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Katerina Tsergouli Department of Microbiology, Medical Faculty, School of Health Sciences, Aristotle University of Thessaloniki, Greece

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Theodoros Karampatakis Department of Microbiology, Medical Faculty, School of Health Sciences, Aristotle University of Thessaloniki, Greece

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Konstantina Kontopoulou Department of Microbiology, “Georgios Gennimatas” General Hospital of Thessaloniki, Greece

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Styliani Pappa Department of Microbiology, Medical Faculty, School of Health Sciences, Aristotle University of Thessaloniki, Greece

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Parthena Kampouridou Department of Pediatrics, “Georgios Gennimatas” General Hospital of Thessaloniki, Greece

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Georgia Kallasidou Department of Pediatrics, “Georgios Gennimatas” General Hospital of Thessaloniki, Greece

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Katerina Tsioka Department of Microbiology, Medical Faculty, School of Health Sciences, Aristotle University of Thessaloniki, Greece

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Sophia Zotou Department of Microbiology, “Georgios Gennimatas” General Hospital of Thessaloniki, Greece

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Εleftheria - Eugenia Farmaki Department of Microbiology, “Georgios Gennimatas” General Hospital of Thessaloniki, Greece

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Charalampos Kotzamanidis Veterinary Research Institute of Thessaloniki, Greek Agricultural Organization-Dimitra, Thermi, Greece

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Anna Papa Department of Microbiology, Medical Faculty, School of Health Sciences, Aristotle University of Thessaloniki, Greece

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Abstract

Introduction

Methicillin-resistant Staphylococcus aureus (MRSA) causes severe community and hospital acquired infections. Identification of staphylococcal cassette chromosome mec (SCCmec), multilocus-sequence typing, and sequencing of S. aureus protein A (spa) gene are used for MRSA typing. The aim was to investigate the spa types of MRSA isolates in a tertiary hospital in Greece and analyse the whole genome sequences of two t127 MRSA isolates.

Methods

Totally, 39 MRSA isolates collected from July 2019 to June 2020 in “Georgios Gennimatas” General Hospital of Thessaloniki, Greece, were included in the study. Identification and antimicrobial susceptibility testing were performed using VITEK II automated system, and spa typing was performed. A minimum spanning tree was used to display the spa type frequencies and the genetic distances among them. Two t127-MRSA isolates (IM-MRSA and PD-MRSA) were selected for WGS.

Results

Six isolates (15.4%) were resistant to mupirocin, 18 (46.2%) to fusidic acid, three (7.7%) to vancomycin and two (5.1%) to teicoplanin. Twenty-two different spa types were detected, with t002, t003, and t422 being the most frequent (5/39, 12.8% each), followed by t1994 (4/39, 10.3%). The isolates presented high genetic diversity and, taking into account the time between hospital admission and sampling, intrahospital spread did not occur. Even the two t127 isolates were assigned to different sequence types, ST9-XII-t127 and ST1-IVa-t127. Plasmids and genes conferring antimicrobial resistance and virulence were also identified.

Conclusions

Various spa types were identified and together with the information about the time between hospital admission and sampling supports polyclonal MRSA spread in the hospital excluding a nosocomial infection. WGS provides a more detailed analysis distinguishing even the isolates belonging to the same spa type.

Abstract

Introduction

Methicillin-resistant Staphylococcus aureus (MRSA) causes severe community and hospital acquired infections. Identification of staphylococcal cassette chromosome mec (SCCmec), multilocus-sequence typing, and sequencing of S. aureus protein A (spa) gene are used for MRSA typing. The aim was to investigate the spa types of MRSA isolates in a tertiary hospital in Greece and analyse the whole genome sequences of two t127 MRSA isolates.

Methods

Totally, 39 MRSA isolates collected from July 2019 to June 2020 in “Georgios Gennimatas” General Hospital of Thessaloniki, Greece, were included in the study. Identification and antimicrobial susceptibility testing were performed using VITEK II automated system, and spa typing was performed. A minimum spanning tree was used to display the spa type frequencies and the genetic distances among them. Two t127-MRSA isolates (IM-MRSA and PD-MRSA) were selected for WGS.

Results

Six isolates (15.4%) were resistant to mupirocin, 18 (46.2%) to fusidic acid, three (7.7%) to vancomycin and two (5.1%) to teicoplanin. Twenty-two different spa types were detected, with t002, t003, and t422 being the most frequent (5/39, 12.8% each), followed by t1994 (4/39, 10.3%). The isolates presented high genetic diversity and, taking into account the time between hospital admission and sampling, intrahospital spread did not occur. Even the two t127 isolates were assigned to different sequence types, ST9-XII-t127 and ST1-IVa-t127. Plasmids and genes conferring antimicrobial resistance and virulence were also identified.

Conclusions

Various spa types were identified and together with the information about the time between hospital admission and sampling supports polyclonal MRSA spread in the hospital excluding a nosocomial infection. WGS provides a more detailed analysis distinguishing even the isolates belonging to the same spa type.

Introduction

Methicillin-resistant Staphylococcus aureus (MRSA) is a gram-positive bacterium causing community-acquired and nosocomial infections worldwide [1, 2]. According to the latest epidemiological report of the European Centre for Disease Prevention and Control (ECDC), the prevalence of MRSA in Greece is among the highest in Europe, reaching 37.6% in 2019 [3].

