Occurrence of nine antibiotics in different kinds of sewage sludge, soils, corn and grapes after sludge spreading

  1. Ana Barreiro 1
  2. Raquel Cela-Dablanca 1
  3. Carolina Nebot 1
  4. Lucía Rodríguez-López 2
  5. Vanesa Santás-Miguel 2
  6. Manuel Arias-Estévez 2
  7. María Fernández-Sanjurjo 1
  8. Avelino Núñez-Delgado 1
  9. Esperanza Álvarez-Rodríguez 1
  1. 1 Universidade de Santiago de Compostela
    info

    Universidade de Santiago de Compostela

    Santiago de Compostela, España

    ROR https://ror.org/030eybx10

  2. 2 Universidade de Vigo
    info

    Universidade de Vigo

    Vigo, España

    ROR https://ror.org/05rdf8595

Journal:
Spanish Journal of Soil Science: SJSS

ISSN: 2253-6574

Year of publication: 2022

Volume: 12

Issue: 1

Type: Article

DOI: 10.3389/SJSS.2022.10741 DIALNET GOOGLE SCHOLAR lock_openDialnet editor

More publications in: Spanish Journal of Soil Science: SJSS

Sustainable development goals

Abstract

The huge worldwide use of antibiotics triggers the accumulation of these substances in sludge from wastewater treatment plants (WWTP) and the possible contamination of soils amended with it, as well as of crops growing in these soils. In this work we analyzed the presence of the antibiotics amoxicillin (AMO), cefuroxime (CEF), ciprofloxacin (CIP), clarithromycin (CLA), levofloxacin (LEV), lincomycin (LIN), norfloxacin (NOR), sulfadiazine (SUL), and trimethoprim (TRI), in sludge from different WWTPs in Galicia (NW Spain), as well as in sludge technically treated by waste-managers, in soils where treated sludge was applied, and in crops (corn and vineyard) growing in the amended areas. The antibiotics were quantified by means of high resolution HPLC-mass-chromatography. The results indicate that almost all the sludge samples contained antibiotics, being ciprofloxacin and levofloxacin the most abundant reaching maximum values of 623 and 893 ng/g, respectively. The sludge treatment significantly reduced the number and the concentrations of antibiotics. In 12% of the soil samples where sludge was applied, some antibiotics were detected, but always in small concentrations. Regarding the crops, no antibiotic was detected in the roots, stalk, leaves and grain of corn, neither in grapes sampled in vineyards. It can be concluded that the treatments currently applied in the WWTPs under study are not totally effective in removing antibiotics from the sludge, although the findings of this research suggest that the additional specific treatment of the sludge derived from these WWTPs is effective in reducing the risk of environmental pollution due to a variety of antibiotics, and specifically in the case of soils amended with these organic materials and crops growing on it.

