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

Leo M. Schouls; Sandra Witteveen; Marga van Santen-Verheuvel; Angela de Haan; Fabian Labdman; Han van der Heide; Ed J. Kuijper; Daan W. Notermans; Thijs Bosch; Antoni P. A. Hendrickx; A. L. E. van Arkel; M. A. Leversteijn-van Hall; W. Van den Bijllaardt; R. van Mansfeld; K. van Dijk; B. Zwart; B. M. W. Diederen; H. Berkhout; D. W. Notermans; A. Ott; K. Waar; W. Ang; J. da Silva; A. L. M. Vlek; A. G. M. Buiting; L. G. M. Bode; A. Jansz; S. Paltansing; A. J. van Griethuysen; J. R. Lo Ten Foe; M. J. C. A. van Trijp; M. Wong; A. E. Muller; M. P. M. van der Linden; M. van Rijn; S. B. Debast; E. Kolwijck; N. Al Naiemi; T. Schulin; S. Dinant; S. P. van Mens; D. C. Melles; J. W. T. Cohen Stuart; P. Gruteke; A. van Dam; I. Maat; B. Maraha; J. C. Sinnige; E. van der Vorm; M. P. A. van Meer; Dutch MRSA surveillance study group

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, Marga van Santen-Verheuvel, Angela de Haan, Fabian Labdman, Han van der Heide, Ed J. Kuijper, Daan W. Notermans, Thijs Bosch, Antoni P. A. Hendrickx, A. L. E. van Arkel, M. A. Leversteijn-van Hall, W. Van den Bijllaardt, R. van Mansfeld, K. van Dijk, B. Zwart, B. M. W. Diederen, H. Berkhout, D. W. Notermans, A. OttK. Waar, W. Ang, J. da Silva, A. L. M. Vlek, A. G. M. Buiting, L. G. M. Bode, A. Jansz, S. Paltansing, A. J. van Griethuysen, J. R. Lo Ten Foe, M. J. C. A. van Trijp, M. Wong, A. E. Muller, M. P. M. van der Linden, M. van Rijn, S. B. Debast, E. Kolwijck, N. Al Naiemi, T. Schulin, S. Dinant, S. P. van Mens, D. C. Melles, J. W. T. Cohen Stuart, P. Gruteke, A. van Dam, I. Maat, B. Maraha, J. C. Sinnige, E. van der Vorm, M. P. A. van Meer, Dutch MRSA surveillance study group

^*Corresponding author for this work

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

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.A group of bacteria that cause difficult-to-treat infections in humans is methicillin-resistant Staphylococcus aureus (MRSA). The aim of this study was to monitor changes in the spread of MRSA, their disease causing potential and resistance to antibiotics used to treat MRSA infections. MRSA from patients and their contacts in the Netherlands were collected over a period of 12 years and characterized. This revealed new types of MRSA emerged and others disappeared. An increasing number of MRSA produces a protein called PVL toxin, enabling MRSA to cause more severe infections. Also, some people appear to carry MRSA without any disease for more than a year. These findings suggest an increasing disease potential of MRSA and possible unnoticed sources of infection. Consequently, it is important to maintain monitoring of these infections to minimize MRSA spread.Schouls et al. characterize 43,321 methicillin-resistant Staphylococcus aureus (MRSA) isolates obtained between 2008 and 2019 in the Netherlands. Genomic changes occur in the MRSA population, with increases in the 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 - 12 Sept 2023

Keywords

RESISTANT STAPHYLOCOCCUS-AUREUS
LOW-PREVALENCE
CC398 CLONE
EPIDEMIOLOGY
TRANSMISSION
ADMISSION
ST398

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Cite this

Schouls, L. M., Witteveen, S., van Santen-Verheuvel, M., de Haan, A., Labdman, F., van der Heide, H., Kuijper, E. J., Notermans, D. W., Bosch, T., Hendrickx, A. P. A., van Arkel, A. L. E., Hall, M. A. L., Van den Bijllaardt, W., van Mansfeld, R., van Dijk, K., Zwart, B., Diederen, B. M. W., Berkhout, H., Notermans, D. W., ... Dutch MRSA surveillance study group (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{f9e8d611be064bbbb5a5601f57e91986,