Various methods are used for MRSA typing, such as the identification of staphylococcal cassette chromosome mec (SCCmec), the multilocus-sequence typing (MLST), and the sequencing of the highly polymorphic repeat region of S. aureus protein A (spa) gene [4–6]. The detection of spa-clusters could be used as a rapid tool for the study of MRSA epidemiology in a hospital and for separation between relapse and re-infection [7].

Previous studies in Greece showed that spa types t044, t003 and t037 are the predominant types among MRSA isolated from clinical sources [8, 9]. In Europe, the most prevalent are the spa-types t032, t008 and t067, while t011, t108 and t034 predominate among livestock-associated (LA)-MRSA [10]. LA-MRSA were first detected in 2003 in pigs [11], while later, they have been isolated also in patients with no previous contact with livestock [12]. Knowledge of MRSA epidemiology is of great importance in organising and implementing infection control measures, especially in hospital settings [13]. Over the last decade, whole-genome sequencing (WGS) is an added value for the investigation of outbreaks caused by MRSA [14]. Although limited, there are reports in Greece based on whole genome MRSA sequences [15–18].

The aim of the present study was to evaluate the antimicrobial resistance patterns and the distribution and prevalence of spa types of MRSA isolated from patients hospitalized in various wards of a tertiary hospital in Greece, and to further characterize the whole genome sequences of two isolates belonging to spa type t127, which is often associated with LA-MRSA.

Material and methods

Bacterial isolates

Thirty-nine MRSA isolates collected during one-year period (July 2019 to June 2020) from 39 patients (18 males, 46%) hospitalized in various wards of “Georgios Gennimatas” General Hospital of Thessaloniki in Greece, were included in the study. The median age of the patients was 59 years (range 0.25–91 years). The isolates were recovered from wound (18, 46.2%), ear swab (five, 12.8%), blood, throat and nasal swabs (four, 10.3% each), central intravenous catheter (two, 5.1%), urine and eye swab samples (one, 2.5%, each) (Table 1). Eight isolates (20.5%) were taken through testing for colonization, while 29 (79.5%) were collected from infection sites. The distinction between infection and colonization was performed using previously described criteria [19]. The time between patients' admission to the hospital and sampling was estimated in order to associate or not with nosocomial infection (>48 or <48 h, respectively) (Table 1).

Table 1.

Characteristics of the 39 MRSA strains included in the study

IDSexAge (years)SampleColonization/InfectionWardIsolation Date>48hSpa typeAntimicrobial Resistance Profile
1F59CVCInfectionCardiologyMay 2020YESt653Ox-Fox-Fu-E
2F45urineInfectionERApr 2020NOt442Ox-Fox-Fu-Le-Mu-Sxt-G
3F72throat swabColonizationICUMay 2020NOt2986Ox-Fox
4F81throat swabColonizationICUJun 2020NOt008Ox-Fox-Le-E
5F70throat swabColonizationInternal medicineSept 2019NOt422Ox-Fox-Fu-Le-E
6M78bloodInfectionInternal medicineDec 2019NOt267Ox-Fox-Fu
7M91bloodInfectionInternal medicineJan 2020NOt328Ox-Fox-Le
8F82throat swabColonizationInternal medicineApr 2020NOt003Ox-Fox-Fu-Le-Tet-E
9M84woundInfectionInternal medicineApr 2020NOt127Ox-Fox-Tet-E
10M75woundInfectionInternal medicineJun 2020NOt002Ox-Fox-Le-E
11F55nasal swabColonizationOrthopaedicJul 2019YESt5452Ox-Fox-E
12F86woundInfectionOrthopaedicNov 2019YESt003Ox-Fox
13M62woundInfectionOrthopaedicNov 2019YESt002Ox-Fox
14M84woundInfectionOrthopaedicDec 2019NOt003Ox-Fox-Fu-Le
15M79nasal swabColonizationOrthopaedicJan 2020YESt002Ox-Fox
16F65woundInfectionOutpatientSept 2019NOt422Ox-Fox-Fu-Le-Mu-Sxt-E-G
17M70woundInfectionOutpatientOct 2019NOt440Ox-Fox-Va-Teic
18F47ear swabInfectionOutpatientOct 2019NOt084Fox-Sxt
19F28ear swabInfectionOutpatientOct 2019NOt422Ox-Fox-Fu-Le
20F0.5woundInfectionOutpatientJan 2020NOt328Ox-Fox
21M0.42woundInfectionOutpatientJan 2020NOt1814Ox-Fox-Sxt
22M0.25ear swabInfectionOutpatientApr 2020NOt131Ox-Fox-Fu-Tet
23F73ear swabInfectionOutpatientMay 2020NOt422Ox-Fox-Le-E
24F7nasal swabColonizationOutpatientJun 2020NOt1994Ox-Fox-Fu-Mu-E
25M11ear swabInfectionOutpatientJun 2020NOt012Ox-Fox-E
26F0.83woundInfectionPDJul 2019NOt1994Fox-Fu-Mu-E
27F0.42woundInfectionPDJul 2019NOt127Ox-Fox-Tet-E
28M4eye swabInfectionPDOct 2019NOt1994Ox-Fox-Fu-Mu-Va
29F0.58nasal swabColonizationPDNov 2019NOt1994Ox-Fox-Fu-Mu
30F59woundInfectionSurgeryAug 2019YESt002Ox-Fox-Fu-Le-E
31M40bloodInfectionSurgerySept 2019YESt002Ox-Fu
32F21woundInfectionSurgeryOct 2019NOt091Ox-Fox-Fu-Le-Tet-Sxt-Va-Teic
33M65woundInfectionSurgeryNov 2019YESt726Ox-Fox
34M22woundInfectionSurgeryMar 2020NOt1309Ox-Fox-Le
35M16woundInfectionSurgeryMar 2020NOt044Ox-Fox-Fu-Tet
36F28CVCInfectionSurgeryMar 2020NOt034Ox-Fox-Tet
37F59woundInfectionSurgeryJun 2020NOt003Ox-Fox-Le-E
38M81bloodInfectionUrologyAug 2019NOt422Ox-Fox-Fu-Le-E
39M45woundInfectionUrologyFeb 2020NOt003Ox-Fox-E

