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Occurrence and distribution of antibiotics in urban soil in Beijing and Shanghai, China

Abstract

The recycling of reclaimed wastewater for irrigation and road cleaning is an important strategy to minimize water scarcity in megacities. However, little is known regarding the potential accumulation of antibiotics contained in reclaimed wastewater in urban soil. We investigated the occurrence and distribution of eight quinolones (QNs), nine sulfonamides (SAs), and five macrolides (MLs) antibiotics in urban surface soil in Beijing and Shanghai, China. QNs, especially norfloxacin (NOR), ofloxacin (OFL), and ciprofloxacin (CIP) were the predominant antibiotics in urban surface soil, and NOR revealed the highest average concentration of 94.6 μg kg−1. The antibiotic concentrations in urban soil in our study were higher than those detected in agricultural soils after long-term wastewater irrigation and manure fertilization. The concentrations of antibiotics in Shanghai urban soil showed a significant negative correlation with soil pH and a positive correlation with total organic carbon (TOC), reflecting the effect of speciation and soil organic matter content on sorption and retention. In addition, antibiotic concentrations in the urban soil were positively correlated with heavy metal contents, likely due to their coexistence in reclaimed wastewater and the promoting effect of metals on the sorption of antibiotics. In several soil samples, NOR, OFL, CIP, enrofloxacin (ENR), and fleroxacin (FLE) showed higher concentrations than the trigger value of 100 μg kg−1 in soil, indicating a potential risk for the environment.

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References

  • Babić S, Horvat AJM, Mutavdžić Pavlović D, Kaštelan-Macan M (2007) Determination of pKa values of active pharmaceutical ingredients. TrAC Trends Anal Chem 26:1043–1061

    Article  Google Scholar 

  • Burkhardt M, Stamm C (2007) Depth distribution of sulfonamide antibiotics in pore water of an undisturbed loamy grassland soil. J Environ Qual 36:588–596

    Article  CAS  Google Scholar 

  • Calza P, Marchisio S, Medana C, Baiocchi C (2009) Fate of antibacterial spiramycin in river waters. Anal Bioanal Chem 396:1539–1550

    Article  Google Scholar 

  • Carrasquillo AJ, Bruland GL, Mackay AA, Vasudevan D (2008) Sorption of ciprofloxacin and oxytetracycline zwitterions to soils and soil minerals: influence of compound structure. Environ Sci Technol 42:7634–7642

    Article  CAS  Google Scholar 

  • Chee-Sanford JC, Mackie RI, Koike S, Krapac IG, Lin YF, Yannarell AC, Maxwell S, Aminov RI (2009) Fate and transport of antibiotic residues and antibiotic resistance genes following land application of manure waste. J Environ Qual 38:1086–1108

    Article  CAS  Google Scholar 

  • Dalkmann P, Broszat M, Siebe C, Willaschek E, Sakinc T, Huebner J, Amelung W, Grohmann E, Siemens J (2012) Accumulation of pharmaceuticals, enterococcus, and resistance genes in soils irrigated with wastewater for zero to 100 years in Central Mexico. Plos One 7:e45397

    Article  CAS  Google Scholar 

  • Dalkmann P, Willaschek E, Schiedung H, Bornemann L, Siebe C, Siemens J (2014) Long-term wastewater irrigation reduces sulfamethoxazole sorption, but not ciprofloxacin binding, in Mexican soils. J Environ Qual 43:964–970

    Article  Google Scholar 

  • Diaz-Cruz M, Lopezdealda M, Barcelo D (2006) Determination of antimicrobials in sludge from infiltration basins at two artificial recharge plants by pressurized liquid extraction–liquid chromatography–tandem mass spectrometry. J Chromatogr A 1130:72–82

    Article  CAS  Google Scholar 

  • Feitosafelizzola J, Chiron S (2009) Occurrence and distribution of selected antibiotics in a small Mediterranean stream (Arc River, Southern France). J Hydrol 364:50–57

