Journal of Soils and Sediments

, Volume 19, Issue 5, pp 2445–2458 | Cite as

Is the long-term application of sewage sludge turning soil into a sink for organic pollutants?: evidence from field studies in the Czech Republic

  • Jana Pulkrabová
  • Jindřich Černý
  • Jiřina SzákováEmail author
  • Andrea Švarcová
  • Tomáš Gramblička
  • Jana Hajšlová
  • Jiří Balík
  • Pavel Tlustoš
Soils, Sec 3 • Remediation and Management of Contaminated or Degraded Lands • Research Article



Long-term microscale field experiments established at four sites in the Czech Republic (since 1996) were used for an assessment of the severity of the wide-scale contamination of treated soils by persistent organic pollutants (POPs) and pharmaceuticals and personal care products (PPCPs) as a result of the long-term regular pollutant load via sewage sludge and farmyard manure applications and for an estimation of the potential environmental risk caused by long-term pollutant inputs to agricultural soils.

Material and methods

The experimental plots were treated as follows: (i) NPK mineral fertilization (NPK); (ii) sewage sludge (SS1); (iii) sewage sludge applied at three times the rate compared to SS1 (SS2); (iv) farmyard manure (FYM); and (v) untreated control. Except for antibiotics, which showed results for all analyses below the detection limit, all groups of the analyzed compounds showed measurable contents in the treated soils.

Results and discussion

Among the POPs, the levels of organochlorine pesticides (OCPs) were detected at two locations at levels exceeding the Czech preventive values for their contents in agricultural soils (7.5 μg/kg for dichlorodiphenyl trichloroethane family, 20 μg/kg for hexachlorbenzene, and 10 μg/kg for α-hexachlorocyclohexane), regardless of the treatment. Similarly, elevated contents of polycyclic aromatic hydrocarbons (PAHs) were occasionally observed without any substantial relationship to the fertilizer application scenario. Thus, these contaminants are connected with atmospheric deposition in the given areas (PAHs) and their long-term stability (OCPs) even several decades after their ban; the role of the fertilizer composition was negligible.


The levels of per- and polyfluoroalkylated substances, brominated flame retardants, and synthetic musk compounds tended to increase in the sewage sludge–treated plots, indicating that sewage sludge can contribute to the abundance of these compounds in soil, although the contaminant levels determined do not represent a direct environmental risk. The levels of these contaminants in sewage sludge and sludge-treated soils should be regularly monitored in further research.


Farmyard manure Long-term trial Persistent organic pollutants Pharmaceuticals and personal care products Sewage sludge 



Correction and improvement of language were provided by Ltd., Devonshire Business Centre, Works Road, Letchworth Garden City SG6 1GJ, United Kingdom.

Funding information

The authors are thankful for financial support of the GAČR 16-07441S project, and the National Programme of Sustainability I″—NPU I (LO1601-No.: MSMT-43760/2015).

Supplementary material

11368_2019_2265_MOESM1_ESM.docx (28 kb)
ESM 1 (DOCX 28 kb)


