Degradation of macrolide antibiotic erythromycin and reduction of antimicrobial activity using persulfate activated by gamma radiation in different water matrices

Chemical Engineering Journal 361 (2019) 156–166

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Degradation of macrolide antibiotic erythromycin and reduction of antimicrobial activity using persulfate activated by gamma radiation in different water matrices

T

⁎

Libing Chua,b, Run Zhuana, Dan Chenc, Jianlong Wanga,b, , Yunpeng Shend a

Collaborative Innovation Center for Advanced Nuclear Energy Technology, INET, Tsinghua University, Beijing 100084, PR China Beijing Key Laboratory of Radioactive Waste Treatment, INET, Tsinghua University, Beijing 100084, PR China c School of Water Resources and Environment, China University of Geosciences, Beijing 100083, PR China d Yili Chuanning Biotechnology Company, Ltd., Xinjiang 835007, PR China b

H I GH L IG H T S

of persulfate by gamma radiation was effective to improve ERY degradation. • Activation 1.4–6.5 times in three kinds of waters by Gamma/PS system. • kTOCincreased reduction increased to 3.4–52% compared to 0.9–25% by gamma radiation alone. • No antimicrobial was observed at 10 kGy to S. aureus in Gamma/PS system. • A higher yield of activity formic and acetic acids by Gamma/PS treatment was observed. • obs

A R T I C LE I N FO

A B S T R A C T

Keywords: Ionizing radiation Antibiotics Persulfate activation Advanced oxidation processes Wastewater treatment

The degradation of macrolide antibiotic erythromycin (ERY) and the reduction of antimicrobial activity was performed using persulfate activated by gamma radiation in different water matrices. The results showed that the rate constant kobs of ERY degradation in γ ray-activated S2O82− (Gamma/PS) system increased by 6.5 times in deionized water, 5.0 times in groundwater and 1.4 times in treated wastewater, respectively. A significant improvement in mineralization rate was observed in Gamma/PS system, with 3.4–52% TOC reduction, compared to 0.9–25% in γ ray system. The results of antimicrobial activity of ERY against E. coli and S. aureus in the three kinds of waters showed that no antimicrobial activity to E. coli was observed at 1 kGy in Gamma/PS system, which required 6 kGy by γ ray alone. The inhibition to S. aureus was still observed at 10 kGy using gamma radiation in groundwater and treated wastewater, which disappeared in Gamma/PS system. The presence of organic substances inhibited ERY degradation more significantly than inorganic anions. In such cases, the ERY degradation rate was promoted by around 2 times and 12 times, respectively in the presence of peptone and glucose in Gamma/PS system. The 14-membered ring of ERY was destroyed by gamma radiation. Formic acid and acetic acid were detected and their yield was higher in Gamma/PS system. The γ ray-activated persulfate process is promising to treat ERY-containing water and wastewater.

1. Introduction Antibiotics have been extensively used in a large amount as therapeutic medicine and veterinary additives to promote growth [1]. Usually, antibiotics are metabolized poorly by body and excreted through urine and feces, which then transported to the sewage treatment plant through sewer networks and eventually enter into the aquatic environment through sewage discharging owing to the fact that

⁎

the conventional secondary biological treatment processes are not effective to remove the antibiotics-like emerging micro-pollutants [2–4]. In addition to producing toxicity to the organisms, antibiotics with the antimicrobial activity could induce the occurrence of antibiotic resistance genes (ARGs) and antibiotic resistance bacteria (ARB) [5,6], which has become a serious issue and drawn increasing attention worldwide [7–9]. Among the antibiotics available, erythromycin (ERY) is widely used

Corresponding author at: Collaborative Innovation Center for Advanced Nuclear Energy Technology, INET, Tsinghua University, Beijing 100084, PR China. E-mail address: [email protected] (J. Wang).

https://doi.org/10.1016/j.cej.2018.12.072 Received 5 September 2018; Received in revised form 12 December 2018; Accepted 14 December 2018 Available online 15 December 2018 1385-8947/ © 2018 Elsevier B.V. All rights reserved.

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Ionizing radiation might activate persulfate by gamma rays or EB (Eqs. (2) and (3)). Moreover, eaq− and H% formed in water radiolysis could also induce the production of SO4%− as described in Eqs. (4) and (5). SO4%− formed could also react with OH− or H2O and convert to %OH (Eqs. (6) and (7)). This demonstrates the unique advantages of ionizing irradiation on activation persulfate. Alkhuraiji et al. [42] reported that γ ray/S2O82− (Gamma/PS) system was more efficient to enhance the mineralization of phenol in aqueous solution. The TOC reduction reached 89% by gamma irradiation with 2.0 mM S2O82− addition, compared to 14.1% by gamma irradiation alone at 10 kGy. Zhang et al. [43] documented that the degradation rate of trimethoprim increased with increasing S2O82− concentrations from 0.5 mM to 2 mM during gamma irradiation. The removal efficiency of TOC and TN increased by around 17% and 35% with 1.5 mM S2O82− addition. However, the enhanced degradation of the macrolide antibiotics in real water matrices by Gamma/PS system was studied scarcely and few literature is available to evaluate the impact of water matrix on the evolution of antimicrobial activity. This information is important for the potential practical application owing to the fact that the dissolved organic substances and some inorganic anions, such as CO32−, HCO3−, NO3− and PO43− existed in the real waters could affect the behavior of degradation and antimicrobial deactivation of the target contaminants.

as both human and veterinary medicine to treat upper and lower respiratory infection caused by Gram-positive bacteria particularly Staphylococcus spp. and feed additives in livestock and poultry farming to promote animals’ growth [10]. The macrolide antibiotics involving ERY, azithromycin and clarithromycin are named in the “watch list” substances of water matrices by the European Union [11]. ERY and its associated ARGs such as ereA, ermA, ermB, mefA and mphB are detected frequently in the secondary effluent, streams and rivers [12–14]. It is necessary to develop an effective technique to reduce ERY in different water matrices. The advanced oxidation processes (AOPs) based on the generation of the powerful %OH, are the promising alternatives to treat the recalcitrant pollutants involving antibiotics [15,16]. The AOPs available include UV photocatalysis [17], O3/H2O2 [18], Fenton and ionizing irradiation [19] and persulfate (PS) activation [20–22], etc. Ionizing irradiation, involving gamma irradiation and electric beam accelerator (EB), belongs to a special AOP because the oxidative species %OH and the reductive species eaq− are generated in situ by water radiolysis (Eq. (1), the value in the bracket means the radiation chemical yield of each species, μmol/J). The organic pollutants could be decomposed effectively via two pathways: oxidation by %OH and reduction by eaq−. The other advantages of ionizing irradiation include good irradiation penetration in aqueous solution, operation at room temperature and no residuals produced [23,24].

S2 O82 −

H2 O→ OH (2.7) + e−aq (2.6) + H·(0.55) + H2 O2 (0.71) + H2 (0.45)

γ − rays/EB HSO− → 5

+ H+ (2.6)

(1)

γ − rays/EB

→

2 SO·4−

(2)

SO·4− + ·OH

(3)

