) models were used for data obtained in the adsorption experiments: n qa = KF Ceq

qa =

(Eq. 1)

KL Ceq qm 1 + KL Ceq

1

(Eq. 2)

TC OTC CTC TC OTC CTC (Qeq + Qeq + Qeq ) = KF (Ceq + Ceq + Ceq )

n

(Eq. 4)

−1

where, regarding the Freundlich model, qa (μmol kg ) is the amount of antibiotic adsorbed at equilibrium; Ceq (μmol L−1) is the concentration of antibiotic present in the solution at equilibrium; KF (Ln μmol1−n kg−1) is the Freundlich affinity coefficient; n (dimensionless) is the Freundlich linearity index. Regarding the Langmuir model, KL (L μmol−1) is a Langmuir constant related to the adsorption energy, and qm (μmol kg−1) is the Langmuir's maximum adsorption capacity. In a further step, the Tempkin model (Eq. (3)) was used:

qa = β ln KT + β ln Ce

OTC TC CTC where Qeq , Qeq and Qeq are the amounts of TC, OTC and CTC adCTC OTC TC , Ceq and Ceq are the concentration of TC, OTC and CTC sorbed, Ceq remaining in solution at equilibrium, and KF and n are the Freundlich's parameters. As indicated above for the model of Murali and Aylmore (1983), several other models have been used to describe the adsorption of individual adsorbates from multi-adsorbate solutions, once again in those cases where all these adsorbates comply with Freundlich equations in the absence of competitors (LeVan and Vermeulen, 1981; Koopal et al., 1994). In the current work, the best fit corresponded to the Murali–Aylmore model (equations (5)–(7)):

(Eq. 3)

where β = RT/bt and bt: Temkin isotherm constant; Kt: Tempkin isotherm equilibrium binding constant (L g−1); T: Temperature (25 °C) (K = 298°), R: universal gas constant (8314 Pa m3/mol K). In addition, taking into account that in multi-component systems there is potential competition for adsorption sites, as well as a variety of interactions, both the Langmuir and Freundlich models could be modified to address interferences. As examples, Arias et al. (2002) proposed modifications of the Freundlich equation to get a better fitting in cases

QeqTC =

nTC + 1 KFTC × CTC CTC + aTC × (COTC + CCTC )

QeqOTC =

3

COTC

nOTC + 1 KFOTC × COTC + aOTC × (CTC + CCTC )

(Eq. 5)

(Eq. 6)

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QeqCTC =

CCTC

nCTC + 1 KFCTC × CCTC + aCTC × (COTC + CTC )

7350, 7753, and 7634 μmol kg−1 for OTC, CTC and TC, respectively, while oak ash adsorbed 7010, 7676, and 7011 μmol kg−1 of OTC, CTC and TC. For both materials, percentage adsorption was close to 100% for any antibiotic concentration added (Fig. 1). This indicates that adsorption surfaces are not saturated at the antibiotics concentrations used, and no competition among antibiotics is evidenced in these circumstances. Regarding mussel shell, the highest adsorption results for the highest dose of antibiotics added were 5740, 2557 and 2015 μmol kg−1 for CTC, TC and OTC, respectively, thus clearly higher for CTC. Adsorption percentages showed few variations depending on the concentration of antibiotic added (Fig. 1), being much higher for CTC (62–78%), than for TC (7–31%) and OTC (1–33%). Fernández-Calviño et al. (2015b), in a previous study with different soils also found higher affinity for CTC than for the other two TCs. This could be attributed to structural factors of the antibiotic molecules. In fact, the presence of a chlorine atom in the C7 position of the CTC molecule could explain the higher adsorption of CTC. It would be due to a decrease in electron charge density of the ring system, caused by the presence of Cl, then resulting in a parallel decrease in the pKa of the structural part corresponding to the phenolic bicketone (pKa2), finally giving an increase in its polarity and solubility (Pils and Laird, 2007). In view of that, the higher affinity of CTC for soil adsorption sites would be related to structural aspects that confer higher ionization of the functional groups dimethylamine and phenolic b-diketone involved in adsorption processes (Pils and Laird, 2007). Thiele-Bruhn (2003) showed that adsorption mechanisms are varied and complex for tetracycline antibiotics, and include H bonds, formation of outer- and inner-sphere complexes, cationic bridges, electrostatic attractions, and ion exchange processes. These mechanisms depend on physic-chemical characteristics of both antibiotics and sorbent materials (Kemper, 2008). Among these characteristics, pH is one of those having most influence on antibiotic/adsorbent interactions, simultaneously affecting chemical speciation of antibiotics and of sorbent surfaces (Figueroa-Diva et al., 2010). Both, tetracycline antibiotics and certain components of some adsorbent materials (components such as organic matter, non-crystalline compounds, etc.), have functional groups that can undergo protonation/deprotonation reactions, depending on the pH of the solution. This makes possible the existence of positive, negative or neutral charges on

