The practice of incorporating animal manure into soil is supported within the European Circular economy as a possible substitute for mineral fertilizers and will become crucial for the sustainability of agriculture. However, this practice may indirectly contribute to the dissemination of antibiotics, resistance bacteria, and resistance genes. In this study, medicated drinking water and poultry litter samples were obtained from a broiler-chick farm. The obtained poultry litter was incorporated into the soil at the experimental field site. The objectives of this research project were first to develop analytical methods able to quantify fluoroquinolones (FQs) in medicated drinking water, poultry litter, and soil samples by LC-MS; second to study the fate of these FQs in the soil environment after incorporation of poultry litter from flock medicated by enrofloxacin (ENR); and third to screen the occurrence of selected fluoroquinolone resistance encoding genes in poultry litter and soil samples (PCR analysis). FQs were quantified in the broiler farm's medicated drinking water (41.0 ± 0.3 mg∙L-1 of ENR) and poultry litter (up to 70 mg∙kg-1 of FQs). The persistence of FQs in the soil environment over 112 days was monitored and evaluated (ENR concentrations ranged from 36 μg∙kg-1 to 9 μg∙kg-1 after 100 days). The presence of resistance genes was confirmed in both poultry litter and soil samples, in agreement with the risk assessment for the selection of AMR in soil based on ENR concentrations. This work provides a new, comprehensive perspective on the entry and long-term fate of antimicrobials in the terrestrial environment and their consequences after the incorporation of poultry litter into agricultural fields.

Central Institute for Supervising and Testing in Agriculture Hroznová 63 2 603 00 Brno Czech Republic

Department of Public Health Faculty of Medicine Masaryk University Kamenice 5 625 00 Brno Czech Republic

Institute for State Control of Veterinary Biologicals and Medicines Hudcova 56 A Brno Czech Republic

Institute of Environmental Chemistry Faculty of Chemistry Brno University of Technology Purkyňova 118 612 00 Brno Czech Republic

Zobrazit více v PubMed

Aga DS, Lenczewski M, Snow D, Muurinen J, Sallach JB, Wallace JS. Challenges in the measurement of antibiotics and in evaluating their impacts in agroecosystems: a critical review. J Environ Qual. 2016;45:407–419. doi: 10.2134/jeq2015.07.0393. PubMed DOI

Albero B, Tadeo JL, Escario M, Miguel E, Pérez RA. Persistence and availability of veterinary antibiotics in soil and soil-manure systems. Sci Total Environ. 2018;643:1562–1570. doi: 10.1016/j.scitotenv.2018.06.314. PubMed DOI

Amr Alliance science-based PNEC targets for risk assessments (2023) Available at: https://www.amrindustryalliance.org/wp-content/uploads/2023/02/AMR-Table-1-Update-20230222_corrected.pdf

An J, Chen H, Wei S, Gu J. Antibiotic contamination in animal manure, soil, and sewage sludge in Shenyang, northeast China. Environ Earth Sci. 2015;74:5077–5086. doi: 10.1007/s12665-015-4528-y. DOI

Arun S, Kumar RM, Ruppa J, Mukhopadhyay M, Ilango K, Chakraborty P. Occurrence, sources and risk assessment of fluoroquinolones in dumpsite soil and sewage sludge from Chennai. India Environmental Toxicology and Pharmacology. 2020;79:103410. doi: 10.1016/j.etap.2020.103410. PubMed DOI

Bartrons M, Peñuelas J. Pharmaceuticals and personal-care products in plants. Trends Plant Sci. 2017;22:194–203. doi: 10.1016/j.tplants.2016.12.010. PubMed DOI

Boxall ABA, Johnson P, Smith EJ, Sinclair CJ, Stutt E, Levy LS. Uptake of veterinary medicines from soils into plants. J Agric Food Chem. 2006;54:2288–2297. doi: 10.1021/jf053041t. PubMed DOI

Butler E, Whelan MJ, Ritz K, Sakrabani R, van Egmond R. The effect of triclosan on microbial community structure in three soils. Chemosphere. 2012;89:1–9. doi: 10.1016/j.chemosphere.2012.04.002. PubMed DOI

Caracciolo AB, Visca A, Rauseo J, Spataro F, Garbini GL, Grenni P, Mariani L, Mazzurco Miritana V, Massini G, Patrolecco L. Bioaccumulation of antibiotics and resistance genes in lettuce following cattle manure and digestate fertilization and their effects on soil and phyllosphere microbial communities. Environ Pollut. 2022;315:120413. doi: 10.1016/j.envpol.2022.120413. PubMed DOI

