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ORIGINAL ARTICLE
Major West Indies MRSA Clones in Human Beings: Do They Travel
With Their Hosts?
Tomasz Chroboczek, MD,∗† Sandrine Boisset, PhD,∗† Jean-Philippe Rasigade, MD,∗†
Helene Meugnier, PhD,∗† Patrick E. Akpaka, MD,‡ Alison Nicholson, MD,§ Muriel Nicolas,
MD,|| Claude Olive, MD,¶ Michele Bes, PhD,∗† François Vandenesch, MD,∗†
Frederic Laurent, PharmD,∗† Jerome Etienne, MD,∗† and Anne Tristan, PharmD∗†
∗
French National Reference Centre for Staphylococci, Hospices Civils de Lyon, Lyon, France; † INSERM U851, Faculté de
Médecine Lyon Est, University of Lyon, Lyon, France; ‡ Pathology/Microbiology Unit, Department of Para-Clinical Sciences,
The University of the West Indies, St. Augustine, Trinidad & Tobago; § Department of Microbiology, The University Hospital
of the West Indies, Kingston 7, Jamaica; || Department of Microbiology, University Hospital of Pointe-à-Pı̂tre, Guadeloupe,
France; ¶ Department of Microbiology, University Hospital of Fort-de-France, Martinique, France
DOI: 10.1111/jtm.12047
Background. Descriptions of the epidemiology of methicillin-resistant Staphylococcus aureus (MRSA) have seldom been produced
in the Caribbean, which is a major tourism destination.
Materials and Methods. Using DNA microarrays and spa typing, we characterized 85 MRSA isolates from human skin and
soft-tissue infections from five different islands.
Results. In the French West Indies (n = 72), the most frequently isolated clones were the same clones that are specifically isolated
from mainland France [Lyon (n = 35) and Geraldine (n = 11) clones], whereas the clones that were most frequently isolated from
the other islands (n = 13) corresponded with clones that have a worldwide endemic spread [Vienna/Hungarian/Brazilian (n = 5),
Panton Valentine leukocidin-positive USA300 (n = 4), New York/Japan (n = 2), and pediatric (n = 1) clones].
Conclusion. The distribution of the major MRSA clones in the French (Guadeloupe and Martinique) and non-French West
Indies (Jamaica, Trinidad, and Tobago) is different, and the clones most closely resemble those found in the home countries of
the travelers who visit the islands most frequently. The distribution might be affected by tourist migration, which is specific to
each island.
T
he Caribbean region is composed of more than
7,000 islands in the Caribbean Sea, which is
located southeast of the Gulf of Mexico east of Central
America and north of South America; because of their
remarkable geographic position (ie, their presence at a
crossroads), the Caribbean islands have associated with
different countries throughout history. For instance,
Guadeloupe and Martinique are currently two overseas
French departments, Jamaica and Trinidad and Tobago
are parts of the Commonwealth, and the Dominican
Republic is part of the Great Antilles, with Spanish
Corresponding Author: Anne Tristan, PharmD, Centre
National de Référence des Staphylocoques, Centre de Biologie
et Pathologie Est—CBPE, Groupement Hospitalier Est, 59
boulevard Pinel, F-69677 Bron, France. E-mail: anne.tristan@
univ-lyon1.fr
as its official language. The Caribbean islands are
also known to be a major tourism destination, having
drawn an estimated 23.8 million tourists from various
geographical origins in 2011 (Table 1).1
It has been shown that the prevalence of methicillin
resistance in Staphylococcus aureus is increasing in these
regions.2 – 6 Akpaka and colleagues studied 60 randomly
selected methicillin-resistant S aureus (MRSA) isolates
from hospitalized patients in three hospitals in Trinidad
and Tobago and found that all of the isolates exhibited
a similar pulsed field gel electrophoresis (PFGE)
banding pattern, which is related to a Canadian strain
named CMRSA-6, and all of the isolates were Panton
Valentine leukocidin (PVL)-negative (−).7 Monecke
and colleagues found that in MRSA isolated from
Trinidad and Tobago, the ST239-MRSA-III clone
represented 76 of 80 isolates.8 Uhlemann and colleagues
studied 22 MRSA strains from the Dominican Republic
© 2013 International Society of Travel Medicine, 1195-1982
Journal of Travel Medicine 2013; Volume 20 (Issue 5): 283–288
284
Chroboczek et al.
