Abstract
Introduction
Methicillin-resistant Staphy lococcus 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.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Tong SY , Davis JS , Eichenberger E , Holland TL , Fowler VG Jr. Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management. Clin Microbiol Rev 2015; 28: 603–661.
-
2.
Maltezou HC , Giamarellou H . Community-acquired methicillin-resistant staphylococcus aureus infections. Int J Antimicrob Agents 2006; 27: 87–96.
-
3.
Antimicrobial resistance in the eu/eea (ears-net) -annual epidemiological report 2019. European Centre for Disease Prevention and Control. 2020; Available from: www.ecdc.europa.eu/sites/default/files/documents/surveillance-antimicrobial-resistance-Europe-2019.pdf.
-
4.
Kaya H , Hasman H , Larsen J , Stegger M , Johannesen TB , Allesoe RL , et al. Sccmecfinder, a web-based tool for typing of staphylococcal cassette chromosome mec in staphylococcus aureus using whole-genome sequence data. mSphere 2018; 3.
-
5.
Enright MC , Day NP , Davies CE , Peacock SJ , Spratt BG . Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of staphylococcus aureus. J Clin Microbiol 2000; 38: 1008–1015.
-
6.
Bosch T , van Luit M , Pluister GN , Frentz D , Haenen A , Landman F , et al. Changing characteristics of livestock-associated meticillin-resistant staphylococcus aureus isolated from humans - emergence of a subclade transmitted without livestock exposure, The Netherlands, 2003 to 2014. Euro Surveill 2016: 21.
-
7.
Satta G , Ling CL , Cunningham ES , McHugh TD , Hopkins S . Utility and limitations of spa-typing in understanding the epidemiology of staphylococcus aureus bacteraemia isolates in a single university hospital. BMC Res Notes 2013; 6: 398.
-
8.
Nikolaras GP , Papaparaskevas J , Samarkos M , Tzouvelekis LS , Psychogiou M , Pavlopoulou I , et al. Changes in the rates and population structure of methicillin-resistant staphylococcus aureus (mrsa) from bloodstream infections: a single-centre experience (2000-2015). J Glob Antimicrob Resist 2019; 17: 117–122.
-
9.
Kachrimanidou M , Tsorlini E , Katsifa E , Vlachou S , Kyriakidou S , Xanthopoulou K , et al. Prevalence and molecular epidemiology of methicillin-resistant staphylococcus aureus in a tertiary Greek hospital. Hippokratia 2014; 18: 24–27.
-
10.
Asadollahi P , Farahani NN , Mirzaii M , Khoramrooz SS , van Belkum A , Asadollahi K , et al. Distribution of the most prevalent spa types among clinical isolates of methicillin-resistant and -susceptible staphylococcus aureus around the world: A review. Front Microbiol 2018; 9: 163.
-
11.
Voss A , Loeffen F , Bakker J , Klaassen C , Wulf M . Methicillin-resistant staphylococcus aureus in pig farming. Emerg Infect Dis 2005; 11: 1965–1966.
-
12.
Larsen J , Petersen A , Larsen AR , Sieber RN , Stegger M , Koch A , et al. Emergence of livestock-associated methicillin-resistant staphylococcus aureus bloodstream infections in Denmark. Clin Infect Dis 2017; 65: 1072–1076.
-
13.
Leekha S , O'Hara LM , Sbarra A , Li S , Harris AD . Comparison of surveillance and clinical cultures to measure the impact of infection control interventions on the incidence of methicillin-resistant staphylococcus aureus and vancomycin-resistant enterococcus in the hospital. Infect Control Hosp Epidemiol 2020; 41: 161–165.
-
14.
McManus BA , Aloba BK , Earls MR , Brennan GI , O'Connell B , Monecke S , et al. Multiple distinct outbreaks of panton-valentine leucocidin-positive community-associated meticillin-resistant staphylococcus aureus in Ireland investigated by whole-genome sequencing. J Hosp Infect 2021; 108: 72–80.
-
15.
Sarrou S , Malli E , Tsilipounidaki K , Florou Z , Medvecky M , Skoulakis A , et al. Mlsb-resistant staphylococcus aureus in central Greece: rate of resistance and molecular characterization. Microb Drug Resist 2019; 25: 543–550.
-
16.
Sabat AJ , Pournaras S , Akkerboom V , Tsakris A , Grundmann H , Friedrich AW . Whole-genome analysis of an oxacillin-susceptible cc80 meca-positive staphylococcus aureus clinical isolate: Insights into the mechanisms of cryptic methicillin resistance. J Antimicrob Chemother 2015; 70: 2956–2964.
-
17.
Karampatakis T , Papadopoulos P , Tsergouli K , Angelidis AS , Sergelidis D , Papa A . Genetic characterization of two methicillin-resistant Staphylococcus aureus spa type t127 strains isolated from workers in the dairy production chain in Greece. Acta Microbiol Immunol Hung 2021; 68: 189–194.
-
18.
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: 2091–2096.
-
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.
-
20.
CLSI . Performance Standards for antimicrobial susceptibility testing: twenty-fifth informational supplement M100-S29. CLSI. Wayne, P.A., USA; 2019.
-
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.
-
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: 493–496.
-
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: 1355–1361.
-
24.
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: 3491–3500.
-
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: 517–525.
-
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: 1501–1510.
-
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: 3895–3903.
-
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: 774–781.
-
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.
-
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: 577–581.
-
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.
-
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: 3453–3461.
-
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: 169–176.
-
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: 3–12.
-
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: 926–934.
-
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: 55–64.
-
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.
-
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: 790–792.
-
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.
-
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: 3582–3592.
-
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.
-
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: 2526–2535.
-
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.
-
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.
Please, download the file from HERE
Editorial Office:
Akadémiai Kiadó Zrt.