  1. Abad E, Martinez K, Planas C, Palacios O, Caixach J, Rivera J (2005) Priority organic pollutant assessment of sludges for agricultural purposes. Chemosphere 61:1358–1369CrossRefGoogle Scholar
  2. Allaire SE, Del Castillo J, Juneau V (2006) Sorption kinetics of chlortetracyline and tylosin on sandy loam and heavy clay soils. J Environ Qual 35:969–972CrossRefGoogle Scholar
  3. Amarakoon ID, Zvomuya F, Sura S, Larney FJ, Cessna AJ, Xu SW, McAllister TA (2016) Dissipation of antimicrobials in feedlot manure compost after oral administration versus fortification after excretion. J Environ Qual 45:503–510CrossRefGoogle Scholar
  4. An J, Chen HW, Wei SH, Gu J (2015) Antibiotic contamination in animal manure, soil, and sewage sludge in Shenyang, Northeast China. Environ Earth Sci 74:5077–5086CrossRefGoogle Scholar
  5. Antolin-Rodriguez J, Sanchez-Bascones M, Martin-Ramos P, Bravo-Sanchez CT, Martin-Gil J (2016) Estimation of PCB content in agricultural soils associated with long-term fertilization with organic waste. Environ Sci Pollut Res 23:12372–12383CrossRefGoogle Scholar
  6. Chen F, Ying G, Ma Y, Chen Z, Lai H, Peng F (2014a) Field dissipation and risk assessment of typical personal care products TCC, TCS, AHTN and HHCB in biosolid-amended soils. Sci Total Environ 470-471:1078–1086CrossRefGoogle Scholar
  7. Chen CH, Zhou QX, Cai Z (2014b) Effect of soil HHCB on cadmium accumulation and phytotoxicity in wheat seedlings. Ecotoxicology 23:1996–2004CrossRefGoogle Scholar
  8. Chow KL, Man YB, Tam NFY, Liang Y, Wong MH (2015) Uptake and transport mechanisms of decabromodiphenyl ether (BDE-209) by rice (Oryza sativa). Chemosphere 119:1262–1267CrossRefGoogle Scholar
  9. Clarke RM, Cummins E (2015) Evaluation of “classic” and emerging contaminants resulting from the application of biosolids to agricultural lands: a review. Hum Ecol Risk Assess 21:492–513CrossRefGoogle Scholar
  10. Cleary DW, Bishop AH, Zhang LH, Topp E, Wellington EMH, Gaze WH (2016) Long-term antibiotic exposure in soil is associated with changes in microbial community structure and prevalence of class 1 integrons. FEMS Microbiol Ecol 92:fiw159CrossRefGoogle Scholar
  11. Ding HY, Wu YX, Zou BC, Lou Q, Zhang WH, Zhong JY, Lu L, Dai GF (2016) Simultaneous removal and degradation characteristics of sulfonamide, tetracycline, and quinolone antibiotics by laccase-mediated oxidation coupled with soil adsorption. J Hazard Mater 307:350–358CrossRefGoogle Scholar
  12. During RA, Gath S (2002) Tillage effects on the accumulation of polychlorinated biphenyls in biosolid-amended soils. J Plant Nutr Soil Sci 165:299–304CrossRefGoogle Scholar
  13. Elskens M, Pussemier L, Dumortier P, Van Langenhove K, Scholl G, Goeyens L, Focant JF (2013) Dioxin levels in fertilizers from Belgium: determination and evaluation of the potential impact on soil contamination. Sci Total Environ 454:66–372Google Scholar
  14. Feng Y, Li ZJ, Hao XQ (2016) Impacts of soil organic matter, iron-aluminium oxides and pH on adsorption-desorption behaviors of oxytetracycline. Res J Biotechnol 11:121–131Google Scholar
  15. Gao P, Ding YJ, Li H, Xagoraraki I (2012) Occurrence of pharmaceuticals in a municipal wastewater treatment plant: mass balance and removal processes. Chemosphere 88:17–24CrossRefGoogle Scholar
  16. Guerra P, Kleywegt S, Payne M, Svoboda ML, Lee HB, Reiner E, Kolic T, Metcalfe C, Smyth SA (2015) Occurrence and fate of trace contaminants during aerobic and anaerobic sludge digestion and dewatering. J Environ Qual 44:1193–1200CrossRefGoogle Scholar
