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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">A Field Guide to Pandemic, Epidemic and Sporadic Clones of
Methicillin-Resistant <italic>Staphylococcus aureus</italic></title><author><name sortKey="Monecke, Stefan" sort="Monecke, Stefan" uniqKey="Monecke S" first="Stefan" last="Monecke">Stefan Monecke</name><affiliation><nlm:aff id="aff1"><addr-line>Institute for Medical Microbiology and Hygiene, Technical University of Dresden, Dresden, Germany</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff13"><addr-line>Alere Technologies GmbH, Jena, Germany</addr-line></nlm:aff></affiliation></author><author><name sortKey="Coombs, Geoffrey" sort="Coombs, Geoffrey" uniqKey="Coombs G" first="Geoffrey" last="Coombs">Geoffrey Coombs</name><affiliation><nlm:aff id="aff2"><addr-line>Department of Microbiology and Infectious Diseases, PathWest Laboratory Medicine - WA, Royal Perth Hospital, Perth, Western Australia, Australia</addr-line></nlm:aff></affiliation></author><author><name sortKey="Shore, Anna C" sort="Shore, Anna C" uniqKey="Shore A" first="Anna C." last="Shore">Anna C. Shore</name><affiliation><nlm:aff id="aff3"><addr-line>Microbiology Research Unit, Dublin Dental University Hospital, University of Dublin, Trinity College, Dublin, Ireland</addr-line></nlm:aff></affiliation></author><author><name sortKey="Coleman, David C" sort="Coleman, David C" uniqKey="Coleman D" first="David C." last="Coleman">David C. Coleman</name><affiliation><nlm:aff id="aff3"><addr-line>Microbiology Research Unit, Dublin Dental University Hospital, University of Dublin, Trinity College, Dublin, Ireland</addr-line></nlm:aff></affiliation></author><author><name sortKey="Akpaka, Patrick" sort="Akpaka, Patrick" uniqKey="Akpaka P" first="Patrick" last="Akpaka">Patrick Akpaka</name><affiliation><nlm:aff id="aff4"><addr-line>Department of Para-Clinical Sciences, The University of the West Indies, St. Augustine, Trinidad and Tobago</addr-line></nlm:aff></affiliation></author><author><name sortKey="Borg, Michael" sort="Borg, Michael" uniqKey="Borg M" first="Michael" last="Borg">Michael Borg</name><affiliation><nlm:aff id="aff5"><addr-line>Infection Control Unit, Mater Dei Hospital, Msida, Malta</addr-line></nlm:aff></affiliation></author><author><name sortKey="Chow, Henry" sort="Chow, Henry" uniqKey="Chow H" first="Henry" last="Chow">Henry Chow</name><affiliation><nlm:aff id="aff6"><addr-line>Department of Microbiology, Faculty of Medicine, The Chinese University of Hong Kong, Shatin, Hong Kong, China</addr-line></nlm:aff></affiliation></author><author><name sortKey="Ip, Margaret" sort="Ip, Margaret" uniqKey="Ip M" first="Margaret" last="Ip">Margaret Ip</name><affiliation><nlm:aff id="aff6"><addr-line>Department of Microbiology, Faculty of Medicine, The Chinese University of Hong Kong, Shatin, Hong Kong, China</addr-line></nlm:aff></affiliation></author><author><name sortKey="Jatzwauk, Lutz" sort="Jatzwauk, Lutz" uniqKey="Jatzwauk L" first="Lutz" last="Jatzwauk">Lutz Jatzwauk</name><affiliation><nlm:aff id="aff7"><addr-line>Infection Control Unit, Dresden University Hospital, Dresden, Germany</addr-line></nlm:aff></affiliation></author><author><name sortKey="Jonas, Daniel" sort="Jonas, Daniel" uniqKey="Jonas D" first="Daniel" last="Jonas">Daniel Jonas</name><affiliation><nlm:aff id="aff8"><addr-line>Department of Environmental Health Sciences, Freiburg University Medical Centre, Freiburg, Germany</addr-line></nlm:aff></affiliation></author><author><name sortKey="Kadlec, Kristina" sort="Kadlec, Kristina" uniqKey="Kadlec K" first="Kristina" last="Kadlec">Kristina Kadlec</name><affiliation><nlm:aff id="aff9"><addr-line>Institute of Farm Animal Genetics, Friedrich-Loeffler-Institut (FLI), Neustadt-Mariensee, Germany</addr-line></nlm:aff></affiliation></author><author><name sortKey="Kearns, Angela" sort="Kearns, Angela" uniqKey="Kearns A" first="Angela" last="Kearns">Angela Kearns</name><affiliation><nlm:aff id="aff10"><addr-line>Staphylococcus Reference Unit, Centre for Infections, Health Protection Agency, London, United Kingdom</addr-line></nlm:aff></affiliation></author><author><name sortKey="Laurent, Frederic" sort="Laurent, Frederic" uniqKey="Laurent F" first="Frederic" last="Laurent">Frederic Laurent</name><affiliation><nlm:aff id="aff11"><addr-line>Université Lyon, Centre National de Référence des Staphylocoques, Lyon, France</addr-line></nlm:aff></affiliation></author><author><name sortKey="O Brien, Frances G" sort="O Brien, Frances G" uniqKey="O Brien F" first="Frances G." last="O'Brien">Frances G. O'Brien</name><affiliation><nlm:aff id="aff12"><addr-line>School of Biomedical Sciences, Curtin University, Perth, Western Australia, Australia</addr-line></nlm:aff></affiliation></author><author><name sortKey="Pearson, Julie" sort="Pearson, Julie" uniqKey="Pearson J" first="Julie" last="Pearson">Julie Pearson</name><affiliation><nlm:aff id="aff2"><addr-line>Department of Microbiology and Infectious Diseases, PathWest Laboratory Medicine - WA, Royal Perth Hospital, Perth, Western Australia, Australia</addr-line></nlm:aff></affiliation></author><author><name sortKey="Ruppelt, Antje" sort="Ruppelt, Antje" uniqKey="Ruppelt A" first="Antje" last="Ruppelt">Antje Ruppelt</name><affiliation><nlm:aff id="aff1"><addr-line>Institute for Medical Microbiology and Hygiene, Technical University of Dresden, Dresden, Germany</addr-line></nlm:aff></affiliation></author><author><name sortKey="Schwarz, Stefan" sort="Schwarz, Stefan" uniqKey="Schwarz S" first="Stefan" last="Schwarz">Stefan Schwarz</name><affiliation><nlm:aff id="aff9"><addr-line>Institute of Farm Animal Genetics, Friedrich-Loeffler-Institut (FLI), Neustadt-Mariensee, Germany</addr-line></nlm:aff></affiliation></author><author><name sortKey="Scicluna, Elizabeth" sort="Scicluna, Elizabeth" uniqKey="Scicluna E" first="Elizabeth" last="Scicluna">Elizabeth Scicluna</name><affiliation><nlm:aff id="aff5"><addr-line>Infection Control Unit, Mater Dei Hospital, Msida, Malta</addr-line></nlm:aff></affiliation></author><author><name sortKey="Slickers, Peter" sort="Slickers, Peter" uniqKey="Slickers P" first="Peter" last="Slickers">Peter Slickers</name><affiliation><nlm:aff id="aff13"><addr-line>Alere Technologies GmbH, Jena, Germany</addr-line></nlm:aff></affiliation></author><author><name sortKey="Tan, Hui Leen" sort="Tan, Hui Leen" uniqKey="Tan H" first="Hui-Leen" last="Tan">Hui-Leen Tan</name><affiliation><nlm:aff id="aff2"><addr-line>Department of Microbiology and Infectious Diseases, PathWest Laboratory Medicine - WA, Royal Perth Hospital, Perth, Western Australia, Australia</addr-line></nlm:aff></affiliation></author><author><name sortKey="Weber, Stefan" sort="Weber, Stefan" uniqKey="Weber S" first="Stefan" last="Weber">Stefan Weber</name><affiliation><nlm:aff id="aff14"><addr-line>Sheikh Khalifa Medical City, Abu Dhabi, United Arab Emirates</addr-line></nlm:aff></affiliation></author><author><name sortKey="Ehricht, Ralf" sort="Ehricht, Ralf" uniqKey="Ehricht R" first="Ralf" last="Ehricht">Ralf Ehricht</name><affiliation><nlm:aff id="aff13"><addr-line>Alere Technologies GmbH, Jena, Germany</addr-line></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">21494333</idno><idno type="pmc">3071808</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3071808</idno><idno type="RBID">PMC:3071808</idno><idno type="doi">10.1371/journal.pone.0017936</idno><date when="2011">2011</date><idno type="wicri:Area/Pmc/Corpus">002C04</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">002C04</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">A Field Guide to Pandemic, Epidemic and Sporadic Clones of
Methicillin-Resistant <italic>Staphylococcus aureus</italic></title><author><name sortKey="Monecke, Stefan" sort="Monecke, Stefan" uniqKey="Monecke S" first="Stefan" last="Monecke">Stefan Monecke</name><affiliation><nlm:aff id="aff1"><addr-line>Institute for Medical Microbiology and Hygiene, Technical University of Dresden, Dresden, Germany</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff13"><addr-line>Alere Technologies GmbH, Jena, Germany</addr-line></nlm:aff></affiliation></author><author><name sortKey="Coombs, Geoffrey" sort="Coombs, Geoffrey" uniqKey="Coombs G" first="Geoffrey" last="Coombs">Geoffrey Coombs</name><affiliation><nlm:aff id="aff2"><addr-line>Department of Microbiology and Infectious Diseases, PathWest Laboratory Medicine - WA, Royal Perth Hospital, Perth, Western Australia, Australia</addr-line></nlm:aff></affiliation></author><author><name sortKey="Shore, Anna C" sort="Shore, Anna C" uniqKey="Shore A" first="Anna C." last="Shore">Anna C. Shore</name><affiliation><nlm:aff id="aff3"><addr-line>Microbiology Research Unit, Dublin Dental University Hospital, University of Dublin, Trinity College, Dublin, Ireland</addr-line></nlm:aff></affiliation></author><author><name sortKey="Coleman, David C" sort="Coleman, David C" uniqKey="Coleman D" first="David C." last="Coleman">David C. Coleman</name><affiliation><nlm:aff id="aff3"><addr-line>Microbiology Research Unit, Dublin Dental University Hospital, University of Dublin, Trinity College, Dublin, Ireland</addr-line></nlm:aff></affiliation></author><author><name sortKey="Akpaka, Patrick" sort="Akpaka, Patrick" uniqKey="Akpaka P" first="Patrick" last="Akpaka">Patrick Akpaka</name><affiliation><nlm:aff id="aff4"><addr-line>Department of Para-Clinical Sciences, The University of the West Indies, St. Augustine, Trinidad and Tobago</addr-line></nlm:aff></affiliation></author><author><name sortKey="Borg, Michael" sort="Borg, Michael" uniqKey="Borg M" first="Michael" last="Borg">Michael Borg</name><affiliation><nlm:aff id="aff5"><addr-line>Infection Control Unit, Mater Dei Hospital, Msida, Malta</addr-line></nlm:aff></affiliation></author><author><name sortKey="Chow, Henry" sort="Chow, Henry" uniqKey="Chow H" first="Henry" last="Chow">Henry Chow</name><affiliation><nlm:aff id="aff6"><addr-line>Department of Microbiology, Faculty of Medicine, The Chinese University of Hong Kong, Shatin, Hong Kong, China</addr-line></nlm:aff></affiliation></author><author><name sortKey="Ip, Margaret" sort="Ip, Margaret" uniqKey="Ip M" first="Margaret" last="Ip">Margaret Ip</name><affiliation><nlm:aff id="aff6"><addr-line>Department of Microbiology, Faculty of Medicine, The Chinese University of Hong Kong, Shatin, Hong Kong, China</addr-line></nlm:aff></affiliation></author><author><name sortKey="Jatzwauk, Lutz" sort="Jatzwauk, Lutz" uniqKey="Jatzwauk L" first="Lutz" last="Jatzwauk">Lutz Jatzwauk</name><affiliation><nlm:aff id="aff7"><addr-line>Infection Control Unit, Dresden University Hospital, Dresden, Germany</addr-line></nlm:aff></affiliation></author><author><name sortKey="Jonas, Daniel" sort="Jonas, Daniel" uniqKey="Jonas D" first="Daniel" last="Jonas">Daniel Jonas</name><affiliation><nlm:aff id="aff8"><addr-line>Department of Environmental Health Sciences, Freiburg University Medical Centre, Freiburg, Germany</addr-line></nlm:aff></affiliation></author><author><name sortKey="Kadlec, Kristina" sort="Kadlec, Kristina" uniqKey="Kadlec K" first="Kristina" last="Kadlec">Kristina Kadlec</name><affiliation><nlm:aff id="aff9"><addr-line>Institute of Farm Animal Genetics, Friedrich-Loeffler-Institut (FLI), Neustadt-Mariensee, Germany</addr-line></nlm:aff></affiliation></author><author><name sortKey="Kearns, Angela" sort="Kearns, Angela" uniqKey="Kearns A" first="Angela" last="Kearns">Angela Kearns</name><affiliation><nlm:aff id="aff10"><addr-line>Staphylococcus Reference Unit, Centre for Infections, Health Protection Agency, London, United Kingdom</addr-line></nlm:aff></affiliation></author><author><name sortKey="Laurent, Frederic" sort="Laurent, Frederic" uniqKey="Laurent F" first="Frederic" last="Laurent">Frederic Laurent</name><affiliation><nlm:aff id="aff11"><addr-line>Université Lyon, Centre National de Référence des Staphylocoques, Lyon, France</addr-line></nlm:aff></affiliation></author><author><name sortKey="O Brien, Frances G" sort="O Brien, Frances G" uniqKey="O Brien F" first="Frances G." last="O'Brien">Frances G. O'Brien</name><affiliation><nlm:aff id="aff12"><addr-line>School of Biomedical Sciences, Curtin University, Perth, Western Australia, Australia</addr-line></nlm:aff></affiliation></author><author><name sortKey="Pearson, Julie" sort="Pearson, Julie" uniqKey="Pearson J" first="Julie" last="Pearson">Julie Pearson</name><affiliation><nlm:aff id="aff2"><addr-line>Department of Microbiology and Infectious Diseases, PathWest Laboratory Medicine - WA, Royal Perth Hospital, Perth, Western Australia, Australia</addr-line></nlm:aff></affiliation></author><author><name sortKey="Ruppelt, Antje" sort="Ruppelt, Antje" uniqKey="Ruppelt A" first="Antje" last="Ruppelt">Antje Ruppelt</name><affiliation><nlm:aff id="aff1"><addr-line>Institute for Medical Microbiology and Hygiene, Technical University of Dresden, Dresden, Germany</addr-line></nlm:aff></affiliation></author><author><name sortKey="Schwarz, Stefan" sort="Schwarz, Stefan" uniqKey="Schwarz S" first="Stefan" last="Schwarz">Stefan Schwarz</name><affiliation><nlm:aff id="aff9"><addr-line>Institute of Farm Animal Genetics, Friedrich-Loeffler-Institut (FLI), Neustadt-Mariensee, Germany</addr-line></nlm:aff></affiliation></author><author><name sortKey="Scicluna, Elizabeth" sort="Scicluna, Elizabeth" uniqKey="Scicluna E" first="Elizabeth" last="Scicluna">Elizabeth Scicluna</name><affiliation><nlm:aff id="aff5"><addr-line>Infection Control Unit, Mater Dei Hospital, Msida, Malta</addr-line></nlm:aff></affiliation></author><author><name sortKey="Slickers, Peter" sort="Slickers, Peter" uniqKey="Slickers P" first="Peter" last="Slickers">Peter Slickers</name><affiliation><nlm:aff id="aff13"><addr-line>Alere Technologies GmbH, Jena, Germany</addr-line></nlm:aff></affiliation></author><author><name sortKey="Tan, Hui Leen" sort="Tan, Hui Leen" uniqKey="Tan H" first="Hui-Leen" last="Tan">Hui-Leen Tan</name><affiliation><nlm:aff id="aff2"><addr-line>Department of Microbiology and Infectious Diseases, PathWest Laboratory Medicine - WA, Royal Perth Hospital, Perth, Western Australia, Australia</addr-line></nlm:aff></affiliation></author><author><name sortKey="Weber, Stefan" sort="Weber, Stefan" uniqKey="Weber S" first="Stefan" last="Weber">Stefan Weber</name><affiliation><nlm:aff id="aff14"><addr-line>Sheikh Khalifa Medical City, Abu Dhabi, United Arab Emirates</addr-line></nlm:aff></affiliation></author><author><name sortKey="Ehricht, Ralf" sort="Ehricht, Ralf" uniqKey="Ehricht R" first="Ralf" last="Ehricht">Ralf Ehricht</name><affiliation><nlm:aff id="aff13"><addr-line>Alere Technologies GmbH, Jena, Germany</addr-line></nlm:aff></affiliation></author></analytic><series><title level="j">PLoS ONE</title><idno type="eISSN">1932-6203</idno><imprint><date when="2011">2011</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>In recent years, methicillin-resistant <italic>Staphylococcus aureus</italic>(MRSA) have become a truly global challenge. In addition to the long-known
healthcare-associated clones, novel strains have also emerged outside of the
hospital settings, in the community as well as in livestock. The emergence and
spread of virulent clones expressing Panton-Valentine leukocidin (PVL) is an
additional cause for concern. In order to provide an overview of pandemic,
epidemic and sporadic strains, more than 3,000 clinical and veterinary isolates
of MRSA mainly from Germany, the United Kingdom, Ireland, France, Malta, Abu
Dhabi, Hong Kong, Australia, Trinidad & Tobago as well as some reference
strains from the United States have been genotyped by DNA microarray analysis.
This technique allowed the assignment of the MRSA isolates to 34 distinct
lineages which can be clearly defined based on non-mobile genes. The results
were in accordance with data from multilocus sequence typing. More than 100
different strains were distinguished based on affiliation to these lineages,
SCC<italic>mec</italic> type and the presence or absence of PVL. These
strains are described here mainly with regard to clinically relevant
antimicrobial resistance- and virulence-associated markers, but also in relation
to epidemiology and geographic distribution. The findings of the study show a
high level of biodiversity among MRSA, especially among strains harbouring
SCC<italic>mec</italic> IV and V elements. The data also indicate a high
rate of genetic recombination in MRSA involving SCC elements, bacteriophages or
other mobile genetic elements and large-scale chromosomal replacements.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Van Belkum, A" uniqKey="Van Belkum A">A van Belkum</name></author><author><name sortKey="Melles, Dc" uniqKey="Melles D">DC Melles</name></author><author><name sortKey="Nouwen, J" uniqKey="Nouwen J">J Nouwen</name></author><author><name sortKey="Van Leeuwen, Wb" uniqKey="Van Leeuwen W">WB van Leeuwen</name></author><author><name sortKey="Van Wamel, W" uniqKey="Van Wamel W">W van Wamel</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Jevons, Mp" uniqKey="Jevons M">MP Jevons</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="El Solh, A" uniqKey="El Solh A">A El Solh</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Ito, T" uniqKey="Ito T">T Ito</name></author><author><name sortKey="Katayama, Y" uniqKey="Katayama 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<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id><journal-id journal-id-type="publisher-id">plos</journal-id><journal-id journal-id-type="pmc">plosone</journal-id><journal-title-group><journal-title>PLoS ONE</journal-title></journal-title-group><issn pub-type="epub">1932-6203</issn><publisher><publisher-name>Public Library of Science</publisher-name><publisher-loc>San Francisco, USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">21494333</article-id><article-id pub-id-type="pmc">3071808</article-id><article-id pub-id-type="publisher-id">PONE-D-10-04419</article-id><article-id pub-id-type="doi">10.1371/journal.pone.0017936</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="Discipline-v2"><subject>Biology</subject><subj-group><subject>Microbiology</subject><subj-group><subject>Bacterial Pathogens</subject><subj-group><subject>Gram Positive</subject><subject>Staphylococci</subject></subj-group></subj-group><subj-group><subject>Medical Microbiology</subject></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v2"><subject>Medicine</subject><subj-group><subject>Epidemiology</subject><subj-group><subject>Molecular Epidemiology</subject></subj-group></subj-group><subj-group><subject>Infectious Diseases</subject><subj-group><subject>Bacterial Diseases</subject><subj-group><subject>Methicillin-resistant Staphylococcus aureus</subject><subject>Panton-Valentine leukocidin</subject><subject>Staph Infections</subject><subject>Staphylococcus Aureus</subject></subj-group></subj-group><subj-group><subject>Infectious Disease Control</subject></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v2"><subject>Veterinary Science</subject><subj-group><subject>Veterinary Microbiology</subject></subj-group></subj-group></article-categories><title-group><article-title>A Field Guide to Pandemic, Epidemic and Sporadic Clones of
Methicillin-Resistant <italic>Staphylococcus aureus</italic></article-title><alt-title alt-title-type="running-head">A Field Guide to MRSA</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Monecke</surname><given-names>Stefan</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff13"><sup>13</sup></xref><xref ref-type="corresp" rid="cor1"><sup>*</sup></xref></contrib><contrib contrib-type="author"><name><surname>Coombs</surname><given-names>Geoffrey</given-names></name><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Shore</surname><given-names>Anna C.</given-names></name><xref ref-type="aff" rid="aff3"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Coleman</surname><given-names>David C.</given-names></name><xref ref-type="aff" rid="aff3"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Akpaka</surname><given-names>Patrick</given-names></name><xref ref-type="aff" rid="aff4"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Borg</surname><given-names>Michael</given-names></name><xref ref-type="aff" rid="aff5"><sup>5</sup></xref></contrib><contrib contrib-type="author"><name><surname>Chow</surname><given-names>Henry</given-names></name><xref ref-type="aff" rid="aff6"><sup>6</sup></xref></contrib><contrib contrib-type="author"><name><surname>Ip</surname><given-names>Margaret</given-names></name><xref ref-type="aff" rid="aff6"><sup>6</sup></xref></contrib><contrib contrib-type="author"><name><surname>Jatzwauk</surname><given-names>Lutz</given-names></name><xref ref-type="aff" rid="aff7"><sup>7</sup></xref></contrib><contrib contrib-type="author"><name><surname>Jonas</surname><given-names>Daniel</given-names></name><xref ref-type="aff" rid="aff8"><sup>8</sup></xref></contrib><contrib contrib-type="author"><name><surname>Kadlec</surname><given-names>Kristina</given-names></name><xref ref-type="aff" rid="aff9"><sup>9</sup></xref></contrib><contrib contrib-type="author"><name><surname>Kearns</surname><given-names>Angela</given-names></name><xref ref-type="aff" rid="aff10"><sup>10</sup></xref></contrib><contrib contrib-type="author"><name><surname>Laurent</surname><given-names>Frederic</given-names></name><xref ref-type="aff" rid="aff11"><sup>11</sup></xref></contrib><contrib contrib-type="author"><name><surname>O'Brien</surname><given-names>Frances G.</given-names></name><xref ref-type="aff" rid="aff12"><sup>12</sup></xref></contrib><contrib contrib-type="author"><name><surname>Pearson</surname><given-names>Julie</given-names></name><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Ruppelt</surname><given-names>Antje</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Schwarz</surname><given-names>Stefan</given-names></name><xref ref-type="aff" rid="aff9"><sup>9</sup></xref></contrib><contrib contrib-type="author"><name><surname>Scicluna</surname><given-names>Elizabeth</given-names></name><xref ref-type="aff" rid="aff5"><sup>5</sup></xref></contrib><contrib contrib-type="author"><name><surname>Slickers</surname><given-names>Peter</given-names></name><xref ref-type="aff" rid="aff13"><sup>13</sup></xref></contrib><contrib contrib-type="author"><name><surname>Tan</surname><given-names>Hui-Leen</given-names></name><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Weber</surname><given-names>Stefan</given-names></name><xref ref-type="aff" rid="aff14"><sup>14</sup></xref></contrib><contrib contrib-type="author"><name><surname>Ehricht</surname><given-names>Ralf</given-names></name><xref ref-type="aff" rid="aff13"><sup>13</sup></xref></contrib></contrib-group><aff id="aff1"><label>1</label><addr-line>Institute for Medical Microbiology and Hygiene, Technical University of Dresden, Dresden, Germany</addr-line></aff><aff id="aff2"><label>2</label><addr-line>Department of Microbiology and Infectious Diseases, PathWest Laboratory Medicine - WA, Royal Perth Hospital, Perth, Western Australia, Australia</addr-line></aff><aff id="aff3"><label>3</label><addr-line>Microbiology Research Unit, Dublin Dental University Hospital, University of Dublin, Trinity College, Dublin, Ireland</addr-line></aff><aff id="aff4"><label>4</label><addr-line>Department of Para-Clinical Sciences, The University of the West Indies, St. Augustine, Trinidad and Tobago</addr-line></aff><aff id="aff5"><label>5</label><addr-line>Infection Control Unit, Mater Dei Hospital, Msida, Malta</addr-line></aff><aff id="aff6"><label>6</label><addr-line>Department of Microbiology, Faculty of Medicine, The Chinese University of Hong Kong, Shatin, Hong Kong, China</addr-line></aff><aff id="aff7"><label>7</label><addr-line>Infection Control Unit, Dresden University Hospital, Dresden, Germany</addr-line></aff><aff id="aff8"><label>8</label><addr-line>Department of Environmental Health Sciences, Freiburg University Medical Centre, Freiburg, Germany</addr-line></aff><aff id="aff9"><label>9</label><addr-line>Institute of Farm Animal Genetics, Friedrich-Loeffler-Institut (FLI), Neustadt-Mariensee, Germany</addr-line></aff><aff id="aff10"><label>10</label><addr-line>Staphylococcus Reference Unit, Centre for Infections, Health Protection Agency, London, United Kingdom</addr-line></aff><aff id="aff11"><label>11</label><addr-line>Université Lyon, Centre National de Référence des Staphylocoques, Lyon, France</addr-line></aff><aff id="aff12"><label>12</label><addr-line>School of Biomedical Sciences, Curtin University, Perth, Western Australia, Australia</addr-line></aff><aff id="aff13"><label>13</label><addr-line>Alere Technologies GmbH, Jena, Germany</addr-line></aff><aff id="aff14"><label>14</label><addr-line>Sheikh Khalifa Medical City, Abu Dhabi, United Arab Emirates</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Planet</surname><given-names>Paul J.</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1">Columbia University, United States of America</aff><author-notes><corresp id="cor1">* E-mail: <email>monecke@rocketmail.com</email></corresp><fn fn-type="con"><p>Conceived and designed the experiments: SM PS RE. Performed the experiments:
AR HC KK JP H-LT. Analyzed the data: SM GC ACS DCC FGO SS RE. Contributed
reagents/materials/analysis tools: SM GC ACS DCC FGO SS KK PA MB MI LJ DJ AK
FL ES SW. Wrote the paper: SM GC ACS DCC RE.</p></fn></author-notes><pub-date pub-type="collection"><year>2011</year></pub-date><pub-date pub-type="epub"><day>6</day><month>4</month><year>2011</year></pub-date><volume>6</volume><issue>4</issue><elocation-id>e17936</elocation-id><history><date date-type="received"><day>1</day><month>11</month><year>2010</year></date><date date-type="accepted"><day>16</day><month>2</month><year>2011</year></date></history><permissions><copyright-statement>Monecke et al. This is an open-access article distributed under the
terms of the Creative Commons Attribution License, which permits unrestricted use,
distribution, and reproduction in any medium, provided the original author and
source are credited.</copyright-statement></permissions><abstract><p>In recent years, methicillin-resistant <italic>Staphylococcus aureus</italic>(MRSA) have become a truly global challenge. In addition to the long-known
healthcare-associated clones, novel strains have also emerged outside of the
hospital settings, in the community as well as in livestock. The emergence and
spread of virulent clones expressing Panton-Valentine leukocidin (PVL) is an
additional cause for concern. In order to provide an overview of pandemic,
epidemic and sporadic strains, more than 3,000 clinical and veterinary isolates
of MRSA mainly from Germany, the United Kingdom, Ireland, France, Malta, Abu
Dhabi, Hong Kong, Australia, Trinidad & Tobago as well as some reference
strains from the United States have been genotyped by DNA microarray analysis.
