Detection of diverse genotypes of Methicillin-resistant Staphylococcus aureus from hospital personnel and the environment in Armenia
Mkrtchyan et al. Antimicrobial Resistance and Infection Control
Detection of diverse genotypes of Methicillin-resistant Staphylococcus aureus from hospital personnel and the environment in Armenia
Hermine V. Mkrtchyan 0 1
Zhen Xu 1
Maria Yacoub 2
Mary M. Ter-Stepanyan 3
Hayk D. Karapetyan 3
Angela M. Kearns 2
Ronald R. Cutler 1
Bruno Pichon 2
Armen Dz Hambardzumyan 3
0 School of Health , Sport and Bioscience , University of East London , Water Lane, London E15 4LZ , UK
1 Queen Mary University of London, School of Biological and Chemical Sciences , Mile End Road, London E1 4NS , UK
2 Antimicrobial Resistance and Healthcare Associated Infections Reference Unit, Public Health England, National Infection Service , Colindale, London , UK
3 Yerevan State Medical University , Yerevan , Armenia
Background: Methicillin-resistant Staphylococcus aureus (MRSA) is a public health concern internationally. Studies examining a range of cohorts have been reported from various regions of the world, but little is known about the molecular epidemiology of MRSA in Armenia. Methods: Between May and September 2013, twenty isolates of methicillin-resistant Staphylococcus aureus (MRSA; mecA positive) were recovered from hospital personnel (n = 10; 9 females, 1 male) and environmental sites (n = 10) in the maternity ward of one of the teaching hospitals in Armenia. Results: Multi-locus sequence type clonal complex (MLST-CC) assignments inferred from spa typing data revealed the majority belonged to 3 pandemic lineages of MRSA including: t008-CC8-SCCmecV (n = 10; 7 from personnel); t021-CC30-SCCmecIV (n = 5; all environmental); and t1523-CC45 (n = 2; 1 from personnel), one harboured SCCmecV the other was SCCmec non-typable. The remainder identified as belonging to genotype t364-CC182, both of which harboured a novel SCCmec cassette with kdp, rif5, ccrB2 and ccrC detected by PCR (both from personnel); and t325-CC88-SCCmecIV (n = 1; environmental). All MRSA were negative for the Panton-Valentine Leukocidin (PVL) locus and three CC8 strains were positive for the arginine catabolic element (ACME). Conclusions: In this small study, we report for the first time of the occurrence of diverse MRSA genotypes belonging to both pandemic and more sporadic international clones in Armenia harbouring the smaller SCCmec types and/or ACME, both of which have been associated with strain fitness. Further surveillance is warranted to better understand the prevalence, clinical and molecular epidemiology of MRSA throughout Armenia.
MRSA; SCCmec; ACME; Pandemic; Maternity ward
Methicillin-resistant Staphylococcus aureus (MRSA) is a
major pathogen responsible for a wide range of mild to
life threatening infections and is estimated to affect
more than 150,000 patients annually in the European
Union with associated costs of EUR 380 million to
healthcare settings .
Reports of MRSA from an expanding range of
ecological niches (healthcare, community, livestock, wildlife,
environmental sources, etc.) are a public health concern
internationally. Diversity in MRSA genotypes and their
prevalence in different geographic areas continue to
increase [2–5]. Studies examining a broad range of cohorts
have been reported from various regions of the world
[6–9], but little is known of the situation in some areas.
Although MRSA clones from some countries have been
well characterized [8, 10], there are few published studies
describing the situation in the former USSR (Russia,
Georgia), and none from Armenia [11–13].
© The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0
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The Republic of Armenia (part of the former Soviet
Union) has three million inhabitants, half of whom live
in the capital of Yerevan. Armenia is a low-middle
income country and, currently, no population surveillance
is being carried out in patients entering the hospital with
the symptoms of illness compatible with staphylococcal
disease. In this study, we report for the first time the
molecular characterisation of MRSA recovered from
hospital personnel and the environment in a University
teaching hospital in the Republic of Armenia (part of the
former Soviet Union). These data provide evidence for
the first time of the occurrence of pandemic and more
sporadic international MRSA clones in Armenia that
harbour the smaller SCCmec types generally associated
with strain fitness.
As part of a pilot surveillance study to assess the
distribution and prevalence of MRSA, 450 samples were taken
from hospital personnel (n = 150) and environmental sites
(n = 300) in the maternity ward of one of the teaching
hospitals in Armenia between May 2013 and September
2013. For hospital-based personnel (doctors, nurses and
theatre nurses), samples were taken from the nasal cavity.
Environmental sites included taps, patient examination
chairs, surgical tables, nurse laboratory coats, baby scales,
door handles and telephones. All specimens were
inoculated onto nutrient agar (Oxoid, Basingstoke, UK) and
incubated aerobically at 37 °C for 24-48 hours.