(Eq. 7)

where CTC, COTC and CCTC are concentrations of each antibiotic remaining in solution at the equilibrium, KFTC , KFOTC y KFCTC , nTC , nOTC and nCTC are Freundlich's parameters included in Table 1 (see below), and aTC , aOTC and aCTC are additional parameters related to competence among all three antibiotics, which could be called selectivity factors. Taking into account that a is placed in the denominator of the quotients, higher a values give lower Qeq values, which means lower amounts of antibiotic adsorbed. Desorption was expressed as the amount of antibiotic desorbed (μmol kg−1), and also as the percentage of antibiotic desorbed with respect to the amount previously adsorbed. The statistical software R, version 3.1.3 (R Core Team, 2015) and the nlstools package for R (Baty et al., 2015) were used to perform adjustments of the adsorption models to the experimental data, while the SPSS 15.0 software was used to carry out bivariate Pearson's correlations (results shown in Tables S2 and S3, Supplementary Material). 3. Results and discussion 3.1. Adsorption of the three tetracycline antibiotics on the various bioadsorbents in a ternary system Firstly, it should be taken into account that previous studies have indicated that adsorption of tetracycline antibiotics is considered fast for soils and other sorbent materials (Chen and Huang, 2010; Kang et al., 2010; Lin et al., 2013), reaching equilibrium in less than 15 h (and in some cases in less than 3 h). Other works have also shown that some changes take place regarding OTC, CTC and TC adsorption/desorption kinetics on soils, comparing individual and competitive experiments (Fernández-Calviño et al., 2015a, b), even if all of them remain rapid. In the current work, when the three antibiotics are added simultaneously and at the same concentration, adsorption increases for all three TCs on all bio-adsorbents as a function of the antibiotics concentration added (Fig. 1). Pine bark, and oak ash, were the sorbents showing the highest adsorptions in all cases. For the highest dose of antibiotics added, adsorption was slightly higher on pine bark, with

Fig. 1. Amounts adsorbed in the three different bio-sorbents (in absolute values and percentages) for each tetracycline antibiotic (OTC, CTC, and TC), when added simultaneously. In all cases, triplicate determinations were performed, and coefficients of variation were always < 5% (shown as error bars). 4