− S2 O82 − + eaq → SO·4− + SO24−

Lin et al. [25] reported that the degradation rate of ERY having a fully saturated CeC bond was slower than that of sulfonamides containing unsaturated aromatic ring by ozonation. With the initial concentration of 40 mg L−1, the reaction time for reaching over 99% removal was 10 min for sulfonamides and 45 min for ERY. Addition of H2O2 with the H2O2/O3 molar ratio of 5 could accelerate ERY degradation greatly. Xekoukoulotakis et al. [26] studied the mineralization of ERY in aqueous solution by using TiO2-UV photocatalysis. With the initial ERY concentration of 10 mg L−1 and TiO2 dose of 200 mg L−1, a TOC removal efficiency of 90% was achieved at a reaction time of 90 min. The degradation intermediates didn’t exhibit antibiotic activity to E coli. Szabó et al. [27] documented that ionizing radiation could eliminate the antimicrobial activity of ERY-containing treated effluent. The inhibition zone cultivated by an agar diffusion test using Staphylococcus aureus disappeared after EB treatment of 4 kGy. Recently, a new reactive sulfate radical (SO4%−) based AOPs that are produced by PS activation, has attracted increasing attention. Similar to %OH, SO4%− has a high redox potential of 2.3–3.1 V, depending on the activation methods, but it has longer half-life time and higher selectivity [28]. The SO4%− react by three ways: addition to aliphatic double bonds, hydrogen abstraction and direct electron transfer [29]. It is reported that the reaction mechanism of SO4%− radical exhibited somewhat difference from that of %OH radical. SO4%− react more easily by electron transfer than %OH but slower by addition and H-abstraction [30]. Thus the degradation efficiency and products pattern might be different. It has been reported that SO4%− is effective to degrade a wide range of toxic pollutants, such as pharmaceuticals [31,32], pesticides [33,34] and dyes [28,35]. Michael-Kordatou et al. [36] studied the UV activated S2O82− photochemical process to degrade ERY and inactivate ERY-resistant Escherichia coli (E. coli) in treated effluent. With an initial ERY concentration of 0.1 mg L−1, 100% of ERY removal could be achieved within 90 min by UV activated PS system, compared to 34% by UV irradiation alone, while the ERY-resistant E. coli was inactivated at a reaction time of 90 min by UV treatment alone and only 45 min by UV/PS system. To produce SO4%−, persulfate needs to be activated by heat [20], UV irradiation [22], alkaline [37], transition metal, such as Fe0, Fe2+, Cu2+, FeS2, bimetallics and trimetallics, etc. [37–40] and biochar [41].

k = 1.1 × 1010 L mol−1 s−1

(4)

S2 O82 − + H·→SO4·− + SO24− + H+ k = 1.4 × 107 L mol−1 s−1

(5)

SO·4− + H2 O→ ·OH + SO24− + H+

(6)

SO·4−

+ OH− → ·OH +

SO24−

k= 360 s−1

k= 1.4 × 107 L mol−1 s−1

(7)

In this work, the treatment of ERY-containing waters by gamma irradiation and Gamma/PS system was investigated. The experiments were carried out: 1) to study the behavior of ERY degradation by gamma irradiation alone at various conditions such as solution pH, the presence of inorganic anions and organic substances such as peptone and glucose; 2) to evaluate the enhancement of H2O2, S2O82− and HSO5− addition; 3) to investigate the improvement of Gamma/PS system on ERY degradation, mineralization and the reduction of antimicrobial activity in deionized water, groundwater and treated wastewater, etc. This study would provide useful information regarding the degradation of antibiotics and the reduction of antimicrobial activity, which will enrich PS activation method by ionizing irradiation. 2. Materials and methods 2.1. Chemicals Erythromycin A, the active constituent of erythromycin-like antibiotics, was purchased from Aladdin Chemical Company with the titer of 2850 μg/mg (CAS 114-07-8). Erythromycin A has a complex chemical structure which contains a 14-membered lactone ring and two sugar groups, L-cladinose and D-desosamine (as shown below). The molecular formula and molecular weight are C37H67O13N and 733.9 g/ mol, respectively (Scheme 1). Potassium monopersulfate triple salt (CAS 70693-62-8) was obtained from Aladdin with KHSO5 basis content > 47%. K2S2O8 (CAS 7727-21-1) was purchased from Alfa Aesar with the purity of 99%. The reagents used in the study including NaCl, Na2CO3, NaHCO3, NaNO3, Na3PO4, Na2SO4 were all analytical grade with purity of higher than 99.0%. Peptone (Oxoid) and humic acid (Aladdin) were technical grade. Glucose, H2O2 (30%) and hydrochloric acid (36–38%) were analytical grade. K2HPO4 for ERY detection was guaranteed reagent 157

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O

ERY solution respectively, which was then irradiated with and without S2O82− addition. 2.4. Analytical methods

OH

ERY concentration was detected by a high-performance liquid chromatography (HPCL) equipped with a photo-diode array detector at the wavelength of 215 nm and XDB-C18 reversed-phase column (4.6 × 150 mm) (Agilent 1200, America). The fluent, flow rate, temperature of column compartment and injection volume were acetonitrile/0.01 M K2HPO4 (55/45), 0.8 mL min−1, 35 °C and 30 μL, respectively. The peak area at around 9.0 min was recorded. The intermediates of ERY degradation were analyzed by a LC–MS analyzer (Shimazu 2010EV, Japan). LC is equipped with a photo-diode array detector and operated at the similar conditions as HPLC, while MS detector is equipped with an APCI ionization source. IC was performed by Dionex ICS 2100 (Thermo Fisher, America) with a IonPac AS19 analytical column (Dionex, 4 × 250 mm), a IonPac AG19 guard column (Dionex, 4 × 50 mm), a DS6 conductive detector and ASRS-4 mm suppressor. The KOH eluent concertation, flow rate, suppressor current, cell temperature and column temperature are 5 mM, 1.0 mL min−1, 13 mA, 35 °C and 35 °C for VFA detection, and 18 mM, 1.0 mL min−1, 45 mA, 35 °C and 30 °C for SO42− detection, respectively. The other equipment used in the study included a TOC analyzer (multi N/C 2100, Analytik Jena) and a pH meter (8103BN, Thermo Orion), and a UV–Vis spectrophotometer (Lambda 25, Perkin Elmer). The sample volume for TOC detection was 4–5 mL. The consumption rate of S2O82− was calculated according the conversion of S2O82− to SO42− since SO42− is the ending products of SO4%− reaction. The reaction stoichiometric efficiency (RSE) was calculated by the concentration of ERY degraded divided by the concentration of S2O82− consumed [38].

N

OH

HO

HO O

O

O

O O

O

O

OH

Scheme 1. The chemical structure of erythromycin A.

(GR). 2.2. Gamma irradiation experiments The gamma irradiation experiments were conducted in the Institute of Nuclear and New Energy Technology of Tsinghua University which is equipped with a high intensity 60Co radiation source. The radioactivity of the 60Co source was 7.4 × 1014 Bq and the dose rate used was 30.8 Gy min−1. The sample tubes with the volume of 40–50 mL were placed at a certain distance from the source and irradiated at room temperatures of 20–22 °C. The different absorbed doses ranging 0.2–10 kGy were obtained by controlling the irradiation time. Each run was carried out more than two times in parallel and the representative data with error bars were shown in the figures. After irradiation, the samples were filtered immediately by 0.45 μm filter and analyzed for ERY and TOC content in most cases. Solution pH was recorded following gamma irradiation. The antimicrobial activity of ERY-containing waters before and after gamma irradiation was tested. The concentrations of volatile fatty acids (VFA) and SO42− were detected by ion chromatograph (IC). The intermediates were identified by LC–MS.

S2 O82 − consumption rate = Csulfate /( C0PS × 2) × 100

(8)

where Csulfate is the concentration of SO42− following gamma tion (mM), and C0PS is the initial S2O82− concentration added

irradia(mM). The antimicrobial activity of ERY in different water matrices following gamma irradiation was evaluated by agar diffusion tests (Standard Kirby-Bauer method) using Staphylococcus aureus (S. aureus) and E. coli as reference strains. Briefly, the Muller Hinton agar plates were prepared and seeded with the bacterial suspension with 106–108 CFU mL−1 concentration. 2–4 holes were punched in each plate using 10–100 μL tip and then around 20 μL samples filled into the holes. After 18 h incubation at 37 °C, the diameter of the inhibition halo formed around the hole was measured to represent the antimicrobial activity.