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 2008-2019, 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.A group of bacteria that cause difficult-to-treat infections in humans is methicillin-resistant Staphylococcus aureus (MRSA). The aim of this study was to monitor changes in the spread of MRSA, their disease causing potential and resistance to antibiotics used to treat MRSA infections. MRSA from patients and their contacts in the Netherlands were collected over a period of 12 years and characterized. This revealed new types of MRSA emerged and others disappeared. An increasing number of MRSA produces a protein called PVL toxin, enabling MRSA to cause more severe infections. Also, some people appear to carry MRSA without any disease for more than a year. These findings suggest an increasing disease potential of MRSA and possible unnoticed sources of infection. Consequently, it is important to maintain monitoring of these infections to minimize MRSA spread.Schouls et al. characterize 43,321 methicillin-resistant Staphylococcus aureus (MRSA) isolates obtained between 2008 and 2019 in the Netherlands. Genomic changes occur in the MRSA population, with increases in the proportion of PVL-positive MRSA.",

keywords = "RESISTANT STAPHYLOCOCCUS-AUREUS, LOW-PREVALENCE, CC398 CLONE, EPIDEMIOLOGY, TRANSMISSION, ADMISSION, ST398",

author = "Schouls, {Leo M.} and Sandra Witteveen and {van Santen-Verheuvel}, Marga and {de Haan}, Angela and Fabian Labdman and {van der Heide}, Han and Kuijper, {Ed J.} and Notermans, {Daan W.} and Thijs Bosch and Hendrickx, {Antoni P. A.} and {van Arkel}, {A. L. E.} and Hall, {M. A. Leversteijn-van} and {Van den Bijllaardt}, W. and {van Mansfeld}, R. and {van Dijk}, K. and B. Zwart and Diederen, {B. M. W.} and H. Berkhout and Notermans, {D. W.} and A. Ott and K. Waar and W. Ang and {da Silva}, J. and Vlek, {A. L. M.} and Buiting, {A. G. M.} and Bode, {L. G. M.} and A. Jansz and S. Paltansing and {van Griethuysen}, {A. J.} and {Ten Foe}, {J. R. Lo} and {van Trijp}, {M. J. C. A.} and M. Wong and Muller, {A. E.} and {van der Linden}, {M. P. M.} and {van Rijn}, M. and Debast, {S. B.} and E. Kolwijck and {Al Naiemi}, N. and T. Schulin and S. Dinant and {van Mens}, {S. P.} and Melles, {D. C.} and Stuart, {J. W. T. Cohen} and P. Gruteke and {van Dam}, A. and I. Maat and B. Maraha and Sinnige, {J. C.} and {van der Vorm}, E. and {van Meer}, {M. P. A.} and {Dutch MRSA surveillance study group}",

year = "2023",

month = sep,

day = "12",

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

language = "English",

volume = "3",

journal = "Communications medicine",

issn = "2730-664X",

publisher = "Nature Publishing Group",

number = "1",

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Schouls, LM, Witteveen, S, van Santen-Verheuvel, M, de Haan, A, Labdman, F, van der Heide, H, Kuijper, EJ, Notermans, DW, Bosch, T, Hendrickx, APA, van Arkel, ALE, Hall, MAL, Van den Bijllaardt, W, van Mansfeld, R, van Dijk, K, Zwart, B, Diederen, BMW, Berkhout, H, Notermans, DW, Ott, A, Waar, K, Ang, W, da Silva, J, Vlek, ALM, Buiting, AGM, Bode, LGM, Jansz, A, Paltansing, S, van Griethuysen, AJ, Ten Foe, JRL, van Trijp, MJCA, Wong, M, Muller, AE, van der Linden, MPM, van Rijn, M, Debast, SB, Kolwijck, E, Al Naiemi, N, Schulin, T, Dinant, S, van Mens, SP, Melles, DC, Stuart, JWTC, Gruteke, P, van Dam, A, Maat, I, Maraha, B, Sinnige, JC, van der Vorm, E, van Meer, MPA & Dutch MRSA surveillance study group 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 - van Santen-Verheuvel, Marga

AU - de Haan, Angela

AU - Labdman, Fabian

AU - van der Heide, Han

AU - Kuijper, Ed J.