Identification of the bacterial isolates
Suspected S. aureus were initially identified using
conventional methods, including growth on Mannitol Salt Agar
(Oxoid Ltd, Basingstoke, UK), slide coagulase and latex
agglutination testing (ProLab Diagnostics, Neston, UK). To
identify possible MRSA, isolates were sub-cultured onto
Chromogenic MRSA agar (Oxoid Ltd, Basingstoke, UK).
Those which grew yielding characteristic blue colonies were
identified further by penicillin-binding protein (PBP2')
agglutination testing (Oxoid Ltd, Basingstoke, UK).
Phenotypic and genotypic characterisation of MRSA
Presumptive MRSA were screened for susceptibility to 4
antimicrobial agents (penicillin, cefoxitin, erythromycin
and gentamicin) by disk diffusion and assigned as
susceptible, intermediate or resistant according to the
recommendations of the Clinical and Laboratory Standard
Institute (CLSI) .
Isolates were characterised by real-time PCR to confirm
they were S. aureus (nuc positive) and to determine their
mecA, mecC and luk-PV status, as described previously
. MRSA were characterised further by spa typing ,
and staphylococcal chromosomal cassette mec (SCCmec)
typing . Spa typing data were used to infer multi-locus
sequence type clonal complex (MLST-CC) assignments by
reference to the spa server (http://spa.ridom.de/mlst.shtml),
MLST (http://saureus.mlst.net) and in-house (Public Health
England) databases. All CC8 MRSA were screened by PCR
for the presence of the ACME element .
Over a 5 month period (May – September 2013), S. aureus
was recovered from a total of 65 samples including 32 of
150 (21.3%) hospital personnel and 33 of 300 (11%)
environmental sites in the maternity ward of one of the teaching
hospitals in Armenia. Twenty (30.8%) S. aureus identified
as MRSA. Half of these (n = 10) were recovered from
hospital personnel including 9 females and one male; the
remainder were recovered from the environment (Table 1).
All MRSA were nuc and mecA positive; no mecC-MRSA
were identified. All were resistant to β-lactams (penicillin
and cefoxitin); three were also resistant to erythromycin
and six showed intermediate resistance (zone sizes
2022 mm); in addition, one MRSA showed intermediate
resistance to gentamicin (zone size 14 mm) (Table 1).
Most (17; 85%) study isolates belonged to pandemic
genotypes of MRSA (Table 1), specifically:
t008-CC8SCCmecV (n = 10); t021-CC30-SCCmecIV (n = 5);
t1523CC45, one of which harboured SCCmecV, the other was
SCCmec non-typable. The remainder belonged to more
sporadic international lineages including
t364-CC182harbouring a novel SCCmec cassette with kdp, rif5, ccrB2
and ccrC detected by PCR (n = 2); and
t325-CC88SCCmecIV (n = 1). All MRSA were PVL negative; three
CC8 strains were ACME positive (Table 1).
The spread of antimicrobial resistant clones such as
MRSA not only in healthcare and community settings but
also livestock and companion animals is a major public
health concern world-wide. In developing countries, the
broader public health impact is worrisome due to the
extensive and uncontrolled use of antimicrobial agents .
The aim of this study was to evaluate the clonal diversity,
virulence and antibiotic susceptibility profiles of MRSA
recovered from personnel and the environment in a
University teaching hospital in the Republic of Armenia.
Twenty (30.8%) out of 65 S. aureus isolates recovered
in this study were identified as MRSA. Various MRSA
clones have been described globally, including some
from the post-soviet countries [11–13, 19–21], however,
little is known about MRSA in Armenia. The
international ST239 clone has been reported as being
dominant in Krasnoyarsk, Vladivostock and Georgia [11–13].
During the course of this small scale study we did not
find evidence of this clone. Nevertheless, other
international lineages were identified and a marked genetic
Table 1 Susceptibility profiles and molecular characterisation of MRSA recovered from hospital personnel and environmental sites in
the maternity wards of one of the teaching hospitals in Armenia
P personnel, E environment, PG penicillin, FOX cefoxitin, GM gentamicin, ERY erythromycin, Spa staphylococcal protein A, MLST-CC Multi-locus sequence type clonal
complex, SCCmec staphylococcal cassette chromosome mec, ACME arginine catabolic mobile element, ND not determined, + positive, - negative, all isolates were
nuc and mecA positive, and luk-PV negative
aSingletons that do not fall into a clonal complex (CC) described in the S. aureus database (Skramm et al., 2007)
bkdp, rif5, ccrB2 and ccrC detected by PCR
R resistant, S susceptible, aI intermediate resistance. Zone sizes for intermediate resistance were aERY 20-22 mm; aGen 14 mm (Cockerill FR, )
diversity was apparent. The CC8-V lineage was
predominant (n = 10; 50%) and was identified in both human and
environmental sources. Three of 10 CC8-V isolates were
recovered from the hospital personnel, the remainder
were from the environment, which may reflect
crosscontamination between personnel and the environment
(Table 1). All CC8-V isolates were resistant to penicillin
and cefoxitin; four also showed non-susceptibility to
erythromycin. Distinct from the pandemic CC8-IV MRSA
lineage associated with both healthcare- and
communityassociated infections [22, 23], CC8-V MRSA have been
reported more sporadically . In contrast to most
reports of CC8-MRSA from various regions of the
world (including Russia and Europe) that encode
SCCmecIV [13, 25–29], all CC8 isolates in our study
encoded SCCmecV and 3 of 10 were ACME positive.