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Bibliographic References

  • Al-Mustafa, Z. H., and Al-Ghamdi, M. S. (2000). Use of Norfloxacin in Poultry Production in the Eastern Province of Saudi Arabia and its Possible Impact on Public Health. Int. J. Environ. Health Res. 10, 291–299. doi:10.1080/0960312002001483
  • Aldeyab, M., López-Lozano, J. M., and Gould, I. M. (2020). “Global Antibiotics Use and Resistance,” in Global Pharmaceutical Policy. Editor Z. Babar (Singapore: Palgrave Macmillan), 331.
  • Alvarenga, P., Mourinha, C., Farto, M., Santos, T., Palma, P., Sengo, J., et al. (2015). Sewage Sludge, Compost and Other Representative Organic Wastes as Agricultural Soil Amendments: Benefits versus Limiting Factors. Waste Manag. 40, 44–52. doi:10.1016/j.wasman.2015.01.027
  • Aydın, S., Ulvi, A., Bedük, F., and Aydın, M. E. (2022). Pharmaceutical Residues in Digested Sewage Sludge: Occurrence, Seasonal Variation and Risk Assessment for Soil. Sci. Total Environ. 817, 152864. doi:10.1016/j.scitotenv.2021.152864
  • Azanu, D., Mortey, C., Darko, G., Juhl Weisser, J., Styrishave, B., and Abaidoo, R. C. (2016). Uptake of Antibiotics from Irrigation Water by Plants. Chemosphere 157, 107–114. doi:10.1016/j.chemosphere.2016.05.035
  • Bascomb, C. (1968). Distribution of Pyrophosphate-Extractable Iron and Organic Carbon in Soils of Various Groups. J. Soil Sci. 19, 251–268. doi:10.1111/j.1365-2389.1968.tb01538.x
  • Bassil, R. J., Bashour, , Sleiman, F. T., and Abou-Jawdeh, Y. A. (2013). Antibiotic Uptake by Plants from Manure-Amended Soils. J. Environ. Sci. Health Part B 48, 570–574. doi:10.1080/03601234.2013.774898
  • Behera, S. K., Kim, H. W., Oh, J. E., and Park, H. S. (2011). Occurrence and Removal of Antibiotics, Hormones and Several Other Pharmaceuticals in Wastewater Treatment Plants of the Largest Industrial City of Korea. Sci. Total Environ. 409, 4351–4360. doi:10.1016/j.scitotenv.2011.07.015
  • Blackmore, L. C. (1978). “Exchange Complex Dominated by Amorphous Material (ECDAM),” in The Andisol Proposal. Editor G. D. Smith (Lower Hutt, New Zealand: New Zealand Soil Bureau), 21.
  • Bruyndonckx, R., Adriaenssens, N., Versporten, A., Hens, N., Monnet, D. L., Molenberghs, G., et al. (2021). Consumption of Antibiotics in the Community, European Union/European Economic Area. J. Antim Chemo, 76. Supplement_2 ii7-ii13. doi:10.1093/jac/dkab172
  • Buta, M., Hubeny, J., Zieliński, W., Harnisz, M., and Korzeniewska, E. (2021). Sewage Sludge in Agriculture – the Effects of Selected Chemical Pollutants and Emerging Genetic Resistance Determinants on the Quality of Soil and Crops – a Review. Ecotoxicol. Environ. Saf. 214, 112070. doi:10.1016/j.ecoenv.2021.112070
  • Cela-Dablanca, R., Barreiro, A., López, L. R., Santás-Miguel, V., Arias-Estévez, M., Núñez-Delgado, A., et al. (2022). Relevance of Sorption in Bio-Reduction of Amoxicillin Taking Place in Forest and Crop Soils. Environ. Res. 208, 112753. doi:10.1016/j.envres.2022.112753
  • Cela-Dablanca, R., Nebot, C., López, L. R., Fernández-Calviño, D., Arias-Estévez, M., Núñez-Delgado, A., et al. (2021). Efficacy of Different Waste and By-Products from Forest and Food Industries in the Removal/retention of the Antibiotic Cefuroxime. Processes 9, 1151. doi:10.3390/pr9071151
