The occurrence and distribution of antibiotics in Lake Chaohu, China: Seasonal variation, potential source and risk assessment

The occurrence and distribution of antibiotics in Lake Chaohu, China: Seasonal variation, potential source and risk assessment

Chemosphere 122 (2015) 154–161 Contents lists available at ScienceDirect Chemosphere journal homepage: www.elsevier.com/locate/chemosphere The occu...

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Chemosphere 122 (2015) 154–161

Contents lists available at ScienceDirect

Chemosphere journal homepage: www.elsevier.com/locate/chemosphere

The occurrence and distribution of antibiotics in Lake Chaohu, China: Seasonal variation, potential source and risk assessment Jun Tang a, Taozhong Shi a, Xiangwei Wu a, Haiqun Cao a, Xuede Li a, Rimao Hua a,⇑, Feng Tang b, Yongde Yue b a b

School of Resource and Environment, Anhui Agricultural University, Hefei 230036, China International Center for Bamboo and Rattan, Beijing 100102, China

h i g h l i g h t s  The highest levels of antibiotics were detected in western inflowing rivers of Lake Chaohu.  Sewage treatment plants were important source of antibiotics input to river.  Seasonal variations and distribution of antibiotics were observed in surface water.  Algae and aquatic plants may be at risk of antibiotics in inflowing river and surface water.

a r t i c l e

i n f o

Article history: Received 6 July 2014 Received in revised form 3 November 2014 Accepted 12 November 2014 Available online 2 December 2014 Handling Editor: Klaus Kümmerer Keywords: Antibiotics Lake Chaohu Rivers STPs effluent Occurrence Risk assessment

a b s t r a c t The distribution and seasonal variation of fifteen antibiotics belonging to three classes (sulfonamides, fluoroquinolones and tetracyclines) were investigated in Lake Chaohu, China. The concentrations of the selected antibiotics in the surface water, eight major inflowing rivers and sewage treatment plant (STP) samples were analyzed by UPLC–MS/MS. The results indicated that sulfamethoxazole and ofloxacin were the predominant antibiotics, with maximum concentrations of 95.6 and 383.4 ng L1, respectively, in the river samples. In Lake Chaohu, the western inflowing rivers (the Nanfei and Shiwuli Rivers) were the primary import routes for the antibiotics, and the domestic effluent from four STPs were considered the primary source of the antibiotics. The level of antibiotics in Lake Chaohu clearly varied with seasonal changes, and the highest detectable frequencies and mean concentrations were found during the winter. The quality of water downstream of Lake Chaohu was influenced by the lake, and the results of risk assessment of the antibiotics on aquatic organisms suggested that sulfamethoxazole, ofloxacin, ciprofloxacin and enrofloxacin in the surface water of Lake Chaohu and inflowing rivers might pose a high risk to algae and plants. Ó 2014 Elsevier Ltd. All rights reserved.

1. Introduction Antibiotics have been used for several decades to prevent and treat diseases in humans and animals and as growth promoters in the animal breeding industry. The global annual production has been estimated as 100 000–200 000 tons (Kümmerer, 2009b), and more than 25 000 tons are used each year in China (Xu et al., 2007). However, the antibiotics were poorly absorbed by the tested organisms (Sarmah et al., 2006), and most of them are excreted with feces or urine in the form of parent compounds or their metabolites (Heuer et al., 2008). Due to their water solubility and

⇑ Corresponding author. Tel.: +86 551 65786320; fax: +86 551 65786296. E-mail address: [email protected] (R. Hua). http://dx.doi.org/10.1016/j.chemosphere.2014.11.032 0045-6535/Ó 2014 Elsevier Ltd. All rights reserved.

degradation resistant characteristics, antibiotics are considered a class of ubiquitous pollutants in aquatic environments (Nödler et al., 2012). Previous studies have indicated that antibiotics were partly eliminated in sewage treatment plants (STPs) and may have reached the aquatic environment with effluents (Brown et al., 2006; Xu et al., 2007; Choi et al., 2008). An additional path for antibiotics into the aquatic environment is their application to livestock followed by fertilization with manure (Zarfl et al., 2009). The direct discharge of wastewater from livestock also leads to contamination by antibiotics in aquatic environments. Antibiotics, including sulfonamides, fluoroquinolones and tetracyclines are widely used for medicine or feed additive, leading to high detectable frequencies and concentrations in some important areas in China, such as Huangpu River (Jiang et al., 2011), Haihe River

