Assessment of phytotoxicity and impact on the enzymatic activity of soil microorganisms caused by veterinary antibiotics used in Brazilian farms

References

• ABCS (Associação Brasileira de Criadores de Suínos). Integral Technical Coordination for Animal Production Solutions. Pig production: Theory and practice (Coordenação Técnica Integral das Soluções em Produção Animal. Produção de suínos: Teoria e prática). Brasília, DF, Brazil, 2014.
   Google Scholar
• Smith, T. C.; Gebreyes, W. A.; Abley, M. J.; Harper, A. L.; Forshey, B. M.; Male, M. J.; Martin, H. W.; Molla, B. Z.; Sreevatsan, S.; Thakur, S.; et al. Methicillin-Resistant Staphylococcus aureus in Pigs and Farm Workers on Conventional and Antibiotic-Free Swine Farms in the USA. PLoS One 2013, 8, e63704. DOI: 10.1371/journal.pone.0063704.
   PubMed Web of Science ®Google Scholar
• Chantziaras, I.; Boyen, F.; Callens, B.; Dewulf, J. Correlation between Veterinary Antimicrobial Use and Antimicrobial Resistance in Food-Producing Animals: A Report on Seven Countries. J. Antimicrob. Chemother. 2014, 69, 827–834. DOI: 10.1093/jac/dkt443.
   PubMed Web of Science ®Google Scholar
• Van Boeckel, T. P.; Brower, C.; Gilbert, M.; Grenfell, B. T.; Levin, S. A.; Robinson, T. P.; Teillant, A.; Laxminarayan, R. Global Trends in Antimicrobial Use in Food Animals. Proc. Natl. Acad. Sci. USA. 2015, 112, 5649–5654. DOI: 10.1073/pnas.1503141112.
   PubMed Web of Science ®Google Scholar
• Stone, J. J.; Dreis, E. K.; Lupo, C. D.; Clay, S. A. Land Application of Tylosin and Chlortetracycline Swine Manure: Impacts to Soil Nutrients and Soil Microbial Community Structure. J. Environ. Sci. Health B 2011, 46, 752–763. DOI: 10.1080/03601234.2011.603988.
   PubMed Web of Science ®Google Scholar
• Popova, I. E.; Josue, R. D. R.; Deng, S.; Hattey, J. A. Tetracycline Resistance in Semi-Arid Agricultural Soils Unde Rlong-Term Swine Effluent Application. J. Environ. Sci. Health B 2017, 52, 298–305. DOI: 10.1080/03601234.2017.1281639.
   PubMed Web of Science ®Google Scholar
• Cycoń, M.; Mrozik, A.; Piotrowska-Seget, Z. Antibiotics in the Soil Environment—Degradation and Their Impact on Microbial Activity and Diversity. Front Microbiol. 2019, 10, 338. DOI: 10.3389/fmicb.2019.00338.
   PubMed Web of Science ®Google Scholar
• Sarker, Y. A.; Rashid, S. Z.; Sachi, S.; Ferdous, J.; Chowdhury, B. L. D.; Tarannum, S. S.; Sikder, M. H. Exposure Pathways and Ecological Risk Assessment of Common Veterinary Antibiotics in the Environment through Poultry Litter in Bangladesh. J. Environ. Sci. Health B 2020, 55, 1061–1068. DOI: 10.1080/03601234.2020.1816090.
   PubMed Web of Science ®Google Scholar
• Spinosa, H. S.; Górniak, S. L.; Palermo-Neto, J. Medicamentos em Animais de Produção. Editora Roca: São Paulo, Brazil, 2014.
   Google Scholar
• Zhao, L.; Dong, Y. H.; 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 Web of Science ®Google Scholar
• Ding, C.; He, J. Effect of Antibiotics in the Environment on Microbial Populations. Appl. Microbiol. Biotechnol. 2010, 87, 925–941. DOI: 10.1007/s00253-010-2649-5.