This technique allowed the assignment of the MRSA isolates to 34 distinct
lineages which can be clearly defined based on non-mobile genes. The results
were in accordance with data from multilocus sequence typing. More than 100
different strains were distinguished based on affiliation to these lineages,
SCC<italic>mec</italic> type and the presence or absence of PVL. These
strains are described here mainly with regard to clinically relevant
antimicrobial resistance- and virulence-associated markers, but also in relation
to epidemiology and geographic distribution. The findings of the study show a
high level of biodiversity among MRSA, especially among strains harbouring
SCC<italic>mec</italic> IV and V elements. The data also indicate a high
rate of genetic recombination in MRSA involving SCC elements, bacteriophages or
other mobile genetic elements and large-scale chromosomal replacements.</p></abstract><counts><page-count count="24"></page-count></counts></article-meta></front><body><sec id="s1"><title>Introduction</title><p><italic>Staphylococcus aureus</italic> is a ubiquitous bacterium colonising
20–30% of the human population <xref ref-type="bibr" rid="pone.0017936-vanBelkum1">[1]</xref>. Beyond asymptomatic
carriage, <italic>S. aureus</italic> causes a wide range of infections, such as skin
and soft tissue infections (SSTI), bone, joint and implant infections, pneumonia,
septicaemia and various toxicoses such as toxic shock syndrome. It also occurs in
many different species of animals, where it may cause comparable disease such as
bovine mastitis.</p><p>Shortly after the introduction of penicillin in the 1940s, the first
penicillinase-producing <italic>S. aureus</italic> strains were detected, leading to
the development of the penicillinase-resistant semi-synthetic penicillins such as
methicillin, oxacillin and the first/second generation cephalosporins. Within a year
after the introduction of these drugs, methicillin-resistant <italic>S.
aureus</italic> (MRSA) were reported in the United Kingdom (UK) <xref ref-type="bibr" rid="pone.0017936-Jevons1">[2]</xref>. Resistance is
due to a modified penicillin binding protein (PBP2' or PBP2a) encoded by the
<italic>mecA</italic> gene. Apart from ceftobiprole <xref ref-type="bibr" rid="pone.0017936-ElSolh1">[3]</xref>, the presence of PBP2a confers
resistance towards all β-lactam antibiotics. As methicillin and oxacillin can be
used as indicators of resistance, PBP2a- or <italic>mecA-</italic>positive
<italic>S. aureus</italic> are referred to as either methicillin-resistant
<italic>S. aureus</italic> (MRSA) or oxacillin-resistant <italic>S.
aureus</italic> (ORSA). The <italic>mecA</italic> gene is located on complex
mobile genetic elements, known as SCC<italic>mec</italic> (“staphylococcal
cassette chromosome” or “staphylococcal chromosomal cassette”
harbouring <italic>mecA</italic>). In addition to <italic>mecA</italic>,
SCC<italic>mec</italic> elements comprise recombinase genes, regulatory elements
and, variably, additional genes encoding resistance to other antimicrobials, such as
aminoglycosides or macrolides, and to heavy metal ions <xref ref-type="bibr" rid="pone.0017936-Ito1">[4]</xref>; <xref ref-type="bibr" rid="pone.0017936-Oliveira1">[ 5]</xref>. SCC<italic>mec</italic>types I, II and III (or 1B, 2A, 3A, <xref ref-type="bibr" rid="pone.0017936-IWGSCC1">[6]</xref>) are typically restricted to MRSA strains associated with
healthcare infections and are not found widely among the healthy population. These
strains, which initially were known as “Epidemic MRSA” (EMRSA), are now
frequently referred to as “hospital-acquired” or
“healthcare-associated” MRSA (HA-MRSA). The presence of their
SCC<italic>mec</italic> elements correlates with a relatively slower growth rate
and it has been assumed that they may confer a selective disadvantage in the absence
of antibiotics <xref ref-type="bibr" rid="pone.0017936-Lee1">[7]</xref>;
<xref ref-type="bibr" rid="pone.0017936-Ender1">[ 8]</xref>.
Subsequently, strains carrying these elements may be less fit to survive in a
competitive environment with faster growing wild type strains once antibiotic
therapy is discontinued.</p><p>The epidemiology of MRSA has changed since the 1990s with the emergence of new
SCC<italic>mec</italic> elements such as types IV and V (2B, 5C2). Strains
carrying these elements evolved predominantly outside of healthcare settings or
proved capable of spreading outside of hospitals, infecting not only patients but
also colonising healthy contact persons. Many different strains of so-called
“community-acquired” or “community-associated” MRSA
(CA-MRSA) have spread worldwide. Some CA-MRSA strains harbour genes encoding the
bi-component toxin Panton-Valentine leukocidin (PVL, <xref ref-type="bibr" rid="pone.0017936-Kaneko1">[9]</xref>). Although this toxin was
identified in <italic>S. aureus</italic> as early as 1932 <xref ref-type="bibr" rid="pone.0017936-Panton1">[10]</xref>, its presence in MRSA is a very
recent phenomenon <xref ref-type="bibr" rid="pone.0017936-CDC1">[11]</xref>. These strains are frequently associated with
chronic/recurrent SSTI as well as with life-threatening necrotising pneumonia <xref ref-type="bibr" rid="pone.0017936-Lina1">[12]</xref>, often in
previously healthy young people. PVL-positive CA-MRSA have become a serious public
health concern because of their virulence, their ability to cause outbreaks in
households and close contact social groups, and their rapid spread in many
countries.</p><p>Since 2003, some notable MRSA strains carrying SCC<italic>mec</italic> IV or V have
spread among livestock revealing the truly zoonotic potential of <italic>S.
aureus</italic>/MRSA. These strains have been dubbed
“livestock-associated“ MRSA (LA-MRSA, <xref ref-type="bibr" rid="pone.0017936-Nemati1">[13]</xref>).</p><p>Additional novel SCC<italic>mec</italic> elements have been described <xref ref-type="bibr" rid="pone.0017936-IWGSCC1">[6]</xref>; <xref ref-type="bibr" rid="pone.0017936-Takano1">[14]</xref>–<xref ref-type="bibr" rid="pone.0017936-Zhang1">[17]</xref> which indicate
an ongoing evolution of antibiotic resistance in <italic>S. aureus</italic>. As
β-lactam antibiotics are the first-line compounds for treatment of
staphylococcal infections, this development may significantly limit therapeutic
options. Alternative drugs that may be used to treat MRSA infections are generally
expensive (<italic>e.g.,</italic> quinupristin-dalfopristin, tigecycline, daptomycin
and linezolid), or are problematic with regard to tissue penetration and efficiency
(<italic>e.g.,</italic> vancomycin) or toxicity (<italic>e.g.,</italic>rifampicin). Of further concern is that resistance of MRSA to these compounds has
already been observed, <italic>e.g., vanA</italic>-mediated vancomycin resistance
<xref ref-type="bibr" rid="pone.0017936-Sievert1">[18]</xref> and
<italic>cfr</italic>-mediated linezolid resistance <xref ref-type="bibr" rid="pone.0017936-Kehrenberg1">[19]</xref>–<xref ref-type="bibr" rid="pone.0017936-Shore2">[21]</xref>.</p><p>The limited choice of therapeutic options available has made it necessary to attempt
to limit the spread of MRSA by using a range of infection prevention and control
measures such as hand hygiene, the use of protective clothing and equipment
(<italic>e.g.,</italic> examination gloves or face masks), and accommodation of
patients in isolation rooms or wards. The cost of these measures as well as the
significant expense of second-line antimicrobials places a serious economic burden
on scarce healthcare resources. Recent studies from Europe indicated that the
average excess costs per MRSA-positive patient range from €5,700 to
€10,000 <xref ref-type="bibr" rid="pone.0017936-Chaberny1">[22]</xref>–<xref ref-type="bibr" rid="pone.0017936-Wernitz1">[24]</xref>. Given the large number of MRSA carriers in Europe and in
the USA, the financial burden to healthcare in these regions may account for
billions of Euro or dollars (<ext-link ext-link-type="uri" xlink:href="http://www.infectioncontroltoday.com/hotnews/55h168584264313.html">http://www.infectioncontroltoday.com/hotnews/55h168584264313.html</ext-link>).</p><p>MRSA have become a real international problem. Some strains predominate in
geographically restricted settings while others have achieved pandemic spread. Since
a bewildering biodiversity of novel strains and SCC<italic>mec</italic> elements has
been described in recent years, the objective of this study is to summarise the
genotypic characteristics of pandemic, epidemic and sporadic MRSA strains from
different parts of the world based on the authors' genotyping experiments and
on the published literature.</p></sec><sec id="s2"><title>Results</title><p>Information on target genes, probes and primers is provided in Supplemental <xref ref-type="supplementary-material" rid="pone.0017936.s001">file S1</xref>. The
sequence types (ST, as defined by multilocus sequence typing, or MLST, <xref ref-type="bibr" rid="pone.0017936-Enright1">[25]</xref>),
<italic>spa</italic>, SCC<italic>mec</italic>, capsule and <italic>agr</italic>types associated with each clonal complex (CC) as well as the names and accession
numbers of associated whole genome sequenced strains are shown in Supplemental <xref ref-type="supplementary-material" rid="pone.0017936.s002">file S2</xref>. An
overview of SCC<italic>mec</italic> types and their array hybridisation patterns is
provided in <xref ref-type="fig" rid="pone-0017936-g001">Figure 1</xref>. The
antimicrobial resistance and virulence-associated genes of each strain are shown in
<xref ref-type="fig" rid="pone-0017936-g002">Figures 2</xref> and <xref ref-type="fig" rid="pone-0017936-g003">3</xref>, respectively, while complete
hybridisation profiles for the individual strains are provided in Supplemental <xref ref-type="supplementary-material" rid="pone.0017936.s003">file S3</xref>.</p><fig id="pone-0017936-g001" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0017936.g001</object-id><label>Figure 1</label><caption><title>Overview of SCC<italic>mec</italic> elements, their variants and DNA
microarray hybridisation patterns.</title><p>Black circles, positive; grey circles, present, but yielding weak or
ambiguous signals; divided circles, variable genes.</p></caption><graphic xlink:href="pone.0017936.g001"></graphic></fig><fig id="pone-0017936-g002" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0017936.g002</object-id><label>Figure 2</label><caption><title>Resistance genes in MRSA strains.</title></caption><graphic xlink:href="pone.0017936.g002"></graphic></fig><fig id="pone-0017936-g003" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0017936.g003</object-id><label>Figure 3</label><caption><title>Virulence-associated genes in MRSA strains (*, see text for further
explanation).</title></caption><graphic xlink:href="pone.0017936.g003"></graphic></fig><sec id="s2a"><title>Clonal complex 1</title><p>CC1 includes several strains of CA-MRSA including MW2/USA400, the first known
PVL-positive MRSA <xref ref-type="bibr" rid="pone.0017936-CDC1">[11]</xref>. The CC1 strains ST573 and ST772 differ significantly
in MLST alleles to all other CC1 isolates and yield deviant hybridisation
patterns. Therefore they will be described separately (see below). The remaining
CC1-MRSA cluster into seven strains that can be differentiated based on the
presence of the PVL genes, SCC<italic>mec</italic> elements IV or V and the
SCC<italic>fus</italic> element. The latter comprises
<italic>ccrA-1</italic> and <italic>ccrB-1</italic> as well as the fusidic
acid resistance marker Q6GD50 (GenBank BX571857.1:SAS0043) first described in
the genome sequence of the CC1-MSSA strain Sanger MSSA 476 <xref ref-type="bibr" rid="pone.0017936-Holden1">[26]</xref>. All isolates of these
CC1-MRSA strains harbour the enterotoxin gene <italic>seh</italic> and many
isolates also carry the enterotoxin genes <italic>sek</italic> and
<italic>seq</italic>. Other enterotoxin genes (<italic>sea-N315, seb,
sec</italic> and <italic>sel</italic>) are only found sporadically. Most
isolates harbour the immune evasion cluster (IEC) genes associated with
β-haemolysin-converting phages in various combinations.</p><p>One CC1-MRSA strain carries SCC<italic>mec</italic> IV and PVL, but lacks
SCC<italic>fus</italic>. The genome sequence of MW2 <xref ref-type="bibr" rid="pone.0017936-Baba1">[27]</xref> is a representative of this
strain, which is also known as USA400 or Canadian MRSA-7 <xref ref-type="bibr" rid="pone.0017936-Christianson1">[28]</xref>. The first known
PVL-positive CA-MRSA belonged to this strain. In the late 1990s, it caused fatal
infections in previously healthy children from Minnesota and North Dakota <xref ref-type="bibr" rid="pone.0017936-CDC1">[11]</xref>. The authors
sporadically found isolates in Australia, Germany and the UK.</p><p>A second strain also carries SCC<italic>mec</italic> IV, lacks
SCC<italic>fus</italic>, but differs from USA400 in being PVL-negative. It
has been found by the authors primarily in Australia where it is designated as
West Australian (WA) MRSA-57 although it also includes some of the isolates
originally described as WA MRSA-1. It has been isolated sporadically in Saxony
(Germany, <xref ref-type="bibr" rid="pone.0017936-Monecke1">[29]</xref>), Ireland <xref ref-type="bibr" rid="pone.0017936-Kinnevey1">[30]</xref> and Egypt (isolate
courtesy of M. Kamal El Din, Cairo).</p><p>A third strain is PVL-negative, but harbours both, SCC<italic>mec</italic> IV and
SCC<italic>fus</italic>. It includes WA MRSA-45 and also some WA MRSA-1
isolates. It has been isolated in Australia as well as, sporadically, in Abu
Dhabi (United Arab Emirates <xref ref-type="bibr" rid="pone.0017936-Weber1">[31]</xref>), the UK and Ireland <xref ref-type="bibr" rid="pone.0017936-Kinnevey1">[30]</xref>.</p><p>Sporadic isolates of PVL-positive CC1-MRSA-IV with SCC<italic>fus</italic>,
PVL-positive CC1-MRSA-V and PVL-negative CC1-MRSA-V with SCC<italic>fus</italic>have been isolated from a small number of cases in Australia. A PVL-positive
CC1-MRSA-V with SCC<italic>fus</italic> has been found in Abu Dhabi <xref ref-type="bibr" rid="pone.0017936-Weber1">[31]</xref>.</p></sec><sec id="s2b"><title>Clonal complex 5</title><p>CC5 is another common and widespread clonal complex, which comprises a large
number of different MRSA strains, both HA- and CA-MRSA, some of which have
attained pandemic spread.</p><p>Several whole genome sequences are available (Supplemental <xref ref-type="supplementary-material" rid="pone.0017936.s002">file S2</xref>)
which comprise the features of the CC5 core genome including characteristic
allelic variants of the <italic>ssl/set</italic> genes and of genes encoding
microbial surface components recognising adhesive matrix molecules of the host
(MSCRAMM genes). CC5 isolates carry the enterotoxin gene cluster
<italic>egc</italic> (<italic>seg, sei, sem, sen, seo</italic> and
<italic>seu/y</italic>), although partial deletions have been observed.
β-haemolysin-converting phages carrying <italic>sak, scn</italic> and
<italic>chp</italic> as well as <italic>sea</italic> or
<italic>sea-N315</italic> in various combinations are commonly detected.
Many variable virulence- or resistance-associated genes and several different
SCC<italic>mec</italic> elements have been found in CC5.</p><p>ST228-MRSA-I is colloquially known as the South German Epidemic Strain, Italian
Clone, <xref ref-type="bibr" rid="pone.0017936-Mato1">[32]</xref>;
<xref ref-type="bibr" rid="pone.0017936-Campanile1">[33]</xref> or
Spanish PFGE types E6/9/15/17/18 <xref ref-type="bibr" rid="pone.0017936-Vindel1">[34]</xref>. The strain occurs in
Germany (where it appears to be a strictly HA-MRSA strain, although its
incidence is decreasing), Hungary (where it replaced the “Hungarian
Clone” ST239-MRSA-III, <xref ref-type="bibr" rid="pone.0017936-Conceicao1">[35]</xref>), Italy <xref ref-type="bibr" rid="pone.0017936-Mato1">[32]</xref>; <xref ref-type="bibr" rid="pone.0017936-Campanile1">[33]</xref>; <xref ref-type="bibr" rid="pone.0017936-Grundmann1">[36]</xref>, Slovenia <xref ref-type="bibr" rid="pone.0017936-Grundmann1">[36]</xref> and
Switzerland <xref ref-type="bibr" rid="pone.0017936-Basset1">[37]</xref>. It was also found sporadically in Austria <xref ref-type="bibr" rid="pone.0017936-Krziwanek1">[38]</xref>, Israel
<xref ref-type="bibr" rid="pone.0017936-Adler1">[39]</xref>, Malta
<xref ref-type="bibr" rid="pone.0017936-Scicluna1">[40]</xref> and
Australia. MLST variants of this strain have been described from Croatia (ST111,
<xref ref-type="bibr" rid="pone.0017936-Budimir1">[41]</xref>) and
Paraguay (ST5, ST221, <xref ref-type="bibr" rid="pone.0017936-Mayor1">[42]</xref>). The isolates harbour SCC<italic>mec</italic> I. A
variant lacking <italic>ccrA/B-1</italic> was identified in Saxony in 2000.
Variable markers <xref ref-type="bibr" rid="pone.0017936-Monecke2">[43]</xref> include the mercury resistance operon, the
β-lactamase operon as well as several other resistance genes (<xref ref-type="fig" rid="pone-0017936-g002">Figure 2</xref>), the toxic shock
syndrome toxin <italic>tst1</italic>, IEC genes and the MSCRAMM genes
<italic>bbp</italic>, <italic>clfA</italic> and <italic>sdrD</italic>. In
contrast to other CC5 strains, ST228-MRSA-I lacks <italic>fnbB</italic>, a gene
encoding a fibronectin-binding protein. Deletions of the leukocidin genes
<italic>lukD+lukE</italic> and of neighbouring genes from the
<italic>egc</italic> locus are common <xref ref-type="bibr" rid="pone.0017936-Monecke2">[43]</xref>.</p><p>A ST5-MRSA-I, known as the Geraldine Clone, is a second SCC<italic>mec</italic> I
strain from CC5. This is a common CA-MRSA clone in France <xref ref-type="bibr" rid="pone.0017936-Dauwalder1">[44]</xref>. Apart from a single
veterinary isolate from Germany (courtesy of B. Walther, FU Berlin), isolates
have not been detected outside of France. Unlike ST228-MRSA-I, Geraldine Clone
isolates harbour Q6GD50, enterotoxin genes <italic>sed, sej</italic> and
<italic>ser</italic> and <italic>fnbB</italic>. Most isolates carry
<italic>tst1</italic> and the enterotoxin genes <italic>sec</italic> and
<italic>sel</italic>. The SCC<italic>mec</italic> element lacks
<italic>pls-</italic>SCC.</p><p>The Australian strains WA MRSA-18, -21 (both ST5) and -48 (ST835) represent a
third group of CC5-MRSA-I. These strains, however, harbour an atypical or
truncated SCC<italic>mec</italic> I element. The genes <italic>mecA, ΔmecR1,
ugpQ</italic> and <italic>ccrB-1</italic> are detectable;
<italic>ccrA-1</italic> occasionally yields a signal and
<italic>pls-</italic>SCC is usually absent. Resistance markers detected
among these CC5-MRSA-I isolates include the β-lactamase operon and, in some
isolates, <italic>qacC</italic> encoding resistance to quaternary ammonium
compounds. In addition to <italic>egc,</italic> the enterotoxin genes
<italic>sed, sej</italic> and <italic>ser</italic> are associated with these
isolates as well as, variably, <italic>sea</italic> or
<italic>sea-N315.</italic></p><p>ST5-MRSA-II is a pandemic CC5 strain. A MLST single locus variant (SLV) of this
strain, ST225-MRSA-II, has been reported <xref ref-type="bibr" rid="pone.0017936-Deurenberg1">[45]</xref>. Different STs as well
as a number of additional genetic polymorphisms within this strain might suggest
a polyphyletic origin by multiple and independent transfers of
SCC<italic>mec</italic> II elements to various CC5-MSSA precursor strains
<xref ref-type="bibr" rid="pone.0017936-Nubel1">[46]</xref>.