  • Conde-Cid, M., Álvarez-Esmorís, C., Paradelo-Núñez, R., Nóvoa-Muñoz, J. C., Arias-Estévez, M., Álvarez-Rodríguez, E., et al. (2018). Ocurrence of Tetracyclines and Sulfonamides in Manures, Agricultural Soils and Crops from Different Areas in Galicia (NW Spain). J. Clean. Prod. 197, 491–500. doi:10.1016/j.jclepro.2018.06.217.2
  • Dolliver, H., Gupta, S., and Noll, S. (2008). Antibiotic Degradation during Manure Composting. J. Environ. Qual. 37, 1245–1253. doi:10.2134/jeq2007.0399
  • ECDC (2021). European Centre for Disease Prevention and Control. Antimicrobial Consumption in the EU/EEA (ESAC-Net). Stockholm: Annual Epidemiological Report 2020.
  • Eggen, T., Asp, T. N., Grave, K., and Hormazabal, V. (2011). Uptake and Translocation of Metformin, Ciprofloxacin and Narasin in Forage- and Crop Plants. Chemosphere 85, 26–33. doi:10.1016/j.chemosphere.2011.06.041
  • Ezzariai, A., Hafidi, M., Khadra, A., Aemig, Q., El Fels, L., Barret, M., et al. (2018). Human and Veterinary Antibiotics during Composting of Sludge or Manure: Global Perspectives on Persistence, Degradation, and Resistance Genes. J. Hazard. Mat. 359, 465–481. doi:10.1016/j.jhazmat.2018.07.092
  • Foged, H. L., Flotats, X., Blasi, A. B., Palatsi, J., Magri, A., and Schelde, K. M. (2011). “Inventory of Manure Processing Activities in Europe,”. Technical Report No. I in Concerning ‘Manure Processing Activities in Europe' to the European Commission (Directorate General Environment), 138
  • Gao, L., Shi, Y., Li, W., Niu, H., Liu, J., and Cai, Y. (2012). Occurrence of Antibiotics in Eight Sewage Treatment Plants in Beijing, China. Chemosphere 86, 665–671. doi:10.1016/j.chemosphere.2011.11.019
  • García-Galán, M. J., Diaz-Cruz, M. S., and Barceló, D. (2011). Occurrence of Sulfonamide Residues along the Ebro River Basin Removal in Wastewater Treatment Plants and Environmental Impact Assessment. Environ. Int. 37, 462–473. doi:10.1016/j.envint.2010.11.011
  • Gobel, A., Thomsen, A., McArdell, C. S., Joss, A., and Giger, W. (2005). Occurrence and Sorption Behavior of Sulfonamides, Macrolides, and Trimethoprim in Activated Sludge Treatment. Environ. Sci. Technol. 39, 3981–3989. doi:10.1021/es048550a
  • Golovko, O., Kumar, V., Fedorova, G., Randak, T., and Grabic, R. (2014). Seasonal Changes in Antibiotics, Antidepressants/psychiatric Drugs, Antihistamines and Lipid Regulators in a Wastewater Treatment Plant. Chemosphere 111, 418–426. doi:10.1016/j.chemosphere.2014.03.132
  • Gros, M., Mas-Pla, J., Boy-Roura, M., Geli, I., Domingo, F., and Petrović, M. (2019). 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. 654, 1337–1349. doi:10.1016/j.scitotenv.2018.11.061
  • Guitián Ojea, F., and Carballas, T. (1976). Técnicas de análisis de suelos. Spanish: Pico Sacro.
  • Henninger, E., Herrel, M., Strehl, E., and Kummer, K. (2001). “Emission of Pharmaceuticals, Contrast Media, Disinfectants, and AOX from Hospitals,” in Pharmaceuticals in the Environment Sources, Fate, Effects, and Risks (Berlin: Springer), 29–41.
  • Huang, F., An, Z., Moran, M. J., and Liu, F. (2020). Recognition of Typical Antibiotic Residues in Environmental Media Related to Groundwater in China (2009-2019). J. Hazard. Mat. 399, 122813. doi:10.1016/j.jhazmat.2020.122813
  • Ivanová, L., Mackuľak, T., Grabic, R., Golovko, O., Koba, O., Staňová, A. V., et al. (2018). Pharmaceuticals and Illicit Drugs - A New Threat to the Application of Sewage Sludge in Agriculture. Sci. Total Environ. 634, 606–615. doi:10.1016/j.scitotenv.2018.04.001