Budafoki út 187-187, A/3, H-1117 Budapest, Hungary
Editorial Correspondence:
Acta Microbiologica et Immunologica Hungarica
Institute of Medical Microbiology
Semmelweis University
P.O. Box 370
H-1445 Budapest, Hungary
Phone: + 36 1 459 1500 ext. 56101
Fax: (36 1) 210 2959
E-mail: amih@med.semmelweis-univ.hu
Indexing and Abstracting Services:
- Biological Abstracts
- BIOSIS Previews
- CAB Abstracts
- CABELLS Journalytics
- Chemical Abstracts
- Global Health
- Index Medicus
- Index Veterinarius
- Medline
- Referativnyi Zhurnal
- SCOPUS
- Science Citation Index Expanded
| 2021 | |
|---|---|
| Web of Science | |
| Total Cites WoS |
696 |
| Journal Impact Factor | 2,298 |
| Rank by Impact Factor | Immunology 141/161 Microbiology 118/136 |
| Impact Factor without Journal Self Cites |
2,143 |
| 5 Year Impact Factor |
1,925 |
| Journal Citation Indicator | 0,39 |
| Rank by Journal Citation Indicator | Immunology 146/177 Microbiology 129/157 |
| Scimago | |
| Scimago H-index |
29 |
| Scimago Journal Rank |
0,362 |
| Scimago Quartile Score | Immunology and Microbiology (miscellaneous) (Q3) Medicine (miscellaneous) (Q3) |
| Scopus | |
| Scopus Cite Score |
3,6 |
| Scopus CIte Score Rank |
General Immunology and Microbiology 26/56 (Q2) Infectious Diseases 149/295 (Q3) Microbiology (medical) 66/118 (Q3) |
| Scopus SNIP |
0,598 |
| 2020 | |
| Total Cites | 662 |
| WoS | |
| Journal Impact Factor |
2,048 |
| Rank by | Immunology 145/162(Q4) |
| Impact Factor | Microbiology 118/137 (Q4) |
| Impact Factor | 1,904 |
| without | |
| Journal Self Cites | |
| 5 Year | 0,671 |
| Impact Factor | |
| Journal | 0,38 |
| Citation Indicator | |
| Rank by Journal | Immunology 146/174 (Q4) |
| Citation Indicator | Microbiology 120/142 (Q4) |
| Citable | 42 |
| Items | |
| Total | 40 |
| Articles | |
| Total | 2 |
| Reviews | |
| Scimago | 28 |
| H-index | |
| Scimago | 0,439 |
| Journal Rank | |
| Scimago | Immunology and Microbiology (miscellaneous) Q4 |
| Quartile Score | Medicine (miscellaneous) Q3 |
| Scopus | 438/167=2,6 |
| Scite Score | |
| Scopus | General Immunology and Microbiology 31/45 (Q3) |
| Scite Score Rank | |
| Scopus | 0,760 |
| SNIP | |
| Days from | 225 |
| submission | |
| to acceptance | |
| Days from | 118 |
| acceptance | |
| to publication | |
| Acceptance | 19% |
| Rate |
| 2019 | |
|---|---|
| Total Cites WoS |
485 |
| Impact Factor | 1,086 |
| Impact Factor without Journal Self Cites |
0,864 |
| 5 Year Impact Factor |
1,233 |
| Immediacy Index |
0,286 |
| Citable Items |
42 |
| Total Articles |
40 |
| Total Reviews |
2 |
| Cited Half-Life |
5,8 |
| Citing Half-Life |
7,7 |
| Eigenfactor Score |
0,00059 |
| Article Influence Score |
0,246 |
| % Articles in Citable Items |
95,24 |
| Normalized Eigenfactor |
0,07317 |
| Average IF Percentile |
7,690 |
| Scimago H-index |
27 |
| Scimago Journal Rank |
0,352 |
| Scopus Scite Score |
320/161=2 |
| Scopus Scite Score Rank |
General Immunology and Microbiology 35/45 (Q4) |
| Scopus SNIP |
0,492 |
| Acceptance Rate |
16% |
| Acta Microbiologica et Immunologica Hungarica | |
|---|---|
| Publication Model | Online only Hybrid |
| Submission Fee | none |
| Article Processing Charge | 1100 EUR/article |
| Regional discounts on country of the funding agency | World Bank Lower-middle-income economies: 50% World Bank Low-income economies: 100% |
| Further Discounts | Editorial Board / Advisory Board members: 50% Corresponding authors, affiliated to an EISZ member institution subscribing to the journal package of Akadémiai Kiadó: 100% |
| Subscription fee 2023 | Online subsscription: 680 EUR / 832 USD Print + online subscription: 760 EUR / 930 USD |
| Subscription Information | Online subscribers are entitled access to all back issues published by Akadémiai Kiadó for each title for the duration of the subscription, as well as Online First content for the subscribed content. |
| Purchase per Title | Individual articles are sold on the displayed price. |
| 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) |
Monthly Content Usage
| Abstract Views | Full Text Views | PDF Downloads | |
|---|---|---|---|
| Oct 2022 | 115 | 5 | 6 |
| Nov 2022 | 60 | 0 | 0 |
| Dec 2022 | 23 | 0 | 0 |
| Jan 2023 | 85 | 0 | 0 |
| Feb 2023 | 34 | 1 | 2 |
| Mar 2023 | 5 | 0 | 0 |
| Apr 2023 | 0 | 0 | 0 |
Copyright Akadémiai Kiadó
AKJournals is the trademark of Akadémiai Kiadó's journal publishing business branch.
Copyright Akadémiai Kiadó AKJournals is the trademark of Akadémiai Kiadó's journal publishing business branch.
Powered by PubFactory