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Journal of Clinical Microbiology, March 2000, p. 1008-1015, Vol. 38, No. 3
Wellcome Trust Centre for the Epidemiology of
Infectious Disease, Department of Zoology, Oxford University, Oxford
OX1 3FY,1 and Wellcome Trust Centre for
Clinical Tropical Medicine, Nuffield Department of
Medicine,2 and Department of
Pathology and Bacteriology,3 Oxford University,
John Radcliffe Hospital, Oxford OX3 9DU, United Kingdom
Received 22 September 1999/Accepted 15 December 1999
A multilocus sequence typing (MLST) scheme has been developed for
Staphylococcus aureus. The sequences of internal fragments of seven housekeeping genes were obtained for 155 S. aureus
isolates from patients with community-acquired and hospital-acquired
invasive disease in the Oxford, United Kingdom, area. Fifty-three
different allelic profiles were identified, and 17 of these were
represented by at least two isolates. The MLST scheme was highly
discriminatory and was validated by showing that pairs of isolates with
the same allelic profile produced very similar SmaI
restriction fragment patterns by pulsed-field gel electrophoresis.
All 22 isolates with the most prevalent allelic profile
were methicillin-resistant S. aureus (MRSA) isolates and
had allelic profiles identical to that of a reference strain of the
epidemic MRSA clone 16 (EMRSA-16). Four MRSA isolates that were
identical in allelic profile to the other major epidemic MRSA clone
prevalent in British hospitals (clone EMRSA-15) were also identified.
The majority of isolates (81%) were methicillin-susceptible S. aureus (MSSA) isolates, and seven MSSA clones included five or
more isolates. Three of the MSSA clones included at least five isolates
from patients with community-acquired invasive disease and may
represent virulent clones with an increased ability to cause disease in
otherwise healthy individuals. The most prevalent MSSA clone (17 isolates) was very closely related to EMRSA-16, and the success of the
latter clone at causing disease in hospitals may be due to its
emergence from a virulent MSSA clone that was already a major cause of
invasive disease in both the community and hospital settings. MLST
provides an unambiguous method for assigning MRSA and MSSA isolates to known clones or assigning them as novel clones via the Internet.
Staphylococcus aureus is
a major pathogen that is associated with serious
community-acquired and nosocomial disease (8, 29). In the
United Kingdom, S. aureus is the second most common isolate from blood cultures after Escherichia coli and is by
far the most common hospital-acquired organism (1). Clinical
syndromes associated with severe disease include bacteremia, pneumonia, endocarditis, septic arthritis, osteomyelitis, and deep abscess formation.
In the preantibiotic era, the rate of mortality from invasive
S. aureus disease was high and the introduction of
penicillin had a dramatic impact on treatment. The semisynthetic
penicillin methicillin was introduced in 1959 to overcome the problems
that arose from the increasing prevalence of
penicillinase-producing isolates of S. aureus
resistant to penicillin G and penicillin V. Methicillin-resistant
S. aureus (MRSA) strains rapidly emerged and became a
major clinical problem within hospitals during the 1960s in Europe and
the 1970s in the United States and elsewhere (12, 20, 27).
Many MRSA strains are resistant to most other classes of antimicrobial
agents and are susceptible only to glycopeptides and new
investigational drugs. The recent reports of MRSA with decreased
susceptibility to glycopeptides (glycopeptide-intermediate S. aureus) [GISA]) threatens to compromise further
our ability to treat hospital-acquired S. aureus infections
(13, 26).
Although the infection control problems caused by MRSA and GISA and the
limited therapeutic options are of major concern for hospitals, the
majority of S. aureus infections acquired within hospitals
and almost all S. aureus infections acquired within the
community are caused by strains that are susceptible to methicillin and
most other classes of antibiotics (methicillin-susceptible S. aureus [MSSA]). Few studies have characterized MSSA isolates (19, 33), and it is unclear whether some MSSA clones that are circulating within the community (or in hospitals) have a particular ability to cause serious infections (hypervirulent clones)
and have an international distribution. We are also ignorant of the
basic features of the population and evolutionary biology of this
important pathogen.
