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2. Evolution of MRSA during hospital transmission and intercontinental spread

Author

Harris, Simon R., Feil, Edward J., Holden, Matthew T.G., Quail, Michael A., Nickerson, Emma K., Chantratita, Narisara, Gardete, Susana, Tavares, Ana, Day, Nick, Lindsay, Jodi A., Edgeworth, Jonathan D., de Lencastre, Herminia, Parkhill, Julian, Peacock, Sharon J., and Bentley, Stephen D.

Subjects
Epidemiology -- Analysis, Genomics -- Analysis, Bacteria, Pathogenic -- Genetic aspects, Staphylococcus aureus -- Research, Science and technology
Abstract

Current methods for differentiating isolates of predominant lineages of pathogenic bacteria often do not provide sufficient resolution to define precise relationships. Here, we describe a high-throughput genomics approach that provides a high-resolution view of the epidemiology and microevolution of a dominant strain of methicillin-resistant Staphylococcus aureus (MRSA). This approach reveals the global geographic structure within the lineage, its intercontinental transmission through four decades, and the potential to trace person-to-person transmission within a hospital environment. The ability to interrogate and resolve bacterial populations is applicable to a range of infectious diseases, as well as microbial ecology. 10.1126/science.1182395

Published
2010
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4. Author response: Improved characterisation of MRSA transmission using within-host bacterial sequence diversity

Author

Hall, Matthew D, primary, Holden, Matthew TG, additional, Srisomang, Pramot, additional, Mahavanakul, Weera, additional, Wuthiekanun, Vanaporn, additional, Limmathurotsakul, Direk, additional, Fountain, Kay, additional, Parkhill, Julian, additional, Nickerson, Emma K, additional, Peacock, Sharon J, additional, and Fraser, Christophe, additional

Published
2019
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5. Panton–Valentine leucocidin is the key determinant of Staphylococcus aureus pyomyositis in a bacterial GWAS

Author

Young, Bernadette C, primary, Earle, Sarah G, additional, Soeng, Sona, additional, Sar, Poda, additional, Kumar, Varun, additional, Hor, Songly, additional, Sar, Vuthy, additional, Bousfield, Rachel, additional, Sanderson, Nicholas D, additional, Barker, Leanne, additional, Stoesser, Nicole, additional, Emary, Katherine RW, additional, Parry, Christopher M, additional, Nickerson, Emma K, additional, Turner, Paul, additional, Bowden, Rory, additional, Crook, Derrick W, additional, Wyllie, David H, additional, Day, Nicholas PJ, additional, Wilson, Daniel J, additional, and Moore, Catrin E, additional

Published
2019
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6. Author response: Panton–Valentine leucocidin is the key determinant of Staphylococcus aureus pyomyositis in a bacterial GWAS

Author

Young, Bernadette C, primary, Earle, Sarah G, additional, Soeng, Sona, additional, Sar, Poda, additional, Kumar, Varun, additional, Hor, Songly, additional, Sar, Vuthy, additional, Bousfield, Rachel, additional, Sanderson, Nicholas D, additional, Barker, Leanne, additional, Stoesser, Nicole, additional, Emary, Katherine RW, additional, Parry, Christopher M, additional, Nickerson, Emma K, additional, Turner, Paul, additional, Bowden, Rory, additional, Crook, Derrick W, additional, Wyllie, David H, additional, Day, Nicholas PJ, additional, Wilson, Daniel J, additional, and Moore, Catrin E, additional

Published
2019
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7. Panton-Valentine leucocidin is the key determinant of Staphylococcus aureus pyomyositis in a bacterial genome-wide association study

Author

Young, Bernadette C, primary, Earle, Sarah G, additional, Soeng, Sona, additional, Sar, Poda, additional, Kumar, Varun, additional, Hor, Songly, additional, Sar, Vuthy, additional, Bousfield, Rachel, additional, Sanderson, Nicholas D, additional, Barker, Leanne, additional, Stoesser, Nicole, additional, Emary, Katherine RW, additional, Parry, Christopher M, additional, Nickerson, Emma K, additional, Turner, Paul, additional, Bowden, Rory, additional, Crook, Derrick, additional, Wyllie, David, additional, Day, Nicholas PJ, additional, Wilson, Daniel J, additional, and Moore, Catrin E, additional