  17. Higgins CP, Luthy RG (2006) Sorption of perfluorinated surfactants on sediments. Environ Sci Technol 40:7251–7256CrossRefGoogle Scholar
  18. Hong S, Khim JS, Park J, Kim M, Kim WK, Jung J, Hyun S, Kim JG, Lee H, Choi HJ, Codling G, Giesy JP (2013) In situ fate and partitioning of waterborne perfluoroalkyl acids (PFAAs) in the Youngsan and Nakdong River estuaries of South Korea. Sci Total Environ 445-446:136–145CrossRefGoogle Scholar
  19. Hou J, Wang C, Mao DQ, Luo Y (2016) The occurrence and fate of tetracyclines in two pharmaceutical wastewater treatment plants of northern China. Environ Sci Pollut Res 23:1722–1731CrossRefGoogle Scholar
  20. Körschens M (2006) The importance of long-term field experiments for soil science and environmental research-a review. Plant Soil Environ 52:1–8CrossRefGoogle Scholar
  21. Kulhánek M, Balik J, Černý J, Vašák F, Shejbalová Š (2014) Influence of long-term fertilizer application on changes of the content of Mehlich-3 estimated soil macronutrients. Plant Soil Environ 60:151–157CrossRefGoogle Scholar
  22. Lee HJ, Kim CJ, Hong GH, Hong SH, Shim WJ, Kim GB (2014) Congener-specific accumulation and environmental risk assessment of polybrominated diphenyl ethers in diverse Korean sewage sludge types. Environ Sci Pollut Res 21:7480–7488CrossRefGoogle Scholar
  23. Li JH, Zhou BX, Xue B, Mo QL, Cai WM (2011) Influence of heavy metals and surfactants on the adsorption of tetracyclines to sediment. Res J Chem Environ 15:71–76Google Scholar
  24. Li YY, Shi S, Zhang L, Liu YS (2016a) Global trends and performances of publication on sewage sludge from 1991 to 2012. In: Li J, Dong F (eds) Selected proceedings of the tenth international conference on waste management and technology Book Series: Procedia Environmental Sciences 31:65–74Google Scholar
  25. Li WL, Ma WL, Jia HL, Hong WJ, Moon HB, Nakata H, Minh NH, Sinha RK, Chi KH, Kannan K (2016b) Polybrominated diphenyl ethers (PBDEs) in surface soils across five Asian countries: levels, spatial distribution, and source contribution. Environ Sci Technol 50:12779–12788CrossRefGoogle Scholar
  26. Macherius A, Eggen T, Lorenz WG, Reemtsma T, Winkler U, Moeder M (2012) Uptake of galaxolide, tonalide, and triclosan by carrot, barley, and meadow fescue plants. J Agric Food Chem 60:7785–7791CrossRefGoogle Scholar
  27. Madaras M, Stehlíková I, Teplá M (2013) The long-term field experiments and their merit for sustainable agriculture. Crop Research Institute, Prague (in Czech)Google Scholar
  28. McClellan K, Halden RU (2010) Pharmaceuticals and personal care products in US biosolids. In: Halden RU (Ed) Contaminants of emerging concern in the environment: ecological and human health considerations. Book Series: ACS Symposium Series 1048:199–211Google Scholar
  29. Meijer SN, Halsall CJ, Harner T, Peters AJ, Ockenden WA, Johnston AE, Jones KC (2001) Organochlorine pesticide residues in archived UK soil. Environ Sci Technol 35:1989–1995CrossRefGoogle Scholar
  30. Naile JE, Khim JS, Hong S, Park J, Kwon BO, Ryu JS, Hwang JH, Jones PD, Giesy JP (2013) Distributions and bioconcentration characteristics of perfluorinated compounds in environmental samples collected from the west coast of Korea. Chemosphere 90:387–394CrossRefGoogle Scholar
  31. Nelson KL, Brozel VS, Gibson SA, Thaler R, Clay SA (2011) Influence of manure from pigs fed chlortetracycline as growth promotant on soil microbial community structure. World J Microbiol Biotechnol 27:659–668CrossRefGoogle Scholar