Synonyms and vernacular names are UK-EMRSA-3, New York-Japan Clone, Rhine-Hesse
Epidemic Strain, Irish AR07.3, Irish AR07.4, Irish AR11, USA100 and Canadian
MRSA-2 <xref ref-type="bibr" rid="pone.0017936-Christianson1">[28]</xref>. Published CC5 genome sequences of isolates belonging
to this strain include Mu3, Mu50, N315, JH1 and JH9. Isolates of
ST5/ST225-MRSA-II have been identified in Austria <xref ref-type="bibr" rid="pone.0017936-Krziwanek1">[38]</xref>, Croatia <xref ref-type="bibr" rid="pone.0017936-Budimir1">[41]</xref>, Hong-Kong
(China, <xref ref-type="bibr" rid="pone.0017936-Ip1">[47]</xref>),
Hungary <xref ref-type="bibr" rid="pone.0017936-Conceicao1">[35]</xref>, Japan <xref ref-type="bibr" rid="pone.0017936-AiresdeSousa1">[48]</xref>, Portugal <xref ref-type="bibr" rid="pone.0017936-AiresdeSousa2">[49]</xref>,
Taiwan <xref ref-type="bibr" rid="pone.0017936-Takano2">[50]</xref>,
the UK and the USA <xref ref-type="bibr" rid="pone.0017936-AiresdeSousa1">[48]</xref>. The authors have identified this strain in Ireland
<xref ref-type="bibr" rid="pone.0017936-Shore1">[15]</xref> and in
different regions of Germany, the UK, Hong Kong and Australia. In
Dresden/Saxony, ST5-MRSA-II is the second most prevalent MRSA strain (accounting
for approximately 30% of isolates), and the most frequently isolated
strain in this region's intensive care units <xref ref-type="bibr" rid="pone.0017936-Kupfer1">[51]</xref>. Transmission of this
strain has been reported in Australia where the index case was shown to be a
healthcare worker who previously underwent surgery in a New York hospital <xref ref-type="bibr" rid="pone.0017936-Coombs1">[52]</xref>.
ST5-MRSA-II isolates usually exhibit <italic>spa</italic> types t002, t003 or,
in Ireland, t045. Antimicrobial resistance markers in ST5/ST225-MRSA-II isolates
may vary (see <xref ref-type="fig" rid="pone-0017936-g002">Figure 2</xref>),
although <italic>erm</italic>(A) and the aminoglycoside resistance gene
<italic>aadD</italic> are commonly present. Variable virulence-associated
genes include <italic>tst1, sea, sea-N315, sec, sed, sej, sel</italic> and
<italic>ser</italic><xref ref-type="bibr" rid="pone.0017936-Monecke2">[43]</xref>.
Variants of this strain harbouring the arginine catabolic mobile element (ACME)
have been isolated in Hong Kong and California/USA (NARSA 642).</p><p>CC5-MRSA-III has been isolated from humans in the South African province of
KwaZulu-Natal <xref ref-type="bibr" rid="pone.0017936-Shittu1">[53]</xref>, from Korean chicken meat samples <xref ref-type="bibr" rid="pone.0017936-Kwon1">[54]</xref>, and from
turkeys or turkey meat in Germany (courtesy of S. Cortez de Jäckel,
Delbrück, Germany, and of the Federal Institute for Risk Assessment,
Berlin, Germany). The latter isolates harbour SCC<italic>mec</italic> IIIA,
lacking <italic>tet</italic>(K) and the mercury resistance operon. CC5-MRSA-III
may initially appear to be methicillin-susceptible but resistance is observed
following growth on selective agar containing methicillin <xref ref-type="bibr" rid="pone.0017936-Kwon1">[54]</xref>.</p><p>CC5-MRSA-IV strains have achieved pandemic spread and significant clinical
relevance. Colloquially strains have been described as the Paediatric Clone
(although the first strain described under that name HDE288 has been
subsequently shown to be CC5-MRSA-VI, <xref ref-type="bibr" rid="pone.0017936-Oliveira2">[55]</xref>), WA MRSA-03 (ST5), -25
(ST575), -39 (ST526), -50 (ST73) and -74 (ST5), USA800 or Marseille Cystic
Fibrosis Clone (ST5; <xref ref-type="bibr" rid="pone.0017936-Rolain1">[56]</xref>). As for ST5/ST225-MRSA-II, a large proportion of
CC5-MRSA-IV isolates carry <italic>sea-N315</italic> and/or
<italic>sed+sej+ser.</italic> Other virulence genes, including
<italic>tst1</italic> and the epidermal cell differentiation inhibitor gene
<italic>edinA,</italic> can be found in a minority of isolates. A novel
enterotoxin gene has recently been located on the same plasmid as
<italic>edinA</italic> (GenBank AP003089.1). Variable resistance markers in
CC5-MRSA-IV are shown in <xref ref-type="fig" rid="pone-0017936-g002">Figure
2</xref>.</p><p>PVL-positive CC5-MRSA-IV has been identified by the authors in patients from the
UK, France, Australia, Switzerland and Senegal and previously in Ireland <xref ref-type="bibr" rid="pone.0017936-Rossney1">[57]</xref>. Based on
toxin gene profiles, these isolates cluster into three major variants harbouring
<italic>sea-N315+sed+sej+ser</italic> or
<italic>sea</italic>+<italic>edinA</italic>, or <italic>edinA.</italic>Variable resistance markers are shown in <xref ref-type="fig" rid="pone-0017936-g002">Figure 2</xref>.</p><p>ST5-MRSA-V has been described in Australia, where it is colloquially known as WA
MRSA-11, -14, -34 and -35, Ireland <xref ref-type="bibr" rid="pone.0017936-Kinnevey1">[30]</xref> and Abu Dhabi.
PVL-positive CC5-MRSA-V has been identified sporadically in Germany and Abu
Dhabi.</p><p>CC5-MRSA-VI was first observed in Portugal in 1992 <xref ref-type="bibr" rid="pone.0017936-SaLeao1">[58]</xref>. It was first described as
Paediatric Clone carrying SCC<italic>mec</italic> IV but was later reclassified
as harbouring a SCC<italic>mec</italic> VI element <xref ref-type="bibr" rid="pone.0017936-Oliveira2">[55]</xref>. In France it was dubbed
the New Paediatric Clone <xref ref-type="bibr" rid="pone.0017936-Dauwalder1">[44]</xref>. This strain has been identified in Portugal,
Colombia, Argentina and the USA <xref ref-type="bibr" rid="pone.0017936-SaLeao1">[58]</xref>. The authors identified New Paediatric Clone isolates
(<italic>spa</italic> type t105 or t777) in France, and very sporadically in
Australia and Germany, as well as PVL-positive CC5-MRSA-VI (<italic>spa</italic>t311) in Switzerland. The latter strain has also been reported from the Azores
and Portugal <xref ref-type="bibr" rid="pone.0017936-Conceicao2">[59]</xref>.</p><p>A further novel SCC<italic>mec</italic> element (SCC<italic>mec</italic> type
VII, <xref ref-type="bibr" rid="pone.0017936-IWGSCC1">[6]</xref> or
SCC<italic>mec</italic> JCSC6082, GenBank: AB373032.1) was recently
described in Sweden <xref ref-type="bibr" rid="pone.0017936-Berglund1">[16]</xref>. This strain (courtesy of C. Berglund, Stockholm,
Sweden) yields signals with probes for <italic>mecA, ΔmecR1, ugpQ</italic>and <italic>ccrC</italic>, and it is positive for <italic>blaZ</italic> and
<italic>tet</italic>(M).</p><p>In addition to the above mentioned strains, several CC5-MRSA carry multiple or
composite SCC<italic>mec</italic> elements. One of these strains (ST149 which is
a MLST single locus variant, SLV, of ST5, <italic>spa-</italic>type t002) was
recently described in Malta <xref ref-type="bibr" rid="pone.0017936-Scicluna1">[40]</xref>. This strain carries a SCC<italic>mec</italic> IV
element as well as Q6GD50 and novel <italic>ccrA</italic> and
<italic>ccrB</italic> genes (GenBank GU066221). The latter are identical to
<italic>ccrASHP+ccrBSHP</italic> in a Chinese isolate of <italic>S.
haemolyticus</italic> (GenBank EU934095.1, <xref ref-type="bibr" rid="pone.0017936-Pi1">[60]</xref>), where these genes were
accompanied by the ACME locus <xref ref-type="bibr" rid="pone.0017936-Diep1">[61]</xref>. This locus, however, is absent in the Maltese
strain. It lacks PVL, but it carries <italic>sea</italic>, <italic>egc</italic>as well as, commonly, <italic>tst1, sec</italic> and <italic>sel</italic>. Some
isolates harbour the resistance genes <italic>erm</italic>(C) and
<italic>tet</italic>(K). This strain appears to be common in Malta <xref ref-type="bibr" rid="pone.0017936-Scicluna1">[40]</xref>, but has
not been reported elsewhere. Another, PVL- and <italic>tst1</italic>-positive
ST149-MRSA-IV has been isolated from a Libyan patient in Switzerland <xref ref-type="bibr" rid="pone.0017936-Francois1">[62]</xref>.</p><p>A composite variant of a SCC<italic>mec</italic> IV has been described in the CC5
strain MRSA-ZH47 <xref ref-type="bibr" rid="pone.0017936-Heusser1">[63]</xref>. It resembles a SCC<italic>mec</italic> IV element,
but also carries a set of SCC<italic>mec</italic> V-like recombinase genes
(<italic>ccrC</italic> and “<italic>ccrAA</italic>”, a putative
recombinase gene, see <xref ref-type="sec" rid="s4">Materials and
Methods</xref>).</p><p>Another CC5 strain with multiple/composite SCC<italic>mec</italic> elements
originates from Spain. Isolates from a German patient hospitalised in the Canary
Islands <xref ref-type="bibr" rid="pone.0017936-Monecke1">[29]</xref>and from a patient in Barcelona (Courtesy of S. Molinos, Barcelona) yielded
hybridisation signals for <italic>mecA, ΔmecR1, ugpQ, ccrA-2, ccrB-2,
ccrA-4</italic> and <italic>ccrB-4</italic>. Because of the carriage of
<italic>erm</italic>(C), <italic>msr</italic>(A), <italic>mph</italic>(C),
<italic>aphA3</italic> and <italic>sat</italic> as well as affiliation to
<italic>spa</italic> type t067, these isolates probably represent an
epidemic strain, or a close relative of it, recently described in Spain <xref ref-type="bibr" rid="pone.0017936-PerezVazquez1">[64]</xref>.
Similar isolates harbouring only <italic>erm</italic>(C) have been found by the
authors in France, Australia and Germany.</p><p>A CC5 strain with a composite SCC<italic>mec</italic> element comprising
SCC<italic>mec</italic> IV, <italic>ccrA-1, ccrB-1</italic> and Q6GD50 has
recently been described in the Netherlands <xref ref-type="bibr" rid="pone.0017936-Beisser1">[65]</xref>.</p><p>Australian ST835 strains WA MRSA-40/46 harbour SCC<italic>mec</italic>V<sub>T</sub> elements and <italic>ccrA/B-2</italic> genes. These strains
vary in the presence of β-lactamase genes, the mupirocin and trimethoprim
resistance genes <italic>mupA</italic> and <italic>dfrA, qacA</italic> as well
as of <italic>sed+sej+ser.</italic> The authors have identified other
CC5-MRSA which harbour composite or multiple SCC<italic>mec</italic> elements
including [<italic>mecA, ΔmecR1, ugpQ, ccrA-1, ccrB-1,
pls-</italic>SCC, <italic>dcs, ccrC</italic>], [<italic>mecA,
ΔmecR1, ugpQ, dcs, ccrA-2, ccrB-2, ccrC</italic>] and
[<italic>mecA, ugpQ,</italic> “<italic>ccrAA</italic>”,
<italic>ccrC, ccrA-4, ccrB-4</italic>]. However, these MRSA strains
were only represented by one or two isolates in each case.</p></sec><sec id="s2c"><title>Sequence type 6</title><p>According to MLST data, ST6 is a double locus variant (DLV) of ST5
(<italic>arcC</italic>-12 and <italic>yqiL</italic>-3 rather than
<italic>arcC</italic>-1 and <italic>yqiL</italic>-10, as in ST5). However,
ST6 isolates differ in <italic>agr</italic> group, capsule and
<italic>spa</italic> types. They harbour different alleles of
<italic>hsdS</italic>-, <italic>set/ssl</italic>- and several MSCRAMM genes
(<italic>bbp, fnbB, sdrC, sdrD, clfA, clfB, sasG</italic>). In addition,
isolates of this ST carry <italic>cna</italic> but lack <italic>egc.</italic>These observations may be explained by a large scale chromosomal replacement
with one parental strain belonging to CC5. The origin of the inserted region has
not yet been determined. The size and location of the insert can be estimated by
analysing the known positions of the probe sequences within the published CC5
genome sequences. Thus, the insert is localised around <italic>oriC,</italic>and ranges from <italic>hsdS3</italic> downstream of <italic>oriC</italic> to
the <italic>ssl/set</italic>-locus upstream of <italic>oriC</italic>. This
equals <italic>ca</italic>. 1.500.000 bp (<italic>i.e.,</italic> about half of
the genome). It can be assumed that the SCC<italic>mec</italic> element is
integrated into that insert. ST6 strains tested for the present study were PVL
negative. They included ST6-MRSA-IV from Australia (where it is known as WA
MRSA-51) and Abu Dhabi <xref ref-type="bibr" rid="pone.0017936-Weber1">[31]</xref> as well as ST6-MRSA-V from Hong Kong.</p></sec><sec id="s2d"><title>Clonal complex 7</title><p>CC7-MRSA are rare. One ST, ST1048, is discussed separately due to its divergent
hybridisation pattern.</p><p>The authors identified single isolates of CC7-MRSA-IV and CC7-MRSA-V in Saxony
and in Australia, respectively. The enterotoxin A allele
<italic>sea-N315,</italic> also known as <italic>sep</italic>, is present in
both isolates (and it is also common in CC7-MSSA). Both isolates are
PVL-negative.</p></sec><sec id="s2e"><title>Clonal complex 8</title><p>Similar to CC5, CC8 is a pandemic MRSA lineage. Numerous MRSA strains have
originated from CC8, including both CA- and HA-MRSA, and several whole genome
sequenced MRSA strains represent this lineage (see Supplemental <xref ref-type="supplementary-material" rid="pone.0017936.s002">file S2</xref>).
Although related to CC8, ST72 and ST239/241 are discussed separately as they
exhibit distinct hybridisation patterns. The core genome genes of the remaining
CC8 strains such as protease, <italic>ssl/set</italic> and MSCRAMM genes of
clinical isolates are in accordance with the sequenced genomes although
occasional deletions of genes such as <italic>bbp, clfA</italic> or
<italic>sdrD</italic> can be observed. Carriage of exotoxins and of
β-haemolysin-converting phages is highly variable. Several different CC8
strains have been described, and can be distinguished based on
SCC<italic>mec</italic> types and exotoxin profiles.</p><p>The first known MRSA was a CC8 strain, ST250-MRSA-I, which is also known as Early
or Ancestral MRSA, Irish AR02 or Irish Phenotype I and II. The genome sequence
(GenBank CP000046) of the strain COL, which was isolated in England in the
1960s, is representative of this strain <xref ref-type="bibr" rid="pone.0017936-Gill1">[66]</xref>. The ST250-MRSA-I clone seems
to be disappearing. However, it is still isolated in Australia, although rarely
(one isolate out of more than 4000 tested, <xref ref-type="bibr" rid="pone.0017936-Coombs2">[67]</xref>). The description in this
study is based on COL and on isolates recovered from hospitalised patients in
Ireland in the 1970s to 1980s <xref ref-type="bibr" rid="pone.0017936-Shore1">[15]</xref>. All isolates closely resemble COL, and they also
show a characteristic deletion of several <italic>ssl/set</italic> genes. The
carriage of <italic>pls-</italic>SCC <xref ref-type="bibr" rid="pone.0017936-Shore1">[15]</xref>, several resistance markers
(see <xref ref-type="fig" rid="pone-0017936-g002">Figure 2</xref>), enterotoxin
genes <italic>seb+sek+seq</italic> and of β-haemolysin-converting
phages (<italic>sak, chp</italic> and <italic>scn</italic>) is variable.</p><p>A very similar and, likewise, ancient strain is ST247-MRSA-I. A reference
isolate, NARSA 209, was recovered in the UK in 1971. Vernacular names include
North German Epidemic Strain, UK-EMRSA-5, -8 and -17, Rome Clone, Spanish PFGE
type E1, <xref ref-type="bibr" rid="pone.0017936-Vindel1">[34]</xref>,
Irish AR22, Irish New02 and, after an outbreak in Barcelona in 1989, Iberian
Clone <xref ref-type="bibr" rid="pone.0017936-Dominguez1">[68]</xref>.
ST247-MRSA-I seems to be receding, as observed, for example, in Portugal <xref ref-type="bibr" rid="pone.0017936-AiresdeSousa2">[49]</xref> and
Spain <xref ref-type="bibr" rid="pone.0017936-Cuevas1">[69]</xref>. It
has not been identified in Dresden, Saxony, since 1997 (<xref ref-type="bibr" rid="pone.0017936-Witte1">[70]</xref> and authors'
observations) or in Ireland since 1999 <xref ref-type="bibr" rid="pone.0017936-Shore1">[15]</xref>. Thus, the description in
this study is based partially on isolates recovered from the 1990s. More
recently, ST247-MRSA-I has been found in Australia, Croatia <xref ref-type="bibr" rid="pone.0017936-Budimir1">[41]</xref>, the Czech
Republic <xref ref-type="bibr" rid="pone.0017936-Melter1">[71]</xref>,
Italy, where it is also becoming increasingly rare <xref ref-type="bibr" rid="pone.0017936-Campanile1">[33]</xref>, and in the Netherlands
(isolates courtesy of P. Beisser, Maastricht). Although this strain yields a
hybridisation profile similar to that of ST250-MRSA-I, it harbours a complete
set of <italic>ssl/set</italic> genes, and with regard to these genes it
resembles the NCTC8325 or USA300 genome sequences more than COL. Enterotoxin
genes <italic>seb+sek+seq</italic> are rare, but about half of the
isolates harbour <italic>sea</italic>. As in other CC8 isolates,
<italic>bbp</italic> is deleted in a number of isolates. In addition to
SCC<italic>mec</italic> I, all tested isolates carry
<italic>tet</italic>(M). Additional resistance markers have been detected in
some isolates (<xref ref-type="fig" rid="pone-0017936-g002">Figure
2</xref>).</p><p>Several different CC8-MRSA-IV strains have been described previously based on
different typing methods. In the following paragraphs, we define these strains
with reference to their carriage of exotoxin genes. However, as these genes are
located on mobile elements such as phages or plasmids, it may be that these
“strains” are in fact polyphyletic clusters. One of these strains
includes CC8-MRSA-IV isolates which lack PVL or any enterotoxin genes (besides
the ubiquitous enterotoxin homologue, GenBank CP000046.1:SACOL1657). They belong
to ST8 or ST576 (<italic>tpi-</italic>19 instead of <italic>tpi</italic>-4) and
include UK-EMRSA-14 and WA MRSA-5, -6 and -31. NARSA 645 is a reference strain
that shows an Iberian Clone-like PFGE pattern (<ext-link ext-link-type="uri" xlink:href="http://www.narsa.net">http://www.narsa.net</ext-link>). The
authors found only a single isolate from Germany. However, in Australia this
strain appears to be rather common. Isolates differ in the carriage of
β-haemolysin-converting phages and of a variety of resistance genes.</p><p>Another PVL-negative CC8-MRSA-IV has been named the Lyon Clone or UK-EMRSA-2. It
is frequently isolated in France <xref ref-type="bibr" rid="pone.0017936-Dauwalder1">[44]</xref>, and can occasionally be
identified in Germany, Ireland <xref ref-type="bibr" rid="pone.0017936-Kinnevey1">[30]</xref>, the UK, the Netherlands
(isolates courtesy of P. Beisser, Maastricht), Norway (courtesy of H. V. Aamont,
Aakershus) and Australia. Most isolates of this strain carry <italic>sea,
sak</italic> and <italic>scn,</italic> as well as, commonly,
<italic>sed+sej+ser.</italic> Some isolates lack the
<italic>sea</italic> gene. These isolates harbour <italic>chp, sak</italic>and <italic>scn,</italic> or they have a non-disrupted <italic>hlb</italic> gene
and lack all IEC genes. Variable resistance markers are the mercury resistance
and β-lactamase operons, <italic>erm</italic>(A), <italic>erm</italic>(C),
<italic>vga</italic>(A)<italic>-BM3327, aacA-aphD, aadD, dfrA, far1,
tet</italic>(K), <italic>tet</italic>(M), <italic>qacA</italic> and
<italic>qacC</italic>. Another related strain has been described as
UK-EMRSA-6. It is also <italic>sea-</italic>positive, and differs from Lyon
Clone/UK-EMRSA-2 in the presence of <italic>aphA3+sat</italic>.</p><p>Another strain of CC8-MRSA-IV carries the enterotoxin genes
<italic>seb+sek+seq</italic>, but lacks PVL. It is known as USA500
with NARSA 385 being a reference strain. Isolates have been identified in the
USA (NARSA 119, -120, -121, -678, -686 and -708) and Australia (as a SLV, ST612,
WA MRSA-20, <xref ref-type="bibr" rid="pone.0017936-Nimmo1">[72]</xref>) as well as, for the present study, in the UK, in
Ireland and, sporadically, in Germany. Some of the German isolates were
recovered from patients with travel histories (Ethiopia, Zimbabwe and
Mozambique) suggesting a wide distribution of this strain in Sub-Saharan Africa.
This is also indicated by frequent observations of ST612 in South Africa <xref ref-type="bibr" rid="pone.0017936-JansenvanRensburg1">[73]</xref>.
USA500 has also been found in horses from the USA, Canada <xref ref-type="bibr" rid="pone.0017936-Weese1">[74]</xref>, Ireland <xref ref-type="bibr" rid="pone.0017936-Kinnevey1">[30]</xref> and
Germany <xref ref-type="bibr" rid="pone.0017936-Walther1">[75]</xref>as well as from humans with contact to horses <xref ref-type="bibr" rid="pone.0017936-Kinnevey1">[30]</xref>. Equine isolates differ
from human isolates of USA500 by the absence of lysogenic β-haemolysin
converting phages and thus they also lack the <italic>sea, sak, chp</italic> and
<italic>scn</italic> genes. The carriage of resistance markers is highly
variable (<xref ref-type="fig" rid="pone-0017936-g002">Figure 2</xref>).</p><p>A notable PVL-positive ST8-MRSA-IV is the widely known strain USA300 (also known
as WA MRSA-12, Canadian MRSA-10 <xref ref-type="bibr" rid="pone.0017936-Christianson1">[28]</xref> or Spanish PFGE type
A, <xref ref-type="bibr" rid="pone.0017936-Vindel1">[34]</xref>).
Within a few years it has spread extensively across the USA, effectively
marginalising other <italic>S. aureus</italic> strains, MRSA as well as MSSA
<xref ref-type="bibr" rid="pone.0017936-Moran1">[76]</xref>. It is
mainly community-associated, but hospital-associated cases also occur <xref ref-type="bibr" rid="pone.0017936-Hulten1">[77]</xref>; <xref ref-type="bibr" rid="pone.0017936-Chua1">[78]</xref>. In Europe,
USA300 has not been isolated frequently. For instance, eight out of 25
PVL-positive CA-MRSA from Ireland were identified as USA300 <xref ref-type="bibr" rid="pone.0017936-Rossney1">[57]</xref>. Since
these isolates originated from a sample of 1,389 MRSA isolates, it can be
concluded that USA300 in particular, and PVL-positive MRSA in general, are much
less of a problem in Ireland than in the USA <xref ref-type="bibr" rid="pone.0017936-Rossney1">[57]</xref>. In Dresden/Saxony, the
authors identified the first case of a USA300 infection in 2005 <xref ref-type="bibr" rid="pone.0017936-Monecke1">[29]</xref>, but only
sporadic isolates have subsequently been observed (including three among 304
genotyped MRSA isolates from patients of the University Hospital Dresden, 2007
to 2009, unpublished observation by the authors). In the UK, USA300 is much less
common than in the USA <xref ref-type="bibr" rid="pone.0017936-Otter1">[79]</xref>. USA300 has also been infrequently found in
Switzerland <xref ref-type="bibr" rid="pone.0017936-Monecke3">[80]</xref> and Spain <xref ref-type="bibr" rid="pone.0017936-Molinos1">[81]</xref>. In Abu Dhabi, three out
of 54 isolates were identified as USA300 <xref ref-type="bibr" rid="pone.0017936-Weber1">[31]</xref>. In Australia, although the
overall prevalence is low, case numbers are steadily increasing <xref ref-type="bibr" rid="pone.0017936-Monecke4">[82]</xref>. Some
infections with this strain have also been noted in Japan <xref ref-type="bibr" rid="pone.0017936-Diep1">[61]</xref> and Hong Kong (in the present
study). Two whole genome sequences of USA300 have been published
(USA300-FPR3757, GenBank CP000255, <xref ref-type="bibr" rid="pone.0017936-Diep1">[61]</xref> and USA300-TCH1516, GenBank
CP000730, <xref ref-type="bibr" rid="pone.0017936-Highlander1">[83]</xref>). Both sequences harbour SCC<italic>mec</italic> IV
and adjacent ACME genes. It has been hypothesised that this locus is related to
enhanced survival of the organism on intact skin and, thus, to increased
transmissibility by skin contact. However, a considerable proportion of
Australian USA300 isolates lack the ACME locus <xref ref-type="bibr" rid="pone.0017936-Monecke4">[82]</xref>. The absence of ACME has
been described in isolates from Colombia, too <xref ref-type="bibr" rid="pone.0017936-Arias1">[84]</xref>. Other genes or gene
clusters are also subject to a high degree of genetic variability in USA300 and
genotyping of 76 West Australian isolates identified 16 different variants of
USA300 <xref ref-type="bibr" rid="pone.0017936-Monecke4">[82]</xref>.