2.3. Samples preparation The stock solution of ERY (0.1 mM) was prepared by spiking 0.0734 g ERY into 1 L water solution and stirred electromagnetically. It should be noted that ERY is always present as dehydrated form (ERYH2O) in the natural environment. Methanol (50 μL/L) was added to improve fast dissolution. The natural pH value of 0.1 mM ERY in deionizing water was 9.2–9.8 and TOC was 41.0 ± 3.0 mg/L. Hydrochloric acid was added into the ERY solution to adjust the pH carefully to around 7.2 and 5.1, respectively to study the effect of initial pH; 1 mM Cl−, CO32−, HCO3−, NO3−, PO43− and SO42− was spiked into ERY solution, respectively to study the effect of inorganic anions. 1 mM glucose (180 mg L−1), and humic acid and peptone with the same amount of 180 mg L−1 as glucose (since humic acid and peptone are mixture of macromolecular substance without the accurate molecular weight) were spiked into ERY solution, respectively to study the effect of organic substances; 1 mM H2O2, HSO5− and S2O82− was added into the ERY solution, respectively to study the enhancement. Under the above conditions, the initial pH of the solution ranged 8.5–9.5. To investigate the effect of water matrices, ERY was dissolved into groundwater and secondary treated municipal wastewater, respectively with the similar method to deionizing water. The content of dissolved organic matters (DOM) detected in groundwater and treated effluent was 0–0.5 mg TOC L−1 and 3.5–5.0 mg TOC L−1, respectively. To analyze the active species responsible for ERY degradation, 500 mM tertiarybutanol (t-BuOH) and methanol as radicals’ scavengers were added into

3. Results and discussion 3.1. Effects of initial ERY concentrations and pH Fig. 1 depicts the efficiency of ERY removal and mineralization following gamma irradiation with different initial ERY concentrations. The ERY concentration declined steadily with increasing the absorbed doses. Almost complete ERY removal could be achieved at 4.0 kGy, 2.0 kGy and 1.0 kGy with initial ERY concentration of 0.10 mM, 0.05 mM and 0.02 mM, respectively. The ERY degradation by gamma irradiation could be determined by pseudo first-order kinetic model as shown below.

c − ln ⎛ ⎞ = kobs D ⎝ c0 ⎠ ⎜

⎟

(9) −1

where D and kobs is the absorbed dose (kGy) and rate constant (kGy ), C0 and C (mM) is ERY concentration at 0 kGy and D kGy, respectively. The ERY degradation was more rapid with decreasing the initial concentration. The kobs value was 1.09, 3.17 and 3.82 kGy−1 at 158

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60

1.0

pH=9.8 pH=7.2 pH=5.1

0.10 50

0.8

30 0.04

-1

10

0.00

0.6

0.8

0.4

0.0 0.0

0.4

20

0.02

1.2

-Ln (C/C 0)

0.06

C/C0

C (mM)

40

TOC (mg L )

0.08

1.6

0.2

0.4

0.6

0.8

1.0

Dose (kGy)

0.2

0 0

2

4

6 Dose (kGy)

8

10

0.0 0

Fig. 1. Degradation and mineralization of ERY at different initial concentrations by gamma irradiation in deionized water.

1

2 Dose (kGy)

3

4

Fig. 2. Effect of initial pH on ERY degradation following gamma irradiation (C0 = 0.1 mM in deionized water).

2

C0 = 0.10, 0.05 and 0.02 mM, respectively with R > 0.98. This could be explained by the increased intermediates of ERY degradation which compete the reactive species formed during gamma irradiation with ERY and the lower ratio of the reactive species to ERY at the higher ERY initial concentration. The degradation rate of ERY was lower than that of the other antibiotics such as tetracyclines, penicillin and sulfanilamide reported in literature by gamma irradiation at the similar initial concentrations. The kobs values of 3.3–4.0 kGy−1 for 0.12 mM tetracyclines [44], 2.10 kGy−1 for 0.3 mM penicillin G [45], 2.9 kGy−1 for 0.07 mM sulfamethazine [46] and 1.73 kGy−1 for 0.08 mM sulfadiazine [47] in pure water were reported, respectively. ERY has no unsaturated C]C bonds or π-bonds, but it does have reactive sites such as dimethylamino moiety, and could be degraded effectively by gamma irradiation. Why different pollutants have different degradation rate by ionizing irradiation, which needs to be further studied in consideration of the experimental conditions, such as pH, dose rate and the chemical structure, etc. As shown in Fig. 1, the mineralization rate of ERY increased with increasing the absorbed doses. The TOC removal efficiency reached 26–52% at 10 kGy with the initial ERY concentrations of 0.02–0.10 mM, which is much lower than ERY removal efficiency owing to the production of intermediates. The AOPs involving gamma irradiation are efficient to decompose the organic pollutants. However, for reaching a higher mineralization extent, a high dose or reaction time is needed which is not economic [19]. Gamma irradiation is often applied in combination with other methods such as persulfate activation [28] and H2O2 [48,49] to improve the degradation and mineralization of organic pollutants which will be discussed later. Solution pH is a critical factor affecting gamma irradiation-induced degradation of organic pollutants, which is related to the G-values of the reactive species and the properties of the pollutants. As shown in Fig. 2, the ERY degradation by gamma irradiation was a little faster at acidic pH 5.0, followed by neutral and alkaline pH 7.2–9.8, with kobs values of 1.59, 1.11 and 1.09 kGy−1, respectively. At acidic pH, eaq− is likely to react with H+ to produce H%, which reduces the recombining reaction between eaq− and %OH, leading to the increase in the effective concentration of %OH. At alkaline conditions, %OH is readily converted to %O−, which is less reactive [50]. In addition, it is reported that ERY is unstable at acidic pH and the decomposition rate increased with the decrease of the solution pH [51].

A 0.12 3-

PO4

2-

SO4

0.10

PO4 SO4

2-

C (mM)

CO3

CO3

-

0.08

HCO3

2-

HCO3

-

Cl

Cl NO3

0.06

3-

2-

-

-

NO3

-

0.0

0.4

0.8 k 1/kGy

1.2

0.04 0.02 0.00 0

2

4

6

8

10

Dose (kGy)

B 0.12

Glucose Peptone Humic acid

ERY concentration (mM)

0.10

Glucose

Peptone

0.08 Humic acid

0.06

0.0

0.4 kobs

0.8 1/kGy

1.2

0.04 0.02 0.00 0

2

4

6

8

10

Dose (kGy) Fig. 3. ERY degradation rate in the presence of inorganic anions (A) and organic substances (B) following gamma irradiation in deionized water (Inset graph represents the rate constant kobs).

3.2. Effects of inorganic anions and organic substances

protein and carbohydrate. The reactive species formed in water radiolysis might be consumed to react with those substances which affect their reaction with the target pollutant. As shown in Fig. 3, the negative impact in the presence of Cl−, NO3−, HCO3− and PO43−, and positive

In realistic waters such as natural waters and treated wastewater, there are various inorganic anions such as NO3−, HCO3−, CO32−, PO43− and Cl−, and the dissolved organic matters such as humic acid, 159

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impact in the presence of SO42− and CO32− on ERY degradation was observed, while a greater inhibition on ERY degradation was observed in the presence of organic substances, especially peptone. The kobs values were 0.90, 0.78, 0.89, 0.90, 1.25 and 1.40 kGy−1 in the presence of Cl−, NO3−, HCO3−, PO43−, SO42− and CO32−, and 0.57, 0.40, 0.80 kGy−1 with glucose, peptone and humic acid addition, respectively. It is noted that ERY was removed by around 35% with addition of humic acid alone which might be due to adsorption. Our previous study also revealed that the inhibition of peptone on penicillin G degradation was much greater than glucose during gamma irradiation [45]. Cl− can act as %OH scavenger with rate constant of 4.3 × 109 L mol−1 s−1, but the ClOH% generated may decompose to form Cl% and %OH again (6.1 × 109 L mol−1 s−1). The declined ERY degradation in the presence of 1 mM Cl− indicates that the reaction with %OH is favored at this condition. HCO3− is acted as %OH scavenger with rate constant of 8.5 × 106 L mol−1 s−1. NO3− exhibited a high reaction rate with both eaq− (9.7 × 109 L mol−1 s−1) and %OH (0.88–1.2 × 108 L mol−1 s−1). PO43− could react with %OH radical (the rate constant < 1.0 × 107 L mol−1 s−1). The slight increase in kobs value with SO42− addition might be explained by the generation of SO4%− (Eq. (10)) and the removal of eaq− from the media (Eq. (11)) to reduce the radical recombination reaction (Eq. (12)) [50]. Gala et al. [52] found that kobs for degrading diatrizoate increased slightly from 1.94 kGy−1 by gamma irradiation alone to 2.1–2.4 kGy−1 in the presence of SO42− (10–1000 mg L−1). Our recent publication showed that the presence of SO42− (0.5–10 mM) had not obvious influence on sulfamethoxazole degradation by gamma irradiation [53]. Abdel daiem et al. [54] documented that the rate constant of diphenolic acid degradation by 137Cs gamma irradiation in deionized water declined with SO42− addition, but the impact was the least compared to other anions, like Cl− and NO3−. Further research to determine the reaction rate constant of ERY with %OH and SO4%− is needed to confirm the reaction mechanism [55].

