An emerging Panton–Valentine leukocidin-positive CC5-meticillin-resistant Staphylococcus aureus-IVc clone recovered from hospital and community settings over a 17-year period from 12 countries investigated by whole-genome sequencing

B. K. Aloba; P. M. Kinnevey; S. Monecke; G. I. Brennan; B. O'Connell; A. Blomfeldt; B. A. McManus; W. Schneider-Brachert; J. Tkadlec; R. Ehricht; A. Senok; M. D. Bartels; D. C. Coleman

doi:10.1016/j.jhin.2022.11.015

An emerging Panton–Valentine leukocidin-positive CC5-meticillin-resistant Staphylococcus aureus-IVc clone recovered from hospital and community settings over a 17-year period from 12 countries investigated by whole-genome sequencing

B. K. Aloba, P. M. Kinnevey, S. Monecke, G. I. Brennan, B. O'Connell, A. Blomfeldt, B. A. McManus, W. Schneider-Brachert, J. Tkadlec, R. Ehricht, A. Senok, M. D. Bartels, D. C. Coleman^*

^*Corresponding author for this work

Research output: Contribution to journal › Journal article › Research › peer-review

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Abstract

Background: A novel Panton–Valentine leukocidin (PVL)-positive meticillin-resistant Staphylococcus aureus (MRSA) clonal complex (CC)5-MRSA-IVc (‘Sri Lankan’ clone) was recently described from Sri Lanka. Similar isolates caused a recent Irish hospital outbreak. Aim: To investigate the international dissemination and diversity of PVL-positive CC5-MRSA-IVc isolates from hospital and community settings using whole-genome sequencing (WGS). Methods: Core-genome single nucleotide polymorphism (cgSNP) analysis, core-genome multi-locus sequence typing (cgMLST) and microarray-based detection of antimicrobial-resistance and virulence genes were used to investigate PVL-positive CC5-MRSA-IVc (N = 214 including 46 ‘Sri Lankan’ clone) from hospital and community settings in 12 countries over 17 years. Comparators included 29 PVL-positive and 23 PVL-negative CC5/ST5-MRSA-I/II/IVa/IVc/IVg/V. Results: Maximum-likelihood cgSNP analysis grouped 209/214 (97.7%) CC5-MRSA-IVc into Clade I; average of 110 cgSNPs between isolates. Clade III contained the five remaining CC5-MRSA-IVc; average of 92 cgSNPs between isolates. Clade II contained seven PVL-positive CC5-MRSA-IVa comparators, whereas the remaining 45 comparators formed an outlier group. Minimum-spanning cgMLST analysis revealed a comparably low average of 57 allelic differences between all CC5/ST5-MRSA-IVc. All 214 CC5/ST5-MRSA-IVc were identified as ‘Sri Lankan’ clone, predominantly spa type t002 (186/214) with low population diversity and harboured a similar range of virulence genes and variable antimicrobial-resistance genes. All 214 Sri Lankan clone isolates and Clade II comparators harboured a 9616-bp chromosomal PVL-encoding phage remnant, suggesting both arose from a PVL-positive meticillin-susceptible ancestor. Over half of Sri Lankan clone isolates were from infections (142/214), and where detailed metadata were available (168/214), most were community associated (85/168). Conclusions: Stable chromosomal retention of pvl may facilitate Sri-Lankan clone dissemination.

Original language	English
Journal	Journal of Hospital Infection
Volume	132
Pages (from-to)	8-19
Number of pages	12
ISSN	0195-6701
DOIs	https://doi.org/10.1016/j.jhin.2022.11.015
Publication status	Published - Feb 2023

Bibliographical note

Publisher Copyright:
© 2022 The Author(s)

