Clinically relevant sequence types of carbapenemase-producing Escherichia coli and Klebsiella pneumoniae detected in Finnish wastewater in 2021–2022

Viivi Heljanko; Olga Tyni; Venla Johansson; Jussa Pekka Virtanen; Kati Räisänen; Kirsi Maarit Lehto; Anssi Lipponen; Sami Oikarinen; Tarja Pitkänen; WastPan Study Group; Annamari Heikinheimo

doi:10.1186/s13756-024-01370-z

Clinically relevant sequence types of carbapenemase-producing Escherichia coli and Klebsiella pneumoniae detected in Finnish wastewater in 2021–2022

Viivi Heljanko^*
, Olga Tyni
, Venla Johansson
, Jussa Pekka Virtanen
, Kati Räisänen
, Kirsi Maarit Lehto
, Anssi Lipponen
, Sami Oikarinen
, Tarja Pitkänen
, WastPan Study Group
, Annamari Heikinheimo

^*Corresponding author for this work

Biosciences

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

16 Citations (Scopus)

13 Downloads (Pure)

Abstract

Background: Antimicrobial resistance (AMR) is a critical threat to human health. Escherichia coli and Klebsiella pneumoniae are clinically the most important species associated with AMR and are the most common carbapenemase-producing (CP) Enterobacterales detected in human specimens in Finland. Wastewater surveillance has emerged as a potential approach for population-level surveillance of AMR, as wastewater could offer a reflection from a larger population with one sample and minimal recognized ethical issues. In this study, we investigated the potential of wastewater surveillance to detect CP E. coli and K. pneumoniae strains similar to those detected in human specimens. Methods: Altogether, 89 composite samples of untreated community wastewater were collected from 10 wastewater treatment plants across Finland in 2021–2022. CP E. coli and K. pneumoniae were isolated using selective culture media and identified using MALDI-TOF MS. Antimicrobial susceptibility testing was performed using disk diffusion test and broth microdilution method, and a subset of isolates was characterized using whole-genome sequencing. Results: CP E. coli was detected in 26 (29.2%) and K. pneumoniae in 25 (28.1%) samples. Among E. coli, the most common sequence type (ST) was ST410 (n = 7/26, 26.9%), while ST359 (n = 4/25, 16.0%) predominated among K. pneumoniae. Globally successful STs were detected in both E. coli (ST410, ST1284, ST167, and ST405) and K. pneumoniae (ST512, ST101, and ST307). K. pneumoniae carbapenemases (KPC) were the most common carbapenemases in both E. coli (n = 11/26, 42.3%) and K. pneumoniae (n = 13/25, 52.0%), yet also other carbapenemases, such as bla _NDM-5, bla _OXA-48, and bla _OXA-181, were detected. We detected isolates harboring similar ST and enzyme type combinations previously linked to clusters in Finland, such as E. coli ST410 with bla _KPC-2 and K. pneumoniae ST512 with bla _KPC-3. Conclusions: Our study highlights the presence of clinically relevant strains of CP E. coli and K. pneumoniae in community wastewater. The results indicate that wastewater surveillance could serve as a monitoring tool for CP Enterobacterales. However, the specificity and sensitivity of the methods should be improved, and technologies, like advanced sequencing methods, should be utilized to distinguish data with public health relevance, harness the full potential of wastewater surveillance, and implement the data in public health surveillance.

Original language	English
Article number	14
Number of pages	11
Journal	Antimicrobial Resistance and Infection Control
Volume	13
Issue number	1
DOIs	https://doi.org/10.1186/s13756-024-01370-z
Publication status	Published - 2024
Publication type	A1 Journal article-refereed