M: Male, F: Female, CVC: Central Venous Catheter, ER: Emergency Room, ICU: Intensive Care Unit, PD: Paediatric ward.

Ox: Oxacillin, Fox: Cefoxitin, Fu: Fusidic acid, Le: Levofloxacin, Mu: Mupirocin, Teic: Teicoplanin.

Te: Tetracycline, SXT: Trimethoprim/Sulfamethoxazole, G: Gentamicin, Va: Vancomycin.

*Erythromycin susceptibility results for strains with ID 6,7,12–15.17–21,28,29, and 31–33 are not available.

Microbiological methods

All samples were cultured in blood agar, and strain identification and antimicrobial susceptibility testing were performed using the GP ID and AST-P659 cards in VITEK II automated system, respectively (BioMérieux, Marcy-l’Étoile, France). The minimum inhibitory concentration (MIC) was interpreted according to the Clinical and Laboratory Standards Institute (CLSI) breakpoints reported in January 2019 [20]. MRSA isolates were defined as resistant to oxacillin [21]. Cefoxitin-screen test in VITEK 2 was used as a surrogate marker for the detection of methicillin resistance [22].

DNA extraction – Spa typing

DNA was extracted using the DNA extraction kit (Qiagen, Hilden, Germany). The spa gene was amplified and sequenced. Typing was performed through the Rindom Spa server (spaserver.ridom.de). A minimum spanning tree (MST) was generated using the spa-clustering method of the spa-typing plugin of BioNumerics v.7.1 software (Applied Maths, Sint-Martens-Latem, Belgium), which is connected to the SeqNet/Ridom Spa Server (https://www.spaserver.ridom.de/).

Whole genome sequencing - Bioinformatic analysis

Since t127 is often related with LA-MRSA, two t127 isolates [one collected from a patient hospitalized in internal medicine (IM-MRSA), and a second one from a patient hospitalized in the pediatric ward (PD-MRSA)] were selected for WGS analysis. WGS was performed on Ion Torrent PGM Platform (Life Technologies Corporation, Grand Island, NY, USA). All procedures were conducted according to manufacturer's guidelines. PCR products were loaded on Ion-316TM chip kit V2BC. The Ion PGM Hi-Q (200) chemistry (Ion PGM Hi-Q Sequencing kit, A25592) was applied.

The consensus sequence was taken using S. aureus strain WHC09 (GenBank accession number CP077755) as reference sequence. MLST analysis was performed using the web-based MLST-DTU tool [23]. Resfinder version 4.1 and the Comprehensive Antibiotic Resistance Database (CARD) were used for the detection of antimicrobial resistance genes [24, 25], while the virulence genes were detected using the Virulence Finder v. 2.0 software [26]. The SCCmec elements of the isolates were identified through the SCCmecFinder database version 1.2 [4]. PlasmidFinder version 2.1 was used for the identification of plasmids [27].

Results

Antimicrobial resistance

The antimicrobial resistance patterns are seen in Table 1. Specifically, 18 isolates (46.2%) displayed resistance to fusidic acid, 16 (41%) to levofloxacin, seven (17.9%) to tetracycline, six (15.4%) to mupirocin, five (12.8%) to trimethoprim/sulfamethoxazole, three (7.7%) to vancomycin and two (5.1%) to teicoplanin. Thirty-seven isolates (94.9%) were resistant to cefoxitin (cefoxitin-screen positive); two isolates (5.1%) were resistant to cefoxitin and sensitive to oxacillin, while one isolate (2.6%) was sensitive to cefoxitin and resistant to oxacillin.

Spa typing

Twenty-two different spa types were detected, with t002, t003, and t422 being the most frequent (5/39, 12.8% each), followed by t1994 (4/39, 10.3%), t127 and t328 (2/39, 5.1% each) (Table 1). Different spa types were detected in the various wards, except the paediatric ward where t1994 (3/4, 75%) predominated. Most of the samples were taken <48h after admission; this was the case also for the t1994 isolates, suggesting that they were not associated with nosocomial infection (Table 1, Fig. 1).

Fig. 1.
Fig. 1.

Minimum spanning tree based on spa-typing results of MRSA strains depending on the department of isolation. Each spa type is represented by a single node. The size of the node depends proportionally on the number of strains within the spa type. The colored sections represent a different ward. The distance between nodes represents the genetic diversity of the isolates

Citation: Acta Microbiologica et Immunologica Hungarica 69, 3; 10.1556/030.2022.01825

Analysis of whole genome sequences

IM-MRSA and PD-MRSA isolates were assigned to ST9 and ST1, respectively. They were carrying SCCmec elements belonging to XII and IVa types, respectively.

