Annual dynamics of antimicrobials and resistance determinants in flocculent and aerobic granular sludge treatment systems

Rebeca Pallares-Vega; Lucia Hernandez Leal; Benjamin N. Fletcher; Eduardo Vias-Torres; Mark C.M. van Loosdrecht; David G. Weissbrodt; Heike Schmitt

doi:10.1016/j.watres.2020.116752

Annual dynamics of antimicrobials and resistance determinants in flocculent and aerobic granular sludge treatment systems

Rebeca Pallares-Vega
, Lucia Hernandez Leal
, Benjamin N. Fletcher
, Eduardo Vias-Torres
, Mark C.M. van Loosdrecht
, David G. Weissbrodt
, Heike Schmitt

IRAS OH Epidemiology Microbial Agents

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

The occurrence and removal patterns of 24 antimicrobial agents and antimicrobial resistant determinants namely 6 antibiotic resistance genes (ARGs) and 2 mobile genetic elements (MGEs), and the fecal indicator E. coli were investigated in three full-scale wastewater treatment plants. Their waterlines and biosolids lines (including secondary treatment based on both granular and activated sludge) were sampled monthly throughout one year. Samples were analyzed by means of LC-MS/MS, qPCR and cell enumeration, respectively. The influence of rainfall, temperature, and turbidity on the occurrence and removal of the aforementioned agents was assessed through statistical linear mixed models. Ten of the antimicrobial agents (macrolides, fluoroquinolones, tetracyclines, and sulfonamides) were commonly found in influent in concentrations of 0.1-2 µg L ⁻¹, and the predominant ARGs were ermB and sul1 (6.4 and 5.9 log ₁₀ mL ⁻¹ respectively). Warmer temperatures slightly reduced gene concentrations in influent whilst increasing that of E. coli and produced an uneven effect on the antimicrobial concentrations across plants. Rainfall diluted both E. coli (-0.25 logs, p < 0.001) and antimicrobials but not genes. The wastewater treatment reduced the absolute abundance of both genes (1.86 logs on average) and E. coli (2.31 logs on average). The antimicrobials agents were also partly removed, but 8 of them were still detectable after treatment, and 6 accumulated in the biosolids. ARGs were also found in biosolids with patterns resembling those of influent. No significant differences in the removal of antimicrobials, genes and E. coli were observed when comparing conventional activated sludge with aerobic granular sludge. Irrespective of the type of sludge treatment, the removal of genes was significantly reduced with increasing hydraulic loads caused by rainfall (-0.35 logs per ∆ average daily flow p < 0.01), and slightly decreased with increasing turbidity (-0.02 logs per ∆1 nephelometric turbidy unit p < 0.05).

Original language	English
Article number	116752
Pages (from-to)	1-16
Number of pages	16
Journal	Water Research
Volume	190
DOIs	https://doi.org/10.1016/j.watres.2020.116752
Publication status	Published - 15 Feb 2021

Bibliographical note

Funding Information:
We would like to thank the waterboards, Royal HaskoningDHV members, and especially to all the plant operators of the three WWTPs for their essential help during the sampling campaign and data gathering. We extend our gratitude to Stina Wegener for her tireless effort during the sample collection and to Gon?alo Macedo for his assistance throughout the data analysis. We finally acknowledge Erwin Tuinhof and the analytical team at Wetsus for the analysis of the antibiotic residues. This work was performed in the cooperation framework of Wetsus, European Centre of Excellence for Sustainable Water Technology (www.wetsus.eu). Wetsus is cofunded by the Dutch Ministry of Economic Affairs and Ministry of Infrastructure and Environment, the European Union Regional Development Fund, the Province of Frysl?n, and the Northern Netherlands Provinces. Besides, this research has received funding from the European Union's Horizon2020 research and innovation program under the Marie Sk?odowska-Curie grant agreement No 665874 and was co-funded by STOWA. The authors would also like to thank the members of the research theme Source Separated Sanitation for the shared knowledge and financial support.

Funding Information:
This work was performed in the cooperation framework of Wetsus, European Centre of Excellence for Sustainable Water Technology (www.wetsus.eu). Wetsus is cofunded by the Dutch Ministry of Economic Affairs and Ministry of Infrastructure and Environment, the European Union Regional Development Fund, the Province of Fryslân, and the Northern Netherlands Provinces. Besides, this research has received funding from the European Union's Horizon2020 research and innovation program under the Marie Skłodowska-Curie grant agreement No 665874 and was co-funded by STOWA . The authors would also like to thank the members of the research theme Source Separated Sanitation for the shared knowledge and financial support.