Funding

The authors warmly thank Kirsi Ristkari for assistance in the laboratory and Kristiina Valkama for help with sample transportation arrangements. The personnel of the wastewater treatment facilities in all WastPan surveillance locations in Finland are gratefully acknowledged for their support and timely efforts in wastewater composite sampling and sample transportation arrangements. WastPan Study Group: Ahmad Al-Mustapha and Paula Kurittu (University of Helsinki, Finland); Annika Länsivaara, Rafiqul Hyder, and Erja Janhonen (Tampere University, Finland); and Ananda Tiwari, Anna-Maria Hokajärvi, Aleksi Kolehmainen, Teemu Möttönen, Oskari Luomala, Aapo Juutinen, Soile Blomqvist, Carita Savolainen-Kopra (Finnish Institute for Health and Welfare, Finland), and Anniina Sarekoski (University of Helsinki and Finnish Institute for Health and Welfare, Finland). Open Access funding provided by University of Helsinki (including Helsinki University Central Hospital). This work was funded by the Academy of Finland (Grant No. 339417) and the Doctoral Program in Food Chain and Health, Faculty of Veterinary Medicine, University of Helsinki, Finland. Open access funded by Helsinki University Library.

Funders	Funder number
Doctoral Program in Food Chain and Health, Faculty of Veterinary Medicine, University of Helsinki
Finnish Institute for Health and Welfare
Helsinki University Library
Helsingin yliopisto
Academy of Finland	339417

UN SDGs

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

SDG 3 Good Health and Well-being

Keywords

Antimicrobial resistance
Carbapenemase-producing Escherichia coli
Carbapenemase-producing Gram-negative bacteria
Carbapenemase-producing Klebsiella pneumoniae
Wastewater surveillance

Publication forum classification

Publication forum level 1

ASJC Scopus subject areas

Public Health, Environmental and Occupational Health
Microbiology (medical)
Infectious Diseases
Pharmacology (medical)

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10.1186/s13756-024-01370-zLicence: CC BY

s13756-024-01370-zFinal published version, 3.05 MBLicence: CC BY

https://urn.fi/URN:NBN:fi:tuni-202404103430Licence: CC BY

Cite this

Heljanko, V., Tyni, O., Johansson, V., Virtanen, J. P., Räisänen, K., Lehto, K. M., Lipponen, A., Oikarinen, S., Pitkänen, T., WastPan Study Group, & Heikinheimo, A. (2024). Clinically relevant sequence types of carbapenemase-producing Escherichia coli and Klebsiella pneumoniae detected in Finnish wastewater in 2021–2022. Antimicrobial Resistance and Infection Control, 13(1), Article 14. https://doi.org/10.1186/s13756-024-01370-z

@article{f9f0e8d350164eb793b8fee8789ed5fc,

title = "Clinically relevant sequence types of carbapenemase-producing Escherichia coli and Klebsiella pneumoniae detected in Finnish wastewater in 2021–2022",

abstract = "Background: Antimicrobial resistance (AMR) is a critical threat to human health. Escherichia coli and Klebsiella pneumoniae are clinically the most important species associated with AMR and are the most common carbapenemase-producing (CP) Enterobacterales detected in human specimens in Finland. Wastewater surveillance has emerged as a potential approach for population-level surveillance of AMR, as wastewater could offer a reflection from a larger population with one sample and minimal recognized ethical issues. In this study, we investigated the potential of wastewater surveillance to detect CP E. coli and K. pneumoniae strains similar to those detected in human specimens. Methods: Altogether, 89 composite samples of untreated community wastewater were collected from 10 wastewater treatment plants across Finland in 2021–2022. CP E. coli and K. pneumoniae were isolated using selective culture media and identified using MALDI-TOF MS. Antimicrobial susceptibility testing was performed using disk diffusion test and broth microdilution method, and a subset of isolates was characterized using whole-genome sequencing. Results: CP E. coli was detected in 26 (29.2\%) and K. pneumoniae in 25 (28.1\%) samples. Among E. coli, the most common sequence type (ST) was ST410 (n = 7/26, 26.9\%), while ST359 (n = 4/25, 16.0\%) predominated among K. pneumoniae. Globally successful STs were detected in both E. coli (ST410, ST1284, ST167, and ST405) and K. pneumoniae (ST512, ST101, and ST307). K. pneumoniae carbapenemases (KPC) were the most common carbapenemases in both E. coli (n = 11/26, 42.3\%) and K. pneumoniae (n = 13/25, 52.0\%), yet also other carbapenemases, such as bla NDM-5, bla OXA-48, and bla OXA-181, were detected. We detected isolates harboring similar ST and enzyme type combinations previously linked to clusters in Finland, such as E. coli ST410 with bla KPC-2 and K. pneumoniae ST512 with bla KPC-3. Conclusions: Our study highlights the presence of clinically relevant strains of CP E. coli and K. pneumoniae in community wastewater. The results indicate that wastewater surveillance could serve as a monitoring tool for CP Enterobacterales. However, the specificity and sensitivity of the methods should be improved, and technologies, like advanced sequencing methods, should be utilized to distinguish data with public health relevance, harness the full potential of wastewater surveillance, and implement the data in public health surveillance.",