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the adjustment in some cases, which is indicated by means of cursive and lower size fonts in the table. In the case of the Freundlich model, R2 values ranged between 0.846 and 0.998. In the Langmuir model, Qm (maximum adsorption capacity) values are higher for mussel shell and pine bark, however, the error of this parameter is very high in some cases, where it can be considered not adjustable, as indicated in the table by means of cursive and lower size fonts. The KL parameter is a constant related to the free energy of adsorption (Khezami and Capart, 2005) and is generally much lower in mussel shell (even if it can be considered not adjustable due to the very high error values). It correlated with different chemical characteristics of the adsorbents: positively and significantly (p < 0.01) with Alo for TC and CTC (r = 0.999, in both cases), and with exchangeable and total cations (always with r > 0.998). For TC and CTC, KL is also significantly correlated (p < 0.05) with Feo (r = 0.999, in both cases), and with eCEC (r > 0.998 in both cases) (Tables S2 and S3, Supplementary Material). The fact of finding good correlations with noncrystalline Al and Fe, and with different cations present in the bio-adsorbents, can be indicative of high adsorption energy for some antibiotics when they are bound to these non-crystalline minerals through a cationic bridge. In fact, KL values are generally higher for oak ash, which is the adsorbent with the most alkaline pH and with the highest low-crystallinity Al and Fe contents. In any case, our KL values are lower than those obtained for soils by Teixidó et al. (2012) (between 0.18 and 1.67 L μmol−1), and by Li et al. (2010) (between 0.038 and 0.067 L μmol−1), with the exception of those of CTC in oak ash and pine bark (but also taking into account that the latter can be considered not adjustable due to too high error values). Regarding the Freundlich model, KF values (related to the adsorption capacity of a given adsorbent, Bhaumik et al., 2012) are clearly lower in the case of mussel shell (and even considered not adjustable due to too high error values) (Table 1), which is coincident with the lower adsorption previously commented for this material. CTC generally has the highest KF values, in agreement with the higher adsorption obtained for this antibiotic. The sequence of KF values for oak ash was: KF CTC > KF TC+OTC+CTC > KF OTC > KF TC; while for pine bark it changed for the two latter: KF CTC > KF TC+OTC+CTC > KF TC > KF OTC; and in the case of mussel shell KF OTC and KF TC values were very similar (Table 1). The n parameter indicates the reactivity and heterogeneity of the active sites of the adsorbent. It can be interpreted as follows: if n = 1, the adsorption is linear, while if n > 1 the adsorption process is mainly of a chemical nature, and if it is < 1, it denotes the presence of heterogeneous high energy adsorption sites, with strong interactions between adsorbate molecules, where physical adsorption would be the most favorable, and high-energy sites are the first to be occupied (Behnajady and Bimeghdar, 2014; Foo and Hameed, 2010; Khezami and Capart, 2005). Table 1 shows that n values are in all cases < 1 for oak ash, as well as for pine bark (except in the case of OTC), indicating the presence of high energy sites and a cooperative-type adsorption. For these two bioadsorbents n is generally close to 1, which is interpreted as a tendency to a linear model. For mussel shell, n value is always > 1, and CTC is the antibiotic showing the highest score. These results indicate an overall higher affinity for adsorption sites, as well as a higher binding energy for CTC (as well as for all three antibiotics as a whole) compared to individual adsorption of TC or OTC in the ternary system. Similarly, Vijayaraghavan et al. (2006) indicate that when KF and 1/n reach their maximum values, adsorption capacity and affinity between the bio adsorbent and the adsorbate are also higher, and in the present study these circumstances take place in oak ash and pine bark, especially for CTC (Table 1). As shown in Table 2, the fitting to the multiadsorbate model of Murali-Aylmore of adsorption data in the ternary system CTC-OTC-TC can be considered satisfactory, in view of the R2 values (between 0.886 and 0.999), with p < 0.05.

the reactive surfaces, and subsequently the formation of different types of bonds (Sun et al., 2010). In fact, the high adsorption found for pine bark can be related to its high organic C content (Table S1). Souza et al. (2016) found a high interaction between TCs and different organic matter fractions, and indicated that these fractions have different affinities for the antibiotics, depending on their characteristics, thus differently affecting adsorption, transport and bioavailability of the antibiotics. At the pH of pine bark (pH 3.99, Table S1), tetracycline antibiotics would be positively charged (H3TC+), or in neutral form (H2TC), and would bind to certain functional groups of organic matter, such as carboxylic, which can be dissociated at pH values between 3 and 6, and thus negatively charged (Edwards et al., 1996). Gu et al. (2007) also found a high retention for TC on humic acids at pH < 6, related to interactions between deprotonated carboxylic groups and the cationic and zwitterionic species of TC. In our study, we found a significant (p < 0.05) and negative correlation between TCs adsorption on pine bark and the pH of the equilibrium solution (r = −0.865 for OTC and CTC, and r = −0.872 for TC) (Tables S2 and S3, Supplementary Material), indicative of a release of H+ during the adsorption process. Oak ash also showed a high adsorption capacity for the three antibiotics. The alkaline nature of this material, and its abundance in components of variable charge, specifically non-crystalline Fe and Al (Feo, Alo) (Table S1), would not favor TCs retention, since this alkaline pH would cause high negative charge density for both the antibiotics and the variable charge components present in the adsorbent, preventing bindings due to electrostatic attractions. However, other mechanisms can act, such as adsorption by means of cationic bridges (Wang and Wang, 2015). Cations can bind to the negatively charged part of the antibiotic, and to adsorbing surfaces also negatively charged, giving ternary complexes (Gu et al., 2007). The high Ca2+ concentrations present in oak ash (Table S1) would favor these interactions, especially in the case of exchangeable Ca, which is clearly higher in oak ash than in mussel shell (Table S1). Parolo et al. (2012) also focused on cationic bridges to explain the high adsorption found for TC on montmorillonite at pH > 5, highlighting the clear implication of Ca2+ in that process. In addition, the alkaline pH prevailing in oak ash (clearly higher than that of mussel shell, Table S1), would favor overall sorption, specifically promoting complexation and precipitation with Ca2+. Furthermore, the low adsorption found for TCs in mussel shell coincides with its lower content in those components reported to be of main relevance in retention, i.e. organic matter and non-crystalline Fe and Al, as well as having a lower pH in relation to ash (Table S1). Fig. S4 (Supplementary Material) shows infrared spectra for the three sorbent materials before and after adsorption of the antibiotics, evidencing some modifications due the adsorption process. In addition, taking into account pH values in the equilibrium solution after adding increasing concentrations of the three tetracycline antibiotics to the bio-sorbents (Table S4, Supplementary Material), two kinds of situations can be found. On the one hand, in the case of pine bark (which had pH < 4.5) a decrease in the solution pH takes place as the added concentration and the subsequent adsorption of the three antibiotics increases, which may be related to an exchange of protons between tetracyclines charged positively and H+ from components of pine bark. On the other hand, this process does not occur for oak ash and mussel shell, for which pH values in the equilibrium solution are always higher than 7.5 (higher than 11.8 for oak ash), causing that tetracyclines can be negatively charge, facilitating adsorption through a cationic bridge, without proton exchange. 3.2. Adjustment of adsorption results to the Langmuir and Freundlich models Table 1 shows that adsorption data fits clearly better to the Freundlich than to the Langmuir model. Even if R2 values ranged in all cases between 0.759 and 0.995 for Langmuir, too high error values invalidate 5