and 56 strains from Martinique and found that the
predominating sequence types (STs) were ST5, ST30,
and ST72 in the Dominican Republic, and ST8 (spa
t304) in Martinique.9
In this study, we aimed to evaluate the possible
relationship between human migration and local MRSA
epidemiology by analyzing (with spa typing and DNA
microarrays) and comparing MRSA isolates that have
been implicated in skin and soft-tissue infections
(SSTIs) from five different islands of the Caribbean
and using data from the literature.
Materials and Methods
Bacterial Strains and Clinical Data
Between 2004 and 2009, 65 MRSA strains were
gathered in the laboratory of a hospital in Martinique.
These strains were subsequently sent to the National
Centre for Staphylococci in Lyon, France, for further
characterization. In 2010 and 2011, this collection was
completed with four more strains from Martinique,
three from Guadeloupe, five from Tobago, five from
Trinidad, and three from Jamaica. All of the strains were
isolated from patients with SSTIs.
The following clinical and demographic information
was retrospectively obtained for the patients infected
in Martinique between 2004 and 2009: age and gender
of each infected patient, type of infection, and date
and site of isolation of the bacterial strains. The
65 bacterial strains from Martinique were isolated
from 35 men and 30 women. The mean age of the
patients was 55.8 years. All but four of the patients
were inpatients. The infections were mostly healthcareassociated (85%, 55/65), even those isolated from
outpatients (75%, 3/4). These infections were hospitalacquired, occurring in patients who had undergone
recent surgical intervention, and most of the patients
possessed other risk factors for acquiring MRSA from
a hospital: chronic hemodialysis, compromised immune
system, hospitalization for more than 48 hours in
the previous 6 months, antibiotic treatment in the
previous 6 months, or regular outpatient wound care.
Most of the SSTIs (78%, 51/65) were secondary
infections occurring at a previous skin lesion. The
14 remaining primary infections consisted of abscesses
(n = 7), dermohypodermitis (n = 3), cellulitis (n = 2),
carbuncle (n = 1), or folliculitis (n = 1).
Antimicrobial Susceptibility Testing
Antimicrobial susceptibility testing was performed by
disk-diffusion assays and interpreted according to the
2011 guidelines of the Antibiogram Committee of the
French Society for Microbiology.10
Genotyping Methods
Bacterial DNA was extracted according to standard
methods using commercial extraction kits (Qiagen,
Hilden, Germany). The diagnostic DNA microarrays,
Identibac S aureus Genotyping (Alere, Waltham,
MA, USA), that were used for this study and the
related procedures and protocols have been previously
described in detail.11 This microarray covers 332
different target sequences corresponding with 185
distinct genes and their allelic variants. The affiliation
of isolates with clonal complexes (CCs) was determined
by a comparison of their hybridization profiles with
previously typed multilocus sequence typing (MLST)
reference strains.11
A DNA sequence-based analysis of the variable
region of the protein A gene was performed as has
been previously described,12 using the nomenclature
described on the Ridom website (http://spa.ridom.de/).
Results
Molecular Typing Results
The characterization of the strains by DNA microarray
separated the 85 isolates into four CCs (MLST
Table 1 Populations of five islands of the West Indies, their respective numbers of tourists per year, and the main provenances
of the tourists
Island
Population
Tourists
401,554∗
396,404∗
383,518∗
501,491∗
Jamaica
Trinidad and Tobago
2,705,800†
1,317,714§
1,957,011‡
371,889¶
Dominican Republic
10,010,590∗∗
4,491,925‡
Guadeloupe
Martinique
Main provenance of tourists
France 92%, Europe 5.6%, other countries 1.6%, unknown <1%∗
France 75.7%, other French overseas departments 10.9%, Europe 5%,
other Caribbean countries 4.1%, USA 2.5%, Canada 1%, other 0.6%∗
USA 63.8%, Canada 19.8%, Europe 11.2%, other 5.1%‡
USA 46%, other Caribbean 20%, Canada 11%, UK 10%, other Europe
5%, South America 5%
USA 32.4%, Europe 25%, Canada 14.8%, other 27.8%‡
∗
Source: Institut National de la Statistique et des Etudes Economiques (INSEE)—information about Guadeloupe from the years 2009 (population and number of
tourists) and 2006 (provenance) and information about Martinique from the years 2009 (population) and 2007 (tourists and provenance).