keywords = "Antimicrobial resistance, Carbapenemase-producing Escherichia coli, Carbapenemase-producing Gram-negative bacteria, Carbapenemase-producing Klebsiella pneumoniae, Wastewater surveillance",

author = "Viivi Heljanko and Olga Tyni and Venla Johansson and Virtanen, \{Jussa Pekka\} and Kati R{\"a}is{\"a}nen and Lehto, \{Kirsi Maarit\} and Anssi Lipponen and Sami Oikarinen and Tarja Pitk{\"a}nen and \{WastPan Study Group\} and Annamari Heikinheimo",

note = "Publisher Copyright: {\textcopyright} 2024, The Author(s).",

year = "2024",

doi = "10.1186/s13756-024-01370-z",

language = "English",

volume = "13",

number = "1",

}

Heljanko, V, Tyni, O, Johansson, V, Virtanen, JP, Räisänen, K, Lehto, KM, Lipponen, A, Oikarinen, S, Pitkänen, T, WastPan Study Group & Heikinheimo, A 2024, 'Clinically relevant sequence types of carbapenemase-producing Escherichia coli and Klebsiella pneumoniae detected in Finnish wastewater in 2021–2022', Antimicrobial Resistance and Infection Control, vol. 13, no. 1, 14. https://doi.org/10.1186/s13756-024-01370-z

TY - JOUR

T1 - Clinically relevant sequence types of carbapenemase-producing Escherichia coli and Klebsiella pneumoniae detected in Finnish wastewater in 2021–2022

AU - Heljanko, Viivi

AU - Tyni, Olga

AU - Johansson, Venla

AU - Virtanen, Jussa Pekka

AU - Räisänen, Kati

AU - Lehto, Kirsi Maarit

AU - Lipponen, Anssi

AU - Oikarinen, Sami

AU - Pitkänen, Tarja

AU - WastPan Study Group

AU - Heikinheimo, Annamari

PY - 2024

Y1 - 2024

N2 - Background: Antimicrobial resistance (AMR) is a critical threat to human health. Escherichia coli and Klebsiella pneumoniae are clinically the most important species associated with AMR and are the most common carbapenemase-producing (CP) Enterobacterales detected in human specimens in Finland. Wastewater surveillance has emerged as a potential approach for population-level surveillance of AMR, as wastewater could offer a reflection from a larger population with one sample and minimal recognized ethical issues. In this study, we investigated the potential of wastewater surveillance to detect CP E. coli and K. pneumoniae strains similar to those detected in human specimens. Methods: Altogether, 89 composite samples of untreated community wastewater were collected from 10 wastewater treatment plants across Finland in 2021–2022. CP E. coli and K. pneumoniae were isolated using selective culture media and identified using MALDI-TOF MS. Antimicrobial susceptibility testing was performed using disk diffusion test and broth microdilution method, and a subset of isolates was characterized using whole-genome sequencing. Results: CP E. coli was detected in 26 (29.2%) and K. pneumoniae in 25 (28.1%) samples. Among E. coli, the most common sequence type (ST) was ST410 (n = 7/26, 26.9%), while ST359 (n = 4/25, 16.0%) predominated among K. pneumoniae. Globally successful STs were detected in both E. coli (ST410, ST1284, ST167, and ST405) and K. pneumoniae (ST512, ST101, and ST307). K. pneumoniae carbapenemases (KPC) were the most common carbapenemases in both E. coli (n = 11/26, 42.3%) and K. pneumoniae (n = 13/25, 52.0%), yet also other carbapenemases, such as bla NDM-5, bla OXA-48, and bla OXA-181, were detected. We detected isolates harboring similar ST and enzyme type combinations previously linked to clusters in Finland, such as E. coli ST410 with bla KPC-2 and K. pneumoniae ST512 with bla KPC-3. Conclusions: Our study highlights the presence of clinically relevant strains of CP E. coli and K. pneumoniae in community wastewater. The results indicate that wastewater surveillance could serve as a monitoring tool for CP Enterobacterales. However, the specificity and sensitivity of the methods should be improved, and technologies, like advanced sequencing methods, should be utilized to distinguish data with public health relevance, harness the full potential of wastewater surveillance, and implement the data in public health surveillance.

