Molecular characterization of MRSA collected during national surveillance between 2008 and 2019 in the Netherlands

Leo M. Schouls; Sandra Witteveen; The Dutch CPE and MRSA Surveillance Study Groups; Marga  van Santen-Verheuvel; Fabian Labdman; Angela de Haan; Ed J. Kuijper; Han van der Heide; Daan W. Notermans; Thijs Bosch; Anthony P.A. Hendrickx; R van Mansfeld; N van Maarseveen; E. de Jong; S.J. Vainio; Esther Heikens; Martijn den Reijer; J.W. (Wendelien) Dorigo-Zetsma; A. Troelstra; E. Bathoorn; J. de Vries; D.W. van Dam; E.I.G.B. de Brauwer; R. Steingrover

doi:10.1038/s43856-023-00348-z

Molecular characterization of MRSA collected during national surveillance between 2008 and 2019 in the Netherlands

Leo M. Schouls^*
, Sandra Witteveen
, The Dutch CPE and MRSA Surveillance Study Groups
, Marga van Santen-Verheuvel
, Fabian Labdman
, Angela de Haan
, Ed J. Kuijper
, Han van der Heide
, Daan W. Notermans
, Thijs Bosch
, Anthony P.A. Hendrickx
, R van Mansfeld
, N van Maarseveen
, E. de Jong
, S.J. Vainio
, Esther Heikens
, Martijn den Reijer
, J.W. (Wendelien) Dorigo-Zetsma
, A. Troelstra
, E. Bathoorn

J. de Vries, D.W. van Dam, E.I.G.B. de Brauwer, R. Steingrover

^*Corresponding author for this work

Medical Microbiology & Infectious Diseases

National Institute of Public Health and the Environment
Leiden University Medical Centre
Ikazia Hospital
Municipal Public Health Service (GGD) Amsterdam
Slingeland Ziekenhuis
Ziekenhuis St. Jansdal and Dialysecentrum Midden Nederland
Star-SHL Medical Diagnostic Center
Centraal Bacteriologisch en Serologisch Laboratorium (CBSL)
University Medical Centre Groningen
VieCuri Medisch Centrum
Zuyderland Medical Center (Heerlen)
St. Maarten Laboratory Service

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

15 Citations (Scopus)

32 Downloads (Pure)

Abstract

Background.
Although the Netherlands is a country with a low endemic level, methicillin-resistant Staphylococcus aureus (MRSA) poses a significant health care problem. Therefore, high coverage national MRSA surveillance has been in place since 1989. To monitor possible changes in the type-distribution and emergence of resistance and virulence, MRSA isolates are molecularly characterized.

Methods.
All 43,321 isolates from 36,520 persons, collected 2008–2019, were typed by multiple-locus variable number tandem repeats analysis (MLVA) with simultaneous PCR detection of the mecA, mecC and lukF-PV genes, indicative for PVL. Next-generation sequencing data of 4991 isolates from 4798 persons were used for whole genome multi-locus sequence typing (wgMLST) and identification of resistance and virulence genes.

Results.
We show temporal change in the molecular characteristics of the MRSA population with the proportion of PVL-positive isolates increasing from 15% in 2008–2010 to 25% in 2017–2019. In livestock-associated MRSA obtained from humans, PVL-positivity increases to 6% in 2017–2019 with isolates predominantly from regions with few pig farms. wgMLST reveals the presence of 35 genogroups with distinct resistance, virulence gene profiles and specimen origin. Typing shows prolonged persistent MRSA carriage with a mean carriage period of 407 days. There is a clear spatial and a weak temporal relationship between isolates that clustered in wgMLST, indicative for regional spread of MRSA strains.

Conclusions.
Using molecular characterization, this exceptionally large study shows genomic changes in the MRSA population at the national level. It reveals waxing and waning of types and genogroups and an increasing proportion of PVL-positive MRSA.