  • Jelic, A., Gros, M., Ginebreda, A., Cespedes-Sánchez, R., Ventura, F., Petrovic, M., et al. (2011). Occurrence, Partition and Removal of Pharmaceuticals in Sewage Water and Sludge during Wastewater Treatment. Water Res. 45, 1165–1176. doi:10.1016/j.watres.2010.11.010
  • Kamprath, E. (1970). Exchangeable Aluminum as a Criterion for Liming Leached Mineral Soils. Soil Sci. Soc. Am. J. 34, 252–254. doi:10.2136/sssaj1970.03615995003400020022x
  • Kang, D. H., Gupta, S., Rosen, C., Fritz, V., Singh, A., Chander, Y., et al. (2013). Antibiotic Uptake by Vegetable Crops from Manure-Applied Soils. J. Agric. Food Chem. 61, 9992–10001. doi:10.1021/jf404045m
  • Khadra, A., Ezzariai, A., Merlina, G., Capdeville, M. J., Budzinski, H., Hamdi, H., et al. (2019). Fate of Antibiotics Present in a Primary Sludge of WWTP during Their Co-composting with Palm Wastes. Waste Manag. 84, 13–19. doi:10.1016/j.wasman.2018.11.009
  • Kimosop, S. J., Getenga, Z. M., Orata, F., Okello, V. A., and Cheruiyot, J. K. (2016). Residue Levels and Discharge Loads of Antibiotics in Wastewater Treatment Plants (WWTPs), Hospital Lagoons, and Rivers within Lake Victoria Basin, Kenya. Environ. Monit. Assess. 188, 532. doi:10.1007/s10661-016-5534-6
  • Klein, E. Y., Van Boeckel, T., Martinez, E. M., Pant, S., Gandra, S., Levin, S. A., et al. (2018). Global Increase and Geographic Convergence in Antibiotic Consumption between 2000 and 2015. Proc. Natl. Acad. Sci. U. S. A. 115, E3463-E3470–E3470. doi:10.1073/pnas.1717295115
  • Kumar, K., Gupta, S. C., Baidoo, S. K., Chander, Y., and Rosen, C. J. (2005). Antibiotic Uptake by Plants from Soil Fertilized with Animal Manure. J. Environ. Qual. 34, 2082–2085. doi:10.2134/jeq2005.0026
  • Lange, F., Cornelissen, S., Kubac, D., Sein, M. M., von Sonntag, J., Hannich, C. B., et al. (2006). Degradation of Macrolide Antibiotics by Ozone: A Mechanistic Case Study with Clarithromycin. Chemosphere 65, 17–23. doi:10.1016/j.chemosphere.2006.03.014
  • Latosinska, J., Kowalik, R., and Gawdzik, J. (2021). Risk Assessment of Soil Contamination with Heavy Metals from Municipal Sewage Sludge. Appl. Sci. (Basel). 11, 548. doi:10.3390/app11020548
  • Loos, R., Carvalho, R., António, D. C., Comero, S., Locoro, G., Tavazzi, S., et al. (2013). EU-Wide Monitoring Survey on Emerging Polar Organic Contaminants in Wastewater Treatment Plant Effluents. Water Res. 47, 6475–6487. doi:10.1016/j.watres.2013.08.024
  • López Alonso, M., Benedito, J. L., Miranda, M., Fernández, J. A., Castillo, C., Hernández, J., et al. (2003). Large-scale Spatial Variation in Mercury Concentrations in Cattle in NW Spain. Environ. Pollut. 125, 173–181. doi:10.1016/S0269-7491(03)00073-3
  • MAMRM, (2009). Characterization of Wastewater Treatment Plants Sludge Genetared in Spain (In Spanish).” in Ministerio Medio Ambiente Y Medio Rural Y Marino.
  • Mao, Y., Cheng, L., Ma, B., and Cai, Y. (2016). The Fate of Mercury in Municipal Wastewater Treatment Plants in China: Significance and Implications for Environmental Cycling. J. Hazard. Mat. 306, 1–7. doi:10.1016/j.jhazmat.2015.11.058
  • Martínez-Orgániz, A., Becerril Bravo, J. E., Llompart, M., Dagnac, T., Lamas, J. P., Vázquez, L., et al. (2021). Emerging Pollutants and Antibiotics Removed by Conventional Activated Sludge Followed by Ultraviolet Radiation in a Municipal Wastewater Treatment Plant in Mexico. Wat Q. Res. J. 56, 167–179. doi:10.2166/wqrj.2021.013
