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. 2024 Oct 10;13(10):953. doi: 10.3390/antibiotics13100953

Molecular Evolution and Pathogenicity of Methicillin-Resistant Staphylococcus aureus

Kunyan Zhang 1,2,3,4,5
PMCID: PMC11505331  PMID: 39452219

Staphylococcus aureus is a Gram-positive and coagulase-positive pathogen, belonging to the Staphylococcaceae family. It has the capability to acquire resistance to most antibiotics and to collect virulence factors [1,2,3]. This ability is further augmented by the constant emergence of new clones [1,4]. Historically, penicillin-resistant S. aureus emerged in 1942 within two years of the introduction of penicillin [5,6,7,8]. A semi-synthetic antibiotic, methicillin, was then developed to act as a substitute for the treatment of penicillin-resistant S. aureus. However, methicillin-resistant S. aureus (MRSA) was clinically identified in 1960 shortly after its introduction in 1959 [9]. Thereafter, worldwide outbreaks of MRSA have occurred in waves [10,11,12,13,14,15,16,17,18,19,20,21,22,23,24]. The dissemination of MRSA is marked by the propagation of a number of clones harboring specific genetic backgrounds in different continents [1,18,25,26,27,28,29,30,31,32,33]. Although most MRSA strains are hospital-acquired originally, community-associated strains (CA-MRSA) have now been increasingly recognized worldwide and are both phenotypically and genotypically different from hospital-associated (HA)-MRSA [1,34,35,36,37,38,39,40]. The importance of livestock-associated (LA)-MRSA has also been frequently reported since the mid-2000s [41,42,43]. Infections due to MRSA, in particular CA-MRSA and LA-MRSA, are associated with more severity and higher mortality rate compared to infections caused by methicillin-susceptible strains [22,44,45,46,47,48].

Staphylococci consist of more than 45 staphylococcal species (Staphylococcus spp.), especially coagulase-negative staphylococci (CoNS). Although most CoNS are harmless and exist as opportunistic pathogens on the skin and mucous membranes of human and other animals, their significance has been boosted with an increasing number of CoNS infections identified, in particular their role in the evolution and pathogenicity of MRSA [49,50,51,52].

In this Special Issue, there were a total of 13 papers including 10 research articles [Contributions 1,3,5–8,10–13] and 3 review/perspective articles [Contributions 2,4,9], with a wide spectrum of staphylococcal research, covering the latest advances in molecular epidemiology, evolution, and pathogenicity of staphylococci.

MRSA molecular epidemiological data from less developed countries are limited. In this Special Issue, Ullah et al. [Contribution 1] described an emerging MRSA strain, ST113-MRSA-IV, which is closely related to ST8 and multi-drug resistance in Pakistan and provided detailed genomic comparative information for this strain. Chai et al. [Contribution 3] investigated the prevalence, antibiogram, and genomic characteristics of methicillin-susceptible S. aureus (MSSA) and MRSA isolated from animal handlers in Peninsular Malaysia and provided background information for further studies on the transmission of S. aureus between animals and humans. Hwang [Contribution 11] showed a general distribution of the major MRSA strains in the Republic of Korea from 1994 to 2020.

For LA-MRSA, Leão et al. [Contribution 6] reported the emergence of a cfr-mediated linezolid-resistant LA-MRSA strain, ST398-t011-MRSA-Vc, from healthy pigs in Portugal. Iurescia et al. [Contribution 8] investigated the genomic variants in association with the linezolid-resistant phenotype in the cfr-mediated linezolid-resistant LA-MRSA isolates from Italian pig farms. These studies implied a transmission risk from livestock to humans by the presence of cfr-positive LA-MRSA and indicated the importance of continuous genomic surveillance of cfr-positive LA-MRSA.

Plasmids and phagemids play a crucial role in MRSA evolution and adaptation, as well as the acquisition and spread of antimicrobial resistance and virulence genes. Al-Trad et al. [Contribution 10] explored the plasmid profiles of the clinical MRSA isolates during the period from 2016 to 2020 obtained from a tertiary hospital in the state of Terengganu, Malaysia. Saei et al. [Contribution 12] gave details of the role of prophage ϕSa3 in the adaption of S. aureus ST398 sub-lineages from human to animal hosts.