Many of the basic questions about the population biology of S. aureus and a better understanding of the origins and spread of
MRSA clones and of the relatedness of MRSA and MSSA clones described by
different laboratories could be answered if we could characterize
isolates of this species unambiguously. The most widely used molecular
typing method for the study of the local and global epidemiologies of
MRSA is pulsed-field gel electrophoresis (PFGE) (2). This
method has proved very successful for the investigation of nosocomial
outbreaks (4, 7, 21) and has also been used to identify MRSA
clones that have a particular ability to cause major outbreaks and to
spread nationally and internationally (epidemic MRSA clones; EMRSA
[6, 22]). A major disadvantage of PFGE and all methods
that depend on comparisons of DNA fragment patterns on gels is the
difficulty of comparing the results from different laboratories. For
this reason there is considerable confusion about the genetic
relatedness of the clones of EMRSA described by different laboratories
and a pressing need for a method that allows EMRSA clones and virulent
MSSA clones to be identified unambiguously without the need to exchange
reference strains.
Multilocus sequence typing (MLST) is a highly discriminatory method of
characterizing bacterial isolates on the basis of the sequences of
~450-bp internal fragments of seven housekeeping genes
(16). For each gene fragment, the different sequences are
assigned as distinct alleles, and each isolate is defined by the
alleles at each of the seven housekeeping loci (the allelic profile or
sequence type [ST]). As there are many alleles at each of seven loci,
isolates are highly unlikely to have identical allelic profiles by
chance, and isolates with the same allelic profile can be assigned as
members of the same clone (16, 28). Sequence data are
readily compared between laboratories, and a major advantage of MLST is
the ability to compare the results obtained in different studies via
the Internet. In addition, the data obtained by MLST can be used to
address basic questions about the evolutionary and population biology
of bacterial species (11, 28).
MLST has been developed for the identification of the hypervirulent
lineages of Neisseria meningitidis (16) and for
assigning Streptococcus pneumoniae strains to the major
hypervirulent clones (9, 10) and to the major
penicillin-resistant and multiple-antibiotic-resistant clones (10,
25). In this report we describe the development and validation of
an MLST scheme for S. aureus and demonstrate the utility of
the method by identifying the MRSA and MSSA clones within a sample of
155 recent isolates from patients with serious community-acquired and
hospital-acquired infections.
Bacterial isolates.
We selected 155 consecutive bacterial
isolates from prospectively selected patients with invasive S. aureus disease identified in the Oxford, United Kingdom, region in
1997 or 1998. Invasive S. aureus disease was defined as the
isolation of the organism from a normally sterile site in a patient
with clinical signs and symptoms consistent with S. aureus
infection. Isolates from patients with deep local infections associated
with prosthetic material were excluded, as were isolates from patients
with septicemia in which S. aureus was isolated from only
one blood culture bottle (of at least two inoculated). Patients were
assigned to one of two groups on the basis of clinical details: those
with community-acquired disease and those with hospital-acquired
disease. Community-acquired disease was defined as an illness
consistent with invasive S. aureus disease that required
admission to hospital and that resulted in the isolation of S. aureus from a specimen taken from a normally sterile site within
24 h of admission. In addition, patients hospitalized for any
reason within the preceding 6 months were excluded from this category.
Of the 155 isolates, 61 were from patients with community-acquired
disease and 94 were from patients with hospital-acquired disease. One
hundred forty isolates were obtained from blood cultures, and the other
15 were obtained from deep pus samples from patients with invasive
S. aureus disease. Isolates were confirmed to be S. aureus by positive tube coagulase and DNase tests. Resistance to
methicillin was determined by measuring the oxacillin MIC for the
organism. This was done by using the oxacillin E-test (AB Biodisk,
Solna, Sweden), with resistance defined as an MIC of >2 µg
ml MLST.
The DNA sequences of 14 housekeeping genes were
supplied by M. Burnham of SmithKline Beecham. The sequences of their
gene products were compared with those in the EMBL/GenBank
database by using BlastP
(http://www.ncbi.nlm.nih.gov/blast/blast.cgi), and the amino
acid sequences of the pneumococcal protein and its homologs were
aligned and the most variable regions were identified. Primers were
designed by using the sequences of the highly conserved regions that
flank the more variable regions. Each primer pair amplified an internal
fragment of the housekeeping gene (about 500 bp) and allowed accurate
sequencing of ~450-bp fragments of each gene on both strands.
0095-1137/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Multilocus Sequence Typing for Characterization of
Methicillin-Resistant and Methicillin-Susceptible Clones of
Staphylococcus aureus
ABSTRACT
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
INTRODUCTION
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
MATERIALS AND METHODS
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Introduction
Materials and Methods
Results
Discussion
References
1 (18).
TABLE 1.