  • Mcardell, C. S., Molnar, E., Suter, M. J. F., and Giger, W. (2003). Occurrence and Fate of Macrolide Antibiotics in Wastewater Treatment Plants and in the Glatt Valley Watershed, Switzerland. Environ. Sci. Technol. 37, 5479–5486. doi:10.1021/es034368i
  • Nas, B., Dolu, T., and Koyuncu, S. (2021). Behavior and Removal of Ciprofloxacin and Sulfamethoxazole Antibiotics in Three Different Types of Full-Scale Wastewater Treatment Plants: A Comparative Study. Water Air Soil Pollut. 232, 127. doi:10.1007/s11270-021-05067-6
  • Nguyen, A. Q., Vu, H. P., Nguyen, L. N., Wang, Q., Djordjevic, S. P., Donner, E., et al. (2021). Monitoring Antibiotic Resistance Genes in Wastewater Treatment: Current Strategies and Future Challenges. Sci. Total Environ. 783, 146964. doi:10.1016/j.scitotenv.2021.146964
  • Okuda, T., Yamashita, N., Tanaka, H., Matsukawa, H., and Tanabe, K. (2009). Development of Extraction Method of Pharmaceuticals and Their Occurrences Found in Japanese Wastewater Treatment Plants. Environ. Int. 35, 815–820. doi:10.1016/j.envint.2009.01.006
  • Olsen, S. R., and Sommers, L. E. (1982). “Phosphorus,” in Methods of Soil Analysis. Part 2. Chemical and Microbiological Properties. Editor A. L. Page (Madison, WI: Agronomy Monographs), 9.
  • Onchoke, K. K., Franclemont, C. M., and Weatherford, P. W. (2018). Structural Characterization and Evaluation of Municipal Wastewater Sludge (Biosolids) from Two Rural Wastewater Treatment Plants in East Texas, USA. Spectrochimica Acta Part A Mol. Biomol. Spectrosc. 204, 514–524. doi:10.1016/j.saa.2018.06.096
  • Onchoke, K. K., Oluwadamilola, O. F., Friedfeld, R. B., and Weatherford, P. W. (2022). Evaluation and Analysis of Perlite and Municipal Wastewater Sludge (Biosolids) from Three Wastewater Treatment Plants in East Texas, USA. Environ. Monit. Assess. 194, 121. doi:10.1007/s10661-022-09794-z
  • Östman, M., Lindberg, R. H., Fick, J., Björn, E., and Tysklind, M. (2017). Screening of Biocides, Metals and Antibiotics in Swedish Sewage Sludge and Wastewater. Water Res. 115, 318–328. doi:10.1016/j.watres.2017.03.011
  • Peech, L., Alexander, L. T., and Dean, L. A. (1947). Methods of Soil Analysis for Soil-Fertility Investigations. Washington D.C. USA: USDA Cir. N° 757.
  • Pereira, A. M. P. T., Silva, L. J. G., Rodrigues, J., Lino, C., and Pena, A. (2018). Risk Assessment of Fluoroquinolones from Poultry Muscle Consumption: Comparing Healthy Adult and Pre-school Populations. Food Chem. Toxicol. 118, 340–347. doi:10.1016/j.fct.2018.05.035
  • Rahube, T. O., Marti, R., Scott, A., Tien, Y. C., Murray, R., Sabourin, L., et al. (2016). Persistence of Antibiotic Resistance and Plasmid-Associated Genes in Soil Following Application of Sewage Sludge and Abundance on Vegetables at Harvest. Can. J. Microbiol. 62, 600–607. doi:10.1139/cjm-2016-0034
  • Rodríguez-López, L., Santás-Miguel, V., Núñez-Delgado, A., Álvarez-Rodríguez, E., Pérez-Rodríguez, P., and Arias-Estévez, M. (2022). Influence of pH, Humic Acids, and Salts on the Dissipation of Amoxicillin and Azithromycin under Simulated Sunlight. Span. J. Soil Sci. 12, 10438. doi:10.3389/sjss.2022.10438
  • Rutgersson, C., Ebmeyer, S., Lassen, S. B., Karkmana, A., Fick, J., Kristiansson, E., et al. (2020). Long-term Application of Swedish Sewage Sludge on Farmland Does Not Cause Clear Changes in the Soil Bacterial Resistome. Environ. Int. 137, 105339. doi:10.1016/j.envint.2019.105339