   PubMed Web of Science ®Google Scholar
• Moura, S. C. N. Identificação e Perfil de Susceptibilidade a Antimicrobianos de Bactérias Isoladas de Biodigestores Anaeróbios Operados Com Dejetos Suínos e Com Dejetos Bovinos. Dissertação. Mestrado Profissional em Ciência e Tecnologia Do Leite e Derivados, EPAMIG: Juiz de Fora, Brazil, 2017.
   Google Scholar
• Schneider, M. C.; Aguilera, X. P.; Smith, R. M.; Moynihan, M. J.; Barbosa da Silva, J.; Jr, Aldighieri, S.; Almirón, M. Importance of Animal/Human Health Interface in Potential Public Health Emergencies of International Concern in the Americas. Rev. Panam Salud Publ. 2011, 29, 371–379. DOI: 10.1590/s1020-49892011000500011.
   PubMed Web of Science ®Google Scholar
• Scaldaferri, L. G.; Tameirão, E. R.; Flores, S. A.; Neves, R. A. S. C.; Correia, T. S.; Carmo, J. R.; Toma, H. S.; Ferrante, M. Formas de resistência microbiana e estratégias Para minimizar sua ocorrência na terapia antimicrobiana: Revisão. PUBVET 2020, 14, 1–10. DOI: 10.31533/pubvet.v14n8a621.1-10.
   Google Scholar
• Gianfreda, L.; Rao, M. A.; Piotrowska, A.; Palumbo, G.; Colombo, C. Soil Enzyme Activities as Affected by Anthropogenic Alterations: Intensive Agricultural Practices and Organic Pollution. Sci. Total Environ. 2005, 341, 265–279. DOI: 10.1016/j.scitotenv.2004.10.005.
   PubMed Web of Science ®Google Scholar
• Lebrun, J. D.; Trinsoutrot-Gattin, I.; Vinceslas-Akpa, M.; Bailleul, C.; Brault, A.; Mougin, C.; Laval, K. Assessing Impacts of Copper on soil enzyme Activities in Regard to Their Natural Spatio-Temporal Variation under Long-Term Different Land Uses. Soil Biol. Biochem. 2012, 49, 150–156. DOI: 10.1016/j.soilbio.2012.02.027.
   Web of Science ®Google Scholar
• Fang, H.; Han, Y. L.; Yin, Y. M.; Jin, X. X.; Wang, S. Y.; Tang, F. F.; Cai, L.; Yu, Y. L. Microbial Response to Repeated Treatments of Manure Containing Sulfadiazine and Chlortetracycline in Soil. J. Environ. Sci. Health B 2014, 49, 609–615. DOI: 10.1080/03601234.2014.911592.
   PubMed Web of Science ®Google Scholar
• Schnürer, J.; Rosswall, T. Fluorescein Diacetate Hydrolysis as a Measure of Total Microbial Activity in Soil and Litter. Appl. Environ. Microbiol. 1982, 43, 1256–1261. DOI: 10.1128/aem.43.6.1256-1261.1982.
   PubMed Web of Science ®Google Scholar
• Green, S. V.; Stott, E. D.; Diack, M. Assay for Fluorescein Diacetate Hydrolytic Activity: Optimization for Soil Samples. Soil Biol. Biochem. 2006, 38, 693–701. DOI: 10.1016/j.soilbio.2005.06.020.
   Web of Science ®Google Scholar
• Knapp, C. W.; Dolfing, J.; Ehlert, P. A. I.; Graham, D. W. Evidence of Increasing Antibiotic Resistance Gene Abundances in Archived Soils since 1940. Environ. Sci. Technol. 2010, 44, 580–587. DOI: 10.1021/es901221x.
   PubMed Web of Science ®Google Scholar
• Tasho, R. P.; Cho, J. Y. Veterinary Antibiotics in Animal Waste, Its Distribution in Soil and Uptake by Plants: A Review. Sci. Total Environ. 2016, 563, 366–376.
   PubMed Web of Science ®Google Scholar
• Lyubenova, M.; Dineva, S.; Georgieva, N.; Miteva, T.; Karadjova, I.; Parvanova, P. Ecotoxicological Assessment Model of Cultural Plant-Soil Complex Treated with Wastewater. Biotechnol. Biotechnol. Equip. 2012, 26, 2883–2893. DOI: 10.5504/BBEQ.2011.0158.
