Highlights
- •This article describes a methicillin-resistant Staphylococcus aureus (MRSA) isolate from Riyadh, Kingdom of Saudi Arabia, which was originally thought to belong to the pandemic UK-EMRSA-15/Barnim epidemic strain.
- •More detailed characterization showed it to harbour a different SCCmec element.
- •Further investigations on CC22 MRSA strains showed a parallel presence of as many as six distinct CC22 MRSA strains in the Arabian Gulf region.
- •However, the original UK-EMRSA-15/Barnim epidemic strain, sensu strictu, was not found in the Kingdom of Saudi Arabia. It was identified in other countries in this region.
Summary
Objectives
CC22-MRSA-IV, UK-EMRSA-15/Barnim EMRSA, is a common and pandemic strain of methicillin-resistant Staphylococcus aureus (MRSA) that has been found mainly in Western Europe, but also in other parts of the world including some Gulf countries. One suspected case of an infection with this strain in a patient who was admitted to the surgical unit in Riyadh, Kingdom of Saudi Arabia (KSA) was investigated in order to check whether this strain has reached KSA.
Methods
Besides the index isolate, 46 additional isolates of CC22-MRSA-IV from patients from KSA, Abu Dhabi, Kuwait, and Germany (patients with a history of travel in the Middle East), were characterized by microarray hybridization.
Results
The study revealed a regional presence of as many as six distinct ‘strains’ of CC22-MRSA-IV that could be distinguished based on carriage of SCCmec IV subtypes and virulence factors. No true UK-EMRSA-15/Barnim EMRSA was identified in Riyadh; all suspected isolates from Riyadh were assigned to other, albeit related strains. However, this strain was identified in Abu Dhabi and Kuwait.
Conclusions
CC22-MRSA-IV from KSA could be linked to other epidemic strains from the Middle East and possibly India, rather than to the Western European UK-EMRSA-15/Barnim EMRSA. High-resolution typing methods, including SCCmec subtyping, might help to differentiate related epidemic strains and to monitor routes of transmission.
Keywords
1. Introduction
Epidemic methicillin-resistant Staphylococcus aureus (EMRSA)-15 (CC22-MRSA-IV) was first identified in the UK in the early 1990s and has become the most prevalent hospital-acquired strain of methicillin-resistant Staphylococcus aureus (MRSA) in the UK.
1
, 2
This pandemic MRSA strain has also been reported from many other regions of the world, including Ireland, Germany (where it is called ‘Barnim EMRSA’ after the county in which it was first found), Denmark, Belgium, Spain, Portugal, Malta, Sweden, Singapore, Australia, New Zealand, Qatar, and Kuwait.1
, 3
, 4
, 5
, 6
, 7
, 8
, 9
, 10
, 11
, 12
, 13
, - Murchan S.
- Kaufmann M.E.
- Deplano A.
- de Ryck R.
- Struelens M.
- Zinn C.E.
- et al.
Harmonization of pulsed-field gel electrophoresis protocols for epidemiological typing of strains of methicillin-resistant Staphylococcus aureus: a single approach developed by consensus in 10 European laboratories and its application for tracing the spread of related strains.
J Clin Microbiol. 2003; 41: 1574-1585
14
, 15
, 16
, 17
, 18
, 19
, 20
, 21
CC22-MRSA-IV that differ in harbouring tst1 (encoding toxic shock toxin) have been reported from the Gaza Strip, Jordan, the United Arab Emirates (UAE), the Kingdom of Saudi Arabia (KSA), Kuwait, the USA, and Italy.11
, 20
, 22
, 23
, 24
, 25
, 26
Furthermore, CC22-MRSA-IV harbouring the genes encoding the Panton–Valentine leukocidin (PVL) have frequently been observed in the Middle East,5
, 11
, 27
Iran,28
and India,29
, 30
, 31
and also in sporadic cases32
and localized outbreaks- Rossney A.S.
- Shore A.C.
- Morgan P.M.
- Fitzgibbon M.M.
- O’Connell B.
- Coleman D.C.
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. 2007; 45: 2554-2563
33
in other regions, such as Western Europe.In this report, the characteristics of CC22-MRSA-IV causing an infection in a patient who presented to the surgical unit of King Khalid University Hospital (KKUH) in Riyadh, KSA, are presented. Furthermore, the molecular typing of CC22-MRSA-IV isolated in the Arabian Gulf region and from patients from Germany with a history of previous travel to the Middle East is discussed.