Carballo EM, González-Barreiro C, Scharf S, Gans O. Environmental monitoring study of selected veterinary antibiotics in animal manure and soils in Austria. Environ Pollut. 2007;148:570–579. doi: 10.1016/j.envpol.2006.11.035. PubMed DOI

Carlsson C, Johansson A-K, Alvan G, Bergman K, Kühler T. Are pharmaceuticals potent environmental pollutants? Sci Total Environ. 2006;364:67–87. doi: 10.1016/j.scitotenv.2005.06.035. PubMed DOI

Cattoir V, Poirel L, Rotimi V, Soussy C-J, Nordmann P. Multiplex PCR for detection of plasmid-mediated quinolone resistance qnr genes in ESBL-producing enterobacterial isolates. J Antimicrob Chemother. 2007;60:394–397. doi: 10.1093/jac/dkm204. PubMed DOI

Cycoń M, Mrozik A, Piotrowska-Seget Z (2019) Antibiotics in the soil environment—degradation and their impact on microbial activity and diversity. Front Microbiol 10:338. 10.3389/fmicb.2019.00338 PubMed PMC

Deschamps BM, Leang S, Bernet N, Daudin J-J, Nélieu S. Multi-residue analysis of pharmaceuticals in aqueous environmental samples by online solid-phase extraction–ultra-high-performance liquid chromatography-tandem mass spectrometry: optimisation and matrix effects reduction by quick, easy, cheap, effective, rugged and safe extraction. J Chromatogr A. 2014;1349:11–23. doi: 10.1016/j.chroma.2014.05.006. PubMed DOI

Deschamps BM, Ferhi S, Bernet N, et al. Fate and impacts of pharmaceuticals and personal care products after repeated applications of organic waste products in long-term field experiments. Sci Total Environ. 2017;607–608:271–280. doi: 10.1016/j.scitotenv.2017.06.240. PubMed DOI

Du L, Liu W. Occurrence, fate, and ecotoxicity of antibiotics in agro-ecosystems A Review. Agron Sustain Dev. 2011;32:309–327. doi: 10.1007/s13593-011-0062-9. DOI

Fatta-Kassinos D, Meric S, Nikolaou A. Pharmaceutical residues in environmental waters and wastewater: current state of knowledge and future research. Anal Bioanal Chem. 2010;399:251–275. doi: 10.1007/s00216-010-4300-9. PubMed DOI

Ferrero GP, Borova V, Dasenaki ME, Τhomaidis ΝS. Simultaneous determination of 148 pharmaceuticals and illicit drugs in sewage sludge based on ultrasound-assisted extraction and liquid chromatography–tandem mass spectrometry. Anal Bioanal Chem. 2015;407:4287–4297. doi: 10.1007/s00216-015-8540-6. PubMed DOI

Gibs J, Heckathorn HA, Meyer MT, Klapinski FR, Alebus M, Lippincott RL. Occurrence and partitioning of antibiotic compounds found in the water column and bottom sediments from a stream receiving two wastewater treatment plant effluents in Northern New Jersey, 2008. Sci Total Environ. 2013;458–460:107–116. doi: 10.1016/j.scitotenv.2013.03.076. PubMed DOI

Gros M, Marti E, Balcázar JL, et al. Fate of pharmaceuticals and antibiotic resistance genes in a full-scale on-farm livestock waste treatment plant. J Hazard Mater. 2019;378:120716. doi: 10.1016/j.jhazmat.2019.05.109. PubMed DOI

Gros M, Mas-Pla J, Boy-Roura M, Geli I, Domingo F, Petrović M. Veterinary pharmaceuticals and antibiotics in manure and slurry and their fate in amended agricultural soils: Findings from an experimental field site (Baix Empordà, NE Catalonia) Sci Total Environ. 2019;654:1337–1349. doi: 10.1016/j.scitotenv.2018.11.061. PubMed DOI

Gutiérrez FJ, Barbosa J, Barrón D. Metabolic study of enrofloxacin and metabolic profile modifications in broiler chicken tissues after drug administration. Food Chem. 2015;172:30–39. doi: 10.1016/j.foodchem.2014.09.025. PubMed DOI

