Fate of fluoroquinolones associated with antimicrobial resistance in circular periurban agriculture

Animal antibiotic use contributes to antimicrobial resistance (AMR) in humans. While animal manure benefits soil fertility, it also acts as hotspot for antibiotic residues, antibiotic-resistant bacteria, and their genes. Amending soils with poultry litter is recognized as “magic” among horticulture...

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Veröffentlicht in:The Science of the total environment 2024-12, Vol.955, p.176874, Article 176874
Hauptverfasser: Prack McCormick, Barbara, Knecht, Camila A., Sokolowski, Ana Clara, Palladino, Pablo Martín, Rojas, Dante Emanuel, Cristos, Diego Sebastián, Rivera, Hernan J., Gonçalves Vila Cova, Carola, De Grazia, Javier, Rodriguez, Hernán A., Tittonell, Pablo, Centrón, Daniela, Barrios, Monica B.
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container_title The Science of the total environment
container_volume 955
creator Prack McCormick, Barbara
Knecht, Camila A.
Sokolowski, Ana Clara
Palladino, Pablo Martín
Rojas, Dante Emanuel
Cristos, Diego Sebastián
Rivera, Hernan J.
Gonçalves Vila Cova, Carola
De Grazia, Javier
Rodriguez, Hernán A.
Tittonell, Pablo
Centrón, Daniela
Barrios, Monica B.
description Animal antibiotic use contributes to antimicrobial resistance (AMR) in humans. While animal manure benefits soil fertility, it also acts as hotspot for antibiotic residues, antibiotic-resistant bacteria, and their genes. Amending soils with poultry litter is recognized as “magic” among horticulture farmers and it remains a common practice globally. However, this poses a risk especially in countries where prophylactic use of antibiotics is allowed. In Argentina, fluoroquinolones are used in this way besides being listed as essential medicines and classified as “watch” by the World Health Organization. Antibiotic selective pressure can favour AMR in the environment but the fate of antibiotic residues and AMR dissemination from these practices remains poorly understood. Our research addresses this gap with a biological model tracing fluoroquinolones from poultry to soil to lettuce and tracking anthropogenic AMR with the proposed biomarker genes sul1 and intI1. Fresh poultry litter was stored for six months before application in a horticulture field experiment. The experiment included control and manured plots where lettuce was cultivated till harvest. Enrofloxacin concentration was 7.3 μg/kg in fresh poultry litter, while its metabolite ciprofloxacin was 39.22 μg/kg after storage. Although no fluoroquinolones were detected in soils, lettuce from manured plots contained enrofloxacin and ciprofloxacin at 14.97 and 9.77 μg/kg, respectively, providing evidence of fluoroquinolone bioaccumulation in plants. Abundance of sul1 and intI1 in poultry litter was not affected by storage. Manured soils showed better soil quality than controls, but sul1 gene abundance was 1.6 times higher, reaching 7.61 Log sul1/g soil. A less sensitive, but significant effect was registered for intI1. These findings show that static storage is insufficient to stop the transmission of antibiotics and AMR biomarkers from poultry to horticulture. Amending soil with industrial poultry litter contributes to pollution with these emergent contaminants and risks human antibiotic exposure through fresh vegetables. [Display omitted] •Fluoroquinolones and AMR pathway in circular periurban agriculture.•In an open-field experiment stored poultry litter (PL) is used as a soil amendment.•Lettuce accumulates enrofloxacin and ciprofloxacin from intensive animal husbandry.•PL improves soil quality but increases sul1 and intI1 gene abundance.•Soil amendment with PL contributes to fluoroquinolone pollution an
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While animal manure benefits soil fertility, it also acts as hotspot for antibiotic residues, antibiotic-resistant bacteria, and their genes. Amending soils with poultry litter is recognized as “magic” among horticulture farmers and it remains a common practice globally. However, this poses a risk especially in countries where prophylactic use of antibiotics is allowed. In Argentina, fluoroquinolones are used in this way besides being listed as essential medicines and classified as “watch” by the World Health Organization. Antibiotic selective pressure can favour AMR in the environment but the fate of antibiotic residues and AMR dissemination from these practices remains poorly understood. Our research addresses this gap with a biological model tracing fluoroquinolones from poultry to soil to lettuce and tracking anthropogenic AMR with the proposed biomarker genes sul1 and intI1. Fresh poultry litter was stored for six months before application in a horticulture field experiment. The experiment included control and manured plots where lettuce was cultivated till harvest. Enrofloxacin concentration was 7.3 μg/kg in fresh poultry litter, while its metabolite ciprofloxacin was 39.22 μg/kg after storage. Although no fluoroquinolones were detected in soils, lettuce from manured plots contained enrofloxacin and ciprofloxacin at 14.97 and 9.77 μg/kg, respectively, providing evidence of fluoroquinolone bioaccumulation in plants. Abundance of sul1 and intI1 in poultry litter was not affected by storage. Manured soils showed better soil quality than controls, but sul1 gene abundance was 1.6 times higher, reaching 7.61 Log sul1/g soil. A less sensitive, but significant effect was registered for intI1. These findings show that static storage is insufficient to stop the transmission of antibiotics and AMR biomarkers from poultry to horticulture. Amending soil with industrial poultry litter contributes to pollution with these emergent contaminants and risks human antibiotic exposure through fresh vegetables. [Display omitted] •Fluoroquinolones and AMR pathway in circular periurban agriculture.