2. Materials and methods
2.1 Case history
A middle-aged male patient presented to the surgical unit of KKUH with a history of intermittent fever and peri-umbilical pain, with an associated peri-umbilical discharge of 2-week duration. The patient gave a history of travel to Egypt (including healthcare exposure) and of two previous surgical interventions at different hospitals during the last few years. The first one was a gastric by-pass procedure; the second one an abdominal herniorrhaphy with mesh implant. He received antibiotics, but neither details of the antibiotic therapy nor information on the laboratory investigations were available. There was no history of any chronic illness apart from the presenting complaints. No family members were documented to have recurrent skin or soft tissue infections.
On admission, the patient had stable vital signs. Physical examination revealed an anterior abdominal wall scar running from the xiphoid process to the umbilicus and a discharging wound in the umbilical area. There was associated tenderness in the para-umbilical and left hypogastric areas. Investigations carried out at presentation included an abdominal computed tomography scan, which was significant for thickening of the anterior abdominal wall with minimal subcutaneous collection. A culture of the wound swab collected at presentation yielded a mixed growth of Klebsiella pneumoniae, which was sensitive to all tested antibiotics, and MRSA, which was resistant to penicillin, ampicillin, and imipenem but susceptible to gentamicin, ciprofloxacin, erythromycin, rifampicin, trimethoprim/sulfamethoxazole, tetracycline, and vancomycin. The patient underwent wound debridement with partial mesh removal and drainage a day after presentation, and the postoperative period was uneventful. He was discharged 3 days after presentation on a combination of clindamycin (450 mg, 8-hourly) and ciprofloxacin (750 mg, 12-hourly). At the 2-week follow-up visit, the patient's wound had healed completely.
2.2 Additional isolates
Additional isolates were included for comparison. All had previously been identified as CC22-MRSA-IV using the StaphyType DNA microarray (see below). These included isolates with hybridization profiles consistent with UK-EMRSA-15/Barnim EMRSA, as well as some randomly selected PVL- or tst1-positive CC22-MRSA-IV strains. These isolates originated from Riyadh (KSA; five isolates sampled in 2014 and 13 sampled in 2010/11), Abu Dhabi (UAE; n = 16 sampled in 2009/10), and Kuwait (n = 6; 2013), as well as from Germany. The German isolates included some local UK-EMRSA-15/Barnim EMRSA isolates (n = 4; 2015/16) and some PVL- or tst1-positive CC22-MRSA-IV from patients with a history of recent travel in the Middle East (n = 3; 2014–2016).
2.3 Array procedures
Molecular characterization of the MRSA isolate from the index case was performed as part of a wider study in which archived MRSA isolates from KKUH were characterized using the StaphyType DNA microarray (Alere Technologies GmbH, Jena, Germany). Probes, primers, and procedures have been described previously in detail,
11
, 34
and protocols are provided by the manufacturer.Additional probes and primers were used in order to discern SCCmec subtypes and CC22 strains (Table 1). Amplification and hybridization protocols were identical to those described previously.