Gworek B, Kijeńska M, Zaborowska M, Wrzosek J, Tokarz L, Chmielewski J. Pharmaceuticals in aquatic environment Fate and behaviour, ecotoxicology and risk assessment – a review. Acta Pol Pharm - Drug Res. 2019;76:397–407. doi: 10.32383/appdr/103368. DOI

Gworek B, Kijeńska M, Wrzosek J, Graniewska M. Pharmaceuticals in the soil and plant environment: a review. Water Air Soil Pollut. 2021 doi: 10.1007/s11270-020-04954-8.10.1007/s11270-020-04954-8. DOI

Han X-M, Hu H-W, Chen Q-L, Yang L-Y, Li H-L, Zhu Y-G, Li X-Z, Ma Y-B. Antibiotic resistance genes and associated bacterial communities in agricultural soils amended with different sources of animal manures. Soil Biol Biochem. 2018;126:91–102. doi: 10.1016/j.soilbio.2018.08.018. DOI

Ho YB, Zakaria MP, Latif PA, Saari N. Occurrence of veterinary antibiotics and progesterone in broiler manure and agricultural soil in Malaysia. Sci Total Environ. 2014;488–489:261–267. doi: 10.1016/j.scitotenv.2014.04.109. PubMed DOI

Hou J, Wan W, Mao D, Wang C, Mu Q, Qin S, Luo Y. Occurrence and distribution of sulfonamides, tetracyclines, quinolones, macrolides, and nitrofurans in livestock manure and amended soils of Northern China. Environ Sci Pollut Res. 2014;22:4545–4554. doi: 10.1007/s11356-014-3632-y. PubMed DOI

Hu X, Zhou Q, Luo Y. Occurrence and source analysis of typical veterinary antibiotics in manure, soil, vegetables and groundwater from organic vegetable bases, northern China. Environ Pollut. 2010;158:2992–2998. doi: 10.1016/j.envpol.2010.05.023. PubMed DOI

Huang Y, Cheng M, Li W, Wu L, Chen Y, Luo Y, Christie P, Zhang H. 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. 2013;5:3721. doi: 10.1039/c3ay40220g. DOI

Jechalke S, Heuer H, Siemens J, Amelung W, Smalla K. Fate and effects of veterinary antibiotics in soil. Trends Microbiol. 2014;22:536–545. doi: 10.1016/j.tim.2014.05.005. PubMed DOI

Kim K-R, Owens G, Kwon S-I, So K-H, Lee D-B, Ok YS. Occurrence and environmental fate of veterinary antibiotics in the terrestrial environment. Water Air Soil Pollut. 2010;214:163–174. doi: 10.1007/s11270-010-0412-2. DOI

Kodešová R, Grabic R, Kočárek M, Klement A, Golovko O, Fér M, Nikodem A, Jakšík O. Pharmaceuticals’ sorptions relative to properties of thirteen different soils. Sci Total Environ. 2015;511:435–443. doi: 10.1016/j.scitotenv.2014.12.088. PubMed DOI

Kuppusamy S, Kakarla D, Venkateswarlu K, Megharaj M, Yoon Y-E, Lee YB. Veterinary antibiotics (VAs) contamination as a global agro-ecological issue: a critical view. Agr Ecosyst Environ. 2018;257:47–59. doi: 10.1016/j.agee.2018.01.026. DOI

Li Y, He J, Qi H, Li H, Boyd SA, Zhang W. Impact of biochar amendment on the uptake, fate and bioavailability of pharmaceuticals in soil-radish systems. J Hazard Mater. 2020;398:122852. doi: 10.1016/j.jhazmat.2020.122852. PubMed DOI

Marti E, Balcázar JL. Real-time PCR assays for quantification of qnr genes in environmental water samples and chicken feces. Appl Environ Microbiol. 2013;79:1743–1745. doi: 10.1128/aem.03409-12. PubMed DOI PMC

Martinez M, McDermott P, Walker R. Pharmacology of the fluoroquinolones: a perspective for the use in domestic animals. Vet J. 2006;172:10–28. doi: 10.1016/j.tvjl.2005.07.010. PubMed DOI

Mohring SAI, Strzysch I, Fernandes MR, Kiffmeyer TK, Tuerk J, Hamscher G. Degradation and elimination of various sulfonamides during anaerobic fermentation: a promising step on the way to sustainable pharmacy? Environ Sci Technol. 2009;43:2569–2574. doi: 10.1021/es802042d. PubMed DOI