Sequences of primers used in the PCR
1 at the cell lysis step. PCRs were carried out
with 50-µl reaction volumes containing 0.5 µl of chromosomal DNA
(approximately 0.5 µg), 0.5 µg of each primer, 1 U of
Taq DNA polymerase (Qiagen, Crawley, United Kingdom), 5 µl
of 10× buffer (supplied with the Taq polymerase), and 0.2 mM deoxynucleoside triphosphates (Perkin-Elmer Applied Biosystems;
Foster City, Calif.). The PCR was performed in a PTC-200 DNA engine (MJ
Research, Boston, Mass.) with an initial 5-min denaturation at 95°C,
followed by 30 cycles of annealing at 55°C for 1 min, extension at
72°C for 1 min, and denaturation at 95°C for 1 min, followed by a
final extension step of 72°C for 5 min. The amplified products were
precipitated with 20% polyethylene glycol-2.5 M NaCl (15),
resuspended in cold 70% ethanol, and reprecipitated; and the sequences
of both strand were determined with an ABI Prism 377 DNA sequencer with
BigDye fluorescent terminators and the primers used in the initial PCR amplification.
For each locus, the sequences obtained from all 155 isolates were
compared and the different sequences were assigned allele numbers. For
each isolate, the alleles at each of the seven loci defined the allelic
profile which corresponded to its ST. The clustering of isolates was
achieved by the unweighted pair group method with arithmetic averages
(UPGMA) from the matrix of the percentage of pairwise differences
between the allelic profiles of the isolates by using Statistica
(StatSoft, Tulsa, Okla.). The nonrandomness in the distribution of
variable sites along the sequence of each gene fragment was examined by
the method of Sawyer (23). Polymorphic sites were displayed
by using Sequence Output, a Macintosh program available from the MLST
website (http://mlst.zoo.ox.ac.uk).
PFGE.
Chromosomal DNA from S. aureus was prepared
in agarose blocks and was cleaved with SmaI by the method of
Bannerman et al. (2). The samples were run on 1% agarose
gel in 0.5% TBE buffer (44.5 mM Tris, 44.5 mM borate, 1 mM EDTA) on a
CHEF DR-III PFGE system (Bio-Rad, Hemel Hempstead, Hertsfordshire,
United Kingdom) by using an initial switching time of 1 s which
was increased to 5 s for 12 h, followed by 12 h with an
initial switching time of 15 s which was increased to 30 s,
by using a voltage of 6 V cm1 (3).
Concatenated bacteriophage lambda DNA (New England Biolabs, Beverly,
Mass.) was used to provide molecular size markers.
Detection of mecA. The presence of mecA was determined by using the primers MR1 and MR2, which were used in the PCR to amplify a 1,339-bp internal fragment of the gene (32). PCR was carried out for 30 cycles of 1 min at 95°C, 1 min at 55°C, and 2 min at 72°C.
Nucleotide sequence accession numbers. The DNA sequences of each allele at the seven loci used in this study have been deposited in GenBank under accession nos. AJ252295-2310, AJ271251-89, AJ271387-403, and AJ271482-510, and can be downloaded from the website mentioned above.
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RESULTS |
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Materials and Methods
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Discussion
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Sequences of the seven housekeeping gene fragments.
Fourteen
housekeeping gene fragments were sequenced from 10 S. aureus strains, obtained from different geographic locations, and
the seven gene fragments that provided the greatest number of alleles
were chosen for use in the MLST scheme. These seven housekeeping gene
fragments, which were of between 402 and 516 bp (Table
2), were then sequenced from each of 155 recent isolates of S. aureus from patients with invasive
disease in the Oxfordshire region. For each isolate, the sequences
obtained at each of the seven loci were compared with those of every
other isolate, and the alleles were numbered consecutively. Sequences
were assigned as distinct alleles even if they differed at a single
nucleotide site; no weighting was applied to reflect the number of
nucleotide differences between alleles.
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Validation of the S. aureus MLST scheme.
Table
3 shows the 53 different allelic profiles
or STs identified among the 155 S. aureus isolates. The MLST
scheme was validated by selecting one pair of isolates from each of the
17 STs that contained multiple isolates and examining by PFGE the
similarities of the SmaI fragments obtained from the
chromosomal DNA of each pair. For STs 12 and 22, which included both
MRSA and MSSA isolates, one of the selected pair was MRSA and one was
MSSA. The SmaI PFGE fingerprints for eight pairs of isolates
are shown in Fig. 2. One of the 17 pairs
of isolates (ST34) had five fragment differences, but the other pairs,
including the two pairs consisting of both MRSA and MSSA isolates,
differed at four fragments or less.