Published
2018
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8. Evolution of the Staphylococcus argenteus ST2250 Clone in Northeastern Thailand Is Linked with the Acquisition of Livestock-Associated Staphylococcal Genes

Author

Moradigaravand, Danesh, primary, Jamrozy, Dorota, additional, Mostowy, Rafal, additional, Anderson, Annaliesa, additional, Nickerson, Emma K., additional, Thaipadungpanit, Janjira, additional, Wuthiekanun, Vanaporn, additional, Limmathurotsakul, Direk, additional, Tandhavanant, Sarunporn, additional, Wikraiphat, Chanthiwa, additional, Wongsuvan, Gumphol, additional, Teerawattanasook, Nittaya, additional, Jutrakul, Yaowaruk, additional, Srisurat, Nuttiya, additional, Chaimanee, Prajuab, additional, Eoin West, T., additional, Blane, Beth, additional, Parkhill, Julian, additional, Chantratita, Narisara, additional, and Peacock, Sharon J., additional

Published
2017
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10. Genome sequencing defines phylogeny and spread of methicillin-resistant Staphylococcus aureus in a high transmission setting

Author

Tong, Steven Y. C., Holden, Matthew T.G., Nickerson, Emma K., Cooper, Ben S., Köser, Claudio U., Cori, Anne, Jombart, Thibaut, Cauchemez, Simon, Fraser, Christophe, Wuthiekanun, Vanaporn, Thaipadungpanit, Janjira, Hongsuwan, Maliwan, Day, Nicholas P. J., Limmathurotsakul, Direk, Parkhill, Julian, Peacock, Sharon J., Tong, Steven Y. C., Holden, Matthew T.G., Nickerson, Emma K., Cooper, Ben S., Köser, Claudio U., Cori, Anne, Jombart, Thibaut, Cauchemez, Simon, Fraser, Christophe, Wuthiekanun, Vanaporn, Thaipadungpanit, Janjira, Hongsuwan, Maliwan, Day, Nicholas P. J., Limmathurotsakul, Direk, Parkhill, Julian, and Peacock, Sharon J.

Abstract

Methicillin-resistant Staphylococcus aureus (MRSA) is a major cause of nosocomial infection. Whole-genome sequencing of MRSA has been used to define phylogeny and transmission in well-resourced healthcare settings, yet the greatest burden of nosocomial infection occurs in resource-restricted settings where barriers to transmission are lower. Here, we study the flux and genetic diversity of MRSA on ward and individual patient levels in a hospital where transmission was common. We repeatedly screened all patients on two intensive care units for MRSA carriage over a 3-mo period. All MRSA belonged to multilocus sequence type 239 (ST 239). We defined the population structure and charted the spread of MRSA by sequencing 79 isolates from 46 patients and five members of staff, including the first MRSA-positive screen isolates and up to two repeat isolates where available. Phylogenetic analysis identified a flux of distinct ST 239 clades over time in each intensive care unit. In total, five main clades were identified, which varied in the carriage of plasmids encoding antiseptic and antimicrobial resistance determinants. Sequence data confirmed intra- and interwards transmission events and identified individual patients who were colonized by more than one clade. One patient on each unit was the source of numerous transmission events, and deep sampling of one of these cases demonstrated colonization with a “cloud” of related MRSA variants. The application of whole-genome sequencing and analysis provides novel insights into the transmission of MRSA in under-resourced healthcare settings and has relevance to wider global health.