However, the most common variant in Germany, Abu Dhabi and Australia is
indistinguishable from the sequenced strain USA300-TCH1516. Variability within
USA300 can involve β-haemolysin converting phages (<italic>sak, chp,
scn</italic>) and enterotoxin genes (<italic>sek, seq</italic>). The authors
also observed isolates that yielded USA300-like hybridisation patterns
(including ACME), but lacked the SCC<italic>mec</italic> element <xref ref-type="bibr" rid="pone.0017936-Monecke4">[82]</xref> or even
the PVL genes (isolate courtesy of P. Beisser, Maastricht), respectively.
Resistance genes in USA300 are highly variable (see <xref ref-type="fig" rid="pone-0017936-g002">Figure 2</xref> and <xref ref-type="bibr" rid="pone.0017936-Monecke4">[82]</xref>). The recent detection of
plasmid-encoded <italic>cfr</italic> in an Irish USA300 isolate <xref ref-type="bibr" rid="pone.0017936-Shore2">[21]</xref> is a reason
for concern as this gene confers resistance to five classes of antimicrobial
drugs including the oxazolidinones (linezolid).</p><p>Other CC8-MRSA-IV strains have been found sporadically in Australia. One carries
PVL and enterotoxin genes <italic>sed+sej+ser</italic> and
<italic>sek+seq</italic>, but lacks ACME (WA MRSA-62). Another harbours
<italic>tst1+sec+sel</italic> and, variably,
<italic>edinA</italic>.</p><p>CC8-MRSA-V has been found occasionally in Saxony and Australia. The Australian
CC8-MRSA-V isolates (WA MRSA-53) carry <italic>sea</italic> and
<italic>seb+sek+seq</italic>. These genes, however, are absent in
the Saxon isolate.</p><p>CC8-MRSA-VIII harbouring a class A <italic>mec</italic> complex and
<italic>ccrA/B-4</italic> genes has been recently described in Canada <xref ref-type="bibr" rid="pone.0017936-Zhang1">[17]</xref> where this
strain is known as Canadian MRSA-9. It was reported to carry enterotoxin genes
<italic>sea</italic> and <italic>seb</italic>. The authors obtained two
isolates (one from Ireland <xref ref-type="bibr" rid="pone.0017936-Shore3">[85]</xref>, and one from Australia, WA MRSA-16) which were
similar with regard to SCC<italic>mec</italic> associated genes. However, they
lacked the enterotoxin genes.</p><p>Several CC8-MRSA carry irregular, multiple or composite SCC<italic>mec</italic>elements. One is ST8-MRSA-II also known as Irish AR05, AR13, AR14, Irish-01 or
Irish New03. This strain was predominant in Ireland <xref ref-type="bibr" rid="pone.0017936-Rossney2">[86]</xref> in the 1990s. However, it
now appears to be marginalised by other strains. Thus, the following description
is based partially on isolates from the 1990s. It is <italic>spa</italic> type
t190. This strain harbours SCC<italic>mec</italic> II, from which the
<italic>kdp</italic> operon is absent <xref ref-type="bibr" rid="pone.0017936-Shore1">[15]</xref>. Based on this observation
as well as on additional variation affecting the <italic>mec</italic> complex
and the presence of pUB110, carrying <italic>aadD</italic>, and
Tn<italic>554</italic>, carrying <italic>erm</italic>(A),
SCC<italic>mec</italic> II subtypes A to E have been described <xref ref-type="bibr" rid="pone.0017936-Shore1">[15]</xref>. Thus, the
microarray allows rapid SCC<italic>mec</italic> II subtyping with
[<italic>aadD+</italic> and <italic>mecI/xylR</italic>+]
being SCC<italic>mec</italic> IIA or IIB (depending on presence and localisation
of Tn<italic>554</italic>), [<italic>aadD</italic>+ and
<italic>mecI/xylR-</italic>] being SCC<italic>mec</italic> IIC,
[<italic>aadD</italic>- and <italic>mecI/xylR</italic>+]
being SCC<italic>mec</italic> IID and finally, [<italic>aadD</italic>- and
<italic>mecI/xylR</italic>-] being SCC<italic>mec</italic> IIE.
Additionally, this strain harbours <italic>ccrA/B-4</italic> genes, which are
more homologous to those of the SCC-CI element from <italic>S.
epidermidis</italic> than to other <italic>ccrA/B-4</italic> sequences from
MRSA <xref ref-type="bibr" rid="pone.0017936-Shore4">[87]</xref>. The
microarray revealed that the mercury resistance operon is usually present, and a
possible link to additional <italic>ccrA/B-4</italic> genes, as seen in a SCC-CI
element from <italic>S. epidermidis</italic> (ATCC12228), is currently under
investigation. Essentially all ST8-MRSA-II, AR13/14 isolates harbour
<italic>erm</italic>(A) and <italic>aacA-aphD</italic>. Other resistance
markers including <italic>blaZ+blaI+blaR</italic> and
<italic>mupA</italic> are variable. The majority of isolates carry a
lysogenic β-haemolysin converting phage (<italic>scn, sak,</italic> and
<italic>sea</italic>). They do not harbour enterotoxin genes apart from
<italic>sea.</italic> Protease genes <italic>splA, splB</italic> and
<italic>splE</italic> as well as <italic>sdrC</italic> are usually
absent.</p><p>Another strain with an irregular or composite SCC<italic>mec</italic> element is
ST8-MRSA-IV+<italic>ccrA/B-4</italic>, also known as Irish AR43,
Irish-02, UK-EMRSA-12 and -13. This strain predominated in Northern Ireland in
1999 <xref ref-type="bibr" rid="pone.0017936-Rossney2">[86]</xref>(when most of the isolates described herein were sampled), but it has also been
found in Norway (isolates courtesy of H. V. Aamont, Aakershus) as well as by the
authors in the UK and Australia. The <italic>spa</italic> type is usually t190
<xref ref-type="bibr" rid="pone.0017936-Shore4">[87]</xref>. This
strain harbours SCC<italic>mec</italic> IV, although some isolates have been
found to lack <italic>ccrA/B-2,</italic> possibly due to <italic>in
vitro</italic> passage or exposure to freezing and thawing during storage.
Variation in the region downstream of the <italic>mec</italic> complex or,
respectively, in the J1 and J3 regions, allowed distinguishing subtypes IVE and
IVF <xref ref-type="bibr" rid="pone.0017936-Shore1">[15]</xref>.
Isolates of Irish AR43 harbour an additional set of <italic>ccrA/B-4</italic>genes similar to Irish AR13/14.</p><p>Irregular SCC<italic>mec</italic> elements can also be observed in ST254-MRSA
which is known as UK-EMRSA-10 or the Hannover Epidemic strain
(<italic>spa</italic> t009 or t036). Although in the 1990s ST254-MRSA was
frequently isolated in German hospitals, it has receded since 2000. However,
this strain is the predominant MRSA isolated from horses in Germany <xref ref-type="bibr" rid="pone.0017936-Walther1">[75]</xref>. There are
two variants of this strain which differ in relation to the carriage of
SCC<italic>mec</italic> associated genes (see <xref ref-type="fig" rid="pone-0017936-g001">Figure 1</xref>). The Hannover Epidemic Strain is a
multi-resistant strain, and the antimicrobial resistance genes
<italic>tet</italic>(M) and <italic>aacA-aphD</italic> are always present.
In addition, <italic>aphA3, sat</italic> as well as the mercury resistance
operon can be detected in most isolates. The MSCRAMM gene <italic>bbp</italic>is usually absent. Enterotoxin genes <italic>seb+sek+seq</italic> are
always detectable. Genes associated with lysogenic β-haemolysin-converting
phages (s<italic>ea, sak</italic> and <italic>scn</italic>) are usually present
in isolates from humans, but have not been detected in equine isolates.</p></sec><sec id="s2f"><title>Clonal complex 9</title><p>Most CC9-MRSA strains have been recovered from veterinary sources. Particular
strains from humans, ST733/834, have been assigned to CC9 by MLST, but will be
discussed separately because of their distinct hybridisation pattern. CC9-MRSA
with SCC<italic>mec</italic> types III and V have mainly been recovered from
pigs or farm workers in mainland China, Hong Kong and Malaysia as well as in
Italy <xref ref-type="bibr" rid="pone.0017936-Wagenaar1">[88]</xref>-<xref ref-type="bibr" rid="pone.0017936-Cui1">[92]</xref>. The authors recently identified isolates of
CC9-MRSA-IV in turkeys (courtesy of S. Cortez de Jäckel, Delbrück) and
in retail chicken meat from Germany. Isolates are PVL-negative and do not carry
other enterotoxin genes besides <italic>egc.</italic> Resistance markers are the
β-lactamase operon, <italic>qacC</italic>, <italic>erm</italic>(B) and
<italic>aadD</italic>.</p></sec><sec id="s2g"><title>Clonal complex 12</title><p>An isolate of CC12-MRSA-IV genotyped for this study was found in Ireland <xref ref-type="bibr" rid="pone.0017936-Shore1">[15]</xref>. This strain
was also observed in a small number of cases in Norway <xref ref-type="bibr" rid="pone.0017936-Hanssen1">[93]</xref>. Another CC12-MRSA strain,
WA MRSA-59 from Australia, has an irregular or truncated SCC<italic>mec</italic>element (<italic>mecA, ugpQ, mecI, mecR1</italic>, but no <italic>xylR</italic>and no detectable recombinase genes). Isolates carried the enterotoxin homologue
ORF CM14, <italic>sea-N315</italic> and <italic>seb</italic>. PVL has not been
detected in this lineage.</p></sec><sec id="s2h"><title>Clonal complex 15</title><p>While CC15-MSSA are abundant among healthy carriers <xref ref-type="bibr" rid="pone.0017936-Monecke5">[94]</xref>, MRSA from this lineage
are extremely rare. To our knowledge, CC15-MRSA has only been detected in a
collection of Italian MRSA strains isolated in 1980. This included three
SCC<italic>mec</italic> I isolates and an isolate described to carry an
SCC<italic>mec</italic> I variant in which <italic>ccrA/B-1</italic> was
replaced by <italic>ccrA/B-2</italic><xref ref-type="bibr" rid="pone.0017936-Campanile1">[33]</xref>.
Within the present study, the authors did not identify a single CC15-MRSA
isolate among approximately 3,000 genotyped MRSA. Thus, the description of the
general features of this CC relies on data from MSSA (Supplemental <xref ref-type="supplementary-material" rid="pone.0017936.s003">file S3</xref>,
<xref ref-type="bibr" rid="pone.0017936-Monecke5">[94]</xref>;
<xref ref-type="bibr" rid="pone.0017936-Luedicke1">[95]</xref>).
Exotoxin genes (<italic>lukF/S-PV</italic>, <italic>sea, etA</italic>) are
detectable only in a very small minority of isolates. The <italic>chp</italic>and <italic>scn</italic> genes are present, but <italic>sak</italic> was absent
from essentially all isolates.</p></sec><sec id="s2i"><title>Clonal complex 20</title><p>A single isolate of a CC20-MRSA-V was identified in 2009 in Australia. It is
negative for PVL genes. It also lacks other toxin genes, although <italic>seb,
sec</italic>, <italic>sel</italic> and <italic>lukM+lukF-P83</italic>genes have been identified by the authors in CC20-MSSA of human and veterinary
origin.</p></sec><sec id="s2j"><title>Clonal complex 22</title><p>CC22 is a common and widespread clonal group and different MRSA strains have
emerged from this genetic background. The sequencing of a complete genome of a
CC22 strain could provide valuable insight in <italic>S. aureus</italic>biodiversity since alleles from CC22 appear to differ from previously published
sequences. For instance, a CC22-specific allele of <italic>ssl7/set1</italic>has already been identified (GenBank AF188836). Many probes on the DNA array
yield irregular or weak signals with CC22 isolates, which could be attributed to
the presence of divergent sequences. Beside <italic>ssl/set</italic>- and
MSCRAMM genes, this also affects the γ-haemolysin locus. Probes for
<italic>lukS/F-hlg</italic> and <italic>hlgA</italic> (derived from CC1, 5
and 8 sequences) yield weak or no signals, while a probe based on a
<italic>lukS-hlg</italic> sequence from CC45 is strongly reactive (GenBank
EF672356) <xref ref-type="bibr" rid="pone.0017936-Monecke6">[96]</xref>). Leukocidin <italic>lukD+lukE</italic> and
proteases <italic>splA, splB</italic> and <italic>splE</italic> have not been
detected in CC22 isolates and it is not yet known whether they may be present as
variant alleles or are absent in this lineage.</p><p>CC22-MRSA with SCC<italic>mec</italic> types I, II or III have, to our knowledge,
not been reported.</p><p>ST22-MRSA-IV is a pandemic CC22-MRSA strain. This strain is known as UK-EMRSA-15,
Irish AR06, Barnim Epidemic Strain or Spanish PFGE type E13, <xref ref-type="bibr" rid="pone.0017936-Vindel1">[34]</xref>, or
Canadian MRSA-8 <xref ref-type="bibr" rid="pone.0017936-Christianson1">[28]</xref>. It has been reported in many countries <xref ref-type="bibr" rid="pone.0017936-Campanile1">[33]</xref>; <xref ref-type="bibr" rid="pone.0017936-Rossney1">[57]</xref>; <xref ref-type="bibr" rid="pone.0017936-Ghebremedhin1">[97]</xref>-<xref ref-type="bibr" rid="pone.0017936-Dsouza1">[104]</xref>. Where
ST22-MRSA-IV occurs, it tends to be abundant. In Dresden, ST22-MRSA-IV accounted
for nearly 50% (141 out of 304 genotyped isolates from 2007 to 2009); in
Portugal for 54% <xref ref-type="bibr" rid="pone.0017936-AiresdeSousa2">[49]</xref>, in Malta for 66% <xref ref-type="bibr" rid="pone.0017936-Scicluna1">[40]</xref>, and in Ireland <xref ref-type="bibr" rid="pone.0017936-Shore3">[85]</xref>; <xref ref-type="bibr" rid="pone.0017936-Rossney3">[105]</xref> as well
as on the Azores <xref ref-type="bibr" rid="pone.0017936-Conceicao2">[59]</xref> for more than 80% of MRSA isolates. In
England, ST22-MRSA-IV is increasingly common (apparently at the expense of
ST36-MRSA-II, UK-MRSA-16, <xref ref-type="bibr" rid="pone.0017936-Ellington1">[106]</xref>), being currently responsible for 85% of MRSA
bacteraemia cases. ST22-MRSA-IV occurs in hospitals as well as in outpatients,
and it has been recovered from animals such as horses <xref ref-type="bibr" rid="pone.0017936-Walther1">[75]</xref>, cats <xref ref-type="bibr" rid="pone.0017936-Moodley1">[107]</xref> and dogs
<xref ref-type="bibr" rid="pone.0017936-Walther2">[102]</xref>;
<xref ref-type="bibr" rid="pone.0017936-Moodley1">[107]</xref>.
Common resistance markers are β-lactamase and <italic>erm</italic>(C). A
high percentage of Maltese ST22-MRSA-IV isolates harbour Q6GD50 which has not
been found in isolates from other geographic regions <xref ref-type="bibr" rid="pone.0017936-Scicluna1">[40]</xref>. Variable virulence
markers in ST22-MRSA-IV are <italic>sec</italic> and <italic>sel</italic> as
well as the IEC genes encoded by lysogenic β-haemolysin-converting phages
(<italic>sak, chp, scn</italic>). The presence of <italic>tst1,</italic> or
sometimes of <italic>tst1</italic> and <italic>sea</italic>, is found in some
isolates from Abu Dhabi <xref ref-type="bibr" rid="pone.0017936-Weber1">[31]</xref>, Egypt (isolates courtesy of M. Kamal El Din, Cairo)
and England (where patients' names suggest a Middle Eastern origin). A case
of an infection with a <italic>tst1-</italic>positive CC22-MRSA-IV has recently
been reported from the USA, where it was one of the first reports of this strain
<xref ref-type="bibr" rid="pone.0017936-Wolter1">[108]</xref>.</p><p>Another, distinct ST22-MRSA-IV strain is found in Dublin, Ireland <xref ref-type="bibr" rid="pone.0017936-Shore5">[109]</xref>. Its most
distinguishing feature is the presence of the ACME-locus. It carries
β-lactamase and <italic>erm</italic>(C) as well as, in the majority of
cases, <italic>lnu</italic>(A), <italic>aacA-aphD, aadD</italic> and
<italic>mupA.</italic></p><p>A large scale nosocomial outbreak of PVL-positive ST22-MRSA-IV has been described
in Bavaria, Germany <xref ref-type="bibr" rid="pone.0017936-Linde1">[110]</xref>. Other isolates have also been found in Australia,
England <xref ref-type="bibr" rid="pone.0017936-Ellington2">[111]</xref>, Ireland <xref ref-type="bibr" rid="pone.0017936-Rossney1">[57]</xref> Abu Dhabi <xref ref-type="bibr" rid="pone.0017936-Weber1">[31]</xref> and Hong
Kong. Additionally, PVL-positive ST22-MRSA-IV has been isolated from patients in
Germany who had family ties to Turkey <xref ref-type="bibr" rid="pone.0017936-Maier1">[112]</xref>. Their presence in
epidemiologically unrelated settings suggested a polyphyletic origin, given that
PVL-positive CC22-MSSA are common and widespread <xref ref-type="bibr" rid="pone.0017936-Monecke7">[113]</xref>. Indeed, the
demonstration of at least three different PVL-encoding phages, ϕPVL,
ϕ108PVL and an unidentified icosahedral phage, in CC22-MRSA from England
and Wales <xref ref-type="bibr" rid="pone.0017936-Scicluna1">[40]</xref> indicates that this “strain” has evolved
on multiple occasions. Furthermore, ST22-MRSA-IV harbouring PVL and
<italic>tst1</italic> genes have been recently described in India <xref ref-type="bibr" rid="pone.0017936-Nadig1">[114]</xref>. Variable
resistance markers in PVL-positive ST22-MRSA-IV include β-lactamase,
<italic>erm</italic>(C), <italic>aacA-aphD, aadD, dfrA</italic> and
Q6GD50.</p><p>Sporadic cases of a PVL-negative CC22-MRSA-V have been identified by the authors
in Saxony, as well as a PVL-positive CC22-MRSA-V in Western Australia.</p></sec><sec id="s2k"><title>Clonal complex 30</title><p>CC30 is another important clonal complex from which HA- and CA-MRSA originate. It
is represented by the genome sequence of Sanger MRSA 252. Core genomic markers,
<italic>ssl/set</italic>- and MSCRAMM genes are present as allelic variants
which differ distinctly from other CCs. Some of these variants resemble alleles
found in other CCs such as CC22 and CC45 <xref ref-type="bibr" rid="pone.0017936-Monecke6">[96]</xref> which may be more closely
related to CC30 than to other CCs such as CC1, CC5 or CC8 <xref ref-type="bibr" rid="pone.0017936-Cooper1">[115]</xref>. Shared features of CC30
strains include the presence of <italic>egc</italic> (although partial deletions
may occur) and <italic>cna</italic>. MSCRAMM genes <italic>bbp, fnbB</italic>and <italic>sdrD</italic> are usually detectable, but may be deleted from
individual isolates. Lysogenic β-haemolysin-converting phages are usually
commonly present. Because of the variable presence of <italic>sea</italic> and
<italic>chp,</italic> it can be assumed that different phages have
integrated into CC30 genomes.</p><p>CC30-MRSA-I was reported in Italy in 1980 <xref ref-type="bibr" rid="pone.0017936-Campanile1">[33]</xref>.</p><p>A more widespread HA-MRSA strain from this lineage is ST36/39-MRSA-II, also known
as UK-EMRSA-16 <xref ref-type="bibr" rid="pone.0017936-Murchan1">[116]</xref>, USA200, Irish AR7.0/AR07.2, Spanish PFGE type E12,
<xref ref-type="bibr" rid="pone.0017936-Vindel1">[34]</xref>, or
Canadian MRSA-4 <xref ref-type="bibr" rid="pone.0017936-Christianson1">[28]</xref>. Although frequently isolated in the UK and Ireland
in the 1990s <xref ref-type="bibr" rid="pone.0017936-Shore1">[15]</xref>, recently it has become increasingly rare <xref ref-type="bibr" rid="pone.0017936-Moodley1">[107]</xref>. Isolates
have also been found in Malta <xref ref-type="bibr" rid="pone.0017936-Scicluna1">[40]</xref>; <xref ref-type="bibr" rid="pone.0017936-Gould1">[117]</xref> and South Africa <xref ref-type="bibr" rid="pone.0017936-JansenvanRensburg1">[73]</xref>. In Germany,
ST36-MRSA-II is very rare. This strain harbours SCC<italic>mec</italic> II
including <italic>aadD</italic> and <italic>erm</italic>(A) in integrated
p<italic>UB110</italic> and Tn<italic>554</italic>, respectively, as well as
the β-lactamase operon and occasional other resistance markers (<xref ref-type="fig" rid="pone-0017936-g002">Figure 2</xref>). Most clinical
isolates carry <italic>tst1,</italic> although this gene is absent in the genome
sequence of Sanger MRSA252. This strain also lacks <italic>sdrD</italic>. The
enterotoxin gene <italic>sea</italic> is also common, although another reference
strain, ATCC43300, is <italic>sea</italic>-negative. ATCC43300 is unique among
the tested ST36/39-MRSA-II in being positive for <italic>sec+sel</italic>and <italic>fnbB</italic>.</p><p>Another important CC30-MRSA strain is the PVL-positive ST30-MRSA-IV, Southwest
Pacific Clone, USA1100 or West Samoan Phage Pattern (WSPP) Clone. This CA-MRSA
strain was first observed among Samoan immigrants in New Zealand, but is
widespread with isolates investigated in the present study coming from Germany,
Switzerland, the UK, Australia <xref ref-type="bibr" rid="pone.0017936-Monecke1">[29]</xref>; <xref ref-type="bibr" rid="pone.0017936-Monecke3">[80]</xref>, Hong Kong, Taiwan <xref ref-type="bibr" rid="pone.0017936-Takano2">[50]</xref>, Abu Dhabi, and the USA
(NARSA 484). Other reports of this strain include Ireland <xref ref-type="bibr" rid="pone.0017936-Rossney1">[57]</xref>, where it is the
predominant PVL-positive MRSA strain, Scandinavia, Latvia <xref ref-type="bibr" rid="pone.0017936-Miklasevics1">[118]</xref> and Kuwait <xref ref-type="bibr" rid="pone.0017936-Udo2">[119]</xref>. The WSPP
Clone apparently evolved from the pandemic phage type 80/81 strain. This MSSA
emerged in the 1950s and caused outbreaks of severe infections worldwide;
however it virtually disappeared after the introduction of
penicillinase-resistant β-lactams <xref ref-type="bibr" rid="pone.0017936-Robinson1">[120]</xref>.</p><p>A PVL-negative, but <italic>tst1</italic>-positive strain of ST30-MRSA-IV is
sporadically isolated in Ireland <xref ref-type="bibr" rid="pone.0017936-Shore1">[15]</xref> and Australia. An infection with a PVL-positive
CC30-MRSA-V has been described in Egypt <xref ref-type="bibr" rid="pone.0017936-Enany1">[121]</xref>. A similar isolate has been
identified from a patient with a SSTI living in the German/Polish border region
(courtesy of R. Hillert, Görlitz).</p></sec><sec id="s2l"><title>Clonal complex 45</title><p>CC45 is another major lineage from which several MRSA strains have emerged. They
cluster into two distinct groups as the majority of isolates belong to
<italic>agr</italic> group I, while some strains yield a unique pattern.