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Clustering of the invasive S. aureus isolates. Figure 3 shows a dendrogram constructed from the matrix of pairwise differences between the allelic profiles of the 155 isolates. ST36 contained the largest number of isolates, all 22 of which were MRSA. The second largest cluster was ST30. The 17 isolates of ST30 were all MSSA and were closely related in genotype to the MRSA isolates of ST36, as their allelic profiles differed at only one locus (pta). Nine other STs were represented by at least five isolates. All 11 of these prevalent STs except ST36, which included only hospital-acquired MRSA isolates, were represented by isolates recovered both from patients with community-acquired infections and from patients with hospital-acquired infections.
Nine of the 11 prevalent STs were part of clonal complexes, which included the isolates of the prevalent ST and closely related isolates whose allelic profiles differed from the profile of the prevalent ST at only a single locus (Fig. 3; Table 3). In three cases, the clonal complexes included a larger number of STs whose allelic profiles differed from each other at only one two loci (Fig. 3; Table 3). For example, the isolates of STs 29 to 38 (see below) were part of a large cluster which included 48 of the 155 isolates (31%) and which included the two major STs. Similarly, STs 44 to 48 and STs 14 to 18 included 14 and 10 closely related isolates, respectively.Analysis of MRSA isolates. Of the 155 isolates, 29 (19%) were methicillin resistant and 126 (81%) were methicillin susceptible. Only one of the MRSA isolates was obtained from a patient with a community-acquired infection. The major clone identified in this study (ST36) included 22 MRSA isolates. Eleven of these MRSA isolates were submitted to the Central Public Health Laboratory (Colindale, London, United Kingdom) and were assigned as members of the EMRSA-16 clone by PFGE. EMRSA-15 (21) and EMRSA-16 (4) are the most common MRSA clones recovered in hospitals in the United Kingdom in recent years (1). The allelic profiles of reference strains of EMRSA-15 (strain 90/10685) and EMRSA-16 (strain 96/32101), kindly provided by B. Cookson of the Central Public Health Laboratory, were determined. The allelic profile of the EMRSA-16 reference strain was identical to those of the 22 MRSA isolates of ST36.
Similarly, the allelic profile of the EMRSA-15 reference strain was identical to those of the isolates of ST22. ST22 included four MRSA isolates, including the only one in the collection that was community acquired, as well as four MSSA, three of which were community acquired. Only three of the MRSA isolates did not belong to either ST36 (EMRSA-16) or ST22 (EMRSA-15). Two of these isolates (which belonged to ST35 and ST38) were very closely related to EMRSA-16, as they differed at only a single locus, and are considered to be minor variants of EMRSA-16. The other MRSA isolate (which belonged to ST12) was indistinguishable from a cluster of four MSSA isolates and was not similar to any of the reference strains of MRSA clones that we examined. The presence of mecA was determined for all isolates of the two STs that included both MRSA and MSSA isolates (STs 12 and 22) and for at least two members of the other STs containing MRSA isolates. All MRSA isolates tested contained the mecA gene, whereas this gene was not detected in the MSSA isolates.Analysis of MSSA isolates. Methicillin-susceptible isolates comprised the majority of the invasive S. aureus isolates collected in this survey (126 isolates; 81%), and they were responsible for 98% of all community-acquired infections and 70% of all hospital-acquired infections. There were 60 community-acquired MSSA isolates and 66 hospital-acquired MSSA isolates among the 155 isolates in the collection.
The majority of the MSSA isolates (71%) had allelic profiles that were identical to that of at least one other MSSA isolate, with 14 of the 17 STs that included multiple isolates consisting entirely of MSSA isolates. There was no clear difference between hospital-acquired and community-acquired MSSA isolates. All 11 STs that were represented by at least three MSSA isolates contained isolates from both patients with hospital-acquired infections and patients with community-acquired infections (Fig. 3). The MSSA clones with the most isolates contained 17 (ST30), 12 (ST25), 8 (ST8 and ST39), and 7 (ST1 and ST5) isolates, accounting for 47% of the MSSA isolates in this study.| |
DISCUSSION |
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Molecular methods have been used to study the epidemiology of MRSA
in hospital, national, and global settings, with PFGE proving the most
satisfactory method on the basis of its discriminatory ability and
reproducibility (24, 30). The major disadvantage of PFGE and
other methods that compare DNA fragments on gels is the difficulty of
comparing the results obtained in different laboratories, even
when reagents and conditions are standardized (3, 5, 34).