  32. Odukkathil G, Vasudevan N (2013) Toxicity and bioremediation of pesticides in agricultural soil. Rev Environ Sci Biotechnol 12:421–444CrossRefGoogle Scholar
  33. Oleszczuk P (2007) Organic pollutants in sewage sludge-amended soil part I. General remarks. Ecol Chem Eng 14:65–76Google Scholar
  34. Österas AH, Allmyr M, Sternbeck J (2015) Screening of organic pollutants in sewage sludge amended arable soils. Swedish Environmental Protection AgencyGoogle Scholar
  35. Ostermann A, Gao J, Welp G, Siemens J, Roelcke M, Heimann L, Nieder R, Xue QY, Lin XY, Sandhage-Hofmann A (2014) Identification of soil contamination hotspots with veterinary antibiotics using heavy metal concentrations and leaching data-a field study in China. Environ Monit Assess 186:7693–7707CrossRefGoogle Scholar
  36. Pan LL, Sun JT, Wu XD, Wei Z, Zhu LZ (2016) Transformation of hydroxylated and methoxylated 2,2 ',4,4 ',5-brominated diphenyl ether (BDE-99) in plants. J Environ Sci 49:197–202CrossRefGoogle Scholar
  37. Plassmann MM, Berger U (2013) Pefluoroalkyl carboxylic acids with up to 22 carbon atoms in snow and soil samples from a ski area. Chemosphere 91:832–837CrossRefGoogle Scholar
  38. Plosz BG, Leknes H, Liltved H, Thomas KV (2010) Diurnal variations in the occurrence and the fate of hormones and antibiotics in activated sludge wastewater treatment in Oslo, Norway. Sci Total Environ 408:1915–1924CrossRefGoogle Scholar
  39. Public notice No. 153/2016 (2016) About the conditions for the protection of the agricultural soil quality. Legal code of The Czech Republic, pp 2692–2699Google Scholar
  40. Ray P, Chen CQ, Knowlton KF, Pruden A, Xia K (2017) Fate and effect of antibiotics in beef and dairy manure during static and turned composting. J Environ Qual 46:45–54CrossRefGoogle Scholar
  41. Roccaro P, Vagliasindi FGA (2014) Risk assessment of the use of biosolids containing emerging organic contaminants in agriculture. In: Ranzi E, Kohse Hoinghaus K (eds) ICONBM: international conference on biomass, PTS 1 and 2. Book Series: Chemical Engineering Transactions 37:817–822Google Scholar
  42. Rychen G, Jurjanz S, Fournier A, Toussaint H, Feidt C (2014) Exposure of ruminants to persistent organic pollutants and potential of decontamination. Environ Sci Pollut Res 21:6440–6447CrossRefGoogle Scholar
  43. Santos JL, Aparicio I, Santos A, Alvarez F, Lopez-Artiguez M, Olano D, Garcia S, Alonso E (2009) Presence of organic pollutants in sludge from anaerobic wastewater stabilization ponds. Desalin Water Treat 4:116–121CrossRefGoogle Scholar
  44. Singh RP, Agrawal M (2008) Potential benefits and risks of land application of sewage sludge. Waste Manag 28:347–358CrossRefGoogle Scholar
  45. Spielmeyer A, Stahl F, Petri MS, Zerr W, Brunn H, Hamscher G (2017) Transformation of sulfonamides and tetracyclines during anaerobic fermentation of liquid manure. J Environ Qual 46:160–168CrossRefGoogle Scholar
  46. Sseburege P, Wasswa J, Mbabazi J, Nyanzi SA, Kiremire BT, Marco JAM (2010) Organochlorine pesticides in soils from south-western Uganda. Chemosphere 78:1250–1255CrossRefGoogle Scholar
  47. Száková J, Pulkrabová J, Černý J, Mercl F, Švarcová A, Gramblička T, Najmanová J, Tlustoš P, Balík J (2018) Selected persistent organic pollutants (POPs) in the rhizosphere of sewage sludge-treated soil: implications for the biodegradability of POPs. Arch Agron Soil Sci:1–16.