AU - Notermans, Daan W.

AU - Bosch, Thijs

AU - Hendrickx, Antoni P. A.

AU - van Arkel, A. L. E.

AU - Hall, M. A. Leversteijn-van

AU - Van den Bijllaardt, W.

AU - van Mansfeld, R.

AU - van Dijk, K.

AU - Zwart, B.

AU - Diederen, B. M. W.

AU - Berkhout, H.

AU - Notermans, D. W.

AU - Ott, A.

AU - Waar, K.

AU - Ang, W.

AU - da Silva, J.

AU - Vlek, A. L. M.

AU - Buiting, A. G. M.

AU - Bode, L. G. M.

AU - Jansz, A.

AU - Paltansing, S.

AU - van Griethuysen, A. J.

AU - Ten Foe, J. R. Lo

AU - van Trijp, M. J. C. A.

AU - Wong, M.

AU - Muller, A. E.

AU - van der Linden, M. P. M.

AU - van Rijn, M.

AU - Debast, S. B.

AU - Kolwijck, E.

AU - Al Naiemi, N.

AU - Schulin, T.

AU - Dinant, S.

AU - van Mens, S. P.

AU - Melles, D. C.

AU - Stuart, J. W. T. Cohen

AU - Gruteke, P.

AU - van Dam, A.

AU - Maat, I.

AU - Maraha, B.

AU - Sinnige, J. C.

AU - van der Vorm, E.

AU - van Meer, M. P. A.

AU - Dutch MRSA surveillance study group

PY - 2023/9/12

Y1 - 2023/9/12

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.A group of bacteria that cause difficult-to-treat infections in humans is methicillin-resistant Staphylococcus aureus (MRSA). The aim of this study was to monitor changes in the spread of MRSA, their disease causing potential and resistance to antibiotics used to treat MRSA infections. MRSA from patients and their contacts in the Netherlands were collected over a period of 12 years and characterized. This revealed new types of MRSA emerged and others disappeared. An increasing number of MRSA produces a protein called PVL toxin, enabling MRSA to cause more severe infections. Also, some people appear to carry MRSA without any disease for more than a year. These findings suggest an increasing disease potential of MRSA and possible unnoticed sources of infection. Consequently, it is important to maintain monitoring of these infections to minimize MRSA spread.Schouls et al. characterize 43,321 methicillin-resistant Staphylococcus aureus (MRSA) isolates obtained between 2008 and 2019 in the Netherlands. Genomic changes occur in the MRSA population, with increases in the 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.A group of bacteria that cause difficult-to-treat infections in humans is methicillin-resistant Staphylococcus aureus (MRSA). The aim of this study was to monitor changes in the spread of MRSA, their disease causing potential and resistance to antibiotics used to treat MRSA infections. MRSA from patients and their contacts in the Netherlands were collected over a period of 12 years and characterized. This revealed new types of MRSA emerged and others disappeared. An increasing number of MRSA produces a protein called PVL toxin, enabling MRSA to cause more severe infections. Also, some people appear to carry MRSA without any disease for more than a year. These findings suggest an increasing disease potential of MRSA and possible unnoticed sources of infection. Consequently, it is important to maintain monitoring of these infections to minimize MRSA spread.Schouls et al. characterize 43,321 methicillin-resistant Staphylococcus aureus (MRSA) isolates obtained between 2008 and 2019 in the Netherlands. Genomic changes occur in the MRSA population, with increases in the proportion of PVL-positive MRSA.

KW - RESISTANT STAPHYLOCOCCUS-AUREUS

KW - LOW-PREVALENCE

KW - CC398 CLONE

KW - EPIDEMIOLOGY

KW - TRANSMISSION

KW - ADMISSION

KW - ST398

U2 - 10.1038/s43856-023-00348-z

DO - 10.1038/s43856-023-00348-z

M3 - Article

SN - 2730-664X

VL - 3

JO - Communications medicine

JF - Communications medicine

IS - 1

M1 - 123

ER -