Publisher Copyright:
© 2020

Keywords

ARGs
Antibiotics
Granular sludge
Rainfall
Temperature
WWTP

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Cite this

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title = "Annual dynamics of antimicrobials and resistance determinants in flocculent and aerobic granular sludge treatment systems",

abstract = "The occurrence and removal patterns of 24 antimicrobial agents and antimicrobial resistant determinants namely 6 antibiotic resistance genes (ARGs) and 2 mobile genetic elements (MGEs), and the fecal indicator E. coli were investigated in three full-scale wastewater treatment plants. Their waterlines and biosolids lines (including secondary treatment based on both granular and activated sludge) were sampled monthly throughout one year. Samples were analyzed by means of LC-MS/MS, qPCR and cell enumeration, respectively. The influence of rainfall, temperature, and turbidity on the occurrence and removal of the aforementioned agents was assessed through statistical linear mixed models. Ten of the antimicrobial agents (macrolides, fluoroquinolones, tetracyclines, and sulfonamides) were commonly found in influent in concentrations of 0.1-2 µg L −1, and the predominant ARGs were ermB and sul1 (6.4 and 5.9 log 10 mL −1 respectively). Warmer temperatures slightly reduced gene concentrations in influent whilst increasing that of E. coli and produced an uneven effect on the antimicrobial concentrations across plants. Rainfall diluted both E. coli (-0.25 logs, p < 0.001) and antimicrobials but not genes. The wastewater treatment reduced the absolute abundance of both genes (1.86 logs on average) and E. coli (2.31 logs on average). The antimicrobials agents were also partly removed, but 8 of them were still detectable after treatment, and 6 accumulated in the biosolids. ARGs were also found in biosolids with patterns resembling those of influent. No significant differences in the removal of antimicrobials, genes and E. coli were observed when comparing conventional activated sludge with aerobic granular sludge. Irrespective of the type of sludge treatment, the removal of genes was significantly reduced with increasing hydraulic loads caused by rainfall (-0.35 logs per ∆ average daily flow p < 0.01), and slightly decreased with increasing turbidity (-0.02 logs per ∆1 nephelometric turbidy unit p < 0.05). ",

keywords = "ARGs, Antibiotics, Granular sludge, Rainfall, Temperature, WWTP",

author = "Rebeca Pallares-Vega and \{Hernandez Leal\}, Lucia and Fletcher, \{Benjamin N.\} and Eduardo Vias-Torres and \{van Loosdrecht\}, \{Mark C.M.\} and Weissbrodt, \{David G.\} and Heike Schmitt",

note = "Funding Information: We would like to thank the waterboards, Royal HaskoningDHV members, and especially to all the plant operators of the three WWTPs for their essential help during the sampling campaign and data gathering. We extend our gratitude to Stina Wegener for her tireless effort during the sample collection and to Gon?alo Macedo for his assistance throughout the data analysis. We finally acknowledge Erwin Tuinhof and the analytical team at Wetsus for the analysis of the antibiotic residues. This work was performed in the cooperation framework of Wetsus, European Centre of Excellence for Sustainable Water Technology (www.wetsus.eu). Wetsus is cofunded by the Dutch Ministry of Economic Affairs and Ministry of Infrastructure and Environment, the European Union Regional Development Fund, the Province of Frysl?n, and the Northern Netherlands Provinces. Besides, this research has received funding from the European Union's Horizon2020 research and innovation program under the Marie Sk?odowska-Curie grant agreement No 665874 and was co-funded by STOWA. The authors would also like to thank the members of the research theme Source Separated Sanitation for the shared knowledge and financial support. Funding Information: This work was performed in the cooperation framework of Wetsus, European Centre of Excellence for Sustainable Water Technology (www.wetsus.eu). Wetsus is cofunded by the Dutch Ministry of Economic Affairs and Ministry of Infrastructure and Environment, the European Union Regional Development Fund, the Province of Frysl{\^a}n, and the Northern Netherlands Provinces. Besides, this research has received funding from the European Union's Horizon2020 research and innovation program under the Marie Sk{\l}odowska-Curie grant agreement No 665874 and was co-funded by STOWA . The authors would also like to thank the members of the research theme Source Separated Sanitation for the shared knowledge and financial support. Publisher Copyright: {\textcopyright} 2020",

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doi = "10.1016/j.watres.2020.116752",

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T1 - Annual dynamics of antimicrobials and resistance determinants in flocculent and aerobic granular sludge treatment systems

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AU - Hernandez Leal, Lucia

AU - Fletcher, Benjamin N.

AU - Vias-Torres, Eduardo

AU - van Loosdrecht, Mark C.M.

AU - Weissbrodt, David G.

AU - Schmitt, Heike

N1 - Funding Information: We would like to thank the waterboards, Royal HaskoningDHV members, and especially to all the plant operators of the three WWTPs for their essential help during the sampling campaign and data gathering. We extend our gratitude to Stina Wegener for her tireless effort during the sample collection and to Gon?alo Macedo for his assistance throughout the data analysis. We finally acknowledge Erwin Tuinhof and the analytical team at Wetsus for the analysis of the antibiotic residues. This work was performed in the cooperation framework of Wetsus, European Centre of Excellence for Sustainable Water Technology (www.wetsus.eu). Wetsus is cofunded by the Dutch Ministry of Economic Affairs and Ministry of Infrastructure and Environment, the European Union Regional Development Fund, the Province of Frysl?n, and the Northern Netherlands Provinces. Besides, this research has received funding from the European Union's Horizon2020 research and innovation program under the Marie Sk?odowska-Curie grant agreement No 665874 and was co-funded by STOWA. The authors would also like to thank the members of the research theme Source Separated Sanitation for the shared knowledge and financial support. Funding Information: This work was performed in the cooperation framework of Wetsus, European Centre of Excellence for Sustainable Water Technology (www.wetsus.eu). Wetsus is cofunded by the Dutch Ministry of Economic Affairs and Ministry of Infrastructure and Environment, the European Union Regional Development Fund, the Province of Fryslân, and the Northern Netherlands Provinces. Besides, this research has received funding from the European Union's Horizon2020 research and innovation program under the Marie Skłodowska-Curie grant agreement No 665874 and was co-funded by STOWA . The authors would also like to thank the members of the research theme Source Separated Sanitation for the shared knowledge and financial support. Publisher Copyright: © 2020