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studied, as commented by authors such as Gao et al. (2012) or Rajapaksha et al. (2015). In addition, to be noted that no correlations were found between Temkin parameters and the studied sorbent materials.

Table 2 Fitting of adsorption data to the adapted equations of Murali and Aylmore (1983) (Eqs. (5)–(7)), using TC, OTC and CTC solutions in relations 1:1:1, with adsorbed antibiotic concentrations expressed in μmol kg−1 and antibiotic concentrations in the equilibrium solution expressed in μmol L−1. Bio-adsorbent

Antibiotic (against competing), and Equation

a

R2

Oak ash

TC (OTC+CTC); OTC (TC+CTC); CTC (TC+OTC); TC (OTC+CTC); OTC (TC+CTC); CTC (TC+OTC); TC (OTC+CTC); OTC (TC+CTC); CTC (TC+OTC);

8.35 7.27 2.54 0.83 15.64 0.77 0.50 0.58 0.69

0.999* 0.979* 0.967* 0.998* 0.984* 0.997* 0.958* 0.886* 0.992*

Pine bark

Mussel shell

Eq. Eq. Eq. Eq. Eq. Eq. Eq. Eq. Eq.

(5) (6) (7) (5) (6) (7) (5) (6) (7)

3.3. Desorption of the three tetracycline antibiotics from the various bioadsorbents in a ternary system Fig. 2 shows negligible desorption for the two lowest concentrations of antibiotics added. However, desorption becomes more evident as added concentration increases, with an overall sequence: oak ash < pine bark < mussel shell. The maximum desorption corresponded in all cases to the highest concentration of antibiotics added, being 1787.78 μmol kg−1 for TC, 1660.95 μmol kg−1 for OTC, and 1096.48 μmol kg−1 for CTC. Expressing desorption as percentage, it is evident that oak ash and pine bark have a high capacity to retain all three tetracycline antibiotics, with practically irreversible adsorption at low and medium doses of TCs. However, mussel shell shows relevant desorption when high concentrations of antibiotics are added, reaching 44, 34.32, and 11.77% for TC, OTC and CTC, respectively. Therefore, mussel shell would not be appropriate for TCs retention, also taking into account its lower capacity for TCs adsorption. However, oak ash and pine bark could be interesting as adsorbents for the three antibiotics, given their high adsorption and low release. In a previous study, Jeong et al. (2012) also obtained high retention for the antibiotic tylosil using other forest by-products, such as wood chips.

a: parameter related to competence among all three antibiotics (selectivity factor); *p < 0.05.