11
, 34
Table 1Markers used for subtyping of CC22-MRSA-IV
| Gene | Gene product/function | Probe(s) | Primer(s) |
|---|---|---|---|
| agr groups I–IV, capsule type 5 and 8 | agr- and capsule-specific probes (agr I and capsule type 8 alleles present in CC22) | 11 , 34 | 11 , 34 |
| mecA | Modified penicillin binding protein (PBP2a) causing oxacillin/methicillin resistance and thus defining MRSA | 11 , 34 | 11 , 34 |
| ccrA/B-2 | Cassette chromosome recombinase A allele found in SCCmec II and IV elements | 11 , 34 | 11 , 34 |
| mvaS-SCC | Truncated 3-hydroxy-3-methylglutaryl CoA synthase, variably present in SCCmec I, II, IV, V | BA000033.2 [37280:37304] and BA000033.2 [37432:37460] | BA000033.2 [37307:37326:r] and BA000033.2 [37488:37510:r] |
| cstB-scc2 (IVa) | CsoR-like sulfur transferase-regulated genes B/metallo-beta-lactamase superfamily protein (truncated); present in SCCmec X, variably present in SCCmec I and IV; marker for IVa | CP000046.1 [54284:54313:r] and CP000046.1 [53882:53910:r] | CP000029.1 [2492569:2492590:r] and CP000046.1 [53836:53854] |
| B2Y834 | Abortive phage resistance protein used for identification of SCCmec IV A, G, c and SCCmec MRSAZH47 | AE015929.1 [51095:51119] | AE015929.1 [51124:51144:r] |
| B6VQU0 | Putative protein used for identification of SCCmec IVh/j | AB425824.1 [20412:20443] | AB425824.1 [20498:20525:r] |
| Q93IB71 | LytTR domain DNA-binding regulator present in some SCCmec III elements and in IVa from CMFT503 GenBank HF569113.1 | FN433596.1 [434532:434550] | FN433596.1 [68041:68058] |
| Q9XB68-dcs | Located at the terminus of SCCmec directly next to orfX, comprises the downstream constant segment (dcs) that includes a copy of the SCC direct repeat DR_SCC (AGAAGCTTATCATAAGTAA) | 11 , 34 | 11 , 34 |
| SCCmec Terminus 1 | SCC integration site alternate to dcs | GU235983.1 [568:594] | FN433596.1 [67354:67380:r] |
| SCCmec Terminus 5 | SCC integration site alternate to dcs | AB425427.1 [754:779] | AB425427.1 [800:824:r] |
| erm(C) | rRNA adenine N-6-methyltransferase macrolide–lincosamide–streptogramin B resistance protein | 11 , 34 | 11 , 34 |
| aacA-aphD | Bifunctional enzyme Aac/Aph, 6′-aminoglycoside N-acetyltransferase/2′′-aminoglycoside phosphotransferase; gentamicin and tobramycin resistance | 11 , 34 | 11 , 34 |
| aadD | Aminoglycoside adenyltransferase, tobramycin resistance | 11 , 34 | 11 , 34 |
| dfrA | Dihydrofolate reductase, mediates trimethoprim resistance | 11 , 34 | 11 , 34 |
| lukF/S-PV | Panton–Valentine leukocidin | 11 , 34 | 11 , 34 |
| tst1 | Toxic shock syndrome toxin | 11 , 34 | 11 , 34 |
| sec+sel | Enterotoxins C and L | 11 , 34 | 11 , 34 |
| egc cluster | Enterotoxin gene cluster (comprising seg, sei sem, sen, seo, seu) | 11 , 34 | 11 , 34 |
| sak, chp, scn | Staphylokinase, chemotaxis-inhibiting protein, staphyl. complement inhibitor | 11 , 34 | 11 , 34 |
| eta, etb, etd | Exfoliative toxins | 11 , 34 | 11 , 34 |
| ACME | Arginine catabolic mobile element | 11 , 34 | 11 , 34 |
| fnbB | Fibronectin binding protein B, variably detected in CC22 because it is in some strains fused with fnbA | 11 , 34 | 11 , 34 |
| cna, sasG | Collagen adhesin; Staphylococcus aureus surface protein G (present in CC22) | 11 , 34 | 11 , 34 |
3. Results
The recovered isolate harboured the accessory gene regulator (agrI) and capsular genes type 5 (cap5), as well as genes for collagen adhesin (cna), Staphylococcus aureus surface protein G (sasG), and the egc cluster. This was in accordance with previously characterized CC22 isolates and strains.
11
, 34
Furthermore, it harboured mecA as part of an SCCmec IV element. It lacked the genes encoding fibronectin-binding protein B (fnbB), exfoliative toxin (etA, etB, and etD), toxic shock toxin (tst), and PVL, as well as the arginine catabolic mobile element (ACME). Based on this profile, the isolate was preliminarily regarded as CC22-MRSA-IV, UK-EMRSA-15/Barnim EMRSA. Staphylokinase (sak), chemotaxis-inhibiting protein (chp), and Staphylococcus complement inhibitor (scn) genes were present, and enterotoxin C and L genes (sec and sel) were absent.SCCmec subtyping using new probes revealed that this isolate differed in SCCmec subtype from Western European UK-EMRSA-15/Barnim EMRSA isolates (that harbour SCCmec IV h/j) in the carriage of an SCCmec element of subtype IVa. The hybridization pattern of the actual isolate (Table 2) matched the computed/predicted pattern for the sequence of strain CMFT503, GenBank HF569113.1, yielding signals for mecA, ugpQ, delta mecR1, mvaS, cstB-SCC2, Q93IB7, ccrA/B-2, and ‘SCCterm 1’ (an intergenic region between orfX and the first codons of the SCC element that is alternative to dcs).