SO24− + ·OH → SO·4− + OH−

k= 3.5 × 105 L mol−1 s−1

0.12 H2O2 1 mM

(11)

e−aq + ·OH → OH− k = 3.0 × 1010 L mol−1 s−1

(12)

TOC removal (%)

C (mM)

0.08

40 30 20 10 0

0.06

H2O2

2S2O8 HSO5 HSO5 alone

0.04 0.02 0.00 0.0

0.5

1.0

1.5

2.0

Dose (kGy) Fig. 4. Changes in ERY concentrations following gamma irradiation and TOC reduction at 10 kGy with H2O2, S2O82− and HSO5− addition.

0.2 mM 0.5 mM 1 mM 2 mM 4 mM

C/C0

0.8

70 60

TOC removal (%)

1.0

0.6

50 40 30 20 10 0

1 2 3 2S2O8 dosage (mM)

4

0.4

0.2

0.0 0.0

It is interesting to note that the ERY removal rate was 1.4 times faster with 1 mM CO32− addition. Similar results were found by Lopez Penalver et al. [44], who reported that the rate constant for degrading 20 mg L−1 tatracycline by gamma radiation increased from 0.01 kGy−1 to 0.015–0.037 kGy−1 in the presence of 10–100 mg L−1 CO32−. This might be attributed to the production of CO3%− radicals from the reaction of CO32− and %OH (Eq. (13)). CO3%− were reported to have sufficient redox of 1.78 v (at pH 7) which could degrade organic pollutants through transferring electron. Recent studies also demonstrated that CO3%− play an important role in photocatalytic degradation of oxytetracycline [56] and cylindrospermopsin [57] in the presence of 1.0–3.0 mM CO32− and in thermal activation PS system to degrade naproxen [58]. It should be noted that the degradation efficiency of the pollutants might decline if a higher CO32− concentration applied. In comparison of the effect of CO3%− and HCO3%− addition, the initial pH values with 1 mM CO3%− addition (9.95) was higher than that with 1 mM HCO3%− addition (8.36). More CO32− were existed in the former solution from CO32−/HCO3− conversion which benefits to CO3%− production (Fig. 4).

CO32 − + ·OH → CO·3− + OH− k = 3.9 × 108 L mol−1 s−1

50

-

HSO5 1 mM

(10)

e−aq + SO24− → N/A k = 1.0 × 106 L mol−1 s−1

60

2-

S2O8 1 mM

0.10

0.5

1.0 Dose (kGy)

1.5

2.0

2-

S2O8 consumption rate (%)

100

80

60 0.2 mM 0.5 mM 1 mM 2 mM 4 mM

40

20

0 0

2

4

6

8

10

Dose (kGy) Fig. 5. Effect of S2O82− dosage on ERY degradation (A) and S2O82− consumption (B) following gamma irradiation (C0 = 0.1 mM in deionized water).

(13) ERY production wastewater owing to the fact that ERY is produced by bacterial fermentation. The residue nutrient media such as peptone and carbohydrate could finally enter into the wastewater and affect the efficacy of ERY degradation by ionizing radiation.

Regarding to the effect of organic substances, the great inhibition on ERY degradation in the presence of peptone and glucose might be due to the fact that the organic substances such as glucose and peptides could be oxidized by %OH and compete with the target pollutants for % OH available [45,59]. This problem should be paid attention in treating 160

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1.0 0.8 0.6 0.4 0.2 0.0

60 50 40 30 20 10 0

0

2

4

Gamma alone Gamma/PS 10 9 8 7 6 5 1mM 4 3 10 0

pH

TOC removal (%)

C/C0

A:Deionized water

Ȗ ray alone

6

Ȗ ray+S 2O 8

2-

8

2

4

6

8

10

0

2

4

6

8

10

0

2

8

10

9.5

1.0 0.8 0.6 0.4 0.2 0.0

50

9.0

40 30

pH

TOC removal (%)

C/C0

B:Groundwater

20 10 0

Ȗ ray alone

2-

Ȗ ray+S 2 O 8 1mM

8.5 8.0 7.5

0

2

4

6

8

10

9.5

1.0 0.8 0.6 0.4 0.2 0.0

30

9.0 20

pH

TOC removal (%)

C/C0

C:Effluent

10 0

Ȗ ray alone

8.5 8.0

2-

Ȗ ray+S 2 O 8 1mM

7.5 0

2

4 6 Dose (kGy)

8

10

4 6 Dose (kGy)

Fig.6. Changes in ERY concentration and solution pH, and TOC reduction at 10 kGy in deionized water, groundwater and treated wastewater by Gamma/PS system and gamma irradiation alone (C0 = 0.1 mM, PS = 1.0 mM).

3.3. Improvement of ERY degradation and mineralization

3.4. Gamma/PS system in different PS dosages and water matrices

The enhancement of H2O2, S2O82− and HSO5− addition on ERY decomposition was investigated, respectively following gamma irradiation (Fig. 5). It is clear that ERY degradation and mineralization using Gamma/PS system was more efficient than that using γ ray/H2O2 system. The kobs values increased significantly to around 7.90 kGy−1 in γ ray/PS system, compared to 1.82 kGy−1 in γ ray/H2O2 system. Moreover, the highest TOC reduction of around 50% was observed in Gamma/PS system, compared to 20% in γ ray/H2O2 system at 10 kGy. The TOC reduction could reach 45% by using γ ray-activated HSO5− system. It is noted that by using S2O82− and HSO5− alone, around 20% and 90% of ERY was removed, but no TOC reduction was observed. Yin et al. [60] also reported that the sulfonamide antibiotics such as sulfamethazine, sulfamethoxazole and sulfathiazole, could be removed by more than 95%, but no TOC reduction was obtained by HSO5− treatment alone. The sulfonamides degradation was ascribed to HSO5− direct oxidation through nonradical pathway. The higher degradation efficiency in Gamma/PS system might be attributed to the oxidation of SO4%− radical. Similar trend was reported by other researchers. Alkhuraiji and Leitner [61] reported that the degradation rate of 2-naphthalenesulfonate was higher in Gamma/PS system than that in γ ray/H2O2 system. At an absorbed dose of 0.5 kGy, the removal efficiency of 2-naphthalenesulfonate reached 76% by gamma irradiation alone, 90% by Gamma/H2O2 and 99% by Gamma/ PS treatment. A faster degradation rate by UV/PS system than UV/H2O2 system for degrading ciprofloxacin [62], ampicillin and cephalothin [63], and mineralization of acetic acid [64] in aqueous solution was observed. But Alkhuraiji et al. [42] reported that the phenol degradation was slightly faster in the Gamma/H2O2 system (kobs = 2.23–2.63 kGy−1) than that in Gamma/PS (kobs = 1.35–1.46 kGy−1), which might be ascribed to the major role of %OH in phenol degradation.

The above results demonstrated that the Gamma/PS system was highly effective to decompose ERY in aqueous solution with a faster ERY degradation rate and higher mineralization. Therefore, the effect of various operational parameters such as PS dosage and water matrices on ERY degradation upon Gamma/PS system was further studied. A series of tests with PS concentrations in a range of 0.2–4.0 mM was conducted to assess the ERY degradation rate and PS consumption rate following gamma irradiation (Fig. 5). As seen, when PS concentrations increased from 0.2 mM to 4.0 mM, kobs increased gradually from 2.5 to 8.9 kGy−1 and more than 99% of ERY removal was achieved within 2.0 kGy. The TOC abatement at 10 kGy increased from around 35% to 60% when PS concentration was increased from 0.2 mM to 2.0 mM, and then dropped slightly to 55% with 4.0 mM PS. With the increase in the PS concertation and absorbed doses, the reactive SO4%− and %OH formed increased, leading to the increase in ERY degradation rate. However, the raised radicals’ concentration increased the possibility of radicals’ recombination (as shown in Eqs. (14) and (15)). Moreover, PS could also react with SO4%− and %OH and behaves as scavengers beyond a certain level (Eqs. (16) and (17)). This could explain the slight drop in TOC reduction at 4.0 mM PS.