    Article  CAS  Google Scholar 

  • Gao LH, Shi YL, Li WH, Niu HY, Liu JM, Cai YQ (2012) Occurrence of antibiotics in eight sewage treatment plants in Beijing, China. Chemosphere 86:665–671

    Article  CAS  Google Scholar 

  • Golet EM, Strehler A, Alder AC, Giger W (2002) Determination of fluoroquinolone antibacterial agents in sewage sludge and sludge-treated soil using accelerated solvent extraction followed by solid-phase extraction. Anal Chem 74:5455–5462

    Article  CAS  Google Scholar 

  • Hamscher G, Sczesny S, Hoper H, Nau H (2002) Determination of persistent tetracycline residues in soil fertilized with liquid manure by high-performance liquid chromatography with electrospray ionization tandem mass spectrometry. Anal Chem 74:1509–1518

    Article  CAS  Google Scholar 

  • Heberer T, Massmann G, Fanck B, Taute T, Dunnbier U (2008) Behaviour and redox sensitivity of antimicrobial residues during bank filtration. Chemosphere 73:451–460

    Article  CAS  Google Scholar 

  • Hu XF, Zhu Q, Chen B, Deng HH (2002) Environmental quality of treated wastewater and its reuse for irrigation. Agro-environ Protect 21:530–534

  • Hu XG, Zhou QX, Luo Y (2010) Occurrence and source analysis of typical veterinary antibiotics in manure, soil, vegetables and groundwater from organic vegetable bases, northern China. Environ Pollut 158:2992–2998

    Article  CAS  Google Scholar 

  • Jacobsen A, Hallingsorensen B, Ingerslev F, Honorehansen S (2004) Simultaneous extraction of tetracycline, macrolide and sulfonamide antibiotics from agricultural soils using pressurised liquid extraction, followed by solid-phase extraction and liquid chromatography–tandem mass spectrometry. J Chromatogr A 1038:157–170

    Article  CAS  Google Scholar 

  • Jiang L, Chen SY, Yang R, Ren ZY, Yin DQ (2008) Occurrence of antibiotics in the aquatic environment of the Changjiang delta, China. Environ Chem 27:371–374

    CAS  Google Scholar 

  • Jiang L, Hu X, Yin D, Zhang H, Yu Z (2011) Occurrence, distribution and seasonal variation of antibiotics in the Huangpu River, Shanghai, China. Chemosphere 82:822–828

    Article  CAS  Google Scholar 

  • Jjemba PK (2002) The potential impact of veterinary and human therapeutic agents in manure and biosolids on plants grown on arable land: a review. Agric Ecosyst Environ 93:267–278

    Article  Google Scholar 

  • Kan CA, Petz M (2000) Residues of veterinary drugs in eggs and their distribution between yolk and white. J Agric Food Chem 48:6397–6403

    Article  CAS  Google Scholar 

  • Karcı A, Balcıoğlu IA (2009) Investigation of the tetracycline, sulfonamide, and fluoroquinolone antimicrobial compounds in animal manure and agricultural soils in Turkey. Sci Total Environ 407:4652–4664

    Article  Google Scholar 

  • Kim SC, Carlson K (2007) Temporal and spatial trends in the occurrence of human and veterinary antibiotics in aqueous and river sediment matrices. Environ Sci Technol 41:50–57

    Article  CAS  Google Scholar 

  • Kim I, Tanaka H (2009) Photodegradation characteristics of PPCPs in water with UV treatment. Environ Int 35:793–802

    Article  CAS  Google Scholar 

  • Kinney CA, Furlong ET, Werner SL, Cahill JD (2006) Presence and distribution of wastewater-derived pharmaceuticals in soil irrigated with reclaimed water. Environ Toxicol Chem 25:317–326

    Article  CAS  Google Scholar 

  • Knapp CW, Dolfing J, Ehlert PAI, Graham DW (2010) Evidence of increasing antibiotic resistance gene abundances in archived soils since 1940. Environ Sci Technol 44:580–587