Table 2CC22-MRSA-IV strains and isolates
| Isolates | CC22-MRSA-IV with SCCmec IVa | UK-EMRSA-15/Barnim EMRSA with SCCmec IV h/j | CC22-MRSA-IV with unknown SCCmec IV h/j variant | tst1-positive ‘Gaza epidemic strain’ with SCCmec IVa | CC22-MRSA-IV with SCCmec IV b/d/i | PVL-positive CC22-MRSA-IV with SCCmec IVc |
|---|---|---|---|---|---|---|
| Index case from the case report and 3 others from Riyadh (2010/11) | 7 isolates from Abu Dhabi (2009/10), 2 from Kuwait (2013), and, for comparison, 4 from Dresden (locals; 2015/16) | 2 from Abu Dhabi (2009/10) | 2 isolates from Abu Dhabi (2009/10), 2 from Kuwait (2013), 2 from Riyadh (2014), 4 from Riyadh (2010/11), 2 from Dresden (with travel history; 2016) | 1 from Riyadh (2014), 1 from Abu Dhabi (2009/10), 1 from Kuwait (2013) | 4 from Abu Dhabi (2009/10), 1 from Kuwait (2013), 1 from Riyadh (2014), 6 from Riyadh (2010/11), 1 from Dresden (with travel history; 2014) | |
| mecA | Positive | Positive | Positive | Positive | Positive | Positive |
| ccrA/B-2 | Positive | Positive | Positive | Positive | Positive | Positive |
| mvaS-SCC | Positive | Positive | Positive | Positive | Positive | Negative |
| cstB-scc2 (IVa) | Positive | Negative | Positive | Positive | Negative | Negative |
| B2Y834 (IVc) | Negative | Negative | Negative | Negative | Negative | Positive |
| B6VQU0 (IV h/,j) | Negative | Positive | Positive | Negative | Negative | Negative |
| Q93IB71 | Positive | Negative | Negative | Positive | Negative | Negative |
| Q9XB68-dcs | Negative | Positive | Negative | Negative | Positive | Positive |
| SCCmec Terminus 1 | Positive | Negative | Negative | Positive | Negative | Negative |
| SCCmec Terminus 5 | Negative | Negative | Positive | Negative | Negative | Negative |
| erm(C) | Negative | Variable | Negative | Variable | Variable | Variable |
| aacA-aphD | Negative | Negative | Negative | Negative | Negative | Positive |
| aadD | Negative | Negative | Negative | Negative | Negative | Variable |
| dfrA | Negative | Negative | Negative | Negative | Negative | Variable |
| lukF/S-PV | Negative | Negative | Negative | Negative | Negative | Positive |
| tst1 | Negative | Negative | Negative | Positive | Negative | Negative |
| sec+sel | Negative | Variable | Negative | Negative | Positive | Negative |
| egc cluster | Positive | Positive | Positive | Positive | Positive | Positive |
| fnbB | Negative | Negative | Negative | Negative | Variable | Variable |
Based on this observation, a convenience sample of 46 additional isolates was selected and subtyped for comparison (see Materials and methods). When focusing on SCCmec IV subtypes as well as on the carriage of PVL and tst1 genes, these 46 isolates could be categorized into six distinct variants, or strains. Details are shown in Table 2. All Saudi isolates differed from the Western European UK-EMRSA-15/Barnim EMRSA CC22-MRSA-IV h/j. However, this strain was identified in Abu Dhabi (UAE) and Kuwait.
4. Discussion
The changing epidemiology of MRSA necessitates the continuous surveillance of patients. Well-documented hospital and community strains of MRSA in Saudi Arabia include ST239-MRSA-III, ST80-MRSA-IVc, and ST30-MRSA-IV.