MLST provides a highly discriminatory method that defines
each isolate as a string of seven integers
the allelic profileand which produces data that can be held in a central database
on the World Wide Web, along with associated epidemiological data, and
which can be interrogated via the Internet (16, 28). This
approach allows any laboratory that uses MLST to submit the sequences
of the seven gene fragments of an S. aureus isolate to the
MLST website (http://mlst.ox.ac.uk), where an allelic profile can be
assigned and compared with those of all of the MRSA and MSSA isolates
maintained in the database.
The clustering of isolates obtained by MLST agreed well with that obtained by PFGE. Isolates that were identical by MLST had either identical SmaI fragment patterns or patterns that differed at two to five fragments. PFGE patterns that have less than four fragment differences are considered to be the same strain, and isolates that differ at four to six fragments are considered to be of the same genetic lineage (31). The criterion for assigning isolates as the same strain by PFGE is used in the context of outbreaks of disease to infer epidemiological links. In many cases, strains from outbreaks are likely to be identical or very similar by PFGE, as they are descended from a common ancestor (the isolate from the index case patient who introduced the outbreak strain) that may have existed only a matter of weeks or months earlier. In MLST, the variation within housekeeping genes accumulates relatively slowly (28), and isolates with the same allelic profile (ST) may be descended from a common ancestor that existed many years ago. It is therefore not surprising that, for some pairs of isolates with the same ST, the number of fragment differences obtained by PFGE is slightly greater than the criterion number used to define isolates of the same strain. STs that appeared to be closely related by MLST also had similar PFGE fragment patterns, whereas those that appeared to be distantly related had very few fragments in common. This congruence between MLST and PFGE was expected since MLST is highly discriminatory, and it is therefore very unlikely that totally unrelated isolates will, by chance, have the same allelic profile.
The major clone (ST36) identified in this study corresponded to clone EMRSA-16, one of the two major MRSA clones circulating in British hospitals in recent years (1). Isolates of the other major British MRSA clone (clone EMRSA-15) were also found (ST22), although at a lower frequency. At present the relatedness between the major MRSA clones described by different laboratories in different countries is unclear. MLST will provide a simple means of defining each MRSA clone unambiguously. The advantage of the MLST approach is shown by the ease with which isolates of STs 22 and 36 were assigned as members of the EMRSA-15 and EMRSA-16 clones. The allelic profiles of the major MRSA clones will be available on the S. aureus MLST database (M. C. Enright, unpublished data), and any MRSA clone (or isolate) can be assigned by MLST to a previously identified clone or as a novel clone by using the Internet.
Three STs (STs 12, 15, and 22) contained both MRSA and MSSA isolates.
The identification of MSSA and MRSA isolates that were indistinguishable by MLST was slightly unexpected, and the possibility that the MLST scheme lacked resolution had to be considered. The expected frequency of occurrence of any allelic profile by chance can
be calculated from the product of the observed frequencies of each of
the seven alleles in the population. The expected frequencies of
isolates of STs 12, 15, and 22 were between 1.5 × 107 and 8 × 108, and it is therefore
highly unlikely that unrelated MSSA and MRSA isolates would be assigned
to the same ST by chance. The close similarity of the MRSA and MSSA
isolates within STs 12, 15, and 22 was also confirmed by PFGE.
We therefore believe that the genotypes of MRSA and MSSA isolates with the same allelic profiles are very closely related. The most likely explanation is that the MSSA isolates represent the genotype from which the MRSA isolates recently arose by the acquisition of the methicillin resistance determinant (mec) by horizontal gene transfer. The mec determinant probably entered S. aureus only after the introduction of methicillin into medicine in 1959 (12), and many MRSA isolates will have arisen much more recently than this by the horizontal transfer of mec into new MSSA lineages (17). There has therefore been little time for MRSA isolates to have accumulated sequence variation within their housekeeping genes that would distinguish them from their MSSA ancestors. Some MRSA clones are therefore expected to be identical or very closely related in allelic profile to their MSSA ancestors. An alternative possibility is that some of the MRSA clones contain isolates in which the mec genes have been lost or inactivated. This possibility is difficult to discount, but none of the MSSA isolates that had the same allelic profiles as MRSA isolates possessed the mecA gene.