SO·4− + ·OH → HSO5−

k = 1.0 × 1010 L mol−1 s−1

(14)

SO·4− + SO·4− → S2 O82 −

k = 3.1 × 108 L mol−1 s−1

(15)

S2 O82 −

+

SO·4−

→

SO24−

+

S2 O·8−

S2 O82 − + ·OH → OH− + S2 O·8−

105 L mol−1 s−1

(16)

k < 1.0 × 106 L mol−1 s−1

(17)

k = 6.6 ×

Regarding to PS consumption rate, it initially increased rapidly and then gradually following gamma irradiation. The lower the PS concentration, the higher the PS consumption rate. The PS consumption rate within 2.0 kGy reached 96%, 88%, 64%, 50% and 31% with the PS concentration of 0.2, 0.5, 1.0, 2.0 and 4.0 mM, respectively. As the absorbed dose increased to 10 kGy, the PS consumption rate could 161

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SO4%− and %OH and present a great radicals’ scavenging for degrading the target pollutants [62,66]. Similar results were reported by other researchers. For example, Michael-Kordatou et al. found that the kobs of ERY degradation by UV/PS system was 0.55 min−1 in ultrapure water, and decreased dramatically to 0.03 min−1 in treated wastewater [36]. Amasha et al. documented that the degradation rate of ketoprofen was declined around 1.5 times in spring water, 6.7–8.3 times in seawater and 4.5–13.3 times in wastewater using activated PS by UV or heat [67]. The Gamma/PS system was considerably more efficient to improve the mineralization of ERY-containing waters. Only slight TOC abatement (1.2%–0.9%) was obtained by direct gamma irradiation, but the TOC reduction increased greatly to 18.7% in groundwater and 8.9% in treated wastewater, respectively by using Gamma/PS system. In deionized water, the TOC abatement at 10 kGy was increased from 25% using gamma irradiation to 47% in Gamma/PS system. It should be mentioned that methanol addition for improving ERY fast dissolution (50 μL/L with the TOC level of around 9.0 mg/L) showed little impact on ERY removal in both systems, but it affected TOC reduction in Gamma/PS system. It was observed that the TOC concentration of methanol solution did not change by gamma irradiation alone, but it reduced to around 5.8 mg/L in Gamma/PS system with the absorbed dose of 10 kGy. If the TOC reduction derived from methanol reduction was deducted, the TOC removal efficiency in Gamma/PS system reached around 52%, 12.9%, 3.4%, respectively in deionized water, groundwater and treated wastewater. The improved mineralization by Gamma/PS system was beneficial for the treatment of antibiotics containing real waters since the antibiotics were eliminated completely rather than transformed to other intermediates. As shown in Fig. 6, the pH values dropped following gamma irradiation and the decrease was remarkably by Gamma/PS treatment, indicating that more acid substances were generated. The pH reduction trend in groundwater and treated wastewater was not as sharp as that in deionized water, which was attributed to the good buffer capacity of the real waters owing to the existence of CO32− or HCO3− alkalinity. This is beneficial for their practical application because the treated effluent after Gamma/PS system could be discharged without pH adjustment. Since the ERY degradation rate eliminated significantly in the presence of peptone and glucose, the Gamma/PS system was assessed to improve its performance. As shown in Fig. 7, in the presence of glucose, the ERY degradation rate was accelerated remarkably in Gamma/PS system as kobs increased remarkably to 6.65 kGy−1 from 0.57 kGy−1 by γ ray irradiation alone. In the presence of peptone, the kobs values increased by 2 times (1.0 mM PS) and 3 times (2.0 mM PS) using Gamma/ PS system. The improvement on ERY decomposition in the presence of glucose by Gamma/PS might be attributed to the glucose activation of persulfate. Watts et al. [68] reported that glucose could activate persulfate at alkaline and neutral conditions to induce the generation of % OH and reductants + nucleophiles. The removal efficiency of nitrobenzene and hexachloroethane was increased remarkably in the glucose-activated persulfate system. The higher ERY degradation in Gamma/PS system in the presence of peptone might be explained by the higher quantum yield of radicals available and the lower reaction rate of SO4%− towards peptone. It was documented that amino acids and several proteins like histone and collagen were readily to react with %OH and acted as %OH scavengers [69]. Morimoto et al. [70] reported that the reaction rate of 1-ethylguanidine with SO4%− (1.1 × 108 L mol−1 s−1) was lower an order than that with %OH (1.1–2.9 × 109 L mol−1 s−1). Further research is needed to study the enhancement mechanism.

2-

Glucose 1mM + S2O8 1mM

1.0

2-

Peptone 180 mg/L + S2O8 1mM 2-

Peptone 180 mg/L + S2O8 1mM

C/C0

0.8 0.6 0.4 0.2 0.0 0

1

2 Dose (kGy)

3

4

B glucose kobs= 0.5735

2.5

2-

glucose+S2O8 1mM kobs= 6.6499 peptone kobs= 0.4041

-ln (C/C0)

2.0

2-

peptone+S2O8 1mM kobs= 0.7903 2-

peptone+S2O8 2mM kobs= 1.2422

1.5

1.0

0.5

0.0 0

1

2

3

4

Dose (kGy) Fig. 7. ERY degradation rate in the presence of glucose and peptone by Gamma/PS system (A) and comparison of rate constant to gamma irradiation alone (B) (C0 = 0.1 mM in deionized water).

reach almost 100% with 0.2 and 0.5 mM PS, more than 85% with 1.0 and 2.0 mM PS, and around 70% with 4.0 mM PS, respectively. In addition, the maximum RSE within 0.5 kGy decreased gradually from 59%, 25%, 15%, 10% to 9.5% with increase of PS dosage from 0.2 mM to 4.0 mM. The 15% RSE in Gamma/PS (1 mM) system for degrading ERY was comparable to 5.2% RSE in Fe0/PS (1 mM) system for degrading sulfamethoxazole [65], but lower than 33% RSE in thermal PS (1 mM) system at 60 °C for degrading ketoprofen [34] and 72% RSE in iron waste/PS (0.1 mM) system for treating ranitidine [38]. Compared to H2O2 use, PS showed much higher RSE since H2O2 efficiency was below 1% for non-specificity for the oxidant. Taking into account of the ERY degradation rate, the PS consumption rate and RSE, the PS dosage of 1.0–2.0 mM with PS/ERY ratio of 10–20 was recommended for the Gamma/PS system. Fig. 6 shows the enhancement of ERY degradation by Gamma/PS (1.0 mM) system in comparison to gamma irradiation alone in different water matrices. The Gamma/PS system was effective to improve ERY degradation and the enhancement extent followed this decreasing order: deionized water > groundwater > treated wastewater. The kobs increased by 6.5 times in deionized water, 5.0 times in groundwater and 1.4 times in treated wastewater, respectively in Gamma/PS system, compared to that using gamma irradiation alone. The groundwater contains high level of inorganic ions, such as HCO3−, NO3− and Cl−, which could quench the reactive radicals. In the case of the treated wastewater, it has a complex composition, including the inorganics ions and DOM such as soluble microbial products, which prone to react with

3.5. Antimicrobial activity The elimination of the antimicrobial activity of ERY against E. coli and S. aureus in the three kinds of waters using the two systems was 162

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Gamma alone Gamma/PS 1mM

E. coli

A 1.2

S. aureus

4 3

0.8

2

0.4

Diameter (cm)

1

0.0

0

B 1.2

4 3

0.8

2

0.4 1

C

0.0

0

1.2

4 3

0.8

2 0.4 1 0

0.0

0

2

4

6

8

10 0 2 Absorbed dose (kGy)

4

6

8

10

Fig. 8. Decrease of antimicrobial activity against S. aureus and E. coli in the three ERY containing waters as a function of absorbed doses by gamma irradiation and γ ray-activated/PS system (A: deionized water, B: Groundwater; C: treated wastewater, C0 = 0.1 mM, PS = 1.0 mM).

0.8

C/C0

using Gamma/PS system. The 14-membered lactone ring is major active position of ERY, while the eOCH3 and eOH groups in cladinose contribute to the antimicrobial activity. It appears that the intermediates formed in the real water system exhibit the antimicrobial activity and the Gamma/PS system was able to enhance the degradation and inactivation of the intermediates. Keen et al. [71] reported that the intermediates of ERY degradation in wastewater effluent by UV/H2O2 treatment still showed the antibacterial activity to B. subtilis and E. coli which was ascribed to complex secondary reaction between the substances in the effluent and the products of ERY degradation during gamma irradiation.