The antimicrobial resistance and virulence genes, and the plasmids carried by the two isolates are seen in Table 2. Specifically, both had antimicrobial resistance genes for β-lactams (mecA and blaZ), aminoglycosides [aph(3′)-ΙΙΙa], and macrolide, lincosamide and streptogramin B (ermC); IM-MRSA carried three additional aminoglycoside resistance genes [ant(6)-Ia, aadD and aac(6′)-aph(2″)], while PD-MRSA harbored one additional aminoglycoside resistance gene [aad(6)]; dfrG gene conferring resistance to trimethoprim was detected only in IM-MRSA. Both isolates carried several efflux pump protein genes conferring resistance to streptogramin A, tetracycline, fluoroquinolones, cephalosporins and lincosamides.

Table 2.

Genetic characteristics of two t127 MRSA strains of the study

PD-MRSAIM-MRSA
Size (bp)2,971,2582,849,316
GC content (%)34.231.0
Number of contigs (with PEGs)5305,636
MLSTST1ST9
SCCmec elementIVaXII
Antimicrobial resistance genes

Efflux pump genes
mecA, blaZ,

aad(6), aph(3′)-IIIa,

ermC,

mepR, norA, mgrA, arlR, arlS, LmrS, tet(45)
mecA, blaZ,

ant(6)-Ia, aph(3′)-IIIa,

aadD, aac(6′)-aph(2″),

dfrG, ermC

tetL, fexA, IsaE, InuB
Plasmid group (rep family)pGSA2 (rep7)pGSA11 (rep22)
pGSA3 (rep10)
pGSA22 (rep5, rep16)
Virulence factor (gene)
Chemotaxis inhibitory protein (chp)
Aureolysin (aur)++
Serine protease (splA, splB)+
Staphylococcal complement inhibitor (scn)+
Staphylokinase (sak)+
γ-hemolysin (hlgA, hlgB, hlgC)++
Other leukocidin components (lukAB, lukED)+ (lukED)
Staphylococcal enterotoxin+ (seh)+ (sei, sem, seo, seu)
Antiseptic resistance genes (qacA, qacB, qacC, qacD)+ (qacC, qacD)

Regarding plasmid content, IM-MRSA carried a plasmid replicon type rep22 (of the pGSA11 group), while PD-MRSA transferred plasmid replicon types rep7a (of the pGSA2 group, which includes the repC cassette), rep7c, rep10 (of the pGSA3 group which includes the ermC gene) and rep5 along with rep16 (of the pGSA22 group which includes the blaZ gene) (Table 2).

Discussion

The present study provides an insight into the distribution of MRSA isolates of various spa types in a tertiary hospital in Greece. Most of the isolates were collected from infection sites and few from colonization sites; however, colonization usually precedes infection [28]. It was shown that most isolates were resistant to several antimicrobial categories. The high resistance to fusidic acid (46.2%) exceeds by far that observed among MRSA globally (2.6%) [29]. The resistance rate to mupirocin (15.4%) was higher than the 3.1% revealed in a previous multicenter surveillance study [30]; this is of crucial importance since resistance to mupirocin could potentially diminish the efficacy of MRSA decolonizing strategies [31]. For both antimicrobials (fusidic acid and mupirocin) further studies are needed to elucidate the genetic background of the increased resistance (whether it is due to mutation(s) and/or acquired resistance genes). In contrast, resistance to levofloxacin was lower than that reported in a recently published study (17.9% versus 87.9%) [32]; further analysis is needed. The resistance rates of vancomycin and teicoplanin were low; although infections caused by vancomycin-resistant MRSA have been described [33], resistance to vancomycin and teicoplanin are rarely identified in MRSA strains, and they remain active against MRSA causing severe infections [34, 35]. It seems that there was no difference in the antimicrobial resistance profile between MRSA isolates that were considered hospital acquired vs community acquired ones (Table 1).

In total, 22 different spa types were identified, and most of them (16/22, 72.7%) were represented as singletons, suggesting a non-clonal MRSA distribution (Table 1, Fig. 1). An exception was the t1994 predominance in the paediatric ward during a four-months’ time period; however, it seems that it was not associated with intra-hospital infection since the time of sampling was <48h from the admission to the hospital. The high prevalence of t002 and t003 spa types seen in the present study, has been reported in recent studies [3637], while the rare t422 type has been previously reported also in another hospital in Thessaloniki [9].

Since t127 type was initially associated with LA-MRSA, and it has been recently detected in Greek workers in the dairy production chain [17], two t127 MRSA isolates (IM-MRSA and PD-MRSA) of the present study were selected for analysis of their whole genome. The two isolates differed each other, as IM-MRSA was assigned to ST9-XII type, while PD-MRSA to ST1-IVa type as was the case in a previous study [17]. The two t127 MRSA isolates transferred the γ-hemolysin genes hlgA, hlgB, hlgC and aureolysin aur gene, which have been previously described in both ST1-IVa and ST9-XII MRSA [38, 39]. PD-MRSA carried the enterotoxin seh gene and the gene encoding leukocidin lukED, as previously described in ST1-IVa MRSA isolates [38, 40]. IM-MRSA lacked leucocidin components, however it carried the enterotoxin sei, sem, seo, seu genes, although enterotoxin genes are usually absent in ST9-XII MRSA isolates [39].