Mompelat S, Jaffrezic A, Jardé E, Le Bot B. Storage of natural water samples and preservation techniques for pharmaceutical quantification. Talanta. 2013;109:31–45. doi: 10.1016/j.talanta.2013.01.042. PubMed DOI

Motoyama M, Nakagawa S, Tanoue R, Sato Y, Nomiyama K, Shinohara R. Residues of pharmaceutical products in recycled organic manure produced from sewage sludge and solid waste from livestock and relationship to their fermentation level. Chemosphere. 2011;84:432–438. doi: 10.1016/j.chemosphere.2011.03.048. PubMed DOI

Mu Q, Li J, Sun Y, Mao D, Wang Q, Luo Y. Occurrence of sulfonamide-, tetracycline-, plasmid-mediated quinolone- and macrolide-resistance genes in livestock feedlots in Northern China. Environ Sci Pollut Res. 2014;22:6932–6940. doi: 10.1007/s11356-014-3905-5. PubMed DOI

Murray CJL, Ikuta KS, Sharara F, et al. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet. 2022;399:629–655. doi: 10.1016/S0140-6736(21)02724-0. PubMed DOI PMC

Niemi L, Taggart M, Boyd K, Zhang Z, Gaffney PPJ, Pfleger S, Gibb S (2020) Assessing hospital impact on pharmaceutical levels in a rural ‘source-to-sink’ water system. Sci Total Environ 737:139618. 10.1016/j.scitotenv.2020.139618 PubMed

Pan M, Chu LM. Adsorption and degradation of five selected antibiotics in agricultural soil. Sci Total Environ. 2016;545–546:48–56. doi: 10.1016/j.scitotenv.2015.12.040. PubMed DOI

Pan M, Chu LM. Fate of antibiotics in soil and their uptake by edible crops. Sci Total Environ. 2017;599–600:500–512. doi: 10.1016/j.scitotenv.2017.04.214. PubMed DOI

Parente CET, Azeredo A, Vollú RE, Zonta E, Azevedo-Silva CE, Brito EMS, Seldin L, Torres JPM, Meire RO, Malm O. Fluoroquinolones in agricultural soils: multi-temporal variation and risks in Rio de Janeiro upland region. Chemosphere. 2019;219:409–417. doi: 10.1016/j.chemosphere.2018.11.184. PubMed DOI

Parente CET, Brito EMS, Azeredo A, Meire RO, Malm O (2019a) Fluoroquinolone antibiotics and their interactions in agricultural soils – a review. Orbital: Electron J Chem. 10.17807/orbital.v11i1.1352

Park CH, Robicsek A, Jacoby GA, Sahm D, Hooper DC. Prevalence in the United States of aac(6 ′ ) - Ib - cr encoding a ciprofloxacin-modifying enzyme. Antimicrob Agents Chemother. 2006;50:3953–3955. doi: 10.1128/aac.00915-06. PubMed DOI PMC

Petrovic M. Methodological challenges of multi-residue analysis of pharmaceuticals in environmental samples. Trends Environ Anal Chem. 2014;1:e25–e33. doi: 10.1016/j.teac.2013.11.004. DOI

Pikkemaat MG, Yassin H, Fels-Klerx HJ, Berendsen BJA (2016) Antibiotic residues and resistance in the environment. RIKILT-report, no. 2016.009, RIKILT, Wageningen. 10.18174/388253

Pino MR, Val J, Mainar AM, Zuriaga E, Español C, Langa E. Acute toxicological effects on the earthworm Eisenia fetida of 18 common pharmaceuticals in artificial soil. Sci Total Environ. 2015;518–519:225–237. doi: 10.1016/j.scitotenv.2015.02.080. PubMed DOI

Pourcher A-M, Jadas-Hécart A, Cotinet P, Dabert P, Ziebal C, Le Roux S, Moraru R, Heddadj D, Kempf I. Effect of land application of manure from enrofloxacin-treated chickens on ciprofloxacin resistance of Enterobacteriaceae in soil. Sci Total Environ. 2014;482–483:269–275. doi: 10.1016/j.scitotenv.2014.02.136. PubMed DOI

Qassim B, Razzak AA, Kamil GM, Heino MM, Morabito D (2020) Quantitative determination of fluoroquinolones in contaminated soils by HPLC with solid-phase extraction. Baghdad Sci J 17:0048. 10.21123/bsj.2020.17.1.0048