Published
2015

12. Genome sequencing defines phylogeny and spread of methicillin-resistant Staphylococcus aureus in a high transmission setting

Author

Tong, Steven Y.C., primary, Holden, Matthew T.G., additional, Nickerson, Emma K., additional, Cooper, Ben S., additional, Köser, Claudio U., additional, Cori, Anne, additional, Jombart, Thibaut, additional, Cauchemez, Simon, additional, Fraser, Christophe, additional, Wuthiekanun, Vanaporn, additional, Thaipadungpanit, Janjira, additional, Hongsuwan, Maliwan, additional, Day, Nicholas P., additional, Limmathurotsakul, Direk, additional, Parkhill, Julian, additional, and Peacock, Sharon J., additional

Published
2014
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13. Correction: Feasibility of Modified Surviving Sepsis Campaign Guidelines in a Resource-Restricted Setting Based on a Cohort Study of Severe S. Aureus Sepsis

Author

Mahavanakul, Weera, primary, Nickerson, Emma K., additional, Srisomang, Pramot, additional, Teparrukkul, Prapit, additional, Lorvinitnun, Pichet, additional, Wongyingsinn, Mingkwan, additional, Chierakul, Wirongrong, additional, Hongsuwan, Maliwan, additional, West, T. Eoin, additional, Day, Nicholas P., additional, Limmathurotsakul, Direk, additional, and Peacock, Sharon J., additional

Published
2012
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14. Feasibility of Modified Surviving Sepsis Campaign Guidelines in a Resource-Restricted Setting Based on a Cohort Study of Severe S. Aureus Sepsis

Author

Mahavanakul, Weera, primary, Nickerson, Emma K., additional, Srisomang, Pramot, additional, Teparrukkul, Prapit, additional, Lorvinitnun, Pichet, additional, Wongyingsinn, Mingkwan, additional, Chierakul, Wirongrong, additional, Hongsuwan, Maliwan, additional, West, T. Eoin, additional, Day, Nicholas P., additional, Limmathurotsakul, Direk, additional, and Peacock, Sharon J., additional

Published
2012
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15. Emergence of Community-Associated Methicillin-Resistant Staphylococcus aureus Carriage in Children in Cambodia

Author

Nickerson, Emma K., primary, Amornchai, Premjit, additional, Wuthiekanun, Vanaporn, additional, Wongdeethai, Nattavut, additional, Peacock, Sharon J., additional, Putchhat, Hor, additional, Thaipadungpanit, Janjira, additional, Chheng, Kheng, additional, Kumar, Varun, additional, Day, Nicholas P., additional, and Chantratita, Narisara, additional

Published
2011
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16. Factors Predicting and Reducing Mortality in Patients with Invasive Staphylococcus aureus Disease in a Developing Country

Author

Nickerson, Emma K., primary, Wuthiekanun, Vanaporn, additional, Wongsuvan, Gumphol, additional, Limmathurosakul, Direk, additional, Srisamang, Pramot, additional, Mahavanakul, Weera, additional, Thaipadungpanit, Janjira, additional, Shah, Krupal R., additional, Arayawichanont, Arkhom, additional, Amornchai, Premjit, additional, Thanwisai, Aunchalee, additional, Day, Nicholas P., additional, and Peacock, Sharon J., additional

Published
2009
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17. Staphylococcus aureus Bacteraemia in a Tropical Setting: Patient Outcome and Impact of Antibiotic Resistance

Author

Nickerson, Emma K., primary, Hongsuwan, Maliwan, additional, Limmathurotsakul, Direk, additional, Wuthiekanun, Vanaporn, additional, Shah, Krupal R., additional, Srisomang, Pramot, additional, Mahavanakul, Weera, additional, Wacharaprechasgul, Therapon, additional, Fowler, Vance G., additional, West, T. Eoin, additional, Teerawatanasuk, Nitaya, additional, Becher, Harald, additional, White, Nicholas J., additional, Chierakul, Wirongrong, additional, Day, Nicholas P., additional, and Peacock, Sharon J., additional

Published
2009
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18. Rapid Detection of the Pandemic Methicillin-Resistant Staphylococcus aureus Clone ST 239, a Dominant Strain in Asian Hospitals

Author

Feil, Edward J., primary, Nickerson, Emma K., additional, Chantratita, Narisara, additional, Wuthiekanun, Vanaporn, additional, Srisomang, Pramot, additional, Cousins, Richard, additional, Pan, WuBin, additional, Zhang, Ge, additional, Xu, BangLao, additional, Day, Nicholas P. J., additional, and Peacock, Sharon J., additional

Published
2008
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20. Genome sequencing defines phylogeny and spread of methicillin-resistant Staphylococcus aureusin a high transmission setting

Author

Tong, Steven Y.C., Holden, Matthew T.G., Nickerson, Emma K., Cooper, Ben S., Köser, Claudio U., Cori, Anne, Jombart, Thibaut, Cauchemez, Simon, Fraser, Christophe, Wuthiekanun, Vanaporn, Thaipadungpanit, Janjira, Hongsuwan, Maliwan, Day, Nicholas P., Limmathurotsakul, Direk, Parkhill, Julian, and Peacock, Sharon J.