†
Source: Statistical Institute of Jamaica (STATIN)—information from the year 2010.
‡
Source: Caribbean Tourism Organization—information from the year 2012.
§
Source: Central Statistical Office of Trinidad and Tobago—information from the year 2010.
¶
Source: Caribbean Tourism Organization—information from the year 2010.
Source: Caribbean Tourism Organization—information from the year 2009.
∗∗
Source: Oficina Nacional de la Estadistica de Republica Dominicana—information from the year 2011.
J Travel Med 2013; 20: 283–288
West Indies MRSA Clones: Do They Travel With Their Hosts?
assignment by microarray): CC5, CC8, CC59, and
CC80. Within these CCs, there were 13 diverse and
well-described clones or subclones (Table 2). These
clones were either healthcare-associated [Lyon clone
(n = 35), pediatric clone (n = 5), Brazilian clone (n = 5),
and New York/Japan clone (n = 2)] or communityassociated [ST8-MRSA-IV corresponding to PVLpositive (+) USA300 clone (n = 9) and its arginine
catabolic mobile element (ACME)-negative variant
(n = 1), the European PVL+ ST80 clone (n = 7)] or
both healthcare- and community-associated clones,
such as the Geraldine clone (n = 11). Four other
clones have also been identified: the UK-EMRSA14, a CC8-MRSA-IV clone (n = 5), the WA-MRSA62, a PVL+ CC8-MRSA-IV clone (n = 2), the PVLnegative ST72-MRSA-IV (USA700) clone (n = 2), and
the ST59-MRSA-V clone (n = 1).
Of the 10 infections that were classified as being
community-associated, 3 were caused by a MRSA strain
belonging to the European ST80 clone, 2 others
to the American epidemic ST8-MRSA-IV USA300
PVL+ clone, and another to the ACME-negative
variant of this American epidemic strain. Of the four
remaining clones, one was classified as the Lyon clone
and one as the Geraldine clone, whereas two strains
could not be assigned to a definite clone by the software
(an agrI/CC8 strain and an agrII/CC5 strain) (Table 2).
spa typing separated the 84 MRSA strains into 18
different spa types, and 1 strain was not able to be
typed by this method [a CC8-MRSA-IV PVL+ (WA
MRSA-62) strain from Tobago] (Table 2). Seventy-four
of the strains clustered into three spa-CCs (spaCC
002, spaCC008, and spaCC044) and a fourth was
clustered with no founder. Ten strains were classified
as singletons.
Discussion
In this study, the characterization of MRSA isolates
from the French West Indies revealed that the most
frequently isolated clones were identical to those that
had been isolated from mainland France in 2006
to 200714 and previously mainly described in that
country.13 Two French clones were specifically isolated
in the French islands: the Lyon clone (35 strains) and the
Geraldine clone (11 strains), whereas 8 of the 13 strains
collected from the other islands (Trinidad, Tobago,
and Jamaica) were identified as belonging to a clone
distributed worldwide, specifically the Brazilian (n = 5),
New York/Japan (n = 2), and pediatric (n = 1) clones.
The major MRSA clones spreading in France were
reported by Dauwalder and colleagues in 2008: the
Lyon clone (a hospital-associated ST8-MRSA-IV clone)
accounted for 69.4% of the isolates, the Geraldine clone
(ST5-MRSA-I truncated) for 6.3% of the isolates, the
classical pediatric clone (ST5-MRSA-IV) for 8.1% of
the isolates, the new pediatric clone (ST5-MRSA-VI)
for 7.2% of the isolates, and the community-associated
European ST80 clone (ST80-MRSA-IV) for 3.6% of
285
the isolates.14 All of these clones were detected in the
French West Indies, except for the new pediatric clone.
The classical description of the Lyon clone in the
literature almost exclusively reports that spa t008 is
its corresponding spa type (not t304, as found in this
study).14 This t304 spa type was also detected in five
strains of the CC8-MRSA-IV UK-EMRSA-14 clone,
which exhibits high homology with the Lyon clone.