AB - Background: Antimicrobial resistance (AMR) is a critical threat to human health. Escherichia coli and Klebsiella pneumoniae are clinically the most important species associated with AMR and are the most common carbapenemase-producing (CP) Enterobacterales detected in human specimens in Finland. Wastewater surveillance has emerged as a potential approach for population-level surveillance of AMR, as wastewater could offer a reflection from a larger population with one sample and minimal recognized ethical issues. In this study, we investigated the potential of wastewater surveillance to detect CP E. coli and K. pneumoniae strains similar to those detected in human specimens. Methods: Altogether, 89 composite samples of untreated community wastewater were collected from 10 wastewater treatment plants across Finland in 2021–2022. CP E. coli and K. pneumoniae were isolated using selective culture media and identified using MALDI-TOF MS. Antimicrobial susceptibility testing was performed using disk diffusion test and broth microdilution method, and a subset of isolates was characterized using whole-genome sequencing. Results: CP E. coli was detected in 26 (29.2%) and K. pneumoniae in 25 (28.1%) samples. Among E. coli, the most common sequence type (ST) was ST410 (n = 7/26, 26.9%), while ST359 (n = 4/25, 16.0%) predominated among K. pneumoniae. Globally successful STs were detected in both E. coli (ST410, ST1284, ST167, and ST405) and K. pneumoniae (ST512, ST101, and ST307). K. pneumoniae carbapenemases (KPC) were the most common carbapenemases in both E. coli (n = 11/26, 42.3%) and K. pneumoniae (n = 13/25, 52.0%), yet also other carbapenemases, such as bla NDM-5, bla OXA-48, and bla OXA-181, were detected. We detected isolates harboring similar ST and enzyme type combinations previously linked to clusters in Finland, such as E. coli ST410 with bla KPC-2 and K. pneumoniae ST512 with bla KPC-3. Conclusions: Our study highlights the presence of clinically relevant strains of CP E. coli and K. pneumoniae in community wastewater. The results indicate that wastewater surveillance could serve as a monitoring tool for CP Enterobacterales. However, the specificity and sensitivity of the methods should be improved, and technologies, like advanced sequencing methods, should be utilized to distinguish data with public health relevance, harness the full potential of wastewater surveillance, and implement the data in public health surveillance.

KW - Antimicrobial resistance

KW - Carbapenemase-producing Escherichia coli

KW - Carbapenemase-producing Gram-negative bacteria

KW - Carbapenemase-producing Klebsiella pneumoniae

KW - Wastewater surveillance

U2 - 10.1186/s13756-024-01370-z

DO - 10.1186/s13756-024-01370-z

M3 - Article

C2 - 38291521

AN - SCOPUS:85183737531

SN - 2047-2994

VL - 13

JO - Antimicrobial Resistance and Infection Control

JF - Antimicrobial Resistance and Infection Control

IS - 1

M1 - 14

ER -

Clinically relevant sequence types of carbapenemase-producing Escherichia coli and Klebsiella pneumoniae detected in Finnish wastewater in 2021–2022

Abstract

Funding

UN SDGs

Keywords

Publication forum classification

ASJC Scopus subject areas

Access to Document

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