    Article  CAS  Google Scholar 

  • Kotzerke A, Sharma S, Schauss K, Heuer H, Thiele-Bruhn S, Smalla K, Wilke BM, Schloter M (2008) Alterations in soil microbial activity and N-transformation processes due to sulfadiazine loads in pig-manure. Environ Pollut 153:315–322

    Article  CAS  Google Scholar 

  • Kümmerer K (2009) Antibiotics in the aquatic environment—a review—Part I. Chemosphere 75:417–434

    Article  Google Scholar 

  • Leung HW, Minh TB, Murphy MB, Lam JCW, So MK, Martin M, Lam PKS, Richardson BJ (2012) Distribution, fate and risk assessment of antibiotics in sewage treatment plants in Hong Kong, South China. Environ Int 42:1–9

    Article  CAS  Google Scholar 

  • Li B, Zhang T (2011) Mass flows and removal of antibiotics in two municipal wastewater treatment plants. Chemosphere 83:1284–1289

    Article  Google Scholar 

  • Li WH, Shi YL, Gao LH, Liu JM, Cai YQ (2012) Investigation of antibiotics in mollusks from coastal waters in the Bohai Sea of China. Environ Pollut 162:56–62

    Article  CAS  Google Scholar 

  • Li WH, Shi YL, Gao LH, Liu JM, Cai YQ (2013) Occurrence and removal of antibiotics in a municipal wastewater reclamation plant in Beijing, China. Chemosphere 92:435–444

    Article  CAS  Google Scholar 

  • Love DC, Rodman S, Neff RA, Nachman KE (2011) Veterinary drug residues in seafood inspected by the European union, United States, Canada, and Japan from 2000 to 2009. Environ Sci Technol 45:7232–7240

    Article  CAS  Google Scholar 

  • Luo Y, Xu L, Rysz M, Wang YQ, Zhang H, Alvarez PJJ (2011) Occurrence and transport of tetracycline, sulfonamide, quinolone, and macrolide antibiotics in the Haihe River Basin, China. Environ Sci Technol 45:1827–1833

    Article  CAS  Google Scholar 

  • Lutzhoft HCH, Halling-Sorensen B, Jorgensen SE (1999) Algal toxicity of antibacterial agents applied in Danish fish farming. Arch Environ Contam Toxicol 36:1–6

    Article  CAS  Google Scholar 

  • Ma M, Huang ZB, Jiao ZH, Miao ZX, Hou LW, Zhou J, Zhao Y (2007) Effects of reclaimed wastewater irrigation on the quality of maize and soy bean. Trans CSAE 23:47–50

    CAS  Google Scholar 

  • Marengo JR, Kok RA, OBrien K, Velagaleti RR, Stamm JM (1997) Aerobic biodegradation of (C-14)-sarafloxacin hydrochloride in soil. Environ Toxicol Chem 16:462–471

    Article  CAS  Google Scholar 

  • Martinez JL (2009) Environmental pollution by antibiotics and by antibiotic resistance determinants. Environ Pollut 157:2893–2902

    Article  CAS  Google Scholar 

  • Ostermann A, Siemens J, Welp G, Xue QY, Lin XY, Liu XJ, Amelung W (2013) Leaching of veterinary antibiotics in calcareous Chinese croplands. Chemosphere 91:928–934

    Article  CAS  Google Scholar 

  • Ostermann A, Gao J, Welp G, Siemens J, Roelcke M, Heimann L, Nieder R, Xue QY, Lin XY, Sandhage-Hofmann A, Amelung W (2014) Identification of soil contamination hotspots with veterinary antibiotics using heavy metal concentrations and leaching data-a field study in China. Environ Monit Assess 186:7693–7707

    Article  CAS  Google Scholar 

  • Park S, Choi K (2008) Hazard assessment of commonly used agricultural antibiotics on aquatic ecosystems. Ecotoxicology 17:526–538