   Web of Science ®Google Scholar
• Radetski, C. M.; Cotelle, S.; Férard, J.-F. Classical and Biochemical Endpoints in the Evaluation of Phytotoxic Effects Caused by the Herbicide Trichloroacetate. Environ. Exp. Bot. 2000, 44, 221–229. DOI: 10.1016/s0098-8472(00)00069-1.
   PubMed Web of Science ®Google Scholar
• Wang, W. Literature Review on Higher Plants for Toxicity Testing. Water. Air. Soil Pollut. 1991, 59, 381–400. DOI: 10.1007/BF00211845.
   Web of Science ®Google Scholar
• Gorsuch, J. W.; Lower, W. R.; Lewis, M. A.; Wang, W. Plants for Toxicity Assessment, Vol. 2, ASTM STP 1115; ASTM: West Conshohocken, PA, 1991.
   Google Scholar
• Santos, H. G. d.; Jacomine, P. K. T.; Anjos, L. H. C. D.; Oliveira, V. A. D.; Lumbreras, J. F.; Coelho, M. R.; Almeida, J. A. D.; Araujo Filho, J. D.; Oliveira, J. B. D.; Cunha, T. J. F. 2018. Sistema Brasileiro De Classificação De Solos. Embrapa: Brasília, Brasil.
   Google Scholar
• BRASIL. Normative Instruction n° 41. National Program for the Prevention and Control of Antimicrobial Resistance in Agriculture – AgroPrevine (in Portuguese), 23 October 2017. http://www.in.gov.br/materia/-/asset_publisher/Kujrw0TZC2Mb/content/id/19401380/do1-2017-11-09-instrucao-normativa-n-41-de-23-de-outubro-de-2017-19401312 (Accessed December 11, 2021).
   Google Scholar
• BRASIL. List of prohibited substances and corresponding legislation (in Portuguese). 2020. https://www.gov.br/agricultura/pt-br/assuntos/insumos-agropecuarios/insumos-pecuarios/alimentacao-animal/aditivos (Accessed December 15, 2021).
   Google Scholar
• Andreotti, R.; Nicodemo, M. L. F. Uso de Antimicrobianos na Produção de Bovinos e Desenvolvimento de Resistência, 1st ed.; Embrapa Gado de Corte, Campo Grande, Brazil, 2004.
   Google Scholar
• Melo, W.; De, O.; Sousa, E. S.; Dos Santos, R. C. B. Feed Additives for Beef Cattle in Brazil (in Portuguese). Nutritime Revista Eletrônica 2018, 15, 8182–8190. http://www.nutritime.com.br/arquivos_internos/artigos/Artigo_469.pdf.
   Google Scholar
• Laurent, J. W. Alternatives to Common Preventive Uses of Antibiotics for Cattle, Swine and Chickens. Natural Resources Defense Council 2018, 1, 1–33. https://www.nrdc.org/resources/alternatives-common-preventive-uses-ntibiotics-cattle-swine-and-chickens.
   Google Scholar
• Prosser, R. S.; Sibley, P. K. Human Health Risk Assessment of Pharmaceuticals and Personal Care Products in Plant Tissue Due to Biosolids and Manure Amendments, and Wastewater Irrigation. Environ. Int. 2015, 75, 223–233. DOI: 10.1016/j.envint.2014.11.020.
   PubMed Web of Science ®Google Scholar
• Postma, M.; Backhans, A.; Collineau, L.; Loesken, S.; Sjolund, M.; Belloc, C.; Emanuelson, U.; Beilage, E. G.; Nielsen, E. O.; Stark, K. D. C.; Dewulf, J. Evaluation of the Relationship between the Biosecurity Status, Production Parameters, Herd Characteristics and Antimicrobial Usage in Farrow-to-Finish Pig Production in Four EU Countries. Porc. Health Manag. 2016, 2, 9.
   PubMed Web of Science ®Google Scholar
• CDC. Antibiotic resistance threats in the United States. Center for Disease Control, Department of Health and Human Services, Atlanta, GA, 2019.