Abstract

Methicillin-resistant Staphylococcus aureus(MRSA) is a major cause of nosocomial infection. Whole-genome sequencing of MRSA has been used to define phylogeny and transmission in well-resourced healthcare settings, yet the greatest burden of nosocomial infection occurs in resource-restricted settings where barriers to transmission are lower. Here, we study the flux and genetic diversity of MRSA on ward and individual patient levels in a hospital where transmission was common. We repeatedly screened all patients on two intensive care units for MRSA carriage over a 3-mo period. All MRSA belonged to multilocus sequence type 239 (ST 239). We defined the population structure and charted the spread of MRSA by sequencing 79 isolates from 46 patients and five members of staff, including the first MRSA-positive screen isolates and up to two repeat isolates where available. Phylogenetic analysis identified a flux of distinct ST 239 clades over time in each intensive care unit. In total, five main clades were identified, which varied in the carriage of plasmids encoding antiseptic and antimicrobial resistance determinants. Sequence data confirmed intra- and interwards transmission events and identified individual patients who were colonized by more than one clade. One patient on each unit was the source of numerous transmission events, and deep sampling of one of these cases demonstrated colonization with a “cloud” of related MRSA variants. The application of whole-genome sequencing and analysis provides novel insights into the transmission of MRSA in under-resourced healthcare settings and has relevance to wider global health.

Published
2015
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21. Clinical and Molecular Epidemiology of Staphylococcus argenteusInfections in Thailand

Author

Thaipadungpanit, Janjira, Amornchai, Premjit, Nickerson, Emma K., Wongsuvan, Gumphol, Wuthiekanun, Vanaporn, Limmathurotsakul, Direk, and Peacock, Sharon J.

Abstract

ABSTRACTMolecular typing of 246 Staphylococcus aureusisolates from unselected patients in Thailand showed that 10 (4.1%) were actually Staphylococcus argenteus. Contrary to the suggestion that S. argenteusis less virulent than S. aureus, we demonstrated comparable rates of morbidity, death, and health care-associated infection in patients infected with either of these two species.

Published
2014
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22. Rapid Detection of the Pandemic Methicillin-Resistant Staphylococcus aureusClone ST 239, a Dominant Strain in Asian Hospitals

Author

Feil, Edward J., Nickerson, Emma K., Chantratita, Narisara, Wuthiekanun, Vanaporn, Srisomang, Pramot, Cousins, Richard, Pan, WuBin, Zhang, Ge, Xu, BangLao, Day, Nicholas P. J., and Peacock, Sharon J.

Abstract

ABSTRACTWe describe and validate a novel PCR assay to detect the pandemic hospital-acquired methicillin-resistant Staphylococcus aureus(HA-MRSA) lineage ST 239. Results based on previously uncharacterized isolates from a hospital in northeast Thailand support the view that at least 90% of HA-MRSA isolates in mainland Asia correspond to ST 239 or close relatives.

