Nationwide surveillance reveals frequent detection of carbapenemase-producing Enterobacterales in Dutch municipal wastewater

Hetty Blaak; Merel A. Kemper; Heleen de Man; Jeroen P.G. van Leuken; Jack F. Schijven; Mark W.J. van Passel; Heike Schmitt; Ana Maria de Roda Husman

doi:10.1016/j.scitotenv.2021.145925

Nationwide surveillance reveals frequent detection of carbapenemase-producing Enterobacterales in Dutch municipal wastewater

Hetty Blaak^*, Merel A. Kemper, Heleen de Man, Jeroen P.G. van Leuken, Jack F. Schijven, Mark W.J. van Passel, Heike Schmitt, Ana Maria de Roda Husman

^*Corresponding author for this work

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

Abstract

Carbapenemase-producing Enterobacterales (CPE) pose a threat to public health necessitating restriction of further spread. Tools to efficiently monitor the prevalence of these still relatively rare resistant bacteria and insight in routes of dissemination are pivotal for the development of prevention strategies. By analysis of untreated and treated wastewater from 100 municipal wastewater treatment plants (WWTPs) together serving over 40% of the Dutch population, this study investigated both the distribution of CPE in the Dutch population, and WWTPs as a source of CPE in the aquatic environment. CPE were detected at 89% of the WWTPs, in 87 influents and 53 effluents. Overall, 15 different CPE-types were detected based on species and carbapenemase gene. The most widely distributed were E. coli carrying bla_OXA-48-like genes, which were detected at 88 WWTPs including small WWTPs without connected health care institutions (HCI). Bla_OXA-48-like-positive-K. pneumoniae, bla_NDM- or bla_KPC-positive E. coli, and bla_NDM- or bla_KPC-positive K. pneumoniae were detected at 33, 20, and 14 WWTPs, respectively. Mean influent and effluent CPE concentrations were 7.9×10² cfu/l and 11 cfu/l. The total daily number of CPE discharged by the 100 WWTPs was estimated to be 2.2×10¹¹ cfu. In multivariate analysis, CPE concentrations in untreated wastewater were positively associated with WWTP size and E. coli concentrations, but not with the presence of HCI. Based on the total number of CPE (9.7×10¹² cfu) and ESBL-E. coli (2.410¹⁵ cfu) in influents, and a prevalence of approximately 5% in the Dutch population for ESBL-E. coli, the prevalence of CPE in the Dutch population was roughly estimated to be 0.02%. Wastewater surveillance is an efficient tool to monitor the distribution of CPE in the population at a national level and may supplement human surveillance data. CPE are emitted to the aquatic environment with treated wastewater and associated public health risks need to be determined.

Original language	English
Article number	145925
Pages (from-to)	1-11
Journal	Science of the Total Environment
Volume	776
DOIs	https://doi.org/10.1016/j.scitotenv.2021.145925
Publication status	Published - 1 Jul 2021

Bibliographical note

Funding Information:
We like to thank Christiaan Veenman and Suzanne Kerkhofs for their contribution to pilot experiments leading to the here used procedures. We are indebted to all Dutch water boards for facilitating the current study, and to all WWTP personnel responsible for the actual sampling of wastewater. This research was financed by the Dutch Ministry of Health, Welfare and Sport .

Publisher Copyright:
© 2021 Elsevier B.V.

Funding

We like to thank Christiaan Veenman and Suzanne Kerkhofs for their contribution to pilot experiments leading to the here used procedures. We are indebted to all Dutch water boards for facilitating the current study, and to all WWTP personnel responsible for the actual sampling of wastewater. This research was financed by the Dutch Ministry of Health, Welfare and Sport .