Original language	English
Article number	123
Number of pages	13
Journal	Communications Medicine
Volume	3
Issue number	1
DOIs	https://doi.org/10.1038/s43856-023-00348-z
Publication status	Published - Dec 2023

Bibliographical note

Publisher Copyright:
© The Author(s) 2023.

UN SDGs

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

SDG 3 Good Health and Well-being

Access to Document

10.1038/s43856-023-00348-zLicence: CC BY

s43856-023-00348-zFinal published version, 2.28 MBLicence: CC BY

Cite this

Schouls, L. M., Witteveen, S., The Dutch CPE and MRSA Surveillance Study Groups, van Santen-Verheuvel, M., Labdman, F., de Haan, A., Kuijper, E. J., van der Heide, H., Notermans, D. W., Bosch, T., Hendrickx, A. P. A., van Mansfeld, R., van Maarseveen, N., de Jong, E., Vainio, S. J., Heikens, E., den Reijer, M., Dorigo-Zetsma, J. W., Troelstra, A., ... Steingrover, R. (2023). Molecular characterization of MRSA collected during national surveillance between 2008 and 2019 in the Netherlands. Communications Medicine, 3(1), Article 123. https://doi.org/10.1038/s43856-023-00348-z

@article{89e53e458175434abc02d55b9d4333df,

title = "Molecular characterization of MRSA collected during national surveillance between 2008 and 2019 in the Netherlands",

abstract = "Background. Although the Netherlands is a country with a low endemic level, methicillin-resistant Staphylococcus aureus (MRSA) poses a significant health care problem. Therefore, high coverage national MRSA surveillance has been in place since 1989. To monitor possible changes in the type-distribution and emergence of resistance and virulence, MRSA isolates are molecularly characterized. Methods. All 43,321 isolates from 36,520 persons, collected 2008{\textendash}2019, were typed by multiple-locus variable number tandem repeats analysis (MLVA) with simultaneous PCR detection of the mecA, mecC and lukF-PV genes, indicative for PVL. Next-generation sequencing data of 4991 isolates from 4798 persons were used for whole genome multi-locus sequence typing (wgMLST) and identification of resistance and virulence genes. Results. We show temporal change in the molecular characteristics of the MRSA population with the proportion of PVL-positive isolates increasing from 15\% in 2008{\textendash}2010 to 25\% in 2017{\textendash}2019. In livestock-associated MRSA obtained from humans, PVL-positivity increases to 6\% in 2017{\textendash}2019 with isolates predominantly from regions with few pig farms. wgMLST reveals the presence of 35 genogroups with distinct resistance, virulence gene profiles and specimen origin. Typing shows prolonged persistent MRSA carriage with a mean carriage period of 407 days. There is a clear spatial and a weak temporal relationship between isolates that clustered in wgMLST, indicative for regional spread of MRSA strains. Conclusions. Using molecular characterization, this exceptionally large study shows genomic changes in the MRSA population at the national level. It reveals waxing and waning of types and genogroups and an increasing proportion of PVL-positive MRSA.",

author = "Schouls, \{Leo M.\} and Sandra Witteveen and \{The Dutch CPE and MRSA Surveillance Study Groups\} and \{van Santen-Verheuvel\}, Marga and Fabian Labdman and \{de Haan\}, Angela and Kuijper, \{Ed J.\} and \{van der Heide\}, Han and Notermans, \{Daan W.\} and Thijs Bosch and Hendrickx, \{Anthony P.A.\} and \{van Arkel\}, ALE and MALV Hall and \{Van den Bijllaardt\}, W and \{van Mansfeld\}, R and \{van Dijk\}, K and B. Zwart and BMW Diederen and H Berkhout and DW Notermans and A Ott and K Waar and W Ang and \{da Silva\}, J and ALM Vlek and AGM Buiting and Bode, \{Lonneke G.M.\} and A Jansz and S Paltansing and \{van Griethuysen\}, AJ and \{Ten Foe\}, JRL and \{van Trijp\}, MJCA and M Wong and AE Muller and \{van der Linden\}, MPM and \{van Rijn\}, M. and SB Debast and E Kolwijck and \{Al Naiemi\}, N and T Schulin and S Dinant and \{van Mens\}, SP and DC Melles and JWTC Stuart and P Gruteke and \{van Dam\}, A and I Maat and B Maraha and JC Sinnige and \{van der Vorm\}, E and \{van Meer\}, MPA and \{van Maarseveen\}, N and \{de Jong\}, E. and S.J. Vainio and Esther Heikens and \{den Reijer\}, Martijn and Dorigo-Zetsma, \{J.W. (Wendelien)\} and A. Troelstra and E. Bathoorn and \{de Vries\}, J. and \{van Dam\}, D.W. and \{de Brauwer\}, E.I.G.B. and R. Steingrover",