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(Gao et al., 2012), Pearl River (Xu et al., 2013), Yellow River (Zhou et al., 2011) and Bohai Bay (Zou et al., 2011). The excess use of antibiotics has increased the residual levels in aquatic environments and has led to the long-term development of antibiotic resistant bacteria and antibiotic resistant genes (ARGs) (Martinez, 2008). The ARGs have been recognized as one of the primary environmental problems facing society in the 21st century (Dantas et al., 2008). The bacterial strains isolated from Jiulong River estuary were resistance or multi-resistance to these antibiotics (Zheng et al., 2011), and tetracycline ARGs found in Pearl River (Tao et al., 2010) will inspire a new wave of research on antibiotic resistance in China. Lake Chaohu is one of the five largest fresh water lakes in China. This lake is situated on flood plains between the Yangtze River and the Huaihe River in the central Anhui Province of eastern China (Wang et al., 2013). Lake Chaohu is a typical shallow lake with a mean depth of 3 m and a surface area of 780 km2. The geological location of the lake is between 31°250 2800 and 31°430 2800 latitude north and between 117°160 5400 and 117°510 4600 longitude east(Xu et al., 2005). More than 80% of the total inflow is supplied by eight major inflowing rivers, including the Nanfei River (NFH), the Shiwuli River (SWLH), the Pai River (PH), the Fengle River (FLH), the Baishishan River (BSSH), the Zhao River (ZH), the Zhegao River (ZGH) and the Shuangqiao River (SQH).The Yuxi River (YXH) is the only outflowing river as well as an influent of Yangtze River. The riverine runoff has been considered as an important route for the transport of contaminants to Lake Chaohu (Wang et al., 2013). More than 9.1 million people live in the Chaohu Lake Basin, and it is a rapidly developing economic region, housing a group of important industries, such as car manufacturers, pharmaceutical factories, among others. Due to the increasing anthropogenic activities of the lake’s watershed over recent decades, the lake has suffered from serious pollution and eutrophication problems (Zan et al., 2010). Lake Chaohu is listed in ‘‘Water pollution prevention and control on the three rivers and three lakes’’ by the state environmental protection administration of China, and more attention should be taken to preserve the water quality. The output of livestock waste was estimated over 25 million tons per year, and about 30% of it was run off directly into Lake Chaohu (Qian, 2014). On the other hand, discharges from sewage treatment plants (STPs) in Hefei city were confirmed to be the major source responsible for the pollution of Chaohu Lake (Wang et al., 2012). Given that antibiotics are widely used in not only human medicine but also in aquaculture and animal husbandry in the lake’s watershed, it is important to evaluate the current status and environmental risks of antibiotic pollution on Lake Chaohu. This study focused on the occurrence, seasonal variation and environmental risk of the selected antibiotics (including five sulfonamides, six fluoroquinolones and four tetracyclines) in inflowing rivers and surface water of Lake Chaohu by conducting four sampling events during different seasons. Meanwhile, the occurrence and remove efficiency of 15 antibiotics at four STPs in Hefei were investigated. To our knowledge, this is the first systematic regional study on the antibiotics pollution in Lake Chaohu, and the resulting data will be useful to enrich the research of trace organic pollution in Lake Chaohu and to develop future pollution control measures. 2. Materials and methods

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MO, USA) and tetracycline (TC), oxytetracycline (OTC), chlortetracycline (CTC), doxycycline (DOC), were obtained from Bio Basic Inc., Canada. All of the standards were dissolved in methanol and stored at 4 °C in dark. Methanol (MeOH) and acetonitrile (ACN) were Optima grade and were obtained from Tedia Co. Inc., Fairfield, USA. Sulfuric acid (SA, 98% pure), formic acid (FA, 99% pure) and disodium ethylenediaminetetraacetate (Na2EDTA) were purchased from Sinopharm Chemical Reagent Co., Ltd., China. Ultrapure water (MQ) was produced by a Milli-Q water purification system (Millipore, Billerica, MA, USA). 2.2. Study sites and sampling The detailed locality of the sampling sites is displayed in Fig. 1. To evaluate the primary source of the antibiotics in Lake Chaohu, waters from eight major inflowing rivers of Lake Chaohu (R1 to R8, 2 km upstream of the estuaries) were obtained in March 2012. In addition, water samples from 8 estuaries (S1–S8), three lakeside towns (S9–S11), the center of the west side of the lake (S12) and the east side of the lake (S13) were collected in March 2012, July 2012, September 2012 and January 2013, respectively, to observe the seasonal variation of the antibiotics in Lake Chaohu. Water samples from Yuxi River (R9) were collected in the meanwhile to evaluate the influence of water quality downstream of Lake Chaohu. All of the water samples were collected 0.5 m below the surface using a water grab sampler and stored in glass bottles (2500 mL). The 24 h composite influent and effluent samples from four main sewage treatment plants (STP1 to STP4, the final effluents input into Nanfei River) were collected in January 2013 to evaluate the potential source of the antibiotics in Lake Chaohu. All of the samples were maintained at 4 °C and were pretreated within one week. 2.3. Sample preparation and extraction The methods for analyzing water samples described in previous studies (Gros et al., 2006; Conley et al., 2008) were used in this study. Briefly, triplicates of all of the water samples were extracted with solid-phase extraction (SPE) method by using Oasis HLB cartridges (500 mg, 6 mL, Waters) and were then eluted with 6.0 mL MeOH. After drying under a gentle nitrogen stream to approximately 20 lL, the analytes were reconstituted using 2 mL of the sample diluents (15:85 MeOH: MQ) and transferred into auto sampling vials for analysis. 2.4. Antibiotics analysis The antibiotics were analyzed by a Waters Acquity™ ultra performance liquid chromatography–tandem mass spectrometry (UPLC–MS/MS) system. Liquid Chromatography was performed on a Waters UPLC (Waters, USA) equipped with an autosampler. An Acquity™ UPLC C18 column (2.1  100 mm, 1.7 lm; Waters, USA) was employed and maintained at 40 °C by a thermostated column oven. The conditions used for the LC system are shown in the Supplementary Material. Mass spectrometry was performed using a Waters TQ-S detector operated with an ESI interface in the positive electrospray ionization mode. The optimal conditions for monitoring of the analytes are summarized in Table S1 (Supplementary material).