27
In this report, the characteristics of a CC22-MRSA-IV (CC22-IV) isolate from a patient in Saudi Arabia are presented; this isolate was similar but not identical to the widely distributed UK-EMRSA-15/Barnim EMRSA. On investigating this case and other similar isolates from KSA and other regions, several different strains (or very distinct variants) of CC22-IV could be distinguished based on SCCmec IV subtypes and the carriage of clinically important toxin genes.
These included UK-EMRSA-15/Barnim EMRSA as described from Western Europe (see Introduction). These isolates have SCCmec IV h/j elements and do not carry tst1 or PVL genes, but frequently harbour enterotoxin C and L genes (sec and sel). Usually they are phenotypically resistant to ciprofloxacin, often also to erythromycin and clindamycin (mediated by erm(C)). Other resistance properties, however, are rather rare. This strain is also susceptible to weak lysis by phage 75.
1
Although some were superficially similar, not a single one of the 18 KSA isolates characterized herein could be assigned to UK-EMRSA-15/Barnim EMRSA, mainly because of the carriage of other SCCmec IV subtypes. Some isolates from Kuwait and Abu Dhabi matched this strain. Furthermore, two additional isolates from Abu Dhabi had an SCCmec IV variant element that has apparently not yet been described or sequenced.
Another related epidemic strain – ST22-MRSA-IVa – is usually reported to carry tst1 as well as SCCmec IVa. It is probably widely distributed in the Middle East and the Mediterranean, and is sometimes dubbed the ‘Gaza epidemic strain’.
11
, 20
, 22
, 23
, 24
, 25
, 27
Study isolates that could be assigned to this strain originated from KSA, Abu Dhabi, and Kuwait, or were isolated in Germany from patients with a history of travel to the Middle East.There were also tst1-negative isolates with SCCmec IVa elements. Previously observed UK-EMRSA-15/Barnim EMRSA-like isolates from KSA have belonged to this category,
27
as well as the isolate from the case described herein. It can be assumed that they might rather be tst1 deletion mutants of the Middle Eastern ‘Gaza epidemic strain’ than derived from imported European UK-EMRSA-15/Barnim EMRSA.Furthermore, three tst1-negative isolates (one each from KSA, Abu Dhabi, and Kuwait) were found to carry SCCmec IV b/d/i elements.
Finally, there were a number of PVL-positive CC22-IV . All characterized isolates of PVL-positive CC22-MRSA-IV had SCCmec IVc elements, ruling out the possibility that they directly evolved from UK-EMRSA-15/Barnim EMRSA by acquisition of a PVL phage. This strain also appears to be present in India (with two recent genome sequences being virtually identical to the isolates tested herein: http://www.ncbi.nlm.nih.gov/bioproject/PRJDB1743 and http://www.ncbi.nlm.nih.gov/bioproject/PRJDB2070). This suggests an epidemiological link to the Arabian Gulf, as previously also assumed for other MRSA.
35
In conclusion, ‘true’ UK-EMRSA-15/Barnim EMRSA was not identified from KSA, with all tested CC22-MRSA-IV differing either in toxin carriage and/or in SCCmec subtype. UK-EMRSA-15/Barnim-like strains from KSA might have evolved independently from other Middle Eastern CC22-MRSA-IV (by loss of tst1) or directly from methicillin-sensitive S. aureus, by acquisition of SCCmec IV b/d/i.
Due to the small number of isolates characterized herein, it is not possible to state that UK-EMRSA-15/Barnim EMRSA does not exist in KSA at all, or whether it is just less common than the other CC22-MRSA-IV strains.
UK-EMRSA-15/Barnim EMRSA was found in other countries in the region. The higher prevalence of this strain in Kuwait and the UAE than in KSA could possibly be attributed to the higher number of European expatriates and tourists in Kuwait and the UAE.
One might also wonder what makes CC22-MRSA-IV so successful an entity that at least six different CC22-MRSA-IV strains co-exist in the Arabian Gulf region.
The isolation and characterization of these isolates underscores the diversity of CC22 MRSA strains based on SCCmec subtyping, as well as the potential of SCCmec subtyping for molecular epidemiology. It also calls for continued surveillance and screening, including the application of highly sensitive molecular methods for the characterization of isolates.