LA-MRSA lack the human evasion genes scn (staphylococcal complement inhibitor), chp (chemotaxis inhibitory protein) and sak (staphylokinase), due to loss of the related φSa3 phage [41]. IM-MRSA lacked these three genes, while PD-MRSA lacked only the chp gene. IM-MRSA was isolated from wound infection and was assigned to ST9-XII, which, due to loss of scn, chp and sak genes, is considered to have been evolved from human to animal host [39]. ST9-XII is rarely reported as cause of infection [42]. Spa-type t127 has not been reported for S. aureus ST9 so far. Since generation of this spa-type from the repeat spa sequences observed in this clonal lineage would need several genetic events (mutations, deletion(s), insertion), the most probable mechanism seems to be the acquisition of the chromosomal sequence which contains spa from a ST9 donor; there are several examples for nontypical spa types for particular STs based on this genetic event, e.g. spa type t030 in MRSA ST239 [43]. Comparative studies are needed to confirm which mechanism(s) took place. The second t127 isolate, PD-MRSA, was isolated from an axillary abscess and belonged to ST1-IVa-t127, which is originally considered a human-associated lineage. ST1-t127 isolates have been reported as one of the most frequent types isolated from human samples [44].

Conclusions

The current study provides an insight into the spa types of MRSA in a tertiary hospital in Greece and together with the information of time interval between admission and sampling suggests polyclonal introductions in the various wards. The extensive resistance to most antimicrobial classes needs further attention since it is associated with high antimicrobial consumption. A more detailed genetic characterization is gained when WGS is applied, as shown by the results of the analysis of the two t127 MRSA isolates, which showed that although they belonged to the same spa type, they were different strains. Molecular surveillance studies are of high priority in the hospitals since they can lead the design of guidelines and infection control measures that must be applied to reduce and prevent the spread of MRSA.

Genome sequences

The whole genome sequences of IM-MRSA and PD-MRSA were submitted to European Nucleotide Archive (ENA) under the study PRJEB47007 and received the Accession numbers ERS7262952 and ERS7262953, respectively.

Declarations

Funding

This work was financially supported by the European Union's Horizon 2020 project VEO (grant number 874735).

Conflicts of interest

The authors have no conflicts of interest to declare that are relevant to the content of this article.

Availability of data and material

Available upon request.

Code availability

Not applicable.

Ethics approval

Not applicable.

Authors' contribution

All authors have equally contributed to the study and preparation of the manuscript.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

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    Karampatakis T, Papadopoulos P, Tsergouli K, Angelidis AS, Melidou A, Sergelidis D, et al. Genetic characterization of livestock-associated methicillin-resistant staphylococcus aureus isolated in Greece. Braz J Microbiol 2021; 52: 20912096.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Geladari A, Karampatakis T, Antachopoulos C, Iosifidis E, Tsiatsiou O, Politi L, et al. Epidemiological surveillance of multidrug-resistant gram-negative bacteria in a solid organ transplantation department. Transpl Infect Dis 2017; 19.

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    • Export Citation
  • 20.

    CLSI. Performance Standards for antimicrobial susceptibility testing: twenty-fifth informational supplement M100-S29. CLSI. Wayne, P.A., USA; 2019.

    • Search Google Scholar
    • Export Citation
  • 21.

    Lee AS, de Lencastre H, Garau J, Kluytmans J, Malhotra-Kumar S, Peschel A, et al. Methicillin-resistant staphylococcus aureus. Nat Rev Dis Primers 2018; 4, 18033.

    • PubMed
    • Search Google Scholar
    • Export Citation
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    John MA, Burden J, Stuart JI, Reyes RC, Lannigan R, Milburn S, et al. Comparison of three phenotypic techniques for detection of methicillin resistance in staphylococcus spp. Reveals a species-dependent performance. J Antimicrob Chemother 2009; 63: 493496.

    • PubMed
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    • Export Citation
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    Larsen MV, Cosentino S, Rasmussen S, Friis C, Hasman H, Marvig RL, et al. Multilocus sequence typing of total-genome-sequenced bacteria. J Clin Microbiol 2012; 50: 13551361.

    • PubMed
    • Search Google Scholar
    • Export Citation
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    Bortolaia V, Kaas RS, Ruppe E, Roberts MC, Schwarz S, Cattoir V, et al. Resfinder 4.0 for predictions of phenotypes from genotypes. J Antimicrob Chemother 2020; 75: 34913500.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Alcock BP, Raphenya AR, Lau TTY, Tsang KK, Bouchard M, Edalatmand A, et al. Antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res 2020; 48: 517525.

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    • Export Citation
  • 26.

    Joensen KG, Scheutz F, Lund O, Hasman H, Kaas RS, Nielsen EM, et al. Real-time whole-genome sequencing for routine typing, surveillance, and outbreak detection of verotoxigenic escherichia coli. J Clin Microbiol 2014; 52: 15011510.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Carattoli A, Zankari E, Garcia-Fernandez A, Voldby Larsen M, Lund O, Villa L, et al. silico detection and typing of plasmids using plasmidfinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother 2014; 58: 38953903.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Love NK, Pichon B, Padfield S, Hughes GJ. A persistent recurring cluster of meticillin-resistant staphylococcus aureus (mrsa) colonizations in a special care baby unit: a matched case-control study. J Hosp Infect 2020; 106: 774781.

    • Search Google Scholar
    • Export Citation
  • 29.