2.1. Chemicals and standards 2.5. Quality control and quality assurance Fifteen antibiotic standards, including sulfadiazine (SDZ), sulfamethoxazole (SMX), sulfamethazine (SMZ), sulfachloropyridazine (SCP), sulfadimethoxine (SDM), norfloxacin (NOR), ofloxacin (OFL), difloxacin (DIF), lomefloxacin (LOM), ciprofloxacin (CIP) and enrofloxacin (ENR) were products of Sigma–Aldrich (St. Louis,

An external standard method was used to quantify the concentrations of the selected antibiotics. In brief, the solvent blank, procedural blank and the mixed standard solutions were run at regular intervals to monitor system performance and potential

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Fig. 1. Maps of the sampling sites in Lake Chaohu, China.

contamination. The analytes were identified based on the corresponding parent ion and the product ions along with the retention time and were quantified based on the calibration standard curves constructed from the SPE and the analysis of the spiked water samples. The calibration curve was prepared within a wide range (0.1–1000 lg L1) of concentrations to reveal strong linearity (r2 > 0.99).The limit of detection (LOD) and the limit of quantification (LOQ) for each antibiotic was defined as the concentrations corresponding signal-to-noise (S/N) ratio of 3 and 10, respectively. The LOD and LOQ of each antibiotic in water were 0.17–1.93 ng L1 and 0.57–6.42 ng L1, respectively. The mean recoveries of 15 antibiotics (25, 160 and 400 ng L1) spiked to surface water (n = 3) were 58–103%, 63–122% and 82–107%, respectively. The analytical method validation for the water samples is described in Table S2 (Supplementary material). 2.6. Risk characterization Risk quotient (RQs) to aquatic organisms are calculated following the formula:

RQ ¼ MEC=PNEC

ð1Þ

where MEC is the maximum measured environmental concentration, and PNEC is the predicted no effect concentration in water. The PNEC in water was calculated following the formula:

PNEC ¼ ðLC50 or EC50 Þ=AF

ð2Þ

where LC50 or EC50 is the lowest median effective concentration value obtained from the available literature, and AF is an appropriate standard assessment factor (1000) (Park and Choi, 2008). The RQ values were classified into the following three risk levels: low (values between 0.01 and 0.1), medium (values between 0.1 and 1) and high (values above 1) (de Souza et al., 2009).

3. Results and discussion 3.1. Distribution of the antibiotics in the inflowing rivers of Lake Chaohu The antibiotics were widely detected in the water samples from the inflowing rivers of Lake Chaohu at the ng L1 level. As shown in Fig. 2, three sulfonamides (SDZ, SMX, and SMZ) and three fluoroquinolones (ENR, OFL and DIF) were the most frequently detected compounds in 100% of the samples. NOR, CIP and LOM showed the second highest detection frequency of 88% followed by SCP, with a detection frequency of 75%. OTC was found in five rivers along with SDM and TC (with a detection frequency of 50%). Among all of the selected antibiotics, SMX and OFL were the predominant antibiotics, with concentrations ranging from 2.5 to 95.6 ng L1 and 2.2 to 383.4 ng L1, respectively, in all of the river samples. Eight major inflowing rivers showed different levels of pollution (Fig. 2(A)), and the order of antibiotic contamination levels in the inflowing rivers was as follows: Nanfei River > Shiwuli River > Zhao River > Shuangqiao River > Baishishan River > Pai River > Zhegao River > Fengle River. The Nanfei River flows through Hefei City and a large rural area, and it contains an important tributary of the Dianpu River, which flows through Feidong County. The Shiwuli River originates to the southwest of Hefei City and flows through a rural area before reaching Lake Chaohu. The substantial use of SAs and FQs in Hefei City and the rural area explain the findings that the two rivers flowing through urban areas were significantly more contaminated by antibiotics than the other rivers. In addition, agriculture may serve as a source of antibiotic residues to the aquatic environment (Arikan et al., 2008). The Zhao, Shuangqiao, Baishishan and Pai Rivers flow via rural areas in which animal husbandry and aquaculture were developed. The amount of antibiotics ranged from 96.1 to 215.2 ng L1, showing a significant contamination level in the rural area. The Nanfei and Shiwuli Rivers, which contributed 66% of the total amount of the