•In an open-field experiment stored poultry litter (PL) is used as a soil amendment.•Lettuce accumulates enrofloxacin and ciprofloxacin from intensive animal husbandry.•PL improves soil quality but increases sul1 and intI1 gene abundance.•Soil amendment with PL contributes to fluoroquinolone pollution and AMR spread.</description><identifier>ISSN: 0048-9697</identifier><identifier>ISSN: 1879-1026</identifier><identifier>EISSN: 1879-1026</identifier><identifier>DOI: 10.1016/j.scitotenv.2024.176874</identifier><identifier>PMID: 39414035</identifier><language>eng</language><publisher>Netherlands: Elsevier B.V</publisher><subject>Agriculture - methods ; Animals ; Anti-Bacterial Agents - analysis ; Argentina ; Drug Resistance, Bacterial - genetics ; Drug Resistance, Microbial - genetics ; Environmental Monitoring ; Fluoroquinolones ; Fluoroquinolones - analysis ; Horticulture ; intI1 ; Lactuca ; Manure ; Poultry ; Poultry litter ; Soil ; Soil - chemistry ; Soil Microbiology ; Soil Pollutants - analysis ; sul1</subject><ispartof>The Science of the total environment, 2024-12, Vol.955, p.176874, Article 176874</ispartof><rights>2024 The Authors</rights><rights>Copyright © 2024 The Authors. 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While animal manure benefits soil fertility, it also acts as hotspot for antibiotic residues, antibiotic-resistant bacteria, and their genes. Amending soils with poultry litter is recognized as “magic” among horticulture farmers and it remains a common practice globally. However, this poses a risk especially in countries where prophylactic use of antibiotics is allowed. In Argentina, fluoroquinolones are used in this way besides being listed as essential medicines and classified as “watch” by the World Health Organization. Antibiotic selective pressure can favour AMR in the environment but the fate of antibiotic residues and AMR dissemination from these practices remains poorly understood. Our research addresses this gap with a biological model tracing fluoroquinolones from poultry to soil to lettuce and tracking anthropogenic AMR with the proposed biomarker genes sul1 and intI1. Fresh poultry litter was stored for six months before application in a horticulture field experiment. The experiment included control and manured plots where lettuce was cultivated till harvest. Enrofloxacin concentration was 7.3 μg/kg in fresh poultry litter, while its metabolite ciprofloxacin was 39.22 μg/kg after storage. Although no fluoroquinolones were detected in soils, lettuce from manured plots contained enrofloxacin and ciprofloxacin at 14.97 and 9.77 μg/kg, respectively, providing evidence of fluoroquinolone bioaccumulation in plants. Abundance of sul1 and intI1 in poultry litter was not affected by storage. Manured soils showed better soil quality than controls, but sul1 gene abundance was 1.6 times higher, reaching 7.61 Log sul1/g soil. A less sensitive, but significant effect was registered for intI1. These findings show that static storage is insufficient to stop the transmission of antibiotics and AMR biomarkers from poultry to horticulture. Amending soil with industrial poultry litter contributes to pollution with these emergent contaminants and risks human antibiotic exposure through fresh vegetables. 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The experiment included control and manured plots where lettuce was cultivated till harvest. Enrofloxacin concentration was 7.3 μg/kg in fresh poultry litter, while its metabolite ciprofloxacin was 39.22 μg/kg after storage. Although no fluoroquinolones were detected in soils, lettuce from manured plots contained enrofloxacin and ciprofloxacin at 14.97 and 9.77 μg/kg, respectively, providing evidence of fluoroquinolone bioaccumulation in plants. Abundance of sul1 and intI1 in poultry litter was not affected by storage. Manured soils showed better soil quality than controls, but sul1 gene abundance was 1.6 times higher, reaching 7.61 Log sul1/g soil. A less sensitive, but significant effect was registered for intI1. These findings show that static storage is insufficient to stop the transmission of antibiotics and AMR biomarkers from poultry to horticulture. Amending soil with industrial poultry litter contributes to pollution with these emergent contaminants and risks human antibiotic exposure through fresh vegetables. [Display omitted] •Fluoroquinolones and AMR pathway in circular periurban agriculture.•In an open-field experiment stored poultry litter (PL) is used as a soil amendment.•Lettuce accumulates enrofloxacin and ciprofloxacin from intensive animal husbandry.•PL improves soil quality but increases sul1 and intI1 gene abundance.•Soil amendment with PL contributes to fluoroquinolone pollution and AMR spread.</abstract><cop>Netherlands</cop><pub>Elsevier B.V</pub><pmid>39414035</pmid><doi>10.1016/j.scitotenv.2024.176874</doi><oa>free_for_read</oa></addata></record>
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subjects Agriculture - methods
Animals
Anti-Bacterial Agents - analysis
Argentina
Drug Resistance, Bacterial - genetics
Drug Resistance, Microbial - genetics
Environmental Monitoring
Fluoroquinolones
Fluoroquinolones - analysis
Horticulture
intI1
Lactuca
Manure
Poultry
Poultry litter
Soil
Soil - chemistry
Soil Microbiology
Soil Pollutants - analysis
sul1
title Fate of fluoroquinolones associated with antimicrobial resistance in circular periurban agriculture
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