They fail to react with all three <italic>agrD</italic>-I probes, but they are
positive with <italic>agrB</italic> and <italic>agrC</italic> probes
corresponding to <italic>agr</italic> groups I and IV (for the sake of
simplicity they are here referred to as CC45/<italic>agr</italic> IV). PVL has
not been detected in the present study among CC45-MRSA isolates. However, two
cases of PVL-positive ST45-MRSA-IV from Belgium <xref ref-type="bibr" rid="pone.0017936-Deurenberg1">[45]</xref> and Germany <xref ref-type="bibr" rid="pone.0017936-Layer1">[122]</xref> have been
reported. Leukocidin genes <italic>lukD+lukE</italic> were not identified.
In contrast to CC22, the γ-haemolysin genes <italic>hlgA</italic> and
<italic>lukF-hlg</italic> can be detected in CC45 isolates, and
<italic>lukS-hlg</italic> was shown to be present in a specific allelic
variant (GenBank EF672356, <xref ref-type="bibr" rid="pone.0017936-Monecke6">[96]</xref>). As observed in CC22, probes for protease genes do
not yield signals. Enterotoxins <italic>sec</italic> and <italic>sel</italic>are occasionally found. Irregular signals for <italic>ssl/set</italic> might
indicate the presence of yet unknown alleles. The gene <italic>cna</italic> is
present, but <italic>sasG</italic> can only be detected in the
CC45/<italic>agr</italic> IV isolates.</p><p>ST45-MRSA-II, (known as USA600, USA600-MRSA-II or Canadian MRSA-1 <xref ref-type="bibr" rid="pone.0017936-Christianson1">[28]</xref>)
appears to be largely restricted to North America, where glycopeptide-resistant
variants and an unusually high mortality rate of bloodstream infections
associated with this strain have been reported <xref ref-type="bibr" rid="pone.0017936-Moore1">[123]</xref>. Outside the USA,
ST45-MRSA-II is rarely isolated, but this strain has, like ST45-MRSA-I and -III,
been sporadically detected in Hong Kong <xref ref-type="bibr" rid="pone.0017936-Ip1">[47]</xref>. In addition, the authors have
identified a single isolate of ST45-MRSA-II in Australia. This isolate as well
as reference strains NARSA 22, NARSA 648 and NARSA 715 were genotyped. They
carry SCC<italic>mec</italic> II, including <italic>aadD</italic> and
<italic>erm</italic>(A), as well as the β-lactamase operon. Variable
resistance markers (positive in NARSA 22) include <italic>aacA-aphD,
dfrA</italic> and <italic>qacC.</italic></p><p>Another important CC45 strain is ST45-MRSA-IV, which is known as the Berlin
Epidemic Strain, WA MRSA-75 or USA600-MRSA-IV. In Saxony, it is a relatively
common MRSA strain (<italic>ca.</italic> 9% of MRSA isolates from
Dresden, 2007-2009), and in Belgium it is the predominant MRSA strain <xref ref-type="bibr" rid="pone.0017936-Deurenberg1">[45]</xref>. This
strain also occurs in the UK, the Netherlands <xref ref-type="bibr" rid="pone.0017936-Deurenberg1">[45]</xref>, Switzerland <xref ref-type="bibr" rid="pone.0017936-Blanc1">[124]</xref>, Croatia
<xref ref-type="bibr" rid="pone.0017936-Budimir1">[41]</xref> and
Australia. Unlike the Australian isolates, most of the Saxon isolates harbour
<italic>aphA3</italic> and <italic>sat.</italic> As in other CC45 strains,
<italic>egc</italic> is present but <italic>seg</italic> is not detectable
in many isolates. Enterotoxin genes <italic>sec</italic> and
<italic>sel</italic> as well as genes <italic>sak, chp</italic> and
<italic>scn</italic>, indicative of lysogenic β-haemolysin-converting
phages, are commonly detected.</p><p>A similar CC45-MRSA-IV strain isolated in Australia carries <italic>sec, sel,
tst1</italic> and ACME.</p><p>ST45-MRSA-V has been found sporadically in Germany and in Australia (WA MRSA-4)
as well as in Portugal <xref ref-type="bibr" rid="pone.0017936-AiresdeSousa2">[49]</xref>. Most isolates tested for this study harbour
<italic>tst1, sek</italic> and <italic>seq.</italic></p><p>A distinct group of CC45 isolates display <italic>agr</italic> IV alleles.
Furthermore, these strains differ from other CC45 strains in that they carry
other alleles of MSCRAMM genes <italic>fnbA, fnbB, sdrD, vwb</italic> and of
<italic>lmrP</italic>. They are positive for <italic>sasG</italic>. Isolates
carry <italic>sej</italic> and usually yield weak signals for
<italic>ser</italic> probes, which may indicate the presence of an allelic
variant of this gene. The gene <italic>sed</italic>, which is normally located
on the same plasmids as <italic>sej</italic> and <italic>ser</italic>(<italic>e.g</italic>., pIB485, GenBank M94872.1) cannot be detected. The
<italic>spa</italic> types associated with CC45/<italic>agr</italic> IV
isolates are t727, t1081 (although this type can also be observed in ST1048 and
ST1774, see below and <xref ref-type="bibr" rid="pone.0017936-Ho1">[125]</xref>) or t1575. CC45/<italic>agr</italic> IV MRSA are
widespread and increasingly common in Australia. There are two different strains
carrying SCC<italic>mec</italic> type IV (WA MRSA-23) or V elements (WA
MRSA-84), respectively. CC45/<italic>agr</italic> IV-MRSA-IV and -V are commonly
isolated in Hong Kong (author's observations, <xref ref-type="bibr" rid="pone.0017936-Ip1">[47]</xref>; <xref ref-type="bibr" rid="pone.0017936-Ho1">[125]</xref>) and few isolates of a
CC45/<italic>agr</italic> IV-MRSA with a combined SCC<italic>mec</italic>IV/V element have been identified as part of this study in Hong Kong. One of
these isolates is ACME-positive. Sporadic isolates of CC45/<italic>agr</italic>IV-MRSA-IV have also been observed in Ireland <xref ref-type="bibr" rid="pone.0017936-Shore1">[15]</xref>.</p></sec><sec id="s2m"><title>Clonal complex 59</title><p>Several strains of CC59-MRSA can be distinguished based on carriage of
SCC<italic>mec</italic> elements and PVL as well as on MLST and
<italic>spa</italic> typing. West Australian strains of CC59 have recently
been described in detail <xref ref-type="bibr" rid="pone.0017936-Coombs3">[126]</xref>.</p><p>One PVL-positive strain, ST59-MRSA-IV, also known as USA1000, is mainly
restricted to the USA (reference strains NARSA 483, NARSA 676). The authors
identified a single isolate of USA1000 from Australia. The <italic>spa</italic>types associated with this strain are t216 or t316. USA1000 carries the
β-lactamase operon and, variably, <italic>erm</italic>(A). Beside PVL, it
harbours <italic>chp, scn</italic> and, variably, the enterotoxin genes
<italic>seb, sek</italic> and <italic>seq</italic>. A sporadic Australian
strain (WA MRSA-73, <italic>spa</italic> t528) is PVL-negative, but otherwise
indistinguishable from USA1000 in terms of overall hybridisation patterns.</p><p>WA MRSA-24 is an infrequently isolated, mainly Australian CC59 strain with a
SCC<italic>mec</italic> IV element. This strain belongs to ST87 (a SLV of
ST59) and <italic>spa</italic> type t216. The β-lactamase operon,
<italic>msr</italic>(A), <italic>mph</italic>(C),
<italic>aphA3</italic>+<italic>sat, seb, sek</italic> and
<italic>seq</italic> are present. This strain is also positive for
<italic>sak</italic>, <italic>chp</italic> and <italic>scn</italic> but
lacks <italic>sea</italic>. PVL is absent.</p><p>A group of sporadic Australian, Hong Kong and UK <xref ref-type="bibr" rid="pone.0017936-Ellington3">[127]</xref> isolates, dubbed WA
MRSA-55/56, are ST59-MRSA-IV/<italic>spa</italic> type t437. These isolates
carry PVL (although one PVL-negative isolate was also identified), <italic>seb,
sek</italic> and <italic>seq.</italic> The gene <italic>sea</italic> is only
detected occasionally.</p><p>The most widespread CC59-MRSA strain is PVL-positive ST59/952-MRSA-V<sub>T</sub>which is known as the Taiwan Clone. Isolates of this strain belong to
<italic>spa</italic> types t437, t1950 or t2365. ST59/952-MRSA-V<sub>T</sub>is a common and clinically important MRSA strain in Taiwan <xref ref-type="bibr" rid="pone.0017936-Takano1">[14]</xref>; <xref ref-type="bibr" rid="pone.0017936-BoyleVavra1">[128]</xref>-<xref ref-type="bibr" rid="pone.0017936-Wang1">[131]</xref>. The authors found this
strain in Hong Kong, Australia, where it is the most frequently isolated
CC59-MRSA strain, Saxony (a single case of recurrent furunculosis, <xref ref-type="bibr" rid="pone.0017936-Monecke1">[29]</xref>) and the
UK <xref ref-type="bibr" rid="pone.0017936-Ellington3">[127]</xref>.
This strain has a characteristic variant of a SCC<italic>mec</italic> V element,
in which two <italic>ccrC</italic> genes are present (SCC<italic>mec</italic>V<sub>T</sub> or 5C2&5, GenBank AB12129, <xref ref-type="bibr" rid="pone.0017936-Zhang2">[132]</xref>). Enterotoxin genes
<italic>seb+sek</italic>+<italic>seq</italic> are usually
detectable. All isolates carry <italic>erm</italic>(B),
<italic>aphA3+sat</italic> and
<italic>blaZ+blaI+blaR</italic>. In addition,
<italic>tet</italic>(K) and <italic>cat</italic> can often be found. This strain
is indistinguishable from WA MRSA-55/56 in all markers covered by the microarray
with the sole exception of the SCC<italic>mec</italic> element. Therefore, it
may be assumed that both strains emerged from the same ancestral MSSA acquiring
different SCC<italic>mec</italic> elements.</p><p>Additionally, there are also ST59-MRSA isolates harbouring a
SCC<italic>mec</italic> V rather than a SCC<italic>mec</italic>V<sub>T</sub> element. PVL-negative ST59-MRSA-V (WA MRSA-9) has occasionally
been observed in Australia <xref ref-type="bibr" rid="pone.0017936-Coombs3">[126]</xref> as well as PVL-positive CC59/ST359-MRSA-V in the UK
<xref ref-type="bibr" rid="pone.0017936-Monecke3">[80]</xref>.</p><p>WA MRSA-15 is another ST59 strain with a composite or novel
SCC<italic>mec</italic> element. This is the second most common CC59-MRSA
strain in Australia <xref ref-type="bibr" rid="pone.0017936-Coombs3">[126]</xref>. Its <italic>spa</italic> type is t976. Microarray
hybridisation and PCR results suggest either the presence of a composite IV and
V SCC<italic>mec</italic> element, or the presence of <italic>ccrC</italic> in
addition to SCC<italic>mec</italic> IV. This strain is PVL-negative, but it
harbours <italic>sea</italic> and usually
<italic>seb+sek</italic>+<italic>seq.</italic> The β-lactamase
operon is present while <italic>msr</italic>(A)<italic>+mph</italic>(C),
<italic>aphA3+sat</italic> and <italic>tet</italic>(K) can be detected
sporadically.</p></sec><sec id="s2n"><title>Sequence type 72</title><p>According to the MLST database, ST72 belongs to CC8. However, isolates yield a
distinctive hybridisation profile. Differences to CC8 include the presence of
<italic>egc</italic> and of CC5-like alleles of several MSCRAMM genes
(<italic>bbp, sdrC, sdrD</italic>). MLST suggests a recombination of CC5 and
CC8. Specifically, <italic>yqiL</italic>, <italic>pta</italic> and
<italic>tpi</italic> may be derived from CC8 (<italic>yqiL</italic>-3,
<italic>pta</italic>-4, <italic>tpi-</italic>4), while <italic>gmk</italic>,
<italic>aroE</italic> and <italic>arcC</italic> suggest CC5 parentage
(<italic>gmk</italic>-8, <italic>aroE</italic>-4, <italic>arcC</italic>-1).
The <italic>glpF</italic> allele (<italic>glpF</italic>-1) may have originated
from either clonal complex. Mapping the positions of probe binding sites over
the known CC5 and CC8 genomes shows that CC5- and CC8-derived genes alternate
through the genome suggesting multiple recombination events. Alleles of some
<italic>ssl/set</italic> genes and <italic>vwB, sasG</italic> and
<italic>clfB</italic> which are not associated with CC5 or CC8 suggest the
involvement of additional, yet unidentified donor strains.</p><p>Two MRSA strains have been identified. One is a PVL-negative ST72-MRSA-IV which
is known as USA700. It does not harbour exotoxins beside <italic>egc</italic>,
and its carriage of resistance genes is variable (<xref ref-type="fig" rid="pone-0017936-g002">Figure 2</xref>). This strain includes NARSA 386 and
689. Isolates have been identified in Saxony and in Abu Dhabi. PVL-positive
ST72-MRSA-IV has been isolated by the authors in Australia (WA MRSA-44) and from
SSTIs of German tourists returning from Costa Rica.</p></sec><sec id="s2o"><title>Clonal complex 75, sequence types 883 and 1303</title><p>CC75 (ST75, ST1304) as well as ST883 and ST1303 are discussed as a group because
they share several distinctive features. ST75-MRSA-IV (WA MRSA-8 and -79)
isolates have been recovered from people residing in remote communities of
Northern and Western Australia, and appear to be largely restricted to this part
of the world. Although it is PVL-negative, this strain is a common cause of
community acquired SSTIs <xref ref-type="bibr" rid="pone.0017936-McDonald1">[133]</xref>. There has been a single report of ST75-MRSA-V <xref ref-type="bibr" rid="pone.0017936-McDonald1">[133]</xref>. One
isolate of ST1304-MRSA-IV (WA MRSA-72) from Australia was characterised. This is
a SLV of ST75-MRSA-IV that also differs in carriage of possibly plasmid-borne
enterotoxin genes (see below). ST883-MRSA-IV (WA MRSA-47) and ST1303-MRSA-IV
occur sporadically in the Northern part of Western Australia.</p><p>Recently it has been shown that MLST genes of these strains differ grossly from
that of any other known <italic>S. aureus</italic> (see <xref ref-type="bibr" rid="pone.0017936-Ng1">[134]</xref> and <xref ref-type="fig" rid="pone-0017936-g004">Figure 4</xref>). Although not phenotypically
different to other <italic>S. aureus</italic>, it has been suggested that ST75
strains should be regarded as a new subspecies of <italic>S. aureus</italic><xref ref-type="bibr" rid="pone.0017936-Ng1">[134]</xref>. These
strains do not yield hybridisation signals with specific probes for capsule
types 1, 5 or 8 and for <italic>agr</italic> groups I to IV. Unique
<italic>agrB, agrD</italic> and <italic>agrC</italic> sequences have been
demonstrated in ST75 (GenBank FJ154839, <xref ref-type="bibr" rid="pone.0017936-Monecke8">[135]</xref>; <xref ref-type="bibr" rid="pone.0017936-Monecke9">[136]</xref>) and ST883 (GenBank
HQ260328, <xref ref-type="bibr" rid="pone.0017936-Monecke9">[136]</xref>). Genes encoding leukocidins and exfoliative toxins
as well as protease genes <italic>splA, splB</italic> and <italic>splE</italic>cannot be detected by microarray hybridisation. Probes for MSCRAMM-,
<italic>ssl/set</italic>- and <italic>hsdS</italic>-genes generally yield
patterns which differ from all other <italic>S. aureus</italic> strains. With
regard to these genes, ST883 and ST1303 resemble each other but differ from
CC75. The gene <italic>cna</italic> is absent and <italic>sasG</italic> can be
detected in CC75 only. The β-haemolysin gene <italic>hlb</italic> can only
be detected when using random primer directed amplification, suggesting the
presence of an allelic variant. CC75 and ST1303 carry <italic>egc</italic>(although <italic>sen</italic> is either absent, or present in an unknown
allele). Seven out of eighteen ST75-MRSA-IV isolates as well as the single
ST1303-MRSA-IV isolate tested carry <italic>seb</italic>. ST1304-MRSA-IV is
positive for <italic>sed+sej+ser.</italic></p><fig id="pone-0017936-g004" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0017936.g004</object-id><label>Figure 4</label><caption><title>Network graph visualising relationships between concatenated MLST
sequences of all STs mentioned in this study.</title></caption><graphic xlink:href="pone.0017936.g004"></graphic></fig></sec><sec id="s2p"><title>Clonal complex 80</title><p>The vast majority of CC80 isolates belong to a PVL-positive strain harbouring
SCC<italic>mec</italic> IV. Although SCC<italic>mec</italic> type I has
previously been described in CC80 <xref ref-type="bibr" rid="pone.0017936-Budimir1">[41]</xref>, the authors did not
identify this strain in this study. Likewise, PVL-negative variants of
CC80-MRSA-IV are infrequently isolated and have only been found in France and
Croatia <xref ref-type="bibr" rid="pone.0017936-Budimir1">[41]</xref>.</p><p>PVL-positive CC80-MRSA-IV has been dubbed the European CA-MRSA Clone. The strain
is widespread and has been isolated in Austria <xref ref-type="bibr" rid="pone.0017936-Krziwanek3">[137]</xref>, Denmark (where this
strain was detected as early as 1993 <xref ref-type="bibr" rid="pone.0017936-Faria1">[138]</xref>), France <xref ref-type="bibr" rid="pone.0017936-Dauwalder1">[44]</xref>, Germany
<xref ref-type="bibr" rid="pone.0017936-Monecke3">[80]</xref>;
<xref ref-type="bibr" rid="pone.0017936-Monecke10">[139]</xref>,
Greece (isolates courtesy of V. Gogou, Larissa, <xref ref-type="bibr" rid="pone.0017936-AiresdeSousa1">[48]</xref>; <xref ref-type="bibr" rid="pone.0017936-Vourli1">[140]</xref>), Ireland
<xref ref-type="bibr" rid="pone.0017936-Rossney1">[57]</xref>,
Malta <xref ref-type="bibr" rid="pone.0017936-Scicluna1">[40]</xref>,
the Netherlands <xref ref-type="bibr" rid="pone.0017936-StamBolink1">[141]</xref>, Norway <xref ref-type="bibr" rid="pone.0017936-Hanssen1">[93]</xref>, Portugal <xref ref-type="bibr" rid="pone.0017936-Conceicao3">[142]</xref>, Sweden
<xref ref-type="bibr" rid="pone.0017936-Fang1">[143]</xref>,
Switzerland <xref ref-type="bibr" rid="pone.0017936-Monecke3">[80]</xref> and the UK <xref ref-type="bibr" rid="pone.0017936-Monecke3">[80]</xref>; <xref ref-type="bibr" rid="pone.0017936-Holmes1">[144]</xref>; <xref ref-type="bibr" rid="pone.0017936-Otter2">[145]</xref>. In Greece, a considerable
percentage of MRSA infections can be attributed to this strain <xref ref-type="bibr" rid="pone.0017936-Vourli1">[140]</xref>. The
authors have identified isolates in Abu Dhabi, and other studies also indicate a
wide distribution in the Middle East including Kuwait <xref ref-type="bibr" rid="pone.0017936-Udo2">[119]</xref>, Lebanon <xref ref-type="bibr" rid="pone.0017936-Tokajian1">[146]</xref>, Israel
<xref ref-type="bibr" rid="pone.0017936-Adler1">[39]</xref>, Egypt
<xref ref-type="bibr" rid="pone.0017936-Enany2">[147]</xref>Algeria <xref ref-type="bibr" rid="pone.0017936-Bekkhoucha1">[148]</xref> and Tunisia <xref ref-type="bibr" rid="pone.0017936-BenNejma1">[149]</xref>. Travellers returning
from the Dead Sea or from Saudi Arabia to Germany <xref ref-type="bibr" rid="pone.0017936-Maier1">[112]</xref>, or from Tunisia or Libya
to Switzerland <xref ref-type="bibr" rid="pone.0017936-Francois1">[62]</xref> as well as patients with family ties to Turkey <xref ref-type="bibr" rid="pone.0017936-Maier1">[112]</xref> have been
found to carry this strain. In Australia, ST80-MRSA-IV as well as two SLVs,
ST583 (WA MRSA-17) and ST728 (WA MRSA-30) are rarely isolated. CC80-MRSA-IV
carries PVL, <italic>etD</italic> and <italic>edinC</italic>, but lack
enterotoxin genes (beside an ubiquitous homologue, GenBank
CP000046.1:SACOL1657). Nearly all CC80-MRSA-IV isolates carry
<italic>aphA3</italic> and <italic>sat</italic>; and they harbour the
plasmid encoded genes <italic>blaZ, tet</italic>(K) and <italic>far1</italic>.
Additional resistance genes <italic>lnu</italic>(A) or <italic>erm</italic>(C)
are rarely detected. Mupirocin resistance in this strain has been reported
previously <xref ref-type="bibr" rid="pone.0017936-Udo3">[150]</xref>.</p></sec><sec id="s2q"><title>Clonal complex 88</title><p>Several different CA-MRSA belong to this CC which appears, based on
<italic>spa</italic> sequences and hybridisation profile, closely related to
CC1 and CC80. It includes ST78-MRSA-IV (as well as its SLVs ST129, ST255,
ST257), which is known in Australia as WA MRSA-2. This strain is PVL-negative,
but usually harbours enterotoxin genes <italic>sec</italic> and
<italic>sel</italic>. In addition, the vast majority of isolates carry
<italic>blaZ</italic> and <italic>erm</italic>(A). It is frequently isolated
in Australia, and a single isolate has been identified, as part of this study,
in a patient from Saxony.</p><p>CC88-MRSA-IV carrying the exfoliative toxin gene <italic>etA</italic> were
identified by the authors in the Netherlands, Portugal, Angola and Senegal.
There is also a report from Japan <xref ref-type="bibr" rid="pone.0017936-Ozaki1">[151]</xref>. PVL-positive CC88-MRSA-IV
has been identified by the authors in the UK <xref ref-type="bibr" rid="pone.0017936-Monecke3">[80]</xref>, Abu Dhabi and Australia.
Other reports of this strain have come from Spain <xref ref-type="bibr" rid="pone.0017936-Aspiroz1">[152]</xref> and Nigeria <xref ref-type="bibr" rid="pone.0017936-Ghebremedhin2">[153]</xref>.</p><p>PVL-positive CC88-MRSA-V and PVL-negative CC88-MRSA-VI have been identified
sporadically by the authors in Western Australia. PVL-positive CC88-MRSA-V were
recently described from Italy <xref ref-type="bibr" rid="pone.0017936-Campanile1">[33]</xref>; <xref ref-type="bibr" rid="pone.0017936-Stefani1">[ 154]</xref>.</p></sec><sec id="s2r"><title>Sequence type 93</title><p>ST93 is a unique ST of <italic>S. aureus</italic>, which is essentially
restricted to Australia. While PVL-negative ST93-MRSA-IV and PVL-positive
ST93-MRSA-V<sub>T</sub> are extremely rare, a PVL-positive ST93-MRSA-IV is
common and currently spreading across Australia <xref ref-type="bibr" rid="pone.0017936-Coombs4">[155]</xref>. This CA-MRSA strain is
also known as the Queensland Clone <xref ref-type="bibr" rid="pone.0017936-Munckhof1">[156]</xref>. A few cases have been
identified in the UK suggesting small scale importation due to travel activities
<xref ref-type="bibr" rid="pone.0017936-Ellington4">[157]</xref>.
Recently, a whole genome sequence, JKD6159 (GenBank CP002114), has been
released. In terms of hybridisation profiles and especially with regard to
<italic>ssl/set</italic> genes, ST93 differs markedly from other <italic>S.
aureus</italic> lineages <xref ref-type="bibr" rid="pone.0017936-Monecke3">[80]</xref>. Enterotoxin genes and <italic>tst1</italic> are
absent but the enterotoxin homologue ORF CM14 is present.</p></sec><sec id="s2s"><title>Clonal complex 97</title><p>CC97-MSSA can often be isolated from cattle <xref ref-type="bibr" rid="pone.0017936-Monecke11">[158]</xref> and occasionally from
humans <xref ref-type="bibr" rid="pone.0017936-Luedicke1">[95]</xref>,
but MRSA from this lineage are rare. CC97-MRSA-IV has sporadically been isolated
from human patients in Australia (WA MRSA-54), Abu Dhabi <xref ref-type="bibr" rid="pone.0017936-Weber1">[31]</xref> and, as part of this study,
in Saxony. A ST97-MRSA-V has been isolated in Egypt (isolate courtesy of M.
