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Total concentrations of heavy metals and occurrence of antibiotics in sewage sludges from cities throughout China

  • SOILS, SEC 3 • REMEDIATION AND MANAGEMENT OF CONTAMINATED OR DEGRADED LANDS • RESEARCH ARTICLE
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Abstract

Purpose

A total of 58 dewatered sludge samples were collected from 58 sewage treatment plants (STPs) geographically located in 31 provincial cities of China; the concentrations of heavy metals and antibiotics were determined to monitor the pollutant levels on a large scale, and the pollutant concentrations in sludge samples from different sources of sewage sludge and different geographical regions were compared.

Materials and methods

All the samples were divided into two portions, one of which was air-dried for determination of heavy metals. The other portion was placed in a brown glass bottle and frozen at −20 °C for antibiotics analysis. Total heavy metals were digested with aqua regia and determined by atomic absorption spectrophotometry (Varian SpectrAA 220FS and Varian SpectrAA 220Z). The antibiotics were extracted with EDTA-sodium phosphate buffer with acetonitrile/Mg(NO3)2-NH3⋅H2O, v/v, 3:1 and analysed by liquid chromatography-electrospray ionization tandem mass spectrometry (LC-ESI-MS/MS) and quantified by the isotope-labelled internal standard method.

Results and discussion

In all the sludge samples, zinc was the most abundant metal followed by copper, with relatively low concentrations of chromium, lead, nickel and cadmium. Only 20 % of samples exceeded the Chinese class A values of heavy metal standards for agricultural use (GJ/T309-2009). Sixteen different antibiotics were detected in all the sludge samples, and fluoroquinolones (FQs) and tetracyclines (TCs) were more abundant than sulfonamides (SAs). Concentrations of ∑FQs, ∑TCs and ∑SAs ranged from 1,569 to 23,825 μg kg−1 (mean 8,274 μg kg−1, dry weight), from 592 to 37,895 μg kg−1 (mean 8,326 μg kg−1, dry weight) and from 20.1 to 117 μg kg−1 (mean 55.4 μg kg−1, dry weight), respectively. Tetracyclines (except chlortetracycline) were significantly correlated with zinc and lead. No significant regional trends were observed in the concentrations of heavy metals and antibiotics in sludges.

Conclusions

Heavy metal concentrations are not the major factor restricting domestic and mixed flow sludge application, but the antibiotic concentrations in sludges are problematic; regulation of antibiotic use and establishment of standards to ensure safe handling of sludges are needed.

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References

  • Alvarez EA, Mochon MC, Sanchez JCJ, Rodriguez MT (2002) Heavy metal extractable forms in sludge from wastewater treatment plants. Chemosphere 47:765–775

    Article  CAS  Google Scholar 

  • Brown KD, Kulis J, Thomson B, Chapman TH, Mawhinney DB (2006) Occurrence of antibiotics in hospital, residential, and dairy, effluent, municipal wastewater, and the Rio Grande in New Mexico. Sci Total Environ 366:772–783

    Article  CAS  Google Scholar 

  • Chen M, Li XM, Yang Q, Zeng GM, Zhang Y, Liao DX, Liu JJ, Hu JM, Guo L (2008) Total concentrations and speciation of heavy metals in municipal sludge from Changsha, Zhuzhou and Xiangtan in middle-south region of China. J Hazard Mater 160:324–329

    Article  CAS  Google Scholar 

  • Chen YS, Zhang HB, Song J, Luo YM (2012) Occurrence and dissipation of veterinary antibiotics in two typical swine wastewater treatment systems in east China. Environ Monit Assess 184:2205–2217

    Article  CAS  Google Scholar 

  • Chen YS, Yu G, Cao QM, Zhang HB, Lin QY, Hong YW (2013) Occurrence and environmental implications of pharmaceuticals in Chinese municipal sewage sludge. Chemosphere 93(9):1767–1772

    Article  Google Scholar 

  • Fernandez-Fontaina E, Pinho I, Carballa M, Omil F, Lema JM (2013) Biodegradation kinetic constants and sorption coefficients of micropollutants in membrane bioreactors. Biodegradation 24:165–177

    Article  CAS  Google Scholar 

  • Foley J, Blackwell A (2003) Ion release from copper phosphate cement and influence on Streptococcus mutans growth in vitro: a comparative study. Caries Res 37:416–424

    Article  CAS  Google Scholar 

  • Fuentes A, Llorens M, Saez J, Soler A, Aguilar MI, Ortuno JF, Meseguer VF (2004) Simple and sequential extractions of heavy metals from different sewage sludges. Chemosphere 54:1039–1047

    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 

  • Garcia-Delgado M, Rodriguez-Cruz MS, Lorenzo LF, Arienzo M, Sanchez-Martin MJ (2007) Seasonal and time variability of heavy metal content and of its chemical forms in sewage sludges from different wastewater treatment plants. Sci Total Environ 382:82–92