Acknowledgements
The authors thank the clinical and laboratory staff of the institutions involved in caring for the patients, culturing S. aureus, and performing conventional identification and susceptibility tests. We acknowledge E. Müller, A. Reissig, B. Stieber (Jena), and A. Ruppelt-Lorz (Dresden) for their technical support with the array experiments, as well as P. Slickers (Jena) for bioinformatics work.
Funding: There was no external funding for this work. Each of the participating institutions covered the costs of experiments performed in the respective institutions, as well as granted the time needed to perform this study.
Ethical approval: MRSA typing (research project E-15-1406) at King Khalid University Hospital, Riyadh, Kingdom of Saudi Arabia, was reviewed and approved by the Institutional Review Board. Any identifying information on the index case has been omitted. The patient gave consent for the publication of this anonymized report. The other parts of this study deal with molecular typing/epidemiological surveillance based on archived isolates without accompanying patient-related information, for which no ethical approval was required.
Conflict of interest: Ralf Ehricht and Stefan Monecke are employees of Alere Technologies, the company that manufactures the microarrays used in this study. The arrays used herein are (or will be developed to be) a marketed product.
References
- Identification and characterization of phage variants of a strain of epidemic methicillin-resistant Staphylococcus aureus (EMRSA-15).J Clin Microbiol. 2001; 39: 1540-1548
- Characterization of a strain of methicillin-resistant Staphylococcus aureus (EMRSA-15) by conventional and molecular methods.J Hosp Infect. 1993; 25: 45-52
- Changing patterns in frequency of recovery of five methicillin-resistant Staphylococcus aureus clones in Portuguese hospitals: surveillance over a 16-year period.J Clin Microbiol. 2008; 46: 2912-2917
- Clonal replacement of epidemic methicillin-resistant Staphylococcus aureus strains in a German university hospital over a period of eleven years.PLoS One. 2011; 6: e28189
- Molecular characterization of methicillin-resistant Staphylococcus aureus isolated over a 2-year period in a Qatari hospital from multinational patients.Clin Microbiol Infect. 2014; 20: 169-173
- The evolutionary history of methicillin-resistant Staphylococcus aureus (MRSA).Proc Natl Acad Sci U S A. 2002; 99: 7687-7692
- Epidemiology of emerging methicillin-resistant Staphylococcus aureus (MRSA) in Denmark: a nationwide study in a country with low prevalence of MRSA infection.J Clin Microbiol. 2005; 43: 1836-1842
- Non-multiresistant methicillin-resistant Staphylococcus aureus bacteraemia in Sydney, Australia: emergence of EMRSA-15, Oceania, Queensland and Western Australian MRSA strains.Pathology. 2006; 38: 239-244
- Evolving EMRSA-15 epidemic in Singapore hospitals.J Med Microbiol. 2007; 56: 376-379
- Extensive genetic diversity identified among sporadic methicillin-resistant Staphylococcus aureus isolates recovered in Irish hospitals between 2000 and 2012.Antimicrob Agents Chemother. 2014; 58: 1907-1917
- A field guide to pandemic, epidemic and sporadic clones of methicillin-resistant Staphylococcus aureus.PLoS One. 2011; 6: e17936
- Molecular characterisation of the dominant UK methicillin-resistant Staphylococcus aureus strains, EMRSA-15 and EMRSA-16.J Med Microbiol. 2002; 51: 516-521
- Harmonization of pulsed-field gel electrophoresis protocols for epidemiological typing of strains of methicillin-resistant Staphylococcus aureus: a single approach developed by consensus in 10 European laboratories and its application for tracing the spread of related strains.J Clin Microbiol. 2003; 41: 1574-1585
- Methicillin-resistant Staphylococcus aureus in the Australian community: an evolving epidemic.Med J Aust. 2006; 184: 384-388
- Diversity among community isolates of methicillin-resistant Staphylococcus aureus in Australia.J Clin Microbiol. 2004; 42: 3185-3190
- Tracking methicillin-resistant Staphylococcus aureus clones during a 5-year period (1998 to 2002) in a Spanish hospital.J Clin Microbiol. 2004; 42: 4649-4656