Gamma/t-BuOH Gamma/Methanol Gamma/PS/t-BuOH Gamma/PS/Methanol

1.0

0.6

0.4

0.2

3.6. Effects of radicals’ quenchers and intermediates of ERY degradation 0.0 0

2

4

6 Dose (kGy)

8

The effect of radicals’ quenchers was studied to determine the reactive species responsible for ERY degradation in both gamma ray and Gamma/PS system (Fig. 9). In the presence of the same radicals’ scavenger, the rate constant of ERY degradation decreased by 1.4–1.7 times in Gamma/PS system (kobs = 4.6–3.5 kGy−1) and by 6.2–8.3 time using gamma irradiation alone (kobs = 0.17–0.13 kGy−1), respectively. This suggests that the reactive radicals formed in Gamma/PS system were much higher than that in gamma-ray system. In addition, t-BuOH exhibited a higher inhibition on ERY degradation in gamma-ray system, while methanol displayed a higher inhibition in Gamma/PS system. tBuOH was considered to be the scavengers of %OH, since t-BuOH reacts with %OH nearly 1000 times faster than that with SO4%− (Eqs. (18) and (19)), whereas methanol could react readily with both %OH and SO4%− (Eqs. (20) and (21), the reaction rate with SO4%− is nearly 40-fold higher than that with %OH) [50]. This implies that %OH is the major reactive specie responsible for ERY degradation by gamma irradiation, while both %OH and SO4%− play a role by Gamma/PS treatment.

10

Fig. 9. Effects of different scavengers (500 mM t-BuOH and methanol) on ERY degradation by gamma irradiation and Gamma/PS system (C0 = 0.1 mM in deionized water).

shown in Fig. 8. The inhibition halo formed to S. aureus was higher than that to E. coli, indicating that ERY is more susceptible to S. aureus. Similar to the ERY degradation trend, the inhibition halo decreased with the increase in the absorbed dose and the elimination rate was faster by using Gamma/PS system in deionized water. A complete inactivity to E. coli was obtained at 1 kGy using Gamma/PS system and 6 kGy was required using γ ray alone. The antimicrobial activity to S. aureus was still observed with 10 kGy of gamma irradiation in groundwater and treated wastewater when ERY was totally removed, while it was totally lost by 163

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Gamma alone

10

-1

Formic acid (mg L )

-1

Acetic acid (mg L )

1.5

Gamma/PS1.0 mM

1.0

0.5

8 6 4 2 0

0.0 0

2

4 6 Dose (kGy)

8

10

0

2

4 6 Dose (kGy)

8

10

Fig. 10. Variation in formic acid and acetic acid formed during gamma irradiation and γ ray-activated/PS treatment (C0 = 0.1 mM, PS = 1.0 mM).

4. Conclusions

Similar results were observed by Michael-Kordatou et al. [36], they reported that the contribution of SO4%− and %OH to ERY degradation was around 63% and 37% in UV/ PS system.

t - BuOH + ·OH → intermediates

k = (3.8 − 7.6) ×

The present work showed that Gamma/PS system was efficient to improve the degradation and mineralization of the ERY-containing waters. With PS dosages 1 mM, the PS consumption rate reached more than 85% and the RSE for degrading ERY was around 15% in deionized water. A complete ERY removal was achieved within 6 kGy and TOC removal efficiency reached 25% in deionized water, only 1.2% and 0.9% in groundwater and treated wastewater, respectively by gamma irradiation alone at 10 kGy. In Gamma/PS system, the rate constant kobs of ERY degradation increased by 6.5–1.4 times and the TOC removal efficiency increased to 52%, 12.9% and 3.4% in three kinds of waters. The antimicrobial active intermediates against S. aureus were observed within 10 kGy of gamma irradiation in groundwater and treated wastewater, while they were deactivated completely in Gamma/PS system. The presence of organic substances such as peptone and glucose could inhibit ERY degradation more significantly than inorganic anions. The Gamma/PS treatment could increase kobs to 6.65 kGy−1 (for glucose) and 0.80 kGy−1 (for peptone), compared to 0.57 and 0.40 kGy−1 using gamma irradiation alone. A higher yield of formic acid and acetic acid in Gamma/PS system was observed. It was proposed that the 14membered ring of ERY was destroyed by gamma irradiation from LC–MS analysis.

1010 L mol−1 s−1 (18)

t - BuOH +

SO·4−

→ intermediates k = (4 − 9.1) ×

105 L mol−1 s−1 (19)

Methanol + ·OH → intermediates Methanol +

SO·4−

→ intermediates

k = 9.7 × k = 2.5 ×

108 L mol−1 s−1

107 L mol−1 s−1

(20) (21)

Formic acid and acetic acid were detected following gamma irradiation and their concentrations increased to 3.0 mg L−1 and 0.8 mg L−1 within 4.0 kGy and then decreased gradually in deionized water (Fig. 10). Oxalic acid and formaldehyde, the commonly detected mineralization intermediates, were not detected in this study. The higher quantum yield of formic acid and acetate acid in the Gamma/PS system is consistent with the higher ERY degradation rate. The concentrations of nitrate and nitrite detected during gamma irradiation were very low (less than 0.15 mg L−1), indicating that the nitrogen compounds mostly exist in the form of organic nitrogen. The ERY degradation products detected by LC–MS analysis during gamma irradiation were erythromycin C N-oxide with m/z 736, pseudoerythomycin A enol ether with m/z 716, erythromycin A hemiketal carboxylic acid with m/z 698, which were reported with a low biological activity [51]. In addition, the adsorption at around 278 nm that is the characteristics adsorption of unsaturated ketone [72] increased following gamma irradiation. The tentative ERY degradation pathway was proposed, suggesting that the14-membered ring and –OCH3 group in cladinose were destroyed by gamma irradiation, which is consistent with the evolution of antimicrobial activity. This study demonstrated that ionizing radiation is a promising technology in the treatment of ERY-containing water and wastewater, with the advantages of no or a few chemicals addition, no residual production, high penetration range and high efficiency. Gamma irradiation is commonly used in the lab-scale experiment, while electron beam (EB) is applied for commercial application owing to the safety without the use of radioisotopes and economics. The operational cost of EB/PS is mainly derived from the energy cost and PS expense. At the absorbed dose of 1 kGy and PS dosage 1 mM, the treatment cost was around $ 0.40–0.57 m−3 (the energy cost was around $ 0.13–0.17 and the cost of PS consumption was around $ 0.27–0.40, considering the electricity cost $ 0.13–0.17 Kw−1 h and PS price $ 1.0–1.5 kg−1 in China for industrial usage), which is competitive in the advanced wastewater processes. Amasha et al. reported that the UV/PS system is more economically efficient than thermal and Fe2+ activation PS systems for degrading ketoprofen [67].

Acknowledgement We thank the financial support provided by the National Natural Science Foundation of China (21777083; 51338005). References [1] V. Homem, L. Santos, Degradation and removal methods of antibiotics from aqueous matrices – a review, J. Environ. Manage. 92 (10) (2011) 2304–2347. [2] J.L. Wang, S.Z. Wang, Removal of pharmaceuticals and personal care products (PPCPs) from wastewater: a review, J. Environ. Manage. 182 (2016) 620–640. [3] Z. Wan, J.L. Wang, Degradation of sulfamethazine using Fe3O4-Mn3O4/reduced graphene oxide hybrid as Fenton-like catalyst, J. Hazard. Mater. 324 (2016) 653–664. [4] Y. Liu, Q. Fan, J.L. Wang, Zn-Fe-CNTs catalytic in situ generation of H2O2 for Fenton-like degradation of sulfamethoxazole, J. Hazard. Mater. 342 (2018) 166–176. [5] X.X. Zhang, T. Zhang, H.H. Fang, Antibiotic resistance genes in water environment, Appl. Microbiol. Biotechnol. 82 (3) (2009) 397–414. [6] A. Pruden, R. Pei, H. Storteboom, K.H. Carlson, Antibioticresistance genes as emerging contaminants: studies in Northern Colorado, Environ. Sci. Technol. 40 (23) (2006) 7445–7450. [7] M.L. Luprano, S.M. De, M.G. Del, I.C. Di, A. Lopez, C. Levantesi, Antibiotic resistance genes fate and removal by a technological treatment solution for water reuse in agriculture, Sci. Total Environ. 571 (2016) 809–818. [8] N. Czekalski, S. Imminger, E. Salhi, M. Veljkovic, K. Kleffel, D. Drissner, F. Hammes, H. Bürgmann, G.U. Von, Inactivation of antibiotic resistant bacteria and resistance genes by ozone: from laboratory experiments to full-scale wastewater treatment, Environ. Sci. Technol. 50 (21) (2016) 11862–11871.