In the literature, there are few articles reporting
the molecular characteristics of MRSA isolated either
from outpatients from Martinique and the Dominican
Republic9 or from Trinidad and Tobago.7,8 Among the
MRSA isolates from the Dominican Republic, ST30,
ST5, and ST72 predominated9 ; we did not detect any
strains of ST30 or ST72. Among the MRSA isolates
from Trinidad and Tobago, the ST239-MRSA-III clone
represented 76 of 80 isolates8 ; in our study, this clone
was detected only in Trinidad and Tobago. The few
strains from Jamaica (three isolates) were either the
USA300 clone (n = 1) or the New York–Japan clone
(n = 2), which was not detected on any other island. Note
that the USA300 clone was detected in Martinique,
Trinidad and Tobago, and Jamaica.
The relationship between human travel and the
geographic dissemination of S aureus has been reported
several times; international travel has been shown to
contribute to the spread of S aureus clones.15 Most of the
published studies have described the epidemiology of
PVL+ strains [MRSA more than methicillin-susceptible
S aureus (MSSA)]. For instance, previous studies have
made the following observations: (1) importation of
MRSA and MSSA through immigration to Denmark16
and Ireland17 ; (2) transmission of the Queensland CAMRSA ST93 clone from Australia to England18 ; and (3)
imported cases of SSTI, including cases of PVL+ MSSA
skin infections in France,19,20 with further transmission
to close contacts.19 Most of these studies have described
the importation of strains from tropical or subtropical
regions.19 – 26 Zanger and colleagues demonstrated that
the genotypes of the PVL+ S aureus clones detected in
returnees from tropical and subtropical regions were
endemic to the visited destinations.26 Stenhem and
colleagues described imported cases of PVL− S aureus
in Sweden between 2000 and 2003; the major part
of this study concerned foreign healthcare-acquired
infections.27 After studying MSSA strains from New
York and the Dominican Republic, Bhat and colleagues
demonstrated a strong correlation between the two
populations by PFGE (with a high frequency of ST398
MSSA), arguing for an ‘‘air-bridge link’’ between the
two sites.28
In light of the characteristics of international tourism
(Table 1), it appears that there is a clear difference
between the French islands (where the tourism that
is almost exclusively of French origin could have
contributed to the strong prevalence of French- and
European-specific clones) and Jamaica and Trinidad
and Tobago (where a much more mixed tourism may
have contributed to the dissemination of clones that have
J Travel Med 2013; 20: 283–288
J Travel Med 2013; 20: 283–288
CC80-MRSA-IV [PVL⇓], European CAMRSA clone∗
CC5-MRSA-IV pediatric clone PVL⇓ subclone
CC5-MRSA-IV, pediatric clone [sed/j/r-posit. subclone]
ST5/ST225-MRSA-II, New York–Japan clone,
EMRSA/UK-EMRSA-3
ST5-MRSA-I, Geraldine clone
ST59-MRSA-V
ST72-MRSA-IV, USA700
ST239-MRSA-III, Vienna/Hungarian/Brazilian clone
WA-MRSA-62 PVL⇓
ST8-MRSA-IV, ACME-NEGATIVE variant of
USA300
ST8-MRSA-IV, USA300
CC8-MRSA-IV, UK-EMRSA-14/WA MRSA-5
CC8-MRSA-IV, Lyon clone/UK-EMRSA-2
Microarrays assignment
008
008
Sgl
Sgl
008
008
008
008
008
008
008
NT
S gl
nf
nf
Sgl
002
002
002
002
Sgl
002
044
044
044
t008
NT
t037
t148
t3682
t216
t002
t2164
t002
t067
t688
t002
t044
t434
t376
spa CC
t304
t648
t3878
t334
t304
t008
t197
t681
t211
t008
spa types
3
2
2
2
2
1
1
1
1
1
1
1
1
1
agr
4
2
1
1
3
1
9
1
1
1
31
1
2
1
5
4
1
Martinique,
n = 69
1
1
1
Guadeloupe,
n= 3
1
3
1
Trinidad,
n= 5
1
2
2
Tobago,
n= 5
2
1
Jamaica,
n= 3
7
1
4
2
11
1
2
5
2
1
9
5
35
Total,
n = 85
Europe
UK, France, Australia, Switzerland,
Senegal, Ireland
Worldwide
Worldwide
France
Worldwide
Worldwide
Germany, United Arab Emirates
Australia
Europe
USA
Europe
France
Previous main
geographical description
Distribution of the different isolates among the five studied islands of West Indies correlated with spa typing and strain assignment by the microarray software
The last column summarizes the main previously described locations (from Monecke and colleagues13 ). The clones colored in light gray were found only in the French islands, and those colored in dark gray only in Trinidad and Tobago
and the Jamaican islands. The other clones were found in the French islands, Trinidad and Tobago, and Jamaica.