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Fig. 2. (A) Concentrations (mean) of antibiotics in inflowing rivers (ng L1). (B) Box-and-whisker plots of antibiotics in inflowing rivers. The horizontal black line in the box represents the median value and the lower and upper edges of the box mark the 25th and 75th percentiles. The whiskers extending from the box show the highest and lowest values. ‘‘d’’ represents extreme values, which were beyond the triplication of the difference between 25th and 75th percentiles. Numbers in parentheses are the number of detectable frequencies of each antibiotics.

antibiotics in all of the eight rivers, should be the primary import route of the antibiotics to Lake Chaohu. The reasons of different distribution of antibiotics in inflowing rivers which flow through rural area could be total amount of antibiotics and hydraulic condition of rivers. Data for discharge of antibiotics was difficult to estimate in condition of lack of current amount of usage in Basin of every river. However, pollutants, such as polybrominated diphenyl ethers (PBDEs) in inflowing rivers of Lake Chaohu were significantly correlated with the concentration of TN (total nitrogen) (Wang et al., 2013), and can be rough estimated by the concentration of TN. The annual discharges amount of TN in Fengle River, Zhegao River and Shuangqiao River were 1176, 316 and 136t, respectively (Wang et al., 2011). In addition, total water discharge amount (108, m3) of the three rivers were 10.464, 0.612 and 0.160, respectively (Wang et al., 2014). Thus, the concentrations of TN in the three rivers were calculated as 1.12, 5.16 and 8.5 mg L1, respectively. The pollution loads of the three rivers was: Shuangqiao River > Zhegao River > Fengle River. Though this estimate is not very accurate, it can reflect the status of antibiotics in inflowing rivers.

Fig. 3. Levels of selected antibiotics in the influent and effluent of four STPs in Hefei City (ng L1). Black bars indicate levels in the influent, and gray bars indicate those detected in the effluent samples. Error bars show maximum levels detected.

3.2. Occurrence of the antibiotics at the four STPs Eight antibiotics in this study were detected in all of the influent and effluent samples from the four STPs, including four sulfonamides (SDZ, SMX, SMZ and SCP), four fluoroquinolones (NOR, CIP, LOM and OFL) and one tetracycline (OTC). As shown in Fig. 3, SMX, NOR and OFL were detected at the highest levels in the influents and effluents of the STPs. The mean concentrations of the predominant antibiotics (SMX, NOR and OFL) in the influent samples were 582.3, 271.2 and 398.7 ng L1, respectively, whereas concentrations of 403.7, 121.5 and 200 ng L1 were found in the effluent samples, respectively. The results in the present study were comparable to the OFL contents in the influent of the STPs in Albuquerque (470 ng L1) and Hagerman (400 ng L1) in the USA (Brown et al., 2006) and were approximately two times higher than the

OFL contents (213 ng L1) and the NOR contents (155 ng L1) in five STPs in Sweden (Lindberg et al., 2005). Compared with SMX, lower levels of the other three sulfonamides (SDZ, SMZ and SCP) were detected in the influent and effluent samples. Typical veterinary antibiotic tetracyclines were found in the STP samples in Wisconsin (Karthikeyan and Meyer, 2006) and in Canadian cities (Miao et al., 2004). In the present study, tetracycline was detected at two sewage treatment plants, with concentrations ranging from 11.9 to 15.9 ng L1 in the influent and from below the LOQ to 12.0 ng L1 in the effluent. DOC and OTC were only found at one plant, with concentrations of 5.1 and 3.2 ng L1, respectively, in the influent and 5.3 ng L1 in the effluent. In contrast, the OTC contents ranged from 12.4 to 81.0 ng L1, with a 100% detection frequency in the influent and from 5.1 to 22.3 ng L1 with a 100%

