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Antibiotics in the Aquatic Environments: a Review of Lakes, China

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Antibiotics in the Aquatic Environments: a Review of Lakes, China Science of the Total Environment 627 (2018) 1195–1208 Contents lists available at ScienceDirect Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv Antibiotics in the aquatic environments: A review of lakes, China Xiaohui Liu a,b, Shaoyong Lu b,⁎,WeiGuoc, Beidou Xi b,WeiliangWangd a School of Environment, Tsinghua University, Beijing 100084, China b State Environmental Protection Scientific Observation and Research Station for Lake Dongting, Chinese Research Academy of Environmental Sciences, Beijing 100012, China c School of Environmental Science and Engineering, North China Electric Power University, Beijing 1002206, China d School of Geography and Environment, Shandong Normal University, Jinan, Shandong 250358, China HIGHLIGHTS GRAPHICAL ABSTRACT • 39 antibiotics are detected in aquatic environment of lakes in China • The quinolone antibiotics are predomi- nant risk and pollution factors in aquatic environment of lakes. • All Lakes experience ARGs pollution with high detection frequencies of sul- fonamide and tetracycline resistance genes. article info abstract Article history: The potential threat of antibiotics to the environment and human health has raised significant concerns in recent Received 17 December 2017 years. The consumption and production of antibiotics in China are the highest in the world due to its rapid eco- Received in revised form 22 January 2018 nomic development and huge population, possibly resulting in the high detection frequencies and concentrations Accepted 26 January 2018 of antibiotics in aquatic environments of China. As a water resource, lakes in China play an important role in sus- Available online 6 February 2018 tainable economic and social development. Understanding the current state of antibiotics in lakes in China is im- Editor: Jay Gan portant. Closed and semi-closed lakes provide an ideal medium for the accumulation of antibiotics and antibiotic resistance genes (ARGs). This review summarizes the current levels of antibiotic exposure in relevant environ- Keywords: mental compartments in lakes. The ecological and health risks of antibiotics are also evaluated. This review con- Antibiotics cludes that 39 antibiotics have been detected in the aquatic environments of lakes in China. The levels of Lake antibiotic contamination in lakes in China is relatively high on the global scale. Antibiotic contamination is higher Aquatic environment in sediment than water and aquatic organisms. Quinolone antibiotics (QNs) pose the greatest risks. The contents Occurrence of antibiotics in aquatic organisms are far lower than their maximum residual limits (MRLs), with the exception Risk of the organisms in Honghu Lake. The lakes experience high levels of ARG contamination. A greater assessment of ARG presence and antibiotic exposure are urgent. © 2018 Elsevier B.V. All rights reserved. ⁎ Corresponding author. E-mail address: [email protected] (S. Lu). https://doi.org/10.1016/j.scitotenv.2018.01.271 0048-9697/© 2018 Elsevier B.V. All rights reserved. 1196 X. Liu et al. / Science of the Total Environment 627 (2018) 1195–1208 Contents 1. Introduction............................................................. 1196 2. Occurrence.............................................................. 1196 2.1. Surfacewater......................................................... 1196 2.2. Sediment........................................................... 1200 2.3. Aquaticorganisms....................................................... 1203 3. Risk................................................................. 1203 3.1. Riskassessment........................................................ 1203 3.1.1. Surfacewater..................................................... 1203 3.1.2. Sediment-acasestudyofDongtingLake......................................... 1204 3.1.3. Excessiveoccurrenceofantibioticresiduesinaquaticorganisms.............................. 1205 3.2. Antibioticresistancegenes................................................... 1205 4. Conclusionsandsuggestions...................................................... 1205 Acknowledgment............................................................. 1205 AppendixA. Supplementarydata..................................................... 1205 References................................................................. 