  • Sabri, N. A., van Holst, S., Schmitt, H., van der Zaan, B. M., Gerritsen, H. W., Rijnaarts, H. H. M., et al. (2020). Fate of Antibiotics and Antibiotic Resistance Genes during Conventional and Additional Treatment Technologies in Wastewater Treatment Plants. Sci. Total Environ. 741, 140199. doi:10.1016/j.scitotenv.2020.140199
  • Santás-Miguel, V., Díaz-Raviña, M., Martín, A., García-Campos, E., Barreiro, A., Núñez-Delgado, A., et al. (2020). Medium-term Influence of Tetracyclines on Total and Specific Microbial Biomass in Cultivated Soils of Galicia (NW Spain). Span. J. Soil Sci. 10, 217–232. doi:10.3232/SJSS.2020.V10.N3.05
  • Sarzynski, S. H., Warner, S., Sun, J., Matsouaka, R., Dekker, J. P., Babiker, A., et al. (2022). Trimethoprim-sulfamethoxazole versus Levofloxacin for Stenotrophomonas Maltophilia Infections: A Retrospective Comparative Effectiveness Study of Electronic Health Records from 154 US Hospitals. Open Forum Infect. Dis. 9, ofab644. doi:10.1093/ofid/ofab644
  • Sörme, L., Lindqvist, A., and Söderberg, H. (2003). Capacity to Influence Sources of Heavy Metals to Wastewater Treatment Sludge. Environ. Manage. 31, 421–428. doi:10.1007/s00267-002-2810-8
  • Spielmeyer, A. (2018). Occurrence and Fate of Antibiotics in Manure during Manure Treatments: A Short Review. Sustain. Chem. Pharm. 9, 76–86. doi:10.1016/j.scp.2018.06.004
  • Sriram, A., Kalanxhi, E., Kapoor, G., Craig, J., Balasubramanian, R., Brar, S., et al. (2021). State of the World'santibiotics 2021: A Global Analysis of Antimicrobial Resistance and its Drivers. Washington DC: Center for Disease Dynamics, Economics & Policy.
  • Tan, K. H. (1996). Soil Sampling, Preparation, and Analysis. New York, USA: Marcel Dekker.
  • Van Boeckel, T. P., Gandra, S., Ashok, A., Caudron, Q., Grenfell, B. T., Levin, S. A., et al. (2014). Global Antibiotic Consumption 2000 to 2010: an Analysis of National Pharmaceutical Sales Data. Lancet Infect. Dis. 14, 742–750. doi:10.1016/S1473-3099(14)70780-7
  • Verlicchi, P., Al Aukidy, M., and Zambello, E. (2012). Occurrence of Pharmaceutical Compounds in Urban Wastewater: Removal, Mass Load and Environmental Risk after a Secondary Treatment-A Review. Sci. Total Environ. 429, 123–155. doi:10.1016/j.scitotenv.2012.04.028
  • Verlicchi, P., and Zambello, E. (2015). Pharmaceuticals and Personal Care Products in Untreated and Treated Sewage Sludge: Occurrence and Environmental Risk in the Case of Application on Soil - A Critical Review. Sci. Total Environ. 538, 750–767. doi:10.1016/j.scitotenv.2015.08.108
  • Yi, S., Gao, B., Sun, Y., Wu, J., Shi, X., Wu, B., et al. (2016). Removal of Levofloxacin from Aqueous Solution Using Rice-Husk and Wood-Chip Biochars. Chemosphere 150, 694–701. doi:10.1016/j.chemosphere.2015.12.112
  • Zhou, L. J., Ying, G. G., Liu, S., Zhao, J. L., Yang, B., Chen, Z. F., et al. (2013). Occurrence and Fate of Eleven Classes of Antibiotics in Two Typical Wastewater Treatment Plants in South China. Sci. Total Environ. 452-453, 365–376. doi:10.1016/j.scitotenv.2013.03.010
  • Zuccato, E., Castiglioni, S., Bagnati, R., Melis, M., and Fanelli, R. (2010). Source, Occurrence and Fate of Antibiotics in the Italian Aquatic Environment. J. Hazard. Mat. 179, 1042–1048. doi:10.1016/j.jhazmat.2010.03.110
Data source: Dialnet