In the virulence realm, Pulia et al. [Contribution 5] studied the staphylococcal virulence gene’s expression in situ in human skin and soft tissue infection patients from two medical centers in Wisconsin, USA, and demonstrated a relative increase in the transcripts of several toxins, adhesion, and regulatory genes. Kim et al. [Contribution 7] used DNA affinity capture assay (DACA) to study the MRSA virulence factor and antibiotic resistance regulation. They showed that the SarA protein bound to all mecA, sarA, and sarR promoters, and the sarA truncated mutant weakened antibiotic resistance to oxacillin and reduced biofilm formation. Phenol-soluble modulin (PSM) belongs to the peptide toxins superfamily and possesses similar alpha-helical and amphipathic secondary structures. It plays significant roles in the pathogenesis of S. aureus and S. epidermidis through its pro-inflammatory, cytolytic, and biofilm-structuring functions. The methicillin resistance-associated PSM locus (psm-mec) is found in the class A mec gene complex within the staphylococcal chromosome cassette mec (SCCmec) in many staphylococcal species. Cheung et al. [Contribution 13] characterized the SCCmec elements from methicillin-resistant S. pseudintermedius (MRSP) isolates representing the four major lineages in the United States and gained insights into the composition of SCCmec elements in MRSP. In particular, this group reported that PSM-mec was expressed in some specific methicillin-resistant isolates of S. pseudintermedius and laid the genetic foundation for further elucidating the SCCmec-encoded virulence and resistance factors.

For the review/perspective, Uehara [Contribution 2] gave an update on the current status of SCCmec. Tenover and Tickler [Contribution 4] commented on the current molecular approaches for rapid detection of MRSA/MSSA in various clinical specimens. De Rose et al. [Contribution 9] reviewed the recent literature on the management of neonatal staphylococcal skin infections and discussed the most appropriate clinical approaches based on four cases of neonatal blistering diseases with staphylococcal infections.

S. aureus, including MRSA and MSSA, will remain a major human and animal pathogen. Further research on molecular evolution, epidemiology, characterization, and pathogenicity of staphylococci is needed to obtain a better understanding of the emerging trends in antibiotic resistance and virulence and to therefore control infections caused by this pathogen.

Conflicts of Interest

The author declares no conflict of interest.

List of Contributions

  1. Ullah, N.; Dar, H.A.; Naz, K.; Andleeb, S.; Rahman, A.; Saeed, M.T.; Hanan, F.; Bae, T.; Ali, A. Genomic investigation of methicillin-resistant Staphylococcus aureus ST113 strains isolated from tertiary care hospitals in Pakistan. Antibiotics 2021, 10, 1121. https://doi.org/10.3390/antibiotics10091121.

  2. Uehara, Y. Current status of staphylococcal cassette chromosome mec (SCCmec). Antibiotics 2022, 11, 86. https://doi.org/10.3390/antibiotics11010086.

  3. Chai, M.; Sukiman, M.Z.; Kamarun Baharin, A.H.; Ramlan, I.; Lai, L.Z.; Liew, Y.; Malayandy, P.; Mohamad, N.M.; Choong, S.; Ariffin, S.M.Z.; et al. Methicillin-Resistant Staphylococcus aureus from peninsular Malaysian animal handlers: Molecular profile, antimicrobial resistance, immune evasion cluster and genotypic categorization. Antibiotics 2022, 11, 103. https://doi.org/10.3390/antibiotics11010103.

  4. Tenover, F.C.; Tickler, I.A. Detection of methicillin-resistant Staphylococcus aureus infections using molecular methods. Antibiotics 2022, 11, 239. https://doi.org/10.3390/antibiotics11020239.

  5. Pulia, M.S.; Anderson, J.; Ye, Z.; Elsayed, N.S.; Le, T.; Patitucci, J.; Ganta, K.; Hall, M.; Singh, V.K.; Shukla, S.K. Expression of staphylococcal virulence genes in situ in human skin and soft tissue infections. Antibiotics 2022, 11, 527. https://doi.org/10.3390/antibiotics11040527.