Table 2 shows that the degree of competence among the three antibiotics (indicated by the selectivity factor, a) varied for the three bioadsorbents studied. As commented above, higher a values give lower amounts of antibiotic adsorbed. The highest a values corresponded to oak ash (except in the case of OTC for pine bark), while the lowest corresponded to mussel shell. In the case of oak ash, TC shows the highest a value (8.35), and thus the lower adsorption, decreasing for OTC (a = 7.27), and mostly for CTC (a = 2.54). In pine bark, OTC shows the highest a score (15.64), with a marked decrease for TC (a = 0.83) and for CTC (a = 0.77), indicating again that CTC is the most competitive and the most adsorbed among all three antibiotics. Mussel shell shows the lowest values for a among the three bio-adsorbents studied, with similar scores for all three antibiotics. In view of that, this model indicates that CTC is the most competitive antibiotic in the ternary system, in the case of oak ash and pine bark, with lower competence among antibiotics in the case of mussel shell. Table 3 shows fitting of adsorption data to the Temkin model, which assumes that adsorption is characterized by uniform binding energies distribution up to the maximum level (Ofomaja and Unuabonah, 2013). The Temkin model takes into account adsorption heat, and assumes that adsorption energy decreases linearly with surface occupation due to adsorbent-adsorbate interactions. In the current work, the Temkin isotherm satisfactorily explains adsorption of the three TCs, with R2 ranging between 0.806 and 0.986, with the lowest values corresponding to OTC and CTC adsorption on pine bark, and the highest to TC and CTC adsorption on oak ash. The Temkin model is considered appropriate for chemical adsorption based on strong electrostatic interactions between positive and negative charges. This further supports the relevance of chemisorption processes in the bio-sorbents here

3.4. Comparison of adsorption/desorption for the three tetracycline antibiotics in individual and ternary systems as a function of molar concentration of antibiotics As first step, the adsorption of each of the three tetracycline antibiotics was compared between an individual system (for a concentration of 200 μmol L−1 of a single antibiotic), and a ternary system (all three TCs together, at the same concentration of 200 μmol L−1 each, reaching a total sum of 600 μmol L−1). Since the final molar concentration in the ternary system is 600 μmol L−1, there will be also different ionic strength compared to the individual systems (with only one antibiotic at 200 μmol L−1). As second step, the individual and ternary systems were compared in situations where molar concentrations were the same, so that in the individual systems each of the TCs was added separately in a concentration of 200 μmol L−1, and in the ternary systems each antibiotic was added in a concentration of 66.67 μmol L−1, giving a final concentration of 200 μmol L−1. Fig. 3 shows adsorption and desorption percentages for the three antibiotics in individual and ternary systems, as well as with equal and different molar concentrations. In the case of pine bark, no competition among TCs was observed, with adsorption always close to 100%. These

Table 3 Fitting of antibiotics (TC, OTC and CTC) adsorption data to the Temkin model, for the three bio-adsorbents used. Bio-adsorbent

Oak ash

Pine bark

Mussel shell

Antibiotic

TC OTC CTC TC OTC CTC TC OTC CTC

Temkin Kt (L g−1)

Error

bt

Error

R2

R2adj

RSS

RMSE

0.3688 1.3914 19.8187 1.9489 1.3050 4.5321 0.0607 0.0502 0.2457

0.0514 0.9136 4.6061 0.7021 0.7814 2.0699 0.0179 0.0131 0.1272

739.2207 1359.033 1439.436 986.887 1240.74 1110.033 2219.112 2519.266 1397.421

363.915 520.280 145.777 575.812 645.998 572.054 239.427 198.813 498.935

0.978 0.879 0.986 0.889 0.806 0.866 0.902 0.909 0.853

0.971 0.838 0.982 0.852 0.742 0.822 0.869 0.879 0.804

673083.66 3774680.0 493762.08 4140370.0 6712520.0 5157020.0 553655.61 360372.38 3455730.0

473.667 1121.707 405.693 1174.786 1495.830 1311.108 429.595 346.589 1073.271

bt: Temkin isotherm constant; Kt: Tempkin isotherm equilibrium binding constant; R2: coefficient of determination; R2adj: adjusted coefficient of determination; RSS: residual sum of squares; RMSE: root mean squared error. 6

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Fig. 2. Desorption from the three different bio-sorbents (absolute values and percentages) for each tetracycline antibiotic (OTC, CTC, and TC), when added simultaneously at different concentrations. In all cases, triplicate determinations were performed, and coefficients of variation were always < 5% (shown as error bars).

results only partially acceptable in the case of CTC (adsorption in the range 66–80%, and desorption < 12%).