    Article  CAS  Google Scholar 

  • Pico Y, Andreu V (2007) Fluoroquinolones in soil—risks and challenges. Anal Bioanal Chem 387:1287–1299

    Article  CAS  Google Scholar 

  • Rosendahl I, Siemens J, Kindler R, Groeneweg J, Zimmermann J, Czerwinski S, Lamshoft M, Laabs V, Wilke BM, Vereecken H, Amelung W (2012) Persistence of the fluoroquinolone antibiotic difloxacin in soil and lacking effects on nitrogen turnover. J Environ Qual 41:1275–1283

    Article  CAS  Google Scholar 

  • Sanderson H, Thomsen M (2009) Comparative analysis of pharmaceuticals versus industrial chemicals acute aquatic toxicity classification according to the United Nations classification system for chemicals. Assessment of the (Q)SAR predictability of pharmaceuticals acute aquatic toxicity and their predominant acute toxic mode-of-action. Toxicol Lett 187:84–93

    Article  CAS  Google Scholar 

  • Sarmah A, Meyer M, Boxall A (2006) A global perspective on the use, sales, exposure pathways, occurrence, fate and effects of veterinary antibiotics (VAs) in the environment. Chemosphere 65:725–759

    Article  CAS  Google Scholar 

  • Schlusener M, Spiteller M, Bester K (2003) Determination of antibiotics from soil by pressurized liquid extraction and liquid chromatography–tandem mass spectrometry. J Chromatogr A 1003:21–28

    Article  CAS  Google Scholar 

  • Shi YL, Gao LH, Li WH, Liu JM, Cai YQ (2012) Investigation of fluoroquinolones, sulfonamides and macrolides in long-term wastewater irrigation soil in Tianjin, China. Bull Environ Contam Toxicol 89:857–861

    Article  CAS  Google Scholar 

  • Siemens J, Huschek G, Walshe G, Siebe C, Kasteel R, Wulf S, Clemens J, Kaupenjohann M (2010) Transport of pharmaceuticals in columns of a wastewater-irrigated Mexican clay soil. J Environ Qual 39:1201–1210

    Article  CAS  Google Scholar 

  • Sithole BB, Guy RD (1987) Models for tetracycline in aquatic environments.1. Interaction with bentonite clay systems. Water Air Soil Pollut 32:303–314

    Article  CAS  Google Scholar 

  • Skinner M, Kanfer I (1992) Intrinsic dissolution rate and solubility studies on josamycin, a macrolide antibiotic. Int J Pharm 88:151–158

    Article  CAS  Google Scholar 

  • Suárez S, Carballa M, Omil F, Lema JM (2008) How are pharmaceutical and personal care products (PPCPs) removed from urban wastewaters? Rev Environ Sci Biotechnol 7:125–138

    Article  Google Scholar 

  • Tamtam F, Mercier F, Le Bot B, Eurin J, Tuc Dinh Q, Clément M, Chevreuil M (2008) Occurrence and fate of antibiotics in the Seine River in various hydrological conditions. Sci Total Environ 393:84–95

    Article  CAS  Google Scholar 

  • Tamtam F, van Oort F, Le Bot B, Dinh T, Mompelat S, Chevreuil M, Lamy I, Thiry M (2011) Assessing the fate of antibiotic contaminants in metal contaminated soils four years after cessation of long-term waste water irrigation. Sci Total Environ 409:540–547

    Article  CAS  Google Scholar 

  • Ternes TA, Bonerz M, Herrmann N, Teiser B, Andersen HR (2007) Irrigation of treated wastewater in Braunschweig, Germany: an option to remove pharmaceuticals and musk fragrances. Chemosphere 66:894–904

    Article  CAS  Google Scholar 

  • Tolls J (2001) Sorption of veterinary pharmaceuticals in soils: a review. Environ Sci Technol 35:3397–3406