Keywords

Carbapenemase-producing Enterobacterales, Antibiotic resistance
Wastewater
Wastewater surveillance
Wastewater treatment plant

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

Access to Document

10.1016/j.scitotenv.2021.145925

Cite this

Blaak, H., Kemper, M. A., de Man, H., van Leuken, J. P. G., Schijven, J. F., van Passel, M. W. J., Schmitt, H., & de Roda Husman, A. M. (2021). Nationwide surveillance reveals frequent detection of carbapenemase-producing Enterobacterales in Dutch municipal wastewater. Science of the Total Environment, 776, 1-11. Article 145925. https://doi.org/10.1016/j.scitotenv.2021.145925

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abstract = "Carbapenemase-producing Enterobacterales (CPE) pose a threat to public health necessitating restriction of further spread. Tools to efficiently monitor the prevalence of these still relatively rare resistant bacteria and insight in routes of dissemination are pivotal for the development of prevention strategies. By analysis of untreated and treated wastewater from 100 municipal wastewater treatment plants (WWTPs) together serving over 40% of the Dutch population, this study investigated both the distribution of CPE in the Dutch population, and WWTPs as a source of CPE in the aquatic environment. CPE were detected at 89% of the WWTPs, in 87 influents and 53 effluents. Overall, 15 different CPE-types were detected based on species and carbapenemase gene. The most widely distributed were E. coli carrying blaOXA-48-like genes, which were detected at 88 WWTPs including small WWTPs without connected health care institutions (HCI). BlaOXA-48-like-positive-K. pneumoniae, blaNDM- or blaKPC-positive E. coli, and blaNDM- or blaKPC-positive K. pneumoniae were detected at 33, 20, and 14 WWTPs, respectively. Mean influent and effluent CPE concentrations were 7.9×102 cfu/l and 11 cfu/l. The total daily number of CPE discharged by the 100 WWTPs was estimated to be 2.2×1011 cfu. In multivariate analysis, CPE concentrations in untreated wastewater were positively associated with WWTP size and E. coli concentrations, but not with the presence of HCI. Based on the total number of CPE (9.7×1012 cfu) and ESBL-E. coli (2.41015 cfu) in influents, and a prevalence of approximately 5% in the Dutch population for ESBL-E. coli, the prevalence of CPE in the Dutch population was roughly estimated to be 0.02%. Wastewater surveillance is an efficient tool to monitor the distribution of CPE in the population at a national level and may supplement human surveillance data. CPE are emitted to the aquatic environment with treated wastewater and associated public health risks need to be determined.",

keywords = "Carbapenemase-producing Enterobacterales, Antibiotic resistance, Wastewater, Wastewater surveillance, Wastewater treatment plant",

author = "Hetty Blaak and Kemper, {Merel A.} and {de Man}, Heleen and {van Leuken}, {Jeroen P.G.} and Schijven, {Jack F.} and {van Passel}, {Mark W.J.} and Heike Schmitt and {de Roda Husman}, {Ana Maria}",

note = "Funding Information: We like to thank Christiaan Veenman and Suzanne Kerkhofs for their contribution to pilot experiments leading to the here used procedures. We are indebted to all Dutch water boards for facilitating the current study, and to all WWTP personnel responsible for the actual sampling of wastewater. This research was financed by the Dutch Ministry of Health, Welfare and Sport . Publisher Copyright: {\textcopyright} 2021 Elsevier B.V.",

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doi = "10.1016/j.scitotenv.2021.145925",

language = "English",

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T1 - Nationwide surveillance reveals frequent detection of carbapenemase-producing Enterobacterales in Dutch municipal wastewater

AU - Blaak, Hetty

AU - Kemper, Merel A.

AU - de Man, Heleen

AU - van Leuken, Jeroen P.G.

AU - Schijven, Jack F.

AU - van Passel, Mark W.J.

AU - Schmitt, Heike

AU - de Roda Husman, Ana Maria

N1 - Funding Information: We like to thank Christiaan Veenman and Suzanne Kerkhofs for their contribution to pilot experiments leading to the here used procedures. We are indebted to all Dutch water boards for facilitating the current study, and to all WWTP personnel responsible for the actual sampling of wastewater. This research was financed by the Dutch Ministry of Health, Welfare and Sport . Publisher Copyright: © 2021 Elsevier B.V.