Qian X, Wang Z, Zhang H, Gu H, Shen G (2022) Occurrence of veterinary antibiotics in animal manure, compost, and agricultural soil, originating from different feedlots in suburbs of Shanghai, East China. Environ Monit Assess 194:379. 10.1007/s10661-022-10010-1 PubMed

Quaik S, Embrandiri A, Ravindran B, Hossain K, Al-Dhabi NA, Arasu MV, Ignacimuthu S, Ismail N. Veterinary antibiotics in animal manure and manure laden soil: scenario and challenges in Asian countries. J King Saud Univ - Sci. 2020;32:1300–1305. doi: 10.1016/j.jksus.2019.11.015. DOI

Rakonjac N, van der Zee SEATM, Wipfler L, Roex E, Kros H. Emission estimation and prioritization of veterinary pharmaceuticals in manure slurries applied to soil. Sci Total Environ. 2022;815:152938. doi: 10.1016/j.scitotenv.2022.152938. PubMed DOI

Rehman MSU, Rashid N, Ashfaq M, Saif A, Ahmad N, Han J-I. Global risk of pharmaceutical contamination from highly populated developing countries. Chemosphere. 2015;138:1045–1055. doi: 10.1016/j.chemosphere.2013.02.036. PubMed DOI

Reyes-Herrera I, Schneider MJ, Blore PJ, Donoghue DJ. The relationship between blood and muscle samples to monitor for residues of the antibiotic enrofloxacin in chickens. Poult Sci. 2011;90:481–485. doi: 10.3382/ps.2010-01057. PubMed DOI

Rusu A, Hancu G, Uivaroşi V. Fluoroquinolone pollution of food, water and soil, and bacterial resistance. Environ Chem Lett. 2014;13:21–36. doi: 10.1007/s10311-014-0481-3. DOI

Sanford JC, Mackie RI, Koike S, Krapac IG, Lin Y, Yannarell AC, Maxwell S, Aminov RI. Fate and transport of antibiotic residues and antibiotic resistance genes following land application of manure waste. J Environ Qual. 2009;38:1086–1108. doi: 10.2134/jeq2008.0128. PubMed DOI

Schlüsener MP, Bester K. Persistence of antibiotics such as macrolides, tiamulin and salinomycin in soil. Environ Pollut. 2006;143:565–571. doi: 10.1016/j.envpol.2005.10.049. PubMed DOI

Silva JJ, Silva BF, Stradiotto NR, Petrovic M, Gago-Ferrero P, Gros M. Pressurized Liquid Extraction (PLE) and QuEChERS evaluation for the analysis of antibiotics in agricultural soils. MethodsX. 2020;7:101171. doi: 10.1016/j.mex.2020.101171. PubMed DOI PMC

Slana M, Sollner-Dolenc M. Enrofloxacin degradation in broiler chicken manure under various laboratory conditions. Environ Sci Pollut Res. 2015;23:4422–4429. doi: 10.1007/s11356-015-5624-y. PubMed DOI

Slana M, Žigon D, Sollner-Dolenc M. Enrofloxacin degradation in broiler chicken manure under field conditions and its residuals effects to the environment. Environ Sci Pollut Res. 2017;24:13722–13731. doi: 10.1007/s11356-017-8722-1. PubMed DOI

Solliec M, Roy-Lachapelle A, Gasser M-O, Coté C, Généreux M, Sauvé S. Fractionation and analysis of veterinary antibiotics and their related degradation products in agricultural soils and drainage waters following swine manure amendment. Sci Total Environ. 2016;543:524–535. doi: 10.1016/j.scitotenv.2015.11.061. PubMed DOI

Song W, Guo M (2014) Residual veterinary pharmaceuticals in animal manures and their environmental behaviors in soils. In: He Z, Zhang H (eds) Applied manure and nutrient chemistry for sustainable agriculture and environment. Springer, Dordrecht. 10.1007/978-94-017-8807-6_2

Strahilevitz J, Jacoby GA, Hooper DC, Robicsek A. Plasmid-mediated quinolone resistance: a multifaceted threat. Clin Microbiol Rev. 2009;22:664–689. doi: 10.1128/cmr.00016-09. PubMed DOI PMC

Sun J, Zeng Q, Tsang DCW, Zhu LZ, Li XD. Antibiotics in the agricultural soils from the Yangtze River Delta, China. Chemosphere. 2017;189:301–308. doi: 10.1016/j.chemosphere.2017.09.040. PubMed DOI