    Article  CAS  Google Scholar 

  • Vasudevan D, Bruland GL, Torrance BS, Upchurch VG, MacKay AA (2009) pH-dependent ciprofloxacin sorption to soils: interaction mechanisms and soil factors influencing sorption. Geoderma 151:68–76

    Article  CAS  Google Scholar 

  • Wang FH, Qiao M, Lv ZE, Guo GX, Jia Y, Su YH, Zhu YG (2014a) Impact of reclaimed water irrigation on antibiotic resistance in public parks, Beijing, China. Environ Pollut 184:247–253

    Article  CAS  Google Scholar 

  • Wang FH, Qiao M, Su JQ, Chen Z, Zhou X, Zhu YG (2014b) High throughput profiling of antibiotic resistance genes in urban park soils with reclaimed water irrigation. Environ Sci Technol 48:9079–9085

    Article  CAS  Google Scholar 

  • Watkinson AJ, Murby EJ, Kolpin DW, Costanzo SD (2009) The occurrence of antibiotics in an urban watershed: from wastewater to drinking water. Sci Total Environ 407:2711–2723

    Article  CAS  Google Scholar 

  • Wei RC, Ge F, Huang SY, Chen M, Wang R (2011) Occurrence of veterinary antibiotics in animal wastewater and surface water around farms in Jiangsu Province, China. Chemosphere 82:1408–1414

    Article  CAS  Google Scholar 

  • Yang S-F, Lin C-F, Yu-Chen Lin A, Andy Hong P-K (2011) Sorption and biodegradation of sulfonamide antibiotics by activated sludge: Experimental assessment using batch data obtained under aerobic conditions. Water Res 45(11):3389–3397

    Article  CAS  Google Scholar 

  • Yiruhan, Wang QJ, Mo CH, Li YW, Gao P, Tai YP, Zhang Y, Ruan ZL, Xu JW (2010) Determination of four fluoroquinolone antibiotics in tap water in Guangzhou and Macao. Environ Pollut 158:2350–2358

    Article  CAS  Google Scholar 

  • Zhang J, Li ZJ, Ge GF, Sun WC, Liang YC, Wu LS (2009) Impacts of soil organic matter, pH and exogenous copper on sorption behavior of norfloxacin in three soils. J Environ Sci-China 21:632–640

  • Zhao L, Dong YH, Wang H (2010) Residues of veterinary antibiotics in manures from feedlot livestock in eight provinces of China. Sci Total Environ 408:1069–1075

    Article  CAS  Google Scholar 

  • Zhou LJ, Ying GG, Zhao JL, Yang JF, Wang L, Yang B, Liu S (2011) Trends in the occurrence of human and veterinary antibiotics in the sediments of the Yellow River, Hai River and Liao River in northern China. Environ Pollut 159:1877–1885

    Article  CAS  Google Scholar 

  • Zorita S, Mårtensson L, Mathiasson L (2009) Occurrence and removal of pharmaceuticals in a municipal sewage treatment system in the south of Sweden. Sci Total Environ 407:2760–2770

    Article  CAS  Google Scholar 

  • Zou SC, Xu WH, Zhang RJ, Tang JH, Chen YJ, Zhang G (2011) Occurrence and distribution of antibiotics in coastal water of the Bohai Bay, China: impacts of river discharge and aquaculture activities. Environ Pollut 159:2913–2920

    Article  CAS  Google Scholar 

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Acknowledgments

This work was financially supported by the National Basic Research Program of China (2014CB114402), the National Natural Science Foundation of China (No. 21321004, 41023005, 21407008), and the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB14010201).

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Correspondence to Jiemin Liu or Yaqi Cai.

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Gao, L., Shi, Y., Li, W. et al. Occurrence and distribution of antibiotics in urban soil in Beijing and Shanghai, China. Environ Sci Pollut Res 22, 11360–11371 (2015). https://doi.org/10.1007/s11356-015-4230-3

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