ST36 (clone EMRSA-16) was very closely related to the major MSSA
clone associated with invasive disease in the Oxford region (ST30);
these STs differed at only one of the seven loci. A dendrogram, as
shown in Fig. 3, identifies the clusters of isolates with identical allelic profiles, but it cannot always accurately represent the relationships between isolates with similar allelic profiles. Figure
4 shows the relationships among the
isolates that differ from ST30 or ST36 at a single locus. The most
parsimonious way of relating the allelic profiles of the isolates in
this clonal complex and their resistance or susceptibility to
methicillin is to propose that one of the several single-locus variants
of ST30 became methicillin resistant to result in EMRSA-16 (ST36), which subsequently expanded to become a prevalent cause of
hospital-acquired invasive disease and which itself spawned
methicillin-resistant single-locus variants (STs 35 and 38). It is
interesting that EMRSA-16 appears to be part of a major cluster of
isolates that are associated with invasive disease (STs 29 to 38) and
that included 31% of the isolates recovered from patients with
invasive disease in the Oxford region. The development of EMRSA-16 from
a virulent clone (ST30) that was a major cause of invasive disease in
both the hospital and the community settings may partly explain the success of EMRSA-16 in causing invasive disease in the hospital setting.
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Most of the MSSA clones were recovered from both patients with community-acquired invasive disease and patients with hospital-acquired invasive disease. The isolates that caused community-acquired invasive S. aureus disease were, with one exception, MSSA. These isolates caused disease in previously healthy individuals, and the prevalent STs associated with community-acquired invasive disease (e.g., STs 1, 25, and 30, isolates of which caused 35% of cases of community-acquired disease) may identify particularly virulent MSSA clones.
Much larger studies that have examined isolates from worldwide sources will be required to establish the existence of widely distributed S. aureus clones that have a special ability to cause community-acquired invasive disease. Such studies are under way. However, the major use of the MLST scheme for S. aureus will probably be to allow investigators to unambiguously identify MRSA or GISA isolates and to probe the origins and evolution of these strains.
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ACKNOWLEDGMENTS |
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This work was supported by The Wellcome Trust. B.G.S. and N.P.J.D. were in receipt of a Wellcome Trust Principal Research Fellowship and a Wellcome Trust Career Development Fellowship, respectively.
We are grateful to Paul Wilkinson for managing our nucleotide sequencing facility, Man-Suen Chan for developing the MLST website, and Martin Burnham for providing S. aureus sequences.
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FOOTNOTES |
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* Corresponding author. Mailing address: Wellcome Trust Centre for the Epidemiology of Infectious Disease, Department of Zoology, South Parks Rd., University of Oxford, Oxford OX1 3FY, United Kingdom. Phone: 44 1865-281274. Fax: 44 1865-281891. E-mail. mark.enright{at}ceid.ox.ac.uk.
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Abstract
Introduction
Materials and Methods
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Discussion
References
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(2007). Changing Molecular Epidemiology of Methicillin-Resistant Staphylococcus aureus in a Small Geographic Area over an Eight-Year Period. J. Clin. Microbiol.
45: 3729-3736
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Johnson, J. K., Arduino, S. M., Stine, O. C., Johnson, J. A., Harris, A. D.
(2007). Multilocus Sequence Typing Compared to Pulsed-Field Gel Electrophoresis for Molecular Typing of Pseudomonas aeruginosa. J. Clin. Microbiol.
45: 3707-3712
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Rabello, R. F., Moreira, B. M., Lopes, R. M. M., Teixeira, L. M., Riley, L. W., Castro, A. C. D.
(2007). Multilocus sequence typing of Staphylococcus aureus isolates recovered from cows with mastitis in Brazilian dairy herds. J Med Microbiol
56: 1505-1511
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Daskalaki, M., Otero, J. R., Sanz, F., Chaves, F.
(2007). Bacteremia Due to Clonally Derived Methicillin-Resistant, Gentamicin-Susceptible Isolates and Methicillin-Susceptible, Gentamicin-Resistant Isolates of Staphylococcus aureus. J. Clin. Microbiol.
45: 3446-3448
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Amorim, M. L., Faria, N. A., Oliveira, D. C., Vasconcelos, C., Cabeda, J. C., Mendes, A. C., Calado, E., Castro, A. P., Ramos, M. H., Amorim, J. M., de Lencastre, H.
(2007). Changes in the Clonal Nature and Antibiotic Resistance Profiles of Methicillin-Resistant Staphylococcus aureus Isolates Associated with Spread of the EMRSA-15 Clone in a Tertiary Care Portuguese Hospital. J. Clin. Microbiol.