Published
2008
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23. Improved characterisation of MRSA transmission using within-host bacterial sequence diversity

Author

Hall, Matthew D, Holden, Matthew Tg, Srisomang, Pramot, Mahavanakul, Weera, Wuthiekanun, Vanaporn, Limmathurotsakul, Direk, Fountain, Kay, Parkhill, Julian, Nickerson, Emma K, Peacock, Sharon J, and Fraser, Christophe

Subjects
Adult, DNA, Bacterial, Methicillin-Resistant Staphylococcus aureus, hospital infections, Cross Infection, Whole Genome Sequencing, global health, Computational Biology, Genetic Variation, MRSA, Staphylococcal Infections, Thailand, molecular epidemiology, Polymorphism, Single Nucleotide, 3. Good health, Disease Outbreaks, Humans, epidemiology, human, Child, Genome, Bacterial, Phylogeny
Abstract

Methicillin-resistant Staphylococcus aureus (MRSA) transmission in the hospital setting has been a frequent subject of investigation using bacterial genomes, but previous approaches have not yet fully utilised the extra deductive power provided when multiple pathogen samples are acquired from each host. Here, we used a large dataset of MRSA sequences from multiply-sampled patients to reconstruct colonisation of individuals in a high-transmission setting in a hospital in Thailand. We reconstructed transmission trees for MRSA. We also investigated transmission between anatomical sites on the same individual, finding that this either occurs repeatedly or involves a wide transmission bottleneck. We examined the between-subject bottleneck, finding considerable variation in the amount of diversity transmitted. Finally, we compared our approach to the simpler method of identifying transmission pairs using single nucleotide polymorphism (SNP) counts. This suggested that the optimum threshold for identifying a pair is 39 SNPs, if sensitivities and specificities are equally weighted.

24. Improved characterisation of MRSA transmission using within-host bacterial sequence diversity

Author

Hall, Matthew D, Holden, Matthew TG, Srisomang, Pramot, Mahavanakul, Weera, Wuthiekanun, Vanaporn, Limmathurotsakul, Direk, Fountain, Kay, Parkhill, Julian, Nickerson, Emma K, Peacock, Sharon J, and Fraser, Christophe

Subjects
hospital infections, Epidemiology and Global Health, MRSA, Other, molecular epidemiology, 3. Good health, Research Article, Human
Abstract

Methicillin-resistant Staphylococcus aureus (MRSA) transmission in the hospital setting has been a frequent subject of investigation using bacterial genomes, but previous approaches have not yet fully utilised the extra deductive power provided when multiple pathogen samples are acquired from each host. Here, we used a large dataset of MRSA sequences from multiply-sampled patients to reconstruct colonisation of individuals in a high-transmission setting in a hospital in Thailand. We reconstructed transmission trees for MRSA. We also investigated transmission between anatomical sites on the same individual, finding that this either occurs repeatedly or involves a wide transmission bottleneck. We examined the between-subject bottleneck, finding considerable variation in the amount of diversity transmitted. Finally, we compared our approach to the simpler method of identifying transmission pairs using single nucleotide polymorphism (SNP) counts. This suggested that the optimum threshold for identifying a pair is 39 SNPs, if sensitivities and specificities are equally weighted.

25. Evolution of the Staphylococcus argenteusST2250 Clone in Northeastern Thailand Is Linked with the Acquisition of Livestock-Associated Staphylococcal Genes

Author

Moradigaravand, Danesh, Jamrozy, Dorota, Mostowy, Rafal, Anderson, Annaliesa, Nickerson, Emma K., Thaipadungpanit, Janjira, Wuthiekanun, Vanaporn, Limmathurotsakul, Direk, Tandhavanant, Sarunporn, Wikraiphat, Chanthiwa, Wongsuvan, Gumphol, Teerawattanasook, Nittaya, Jutrakul, Yaowaruk, Srisurat, Nuttiya, Chaimanee, Prajuab, Eoin West, T., Blane, Beth, Parkhill, Julian, Chantratita, Narisara, and Peacock, Sharon J.