  6. Leão, C.; Clemente, L.; Cara d’Anjo, M.; Albuquerque, T.; Amaro, A. Emergence of cfr-mediated linezolid resistance among livestock-associated methicillin-resistant Staphylococcus aureus (LA-MRSA) from healthy pigs in Portugal. Antibiotics 2022, 11, 1439. https://doi.org/10.3390/antibiotics11101439.

  7. Kim, B.; Lee, H.-J.; Jo, S.-H.; Kim, M.-G.; Lee, Y.; Lee, W.; Kim, W.; Joo, H.-S.; Kim, Y.-G.; Kim, J.-S.; et al. Study of sarA by DNA affinity capture assay (DACA) employing three promoters of key virulence and resistance genes in methicillin-resistant Staphylococcus aureus. Antibiotics 2022, 11, 1714. https://doi.org/10.3390/antibiotics11121714.

  8. Iurescia, M.; Diaconu, E.L.; Alba, P.; Feltrin, F.; Buccella, C.; Onorati, R.; Giacomi, A.; Caprioli, A.; Franco, A.; Battisti, A.; et al. Genomics insight into cfr-mediated linezolid-resistant LA-MRSA in Italian pig holdings. Antibiotics 2023, 12, 530. https://doi.org/10.3390/antibiotics12030530.

  9. De Rose, D.U.; Pugnaloni, F.; Martini, L.; Bersani, I.; Ronchetti, M.P.; Diociaiuti, A.; El Hachem, M.; Dotta, A.; Auriti, C. Staphylococcal infections and neonatal skin: Data from literature and suggestions for the clinical management from four challenging patients. Antibiotics 2023, 12, 632. https://doi.org/10.3390/antibiotics12040632.

  10. Al-Trad, E.I.; Chew, C.H.; Che Hamzah, A.M.; Suhaili, Z.; Rahman, N.I.A.; Ismail, S.; Puah, S.M.; Chua, K.H.; Kwong, S.M.; Yeo, C.C. The plasmidomic landscape of clinical methicillin-resistant Staphylococcus aureus isolates from Malaysia. Antibiotics 2023, 12, 733. https://doi.org/10.3390/antibiotics12040733.

  11. Hwang, Y.-J. Comparing the phylogenetic distribution of multilocus sequence typing, staphylococcal protein A, and staphylococcal cassette chromosome mec types in methicillin-resistant Staphylococcus aureus (MRSA) in Korea from 1994 to 2020. Antibiotics 2023, 12, 1397. https://doi.org/10.3390/antibiotics12091397.

  12. Saei, H.D.; McClure, J.; Kashif, A.; Chen, S.; Conly, J.M.; Zhang, K. The role of prophage φSa3 in the adaption of Staphylococcus aureus ST398 sublineages from human to animal hosts. Antibiotics 2024, 13, 112. https://doi.org/10.3390/antibiotics13020112.

  13. Cheung, G.Y.C.; Lee, J.H.; Liu, R.; Lawhon, S.D.; Yang, C.; Otto, M. Methicillin resistance elements in the canine pathogen Staphylococcus pseudintermedius and their association with the peptide toxin PSM-mec. Antibiotics 2024, 13, 130. https://doi.org/10.3390/antibiotics13020130.