    Article  CAS  Google Scholar 

  • Giger W, Alder AC, Golet EM, Kohler HPE, McArdell CS, Molnar E, Siegrist H, Suter MJF (2003) Occurrence and fate of antibiotics as trace contaminants in wastewaters, sewage sludges, and surface waters. Chimia 57:485–491

    Article  CAS  Google Scholar 

  • Gobel A, Thomsen A, McArdell CS, Joss A, Giger W (2005) Occurrence and sorption behavior of sulfonamides, macrolides, and trimethoprim in activated sludge treatment. Environ Sci Technol 39:3981–3989

    Article  Google Scholar 

  • Golet EM, Alder AC, Hartmann A, Ternes TA, Giger W (2001) Trace determination of fluoroquinolone antibacterial agents in solid-phase extraction urban wastewater by and liquid chromatography with fluorescence detection. Anal Chem 73:3632–3638

    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 

  • Golet EM, Xifra I, Siegrist H, Alder AC, Giger W (2003) Environmental exposure assessment of fluoroquinolone antibacterial agents from sewage to soil. Environ Sci Technol 37:3243–3249

    Article  CAS  Google Scholar 

  • Haller MY, Muller SR, McArdell CS, Alder AC, Suter MJF (2002) Quantification of veterinary antibiotics (sulfonamides and trimethoprim) in animal manure by liquid chromatography-mass spectrometry. J Chromatogr A 952:111–120

    Article  CAS  Google Scholar 

  • Hu JY, Shi JC, Chang H, Li D, Yang M, Kamagata YC (2008) Phenotyping and genotyping of antibiotic-resistant Escherichia coli isolated from a natural river basin. Environ Sci Technol 42:3415–3420

    Article  CAS  Google Scholar 

  • 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 

  • Hu W, Ma LL, Guo CS, Sha J, Zhu XW, Wang YQ (2012) Simultaneous extraction and determination of fluoroquinolones, tetracyclines and sulfonamides antibiotics in soils using optimised solid phase extraction chromatography-tandem mass spectrometry. Int J Environ Anal Chem 92:698–713

    Article  CAS  Google Scholar 

  • Huang YJ, Cheng MM, Li WH, Wu LH, Chen YS, Luo YM, Christie P, Zhang HB (2013) Simultaneous extraction of four classes of antibiotics in soil, manure and sewage sludge and analysis by liquid chromatography-tandem mass spectrometry with the isotope-labelled internal standard method. Anal Methods 5:3721–3731

    Article  CAS  Google Scholar 

  • Illera V, Walter I, Souza P, Cala V (2000) Short-term effects of biosolid and municipal solid waste applications on heavy metals distribution in a degraded soil under a semi-arid environment. Sci Total Environ 255:29–44

    Article  CAS  Google Scholar 

  • Ji XL, Shen QH, Liu F, Ma J, Xu G, Wang YL, Wu MH (2012) Antibiotic resistance gene abundances associated with antibiotics and heavy metals in animal manures and agricultural soils adjacent to feedlots in Shanghai, China. J Hazard Mater 235–236:178–185

    Article  Google Scholar 

  • Jia A, Wan Y, Xiao Y, Hu JY (2012) Occurrence and fate of quinolone and fluoroquinolone antibiotics in a municipal sewage treatment plant. Water Res 46:387–394

    Article  CAS  Google Scholar 

  • Karvelas M, Katsoyiannis A, Samara C (2003) Occurrence and fate of heavy metals in the wastewater treatment process. Chemosphere 53:1201–1210

    Article  CAS  Google Scholar 

  • Kemper N (2008) Veterinary antibiotics in the aquatic and terrestrial environment. Ecol Indic 8:1–13

    Article  CAS  Google Scholar 

  • Kim S, Eichhorn P, Jensen JN, Weber AS, Aga DS (2005) Removal of antibiotics in wastewater: effect of hydraulic and solid retention times on the fate of tetracycline in the activated sludge process. Environ Sci Technol 39:5816–5823

    Article  CAS  Google Scholar 

  • Kinney CA, Furlong ET, Zaugg SD, Burkhard MR, Werner SL, Cahill JD, Jorgensen GR (2006) Survey of organic wastewater contaminants in biosolids destined for land application. Environ Sci Technol 40:7207–7215

    Article  CAS  Google Scholar 

  • Kummerer K, Henninger A (2003) Promoting resistance by the emission of antibiotics from hospitals and households into effluent. Clin Microbiol Infect 9:1203–1214

    Article  CAS  Google Scholar 

  • Lasheen MR, Ammar NS (2009) Assessment of metals speciation in sewage sludge and stabilized sludge from different wastewater treatment plants, Greater Cairo, Egypt. J Hazard Mater 164:740–749