PY - 2021/2/15

Y1 - 2021/2/15

N2 - The occurrence and removal patterns of 24 antimicrobial agents and antimicrobial resistant determinants namely 6 antibiotic resistance genes (ARGs) and 2 mobile genetic elements (MGEs), and the fecal indicator E. coli were investigated in three full-scale wastewater treatment plants. Their waterlines and biosolids lines (including secondary treatment based on both granular and activated sludge) were sampled monthly throughout one year. Samples were analyzed by means of LC-MS/MS, qPCR and cell enumeration, respectively. The influence of rainfall, temperature, and turbidity on the occurrence and removal of the aforementioned agents was assessed through statistical linear mixed models. Ten of the antimicrobial agents (macrolides, fluoroquinolones, tetracyclines, and sulfonamides) were commonly found in influent in concentrations of 0.1-2 µg L −1, and the predominant ARGs were ermB and sul1 (6.4 and 5.9 log 10 mL −1 respectively). Warmer temperatures slightly reduced gene concentrations in influent whilst increasing that of E. coli and produced an uneven effect on the antimicrobial concentrations across plants. Rainfall diluted both E. coli (-0.25 logs, p < 0.001) and antimicrobials but not genes. The wastewater treatment reduced the absolute abundance of both genes (1.86 logs on average) and E. coli (2.31 logs on average). The antimicrobials agents were also partly removed, but 8 of them were still detectable after treatment, and 6 accumulated in the biosolids. ARGs were also found in biosolids with patterns resembling those of influent. No significant differences in the removal of antimicrobials, genes and E. coli were observed when comparing conventional activated sludge with aerobic granular sludge. Irrespective of the type of sludge treatment, the removal of genes was significantly reduced with increasing hydraulic loads caused by rainfall (-0.35 logs per ∆ average daily flow p < 0.01), and slightly decreased with increasing turbidity (-0.02 logs per ∆1 nephelometric turbidy unit p < 0.05).

AB - The occurrence and removal patterns of 24 antimicrobial agents and antimicrobial resistant determinants namely 6 antibiotic resistance genes (ARGs) and 2 mobile genetic elements (MGEs), and the fecal indicator E. coli were investigated in three full-scale wastewater treatment plants. Their waterlines and biosolids lines (including secondary treatment based on both granular and activated sludge) were sampled monthly throughout one year. Samples were analyzed by means of LC-MS/MS, qPCR and cell enumeration, respectively. The influence of rainfall, temperature, and turbidity on the occurrence and removal of the aforementioned agents was assessed through statistical linear mixed models. Ten of the antimicrobial agents (macrolides, fluoroquinolones, tetracyclines, and sulfonamides) were commonly found in influent in concentrations of 0.1-2 µg L −1, and the predominant ARGs were ermB and sul1 (6.4 and 5.9 log 10 mL −1 respectively). Warmer temperatures slightly reduced gene concentrations in influent whilst increasing that of E. coli and produced an uneven effect on the antimicrobial concentrations across plants. Rainfall diluted both E. coli (-0.25 logs, p < 0.001) and antimicrobials but not genes. The wastewater treatment reduced the absolute abundance of both genes (1.86 logs on average) and E. coli (2.31 logs on average). The antimicrobials agents were also partly removed, but 8 of them were still detectable after treatment, and 6 accumulated in the biosolids. ARGs were also found in biosolids with patterns resembling those of influent. No significant differences in the removal of antimicrobials, genes and E. coli were observed when comparing conventional activated sludge with aerobic granular sludge. Irrespective of the type of sludge treatment, the removal of genes was significantly reduced with increasing hydraulic loads caused by rainfall (-0.35 logs per ∆ average daily flow p < 0.01), and slightly decreased with increasing turbidity (-0.02 logs per ∆1 nephelometric turbidy unit p < 0.05).

KW - ARGs

KW - Antibiotics

KW - Granular sludge

KW - Rainfall

KW - Temperature

KW - WWTP

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DO - 10.1016/j.watres.2020.116752

M3 - Article

C2 - 33385875

SN - 0043-1354

VL - 190

SP - 1

EP - 16

JO - Water Research

JF - Water Research

M1 - 116752

ER -

Annual dynamics of antimicrobials and resistance determinants in flocculent and aerobic granular sludge treatment systems

Abstract

Bibliographical note

Keywords

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