45: 2881-2888
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Holtfreter, S., Grumann, D., Schmudde, M., Nguyen, H. T. T., Eichler, P., Strommenger, B., Kopron, K., Kolata, J., Giedrys-Kalemba, S., Steinmetz, I., Witte, W., Broker, B. M.
(2007). Clonal Distribution of Superantigen Genes in Clinical Staphylococcus aureus Isolates. J. Clin. Microbiol.
45: 2669-2680
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Brady, J. M., Stemper, M. E., Weigel, A., Chyou, P.-H., Reed, K. D., Shukla, S. K.
(2007). Sporadic "Transitional" Community-Associated Methicillin-Resistant Staphylococcus aureus Strains from Health Care Facilities in the United States. J. Clin. Microbiol.
45: 2654-2661
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Rossney, A. S., Shore, A. C., Morgan, P. M., Fitzgibbon, M. M., O'Connell, B., Coleman, D. C.
(2007). The Emergence and Importation of Diverse Genotypes of Methicillin-Resistant Staphylococcus aureus (MRSA) Harboring the Panton-Valentine Leukocidin Gene (pvl) Reveal that pvl Is a Poor Marker for Community-Acquired MRSA Strains in Ireland. J. Clin. Microbiol.
45: 2554-2563
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Sergio, D. M. B., Koh, T. H., Hsu, L.-Y., Ogden, B. E., Goh, A. L. H., Chow, P. K. H.
(2007). Investigation of meticillin-resistant Staphylococcus aureus in pigs used for research. J Med Microbiol
56: 1107-1109
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Balajee, S. A., Tay, S. T., Lasker, B. A., Hurst, S. F., Rooney, A. P.
(2007). Characterization of a Novel Gene for Strain Typing Reveals Substructuring of Aspergillus fumigatus across North America. Eukaryot Cell
6: 1392-1399
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Aires-de-Sousa, M., Parente, C. E. S. R., Vieira-da-Motta, O., Bonna, I. C. F., Silva, D. A., de Lencastre, H.
(2007). Characterization of Staphylococcus aureus Isolates from Buffalo, Bovine, Ovine, and Caprine Milk Samples Collected in Rio de Janeiro State, Brazil. Appl. Environ. Microbiol.
73: 3845-3849
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Sung, J. M.-L., Lindsay, J. A.
(2007). Staphylococcus aureus Strains That are Hypersusceptible to Resistance Gene Transfer from Enterococci. Antimicrob. Agents Chemother.
51: 2189-2191
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Bhattacharya, D., Carleton, H., Tsai, C. J., Baron, E. J., Perdreau-Remington, F.
(2007). Differences in Clinical and Molecular Characteristics of Skin and Soft Tissue Methicillin-Resistant Staphylococcus aureus Isolates between Two Hospitals in Northern California. J. Clin. Microbiol.
45: 1798-1803
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Christianson, S., Golding, G. R., Campbell, J., the Canadian Nosocomial Infection Surveillance Pro, , Mulvey, M. R.
(2007). Comparative Genomics of Canadian Epidemic Lineages of Methicillin-Resistant Staphylococcus aureus. J. Clin. Microbiol.
45: 1904-1911
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Cookson, B. D., Robinson, D. A., Monk, A. B., Murchan, S., Deplano, A., de Ryck, R., Struelens, M. J., Scheel, C., Fussing, V., Salmenlinna, S., Vuopio-Varkila, J., Cuny, C., Witte, W., Tassios, P. T., Legakis, N. J., van Leeuwen, W., van Belkum, A., Vindel, A., Garaizar, J., Haeggman, S., Olsson-Liljequist, B., Ransjo, U., Muller-Premru, M., Hryniewicz, W., Rossney, A., O'Connell, B., Short, B. D., Thomas, J., O'Hanlon, S., Enright, M. C.
(2007). Evaluation of Molecular Typing Methods in Characterizing a European Collection of Epidemic Methicillin-Resistant Staphylococcus aureus Strains: the HARMONY Collection. J. Clin. Microbiol.
45: 1830-1837
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Moojen, D. J. F., Spijkers, S. N.M., Schot, C. S., Nijhof, M. W., Vogely, H. C., Fleer, A., Verbout, A. J., Castelein, R. M., Dhert, W. J.A., Schouls, L. M.
(2007). Identification of Orthopaedic Infections Using Broad-Range Polymerase Chain Reaction and Reverse Line Blot Hybridization. JBJS
89: 1298-1305
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Ma, S. H., Lee, Y. S., Lee, S. H., Kim, H. K., Jin, J. S., Shin, E. K., Lee, J. C.