Keywords

CC5-MRSA-IVc
Dissemination
Epidemiology
Phylogenomics
PVL
Sri Lankan clone

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Aloba, B. K., Kinnevey, P. M., Monecke, S., Brennan, G. I., O'Connell, B., Blomfeldt, A., McManus, B. A., Schneider-Brachert, W., Tkadlec, J., Ehricht, R., Senok, A., Bartels, M. D., & Coleman, D. C. (2023). An emerging Panton–Valentine leukocidin-positive CC5-meticillin-resistant Staphylococcus aureus-IVc clone recovered from hospital and community settings over a 17-year period from 12 countries investigated by whole-genome sequencing. Journal of Hospital Infection, 132, 8-19. https://doi.org/10.1016/j.jhin.2022.11.015

An emerging Panton–Valentine leukocidin-positive CC5-meticillin-resistant Staphylococcus aureus-IVc clone recovered from hospital and community settings over a 17-year period from 12 countries investigated by whole-genome sequencing. / Aloba, B. K.; Kinnevey, P. M.; Monecke, S.; Brennan, G. I.; O'Connell, B.; Blomfeldt, A.; McManus, B. A.; Schneider-Brachert, W.; Tkadlec, J.; Ehricht, R.; Senok, A.; Bartels, M. D.; Coleman, D. C.

In: Journal of Hospital Infection, Vol. 132, 02.2023, p. 8-19.

Research output: Contribution to journal › Journal article › Research › peer-review

Aloba, BK, Kinnevey, PM, Monecke, S, Brennan, GI, O'Connell, B, Blomfeldt, A, McManus, BA, Schneider-Brachert, W, Tkadlec, J, Ehricht, R, Senok, A, Bartels, MD & Coleman, DC 2023, 'An emerging Panton–Valentine leukocidin-positive CC5-meticillin-resistant Staphylococcus aureus-IVc clone recovered from hospital and community settings over a 17-year period from 12 countries investigated by whole-genome sequencing', Journal of Hospital Infection, vol. 132, pp. 8-19. https://doi.org/10.1016/j.jhin.2022.11.015

Aloba BK, Kinnevey PM, Monecke S, Brennan GI, O'Connell B, Blomfeldt A et al. An emerging Panton–Valentine leukocidin-positive CC5-meticillin-resistant Staphylococcus aureus-IVc clone recovered from hospital and community settings over a 17-year period from 12 countries investigated by whole-genome sequencing. Journal of Hospital Infection. 2023 Feb;132:8-19. https://doi.org/10.1016/j.jhin.2022.11.015

Aloba, B. K. ; Kinnevey, P. M. ; Monecke, S. ; Brennan, G. I. ; O'Connell, B. ; Blomfeldt, A. ; McManus, B. A. ; Schneider-Brachert, W. ; Tkadlec, J. ; Ehricht, R. ; Senok, A. ; Bartels, M. D. ; Coleman, D. C. / An emerging Panton–Valentine leukocidin-positive CC5-meticillin-resistant Staphylococcus aureus-IVc clone recovered from hospital and community settings over a 17-year period from 12 countries investigated by whole-genome sequencing. In: Journal of Hospital Infection. 2023 ; Vol. 132. pp. 8-19.

@article{c28dd37bde004365ae1c49f76f733dca,

title = "An emerging Panton–Valentine leukocidin-positive CC5-meticillin-resistant Staphylococcus aureus-IVc clone recovered from hospital and community settings over a 17-year period from 12 countries investigated by whole-genome sequencing",