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detection frequency in the effluent. The higher detection frequency of OTC was most likely caused by its wide used as a growth promoter in the livestock breeding industry and the significant amount of annual use in China. The occurrence of antibiotics in the effluent of the STPs was similar to that in the Nanfei and Shiwuli Rivers, indicating that the domestic effluents in Hefei City are a primary source of antibiotics in the inflowing rivers of Lake Chaohu. STPs play an important role in the life cycle of antibiotics in modern society, and their partial elimination may pollute the ambient environment (Xu et al., 2007). A low SMX removal efficiency rate at the STPs has been documented in Korea (Choi et al., 2008), and a rate of only 20% has been documented in New Mexico, USA (Brown et al., 2006). In the present study, the removal efficiency rate for SMX (30.7%) was also lower compared with NOR (55.2%) and OFL (49.8%). The differences in the chemical properties of these compounds might contribute to the variability. Fluoroquinolones, such as ofloxacin and NOR, are readily sorbed by sewage sludge (Golet et al., 2002), which may explain their higher removal efficiency rates. Sulfonamides, such as SMX, have a high potential to resist degradation and are sufficiently hydrophilic to exist in an aquatic environment (Jiang et al., 2011), which may result in a low removal efficiency. Because SMX was the dominant pollutant in the influent and effluent at the four STPs in Hefei City, improvement of the removal efficiency rate for this compound is required.

September (Wang et al., 2013); the antibiotic contents may decrease because of the lake water dilution. In addition, biodegradation and photo-degradation of the antibiotics might be more significant during the summer than during the winter (Karthikeyan and Meyer, 2006; Guerard et al., 2009). However, during other seasons, the antibiotics showed significantly higher levels; typically, during the winter, thirteen antibiotics (87% of the 15 analytes) were detected in more than half of the samples, with median concentrations up to 41.8 ng L1 for all of the analytes. Nine antibiotics (60% of the 15 analytes) during the spring and autumn were detected in more than half of the samples, with median concentrations up to 8.8 ng L1 and 29.4 ng L1, respectively. As described above, SMX was frequently found in the inflowing rivers. In Lake Chaohu, SMX showed the same occurrence during the different seasons, and the detection frequencies ranged from 85% to 100%, with median concentrations from 6.1 to 41.8 ng L1 in every sampling event. SMX was the dominant antibiotic pollutant in Lake Chaohu and in the interrelated water body followed by OFL, with detection frequency rates from 69% to 100%. In contrast, NOR and CIP showed a different result in Lake Chaohu, with low levels (below the limits of quantification) during the summer and autumn compared with the spring and winter. Total amount of antibiotics in S7, S8 and S9, which located in eastern side of Lake Chaohu were 10.7–67.5 ng L1, 17.3–75.5 ng L1 and 9.3–64.5 ng L1, respectively. SMX was found primary pollution with maximum concentration 41.8 ng L1 (S7 in January). The antibiotics in S7, S8 and S9 mainly original from the discharge of waste water or agricultural activities, and indicated that water treatment facility is wanted in towns around Lake Chaohu. Moreover, S7 is close to the intake of waterworks that supply drinking water for Chaohu City. The concentration of the selected antibiotics at S7 ranged from 10.7 to 67.5 ng L1 in four sampling events. The data may draw more attention to these emerging trace organic pollutants in the drinking water source in Chaohu city. Generally, the concentrations of SDZ and SMX were relatively high among all the sulfonamides, and their maximum concentrations were higher than those in Huangpu River (China) (Jiang et al., 2011) and Pearl River Estuary (China) (Liang et al., 2013). As shown in Table S3 (Supplemental material), fluoroquinolones, such as OFL, ENR and DIF, in Lake Chaohu were higer than those in Huangpu River (China) (Jiang et al., 2011), Yangtze River (China)

3.3. Seasonal variation of the antibiotics The antibiotic contents of Lake Chaohu clearly varied with seasonal changes in the present study. All of the selected antibiotics were detected during the spring (March in 2012) and the winter (January in 2013), whereas certain antibiotics were not found during the summer (July in 2012) and autumn (September in 2012). The results are listed in Table 1 and shown in Fig. S1 (Supplementary material). Four sulfonamides (SDZ, SMX, SMZ and SDM), five fluoroquinolones (NOR, CIP, LOM, ENR and OFL) and tetracycline were detected during every sampling event. During the summer, only three antibiotics (20% of the 15 analytes) were detected in more than half of the samples, with median concentrations up to 6.1 ng L1. This result could be partly explained by the annual flood season of the Lake Chaohu Basin, which begins in June and ends in

Table 1 Concentrations of the antibiotics in the water samples collected from Lake Chaohu during different seasons (ng L1). Analytes

SDZ SMX SMZ SCP SDM NOR CIP LOM ENR OFL DIF DOC TC OTC CTC

March, 2012

July, 2012

September, 2012

January, 2013

Frea

Minb

Maxc

Medd

Meane

Fre

Min

Max

Med

Mean

Fre

Min

Max

Med

Mean

Fre

Min

Max

Med

Mean

85 92 85 54 38 85 38 77 62 100 54 15 15 31 8

n.d. n.d. 0.7 n.d. n.d. n.d. n.d. n.d. n.d. 1.2 n.d. n.d. n.d. n.d. n.d.