Temmerman R, Pelligand L, Schelstraete W, Antonissen G, Garmyn A, Devreese M. Enrofloxacin dose optimization for the treatment of colibacillosis in broiler chickens using a drinking behaviour pharmacokinetic model. Antibiotics. 2021;10:604. doi: 10.3390/antibiotics10050604. PubMed DOI PMC

Turiel E, Martín-Esteban A, Tadeo JL. Multiresidue analysis of quinolones and fluoroquinolones in soil by ultrasonic-assisted extraction in small columns and HPLC-UV. Anal Chim Acta. 2006;562:30–35. doi: 10.1016/j.aca.2006.01.054. DOI

Uslu MÖ, Yediler A, Balcıoğlu IA, Schulte-Hostede S. Analysis and sorption behavior of fluoroquinolones in solid matrices. Water Air Soil Pollut. 2007;190:55–63. doi: 10.1007/s11270-007-9580-0. DOI

Veldman K, Cavaco LM, Mevius D, et al. International collaborative study on the occurrence of plasmid-mediated quinolone resistance in Salmonella enterica and Escherichia coli isolated from animals, humans, food and the environment in 13 European countries. J Antimicrob Chemother. 2011;66:1278–1286. doi: 10.1093/jac/dkr084. PubMed DOI

Wang F, Fu Y-H, Sheng H-J, Topp E, Jiang X, Zhu Y-G, Tiedje JM. Antibiotic resistance in the soil ecosystem: a one health perspective. Curr Opin Environ Sci Health. 2021;20:100230. doi: 10.1016/j.coesh.2021.100230. DOI

Wei R, Ge F, Zhang L, Hou X, Cao Y, Gong L, Chen M, Wang R, Bao E. Occurrence of 13 veterinary drugs in animal manure-amended soils in Eastern China. Chemosphere. 2016;144:2377–2383. doi: 10.1016/j.chemosphere.2015.10.126. PubMed DOI

Xu Y, Yu W, Ma Q, Zhou H. Occurrence of (fluoro)quinolones and (fluoro)quinolone resistance in soil receiving swine manure for 11 years. Sci Total Environ. 2015;530–531:191–197. doi: 10.1016/j.scitotenv.2015.04.046. PubMed DOI

Xu Y, Li H, Shi R, Lv J, Li B, Yang F, Zheng X, Xu J. Antibiotic resistance genes in different animal manures and their derived organic fertilizer. Environ Sci Eur. 2020 doi: 10.1186/s12302-020-00381-y. DOI

Yamane K, Wachino J, Suzuki S, Arakawa Y. Plasmid-mediated qepA gene among Escherichia coli clinical isolates from Japan. Antimicrob Agents Chemother. 2008;52:1564–1566. doi: 10.1128/aac.01137-07. PubMed DOI PMC

Yang L, Wu L, Liu W, Huang Y, Luo Y, Christie P. Dissipation of antibiotics in three different agricultural soils after repeated application of biosolids. Environ Sci Pollut Res. 2016;25:104–114. doi: 10.1007/s11356-016-8062-6. PubMed DOI

Yu Z, Yediler A, Yang M, Schulte-Hostede S. Leaching behavior of enrofloxacin in three different soils and the influence of a surfactant on its mobility. J Environ Sci. 2012;24:435–439. doi: 10.1016/s1001-0742(11)60771-7. PubMed DOI

Zeri M, Alvalá RS, Carneiro R, Cunha-Zeri G, Costa J, Rossato Spatafora L, Urbano D, Vall-Llossera M, Marengo J. Tools for communicating agricultural drought over the Brazilian semiarid using the soil moisture index. Water. 2018;10:1421. doi: 10.3390/w10101421. DOI

Zhang H, Luo Y, Wu L, Huang Y, Christie P. Residues and potential ecological risks of veterinary antibiotics in manures and composts associated with protected vegetable farming. Environ Sci Pollut Res. 2014;22:5908–5918. doi: 10.1007/s11356-014-3731-9. PubMed DOI

Zhao L, Dong YH, Wang H. Residues of veterinary antibiotics in manures from feedlot livestock in eight provinces of China. Sci Total Environ. 2010;408:1069–1075. doi: 10.1016/j.scitotenv.2009.11.014. PubMed DOI