    Article  CAS  Google Scholar 

  • Li JH, Zhou BX, Xue B, Mo QL, Cai WM (2011a) Influence of heavy metals and surfactants on the adsorption of tetracyclines to sediment. Res J Chem Environ 15:71–76

    CAS  Google Scholar 

  • Li YW, Wu XL, Mo CH, Tai YP, Huang XP, Xiang L (2011b) Investigation of sulfonamide, tetracycline, and quinolone antibiotics in vegetable farmland soil in the Pearl River Delta area, Southern China. J Agric Food Chem 59:7268–7276

    Article  Google Scholar 

  • Li WH, Shi YL, Gao LH, Liu JM, Cai YQ (2013) Occurrence, distribution and potential affecting factors of antibiotics in sewage sludge of wastewater treatment plants in China. Sci Total Environ 445–446:306–313

    Article  Google Scholar 

  • Lindberg RH, Wennberg P, Johansson MI, Tysklind M, Andersson BAV (2005) Screening of human antibiotic substances and determination of weekly mass flows in five sewage treatment plants in Sweden. Environ Sci Technol 39:3421–3429

    Article  CAS  Google Scholar 

  • Lindberg RH, Olofsson U, Rendahl P, Johansson MI, Tysklind M, Andersson BAV (2006) Behavior of fluoroquinolones and trimethoprim during mechanical, chemical, and active sludge treatment of sewage water and digestion of sludge. Environ Sci Technol 40:1042–1048

    Article  CAS  Google Scholar 

  • Martín J, Camacho-Muñoz MA, Santos JL, Aparicio I, Alonso E (2012) Distribution and temporal evolution of pharmaceutically active compounds alongside sewage sludge treatment. Risk assessment of sludge application onto soils. J Environ Manag 102:18–25

    Article  Google Scholar 

  • Martinez F, Cuevas G, Calvo R, Walter I (2003) Biowaste effects on soil and native plants in a semiarid ecosystem. J Environ Qual 32:472–479

    Article  CAS  Google Scholar 

  • McCartney D, Zhang Y, Grant C (2001) Characterization of compost produced at a golf course: impact of historic mercury accumulations in putting green soil. Compost Sci Util 9:73–91

    Article  Google Scholar 

  • McClellan K, Halden RU (2010) Pharmaceuticals and personal care products in archived U.S. biosolids from the 2001 EPA national sewage sludge survey. Water Res 44:658–668

    Article  CAS  Google Scholar 

  • McGrath SP, Cunliffe CH (1985) A simplified method for the extraction of the metals Fe, Zn, Cu, Ni, Cd, Pb, Cr, Co and Mn from soils and sewage sludges. J Sci Food Agric 36:794–798

    Article  CAS  Google Scholar 

  • Miao XS, Bishay F, Chen M, Metcalfe CD (2004) Occurrence of antimicrobials in the final effluents of wastewater treatment plants in Canada. Environ Sci Technol 38:3533–3541

    Article  CAS  Google Scholar 

  • Nwosu VC (2001) Antibiotic resistance with particular reference to soil microorganisms. Res Microbiol 152:421–430

    Article  CAS  Google Scholar 

  • Okuda T, Yamashita N, Tanaka H, Matsukawa H, Tanabe K (2009) Development of extraction method of pharmaceuticals and their occurrences found in Japanese wastewater treatment plants. Environ Int 35:815–820

    Article  CAS  Google Scholar 

  • Przewrocki P, Kulczycka J, Wzorek Z, Kowalski Z, Gorazda K, Jodko M (2004) Risk analysis of sewage sludge—Poland and EU comparative approach. Pol J Environ Stud 13:237–244

    CAS  Google Scholar 

  • Richardson BJ, Larn PKS, Martin M (2005) Emerging chemicals of concern: pharmaceuticals and personal care products (PPCPs) in Asia, with particular reference to Southern China. Mar Pollut Bull 50:913–920

    Article  CAS  Google Scholar 

  • Rysz M, Alvarez PJJ (2004) Amplification and attenuation of tetracycline resistance in soil bacteria: aquifer column experiments. Water Res 38:3705–3712

    Article  CAS  Google Scholar 

  • Scancar J, Milacic R, Strazar M, Burica O (2000) Total metal concentrations and partitioning of Cd, Cr, Cu, Fe, Ni and Zn in sewage sludge. Sci Total Environ 250:9–19

    Article  CAS  Google Scholar 

  • Smith SR (2009) Organic contaminants in sewage sludge (biosolids) and their significance for agricultural recycling. Phil Trans R Soc A 367:4005–4041

    Article  CAS  Google Scholar 

  • Spongberg AL, Witter JD (2008) Pharmaceutical compounds in the wastewater process stream in Northwest Ohio. Sci Total Environ 397:148–157