note = "Publisher Copyright: {\textcopyright} The Author(s) 2023.",

year = "2023",

month = dec,

doi = "10.1038/s43856-023-00348-z",

language = "English",

volume = "3",

journal = "Communications Medicine",

issn = "2730-664X",

publisher = "Springer Nature",

number = "1",

}

Schouls, LM, Witteveen, S, The Dutch CPE and MRSA Surveillance Study Groups, van Santen-Verheuvel, M, Labdman, F, de Haan, A, Kuijper, EJ, van der Heide, H, Notermans, DW, Bosch, T, Hendrickx, APA, van Mansfeld, R, van Maarseveen, N, de Jong, E, Vainio, SJ, Heikens, E, den Reijer, M, Dorigo-Zetsma, JW, Troelstra, A, Bathoorn, E, de Vries, J, van Dam, DW, de Brauwer, EIGB & Steingrover, R 2023, 'Molecular characterization of MRSA collected during national surveillance between 2008 and 2019 in the Netherlands', Communications Medicine, vol. 3, no. 1, 123. https://doi.org/10.1038/s43856-023-00348-z

TY - JOUR

T1 - Molecular characterization of MRSA collected during national surveillance between 2008 and 2019 in the Netherlands

AU - Schouls, Leo M.

AU - Witteveen, Sandra

AU - The Dutch CPE and MRSA Surveillance Study Groups

AU - van Santen-Verheuvel, Marga

AU - Labdman, Fabian

AU - de Haan, Angela

AU - Kuijper, Ed J.

AU - van der Heide, Han

AU - Notermans, Daan W.

AU - Bosch, Thijs

AU - Hendrickx, Anthony P.A.

AU - van Arkel, ALE

AU - Hall, MALV

AU - Van den Bijllaardt, W

AU - van Mansfeld, R

AU - van Dijk, K

AU - Zwart, B.

AU - Diederen, BMW

AU - Berkhout, H

AU - Notermans, DW

AU - Ott, A

AU - Waar, K

AU - Ang, W

AU - da Silva, J

AU - Vlek, ALM

AU - Buiting, AGM

AU - Bode, Lonneke G.M.

AU - Jansz, A

AU - Paltansing, S

AU - van Griethuysen, AJ

AU - Ten Foe, JRL

AU - van Trijp, MJCA

AU - Wong, M

AU - Muller, AE

AU - van der Linden, MPM

AU - van Rijn, M.

AU - Debast, SB

AU - Kolwijck, E

AU - Al Naiemi, N

AU - Schulin, T

AU - Dinant, S

AU - van Mens, SP

AU - Melles, DC

AU - Stuart, JWTC

AU - Gruteke, P

AU - van Dam, A

AU - Maat, I

AU - Maraha, B

AU - Sinnige, JC

AU - van der Vorm, E

AU - van Meer, MPA

AU - van Maarseveen, N

AU - de Jong, E.

AU - Vainio, S.J.

AU - Heikens, Esther

AU - den Reijer, Martijn

AU - Dorigo-Zetsma, J.W. (Wendelien)

AU - Troelstra, A.