    Hajikhani B, Goudarzi M, Kakavandi S, Amini S, Zamani S, van Belkum A, et al. The global prevalence of fusidic acid resistance in clinical isolates of staphylococcus aureus: a systematic review and meta-analysis. Antimicrob Resist Infect Control 2021; 10: 75.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Kresken M, Hafner D, Schmitz FJ, Wichelhaus TA, Paul-Ehrlich-Society for C. Prevalence of mupirocin resistance in clinical isolates of staphylococcus aureus and staphylococcus epidermidis: results of the antimicrobial resistance surveillance study of the Paul-ehrlich-society for chemotherapy, 2001. Int J Antimicrob Agents 2004; 23: 577581.

    • PubMed
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    • Export Citation
  • 31.

    Bes TM, Perdigao-Neto L, Martins RR, Heijden I, Trindade PA, Camilo G, et al. Susceptibility to chlorhexidine and mupirocin among methicillin-resistant staphylococcus aureus clinical isolates from a teaching hospital. Rev Inst Med Trop Sao Paulo 2021; 63: e27.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Antonelli A, Giani T, Coppi M, Di Pilato V, Arena F, Colavecchio OL, et al. Staphylococcus aureus from hospital-acquired pneumonia from an Italian nationwide survey: activity of ceftobiprole and other anti-staphylococcal agents, and molecular epidemiology of methicillin-resistant isolates. J Antimicrob Chemother 2019; 74: 34533461.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    Cong Y, Yang S, Rao X. Vancomycin resistant staphylococcus aureus infections: A review of case updating and clinical features. J Adv Res 2020; 21: 169176.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34.

    Beibei L, Yun C, Mengli C, Nan B, Xuhong Y, Rui W. Linezolid versus vancomycin for the treatment of gram-positive bacterial infections: Meta-analysis of randomised controlled trials. Int J Antimicrob Agents 2010; 35: 312.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35.

    Chen H, Li L, Wu M, Xu S, Wang M, Li J, et al. Efficacy and safety of linezolid versus teicoplanin for the treatment of mrsa infections: A meta-analysis. J Infect Dev Ctries 2018; 11: 926934.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36.

    Tkadlec J, Capek V, Brajerova M, Smelikova E, Melter O, Bergerova T, et al. The molecular epidemiology of methicillin-resistant staphylococcus aureus (mrsa) in the Czech republic. J Antimicrob Chemother 2021; 76: 5564.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37.

    Engelthaler DM, Kelley E, Driebe EM, Bowers J, Eberhard CF, Trujillo J, et al. Rapid and robust phylotyping of spa t003, a dominant mrsa clone in Luxembourg and other european countries. BMC Infect Dis 2013; 13: 339.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38.

    Cortes MF, Costa MO, Lima NC, Souza RC, Almeida LG, Guedes LPC, et al. Complete genome sequence of community-associated methicillin-resistant staphylococcus aureus (strain USA400-0051), a prototype of the USA400 clone. Mem Inst Oswaldo Cruz 2017; 112: 790792.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39.

    Yu F, Cienfuegos-Gallet AV, Cunningham MH, Jin Y, Wang B, Kreiswirth BN, et al. Molecular evolution and adaptation of livestock-associated methicillin-resistant staphylococcus aureus (la-mrsa) sequence type 9. mSystems 2021; 6, e0049221.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40.

    Shukla SK, Karow ME, Brady JM, Stemper ME, Kislow J, Moore N, et al. Virulence genes and genotypic associations in nasal carriage, community-associated methicillin-susceptible and methicillin-resistant USA400 staphylococcus aureus isolates. J Clin Microbiol 2010; 48: 35823592.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41.

    Price LB, Stegger M, Hasman H, Aziz M, Larsen J, Andersen PS, et al. Staphylococcus aureus cc398: Host adaptation and emergence of methicillin resistance in livestock. mBio 2012; 3.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42.

    Jin Y, Yu X, Chen Y, Chen W, Shen P, Luo Q, et al. Characterization of highly virulent community-associated methicillin-resistant staphylococcus aureus st9-sccmec xii causing bloodstream infection in China. Emerg Microbes Infect 2020; 9: 25262535.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43.

    Monecke S, Slickers P, Gawlik D, Muller E, Reissig A, Ruppelt-Lorz A, et al. Molecular typing of st239-mrsa-iii from diverse geographic locations and the evolution of the sccmec iii element during its intercontinental spread. Front Microbiol 2018; 9: 1436.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44.

    Monaco M, Pedroni P, Sanchini A, Bonomini A, Indelicato A, Pantosti A. Livestock-associated methicillin-resistant staphylococcus aureus responsible for human colonization and infection in an area of Italy with high density of pig farming. BMC Infect Dis 2013; 13: 258.

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    • Export Citation
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    Karampatakis T, Papadopoulos P, Tsergouli K, Angelidis AS, Melidou A, Sergelidis D, et al. Genetic characterization of livestock-associated methicillin-resistant staphylococcus aureus isolated in Greece. Braz J Microbiol 2021; 52: 20912096.

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    Geladari A, Karampatakis T, Antachopoulos C, Iosifidis E, Tsiatsiou O, Politi L, et al. Epidemiological surveillance of multidrug-resistant gram-negative bacteria in a solid organ transplantation department. Transpl Infect Dis 2017; 19.

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    • Export Citation
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    CLSI. Performance Standards for antimicrobial susceptibility testing: twenty-fifth informational supplement M100-S29. CLSI. Wayne, P.A., USA; 2019.