Footnotes

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References

  • 1.Lakhundi S., Zhang K. Methicillin-resistant Staphylococcus aureus: Molecular characterization, evolution, and epidemiology. Clin. Microbiol. Rev. 2018;31:4. doi: 10.1128/CMR.00020-18. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Howden B.P., Giulieri S.G., Wong Fok Lung T., Baines S.L., Sharkey L.K., Lee J.Y.H., Hachani A., Monk I.R., Stinear T.P. Staphylococcus aureus host interactions and adaptation. Nat. Rev. Microbiol. 2023;21:380–395. doi: 10.1038/s41579-023-00852-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Vestergaard M., Frees D., Ingmer H. Antibiotic resistance and the MRSA problem. Microbiol. Spectr. 2019;7:GPP3-0057-2018. doi: 10.1128/microbiolspec.GPP3-0057-2018. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Turner N.A., Sharma-Kuinkel B.K., Maskarinec S.A., Eichenberger E.M., Shah P.P., Carugati M., Holland T.L., Fowler V.G., Jr. Methicillin-resistant Staphylococcus aureus: An overview of basic and clinical research. Nat. Rev. Microbiol. 2019;17:203–218. doi: 10.1038/s41579-018-0147-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5.Kirby W.M. Extraction of a highly potent penicillin inactivator from penicillin resistant staphylococci. Science. 1944;99:452–453. doi: 10.1126/science.99.2579.452. [DOI] [PubMed] [Google Scholar]
  • 6.Lowy F.D. Antimicrobial resistance: The example of Staphylococcus aureus. J. Clin. Investig. 2003;111:1265–1273. doi: 10.1172/JCI18535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.Rammelkamp C.H., Maxon T. Resistance of Staphylococcus aureus to the action of penicillin. Proc. Soc. Exp. Biol. Med. 1942;51:386–389. doi: 10.3181/00379727-51-13986. [DOI] [Google Scholar]
  • 8.Bondi A., Jr., Dietz C.C. Penicillin resistant staphylococci. Proc. Soc. Exp. Biol. Med. 1945;60:55–58. doi: 10.3181/00379727-60-15089. [DOI] [PubMed] [Google Scholar]
  • 9.Jevons M.P. “Celbenin”-resistant Staphylococci. Br. Med. J. 1961;1:124–125. doi: 10.1136/bmj.1.5219.124-a. [DOI] [Google Scholar]
  • 10.Thompson R.L., Cabezudo I., Wenzel R.P. Epidemiology of nosocomial infections caused by methicillin-resistant Staphylococcus aureus. Ann. Intern. Med. 1982;97:309–317. doi: 10.7326/0003-4819-97-3-309. [DOI] [PubMed] [Google Scholar]
  • 11.Hanifah Y.A., Hiramatsu K., Yokota T. Characterization of methicillin-resistant Staphylococcus aureus associated with nosocomial infections in the University Hospital, Kuala Lumpur. J. Hosp. Infect. 1992;21:15–28. doi: 10.1016/0195-6701(92)90150-K. [DOI] [PubMed] [Google Scholar]
  • 12.Faoagali J.L., Thong M.L., Grant D. Ten years’ experience with methicillin-resistant Staphylococcus aureus in a large Australian hospital. J. Hosp. Infect. 1992;20:113–119. doi: 10.1016/0195-6701(92)90113-Z. [DOI] [PubMed] [Google Scholar]
  • 13.Cafferkey M.T., Hone R., Coleman D., Pomeroy H., McGrath B., Ruddy R., Keane C.T. Methicillin-resistant Staphylococcus aureus in Dublin 1971-84. Lancet. 1985;2:705–708. doi: 10.1016/S0140-6736(85)92942-3. [DOI] [PubMed] [Google Scholar]
  • 14.Bradley J.M., Noone P., Townsend D.E., Grubb W.B. Methicillin-resistant Staphylococcus aureus in a London hospital. Lancet. 1985;1:1493–1495. doi: 10.1016/S0140-6736(85)92263-9. [DOI] [PubMed] [Google Scholar]
  • 15.Torvaldsen S., Roberts C., Riley T.V. The continuing evolution of methicillin-resistant Staphylococcus aureus in Western Australia. Infect. Control Hosp. Epidemiol. 1999;20:133–135. doi: 10.1086/501594. [DOI] [PubMed] [Google Scholar]