   Google Scholar
• You, Y.; Silbergeld, E. K. Learning from Agriculture: Understanding Low-Dose Antimicrobials as Drivers of Resistome Expansion. Front. Microbiol. 2014, 4, 1–10.
   Google Scholar
• Barton, M. D. Impact of Antibiotic Use in the Swine Industry. Curr. Opin. Microbiol. 2014, 19, 9–15. DOI: 10.1016/j.mib.2014.05.017.
   PubMed Web of Science ®Google Scholar
• Li, C.; Jiang, C.; Wu, Z.; Cheng, B.; An, X.; Wang, H.; Sun, Y.; Huang, M.; Chen, X.; Wang, J. Diversity of Antibiotic Resistance Genes and Encoding Ribosomal Protection Proteins Gene in Livestock Waste Polluted Environment. J. Environ. Sci. Health B 2018, 53, 423–433. DOI: 10.1080/03601234.2018.1438836.
   PubMed Web of Science ®Google Scholar
• Pantosti, A. Methicillin-Resistant Staphylococcus aureus Associated with Animals and Its Relevance to Human Health. Front. Microbiol. 2012, 3, 1–11.
   PubMed Web of Science ®Google Scholar
• Adam, G.; Duncan, H. Development of a Sensitive and Rapid Method for the Measurement of Total Microbial Activity Using Fluorescein Diacetate (FDA) in a Range of Soils. Soil Biol. Biochem. 2001, 33, 943–951. DOI: 10.1016/S0038-0717(00)00244-3.
   Web of Science ®Google Scholar
• Kotzerke, A.; Hammesfahr, U.; Kleineidam, K.; Lamshoft, M.; Thiele-Bruhn, S.; Schloter, M.; Wilke, B. M. Influence of Difloxacin-Contaminated Manure on Microbial Community Structure and Function in Soils. Biol. Fertil. Soils 2011, 47, 177–186. DOI: 10.1007/s00374-010-0517-1.
   Web of Science ®Google Scholar
• Reichel, R.; Rosendahl, I.; Peeters, E. T. H. M.; Focks, A.; Groeneweg, J.; Bierl, R.; Schlichting, A.; Amelung, W.; Thiele-Bruhn, S. Effects of Slurry from Sulfadiazine- (SDZ) and Difloxacin- (DIF) Medicated Pigs on the Structural Diversity of Microorganisms in Bulk and Rhizosphere Soil. Soil Biol. Biochem. 2013, 62, 82–91. DOI: 10.1016/j.soilbio.2013.03.007.
   Web of Science ®Google Scholar
• Yuan, Z.; Liu, H.; Han, J.; Sun, J.; Wu, X.; Yao, J. Monitoring Soil Microbial Activities in Different Cropping Systems Using Combined Methods. Pedosphere 2017, 27, 138–146. DOI: 10.1016/S1002-0160(15)60100-X.
   Web of Science ®Google Scholar
• Braschi, I.; Blasioli, S.; Fellet, C.; Lorenzini, R.; Garelli, A.; Pori, M.; Giacomini, D. Persistence and Degradation of New β-Lactam Antibiotics in the Soil and Water Environment. Chemosphere 2013, 93, 152–159. DOI: 10.1016/j.chemosphere.2013.05.016.
   PubMed Web of Science ®Google Scholar
• Picó, Y.; Andreu, V. Fluoroquinolones in Soil - Risks and Challenges. Anal. Bioanal. Chem. 2007, 387, 1287–1299. DOI: 10.1007/s00216-006-0843-1.
   PubMed Web of Science ®Google Scholar
• Pan, M.; Chu, L. M. Phytotoxicity of Veterinary Antibiotics to Seed Germination and Root Elongation of Crops. Ecotoxicol. Environ. Saf. 2016, 126, 228–237. DOI: 10.1016/j.ecoenv.2015.12.027.