Kamal El Din, Cairo). A further CC97-MRSA strain has recently been described
from the UK <xref ref-type="bibr" rid="pone.0017936-Ellington5">[159]</xref>; <xref ref-type="bibr" rid="pone.0017936-Ellington6">[160]</xref>, in which a SCC<italic>mec</italic> V element, ACME
and <italic>ccrA/B-4</italic> genes are detectable. A CC97-MRSA strain was
identified by the authors in swine from Germany. The strain carries a novel or
composite/hybrid SCC<italic>mec</italic> element yielding signals with probes
for <italic>mecA, ugpQ, ccrA-1, ccrB-1,</italic>“<italic>ccrAA</italic>” and <italic>ccrC</italic>. All CC97-MRSA
isolates tested are PVL-negative.</p></sec><sec id="s2t"><title>Clonal complex 121</title><p>Although CC121-MSSA are a common cause of SSTI worldwide <xref ref-type="bibr" rid="pone.0017936-Monecke7">[113]</xref>; <xref ref-type="bibr" rid="pone.0017936-Conceicao3">[142]</xref>; <xref ref-type="bibr" rid="pone.0017936-Ghebremedhin2">[153]</xref>; <xref ref-type="bibr" rid="pone.0017936-Schefold1">[161]</xref>; <xref ref-type="bibr" rid="pone.0017936-Vorobieva1">[162]</xref>, MRSA
from this lineage appear to be very rare. The authors found a single MRSA
isolate, CC121/ST577-MRSA-V (WA MRSA-22), in Australia. While PVL is common in
CC121-MSSA <xref ref-type="bibr" rid="pone.0017936-Monecke7">[113]</xref>, this isolate is PVL-negative. It harbours
<italic>etA</italic> and <italic>edinA</italic>. Further CC121-MRSA-IV have
been described from sporadic cases in the UK <xref ref-type="bibr" rid="pone.0017936-Otter2">[145]</xref>, Portugal <xref ref-type="bibr" rid="pone.0017936-Amorim1">[163]</xref>, Poland
(<ext-link ext-link-type="uri" xlink:href="http://www.isssi2008.com/abstract/13.asp">http://www.isssi2008.com/abstract/13.asp</ext-link>), China (see MLST
database, quoted in <xref ref-type="bibr" rid="pone.0017936-Amorim1">[163]</xref>) and the USA <xref ref-type="bibr" rid="pone.0017936-Pan1">[164]</xref>. A PVL-positive CC121-MRSA-V
strain was identified recently in two unrelated paediatric patients from
Cambodia <xref ref-type="bibr" rid="pone.0017936-Chheng1">[165]</xref>.</p></sec><sec id="s2u"><title>Clonal complex 152</title><p>CC152-MRSA-V has been found sporadically in Germany <xref ref-type="bibr" rid="pone.0017936-Monecke3">[80]</xref>, Sweden <xref ref-type="bibr" rid="pone.0017936-Berglund2">[166]</xref>,
Switzerland <xref ref-type="bibr" rid="pone.0017936-Francois1">[62]</xref> and Australia (WA MRSA-89). Some patients infected
with this strain had ties to Balkan countries (Macedonia, Kosovo <xref ref-type="bibr" rid="pone.0017936-Francois1">[62]</xref>; <xref ref-type="bibr" rid="pone.0017936-Monecke3">[80]</xref>) which
might indicate a wider distribution in that region. All isolates of this strain
carry PVL genes and <italic>edinB</italic>. Probes for
<italic>lukD+lukE</italic> as well as
<italic>hlgA+lukS-hlg+lukF-hlg</italic> yield signals only after
random amplification, which suggests the presence of hitherto unknown alleles.
Enterotoxin genes and most <italic>ssl/set</italic> genes are not
detectable.</p><p>ST377-MRSA-V has been observed in France, the Netherlands, Switzerland and
Australia <xref ref-type="bibr" rid="pone.0017936-Garnier1">[167]</xref>. It is closely related to ST152 and cannot be
distinguished using standard MLST primers. Specific <italic>gmk</italic> primers
able to distinguish ST152 from ST377 have been described by Garnier <xref ref-type="bibr" rid="pone.0017936-Garnier1">[167]</xref>. A
ST152-MRSA with a non-typeable SCC<italic>mec</italic> element has been isolated
in Denmark from a patient with a travel history to Kosovo <xref ref-type="bibr" rid="pone.0017936-Faria1">[138]</xref>.</p></sec><sec id="s2v"><title>Sequence type 154</title><p>Two ST154-MRSA isolates have been characterised in this study, both cultured from
central Asian immigrants to Western Europe <xref ref-type="bibr" rid="pone.0017936-Rossney1">[57]</xref>; <xref ref-type="bibr" rid="pone.0017936-Berglund2">[166]</xref>. The origin of these two
isolates as well as a report from Mongolia <xref ref-type="bibr" rid="pone.0017936-Orth1">[168]</xref> suggests a wide distribution
of this strain in Central Asia. One isolate harbours a typical
SCC<italic>mec</italic> IV element, while the other (courtesy of C.
Berglund, Stockholm) lacks <italic>ccrA-2</italic> and <italic>ccrB-2</italic>.
Both isolates are PVL-positive.</p></sec><sec id="s2w"><title>Clonal complex 188</title><p>According to MLST data, CC188 is related to CC1 although it differs in two
alleles (<italic>arcC-</italic>3 and <italic>gmk</italic>-8 instead of
<italic>arcC-</italic>1 and <italic>gmk</italic>-1 <xref ref-type="bibr" rid="pone.0017936-Feil1">[169]</xref>). However, CC188
hybridisation profiles are clearly distinct. Differences include the alleles of
the <italic>agr</italic> locus, <italic>clfA, clfB, ebh, ebpS, fnbA, fnbB, hsdS,
sdrC, sdrD</italic> and <italic>vwb</italic>, the presence of
<italic>cna</italic> as well as the absence of <italic>sasG, seh,
splA</italic> and <italic>Q2FXC0</italic>. Since these genes are distributed
widely across the genome, the differences to CC1 strains cannot readily be
explained by chromosomal replacement as previously observed for ST34 and ST239
<xref ref-type="bibr" rid="pone.0017936-Robinson2">[170]</xref>.
Therefore, either the positions of the genes in the genome may be different than
in the sequenced genomes, or CC188 originates from multiple recombination
events.</p><p>ST188-MRSA-IV has been found sporadically in Australia (WA MRSA-38 or -78, <xref ref-type="bibr" rid="pone.0017936-Nimmo1">[72]</xref>). Apart from
SCC<italic>mec</italic> IV, β-lactamase and <italic>aacA-aphD</italic>,
this strain may carry <italic>erm</italic>(B), <italic>tet</italic>(K) and
<italic>cat.</italic> PVL, enterotoxin genes and <italic>tst1</italic> are
not present. Other ST188-MRSA have been observed from Asian countries:
ST188-MRSA-III/<italic>spa</italic> t189 in Korea <xref ref-type="bibr" rid="pone.0017936-Peck1">[171]</xref>, PVL-negative CC188-MRSA-V
in Hong Kong, and PVL-positive ST188-MRSA-V in Malaysia <xref ref-type="bibr" rid="pone.0017936-GhaznaviRad1">[172]</xref>.</p></sec><sec id="s2x"><title>Sequence type 239</title><p>ST239 isolates belong to CC8. However, ST239 (including ST240 and ST241, which
differ only in mutations in <italic>pta</italic> or <italic>yqiL</italic> genes,
respectively) is discussed separately from CC8. The reason is the integration of
a CC30 DNA fragment of approximately 635,000 base pairs (or <italic>ca.</italic>20% of the genome, <xref ref-type="bibr" rid="pone.0017936-Robinson2">[170]</xref>; <xref ref-type="bibr" rid="pone.0017936-Holden2">[173]</xref>) into a CC8 parent strain, with the integration site
being localised around <italic>oriC</italic>. This has led to divergent MLST
profiles (<italic>arcC</italic>-2, rather than <italic>arcC</italic>-3, <xref ref-type="bibr" rid="pone.0017936-Robinson2">[170]</xref>; <xref ref-type="bibr" rid="pone.0017936-Holden2">[173]</xref>),
<italic>spa</italic> types and hybridisation profiles. Differences to other
CC8 strains include the affiliation to capsule type 5, the alleles of
<italic>aur, clfB</italic> and <italic>isaB</italic> and the presence of
<italic>cna,</italic> while other markers (such as <italic>agr</italic>group I alleles, <italic>ssl/set</italic> genes <italic>etc.</italic>) are in
accordance to CC8. Two genome sequences of ST239-MRSA-III have recently been
released (strain TW20, <xref ref-type="bibr" rid="pone.0017936-Holden2">[173]</xref> and JKD6008, <xref ref-type="bibr" rid="pone.0017936-Howden1">[174]</xref>).</p><p>ST239-MRSA-III is probably the oldest pandemic MRSA strain. It has been reported
in many European countries including Croatia <xref ref-type="bibr" rid="pone.0017936-Budimir1">[41]</xref> the Czech Republic <xref ref-type="bibr" rid="pone.0017936-Melter1">[71]</xref>; <xref ref-type="bibr" rid="pone.0017936-Melter2">[175]</xref>, Greece
(isolates courtesy of V. Gogou, Larissa), Italy <xref ref-type="bibr" rid="pone.0017936-Campanile1">[33]</xref>, Malta <xref ref-type="bibr" rid="pone.0017936-Scicluna1">[40]</xref>, Portugal
<xref ref-type="bibr" rid="pone.0017936-AiresdeSousa2">[49]</xref>; <xref ref-type="bibr" rid="pone.0017936-Smyth1">[176]</xref>, Spain <xref ref-type="bibr" rid="pone.0017936-Cuevas1">[69]</xref> and the UK. In Hungary, it
was common but it has been largely replaced by ST228-MRSA-I <xref ref-type="bibr" rid="pone.0017936-Conceicao1">[35]</xref>. In
Ireland, ST239-MRSA-III became the predominant strain in the 1980s <xref ref-type="bibr" rid="pone.0017936-Shore1">[15]</xref>, after it
was introduced into the country following the repatriation from Iraq of a trauma
patient <xref ref-type="bibr" rid="pone.0017936-Humphreys1">[177]</xref>. In Saxony, this strain is rarely isolated and has
been identified by the authors in patients with travel histories to Greece <xref ref-type="bibr" rid="pone.0017936-Monecke1">[29]</xref> or Turkey.
This strain is frequently isolated in Turkey <xref ref-type="bibr" rid="pone.0017936-Alp1">[178]</xref>, Iran <xref ref-type="bibr" rid="pone.0017936-Fatholahzadeh1">[179]</xref>, Saudi Arabia <xref ref-type="bibr" rid="pone.0017936-Cirlan1">[180]</xref>, Hong Kong
<xref ref-type="bibr" rid="pone.0017936-Ip1">[47]</xref>, mainland
China <xref ref-type="bibr" rid="pone.0017936-AiresdeSousa3">[181]</xref>; <xref ref-type="bibr" rid="pone.0017936-Chen1">[182]</xref>, Taiwan <xref ref-type="bibr" rid="pone.0017936-Takano1">[14]</xref>; <xref ref-type="bibr" rid="pone.0017936-AiresdeSousa3">[181]</xref> and Singapore <xref ref-type="bibr" rid="pone.0017936-Hsu1">[183]</xref>. In Trinidad
& Tobago <xref ref-type="bibr" rid="pone.0017936-Akpaka1">[184]</xref> it is virtually the only existent MRSA. In
Australia, it is a common cause of hospital-acquired infection in the East coast
states, and large outbreaks in the 1980s were attributable to this strain <xref ref-type="bibr" rid="pone.0017936-Coombs4">[155]</xref>.
Furthermore, ST239-MRSA-III has also been reported in Argentina <xref ref-type="bibr" rid="pone.0017936-AiresDeSousa1">[185]</xref>,
Brazil <xref ref-type="bibr" rid="pone.0017936-Teixeira1">[186]</xref>; <xref ref-type="bibr" rid="pone.0017936-Vivoni1">[187]</xref>, Chile <xref ref-type="bibr" rid="pone.0017936-AiresDeSousa1">[185]</xref>, Egypt (isolates
courtesy of M. Kamal El Din, Cairo), India <xref ref-type="bibr" rid="pone.0017936-Dsouza1">[104]</xref>, Korea <xref ref-type="bibr" rid="pone.0017936-Peck1">[171]</xref>, Malaysia
<xref ref-type="bibr" rid="pone.0017936-GhaznaviRad1">[172]</xref>, Mongolia <xref ref-type="bibr" rid="pone.0017936-Orth1">[168]</xref>, New Zealand <xref ref-type="bibr" rid="pone.0017936-Howden1">[174]</xref>, Pakistan <xref ref-type="bibr" rid="pone.0017936-Zafar1">[188]</xref>, Paraguay
<xref ref-type="bibr" rid="pone.0017936-Mayor1">[42]</xref>,
Russia <xref ref-type="bibr" rid="pone.0017936-Baranovich1">[189]</xref>, South Africa <xref ref-type="bibr" rid="pone.0017936-JansenvanRensburg1">[73]</xref>, Thailand <xref ref-type="bibr" rid="pone.0017936-Smyth1">[176]</xref> and Uruguay
<xref ref-type="bibr" rid="pone.0017936-AiresDeSousa1">[185]</xref>. The reference strain ATCC33592, recovered in a
hospital in New York <xref ref-type="bibr" rid="pone.0017936-Schaefler1">[190]</xref>, belongs also to ST239-MRSA-III.</p><p>The evolution of this strain has recently been reviewed based on genome sequences
of 63 isolates from different parts of the world analysing genome-wide
single-nucleotide polymorphisms, insertions or deletions <xref ref-type="bibr" rid="pone.0017936-Harris1">[191]</xref>. In short, ST239-MRSA-III
can be divided into three clades; a European, presumably ancestral one, an Asian
and a South-American. However, there is some evidence for secondary,
travel-associated cross-transmission <xref ref-type="bibr" rid="pone.0017936-Harris1">[191]</xref>.</p><p>ST239-MRSA-III is colloquially known as the Czech, Vienna, Hungarian, Portuguese
or Brazilian Clone, UK-EMRSA-1, -4, -7, -9 or -11, AUS-EMRSA-2 or -3, Irish
Phenotype III, Irish AR01, -09, -15 or -23, Canadian MRSA-3 (this refers to the
ST241 SLV, <xref ref-type="bibr" rid="pone.0017936-Christianson1">[28]</xref>) or as Canadian MRSA-6 <xref ref-type="bibr" rid="pone.0017936-Christianson1">[28]</xref>. However, all these
designations should be regarded as synonyms as their distinction is not always
clear-cut. For instance, the Hungarian Clone was described as harbouring
SCC<italic>mec</italic> III, while the Brazilian Clone carries
SCC<italic>mec</italic> IIIA <xref ref-type="bibr" rid="pone.0017936-Vandenesch1">[192]</xref>. The difference is
only the presence (III) or absence (IIIA) of an integrated plasmid
p<italic>T181</italic>, which encompasses, among other genes,
<italic>tet</italic>(K). Since the SCC<italic>mec</italic>-associated
mercury resistance operon and other resistance and enterotoxin genes vary
independently of p<italic>T181</italic>/<italic>tet</italic>(K) among these
clones and since <italic>tet</italic>(K) might also be part of free plasmids,
<italic>tet</italic>(K) could be regarded just as one mobile element among
many others. Beyond the issue of <italic>tet</italic>(K), there are also other
variations of the SCC<italic>mec</italic> III element. About two thirds of
tested isolates harbour the mercury resistance operon. It is often, but not
always, accompanied by
“<italic>ccrAA</italic>”<italic>+ccrC.</italic> This
indicates a linkage of SCC<italic>mec</italic> III to SCC<italic>mer</italic><xref ref-type="bibr" rid="pone.0017936-Ito1">[4]</xref>. Some
isolates do not yield signals with a probe which normally reacts in both,
<italic>mecR1</italic> and <italic>ΔmecR1</italic>; this could probably
be attributed to another partial deletion of the <italic>mecR1</italic> gene. In
one case, the authors found the absence of <italic>mecI, mecR1</italic> and
<italic>xylR.</italic> Variable resistance genes in ST239-MRSA-III include
<italic>erm</italic>(A), <italic>erm</italic>(C), <italic>aacA-aphD, aadD,
aphA3, sat, dfrA, mupA, tet</italic>(K), different alleles of
<italic>cat</italic>, <italic>qacA</italic> and <italic>qacC.</italic> PVL
has not been detected in ST239-MRSA-III. Enterotoxin genes <italic>sea,
sek</italic> and <italic>seq</italic> as well as phage-associated genes
<italic>sak, scn</italic> and <italic>chp</italic> are variable. The ACME
locus is present in a minority of isolates (<xref ref-type="bibr" rid="pone.0017936-GhaznaviRad1">[172]</xref>, and in three out of
some 200 tested by the authors).</p></sec><sec id="s2y"><title>Clonal complex 361</title><p>The authors observed three different CC361-MRSA strains. All are PVL-negative.
CC361-MRSA-IV is detected sporadically in Western Australia (ST672-MRSA-IV or WA
MRSA-29, <xref ref-type="bibr" rid="pone.0017936-Nimmo1">[72]</xref>)
and one isolate originated from Ireland. CC361-MRSA-V was isolated in Abu Dhabi
where it appears to be rare <xref ref-type="bibr" rid="pone.0017936-Weber1">[31]</xref>. A CC361-MRSA-VIII was found in Australia where it is
referred to as WA MRSA-28 <xref ref-type="bibr" rid="pone.0017936-Nimmo1">[72]</xref>. Isolates harbour the enterotoxin gene locus
<italic>egc,</italic> which, however, might be partially deleted. One out of
three tested WA MRSA-29 isolates carries <italic>tst1</italic> and
<italic>seb</italic>, which is a highly unusual combination of virulence
genes <xref ref-type="bibr" rid="pone.0017936-Novick1">[193]</xref>.</p></sec><sec id="s2z"><title>Clonal complex 398</title><p>CC398-MRSA has recently received a lot of attention as strains from this lineage
are of animal origin but are able to cause disease in humans. This has led to
intense investigations including the sequencing of a complete genome of a
ST398-MRSA-V strain, S0385, from the Netherlands <xref ref-type="bibr" rid="pone.0017936-Schijffelen1">[194]</xref>.</p><p>ST398-MRSA-III, <italic>spa</italic> type t567, has been observed in Belgium
<xref ref-type="bibr" rid="pone.0017936-Nemati1">[13]</xref>.
ST398-MRSA-IV isolates appear to be a rare livestock-associated MRSA (LA-MRSA)
strain. Two infections of humans were observed in Hong-Kong <xref ref-type="bibr" rid="pone.0017936-Ip1">[47]</xref> and isolates
from poultry have been reported from Belgium <xref ref-type="bibr" rid="pone.0017936-Nemati1">[13]</xref>. In Germany, this strain
has been detected in cattle <xref ref-type="bibr" rid="pone.0017936-Fessler1">[195]</xref> and in turkeys (courtesy of S. Cortez de
Jäckel, Delbrück), and by the authors in turkey meat samples. Isolates
are negative for exotoxin genes and for <italic>sak, scn</italic> and
<italic>chp.</italic></p><p>PVL-negative ST398-MRSA-V is frequently found in association with livestock,
although this strain is also increasingly isolated from human patients without
animal contact. It was first discovered in a family outbreak in the Netherlands
in 2006. Family members were farmers, and the strain was subsequently found in
pigs from the same farm. Further investigations showed its presence in a high
proportion of Dutch pigs as well as in farm personnel, veterinarians and
students <xref ref-type="bibr" rid="pone.0017936-Huijsdens1">[196]</xref>-<xref ref-type="bibr" rid="pone.0017936-deNeeling1">[200]</xref>. Recently, this strain has been observed not only in
pigs, but in humans, cattle <xref ref-type="bibr" rid="pone.0017936-Monecke11">[158]</xref>; <xref ref-type="bibr" rid="pone.0017936-Fessler1">[195]</xref>, horses <xref ref-type="bibr" rid="pone.0017936-Walther1">[75]</xref>, dogs <xref ref-type="bibr" rid="pone.0017936-Nienhoff1">[201]</xref>, poultry
<xref ref-type="bibr" rid="pone.0017936-Nemati1">[13]</xref>,
chickens and turkeys (courtesy of S. Cortez de Jäckel, Delbrück and of
the Federal Institute for Risk Assessment, Berlin). It was also found in retail
meat of different domestic animals <xref ref-type="bibr" rid="pone.0017936-Lozano1">[202]</xref>; <xref ref-type="bibr" rid="pone.0017936-deBoer1">[203]</xref>. In addition to the
Netherlands, ST398-MRSA-V has been identified in Germany, Belgium, Italy,
Austria, Spain <xref ref-type="bibr" rid="pone.0017936-Nemati1">[13]</xref>; <xref ref-type="bibr" rid="pone.0017936-Battisti1">[90]</xref>; <xref ref-type="bibr" rid="pone.0017936-Lozano1">[202]</xref>; <xref ref-type="bibr" rid="pone.0017936-Soavi1">[204]</xref>-<xref ref-type="bibr" rid="pone.0017936-Potel1">[208]</xref> Canada (<ext-link ext-link-type="uri" xlink:href="http://promedmail.oracle.com/pls/otn/f?p=2400:1001:8447806422203976::NO::F2400_P1001_BACK_PAGE,F2400_P1001_PUB_MAIL_ID:1010,81749">http://promedmail.oracle.com/pls/otn/f?p=2400:1001:8447806422203976::NO::F2400_P1001_BACK_PAGE,F2400_P1001_PUB_MAIL_ID:1010,81749</ext-link>),
the USA <xref ref-type="bibr" rid="pone.0017936-Smith1">[209]</xref>and Australia (author's unpublished observation). This strain shows a
remarkable diversity with regard to resistance genes. Isolates carry
SCC<italic>mec</italic> V, or rather SCC<italic>mec</italic> V<sub>T</sub>,
as indicated by the genome sequence of strain S0385 <xref ref-type="bibr" rid="pone.0017936-Schijffelen1">[194]</xref>. Rarely, recombinase
genes “<italic>ccrAA</italic>” and <italic>ccrC</italic> may be
absent. Essentially all isolates harbour the β-lactamase operon and
<italic>tet</italic>(M). Additionally, <italic>tet</italic>(K) is frequently
detected. The multidrug resistance gene <italic>cfr</italic> has recently been
observed in ST398-MRSA-V <xref ref-type="bibr" rid="pone.0017936-Kehrenberg1">[19]</xref>. In addition to the resistance markers detected by
array hybridisation (<xref ref-type="fig" rid="pone-0017936-g002">Figure
2</xref>), <italic>tet</italic>(L), <italic>dfrK</italic> and
<italic>dfrG</italic> can be found by PCR in some isolates <xref ref-type="bibr" rid="pone.0017936-Kadlec1">[210]</xref>–<xref ref-type="bibr" rid="pone.0017936-Kadlec2">[212]</xref>. Recently, the novel
trimethoprim resistance gene <italic>dfrK</italic><xref ref-type="bibr" rid="pone.0017936-Kadlec1">[210]</xref>, the
macrolide-lincosamide-streptogramin B resistance gene <italic>erm</italic>(T)
<xref ref-type="bibr" rid="pone.0017936-Kadlec2">[212]</xref>, a
ABC transporter gene <italic>vga</italic>(C) for streptgramin
A-lincosamide-pleuromutilin resistance (<xref ref-type="bibr" rid="pone.0017936-Kadlec3">[213]</xref>) and the novel apramycin
resistance gene <italic>apmA</italic><xref ref-type="bibr" rid="pone.0017936-Fessler2">[214]</xref> have
been described on plasmids from this strain. Many isolates of ST398-MRSA-V
harbour multiple resistance genes which provide the same resistance phenotypes
(<italic>tet</italic>(K)<italic>+tet</italic>(M),
<italic>tet</italic>(L)<italic>+tet</italic>(M) or
<italic>tet</italic>(K)<italic>+tet</italic>(L)<italic>+tet</italic>(M);
<italic>erm</italic>(A)<italic>+erm</italic>(C) or
<italic>erm</italic>(A)<italic>+erm</italic>(B)). The vast majority of
ST398-MRSA-V isolates are negative for enterotoxin genes. Among 54 swine
isolates from Germany, <italic>seb</italic> was detected only once, and
<italic>sek+seq</italic> were detected in three isolates <xref ref-type="bibr" rid="pone.0017936-Kadlec4">[215]</xref>. The genes
<italic>sak, scn</italic> and <italic>chp</italic> were absent from isolates
of the European LA-MRSA strain. However, these genes where detected by the
authors in two human isolates from Hong Kong; one of which harbours
<italic>sea</italic>.</p><p>PVL-positive ST398-MRSA-V has been described in China <xref ref-type="bibr" rid="pone.0017936-Yu1">[216]</xref>, and in children of Asian
origin living in Sweden <xref ref-type="bibr" rid="pone.0017936-WelinderOlsson1">[217]</xref>. Two isolates (courtesy of C. Welinder-Olsson,
Gothenburg, Sweden) have been genotyped. In contrast to the livestock-associated
ST398-MRSA-V isolates, they carry <italic>sak, scn</italic> and
<italic>chp.</italic> One isolate harbours also <italic>sea</italic>.</p></sec><sec id="s2aa"><title>Sequence type 426</title><p>ST426-MRSA-IV has recently been described from the Arkhangelsk region in Russia
<xref ref-type="bibr" rid="pone.0017936-Vorobieva1">[162]</xref>.