45.6 137.9 4.7 4.6 8.8 34.8 13.6 2.6 82.7 182.7 4.4 42.3 9.8 4.9 2.6

1.8 8.8 1.0 blq. n.d. blq. n.d. 1.1 2.7 2.0 blq. n.d. n.d. n.d. n.d.

4.9 17.8 1.4 0.6 1.1 6.6 2.4 1.0 8.2 20.0 0.6 3.3 0.8 1.0 0.2

23 85 23 0 15 15 23 15 62 77 0 0 23 0 0

n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d.

1.3 11.7 0.8 n.d. blq. blq. blq. 1.1 3.3 10.5 n.d. n.d. 17.8 n.d. n.d.

n.d. 6.1 n.d. n.d. n.d. n.d. n.d. n.d. blq. 1.4 n.d. n.d. n.d. n.d. n.d.

0.1 5.8 0.1 0 0 0 0 0.1 1.2 2.4 0 0 2.7 0 0

100 100 100 85 62 31 31 92 85 69 38 54 38 15 15

blq. 4.9 0.7 n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d.

6.2 79.6 5.5 3.0 1.1 blq. blq. 5.5 10.8 27.3 5.8 5.6 7.2 blq. blq.

2.0 29.4 blq. blq. blq. n.d. n.d. blq. 7.6 18.0 n.d. blq. n.d. n.d. n.d.

2.0 29.5 3.0 0.8 0.1 0 0 1.2 5.1 13.4 0.4 0.8 1.6 0 0

85 92 92 85 38 54 100 92 85 77 69 77 77 62 38

n.d. n.d. n.d. n.d. n.d. n.d. blq. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d.

8.4 171.6 9.9 3.7 3.7 70.2 23.2 1.2 4.7 50.6 10.4 5.7 7.5 2.5 4.0

3.3 41.8 4.0 1.5 n.d. blq. 9.6 blq 2.1 blq blq blq blq blq n.d.

3.2 56.1 4.5 1.3 1.0 16.6 9.0 0.2 1.5 4.4 1.3 1.2 1.6 0.9 1.3

n.d.: below the limit of detection. blq.: below the limit of quantification. a Frequency of concentrations above the limit of detection (%). b Minimum. c Maximum. d Median. e Values below the limit of detection and below the limit of quantification were considered 0 to calculate the mean concentration.

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(Yan et al., 2013), Haihe River (China) (Gao et al., 2012), Baiyangdian Lake (China) (Li et al., 2012) and Seine River(France)(Tamtam et al., 2008). The maximum concentrations of tetracyclines in Lake Chaohu and inflowing rivers were much lower than those in Huangpu River (China) (Jiang et al., 2011), but higher than those in Yangtze River (China) (except OTC) (Yan et al., 2013). However, sulfonamides and tetracyclines in this study was lower than those in Seine River (France) (Tamtam et al., 2008), 139 streams (America) (Kolpin et al., 2002) and Urban water (Australia) (Watkinson et al., 2009). The results reveals that, Lake Chaohu is an exceptionally antibiotics polluted area in China, and much more measures should be taken to eliminate the pollution in the future. Concentrations of antibiotics in Yuxi River varioused significantly with the seasons changing. As shown in Fig. 4, the total amount of antibiotics in Yuxi River were 47.7 ng L1 (in January), 7.6 ng L1 (in March), 20.1 ng L1 (in July) and 48.9 ng L1 (in September), respectively. Tetracyclines (DOC, TC, OTC and CTC) were not detected, while SDM, NOR and CIP were below limit of quantification in every sampling time. SMX was found to be the primary pollutant (2.55–34.9 ng L1) in four seasons. The occurrences of antibiotics in Yuxi River were similar to those in sites S7 and S8 in every sampling time, and informed that the water quality downstream of the lake was influenced by the lake. As an influent of Yangtze River, Yuxi River was reported contribute some amount of PBDEs in Yangtze River (Wang et al., 2013). Therefore, Yuxi River might be a source of antibiotics in Yangtze River, and the contribution of Yuxi River should be defined in future. 3.4. Spatial distribution of the antibiotics Among all of the sampling sites, S1 to S4, which were located within an urban area on the west side of the lake, showed an overall trend of higher contamination compared with the S5 to S11 sampling sites, which were located in suburban areas. The highest total concentration of the selected antibiotics for all of the sampling sites during the different seasons was detected at S4 during the spring (353.6 ng L1) and autumn (123.3 ng L1), S2 during the summer (31.3 ng L1) and S1 during the winter (207.5 ng L1) (Fig. S1 (Supplementary material)). For the sulfonamides and fluoroquinolones, the highest concentrations were found at S1 for SMX (171.6 ng L1) during the winter and at S4 for OFL (182.7 ng L1) during the spring. These results may be caused by the substantial use of OFL and SMX in the urban area. Tetracyclines, due to their strong absorption to sediments, have seldom been reported in natural water (Mette and Niels, 2000; Sarmah et al., 2006). However, in China, tetracyclines have been found with high detection frequencies in the Huangpu River (Jiang et al., 2011). In the present

Fig. 4. Concentrations (mean) of selected antibiotics in the Yuxi River (ng L1).