AU - Bathoorn, E.

AU - de Vries, J.

AU - van Dam, D.W.

AU - de Brauwer, E.I.G.B.

AU - Steingrover, R.

PY - 2023/12

Y1 - 2023/12

N2 - Background. Although the Netherlands is a country with a low endemic level, methicillin-resistant Staphylococcus aureus (MRSA) poses a significant health care problem. Therefore, high coverage national MRSA surveillance has been in place since 1989. To monitor possible changes in the type-distribution and emergence of resistance and virulence, MRSA isolates are molecularly characterized. Methods. All 43,321 isolates from 36,520 persons, collected 2008–2019, were typed by multiple-locus variable number tandem repeats analysis (MLVA) with simultaneous PCR detection of the mecA, mecC and lukF-PV genes, indicative for PVL. Next-generation sequencing data of 4991 isolates from 4798 persons were used for whole genome multi-locus sequence typing (wgMLST) and identification of resistance and virulence genes. Results. We show temporal change in the molecular characteristics of the MRSA population with the proportion of PVL-positive isolates increasing from 15% in 2008–2010 to 25% in 2017–2019. In livestock-associated MRSA obtained from humans, PVL-positivity increases to 6% in 2017–2019 with isolates predominantly from regions with few pig farms. wgMLST reveals the presence of 35 genogroups with distinct resistance, virulence gene profiles and specimen origin. Typing shows prolonged persistent MRSA carriage with a mean carriage period of 407 days. There is a clear spatial and a weak temporal relationship between isolates that clustered in wgMLST, indicative for regional spread of MRSA strains. Conclusions. Using molecular characterization, this exceptionally large study shows genomic changes in the MRSA population at the national level. It reveals waxing and waning of types and genogroups and an increasing proportion of PVL-positive MRSA.

AB - Background. Although the Netherlands is a country with a low endemic level, methicillin-resistant Staphylococcus aureus (MRSA) poses a significant health care problem. Therefore, high coverage national MRSA surveillance has been in place since 1989. To monitor possible changes in the type-distribution and emergence of resistance and virulence, MRSA isolates are molecularly characterized. Methods. All 43,321 isolates from 36,520 persons, collected 2008–2019, were typed by multiple-locus variable number tandem repeats analysis (MLVA) with simultaneous PCR detection of the mecA, mecC and lukF-PV genes, indicative for PVL. Next-generation sequencing data of 4991 isolates from 4798 persons were used for whole genome multi-locus sequence typing (wgMLST) and identification of resistance and virulence genes. Results. We show temporal change in the molecular characteristics of the MRSA population with the proportion of PVL-positive isolates increasing from 15% in 2008–2010 to 25% in 2017–2019. In livestock-associated MRSA obtained from humans, PVL-positivity increases to 6% in 2017–2019 with isolates predominantly from regions with few pig farms. wgMLST reveals the presence of 35 genogroups with distinct resistance, virulence gene profiles and specimen origin. Typing shows prolonged persistent MRSA carriage with a mean carriage period of 407 days. There is a clear spatial and a weak temporal relationship between isolates that clustered in wgMLST, indicative for regional spread of MRSA strains. Conclusions. Using molecular characterization, this exceptionally large study shows genomic changes in the MRSA population at the national level. It reveals waxing and waning of types and genogroups and an increasing proportion of PVL-positive MRSA.

UR - https://www.scopus.com/pages/publications/85185503646

U2 - 10.1038/s43856-023-00348-z

DO - 10.1038/s43856-023-00348-z

M3 - Article

C2 - 37700016

SN - 2730-664X

VL - 3

JO - Communications Medicine

JF - Communications Medicine

IS - 1

M1 - 123

ER -

Molecular characterization of MRSA collected during national surveillance between 2008 and 2019 in the Netherlands

Abstract

Bibliographical note

UN SDGs

Access to Document

Other files and links

Fingerprint

Cite this