high adsorption results are maintained both in individual and ternary systems, with the same or different molar concentration/ionic strength. In the case of oak ash, adsorption is also high (> 80%), and molar concentration has low effect. Adsorption was always lower in mussel shell, and the differences between individual and ternary system are more pronounced. In fact, in ternary systems adsorption increased for TC and OTC, while decreased for CTC, as compared to individual systems. The presence of CTC favors OTC and TC adsorption in mussel shell, and that of OTC in oak ash, independently of the molar concentration/ionic strength. It could be related to the higher CTC adsorption onto the adsorbent surfaces due to the presence of a chlorine atom at the C7 position of the molecule, which increases its polarity and solubility in water, as noted above. With that in mind, and taking into account that polar-type interactions control the binding of these antibiotics to the adsorbent surfaces (Pils and Laird, 2007), it could explain the potentiating effect of CTC on the adsorption of the other TCs observed in the ternary systems. Luo et al. (2018), studying the adsorption of oxytetracycline on bio-char, also found an increase in the adsorption efficiency in a ternary system with respect to an individual system. Fig. 3 also shows that percentage desorption was very low in the individual system, indicating the irreversibility of the process. However, in the ternary system an increase in percentage desorption is observed, slightly higher when the ionic strength is increased. Desorption was always lower than 4% and 12%, for oak ash and pine bark, respectively, reaching values between 4 and 30% for mussel shell. All three antibiotics are desorbed in higher percentage in ternary than in individual systems. In addition, CTC is the antibiotic showing the lowest desorption results in all cases, due to its high affinity for the adsorbent surfaces. In a previous study, Fernández-Calviño et al. (2015b) compared their results for competitive desorption of the same three TCs with other non-competitive experiments reported in Fernández-Calviño et al. (2015a), also finding that desorption percentages were slightly higher in competitive trials. As overall result, it is clear that both pine bark and oak ash can be affective sorbents for the removal/retention of all three antibiotics, showing high adsorption and low desorption, even when all three TCs are present simultaneously at concentrations of 200 μmol L−1 each. However, mussel shell showed clearly lower retention potential, with

4. Conclusions Among the three byproducts used, those of forest origin performed as excellent bio-adsorbents for the three tetracycline antibiotics studied. Specifically, these sorbents were pine bark (a material with high C content and low pH), and oak ash (with high content in non-crystalline minerals, and high pH). Both forest byproducts showed high adsorption and low desorption for CT, OTC and CTC, both when the antibiotics were added separately (individual systems), or simultaneously (ternary system). The high adsorption results found for pine bark can be attributed to electrostatic attractions between antibiotics and variable charge components present in the bark, which would be positively charged at the acidic conditions prevailing. In the case of oak ash, the most likely mechanisms are bindings through cationic bridges between antibiotics and non-crystalline minerals of the adsorbent. Desorption from pine bark was slightly higher than that from oak ash, especially in the case of OTC added at high doses. The third of the byproducts, mussel shell, is characterized by having the lowest adsorption and retention capacity for the three antibiotics studied, although this bioadsorbent performed acceptably for CTC. For both pine bark and oak ash, differences in the adsorption between individual and ternary systems are scarce. However, in the case of mussel shell the simultaneous presence of the three antibiotics increased the adsorption of TC and OTC, and decreased that of CTC. In addition, the adsorption of the three antibiotics in this bio-adsorbent is increased when the ionic strength is higher. For all antibiotics and bio-adsorbents, desorption increased in the ternary system, especially when the ionic strength was higher. In view of the results of this study, both forest by-products can be recommendable for the removal/retention of tetracycline antibiotics, whether they appear independently or simultaneously. Mussel shell could perform acceptably just for CTC, but it would not be advisable for retaining TC and OTC. All these results could be useful to control soil and water pollution due to tetracycline antibiotics, thus reducing risks for human and environmental health. 7

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Fig. 3. Adsorption and desorption percentages for each tetracycline antibiotic (OTC, CTC, and TC) in the three different bio-sorbents, both in individual (each antibiotic separately) and ternary systems (all three antibiotics simultaneously), with the same or different molar concentration and ionic strength value. In all cases, triplicated determinations were performed, and coefficients of variation were always < 5% (shown as error bars).

Declarations of interest

by the Improving Coordination of Senior Staff (CAPES), Post-Doctoral Program Abroad (PDE)/Process number {88881.172297/2018-01} of the Brazilian Government. The sponsors had not involvement in study design; in the collection, analysis and interpretation of data; in the writing of the report, and in the decision to submit the article for publication.

None. Acknowledgements Funding: This work was supported by the Spanish Ministry of Economy and Competitiveness [grant numbers CGL2015-67333-C2-1-R and CGL2015-67333-C2-2-R]. It also received funds from the European Regional Development Fund (ERDF) (FEDER in Spain), being a complement to the previous grants, without additional grant number. M. Conde-Cid holds a pre-doctoral contract (FPU15/0280, Spanish Government). The research of Dr. Gustavo F. Coelho was also supported

Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.jenvman.2019.109509.

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