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study, tetracyclines were also found at different sampling sites, and the maximum concentration was detected at S2 for DOC (42.3 ng L1) during the spring. This result may be explained by the veterinary use of tetracyclines, such as DOC and TC, in livestock breeding industries in the suburban area of the Shiwuli River basin. Interestingly, the total concentration of the antibiotics at S4 was significantly higher than that in the water of the Pai River at the same sampling time during the spring. Zou et al. (2011) has reported the same phenomenon in the Bohai Bay and has suggested that point sources, such as drain outlets, were an important pollution source for antibiotics. In the present study, several drain outlets were found approximately two kilometers from sampling sites R3 to S4 (estuary of the Pai River) in both sides of the Pai River, and effluents from the pond and village area were discharged into the estuary without any purification treatment. Therefore, the point source of the antibiotics also exists in Lake Chaohu, and it should be considered for future antibiotic pollution control in the rural village. In addition, note that the levels of antibiotics pollution in the center of the west side of the lake (site 12) were higher than in the center of the east side of the lake (site 13) during every sampling event, and the total concentrations of the antibiotics at S12 were more than eleven and five times higher than those at S13 during the spring and winter, respectively. The same situation was also reported by eutrophication (Yu et al., 2011), polychlorinated biphenyls (Wang et al., 2014), and organochlorine pesticides (Liu et al., 2013) and tetrabromobisphenol A (Yang et al., 2012) pollution in the western part of Lake Chaohu compared with the eastern part of the lake. Therefore, the western part of the lake was more seriously polluted by the antibiotics, and the western part of Lake Chaohu, including the estuary of the Nanfei River, should be given special attention. 3.5. Environmental risk assessment The risk quotient (RQs) of antibiotics in the surface water for the organisms in this study are shown in Table 2. Although the selected antibiotics in Lake Chaohu and the major inflowing rivers were detected at low levels, the RQ values of SMX, CIP, ENR and OFL were 5.72, 1.36, 1.68 and 8.70 for algae, respectively, indicating that these antibiotics might present a significant environmental risk to the algae in Lake Chaohu. In addition, the RQ values of SMX and OFL were 2.12 and 1.45, respectively, suggesting their high ecological risk to aquatic plants. The antibiotics in inflowing rivers showed a clear ecological risk to the aquatic organisms, and the RQ values of SMX and OFL were 3.19 and 18.26 for algae, respectively, and 1.18 and 3.04 for plants, respectively. In this study, invertebrates and fish were not likely to be at high risk because their RQ values are significantly less than 1. In previous reports (Kümmerer, 2009a; Li et al., 2012), invertebrates and fish were certified to be less affected by exposure to antibiotics compared with algae. However, antibiotics residue in aquatic environment may impose selective stress on the microbe communities and promote the antibiotic resistance of bacteria (Kümmerer, 2009a,b). Up to 97.1% of 35 bacterial strains isolated from Jiulong River Estuary exhibited resistance or multi-resistance to commonly detected antibiotics, such as sulfonamides in China (Zheng et al., 2011). Meanwhile, antibiotic resistance was found in Pearl River, and tetracycline resistance genes were confirmed to transfer between different species of bacteria (Tao et al., 2010). The presence of antibiotic resistant genes (ARGs) will be a potential threat to human health and the risk of antibiotic resistance will be one of the serious environmental problems in future. Due to the development of the population and urbanization in Hefei City (the capital of the Anhui Province), more antibiotics will be discharged into Lake Chaohu by STP effluents and riverine runoff. Therefore, more

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J. Tang et al. / Chemosphere 122 (2015) 154–161

Table 2 The risk quotient (RQs) for the aquatic organisms as calculated from the measured environmental concentrations (MECs) and the predicted environmental concentrations (PNECs). Analytes

Taxonomic group

L(E)C50 (mg L1)

PNEC (ng L1)

Maximum MEC (ng L1)

Maximum RQ (MEC/PNEC)

Lake

Lake

Rivers

0.0205 0.6514 0.0002

0.0014 0.0457 0.00001

Bialk-Bielinska et al. (2011) Bialk-Bielinska et al. (2011) Wollenberger et al. (2000)