- Characterisation of MRSA from Malta and the description of a Maltese epidemic MRSA strain.Eur J Clin Microbiol Infect Dis. 2010; 29: 163-170
- A decade of community MRSA in New Zealand.Epidemiol Infect. 2005; 133: 899-904
- High prevalence of hospital-associated methicillin-resistant Staphylococcus aureus in the community in Portugal: evidence for the blurring of community–hospital boundaries.Eur J Clin Microbiol Infect Dis. 2013; 32: 1269-1283
- Characterisation of non-multiresistant methicillin-resistant Staphylococcus aureus (including EMRSA-15) in Kuwait Hospitals.Clin Microbiol Infect. 2006; 12: 262-269
- Characteristics of a new epidemic MRSA in Germany ancestral to United Kingdom EMRSA 15.Int J Med Microbiol. 2001; 290: 677-682
- Molecular epidemiology of nasal isolates of methicillin-resistant Staphylococcus aureus from Jordan.J Infect Public Health. 2015; 8: 90-97
- A typical hospital-acquired methicillin-resistant Staphylococcus aureus clone is widespread in the community in the Gaza Strip.PLoS One. 2012; 7: e42864
- MRSA clonal complex 22 strains harboring toxic shock syndrome toxin (TSST-1) are endemic in the primary hospital in Gaza.Palestine. PLoS One. 2015; 10: e0120008
- High prevalence of toxic shock syndrome toxin-producing epidemic methicillin-resistant Staphylococcus aureus 15 (EMRSA-15) strains in Kuwait hospitals.New Microbes New Infect. 2016; 12: 24-30
- Isolation and characterization of an epidemic methicillin-resistant Staphylococcus aureus 15 variant in the central United States.J Clin Microbiol. 2008; 46: 3548-3549
- Characterisation of MRSA strains isolated from patients in a hospital in Riyadh, Kingdom of Saudi Arabia.BMC Microbiol. 2012; 12: 146
- Molecular characterization of methicillin resistant Staphylococcus aureus strains isolated from intensive care units in Iran: ST22-SCCmec IV/t790 emerges as the major clone.PLoS One. 2016; 11: e0155529
- Molecular characterization of methicillin resistant Staphylococcus aureus (MRSA) with emergence of epidemic clones ST 22 and ST 772, in Mumbai, India.J Clin Microbiol. 2010; 48: 1806-1811
- Epidemic methicillin resistant Staphylococcus aureus (EMRSA-15) variants detected from healthy and diseased individuals in India.J Med Microbiol. 2010; 59: 815-821
- Genotyping of community-associated methicillin resistant Staphylococcus aureus (CA-MRSA) in a tertiary care centre in Mysore South India: ST2371-SCCmec IV emerges as the major clone.Infect Genet Evol. 2015; 34: 230-235
- 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. 2007; 45: 2554-2563
- Healthcare-associated outbreaks and community-acquired infections due to MRSA carrying the Panton–Valentine leucocidin gene in southeastern Germany.Eur J Clin Microbiol Infect Dis. 2005; 24: 419-422
- Assignment of Staphylococcus aureus isolates to clonal complexes based on microarray analysis and pattern recognition.FEMS Immunol Med Microbiol. 2008; 53: 237-251
- Genome sequencing and molecular characterisation of Staphylococcus aureus ST772-MRSA-V, “Bengal Bay Clone”.BMC Res Notes. 2013; 6: 1-7
Article info
Publication history
Published online: August 28, 2016
Accepted:
August 23,
2016
Received in revised form:
August 19,
2016
Received:
July 13,
2016
Corresponding Editor: Eskild Petersen, Aarhus, Denmark.Identification
Copyright
© 2016 The Authors. Published by Elsevier Ltd on behalf of International Society for Infectious Diseases.
User license
Creative Commons Attribution – NonCommercial – NoDerivs (CC BY-NC-ND 4.0) | How you can reuse 
Elsevier's open access license policy
Creative Commons Attribution – NonCommercial – NoDerivs (CC BY-NC-ND 4.0)
Permitted
For non-commercial purposes:
- Read, print & download
- Redistribute or republish the final article
- Text & data mine
- Translate the article (private use only, not for distribution)
- Reuse portions or extracts from the article in other works
Not Permitted
- Sell or re-use for commercial purposes
- Distribute translations or adaptations of the article
Elsevier's open access license policy