   PubMed Web of Science ®Google Scholar
• Gottschall, N.; Topp, E.; Metcalfe, C.; Edwards, M.; Payne, M.; Kleywegt, S.; Russell, P.; Lapen, D. R. Pharmaceutical and Personal Care Products in Groundwater, Subsurface Drainage, Soil, and Wheat Grain, following a High Single Application of Municipal Biosolids to a Field. Chemosphere 2012, 87, 194–203. DOI: 10.1016/j.chemosphere.2011.12.018.
   PubMed Web of Science ®Google Scholar
• Scherer, E. E.; Nesi, C. N.; Massotti, Z. Atributos Químicos Do Solo Influenciados Por Sucessivas Aplicações de Dejetos Suínos em Áreas Agrícolas de Santa Catarina. Rev. Bras. Ciênc. Solo 2010, 34, 1375–1383. DOI: 10.1590/S0100-06832010000400034.
   Web of Science ®Google Scholar
• Risse, L. M.; Cabrera, M. L.; Franzluebbers, A. J.; Gaskin, J. W.; Gilley, J. E.; Killorn, R.; Radcliffe, D. E.; Tollner, W. E.; Zhang, H. Land Application of Manure for Beneficial Reuse. In Animal Agriculture and the Environment, National Center for Manure and Animal Waste Management White Papers, Rice, J. M.; Caldwell, D. F.; Humenik, F. J., Eds.; American Society of Agricultural and Biological Engineers: St. Joseph, MI, 2006; pp. 283–316. DOI: 10.13031/2013.20257.
   Google Scholar
• Yang, Q.; Wang, R.; Ren, S.; Szoboszlay, M.; Moe, L. A. Practical Survey on Antibiotic-Resistant Bacterial Communities in Livestock Manure and Manure-Amended Soil. J. Environ. Sci. Health B 2016, 51, 14–23. DOI: 10.1080/03601234.2015.1080481.
   PubMed Web of Science ®Google Scholar
• Singer, A. C.; Shaw, H.; Rhodes, V.; Hart, A. Review of Antimicrobial Resistance in the Environment and Its Relevance to Environmental Regulators. Front. Microbiol. 2016, 7, 1–22. DOI: 10.3389/fmicb.2016.01728.
   PubMed Web of Science ®Google Scholar
• Martínez-Carballo, E.; González-Barreiro, C.; Scharf, S.; Gans, O. Environmental Monitoring Study of Selected Veterinary Antibiotics in Animal Manure Ands Oils in Austria. Environ. Pollut. 2007, 148, 570–579. DOI: 10.1016/j.envpol.2006.11.035.
   PubMed Web of Science ®Google Scholar
• Kemper, N. Veterinary Antibiotics in the Aquatic and Terrestrial Environment. Ecol. Ind. 2008, 8, 1–13. DOI: 10.1016/j.ecolind.2007.06.002.
   Web of Science ®Google Scholar
• Subbiah, M.; Mitchell, M. S.; Ullman, J. L.; Call, D. R. β-Lactams and Florfenicol Antibiotics Remain Bioactive in Soils While Ciprofloxacin, Neomycin, and Tetracycline Are Neutralized. Appl. Environ. Microbiol. 2011, 77, 7255–7260. DOI: 10.1128/AEM.05352-11.
   PubMed Web of Science ®Google Scholar
• Bhatt, E.; Gauba, P. Impact of Antibiotics on Plants. Int. J. Pharm. Sci. Rev. Res. 2018, 52, 49–53.
   Google Scholar
• Wei, X.; Wu, S. C.; Nie, X. P.; Yediler, A.; Wong, M. H. The Effects of Residual Tetracycline on Soil Enzymatic Activities and Plant Growth. J. Environ. Sci. Health B 2009, 44, 461–471. DOI: 10.1080/03601230902935139.
   PubMed Web of Science ®Google Scholar
• Hillis, D. G.; Fletcher, J.; Solomon, K. R.; Sibley, P. K. Effects of Tem Antibiotics on Seed Germination and Root Elongation in Three Plant Species. Arch. Environ. Contam. Toxicol. 2011, 60, 220–232. DOI: 10.1007/s00244-010-9624-0.
   PubMed Web of Science ®Google Scholar