164

Chemical Engineering Journal 361 (2019) 156–166

L. Chu et al.

[38] S. Naim, A. Ghauch, Ranitidine abatement in chemically activated persulfate systems: assessment of industrial iron waste for sustainable applications, Chem. Eng. J. 288 (2016) 276–288. [39] G. Ayoub, A. Ghauch, Assessment of bimetallic and trimetallic iron-based systems for persulfate activation: application to sulfamethoxazole degradation, Chem. Eng. J. 256 (6) (2014) 280–292. [40] Y. Zhou, X. Wang, C. Zhu, D.D. Dionysiou, G. Zhao, G. Fang, D. Zhou, New insight into the mechanism of peroxymonosulfate activation by sulfur-containing minerals: role of sulfur conversion in sulfate radical generation, Water Res. 142 (2018) 208–216. [41] S.Z. Wang, J.L. Wang, Activation of peroxymonosulfate by sludge-derived biochar for the degradation of triclosan in water and wastewater, Chem. Eng. J. 356 (2019) 350–358. [42] T.S. Alkhuraiji, S.O. Boukari, F.S. Alfadhl, Gamma irradiation-induced complete degradation and mineralization of phenol in aqueous solution: effects of reagent, J. Hazard. Mater. 328 (2017) 29–36. [43] Z.L. Zhang, Q. Yang, J.L. Wang, Degradation of trimethoprim by gamma irradiation in the presence of persulfate, Radiat. Phys. Chem. 127 (2016) 85–91. [44] J.J. Lopez Penalver, C.V. Gomez Pacheco, M. Sanchez Polo, J. Rivera, Utrilla, Degradation of tetracyclines in different water matrices by advanced oxidation/ reduction processes based on gamma radiation, J. Chem. Technol. Biotechnol. 88 (6) (2012) 1096–1108. [45] L.B. Chu, S.T. Zhuang, J.L. Wang, Degradation kinetics and mechanism of penicillin G in aqueous matrices by ionizing radiation, Radiat. Phys. Chem. 145 (2018) 34–38. [46] Y.K. Liu, J.L. Wang, Degradation of sulfamethazine by gamma irradiation in the presence of hydrogen peroxide, J. Hazard. Mater. 250 (2013) 99–105. [47] Z. Guo, F. Zhou, Y. Zhao, C. Zhang, F. Liu, C. Bao, M. Lin, Gamma irradiationinduced sulfadiazine degradation and its removal mechanisms, Chem. Eng. J. 191 (2012) 256–262. [48] M. Iqbal, J. Nisar, Cytotoxicity and mutagenicity evaluation of gamma radiation and hydrogen peroxide treated textile effluents using bioassays, J. Environ. Chem. Eng. 3 (3) (2015) 1912–1917. [49] M. Iqbal, I.A. Bhatti, Gamma radiation/H2O2 treatment of a nonylphenol ethoxylates: degradation, cytotoxicity, and mutagenicity evaluation, J. Hazard. Mater. 299 (2015) 351–360. [50] G.V. Buxton, C.L. Greenstock, W.P. Helman, A.B. Ross, Critical review of rate constants for reactions of hydrated electrons, hydrogen atoms and hydroxyl radicals (•OH/•O−) in aqueous solution, J. Phys. Chem. Ref. Data 17 (2) (1988) 513–886. [51] Y.H. Kim, T.M. Heinze, R. Beger, J.V. Pothuluri, C.E. Cerniglia, A kinetic study on the degradation of erythromycin A in aqueous solution, Int. J. Pharm. 271 (1-2) (2004) 63. [52] I.V. Gala, J.J.L. Penalver, M.S. Polo, J.R. Utrilla, Degradation of X-ray contrast media diatrizoate in different water matrices by gamma irradiation, J. Chem. Technol. Biotechnol. 88 (7) (2013) 1336–1343. [53] S.Z. Wang, J.L. Wang, Radiation-induced degradation of sulfamethoxazole in the presence of various inorganic anions, Chem. Eng. J. 351 (2018) 688–696. [54] M.M. Abdel daiem, J. Rivera-Utrilla, R. Ocampo-Perez, M. Sanchez-Polo, J.J. LopezPenalver, Treatment of water contaminated with diphenolic acid by gamma radiation in the presence of different compounds, Chem. Eng. J. 219 (2013) 371–379. [55] S.M. Aschmann, A. Janet, A. Roger, Kinetics and products of the reaction of OH radicals with 3-methoxy-3-methyl-1-butanol, Environ. Sci. Technol. 45 (16) (2011) 6896–6901. [56] Y. Liu, X. He, X. Duan, Y. Fu, D.D. Dionysiou, Photochemical degradation of oxytetracycline: Influence of pH and role of carbonate radical, Chem. Eng. J. 276 (2015) 113–121. [57] G. Zhang, X. He, M.N. Nadagouda, K.E. O'Shea, D.D. Dionysiou, The effect of basic pH and carbonate ion on the mechanism of photocatalytic destruction of cylindrospermopsin, Water Res. 73 (4) (2015) 353. [58] A. Ghauch, A.M. Tuqan, N. Kibbi, Naproxen abatement by thermally activated persulfate in aqueous systems, Chem. Eng. J. 279 (2015) 861–873. [59] F. Liu, S. Lai, H. Tong, P.S. Lakey, M. Shiraiwa, M.G. Weller, U. Pöschl, C.J. Kampf, Release of free amino acids upon oxidation of peptides and proteins by hydroxyl radicals, Anal. Bioanal. Chem. 409 (9) (2017) 2411–2420. [60] R. Yin, W. Guo, H. Wang, J. Du, X. Zhou, Q. Wu, H. Zheng, J. Chang, N. Ren, Selective degradation of sulfonamide antibiotics by peroxymonosulfate alone: direct oxidation and nonradical mechanisms, Chem. Eng. J. 334 (2017) 2539–2546. [61] T.S. Alkhuraiji, N.K.V. Leitner, Effect of oxidant addition on the elimination of 2naphthalenesulfonate in aqueous solutions by electron beam irradiation, Radiat. Phys. Chem. 126 (2016) 95–102. [62] M. Mahdi-Ahmed, S. Chiron, Ciprofloxacin oxidation by UV-C activated peroxymonosulfate in wastewater, J. Hazard. Mater. 265 (2014) 41–46. [63] X. He, S.P. Mezyk, I. Michael, D. Fatta-Kassinos, D.D. Dionysiou, Degradation kinetics and mechanism of β-lactam antibiotics by the activation of H2O2 and Na2S2O8 under UV-254 nm irradiation, J. Hazard. Mater. 279 (6) (2014) 375–383. [64] J. Criquet, N.K.V. Leitner, Degradation of acetic acid with sulfate radical generated by persulfate ions photolysis, Chemosphere 77 (2) (2009) 194–200. [65] A. Ghauch, G. Ayoub, S. Naim, Degradation of sulfamethoxazole by persulfate assisted micrometric Fe0 in aqueous solution, Chem. Eng. J. 228 (2013) 1168–1181. [66] M. Sanchez-Polo, J. Lopez-Penalver, G. Prados-Joya, M.A. Ferro-Garcia, J. RiveraUtrilla, Gamma irradiation of pharmaceutical compounds, nitroimidazoles, as a new alternative for water treatment, Water Res. 43 (16) (2009) 4028–4036. [67] M. Amasha, A. Baalbaki, A. Ghauch, A comparative study of the common persulfate activation techniques for the complete degradation of an NSAID: the case of ketoprofen, Chem. Eng. J. 350 (2018) 395–410. [68] R.J. Watts, M. Ahmad, A.K. Hohner, A.L. Teel, Persulfate activation by glucose for in situ chemical oxidation, Water Res. 133 (2018) 247–254.