Rivers

References

SDZ

Algae Plant Invertebrate

2.22(24 h) 0.07(72 h) 221(48 h)

2220 70 221 000

45.6

3.2

SMX

Algae Plant Invertebrate Fish

0.03(96 h) 0.081(7d) 15.51(48 h) 562.5(96 h)

30 81 15 510 562 500

171.6

95.6

5.720 2.1185 0.0111 0.00031

3.1867 1.1802 0.0062 0.00017

Nunes et al. (2005) Li et al. (2012) Isidori et al. (2005) Li et al. (2012)

SMZ

Algae Invertebrate

1.277(7d) 147.5(96 h)

1277 147 500

9.9

14.9

0.0078 0.00007

0.0117 0.0001

Brain et al. (2004) Jung et al. (2008)

SCP

Algae Plant

32.25(24 h) 2.48(72 h)

32 250 2480

4.6

1.6

0.0001 0.0018

0.00005 0.0006

Bialk-Bielinska et al. (2011) Bialk-Bielinska et al. (2011)

SDM

Algae Plant

9.85(24 h) 0.02(72 h)

9850 20

8.8

0

0.0009 0.44

0 0

Bialk-Bielinska et al. (2011) Bialk-Bielinska et al. (2011)

NOR

Algae Plant Invertebrate

50.18(96 h) 0.913(7d) 194.98(48 h)

50 180 913 194 980

70.2

107.4

0.0014 0.0769 0.0004

0.0021 0.1176 0.0006

Li et al. (2012) Li et al. (2012) Li et al. (2012)

CIP

Algae Plant

0.017(24 h) 0.203(7d)

17 203

23.2

11.9

1.3647 0.1143

0.70 0.0586

Robinson et al. (2005) Robinson et al. (2005)

LOM

Algae Plant

0.186(24 h) 0.106(7d)

186 106

5.5

24.0

0.0296 0.0519

0.1290 0.2264

Robinson et al. (2005) Robinson et al. (2005)

ENR

Algae Plant Invertebrate Fish

0.049(5d) 0.114(7d) 56.7(48 h) >100(48 h)

49 114 56 700 100 000

82.7

20.7

1.6878 0.7254 0.0015 0.0008

0.4224 0.1816 0.0004 0.0002

Robinson et al. (2005) Robinson et al. (2005) Li et al. (2012) Li et al. (2012)

OFL

Algae Plant Invertebrate

0.021(24 h) 0.126(7d) 17.41(48 h)

21 126 17 410

182.7

383.4

8.70 1.45 0.0105

18.2571 3.0429 0.022

Robinson et al. (2005) Robinson et al. (2005) Robinson et al. (2005)

TC

Algae

0.09(7d)

90

17.8

1.9

0.1978

0.0211

Halling-Sørensen (2000)

OTC

Algae Invertebrate Fish

0.17(72 h) 0.18(7d) 62.5(96 h)

170 180 62 500

4.9

16.5

0.0288 0.0272 0.0001

0.0971 0.0917 0.0003

Nunes et al. (2005) Isidori et al. (2005) Park and Choi (2008)

CTC

Algae Invertebrate Fish

0.05(7d) 225(48 h) 78.9(96 h)

50 225 000 78 900

4.0

4.2

0.08 0.00002 0.00005

0.084 0.00002 0.00005

Halling-Sørensen (2000) Park and Choi (2008) Park and Choi (2008)

attention should be given to antibiotic resistance in Lake Chaohu, especially in the west side of the lake and the estuary of the Nanfei River and Shiwuli River.

rivers. Further research is needed to investigate the fate of these antibiotics and the occurrence of antibiotic resistance in Lake Chaohu.

4. Conclusion

Acknowledgments

In the present study, the concentrations of the selected antibiotics in all of the water samples were typically at the ng L1 level, and SMX and OFL were the dominant antibiotic pollutants, with high detection frequencies and concentrations in Lake Chaohu. The occurrence of the antibiotics during the winter was significantly higher than during the other seasons, and the concentrations of the antibiotics in the west side of the lake were higher than in the east side of the lake. The western inflowing rivers, such as the Naifei and Shiwuli Rivers were the primary import routes of the antibiotics in Lake Chaohu. The concentrations of the antibiotics in the effluent of four STPs in Hefei City were similar to those in urban rivers, suggesting that the domestic effluent was the major source. The quality of water downstream of Lake Chaohu was influenced by the lake, and the risk assessment of the antibiotics on aquatic organisms suggested that algae and plants might be at high risk in the surface water of Lake Chaohu and in the inflowing rivers. These results revealed the potential source of antibiotics and indicated that the pollution control for STPs should be strengthened, and more attention should be given to the western inflowing

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