Sgl = singletons; nf = no founder; NT = not able to be typed; CC = clonal complex; PVL+ = Panton and Valentine leukocidin-positive strains.
∗
Described in the text as the European ST80 clone.
CC80
CC59
CC5
CC8
Table 2
286
Chroboczek et al.
287
West Indies MRSA Clones: Do They Travel With Their Hosts?
worldwide distribution). Nevertheless, there are other
potential explanations for this difference, and tourism
might only be one of several potential contributing
factors. Differing medical practices, especially different
antibiotic strategies, could be another major factor.
Indeed, it has been established that the increase in HAMRSA infections reflects the growing impact of medical
interventions, resulting in the selection and spread of
a limited number of clones.29,30 In our study, HAMRSA strains represented the majority of isolates in
Martinique (85%). Unfortunately, information could
not be recovered for all of the patients from the
other islands. Thus, additional risk factors (such as
old age, comorbidities for HA-MRSA acquisition,
or belonging to a particular community likely to
acquire CA-MRSA29 ) were not available to support
this hypothesis. Another question is related to the
discriminative efficiency of the genotyping tool used
to define the different MRSA clones and whether
this tool is well adapted for identifying these clones.
By identifying discrepancies in the results of different
typing methods of 135 ST5 MSSA and MRSA isolates,
Nubel and colleagues hypothesized that MRSA could
have arisen on multiple independent occasions31 (and is
not the result of the global spread of a small number
of strains with acquired resistance capacities, as is
usually argued regarding HA-MRSA32 ). In our study,
we chose to use both spa typing and DNA microarrays,
which we believe to be complementary: spa typing
is a well-validated method that has an intermediate
discriminatory power33 and has been shown to be useful
in characterizing the global genetic evolution of an S
aureus population.34 A DNA microarray allows for the
rapid identification of a large number of genes11 and the
extrapolation of the ST of the studied strains.11
We established the presence of several MRSA
clones from different Caribbean islands in light of
their previous geographic descriptions (Table 2). We
hypothesized that a link could exist between the
presence of these clones and touristic migrations, but
we did not explore the dynamics of their dissemination.
The comparison of the strains from the French West
Indies to strains collected in mainland France and the
demonstration that these strains belong to the same
clones using phylogenic hierarchization (by spa typing
for instance) could provide information on the evolution
dynamic of MRSA over time.
The limitations of our study resulted from its design,
which caused a non-negligible selection bias. Strains
were collected from Martinique between 2004 and 2011,
whereas strains from the other islands were collected
in 2010 and 2011 only; although we gathered a larger
number of strains from Martinique, we managed to
recover only a few strains from the other islands. Hence,
there is a bias in the timing of the strain collection when
comparing the results of the isolates from Martinique
with those from other islands, as the epidemiology could
have changed during this time. Another bias is owing
to the lack of information concerning the hospital or
community acquisition of the strains, which limited the
exploitation of the results. Similarly, only limited clinical
information was obtained from the microbiologists who
provided the strains. In particular, the proportion of
HA-MRSA in the population collected in 2010 and
2011 was not known. However, as the selection of the
strains was performed according to the same procedure,
we consider the populations to be comparable.
Acknowledgments
We are fully indebted to the physicians and
microbiologists who participated in this study. We also
wish to thank Christine Gardon, Christine Courtier,
Caroline Bouveyron, and Virginie Dumoulin for
excellent technical assistance.
Declaration of Interests
The authors state that they have no conflicts of interest.
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