Abstract

ABSTRACTStaphylococcus argenteusis a newly named species previously described as a divergent lineage of Staphylococcus aureusthat has recently been shown to have a global distribution. Despite growing evidence of the clinical importance of this species, knowledge about its population epidemiology and genomic architecture is limited. We used whole-genome sequencing to evaluate and compare S. aureus(n= 251) and S. argenteus(n= 68) isolates from adults with staphylococcal sepsis at several hospitals in northeastern Thailand between 2006 and 2013. The majority (82%) of the S. argenteusisolates were of multilocus sequence type 2250 (ST2250). S. aureuswas more diverse, although 43% of the isolates belonged to ST121. Bayesian analysis suggested an S. argenteusST2250 substitution rate of 4.66 (95% confidence interval [CI], 3.12 to 6.38) mutations per genome per year, which was comparable to the S. aureusST121 substitution rate of 4.07 (95% CI, 2.61 to 5.55). S. argenteusST2250 emerged in Thailand an estimated 15 years ago, which contrasts with the S. aureusST1, ST88, and ST121 clades that emerged around 100 to 150 years ago. Comparison of S. argenteusST2250 genomes from Thailand and a global collection indicated a single introduction into Thailand, followed by transmission to local and more distant countries in Southeast Asia and further afield. S. argenteusand S. aureusshared around half of their core gene repertoire, indicating a high level of divergence and providing strong support for their classification as separate species. Several gene clusters were present in ST2250 isolates but absent from the other S. argenteusand S. aureusstudy isolates. These included multiple exotoxins and antibiotic resistance genes that have been linked previously with livestock-associated S. aureus, consistent with a livestock reservoir for S. argenteus. These genes appeared to be associated with plasmids and mobile genetic elements and may have contributed to the biological success of ST2250.IMPORTANCEIn this study, we used whole-genome sequencing to understand the genome evolution and population structure of a systematic collection of ST2250 S. argenteusisolates. A newly identified ancestral species of S. aureus, S. argenteushas become increasingly known as a clinically important species that has been reported recently across various countries. Our results indicate that S. argenteushas spread at a relatively rapid pace over the past 2 decades across northeastern Thailand and acquired multiple exotoxin and antibiotic resistance genes that have been linked previously with livestock-associated S. aureus. Our findings highlight the clinical importance and potential pathogenicity of S. argenteusas a recently emerging pathogen.

Published
2017
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26. Genome sequencing defines phylogeny and spread of methicillin-resistant Staphylococcus aureus in a high transmission setting.

Author

Tong SY, Holden MT, Nickerson EK, Cooper BS, Köser CU, Cori A, Jombart T, Cauchemez S, Fraser C, Wuthiekanun V, Thaipadungpanit J, Hongsuwan M, Day NP, Limmathurotsakul D, Parkhill J, and Peacock SJ

Subjects
Adult, Bacterial Typing Techniques, Child, Computational Biology, DNA, Bacterial genetics, High-Throughput Nucleotide Sequencing, Humans, Linear Models, Methicillin-Resistant Staphylococcus aureus classification, Polymorphism, Single Nucleotide, Prospective Studies, Sequence Analysis, DNA, Staphylococcal Infections microbiology, Cross Infection microbiology, Disease Outbreaks, Methicillin-Resistant Staphylococcus aureus genetics, Phylogeny
Abstract

Methicillin-resistant Staphylococcus aureus (MRSA) is a major cause of nosocomial infection. Whole-genome sequencing of MRSA has been used to define phylogeny and transmission in well-resourced healthcare settings, yet the greatest burden of nosocomial infection occurs in resource-restricted settings where barriers to transmission are lower. Here, we study the flux and genetic diversity of MRSA on ward and individual patient levels in a hospital where transmission was common. We repeatedly screened all patients on two intensive care units for MRSA carriage over a 3-mo period. All MRSA belonged to multilocus sequence type 239 (ST 239). We defined the population structure and charted the spread of MRSA by sequencing 79 isolates from 46 patients and five members of staff, including the first MRSA-positive screen isolates and up to two repeat isolates where available. Phylogenetic analysis identified a flux of distinct ST 239 clades over time in each intensive care unit. In total, five main clades were identified, which varied in the carriage of plasmids encoding antiseptic and antimicrobial resistance determinants. Sequence data confirmed intra- and interwards transmission events and identified individual patients who were colonized by more than one clade. One patient on each unit was the source of numerous transmission events, and deep sampling of one of these cases demonstrated colonization with a "cloud" of related MRSA variants. The application of whole-genome sequencing and analysis provides novel insights into the transmission of MRSA in under-resourced healthcare settings and has relevance to wider global health., (© 2015 Tong et al.; Published by Cold Spring Harbor Laboratory Press.)

Published
2015
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