[9] N. Li, G.P. Sheng, Y.Z. Lu, R.J. Zeng, H.Q. Yu, Removal of antibiotic resistance genes from wastewater treatment plant effluent by coagulation, Water Res. 111 (2017) 204–212. [10] S. Omura, Macrolide Antibiotics: Chemistry, Biology, and Practice, second ed., Academic Press, San Diego, 2003. [11] EU2015/495, Commission implementing decision establishing a watch list of substances for union-wide monitoring in the field of water policy pursuant to Directive 2008/105/EC of the European Parliament and of the Council. http://eur-lex. europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32015D0495&from=EN. [12] E. Szekeres, A. Baricz, C.M. Chiriac, A. Farkas, O. Opris, M.L. Soran, A.S. Andrei, K. Rudi, J.L. Balcázar, N. Dragos, Abundance of antibiotics, antibiotic resistance genes and bacterial community composition in wastewater effluents from different Romanian hospitals, Environ. Pollut. 225 (2017) 304–315. [13] S. Heß, F. Lüddeke, C. Gallert, Concentration of facultative pathogenic bacteria and antibiotic resistance genes during sewage treatment and in receiving rivers, Water Sci. Technol. 74 (8) (2016) 1753–1763. [14] D.W. Kolpin, E.T. Furlong, M.T. Meyer, E.M. Thurman, S.D. Zaugg, L.B. Barber, H.T. Buxton, Pharmaceuticals, hormones, and other organic wastewater contaminants in U.S. Streams, 1999–2000: a national reconnaissance, Environ. Sci. Technol. 36 (6) (2002) 1202–1211. [15] J.L. Wang, Z.Y. Bai, Fe-Based Catalysts for heterogeneous catalytic ozonation of emerging contaminants in water and wastewater, Chem. Eng. J. 312 (2017) 79–98. [16] M. Iqbal, J. Nisar, M. Adil, M. Abbas, M. Riaz, M.A. Tahir, M. Younus, M. Shahid, Mutagenicity and cytotoxicity evaluation of photo-catalytically treated petroleum refinery wastewater using an array of bioassays, Chemosphere 168 (2017) 590–598. [17] W.L. Wang, Q.Y. Wu, N. Huang, Z.B. Xu, M.Y. Lee, H.Y. Hu, Potential risks from UV/H2O2 oxidation and UV photocatalysis: a review of toxic, assimilable, and sensory-unpleasant transformation products, Water Res. 141 (2018) 109–125. [18] I. Akmehmet Balcıoğlu, M. Ötker, Treatment of pharmaceutical wastewater containing antibiotics by O3 and O3/H2O2 processes, Chemosphere 50 (1) (2003) 85–95. [19] J.L. Wang, L.J. Xu, Advanced oxidation processes for wastewater treatment: formation of hydroxyl radical and application, Crit. Rev. Environ. Sci. Technol. 42 (3) (2012) 251–325. [20] A. Ghauch, A.M. Tuqan, N. Kibbi, Ibuprofen removal by heated persulfate in aqueous solution: a kinetics study, Chem. Eng. J. 197 (14) (2012) 483–492. [21] A. Ghauch, G. Ayoub, S. Naim, Degradation of sulfamethoxazole by persulfate assisted micrometric Fe0 in aqueous solution, Chem. Eng. J. 228 (28) (2013) 1168–1181. [22] A. Ghauch, A. Baalbaki, M. Amasha, R.E. Asmar, O. Tantawi, Contribution of persulfate in UV-254 nm activated systems for complete degradation of chloramphenicol antibiotic in water, Chem. Eng. J. 317 (2017) 1012–1025. [23] J.L. Wang, J.Z. Wang, Application of radiation technology to sewage sludge processing: a review, J. Hazard. Mater. 143 (1–2) (2007) 2–7. [24] M.A. Rauf, S.S. Ashraf, Radiation induced degradation of dyes-an overview, J. Hazard. Mater. 166 (1) (2009) 6–16. [25] Y.-C.A. Lin, C.-F. Lin, J. Chiou, P.K.A. Hong, O3 and O3/H2O2 treatment of sulfonamide and macrolide antibiotics in wastewater, J. Hazard. Mater. 171 (1-3) (2009) 452. [26] N.P. Xekoukoulotakis, C. Drosou, C. Brebou, E. Chatzisymeon, E. Hapeshi, D. FattaKassinos, D. Mantzavinos, Kinetics of UV-A/TiO2 photocatalytic degradation and mineralization of the antibiotic sulfamethoxazole in aqueous matrices, Catal. Today 161 (1) (2011) 163–168. [27] L. Szabó, J. Szabó, E. Illés, A. Kovács, Á. Belák, C. Mohácsi-Farkas, E. Takács, L. Wojnárovits, Electron beam treatment for tackling the escalating problems of antibiotic resistance: eliminating the antimicrobial activity of wastewater matrices originating from erythromycin, Chem. Eng. J. 321 (2017) 314–324. [28] P. Devi, U. Das, A.K. Dalai, In-situ chemical oxidation: principle and applications of peroxide and persulfate treatments in wastewater systems, Sci. Total Environ. 571 (2016) 643–657. [29] M.M. Ahmed, S. Barbati, P. Doumenq, S. Chiron, Sulfate radical anion oxidation of diclofenac and sulfamethoxazole for water decontamination, Chem. Eng. J. 197 (14) (2012) 440–447. [30] H.V. Lutze, S. Bircher, I. Rapp, N. Kerlin, R. Bakkour, M. Geisler, C.V. Sonntag, T.C. Schmidt, Degradation of chlorotriazine pesticides by sulfate radicals and the influence of organic matter, Environ. Sci. Technol. 49 (3) (2015) 1673. [31] C. Jiang, Y. Ji, Y. Shi, J. Chen, T. Cai, Sulfate radical-based oxidation of fluoroquinolone antibiotics: kinetics, mechanisms and effects of natural water matrices, Water Res. 106 (2016) 507. [32] A. Ghauch, A.M. Tuqan, Oxidation of bisoprolol in heated persulfate/H2O systems: kinetics and products, Chem. Eng. J. 183 (8) (2012) 162–171. [33] J.A. Khan, X. He, H.M. Khan, N.S. Shah, D.D. Dionysiou, Oxidative degradation of atrazine in aqueous solution by UV/H2O2/Fe2+, UV/S2O82−/Fe2+ and UV/HSO5−/ Fe2+ processes: a comparative study, Chem. Eng. J. 218 (218) (2013) 376–383. [34] M. Amasha, A. Baalbaki, S. Al Hakim, R. El Asmar, A. Ghauch, Degradation of a toxic molecule o-toluidine in industrial effluents using UV254/PS System, J. Adv. Oxid. Technol. 21 (2018) (1). [35] A. Ghauch, A.M. Tuqan, N. Kibbi, S. Geryes, Methylene blue discoloration by heated persulfate in aqueous solution, Chem. Eng. J. 213 (12) (2012) 259–271. [36] I. Michael-Kordatou, M. Iacovou, Z. Frontistis, E. Hapeshi, D.D. Dionysiou, D. FattaKassinos, Erythromycin oxidation and ERY-resistant Escherichia coli inactivation in urban wastewater by sulfate radical-based oxidation process under UV-C irradiation, Water Res. 85 (2015) 346. [37] J.L. Wang, S.Z. Wang, Activation of persulfate (PS) and peroxymonosulfate (PMS) and application for the degradation of emerging contaminants, Chem. Eng. J. 334 (2017) 1502–1517.

165

Chemical Engineering Journal 361 (2019) 156–166

L. Chu et al.

[71] O.S. Keen, K.G. Linden, Degradation of antibiotic activity during UV/H2O2 advanced oxidation and photolysis in wastewater effluent, Environ. Sci. Technol. 47 (22) (2017) 13020–13030. [72] M.V.S. Sigal, P.F. Wiley, K. Gerzon, E.H. Flynn, U.C. Quarck, O. Weaver, Erythromycin VI degradation studies, J. Am. Chem. Soc. 78 (2) (1956) 388–395.

[69] I.Zs. -Nagy, R.A. Floyd, Hydroxyl free radical reactions with amino acids and proteins studied by electron spin resonance spectroscopy and spin-trapping, Biochim. Biophys. Acta 790 (1984) 238–250. [70] S. Morimoto, T. Ito, S. Fujita, S. Nishimoto, A pulse radiolysis study on the reactions of hydroxyl radical and sulfate radical anion with guanidine derivatives in aqueous solution, Chem. Phys. Lett. 461 (4) (2008) 300–304.

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