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    • Export Citation
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    Lee AS, de Lencastre H, Garau J, Kluytmans J, Malhotra-Kumar S, Peschel A, et al. Methicillin-resistant staphylococcus aureus. Nat Rev Dis Primers 2018; 4, 18033.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    John MA, Burden J, Stuart JI, Reyes RC, Lannigan R, Milburn S, et al. Comparison of three phenotypic techniques for detection of methicillin resistance in staphylococcus spp. Reveals a species-dependent performance. J Antimicrob Chemother 2009; 63: 493496.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Larsen MV, Cosentino S, Rasmussen S, Friis C, Hasman H, Marvig RL, et al. Multilocus sequence typing of total-genome-sequenced bacteria. J Clin Microbiol 2012; 50: 13551361.

    • PubMed
    • Search Google Scholar
    • Export Citation
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    Bortolaia V, Kaas RS, Ruppe E, Roberts MC, Schwarz S, Cattoir V, et al. Resfinder 4.0 for predictions of phenotypes from genotypes. J Antimicrob Chemother 2020; 75: 34913500.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Alcock BP, Raphenya AR, Lau TTY, Tsang KK, Bouchard M, Edalatmand A, et al. Antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res 2020; 48: 517525.

    • Search Google Scholar
    • Export Citation
  • 26.

    Joensen KG, Scheutz F, Lund O, Hasman H, Kaas RS, Nielsen EM, et al. Real-time whole-genome sequencing for routine typing, surveillance, and outbreak detection of verotoxigenic escherichia coli. J Clin Microbiol 2014; 52: 15011510.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Carattoli A, Zankari E, Garcia-Fernandez A, Voldby Larsen M, Lund O, Villa L, et al. silico detection and typing of plasmids using plasmidfinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother 2014; 58: 38953903.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Love NK, Pichon B, Padfield S, Hughes GJ. A persistent recurring cluster of meticillin-resistant staphylococcus aureus (mrsa) colonizations in a special care baby unit: a matched case-control study. J Hosp Infect 2020; 106: 774781.

    • Search Google Scholar
    • Export Citation
  • 29.

    Hajikhani B, Goudarzi M, Kakavandi S, Amini S, Zamani S, van Belkum A, et al. The global prevalence of fusidic acid resistance in clinical isolates of staphylococcus aureus: a systematic review and meta-analysis. Antimicrob Resist Infect Control 2021; 10: 75.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Kresken M, Hafner D, Schmitz FJ, Wichelhaus TA, Paul-Ehrlich-Society for C. Prevalence of mupirocin resistance in clinical isolates of staphylococcus aureus and staphylococcus epidermidis: results of the antimicrobial resistance surveillance study of the Paul-ehrlich-society for chemotherapy, 2001. Int J Antimicrob Agents 2004; 23: 577581.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Bes TM, Perdigao-Neto L, Martins RR, Heijden I, Trindade PA, Camilo G, et al. Susceptibility to chlorhexidine and mupirocin among methicillin-resistant staphylococcus aureus clinical isolates from a teaching hospital. Rev Inst Med Trop Sao Paulo 2021; 63: e27.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Antonelli A, Giani T, Coppi M, Di Pilato V, Arena F, Colavecchio OL, et al. Staphylococcus aureus from hospital-acquired pneumonia from an Italian nationwide survey: activity of ceftobiprole and other anti-staphylococcal agents, and molecular epidemiology of methicillin-resistant isolates. J Antimicrob Chemother 2019; 74: 34533461.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    Cong Y, Yang S, Rao X. Vancomycin resistant staphylococcus aureus infections: A review of case updating and clinical features. J Adv Res 2020; 21: 169176.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34.

    Beibei L, Yun C, Mengli C, Nan B, Xuhong Y, Rui W. Linezolid versus vancomycin for the treatment of gram-positive bacterial infections: Meta-analysis of randomised controlled trials. Int J Antimicrob Agents 2010; 35: 312.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35.

    Chen H, Li L, Wu M, Xu S, Wang M, Li J, et al. Efficacy and safety of linezolid versus teicoplanin for the treatment of mrsa infections: A meta-analysis. J Infect Dev Ctries 2018; 11: 926934.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36.

    Tkadlec J, Capek V, Brajerova M, Smelikova E, Melter O, Bergerova T, et al. The molecular epidemiology of methicillin-resistant staphylococcus aureus (mrsa) in the Czech republic. J Antimicrob Chemother 2021; 76: 5564.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37.

    Engelthaler DM, Kelley E, Driebe EM, Bowers J, Eberhard CF, Trujillo J, et al. Rapid and robust phylotyping of spa t003, a dominant mrsa clone in Luxembourg and other european countries. BMC Infect Dis 2013; 13: 339.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38.

    Cortes MF, Costa MO, Lima NC, Souza RC, Almeida LG, Guedes LPC, et al. Complete genome sequence of community-associated methicillin-resistant staphylococcus aureus (strain USA400-0051), a prototype of the USA400 clone. Mem Inst Oswaldo Cruz 2017; 112: 790792.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39.

    Yu F, Cienfuegos-Gallet AV, Cunningham MH, Jin Y, Wang B, Kreiswirth BN, et al. Molecular evolution and adaptation of livestock-associated methicillin-resistant staphylococcus aureus (la-mrsa) sequence type 9. mSystems 2021; 6, e0049221.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40.