(2007). Meticillin-resistant Staphylococcus aureus clones with distinct clinical and microbiological features in a Korean community. J Med Microbiol
56: 866-868
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Elizur, A., Orscheln, R. C., Ferkol, T. W., Atkinson, J. J., Dunne, W. M. Jr, Buller, R. S., Armstrong, J. R., Mardis, E. R., Storch, G. A., Cannon, C. L.
(2007). Panton-Valentine Leukocidin-Positive Methicillin-Resistant Staphylococcus aureus Lung Infection in Patients With Cystic Fibrosis. Chest
131: 1718-1725
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Mwangi, M. M., Wu, S. W., Zhou, Y., Sieradzki, K., de Lencastre, H., Richardson, P., Bruce, D., Rubin, E., Myers, E., Siggia, E. D., Tomasz, A.
(2007). Tracking the in vivo evolution of multidrug resistance in Staphylococcus aureus by whole-genome sequencing. Proc. Natl. Acad. Sci. USA
104: 9451-9456
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Tavanti, A., Hensgens, L. A. M., Ghelardi, E., Campa, M., Senesi, S.
(2007). Genotyping of Candida orthopsilosis Clinical Isolates by Amplification Fragment Length Polymorphism Reveals Genetic Diversity among Independent Isolates and Strain Maintenance within Patients. J. Clin. Microbiol.
45: 1455-1462
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O'Neill, A. J., Larsen, A. R., Skov, R., Henriksen, A. S., Chopra, I.
(2007). Characterization of the Epidemic European Fusidic Acid-Resistant Impetigo Clone of Staphylococcus aureus. J. Clin. Microbiol.
45: 1505-1510
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Cockfield, J. D., Pathak, S., Edgeworth, J. D., Lindsay, J. A.
(2007). Rapid determination of hospital-acquired meticillin-resistant Staphylococcus aureus lineages. J Med Microbiol
56: 614-619
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van der Mee-Marquet, N., Epinette, C., Loyau, J., Arnault, L., Domelier, A.-S., Losfelt, B., Girard, N., Quentin, R., and the Bloodstream Infection Study Group of the R,
(2007). Staphylococcus aureus Strains Isolated from Bloodstream Infections Changed Significantly in 2006. J. Clin. Microbiol.
45: 851-857
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Hallin, M., Denis, O., Deplano, A., De Mendonca, R., De Ryck, R., Rottiers, S., Struelens, M. J.
(2007). Genetic relatedness between methicillin-susceptible and methicillin-resistant Staphylococcus aureus: results of a national survey. J Antimicrob Chemother
59: 465-472
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Ghebremedhin, B., Konig, W., Witte, W., Hardy, K. J., Hawkey, P. M., Konig, B.
(2007). Subtyping of ST22-MRSA-IV (Barnim epidemic MRSA strain) at a university clinic in Germany from 2002 to 2005. J Med Microbiol
56: 365-375
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Hsu, L.-Y., Loomba-Chlebicka, N., Koh, Y.-L., Tan, T.-Y., Krishnan, P., Lin, R. T.-P., Tee, N. W.-S., Fisher, D. A., Koh, T.-H.
(2007). Evolving EMRSA-15 epidemic in Singapore hospitals. J Med Microbiol
56: 376-379
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Thomas, J. C., Vargas, M. R., Miragaia, M., Peacock, S. J., Archer, G. L., Enright, M. C.
(2007). Improved Multilocus Sequence Typing Scheme for Staphylococcus epidermidis. J. Clin. Microbiol.
45: 616-619
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Morgan, W. R., Caldwell, M. D., Brady, J. M., Stemper, M. E., Reed, K. D., Shukla, S. K.
(2007). Necrotizing Fasciitis Due to a Methicillin-Sensitive Staphylococcus aureus Isolate Harboring an Enterotoxin Gene Cluster. J. Clin. Microbiol.
45: 668-671
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Seaman, P. F., Ochs, D., Day, M. J.
(2007). Small-colony variants: a novel mechanism for triclosan resistance in methicillin-resistant Staphylococcus aureus. J Antimicrob Chemother
59: 43-50
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Kuhn, G., Francioli, P., Blanc, D. S.
(2007). Double-Locus Sequence Typing Using clfB and spa, a Fast and Simple Method for Epidemiological Typing of Methicillin-Resistant Staphylococcus aureus. J. Clin. Microbiol.
45: 54-62
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