PY - 2021/7/1

Y1 - 2021/7/1

N2 - Carbapenemase-producing Enterobacterales (CPE) pose a threat to public health necessitating restriction of further spread. Tools to efficiently monitor the prevalence of these still relatively rare resistant bacteria and insight in routes of dissemination are pivotal for the development of prevention strategies. By analysis of untreated and treated wastewater from 100 municipal wastewater treatment plants (WWTPs) together serving over 40% of the Dutch population, this study investigated both the distribution of CPE in the Dutch population, and WWTPs as a source of CPE in the aquatic environment. CPE were detected at 89% of the WWTPs, in 87 influents and 53 effluents. Overall, 15 different CPE-types were detected based on species and carbapenemase gene. The most widely distributed were E. coli carrying blaOXA-48-like genes, which were detected at 88 WWTPs including small WWTPs without connected health care institutions (HCI). BlaOXA-48-like-positive-K. pneumoniae, blaNDM- or blaKPC-positive E. coli, and blaNDM- or blaKPC-positive K. pneumoniae were detected at 33, 20, and 14 WWTPs, respectively. Mean influent and effluent CPE concentrations were 7.9×102 cfu/l and 11 cfu/l. The total daily number of CPE discharged by the 100 WWTPs was estimated to be 2.2×1011 cfu. In multivariate analysis, CPE concentrations in untreated wastewater were positively associated with WWTP size and E. coli concentrations, but not with the presence of HCI. Based on the total number of CPE (9.7×1012 cfu) and ESBL-E. coli (2.41015 cfu) in influents, and a prevalence of approximately 5% in the Dutch population for ESBL-E. coli, the prevalence of CPE in the Dutch population was roughly estimated to be 0.02%. Wastewater surveillance is an efficient tool to monitor the distribution of CPE in the population at a national level and may supplement human surveillance data. CPE are emitted to the aquatic environment with treated wastewater and associated public health risks need to be determined.

AB - Carbapenemase-producing Enterobacterales (CPE) pose a threat to public health necessitating restriction of further spread. Tools to efficiently monitor the prevalence of these still relatively rare resistant bacteria and insight in routes of dissemination are pivotal for the development of prevention strategies. By analysis of untreated and treated wastewater from 100 municipal wastewater treatment plants (WWTPs) together serving over 40% of the Dutch population, this study investigated both the distribution of CPE in the Dutch population, and WWTPs as a source of CPE in the aquatic environment. CPE were detected at 89% of the WWTPs, in 87 influents and 53 effluents. Overall, 15 different CPE-types were detected based on species and carbapenemase gene. The most widely distributed were E. coli carrying blaOXA-48-like genes, which were detected at 88 WWTPs including small WWTPs without connected health care institutions (HCI). BlaOXA-48-like-positive-K. pneumoniae, blaNDM- or blaKPC-positive E. coli, and blaNDM- or blaKPC-positive K. pneumoniae were detected at 33, 20, and 14 WWTPs, respectively. Mean influent and effluent CPE concentrations were 7.9×102 cfu/l and 11 cfu/l. The total daily number of CPE discharged by the 100 WWTPs was estimated to be 2.2×1011 cfu. In multivariate analysis, CPE concentrations in untreated wastewater were positively associated with WWTP size and E. coli concentrations, but not with the presence of HCI. Based on the total number of CPE (9.7×1012 cfu) and ESBL-E. coli (2.41015 cfu) in influents, and a prevalence of approximately 5% in the Dutch population for ESBL-E. coli, the prevalence of CPE in the Dutch population was roughly estimated to be 0.02%. Wastewater surveillance is an efficient tool to monitor the distribution of CPE in the population at a national level and may supplement human surveillance data. CPE are emitted to the aquatic environment with treated wastewater and associated public health risks need to be determined.

KW - Carbapenemase-producing Enterobacterales, Antibiotic resistance

KW - Wastewater

KW - Wastewater surveillance

KW - Wastewater treatment plant

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U2 - 10.1016/j.scitotenv.2021.145925

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M1 - 145925

ER -

Nationwide surveillance reveals frequent detection of carbapenemase-producing Enterobacterales in Dutch municipal wastewater

Abstract

Bibliographical note

Funding

Keywords

UN SDGs

Access to Document

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