abstract = "Background: A novel Panton–Valentine leukocidin (PVL)-positive meticillin-resistant Staphylococcus aureus (MRSA) clonal complex (CC)5-MRSA-IVc ({\textquoteleft}Sri Lankan{\textquoteright} clone) was recently described from Sri Lanka. Similar isolates caused a recent Irish hospital outbreak. Aim: To investigate the international dissemination and diversity of PVL-positive CC5-MRSA-IVc isolates from hospital and community settings using whole-genome sequencing (WGS). Methods: Core-genome single nucleotide polymorphism (cgSNP) analysis, core-genome multi-locus sequence typing (cgMLST) and microarray-based detection of antimicrobial-resistance and virulence genes were used to investigate PVL-positive CC5-MRSA-IVc (N = 214 including 46 {\textquoteleft}Sri Lankan{\textquoteright} clone) from hospital and community settings in 12 countries over 17 years. Comparators included 29 PVL-positive and 23 PVL-negative CC5/ST5-MRSA-I/II/IVa/IVc/IVg/V. Results: Maximum-likelihood cgSNP analysis grouped 209/214 (97.7%) CC5-MRSA-IVc into Clade I; average of 110 cgSNPs between isolates. Clade III contained the five remaining CC5-MRSA-IVc; average of 92 cgSNPs between isolates. Clade II contained seven PVL-positive CC5-MRSA-IVa comparators, whereas the remaining 45 comparators formed an outlier group. Minimum-spanning cgMLST analysis revealed a comparably low average of 57 allelic differences between all CC5/ST5-MRSA-IVc. All 214 CC5/ST5-MRSA-IVc were identified as {\textquoteleft}Sri Lankan{\textquoteright} clone, predominantly spa type t002 (186/214) with low population diversity and harboured a similar range of virulence genes and variable antimicrobial-resistance genes. All 214 Sri Lankan clone isolates and Clade II comparators harboured a 9616-bp chromosomal PVL-encoding phage remnant, suggesting both arose from a PVL-positive meticillin-susceptible ancestor. Over half of Sri Lankan clone isolates were from infections (142/214), and where detailed metadata were available (168/214), most were community associated (85/168). Conclusions: Stable chromosomal retention of pvl may facilitate Sri-Lankan clone dissemination.",

keywords = "CC5-MRSA-IVc, Dissemination, Epidemiology, Phylogenomics, PVL, Sri Lankan clone",

author = "Aloba, {B. K.} and Kinnevey, {P. M.} and S. Monecke and Brennan, {G. I.} and B. O'Connell and A. Blomfeldt and McManus, {B. A.} and W. Schneider-Brachert and J. Tkadlec and R. Ehricht and A. Senok and Bartels, {M. D.} and Coleman, {D. C.}",

note = "Publisher Copyright: {\textcopyright} 2022 The Author(s)",

year = "2023",

month = feb,

doi = "10.1016/j.jhin.2022.11.015",

language = "English",

volume = "132",

pages = "8--19",

journal = "Journal of Hospital Infection",

issn = "0195-6701",

publisher = "W.B.Saunders Co. Ltd.",

}

TY - JOUR

T1 - An emerging Panton–Valentine leukocidin-positive CC5-meticillin-resistant Staphylococcus aureus-IVc clone recovered from hospital and community settings over a 17-year period from 12 countries investigated by whole-genome sequencing

AU - Aloba, B. K.

AU - Kinnevey, P. M.

AU - Monecke, S.

AU - Brennan, G. I.

AU - O'Connell, B.

AU - Blomfeldt, A.

AU - McManus, B. A.

AU - Schneider-Brachert, W.

AU - Tkadlec, J.

AU - Ehricht, R.

AU - Senok, A.

AU - Bartels, M. D.

AU - Coleman, D. C.