    Shukla SK, Karow ME, Brady JM, Stemper ME, Kislow J, Moore N, et al. Virulence genes and genotypic associations in nasal carriage, community-associated methicillin-susceptible and methicillin-resistant USA400 staphylococcus aureus isolates. J Clin Microbiol 2010; 48: 35823592.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41.

    Price LB, Stegger M, Hasman H, Aziz M, Larsen J, Andersen PS, et al. Staphylococcus aureus cc398: Host adaptation and emergence of methicillin resistance in livestock. mBio 2012; 3.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42.

    Jin Y, Yu X, Chen Y, Chen W, Shen P, Luo Q, et al. Characterization of highly virulent community-associated methicillin-resistant staphylococcus aureus st9-sccmec xii causing bloodstream infection in China. Emerg Microbes Infect 2020; 9: 25262535.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43.

    Monecke S, Slickers P, Gawlik D, Muller E, Reissig A, Ruppelt-Lorz A, et al. Molecular typing of st239-mrsa-iii from diverse geographic locations and the evolution of the sccmec iii element during its intercontinental spread. Front Microbiol 2018; 9: 1436.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44.

    Monaco M, Pedroni P, Sanchini A, Bonomini A, Indelicato A, Pantosti A. Livestock-associated methicillin-resistant staphylococcus aureus responsible for human colonization and infection in an area of Italy with high density of pig farming. BMC Infect Dis 2013; 13: 258.

    • Search Google Scholar
    • Export Citation
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Senior editors

Editor-in-Chief: Prof. Dóra Szabó (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)

Managing Editor: Dr. Béla Kocsis (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)

Co-editor: Dr. Andrea Horváth (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)

Editorial Board

  • Prof. Éva ÁDÁM (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)
  • Prof. Sebastian AMYES (Department of Medical Microbiology, University of Edinburgh, Edinburgh, UK.)
  • Dr. Katalin BURIÁN (Institute of Clinical Microbiology University of Szeged, Szeged, Hungary; Department of Medical Microbiology and Immunobiology, University of Szeged, Szeged, Hungary.)
  • Dr. Orsolya DOBAY (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)
  • Prof. Ildikó Rita DUNAY (Institute of Inflammation and Neurodegeneration, Medical Faculty, Otto-von-Guericke University, Magdeburg, Germany; Center for Behavioral Brain Sciences (CBBS), Magdeburg, Germany)
  • Prof. Levente EMŐDY(Department of Medical Microbiology and Immunology, University of Pécs, Pécs, Hungary.)
  • Prof. Anna ERDEI (Department of Immunology, Eötvös Loránd University, Budapest, Hungary, MTA-ELTE Immunology Research Group, Eötvös Loránd University, Budapest, Hungary.)
  • Prof. Éva Mária FENYŐ (Division of Medical Microbiology, University of Lund, Lund, Sweden)
  • Prof. László FODOR (Department of Microbiology and Infectious Diseases, University of Veterinary Medicine, Budapest, Hungary)
  • Prof. József KÓNYA (Department of Medical Microbiology, University of Debrecen, Debrecen, Hungary)
  • Prof. Yvette MÁNDI (Department of Medical Microbiology and Immunobiology, University of Szeged, Szeged, Hungary)
  • Prof. Károly MÁRIALIGETI (Department of Microbiology, Eötvös Loránd University, Budapest, Hungary)
  • Prof. János MINÁROVITS (Department of Oral Biology and Experimental Dental Research, University of Szeged, Szeged, Hungary)
  • Prof. Béla NAGY (Centre for Agricultural Research, Institute for Veterinary Medical Research, Budapest, Hungary.)
  • Prof. István NÁSZ (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)
  • Prof. Kristóf NÉKÁM (Hospital of the Hospitaller Brothers in Buda, Budapest, Hungary.)
  • Dr. Eszter OSTORHÁZI (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)
  • Prof. Rozália PUSZTAI (Department of Medical Microbiology and Immunobiology, University of Szeged, Szeged, Hungary)
  • Prof. Peter L. RÁDY (Department of Dermatology, University of Texas, Houston, Texas, USA)
  • Prof. Éva RAJNAVÖLGYI (Department of Immunology, Faculty of Medicine, University of Debrecen, Debrecen, Hungary)
  • Prof. Ferenc ROZGONYI (Institute of Laboratory Medicine, Semmelweis University, Budapest, Hungary)
  • Prof. Joseph G. SINKOVICS (The Cancer Institute, St. Joseph’s Hospital, Tampa, Florida, USA)
  • Prof. Júlia SZEKERES (Department of Medical Biology, University of Pécs, Pécs, Hungary.)
  • Prof. Mária TAKÁCS (National Reference Laboratory for Viral Zoonoses, National Public Health Center, Budapest, Hungary.)
  • Prof. Edit URBÁN (Department of Medical Microbiology and Immunology University of Pécs, Pécs, Hungary; Institute of Translational Medicine, University of Pécs, Pécs, Hungary.)

 

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Acta Microbiologica et Immunologica Hungarica
Language English
Size A4
Year of
Foundation
1954
Volumes
per Year
1
Issues
per Year
4
Founder Magyar Tudományos Akadémia
Founder's
Address
H-1051 Budapest, Hungary, Széchenyi István tér 9.
Publisher Akadémiai Kiadó
Publisher's
Address
H-1117 Budapest, Hungary 1516 Budapest, PO Box 245.
Responsible
Publisher
Chief Executive Officer, Akadémiai Kiadó
ISSN 1217-8950 (Print)
ISSN 1588-2640 (Online)

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