1205 1. Introduction Some information of Lakes are provided in Table S1. This review aims to summarize the contamination status of current antibiotics and antibi- Antibiotics are routinely used in human and veterinary medicine for otic resistance genes in different environmental media of Lakes in China the therapeutic treatment of infectious diseases, as well as for animal and assess their potential threats to environment and health risk. The growth promoters (Kümmerer, 2009a; Zhu et al., 2013). However, anti- results could provide reliable information regarding the exposure and biotics are excreted as the parent compounds or metabolites due to poor risk levels of antibiotics of Lakes in China, which are important for estab- gut absorption or incomplete metabolism (Q. Chen et al., 2017, Y. Chen lishment the supervision legal framework (market entry permitting et al., 2017), resulting in frequent detection in aquatic environment due system, drug advertising restrictions and strict and clear application to incomplete removal of antibiotics during wastewater treatment and process for antibiotic use) of the antibiotic misuse and the water quality their continued release into the environment (Hirsch et al., 1999; criteria and discharging standard of antibiotics. Kümmerer, 2009b; Ma et al., 2016). The consumption and production of antibiotics in China are the highest in the world (Xin, 2014). The pre- 2. Occurrence scriptions including antibiotics account for 70%, while the proportion is only about 30% in western countries, and annual per-capita consump- 2.1. Surface water tion reaching 138 g are approximately 2 times those of the Europe and 10 times those of the United States (Richardson et al., 2005; Yang The concentrations of antibiotics in the surface water of typical lakes et al., 2012; Kan et al., 2015). The production of antibiotics in 2013 in China are provided in Table 1. Thirty-seven antibiotics, including 14 was up to 2.48 × 105 t which had almost tripled since 2009, and the sulfonamides (SAs), trimethoprim (TMP), 9 quinolones (QNs), 5 tetra- usage of antibiotics in 2013 is up to 1.62 × 105t with antibiotics of 5.0 cyclines (TCs), 6 macrolides (MCs) and 2 lincosamides (LNs), have ×104t/yr into water and soil environment (Zhang et al., 2015). There- been detected in the surface water of typical lakes in China. Some infor- fore, the concentrations and detection frequencies of antibiotics in mation about antibiotics is provided in Table S2. The sulfonamides and aquatic environment in China are higher than that of some western quinolone antibiotics are the main contamination factors, which is sim- countries (Qiao et al., 2017). Antibiotics could lead to a selective pres- ilar to the case in other surface water bodies (Table 2). The concentra- sure on the water bacteria and induce the formation of antibiotic resis- tions of antibiotics in the surface water of lakes range from not tant bacteria, reducing their therapeutic potential against human and detected (ND) (a concentration below the smallest value that the ana- animal pathogens (Carvalho and Santos, 2016; Qiao et al., 2017). There- lytical methods measured) to 940 ng L−1, which is below the μgL−1 fore, the antibiotic residues in aquatic environment could pose a poten- grade. tial threat to environment and human health. The concentrations of SAs range from ND-940 ng L−1 (Table 1). The Lakes, which are important freshwater resources and for flood regu- concentration of sulfamethoxazole (SMX) is higher than that of other lation, are closely related to human production and life (Feng et al., SAs and includes the highest concentration, 940 ng L−1. The highest 2012; Chen et al., 2014). China is a country with many lakes, and prelim- concentration indicates that the exposure level to SMX is highest in inary statistics show that China has approximately 2800 lakes with an Baiyangdian Lake, followed by Chaohu Lake and Taihu Lake. The produc- area larger than 1 km2 (Le et al., 2010, G. Yang et al., 2010, J.F. Yang tion scale and the uses of SMX in China are among the highest in the et al., 2010). The freshwater resources amount to 2.3 × 1011 m3 (Lu world. In addition, detecting SMX, one of 14 sulfonamide antibiotics, et al., 2017). Approximately 50% of urban drinking water sources, al- needs to be prioritized according to the U.S. Food and Drug Administra- most 1/3 of national grain output and over 30% of the total output tion (FDA) (Wang et al., 2016). SMX is among the most widely used pre- value of industry and agriculture are from lake basins (Leng et al., scribed antibiotics: the usage of SMX is sixth in Canada (Nasuhoglu 2003), However, rapid development has greatly expanded the industry, et al., 2011), and the frequency of SMX detection in aquatic environ- agriculture and aquaculture of lake basins, which inevitably causes a ments is high (Wang et al., 2014). The large scale of livestock and poul- large number of antibiotics to be used. Zhang et al. (2015) found that try farming and the high population density in lake basins result in high − the emissions of antibiotics (2190–3560 t yr 1) in the Dongting Lake usage of SMX. The highest concentrations of sulfamethazine
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