The authors did not isolate ST426-MRSA within the present study, but genotyping
data of ST426-MSSA isolates <xref ref-type="bibr" rid="pone.0017936-Monecke5">[94]</xref>; <xref ref-type="bibr" rid="pone.0017936-Luedicke1">[95]</xref>; <xref ref-type="bibr" rid="pone.0017936-Monecke7">[113]</xref> allow the general features of that sequence type to
be described. ST426-MSSA isolates harbour <italic>tst1, sea</italic> and ORF
CM14 as well as, variably <italic>sec+sel, see</italic> and/or
<italic>sek+seq</italic>. The gene <italic>cna</italic> can be detected
in most isolates. Notably, <italic>nuc</italic> (encoding thermostable nuclease,
DNAse) is not detectable by hybridisation. Since ST426 isolates are
phenotypically DNAse-positive, the presence of a variant <italic>nuc</italic>allele can be assumed.</p></sec><sec id="s2ab"><title>Clonal complex 509</title><p>CC509 appears to be a very rare CC <xref ref-type="bibr" rid="pone.0017936-Monecke5">[94]</xref>; <xref ref-type="bibr" rid="pone.0017936-Munckhof2">[218]</xref>, but MRSA belonging to
it have previously been observed in Queensland, Australia <xref ref-type="bibr" rid="pone.0017936-Munckhof2">[218]</xref>. One isolate of
CC509/ST207-MRSA-V from New South Wales, Australia was genotyped. It is
PVL-negative. The <italic>egc</italic> locus appears to be present in a variant
or truncated form with only genes <italic>sem</italic> and <italic>seo</italic>being detectable.</p></sec><sec id="s2ac"><title>Sequence types 573 and 772</title><p>Sequence types 573 and 772 belong, according to the MLST database, to CC1.
However, with respect to the <italic>pta</italic> allele these strains differ
from other CC1 (<italic>pta</italic>-12 or <italic>pta</italic>-22,
respectively). Their hybridisation profile is also distinct, which may be
attributed to one or multiple recombination events that have introduced genes
from other CCs into CC1. This includes <italic>agr</italic> (group II rather
than III), genes encoding the capsule type (5 rather than 8), the
<italic>egc</italic> enterotoxin gene cluster, and the enterotoxin homologue
ORF CM14. The enterotoxin H gene <italic>seh</italic>, which is otherwise
typical for CC1 strains, cannot be detected in ST573/772. The genes
<italic>cna</italic> and <italic>sasG</italic> are present. Protease genes
<italic>splA, splB</italic> and <italic>splE</italic> are absent.</p><p>A PVL-negative ST573-MRSA-V strain has been described from Australia (WA MRSA-10,
<xref ref-type="bibr" rid="pone.0017936-Nimmo1">[72]</xref>).</p><p>PVL-positive ST772-MRSA-V, which is known as WA MRSA-60 or the Bengal Bay Clone
<xref ref-type="bibr" rid="pone.0017936-Ellington2">[111]</xref>,
is relatively multi-resistant compared to other CA-MRSA. In addition to a
SCC<italic>mec</italic> V (specifically, a V<sub>T</sub><xref ref-type="bibr" rid="pone.0017936-Ellington3">[127]</xref>)
element, they carry variably <italic>blaZ</italic>, <italic>erm</italic>(C),
<italic>msr</italic>(A), <italic>mph</italic>(C), <italic>aacA-aphD, aphA3,
sat</italic> and <italic>tet</italic>(K). Besides the PVL genes, all
isolates tested harbour <italic>sea</italic>, and most carry
<italic>sec</italic> and <italic>sel.</italic> This strain was found by the
authors in Australia, Germany, the UK, Hong Kong and Abu Dhabi. German and
British patients usually had a travel history or family background suggesting an
infection in India or Bangladesh (<xref ref-type="bibr" rid="pone.0017936-Ellington2">[111]</xref>, H.J. Linde,
Regensburg, Germany, pers. communication, and own observations) where it appears
to be increasingly common <xref ref-type="bibr" rid="pone.0017936-Dsouza1">[104]</xref>.</p></sec><sec id="s2ad"><title>Sequence type 779</title><p>ST799-MRSA has been found sporadically by the authors in the UK, Ireland, France
and Australia. Isolates harbour a C2 <italic>mec</italic> gene complex
(<italic>mecA, ugpQ</italic>) but carriage of <italic>ccr</italic> genes
varies (“<italic>ccrAA</italic>”<italic>+ccrC</italic> or
“<italic>ccrAA</italic>”<italic>+ccrA/B4</italic>, or no
detectable recombinases). Q6GD50 is detectable, possibly indicating a
combination of SCC<italic>mec</italic> and SCC<italic>fus</italic> elements.
ST779-MRSA are PVL-negative, but carry <italic>etD</italic> and
<italic>edinB.</italic></p></sec><sec id="s2ae"><title>Sequence type 834</title><p>According to the MLST database, ST834 belongs to CC9. However, microarray
hybridisation profiles differ from other CC9 strains in several key features
such as <italic>agr</italic> allele (<italic>agr</italic> group I rather than
II), capsule type (8 rather than 5), <italic>spa</italic> type, presence of
<italic>sasG</italic> and alleles of some MSCRAMM genes (<italic>bbp, map,
vwb</italic>). ST834-MRSA-IV occurs rarely in Australia, where it has been
described as WA MRSA-13. The tested isolates harbour <italic>tst1, sec</italic>and <italic>sel</italic>, but lack PVL genes. PVL-negative ST834-MRSA-IV also
has been observed in Cambodia <xref ref-type="bibr" rid="pone.0017936-Chheng1">[165]</xref>.</p></sec><sec id="s2af"><title>Clonal complex 913</title><p>A single isolate of a ST913-MRSA-IV was identified by the authors from a Lebanese
refugee in Germany who suffered from haemorrhagic bronchitis. It is positive for
two genes encoding exfoliative toxins (<italic>etA</italic> and
<italic>etD</italic>) as well as for <italic>edinB</italic>. It lacks
enterotoxins and PVL. A recent paper <xref ref-type="bibr" rid="pone.0017936-Adler1">[39]</xref> on MRSA isolates from the
Negev region of Israel suggests a wider distribution of this strain in the
Middle East as well as the presence of closely related ST912 and ST914.</p></sec><sec id="s2ag"><title>Sequence type 1048</title><p>This sequence type has only been reported in Hong Kong where it was sporadically
isolated in nursing homes <xref ref-type="bibr" rid="pone.0017936-Ho1">[125]</xref>. The authors found a single isolate from Hong Kong.
ST1048 is related to CC7, but differs in some markers including the presence of
<italic>sasG</italic> and <italic>cna</italic>, and the alleles of
<italic>arcC</italic> and <italic>spa.</italic> It has <italic>spa</italic>type t1081, which can also be observed in CC45 and ST1774. The tested isolate
carries SCC<italic>mec</italic> IV, <italic>ccrC,</italic> and ACME. It is
negative for PVL and enterotoxin genes, but a previous study <xref ref-type="bibr" rid="pone.0017936-Ho1">[125]</xref> indicated the
presence of <italic>egc</italic> genes <italic>seg</italic> and
<italic>sei</italic> in some isolates of this ST.</p></sec><sec id="s2ah"><title>Sequence type 1774</title><p>This strain was isolated from several patients in Hong Kong and has not been
described previously. It shares <italic>spa</italic> type t1081 with other
clones (CC45 and ST1048, see <xref ref-type="bibr" rid="pone.0017936-Ho1">[125]</xref>). Isolates carry SCC<italic>mec</italic> IV,
<italic>ccrC,</italic> and ACME. PVL and enterotoxin genes cannot be
detected. Variable resistance markers include the β-lactamase operon and
<italic>qacC</italic>.</p></sec></sec><sec id="s3"><title>Discussion</title><sec id="s3a"><title>Strain definition and nomenclature</title><p>Genes of the “core genome” and the “core variable genome”
<xref ref-type="bibr" rid="pone.0017936-Lindsay1">[219]</xref>yield essentially the same phylogenetic information as the seven housekeeping
genes used for MLST. Consequently, a MLST clonal complex can be identified by
microarray hybridisation based on a characteristic fingerprint pattern <xref ref-type="bibr" rid="pone.0017936-Monecke6">[96]</xref>, provided
that a hybridisation pattern for this CC has been defined previously. For CC
assignment, the presence or absence of <italic>sasG, cna, fosB</italic>,
<italic>lukD+lukE</italic>, <italic>egc</italic>, <italic>seh</italic>,
ORF CM14 as well as the identification of the actual allelic variant of genes of
the <italic>agr, ssl/set</italic>, <italic>hysA</italic>, <italic>hsdS,</italic>and capsule loci and of genes encoding MSCRAMMs, proteases and a leukocidin
homologue (“<italic>lukY</italic>”) are used <xref ref-type="bibr" rid="pone.0017936-Monecke6">[96]</xref>. Whilst clonal complex
affiliation can be easily determined, the assignment to “strains” is
not that straightforward. The concept of the “strain” can be
beneficial for infection control purposes and subsequently, a wide variety of
different epidemic or pandemic MRSA strains have been described. Unfortunately,
different criteria and different methods have been applied for defining and
naming MRSA strains. This has resulted in a confusing situation with several
strains having multiple designations. For instance, ST5-MRSA-II is known as the
Rhine-Hesse Epidemic Strain in Germany, UK-EMRSA-3 in the UK, USA100 in the USA,
CMRSA-2 in Canada, AR07.3, AR07.4 or AR11 in Ireland, and New York-Japan Clone
in Australia and elsewhere. For this reason, Enright <italic>et al</italic>.
<xref ref-type="bibr" rid="pone.0017936-Enright2">[220]</xref>proposed to designate strains by “sequence
type-MRSA-SCC<italic>mec</italic> type” such as
“ST5-MRSA-II”. We largely followed this principle. However, this
nomenclature has shortcomings if clearly different strains have the same ST and
SCC<italic>mec</italic> type (such as the various ST8-MRSA-IV). Additional
information, such as PVL status or carriage of superantigens, is of relevance in
defining the “pathotype” of the organism, which is important for
clinical management purposes. Thus, PVL-positive and PVL-negative strains of the
same ST and SCC<italic>mec</italic> affiliation are treated separately here, as
their clinical significance may be different.</p><p>Another challenge, beyond the definition of individual strains, is that the
concept of a “strain” in itself cannot properly be defined.
Traditionally a strain has been defined as “an isolate or group of
isolates that can be distinguished from other isolates of the same genus and
species by phenotypic characteristics or genotypic characteristics or
both” <xref ref-type="bibr" rid="pone.0017936-Tenover1">[221]</xref>; <xref ref-type="bibr" rid="pone.0017936-Dijkshoorn1">[222]</xref>, which is essentially
the same as a clone which is defined as a group of “isolates that are
indistinguishable from each other by a variety of genetic tests” <xref ref-type="bibr" rid="pone.0017936-Tenover1">[221]</xref>; <xref ref-type="bibr" rid="pone.0017936-Dijkshoorn1">[222]</xref>. Thus,
the definition of a clone or strain depends on the discriminatory power of the
test and/or on the number of different tests applied. Isolates which appear to
be indistinguishable by, <italic>e.g.</italic>, PFGE might yield differences
detectable by microarray hybridisation or genome sequencing. In the case of
<italic>S. aureus</italic>, all previously defined strains can be subdivided
into a considerable number of variants as they harbour variable genes in
different combinations <xref ref-type="bibr" rid="pone.0017936-Monecke1">[29]</xref>; <xref ref-type="bibr" rid="pone.0017936-Monecke2">[43]</xref>; <xref ref-type="bibr" rid="pone.0017936-Monecke4">[82]</xref>. Of course, it is not practical to regard all these
variants as “strains” and to invent and to use different names for,
<italic>e.g</italic>. the variants of ST22-MRSA-IV which just differ in
carriage of <italic>erm</italic>(C) or <italic>sec+sel.</italic> However,
UK-EMRSA-2 and UK-EMRSA-6 (both CC8-MRSA-IV) are regarded as different
“strains” although they differ only in the presence of
<italic>aphA3</italic> and <italic>sat</italic>, neither of which are
particularly important from a clinical perspective. Similarly, Vienna and
Hungarian epidemic strains differ basically in the presence of
<italic>tet</italic>(K). On the other hand, isolates which are known as the
Hannover Epidemic Strain could easily be divided into two “strains”
based on their different SCC<italic>mec</italic> elements. In fact, a
“strain” may be of polyphyletic origin. MSSA from different branches
of one clonal group may have acquired the same SCC<italic>mec</italic> element
independently on several occasions. This has previously been proposed in the
case of ST5-MRSA-II <xref ref-type="bibr" rid="pone.0017936-Nubel1">[46]</xref>. These few examples emphasise the fact that the
concept of “strains”, although convenient and practical, is in fact
a rather arbitrary approach of forcing taxonomy on permanently changing and
evolving biological subjects. When scrutinised by methods such as genome
sequencing or microarray hybridisation, “strains” are not static
blocks comprised of identical isolates, but rather consist of groups of isolates
with similar sequences. These sequences might differ in single point mutations
(as sometimes obvious in MLST, <italic>e.g</italic>., Taiwan Clone isolates may
have different <italic>gmk</italic> alleles), in the composition and sequence of
single loci (such as the variable part of the <italic>spa</italic> gene or the
<italic>dru</italic> region within the SCC<italic>mec</italic> element) or
in the presence or absence of complete genes or multi-gene mobile elements.
Thus, the concept of “quasispecies” <xref ref-type="bibr" rid="pone.0017936-Eigen1">[223]</xref>-<xref ref-type="bibr" rid="pone.0017936-Steinhauer1">[227]</xref> could be applied in
which the genome “cannot be described as a defined structure, but rather
as a weighted average of a large number of individual sequences” <xref ref-type="bibr" rid="pone.0017936-Domingo1">[228]</xref>. The
difference between <italic>S. aureus</italic> and the RNA-viruses (to which this
concept has been applied first <xref ref-type="bibr" rid="pone.0017936-Domingo1">[228]</xref>), is basically the time frame in which variations
evolve. Conveniently, the extent and time frame of variability in <italic>S.
aureus</italic> provide ample opportunities for typing,
<italic>i.e.,</italic> for outbreak investigations and infection control
purposes.</p></sec><sec id="s3b"><title>Biodiversity of MRSA and SCC<italic>mec</italic> elements</title><p>For more than three decades, MRSA was mainly an issue of hospital hygiene and
infection prevention and control. Interestingly, the “older”
SCC<italic>mec</italic> elements found in HA-MRSA strains have largely been
observed in and restricted to a few genotypes, mainly to CC5 and CC8. CC5 and
CC8 harbour the widest diversity of SCC<italic>mec</italic> elements, and some
of the most recently described types have only been found in these CCs (<xref ref-type="fig" rid="pone-0017936-g005">Figure 5</xref>). This is not related
to their overall abundance, <italic>i.e</italic>., to the statistical
probability of a gene transfer event. In contrast, MRSA from the equally
abundant CC15 <xref ref-type="bibr" rid="pone.0017936-Monecke5">[94]</xref> has only been described once, some 30 years ago <xref ref-type="bibr" rid="pone.0017936-Campanile1">[33]</xref>. Thus,
SCC<italic>mec</italic> elements from other species may be more readily
integrated into CC5 and CC8 than into other <italic>S. aureus</italic> lineages.
These two CCs might serve as some kind of “entry gate” of
SCC<italic>mec</italic> elements into the <italic>S. aureus</italic> gene
pool from which, possibly after some adaptations, these elements can be
transferred into other <italic>S. aureus</italic> lineages. The reason for this
is unclear, but peculiarities of, <italic>e.g</italic>., lineage-specific
restriction-modification systems which can control horizontal gene transfer into
<italic>S. aureus</italic> and between different <italic>S. aureus</italic>could be scrutinised with in this regard.</p><fig id="pone-0017936-g005" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0017936.g005</object-id><label>Figure 5</label><caption><title>Network graph based on hybridisation profiles, visualising
similarities and relationships between clonal complexes and the spread
of SCC<italic>mec</italic> elements.</title><p>Roman numerals indicate SCC<italic>mec</italic> types; PVL-negative
strains are shown with black letters on white background, PVL-positive
in white letters on black. A, ACME; F, SCC<italic>fus</italic>; M,
SCC<italic>mer</italic>; IRR, irregular SCC<italic>mec</italic>elements; COM, composite or multiple SCC<italic>mec</italic>elements.</p></caption><graphic xlink:href="pone.0017936.g005"></graphic></fig><p>The epidemiology of MRSA has changed over the last two decades with the rise of
CA- and LA-MRSA harbouring a previously unknown variety of
SCC<italic>mec</italic> elements. It is tempting to speculate that the rise
of new strains was not only paralleled, but triggered by the emergence of these
elements, especially of SCC<italic>mec</italic> IV. Compared to other
SCC<italic>mec</italic> elements, SCC<italic>mec</italic> IV can be found in
a wide diversity of different <italic>S. aureus</italic> clonal lineages (<xref ref-type="fig" rid="pone-0017936-g005">Figure 5</xref>). Interestingly, it
is also the most common SCC<italic>mec</italic> element in <italic>S.
epidermidis.</italic> It has been detected in approximately 40% of
methicillin-resistant <italic>S. epidermidis</italic> from humans, which
belonged to wide variety of genetic backgrounds <xref ref-type="bibr" rid="pone.0017936-Miragaia1">[229]</xref>; and it is also common
among coagulase-negative staphylococci from animals <xref ref-type="bibr" rid="pone.0017936-Fessler3">[230]</xref>. The evolutionary success
of this element might suggest either a better ability to be transmitted between
different strains, and even species, and/or lower fitness costs <xref ref-type="bibr" rid="pone.0017936-Lee1">[7]</xref>; <xref ref-type="bibr" rid="pone.0017936-Ender1">[8]</xref>. Recently, a
variety of “atypical” SCC<italic>mec</italic> elements have been
observed, some of which are described in this study. Whether they are variants
of previously known types or entirely new elements still needs to be determined.
However, these observations indicate that the spread and evolution of
SCC<italic>mec</italic> elements is still ongoing. This prompts the question
of where novel elements originated from. Apparently, these elements evolve
independently of the <italic>S. aureus</italic> genome they actually reside in.
Different SCC<italic>mec</italic> elements may be observed in otherwise
virtually identical strains, and strains from completely different clonal
complexes may acquire the same SCC<italic>mec</italic> elements. Similar to
other mobile genetic elements they could be considered as “selfish
genes” <xref ref-type="bibr" rid="pone.0017936-Dawkins1">[231]</xref>, <italic>i.e.</italic>, as parasitic pieces of
genetic information which undergo their own evolution and compete against each
other, as previously discussed by Novick (“Mobile genetic elements are
arguably selfish in that their evolution is driven by selective forces that
operate on the elements themselves, independently of the host organisms within
which they must of necessity reside” <xref ref-type="bibr" rid="pone.0017936-Novick1">[193]</xref>). However, contrary to
other “selfish” mobile genes (such as endogenous retroviruses in
eukaryotic genomes) they confer an advantage to their “host
organism” by introducing antibiotic resistance properties and even
additional virulence factors such as a recently discovered phenol-soluble
modulin <xref ref-type="bibr" rid="pone.0017936-Queck1">[232]</xref>.
The relative independence of such elements from host genomes also allows them to
reside in other species, and, indeed, a wide range of SCC<italic>mec</italic>elements can be found in other staphylococci <xref ref-type="bibr" rid="pone.0017936-Miragaia1">[229]</xref>. These bacteria provide
an ample pool of additional hosts for the SCC<italic>mec</italic> elements, and
it can be expected that novel elements may be transferred from other
staphylococci to <italic>S. aureus</italic>. For that reason, the evolution of
antibiotic resistance in bacteria infecting/colonising livestock is highly
relevant. Many animal species harbour <italic>S. aureus</italic> as well as
their own host-specific staphylococci (such as <italic>S. hyicus</italic> in
swine or <italic>S. pseudintermedius</italic> in dogs). Global livestock
populations now exceed the populations of most wild animals which might serve as
hosts for <italic>S. aureus</italic>. For example, there are 1,300 million
cattle, 900 million pigs, 500 million cats and 400 million dogs in the world
[<ext-link ext-link-type="uri" xlink:href="http://www.cattle-today.com/">http://www.cattle-today.com/</ext-link>, <ext-link ext-link-type="uri" xlink:href="http://en.wikipedia.org">http://en.wikipedia.org</ext-link>]. Because of their close proximity to
humans, domestic animals might serve as reservoir for new strains as well as for
novel SCC<italic>mec</italic> elements. While some animal-specific <italic>S.
aureus</italic> such as ST151 have so far failed to evolve into MRSA or to
infect humans, others have truly zoonotic potential with the best documented
example being ST398-MRSA-V.</p></sec><sec id="s3c"><title>The role of Panton-Valentine leukocidin</title><p>Although PVL has been known for a long time <xref ref-type="bibr" rid="pone.0017936-Panton1">[10]</xref>; <xref ref-type="bibr" rid="pone.0017936-VandeVelde1">[233]</xref>, its occurrence in
MRSA strains is a recent phenomenon. Since PVL is phage-encoded, it can be found
in <italic>S. aureus</italic> belonging to many different clonal complexes.
Occurrence in diverse MSSA has been discussed previously <xref ref-type="bibr" rid="pone.0017936-Monecke7">[113]</xref>. PVL-positive MRSA are
found in clonal complexes or sequence types CC1, CC5, CC8, CC22, CC30, CC59,
ST72, CC80, CC88, ST93, ST154, ST398 and ST772 (<xref ref-type="fig" rid="pone-0017936-g005">Figure 5</xref>). Additionally, PVL-positive
ST45-MRSA have recently been reported <xref ref-type="bibr" rid="pone.0017936-Deurenberg1">[45]</xref>; <xref ref-type="bibr" rid="pone.0017936-Layer1">[122]</xref>. As with
SCC<italic>mec</italic> elements, PVL phages undergo a host-independent
evolution. As a set of “selfish genes” they evolved to confer a
selective advantage to their staphylococcal hosts in helping them to cope with
the immune defences of the vertebrates in which these staphylococci parasitize.
Thus, these phages compensate their staphylococcal host for the fitness costs
they may cause. This strategy appears to be evolutionary successful as it
evolved on multiple occasions. Staphylokinase-encoding phages in <italic>S.
aureus</italic> can be regarded as another example. Staphylokinase improves
the fitness of <italic>S. aureus</italic> in the human host by facilitating
their entry into deeper host tissues and by inhibiting host defensins <xref ref-type="bibr" rid="pone.0017936-Bokarewa1">[234]</xref>.
SCC<italic>mec</italic> elements also “pay” for being
transmitted and multiplied by helping their staphylococcal hosts to cope with
antibiotic compounds, which in a certain sense also belong to the defences of
the human host against staphylococcal infection.</p><p>Some of the recently emerged PVL-positive MRSA strains are known to occur and
predominate in certain regions such as USA300 in the USA, ST80-MRSA-IV in Europe
and the Middle East, ST772-MRSA-V in India, ST59-MRSA-V<sub>T</sub> in Taiwan
and ST93-MRSA-IV in Australia. Cases outside these regions are increasingly
being reported. In part, this can be attributed to human travel activities.