PY - 2023/2

Y1 - 2023/2

N2 - Background: A novel Panton–Valentine leukocidin (PVL)-positive meticillin-resistant Staphylococcus aureus (MRSA) clonal complex (CC)5-MRSA-IVc (‘Sri Lankan’ clone) was recently described from Sri Lanka. Similar isolates caused a recent Irish hospital outbreak. Aim: To investigate the international dissemination and diversity of PVL-positive CC5-MRSA-IVc isolates from hospital and community settings using whole-genome sequencing (WGS). Methods: Core-genome single nucleotide polymorphism (cgSNP) analysis, core-genome multi-locus sequence typing (cgMLST) and microarray-based detection of antimicrobial-resistance and virulence genes were used to investigate PVL-positive CC5-MRSA-IVc (N = 214 including 46 ‘Sri Lankan’ clone) from hospital and community settings in 12 countries over 17 years. Comparators included 29 PVL-positive and 23 PVL-negative CC5/ST5-MRSA-I/II/IVa/IVc/IVg/V. Results: Maximum-likelihood cgSNP analysis grouped 209/214 (97.7%) CC5-MRSA-IVc into Clade I; average of 110 cgSNPs between isolates. Clade III contained the five remaining CC5-MRSA-IVc; average of 92 cgSNPs between isolates. Clade II contained seven PVL-positive CC5-MRSA-IVa comparators, whereas the remaining 45 comparators formed an outlier group. Minimum-spanning cgMLST analysis revealed a comparably low average of 57 allelic differences between all CC5/ST5-MRSA-IVc. All 214 CC5/ST5-MRSA-IVc were identified as ‘Sri Lankan’ clone, predominantly spa type t002 (186/214) with low population diversity and harboured a similar range of virulence genes and variable antimicrobial-resistance genes. All 214 Sri Lankan clone isolates and Clade II comparators harboured a 9616-bp chromosomal PVL-encoding phage remnant, suggesting both arose from a PVL-positive meticillin-susceptible ancestor. Over half of Sri Lankan clone isolates were from infections (142/214), and where detailed metadata were available (168/214), most were community associated (85/168). Conclusions: Stable chromosomal retention of pvl may facilitate Sri-Lankan clone dissemination.

AB - Background: A novel Panton–Valentine leukocidin (PVL)-positive meticillin-resistant Staphylococcus aureus (MRSA) clonal complex (CC)5-MRSA-IVc (‘Sri Lankan’ clone) was recently described from Sri Lanka. Similar isolates caused a recent Irish hospital outbreak. Aim: To investigate the international dissemination and diversity of PVL-positive CC5-MRSA-IVc isolates from hospital and community settings using whole-genome sequencing (WGS). Methods: Core-genome single nucleotide polymorphism (cgSNP) analysis, core-genome multi-locus sequence typing (cgMLST) and microarray-based detection of antimicrobial-resistance and virulence genes were used to investigate PVL-positive CC5-MRSA-IVc (N = 214 including 46 ‘Sri Lankan’ clone) from hospital and community settings in 12 countries over 17 years. Comparators included 29 PVL-positive and 23 PVL-negative CC5/ST5-MRSA-I/II/IVa/IVc/IVg/V. Results: Maximum-likelihood cgSNP analysis grouped 209/214 (97.7%) CC5-MRSA-IVc into Clade I; average of 110 cgSNPs between isolates. Clade III contained the five remaining CC5-MRSA-IVc; average of 92 cgSNPs between isolates. Clade II contained seven PVL-positive CC5-MRSA-IVa comparators, whereas the remaining 45 comparators formed an outlier group. Minimum-spanning cgMLST analysis revealed a comparably low average of 57 allelic differences between all CC5/ST5-MRSA-IVc. All 214 CC5/ST5-MRSA-IVc were identified as ‘Sri Lankan’ clone, predominantly spa type t002 (186/214) with low population diversity and harboured a similar range of virulence genes and variable antimicrobial-resistance genes. All 214 Sri Lankan clone isolates and Clade II comparators harboured a 9616-bp chromosomal PVL-encoding phage remnant, suggesting both arose from a PVL-positive meticillin-susceptible ancestor. Over half of Sri Lankan clone isolates were from infections (142/214), and where detailed metadata were available (168/214), most were community associated (85/168). Conclusions: Stable chromosomal retention of pvl may facilitate Sri-Lankan clone dissemination.

KW - CC5-MRSA-IVc

KW - Dissemination

KW - Epidemiology

KW - Phylogenomics

KW - PVL

KW - Sri Lankan clone

U2 - 10.1016/j.jhin.2022.11.015

DO - 10.1016/j.jhin.2022.11.015

M3 - Journal article

C2 - 36481685

AN - SCOPUS:85145710218

VL - 132

SP - 8

EP - 19

JO - Journal of Hospital Infection

JF - Journal of Hospital Infection

SN - 0195-6701

ER -