Aside from the successful USA300 (CC8-IV) clone of
CA-MRSA in North America, the ACME element has
been identified in a limited number of MRSA genotypes
including ST5-II, ST59-IV, ST97-V, ST1-IV, ST5-IV and
ST239-III [23, 30]. Interestingly, CC8-V has been found
sporadically in Australia and Africa  but, to our
knowledge, this is the first report of ACME in this
lineage. Of note, the first case of CA-MRSA
infection in Portugal caused by an ST8, spa type t008
strain was recovered from a male of Armenian
ethnicity . However, the isolate encoded SCCmecIV
which differs from the CC8-V isolates identified in this
The second most common lineage identified was
CC30IV. CC30 is a widely disseminated pandemic clone, that
has been associated with HA-MRSA, CA-MRSA and
LAMRSA . In this study all (n = 5) CC30-IV isolates were
recovered from the environment (Table 1). Whilst the
pandemic HA-MRSA lineage encodes SCCmecII (ST36-II;
UK EMRSA-16 clone), PVL-negative CC30-IV MRSA
strains have been reported in countries such as Ireland
 and Australia .
Two isolates belonged to CC45, spa type t1523 one
with SCCmecV, the other was SCCmec non-typable. CC45
has is predominantly been associated with SCCmec type
IV, which is also known as Berlin Epidemic strain or USA
600 . However, CC45-MRSA-V strains have been
reported in Germany, Australia and Portugal [32, 34]. Two
isolates belonged to CC182; this clonal complex has been
reported as a singleton  and MRSA belonging to
CC182 have occasionally been identified in the UK and
the Netherlands (http://spa.ridom.de/index.shtml).
In the current study we also identified a single CC88-IV
strain. The CC88 lineage is prevalent among MRSA isolates
from Africa  but has also been reported in Australia,
Germany  the Netherlands, Portugal, Angola and Japan
. Interestingly, CC45-t1523 isolates (n = 2) were
recovered from both hospital personnel and the environment,
whereas CC182-t364 were isolated from the personnel only
and CC88-t325 were identified from the environment only
(Table 1). All 20 MRSA in our study were PVL-negative.
This is consistent with the observations of other workers
that PVL-positive MRSA is less prevalent in Europe than in
the USA [32, 37]. As there are large Armenian
communities in the US, Europe and Russia with relevant
family links in Armenia it seems plausible that these
clones were imported into Armenia from abroad in
parallel with exchange of mobile genetic elements
within the staphylococcal gene pool such as SCCmec
There are clear limitations in this small scale study.
Clinical and epidemiological data were lacking; it is
unclear whether any of the isolates may have been
outbreak related or there were underlying risk factors
such as previous healthcare contact or travel abroad.
Similarly, we do not know if any isolates were multiply
resistant as only a limited range of susceptibilities
were determined. Nevertheless, this study provides
insights into a previously unrecognised diversity of
MRSA clones in Armenia including pandemic and
more sporadic lineages seen internationally. These data
also provide evidence that MRSA with a community-like
genotype may be infiltrating healthcare settings in this
country. In low and middle income countries
healthcareand community-associated infections are more
challenging due to the lack of effective antimicrobial stewardship
allied to infection control and prevention programmes
. Currently, no MRSA infection control programme
exists in Armenia and no formal surveillance is being
carried out in patients admitted to hospital with recognised
risk factors, signs or symptoms compatible with MRSA/
staphylococcal disease. Additional studies are warranted
to further our understanding of the prevalence and
molecular epidemiology of MRSA in healthcare settings
in Armenia. In particular, we plan a more structured
surveillance study of patients and hospital personnel
with more detailed analyses to further our
understanding of possible risk factors, burden of disease,
genetic diversity and antimicrobial resistance rates to
help inform national policy.
ACME: Arginine catabolic mobile element; CLSI: Clinical and Laboratory
Standard Institute; ERY: Erythromycin; FOX: Cefoxitin; GM: Gentamicin;
MLST-CC: Multi-locus sequence type clonal complex; MRSA:
Methicillinresistant Staphylococcus aureus; PG: Penicillin; PVL: Panton-Valentine
Leukocidin; SCCmec: Staphylococcal cassette chromosome mec
HVM study design, laboratory work, data analysis, manuscript preparation; ZX
laboratory work, manuscript preparation; MY laboratory work; MMTS laboratory
work; HDK laboratory work; AMK data analysis, manuscript preparation; RRC
study design; BP data analysis, manuscript preparation; ADH study design,
laboratory work. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
Consent for publication
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