  • 16.Tiemersma E.W., Bronzwaer S.L., Lyytikainen O., Degener J.E., Schrijnemakers P., Bruinsma N., Monen J., Witte W., Grundman H. European Antimicrobial Resistance Surveillance System Participants. Methicillin-resistant Staphylococcus aureus in Europe, 1999–2002. Emerg. Infect. Dis. 2004;10:1627–1634. doi: 10.3201/eid1009.040069. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Takizawa Y., Taneike I., Nakagawa S., Oishi T., Nitahara Y., Iwakura N., Ozaki K., Takano M., Nakayama T., Yamamoto T. A Panton-Valentine leucocidin (PVL)-positive community-acquired methicillin-resistant Staphylococcus aureus (MRSA) strain, another such strain carrying a multiple-drug resistance plasmid, and other more-typical PVL-negative MRSA strains found in Japan. J. Clin. Microbiol. 2005;43:3356–3363. doi: 10.1128/JCM.43.7.3356-3363.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Song J.H., Hsueh P.R., Chung D.R., Ko K.S., Kang C.I., Peck K.R., Yeom J.S., Kim S.W., Chang H.H., Kim Y.S., et al. Spread of methicillin-resistant Staphylococcus aureus between the community and the hospitals in Asian countries: An ANSORP study. J. Antimicrob. Chemother. 2011;66:1061–1069. doi: 10.1093/jac/dkr024. [DOI] [PubMed] [Google Scholar]
  • 19.Rountree P.M., Beard M.A. Hospital strains of Staphylococcus aureus, with particular reference to methicillin-resistant strains. Med. J. Aust. 1968;2:1163–1168. doi: 10.5694/j.1326-5377.1968.tb83502.x. [DOI] [PubMed] [Google Scholar]
  • 20.Kerttula A.M., Lyytikainen O., Karden-Lilja M., Ibrahem S., Salmenlinna S., Virolainen A., Vuopio-Varkila J. Nationwide trends in molecular epidemiology of methicillin-resistant Staphylococcus aureus, Finland, 1997–2004. BMC Infect. Dis. 2007;7:94. doi: 10.1186/1471-2334-7-94. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Kayaba H., Kodama K., Tamura H., Fujiwara Y. The spread of methicillin-resistant Staphylococcus aureus in a rural community: Will it become a common microorganism colonizing among the general population? Surg. Today. 1997;27:217–219. doi: 10.1007/BF00941648. [DOI] [PubMed] [Google Scholar]
  • 22.Griffiths C., Lamagni T.L., Crowcroft N.S., Duckworth G., Rooney C. Trends in MRSA in England and Wales: Analysis of morbidity and mortality data for 1993–2002. Health Stat. Q. 2004;21:15–22. [PubMed] [Google Scholar]
  • 23.Givney R., Vickery A., Holliday A., Pegler M., Benn R. Evolution of an endemic methicillin-resistant Staphylococcus aureus population in an Australian hospital from 1967 to 1996. J. Clin. Microbiol. 1998;36:552–556. doi: 10.1128/JCM.36.2.552-556.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Enright M.C., Robinson D.A., Randle G., Feil E.J., Grundmann H., Spratt B.G. The evolutionary history of methicillin-resistant Staphylococcus aureus (MRSA) Proc. Natl. Acad. Sci. USA. 2002;99:7687–7692. doi: 10.1073/pnas.122108599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.Rodríguez-Noriega E., Seas C., Guzmán-Blanco M., Mejía C., Alvarez C., Bavestrello L., Zurita J., Lebarca J., Luna C.M., Salles M.J.C., et al. Evolution of methicillin-resistant Staphylococcus aureus clones in Latin America. Int. J. Infect. Dis. 2010;14:e560–e566. doi: 10.1016/j.ijid.2009.08.018. [DOI] [PubMed] [Google Scholar]
  • 26.Moodley A., Oosthuysen W.F., Duse A.G., Marais E. South African MRSA Surveillance group. Molecular characterization of clinical methicillin-resistant Staphylococcus aureus isolates in South Africa. J. Clin. Microbiol. 2010;48:4608–4611. doi: 10.1128/JCM.01704-10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Ghaznavi-Rad E., Nor Shamsudin M., Sekawi Z., Khoon L.Y., Aziz M.N., Hamat R.A., Othman N., Chong P.P., van Belkum A., Ghasemzadeh-Moghaddam H., et al. Predominance and emergence of clones of hospital-acquired methicillin-resistant Staphylococcus aureus in Malaysia. J. Clin. Microbiol. 2010;48:867–872. doi: 10.1128/JCM.01112-09. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Feil E.J., Cooper J.E., Grundmann H., Robinson D.A., Enright M.C., Berendt T., Peacock S.J., Smith J.M., Murphy M., Sratt B.G., et al. How clonal is Staphylococcus aureus? J. Bacteriol. 