Other PVL-positive strains have been found in multiple distant settings
(<italic>e.g.</italic>, ST22-MRSA-IV in Bavaria, Germany, in Australian
patients of Indian origin, in Abu Dhabi and in Great Britain) which might
suggest a polyphyletic origin (see also <xref ref-type="bibr" rid="pone.0017936-Scicluna1">[40]</xref>). Crudely, three
different epidemiological situations can be distinguished. First, in European
countries (such as Germany, <xref ref-type="bibr" rid="pone.0017936-Monecke1">[29]</xref>; ; the UK, <xref ref-type="bibr" rid="pone.0017936-Ellington2">[111]</xref>; Malta, <xref ref-type="bibr" rid="pone.0017936-Scicluna1">[40]</xref> or
Ireland, <xref ref-type="bibr" rid="pone.0017936-Rossney1">[57]</xref>; <xref ref-type="bibr" rid="pone.0017936-Rossney4">[235]</xref>), the prevalence of PVL-MRSA is low and has remained
low for several years. In these countries, a variety of different strains can be
observed and individual cases can often be traced to travel histories or to the
foreign origin of patients. Thus, detection of such strains in travellers might
indicate an epidemic situation elsewhere, and should prompt a thorough
documentation of the patient's travel history. It may be speculated that an
overwhelming presence of successful PVL-negative clones (ST22-MRSA-IV and
ST398-MRSA-V) may hinder the dissemination of PVL-positive clones. However,
there are no data indicating whether these strains would prevail in direct
competition with a successful PVL-MRSA-clone, and generally it is not known
which properties might render a strain “successful”. Secondly, in
Australia or Abu Dhabi <xref ref-type="bibr" rid="pone.0017936-Weber1">[31]</xref> PVL-MRSA are common and a number of different strains
co-exist. Since Australia as well as the Gulf Emirates witnessed a recent and
massive immigration of people from all over the world, it can be assumed that
these people have introduced epidemic strains from their respective home
countries. For instance, USA300 may have come with North American expatriates,
or ST772-MRSA-V from India <xref ref-type="bibr" rid="pone.0017936-Ellington2">[111]</xref>. Thirdly, another situation emerged in the USA,
where a single strain of PVL-MRSA (USA300) spread extensively and where this one
strain effectively marginalised all other strains, whether PVL-positive or not
<xref ref-type="bibr" rid="pone.0017936-Moran1">[76]</xref>.
Similarly, in Taiwan, most MRSA infections are caused by ST59-MRSA-V<sub>T</sub><xref ref-type="bibr" rid="pone.0017936-Takano1">[14]</xref>; <xref ref-type="bibr" rid="pone.0017936-Wang2">[236]</xref>. A
comparable picture may currently evolve in Australia due to a massive increase
in ST93-MRSA-IV infections.</p><p>The role of PVL in MRSA and especially in USA300 has been extensively and
controversially discussed <xref ref-type="bibr" rid="pone.0017936-Diep1">[61]</xref>; <xref ref-type="bibr" rid="pone.0017936-Voyich1">[237]</xref>-<xref ref-type="bibr" rid="pone.0017936-LabandeiraRey1">[239]</xref>, with particular
emphasis on the situation in the USA. However, other parts of the world harbour
other PVL-MRSA. If different strains from diverse clonal groups cause the same
distinct syndromes (such as chronic/recurrent SSTI in immunocompetent young
adults) the causative factor should be present in all of them. Thus, the
observation that, <italic>e.g.,</italic> PVL-positive CC5, CC8 and CC30 isolates
can cause the same symptoms, but behave differently than essentially isogenic
but PVL-negative CC5, CC8 and CC30 strains rendered it improbable that a factor
other than PVL was the key marker of virulence in PVL-positive MRSA. As PVL-MRSA
belong to different <italic>agr-</italic>groups, a connection of the
evolutionary success of PVL-MRSA to <italic>agr</italic> group affiliation,
<italic>i.e</italic>., to peculiarities of gene regulation is also
improbable. The diversity and abundance of PVL-MRSA clones in Abu Dhabi and
Australia could also indicate that no USA300-specific factor besides PVL (such
as ACME) was necessary for the expansion of a PVL-MRSA clone. Thus, our
observations suggest that PVL plays a key role in the evolutionary success of
MRSA in a clearly defined ecological niche of chronic/recurrent SSTI in
otherwise healthy young adults and, rarely, of necrotising pneumonia. In
settings where PVL-MRSA is abundant, they also have been observed to cause,
<italic>e.g</italic>., bloodstream infections <xref ref-type="bibr" rid="pone.0017936-Seybold1">[240]</xref>. However, this can be
attributed to their overall abundance and to the relative rarity of other
strains, since PVL is thought not to contribute to the pathogenesis of
bloodstream infections <xref ref-type="bibr" rid="pone.0017936-Ellington7">[241]</xref>.</p></sec><sec id="s3d"><title>Outlook</title><p>The evolving issue of community-acquired and livestock-associated MRSA poses a
major public health threat. The biological diversity of MRSA is increasing and
this enables MRSA to move out of the small and relatively controllable
ecological niche of hospitals and intensive care units into the general
population of developed and developing nations and into livestock animals.
Consequently, it can no longer be considered an exclusive hospital-associated
problem, and it cannot be fought by hospital infection prevention and control
measures alone. Some of the MRSA strains may replace MSSA in a similar way as
penicillinase-positive strains replaced penicillinase-negative strains in the
1950s and 1960s. A consequence of such a development may be that β-lactam
antibiotics could only be used when proven to be effective,
<italic>i.e.</italic> not as an initial therapy but only after
susceptibility testing has been performed. This would result in an increased use
of antimicrobials which are more expensive and/or less effective and in dire
consequences for individual patients as well as for entire national healthcare
systems.</p><p>Due to the increasing biodiversity of MRSA and the resulting exploitation of
novel ecological niches outside of hospitals it cannot be realistically expected
that MRSA might be eradicated easily. In order to check its current
proliferation, factors which confer advantage to MRSA need to be turned into a
disadvantage. Thus, carriage of <italic>mecA</italic> and/or PVL needs to be
“penalised” by consequent treatment, eradication and infection
prevention and control measures. Practically, a “search-and-destroy”
policy as in Scandinavian countries, the Netherlands and Western Australia is
warranted. This requires routine screening assays for <italic>mecA</italic>and/or PVL as well as advanced typing techniques and we anticipate that the
methods and data from our study might contribute to this.</p></sec></sec><sec sec-type="materials|methods" id="s4"><title>Materials and Methods</title><sec id="s4a"><title>Strains and isolates</title><p>A database of microarray experiments performed by the authors on more than 3,000
MRSA isolates has been used for this study. Isolates have been collected as part
of routine diagnostic work from the following sources: the Dresden University
Hospital (Saxony, Germany) and hospitals of Hoyerswerda (Saxony, Germany) and
Saarbrücken (Saarland, Germany), a variety of German intensive care units
(as part of the S.A.R.I. study, <xref ref-type="bibr" rid="pone.0017936-Meyer1">[242]</xref>), the “Friedrich-Loeffler-Institut”
(Federal Research Institute for Animal Health, Germany), the national MRSA
reference centres in London (UK), Lyon (France) and Dublin (Ireland), hospitals
in Ireland, Msida (Malta), Abu Dhabi (United Arab Emirates), Hong Kong (China),
Trinidad & Tobago and from the Gram-positive Bacteria Typing and Research
Unit, Perth (Australia). The majority of isolates were sampled between 2000 and
August 2010. A small number of older isolates were also included (such as for
ST247- and ST250-MRSA-I); this is mentioned in the text along with the strain
descriptions. Additionally, a collection of reference strains from the Network
on Antimicrobial Resistance in <italic>S. aureus</italic> (NARSA, Herndon,
Virginia, USA) was characterised, mainly to reflect the diversity of MRSA
strains in the USA. A few strains originated from other sources that are
acknowledged in the respective sections and in the Acknowledgments.</p><p>Additional information on emerging MRSA strains and their geographic
distributions as reported in recent publications has also been included.</p></sec><sec id="s4b"><title>Sequence-based typing</title><p>Multilocus sequence typing (MLST), which is based on sequencing of internal
fragments of <italic>arcC, aroE, glpF, gmk, pta, tpi</italic> and
<italic>yqiL</italic> housekeeping genes, was performed on selected
isolates. The protocol used was as described by Enright <italic>et al</italic>.
<xref ref-type="bibr" rid="pone.0017936-Enright1">[25]</xref>. The
sequences obtained were compared with those at the MLST website (<ext-link ext-link-type="uri" xlink:href="http://saureus.mlst.net/">http://saureus.mlst.net/</ext-link>) to assign a sequence type (ST).
Related sequence types were clustered to clonal complexes (CC) using BURST
analyses as provided on the MLST website.</p><p>The <italic>spa</italic> typing procedures were performed according to previously
published protocols <xref ref-type="bibr" rid="pone.0017936-Harmsen1">[243]</xref> using the nomenclature as described on the Ridom
website (<ext-link ext-link-type="uri" xlink:href="http://spa.ridom.de/">http://spa.ridom.de/</ext-link>) and either the RIDOM or SPATYPEMAPPER
(freeware, download at <ext-link ext-link-type="uri" xlink:href="http://www.clondiag.com/fileadmin/Media/Downloads/SPATypeMapper_0_6.zip">http://www.clondiag.com/fileadmin/Media/Downloads/SPATypeMapper_0_6.zip</ext-link>)
software packages.</p></sec><sec id="s4c"><title>DNA microarray-based typing</title><p>The Alere StaphyType DNA microarray was employed using protocols and procedures
previously described in detail <xref ref-type="bibr" rid="pone.0017936-Monecke1">[29]</xref>; <xref ref-type="bibr" rid="pone.0017936-Monecke6">[ 96]</xref>. The DNA microarray covers 334 target sequences,
(approximately 170 distinct genes and their allelic variants) including species
markers, SCC<italic>mec</italic>, capsule and <italic>agr</italic> group typing
markers, resistance genes, exotoxins, and MSCRAMM genes. Primer and probe
sequences have been published previously <xref ref-type="bibr" rid="pone.0017936-Monecke1">[29]</xref>; <xref ref-type="bibr" rid="pone.0017936-Monecke6">[96]</xref>.</p><p>Target genes and information on primers and probes are provided in Supplemental
<xref ref-type="supplementary-material" rid="pone.0017936.s001">file
S1</xref>.</p><p>MRSA were grown on Columbia blood agar and incubated overnight at 37°C.
Culture material was enzymatically lysed prior to DNA preparation using
commercially available spin columns (Qiagen, Hilden, Germany). Purified DNA
samples were used as templates in a linear primer elongation using one primer
per target. All targets were amplified simultaneously, and within this step,
biotin-16-dUTP was incorporated into the resulting amplicons. An alternate
protocol was used for a few isolates in which amplification and labelling were
directed by random primers <xref ref-type="bibr" rid="pone.0017936-Monecke10">[139]</xref>; <xref ref-type="bibr" rid="pone.0017936-Monecke12">[244]</xref>. As this protocol does not rely on conserved primer
binding sites, it proved to be useful for characterisation of unusual strains
which are not fully represented by the published genome sequences
(<italic>e.g.,</italic> ST75 strains).</p><p>Amplicons obtained using either protocol were hybridised to the microarray
followed by washing and blocking steps, and the addition of
horseradish-peroxidase-streptavidin conjugate. After further incubation and
washing steps, hybridisations were visualised by using a precipitating dye. An
image of the microarray was taken and analysed using a designated reader and
software (ALERE Technologies GmbH, Jena, Germany). Normalised intensities of the
spots were calculated based their average intensities and on the local
background <xref ref-type="bibr" rid="pone.0017936-Monecke6">[96]</xref>. Results were regarded as negative if the normalised
intensity for a given probe was below 25% of the median value of species
markers (<italic>coa, eno, fnbA, gapA, katA, nuc, rrn, sarA sbi, spa,
vraS</italic>) and a biotin staining control. If the normalised intensity of
a given probe was higher than 50% of this breakpoint, it was interpreted
positive. If it was between 25% and 50%, the result was regarded
as ambiguous. For some markers, for which allelic variants were to be
discriminated (<italic>bbp, clfA, clfB</italic> and <italic>fnbB</italic> as
well as some <italic>set/ssl</italic> genes, <italic>isaB, mprF</italic> and
<italic>isdA</italic>), a different approach was used because these alleles
differed only in single nucleotides. Here, only the probe with the strongest
signal value was regarded as positive, provided that it exceeded the 50%
breakpoint. All others were regarded as ambiguous or, if below the 25%
breakpoint, as negative. This allowed an easy and clear distinction of clonal
complex-specific variants of these genes. Genes which are not present in all
tested isolates are labelled as rare, variable or common in <xref ref-type="fig" rid="pone-0017936-g002">Figures 2</xref> and <xref ref-type="fig" rid="pone-0017936-g003">3</xref> as well as in Supplement S2 (see
legends).</p><p>The affiliation of isolates to clonal complexes (CCs) or sequence types (STs) as
defined by MLST <xref ref-type="bibr" rid="pone.0017936-Enright1">[25]</xref> was determined by an automated comparison of
hybridisation profiles to a collection of reference strains previously
characterised by MLST <xref ref-type="bibr" rid="pone.0017936-Monecke1">[29]</xref>; <xref ref-type="bibr" rid="pone.0017936-Monecke6">[96]</xref>. Analysis of hybridisation patterns cannot
discriminate sequence types which differ only in single point mutations
affecting MLST genes (<italic>e.g.,</italic> ST5 and ST225, or ST59 and ST952).
However, there are also sequence types which originate from chromosomal
replacements as previously described <xref ref-type="bibr" rid="pone.0017936-Robinson2">[170]</xref>; <xref ref-type="bibr" rid="pone.0017936-Holden2">[173]</xref>. As these events result in
different hybridisation patterns, such STs can be easily identified. MRSA
strains which belong to these sequence types will be described separately from
the parental CCs.</p></sec><sec id="s4d"><title>SCC<italic>mec</italic> typing</title><p>The SCC<italic>mec</italic> elements were typed using previously described PCR
primers and conditions and by array hybridisation as described below.</p><p>For PCR-based typing, structural architecture and <italic>mec</italic>-complex
were determined using the primers described by Zhang <italic>et al.,</italic>2005 <xref ref-type="bibr" rid="pone.0017936-Zhang2">[132]</xref>.
SCC<italic>mec</italic> type IV was further sub-typed using published
primers <xref ref-type="bibr" rid="pone.0017936-Milheirico1">[245]</xref>. The cassette chromosome recombinase
(<italic>ccr</italic>) was typed as described previously <xref ref-type="bibr" rid="pone.0017936-Kondo1">[246]</xref>. An
ISau4-like transposase (GenBank accession number DQ680163) inserted into the
open reading frame V011 of SCC<italic>mec</italic> V<sub>T</sub> was detected by
the production of a <italic>ca</italic>. 1,600-bp PCR and confirmed by
sequencing <xref ref-type="bibr" rid="pone.0017936-Coombs3">[126]</xref>.</p><p>All Irish MRSA isolates underwent SCC<italic>mec</italic> typing for (i) the
<italic>ccr</italic> and <italic>mec</italic> complex genes and (ii) the J
regions and <italic>mecI</italic><xref ref-type="bibr" rid="pone.0017936-Shore1">[15]</xref>; <xref ref-type="bibr" rid="pone.0017936-Shore3">[85]</xref>; <xref ref-type="bibr" rid="pone.0017936-Kondo1">[246]</xref>; <xref ref-type="bibr" rid="pone.0017936-Oliveira3">[247]</xref>. In
addition, isolates harbouring SCC<italic>mec</italic> IV underwent
SCC<italic>mec</italic> IV sub-typing. Sub-typing of variant
SCC<italic>mec</italic> II and IV elements from Irish isolates was performed
as described previously <xref ref-type="bibr" rid="pone.0017936-Shore1">[15]</xref>; <xref ref-type="bibr" rid="pone.0017936-Milheirico1">[ 245]</xref>.</p><p>The array includes probes for <italic>mecA</italic>, an accompanying gene,
<italic>ugpQ</italic>, <italic>mecI</italic> and <italic>xylR</italic>. Two
different probes for <italic>mecR1</italic> allow the discrimination of
un-truncated <italic>mecR1</italic> and truncated <italic>mecR1
(ΔmecR1)</italic>. Four different alleles of <italic>ccrA</italic> and
<italic>ccrB</italic> (<italic>ccrA-1, ccrB-1, ccrA-2, ccrB-2, ccrA-3,
ccrB-3, ccrA-4</italic> and <italic>ccrB-4</italic>) can be distinguished.
The gene <italic>ccrC</italic> and a “hypothetical protein”
accompanying <italic>ccrC</italic> form an additional pair of recombinase genes.
Because the latter is an analogue to <italic>ccrA</italic>, it is here
tentatively named “<italic>ccrAA</italic>”. Alleles from strain
85-2082 (GenBank AB037671) and strain MRSAZH47 (GenBank AM292304) can be
distinguished by different probes. While all SCC<italic>mec</italic> V strains
react with the former probe, only a part of them yield signals with probes for
the latter variant. This includes strains ST398-MRSA-V and Taiwan Clone
ST59-MRSA-V<sub>T</sub> which are known to harbour a distinct variant,
SCC<italic>mec</italic> V<sub>T</sub> (5C2&5).</p><p>J-region genes <italic>dcs</italic>, <italic>pls-</italic>SCC and the
<italic>kdp</italic>-operon can also be detected. Other genes with relevance
for SCC<italic>mec</italic> are a mercury resistance operon, the tobramycin
resistance gene <italic>aadD,</italic> the macrolide, lincosamide and
streptogramin B resistance gene <italic>erm</italic>(A), the tetracycline
resistance gene <italic>tet</italic>(K) and the fusidic acid resistance marker
Q6GD50. However, as these genes are plasmid- or transposon-encoded, they are not
necessarily restricted to SCC<italic>mec</italic> elements. An overview on
hybridisation patterns associated with the different SCC<italic>mec</italic>types is provided in <xref ref-type="fig" rid="pone-0017936-g001">Figure
1</xref>.</p></sec><sec id="s4e"><title>Tree reconstruction</title><p>In order to visualise similarities between hybridisation profiles, a network tree
using SplitsTree software <xref ref-type="bibr" rid="pone.0017936-Huson1">[248]</xref> was constructed. Array hybridisation profiles of the
tested strains (Supplemental <xref ref-type="supplementary-material" rid="pone.0017936.s003">file S3</xref>) were converted into a series of
‘sequences’ (Supplemental <xref ref-type="supplementary-material" rid="pone.0017936.s005">file S5</xref>). Each position in this
‘sequence’, <italic>i.e</italic>., each probe, could have a value of
‘positive’ (‘C’), ‘negative’
(‘G’), ‘ambiguous’ (‘A’) or
‘variable’ (‘T’) with the latter including all these
markers which are in Supplemental <xref ref-type="supplementary-material" rid="pone.0017936.s003">file S3</xref> designated as ‘rare’,
‘variable’ or as ‘common’. These ‘sequences’
were used with SplitsTree version 4.11.3 on default settings (characters
transformation: uncorrected P/ignore ambiguous states, distance transformation:
Neighbour-Net, and variance: ordinary least squares). For CC15 and ST426, data
from MSSA <xref ref-type="bibr" rid="pone.0017936-Monecke6">[96]</xref> were used as no MRSA isolates were found. The scale
bar represents the number of differences between signal strings (with 0.1
meaning 10% difference).</p><p>Due to the high rate of recombination affecting many genes covered by the array,
this tree does not reflect necessarily true phylogenetic relations. However, the
observation that strains of the same clonal complex cluster together indicates
that phylogenetic relationships indeed result in similar hybridisation patterns
and, on a practical level, that the hybridisation profile can be used to predict
CC affiliation <xref ref-type="bibr" rid="pone.0017936-Monecke6">[96]</xref>. Similarly, also CCs which are related according to
sequence analyses (<italic>e.g</italic>., CC22, CC30, CC45 and ST207, see <xref ref-type="bibr" rid="pone.0017936-Cooper1">[115]</xref>) also
cluster together.</p><p>For comparison, a SplitsTree analysis of the concatenated MLST sequences
(Supplemental <xref ref-type="supplementary-material" rid="pone.0017936.s004">file S4</xref>) of all STs mentioned herein is provided as <xref ref-type="fig" rid="pone-0017936-g004">Figure 4</xref>.</p></sec></sec><sec sec-type="supplementary-material" id="s5"><title>Supporting Information</title><supplementary-material content-type="local-data" id="pone.0017936.s001"><label>File S1</label><caption><p>Target genes, probes and primers.</p><p>(PDF)</p></caption><media xlink:href="pone.0017936.s001.pdf" mimetype="application" mime-subtype="pdf"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="pone.0017936.s002"><label>File S2</label><caption><p>Overview of sequence types (STs), <italic>spa</italic> types, some
characteristic genomic markers and fully sequenced genomes of the clonal
complexes (CCs) described in this study (<bold>bold typeset</bold> indicates
STs and <italic>spa</italic> types identified in the present study;
<italic>italic typeset</italic> indicates STs found by the authors in
MSSA isolates or <italic>spa</italic> types described in literature or
public databases such as RIDOM; *, see text for further
explanation).</p><p>(PDF)</p></caption><media xlink:href="pone.0017936.s002.pdf" mimetype="application" mime-subtype="pdf"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="pone.0017936.s003"><label>File S3</label><caption><p>Complete hybridisation results for MRSA strains examined in this study.</p><p>(PDF)</p></caption><media xlink:href="pone.0017936.s003.pdf" mimetype="application" mime-subtype="pdf"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="pone.0017936.s004"><label>File S4</label><caption><p>"nexus"-file used for the network graph based on concatenated MLST sequences
(<xref ref-type="fig" rid="pone-0017936-g004">Figure 4</xref>).</p><p>(NEX)</p></caption><media xlink:href="pone.0017936.s004.nex" mimetype="text" mime-subtype="plain"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="pone.0017936.s005"><label>File S5</label><caption><p>"nexus"-file used for the network graph based on hybridisation profiles
(<xref ref-type="fig" rid="pone-0017936-g005">Figure 5</xref>).</p><p>(NEX)</p></caption><media xlink:href="pone.0017936.s005.nex" mimetype="text" mime-subtype="plain"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material></sec></body><back><ack><p>We acknowledge H. Kanig, H. Nitschke (Dresden, Germany), E. Müller, I.
Engelmann, G. Rößler, J. Sachtschal (Jena, Germany), O. Brennan and P.
Kinnevey (Dublin, Ireland) as well as the staff of the bacteriological laboratory,
Institute for Medical Microbiology and Hygiene, Technical University of Dresden for
excellent help and technical assistance. V. Baier, R. Schuster and T. Uhlig (Jena,
Germany) developed software used for this work. We thank Prof. E. Jacobs (Dresden,
Germany) and E. Ermantraut (Jena, Germany) for supporting this work. We acknowledge
H. V. Aamont (Aakershus, Norway), P. Beisser (Maastricht, Netherlands), B.
Berger-Bächi (Zürich, Switzerland), C. Berglund (Stockholm, Sweden), S.
Cortez de Jäckel (Delbrück, Germany), V. Gogou (Larissa, Greece), R.
Hillert (Görlitz, Germany), M. Kamal El Din (Cairo, Egypt), S. Molinos
(Barcelona, Spain), C. Welinder-Olsson (Gothenburg, Sweden), B. Walther (Berlin,
Germany), the Federal Institute for Risk Assessment (Berlin, Germany), the Institut
Pasteur (Paris, France) and the Network on Antimicrobial Resistance in
<italic>Staphylococcus aureus</italic> (Hendon, Virginia, USA) for supplying
additional strains.</p></ack><fn-group><fn fn-type="conflict"><p><bold>Competing Interests: </bold>R. Ehricht, P. Slickers and, since March 14, 2011, S. Monecke are employees of
Alere Technologies GmbH. This does not alter the authors' adherence to all
the PLoS ONE policies on sharing data and materials. There are no patents,
products in development or marketed products to declare.</p></fn><fn fn-type="financial-disclosure"><p><bold>Funding: </bold>R. Ehricht and P. Slickers are employees of Alere Technologies GmbH. The
Vice-Rectorate for Research of the Medical Faculty Dresden partially financed
this work. Each of the participating institutions regularly purchased test kits
and reagents form commercial providers, which included Alere Technologies GmbH,
and covered the costs of experiments performed in the respective institutions,
as well as granting the time needed to perform this study. Decisions on study
design, data collection and analysis, publication or preparation of the
manuscript were agreed upon by the authors involved without influence by the
funding institutions.</p></fn></fn-group><ref-list><title>References</title><ref id="pone.0017936-vanBelkum1"><label>1</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>van Belkum</surname><given-names>A</given-names></name><name><surname>Melles</surname><given-names>DC</given-names></name><name><surname>Nouwen</surname><given-names>J</given-names></name><name><surname>van Leeuwen</surname><given-names>WB</given-names></name><name><surname>van Wamel</surname><given-names>W</given-names></name><etal></etal></person-group><year>2009</year><article-title>Co-evolutionary aspects of human colonisation and infection by
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