  48. Topp E, Metcalfe CD, Boxall AB, Lapen DR (2010) Transport of PPCPs and veterinary medicines from agricultural fields following application of biosolids or manure. In: Halden RU (ed) Contaminants of emerging concern in the environment: ecological and human health considerations. Book Series: ACS Symposium Series 1048:227–240Google Scholar
  49. Umlauf G, Christoph EH, Lanzini L, Savolainen R, Skejo H, Bidoglio G, Clemens J, Goldbach H, Scherer H (2011) PCDD/F and dioxin-like PCB profiles in soils amended with sewage sludge, compost, farmyard manure, and mineral fertilizer since 1962. Environ Sci Pollut Res 18:461–470CrossRefGoogle Scholar
  50. Vane CH, Kim AW, Beriro DJ, Cave MR, Knights K, Moss-Hayes V, Nathanail PC (2014) Polycyclic aromatic hydrocarbons (PAH) and polychlorinated biphenyls (PCB) in urban soils of greater London, UK. Appl Geochem 51:303–314CrossRefGoogle Scholar
  51. Vašák F, Černý J, Buráňová Š, Kulhánek M, Balík J (2015) Soil pH changes in long-term field experiments with different fertilizing systems. Soil Water Res 10:19–23CrossRefGoogle Scholar
  52. Venkatesan AK, Halden RU (2014) Brominated flame retardants in US biosolids from the EPA national sewage sludge survey and chemical persistence in outdoor soil mesocosms. Water Res 55:133–142CrossRefGoogle Scholar
  53. Wang Y, Luo C, Li J, Yin H, Li X, Zhang G (2011) Characterization of PBDEs in soils and vegetations near an e-waste recycling site in South China. Environ Pollut 159:2443–2448CrossRefGoogle Scholar
  54. Wilson SC, Alcock RE, Sewart AP, Jones KC (1997) Persistence of organic contaminants in sewage sludge-amended soil: a field experiment. J Environ Qual 26:1467–1477CrossRefGoogle Scholar
  55. Xiang L, Wu, XL, Jiang YN, Yan QY, Li YW, Huang XP, Cai QY, Mo CH (2016) Occurrence and risk assessment of tetracycline antibiotics in soil from organic vegetable farms in a subtropical city, south China. Environ Sci Pollut Res 23:13984–13995Google Scholar
  56. Xiao F, Simcik MF, Halbach TR, Gulliver JS (2015) Perfluorooctane sulfonate (PFOS) and perfluorooctanoate (PFOA) in soils and groundwater of a U.S. metropolitan area: migration and implications for human exposure. Water Res 72:64–74CrossRefGoogle Scholar
  57. Yang J, Metcalfe CD (2006) Fate of synthetic musks in a domestic wastewater treatment plant and in an agricultural field amended with biosolids. Sci Total Environ 363:149–165CrossRefGoogle Scholar
  58. Yi LY, Zhao HH, Yuan Z, Zhou DL, Liang YT (2016) Depression of soil microbial respiration, ammonification and cellulose degradation under the stress of antibiotic residuals. Environ Eng Manag J 15:2189–2194CrossRefGoogle Scholar
  59. Zennegg M, Munoz M, Schmid P, Gerecke AC (2013) Temporal trends of persistent organic pollutants in digested sewage sludge (1993–2012). Environ Int 60:202–208CrossRefGoogle Scholar
  60. Zhu Z, Chen S, Zheng J, Tian M, Feng A, Luo X, Mai B (2014) Occurrence of brominated flame retardants (BFRs), organochlorine pesticides (OCPs), and polychlorinated biphenyls (PCBs) in agricultural soils in a BFR-manufacturing region of North China. Sci Total Environ 481:47–54CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Food Analysis and Nutrition, Faculty of Food and Biochemical TechnologyUniversity of Chemistry and Technology, PraguePrague 6Czech Republic
  2. 2.Department of Agroenvironmental Chemistry and Plant NutritionCzech University of Life SciencesPrague 6Czech Republic

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