    Article  CAS  Google Scholar 

  • Sun YH, Luo YM, Wu LH, Teng Y (2009) Heavy metals concentration in sewage sludge of Yangtze River Delta (in Chinese). Environ Protect Sci 35:26–29

    Google Scholar 

  • Tella M, Doelsch E, Letourmy P, Chataing S, Cuoq F, Bravin MN, Saint Macary H (2013) Investigation of potentially toxic heavy metals in different organic wastes used to fertilize market garden crops. Waste Manag 33:184–192

    Article  CAS  Google Scholar 

  • Thiele-Bruhn S (2003) Pharmaceutical antibiotic compounds in soils—a review. J Plant Nutr Soil Sci 166:145–167

    Article  CAS  Google Scholar 

  • Tong L, Li P, Wang YX, Zhu KZ (2009) Analysis of veterinary antibiotic residues in swine wastewater and environmental water samples using optimized SPE-LC/MS/MS. Chemosphere 74:1090–1097

    Article  CAS  Google Scholar 

  • Tu JC, Zhao QL, Wei LL, Yang QQ (2012) Heavy metal concentration and speciation of seven representative municipal sludges from wastewater treatment plants in Northeast China. Environ Monit Assess 184:1645–1655

    Article  CAS  Google Scholar 

  • Wang C, Hu X, Chen ML, Wu YH (2005) Total concentrations and fractions of Cd, Cr, Pb, Cu, Ni and Zn in sewage sludge from municipal and industrial wastewater treatment plants. J Hazard Mater 119:245–249

    Article  CAS  Google Scholar 

  • Wang YJ, Jia DA, Sun RJ, Zhu HW, Zhou DM (2008) Adsorption and cosorption of tetracycline and copper(II) on montmorillonite as affected by solution pH. Environ Sci Technol 42:3254–3259

    Article  CAS  Google Scholar 

  • Wollenberger L, Halling-Sorensen B, Kusk KO (2000) Acute and chronic toxicity of veterinary antibiotics to Daphnia magna. Chemosphere 40:723–730

    Article  CAS  Google Scholar 

  • Wu LH, Cheng MM, Li Z, Ren J, Shen LB, Wang SF, Luo YM, Christie P (2012) Major nutrients, heavy metals and PBDEs in soils after long-term sewage sludge application. J Soils Sediments 12:531–541

    Article  CAS  Google Scholar 

  • Xu WH, Zhang G, Li XD, Zou SC, Li P, Hu ZH, Li J (2007) Occurrence and elimination of antibiotics at four sewage treatment plants in the Pearl River Delta (PRD), South China. Water Res 41:4526–4534

    Article  CAS  Google Scholar 

  • Zhang T, Li B (2011) Occurrence, transformation, and fate of antibiotics in municipal wastewater treatment plants. Crit Rev Environ Sci Technol 41:951–998

    Article  CAS  Google Scholar 

  • Zhang XX, Wu B, Zhang Y, Zhang T, Yang LY, Fang HHP, Ford T, Cheng SP (2009) Class 1 integronase gene and tetracycline resistance genes tetA and tetC in different water environments of Jiangsu Province, China. Ecotoxicology 18:652–660

    Article  CAS  Google Scholar 

  • Zhao YP, Geng JJ, Wang XR, Gu XY, Gao SX (2011a) Adsorption of tetracycline onto goethite in the presence of metal cations and humic substances. J Colloid Interface Sci 361:247–251

    Article  CAS  Google Scholar 

  • Zhao YP, Geng JJ, Wang XR, Gu XY, Gao SX (2011b) Tetracycline adsorption on kaolinite: pH, metal cations and humic acid effects. Ecotoxicology 20:1141–1147

    Article  CAS  Google Scholar 

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Acknowledgments

We thank the National Natural Science Foundation of China (Projects 40930739 and 41271326) for the grant-aided support. We also thank our colleagues from the universities or institutes in the provincial cities for their kind help with the collection of sewage sludge samples.

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Authors and Affiliations

  1. Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, 210008, China

    Miaomiao Cheng, Longhua Wu, Yujuan Huang, Yongming Luo & Peter Christie

  2. University of Chinese Academy of Sciences, Beijing, 100049, People’s Republic of China

    Miaomiao Cheng

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  1. Miaomiao Cheng
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  2. Longhua Wu
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  3. Yujuan Huang
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  4. Yongming Luo
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Correspondence to Longhua Wu.

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Responsible editor: Bernd Markert

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Cheng, M., Wu, L., Huang, Y. et al. Total concentrations of heavy metals and occurrence of antibiotics in sewage sludges from cities throughout China. J Soils Sediments 14, 1123–1135 (2014). https://doi.org/10.1007/s11368-014-0850-3

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