2003;185:3307–3316. doi: 10.1128/JB.185.11.3307-3316.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.D’Souza N., Rodrigues C., Mehta A. Molecular characterization of methicillin-resistant Staphylococcus aureus with emergence of epidemic clones of sequence type (ST) 22 and ST 772 in Mumbai, India. J. Clin. Microbiol. 2010;48:1806–1811. doi: 10.1128/JCM.01867-09. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Chen H., Liu Y., Jiang X., Chen M., Wang H. Rapid change of methicillin-resistant Staphylococcus aureus clones in a Chinese tertiary care hospital over a 15-year period. Antimicrob. Agents Chemother. 2010;54:1842–1847. doi: 10.1128/AAC.01563-09. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31.Chambers H.F., Deleo F.R. Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat. Rev. Microbiol. 2009;7:629–641. doi: 10.1038/nrmicro2200. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 32.Campanile F., Bongiorno D., Borbone S., Stefani S. Methicillin-resistant Staphylococcus aureus evolution: The multiple facets of an old pathogen. Eur. Infect. Dis. 2010;4:70–76. [Google Scholar]
  • 33.Breurec S., Fall C., Pouillot R., Boisier P., Brisse S., Diene-Sarr F., Djibo S., Etienne J., Fonkoua M.C., Perrier-Gros-Claude J.D., et al. Epidemiology of methicillin-susceptible Staphylococcus aureus lineages in five major African towns: High prevalence of Panton-Valentine leukocidin genes. Clin. Microbiol. Infect. 2011;17:633–639. doi: 10.1111/j.1469-0691.2010.03320.x. [DOI] [PubMed] [Google Scholar]
  • 34.Udo E.E., Pearman J.W., Grubb W.B. Genetic analysis of community isolates of methicillin-resistant Staphylococcus aureus in Western Australia. J. Hosp. Infect. 1993;25:97–108. doi: 10.1016/0195-6701(93)90100-E. [DOI] [PubMed] [Google Scholar]
  • 35.Otter J.A., French G.L. Community-associated meticillin-resistant Staphylococcus aureus strains as a cause of healthcare-associated infection. J. Hosp. Infect. 2011;79:189–193. doi: 10.1016/j.jhin.2011.04.028. [DOI] [PubMed] [Google Scholar]
  • 36.Elston D.M. Community-acquired methicillin-resistant Staphylococcus aureus. J. Am. Acad. Dermatol. 2007;56:1–16. doi: 10.1016/j.jaad.2006.04.018. quiz 17–20. [DOI] [PubMed] [Google Scholar]
  • 37.David M.Z., Glikman D., Crawford S.E., Peng J., King K.J., Hostetler M.A., Boyle-Vavra S., Daum R.S. What is community-associated methicillin-resistant Staphylococcus aureus? J. Infect. Dis. 2008;197:1235–1243. doi: 10.1086/533502. [DOI] [PubMed] [Google Scholar]
  • 38.David M.Z., Daum R.S. Community-associated methicillin-resistant Staphylococcus aureus: Epidemiology and clinical consequences of an emerging epidemic. Clin. Microbiol. Rev. 2010;23:616–687. doi: 10.1128/CMR.00081-09. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 39.Coombs G.W., Pearson J.C., O’Brien F.G., Murray R.J., Grubb W.B., Christiansen K.J. Methicillin-resistant Staphylococcus aureus clones, Western Australia. Emerg. Infect. Dis. 2006;12:241–247. doi: 10.3201/eid1202.050454. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 40.Centers for Disease Contol and Prevention Four pediatric deaths from community-acquired methicillin-resistant Staphylococcus aureus-Minnesota and North Dakota, 1997–1999. MMWR Morb. Mortal. Wkly. Rep. 1999;48:707–710. [PubMed] [Google Scholar]
  • 41.Weese J.S. Methicillin-resistant Staphylococcus aureus in animals. ILAR J. 2010;51:233–244. doi: 10.1093/ilar.51.3.233. [DOI] [PubMed] [Google Scholar]
  • 42.Graveland H., Wagenaar J.A., Bergs K., Heesterbeek H., Heederik D. Persistence of livestock associated MRSA CC398 in humans is dependent on intensity of animal contact. PLoS ONE. 2011;6:e16830. doi: 10.1371/journal.pone.0016830. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 43.Cuny C., Friedrich A., Kozytska S., Layer F., Nubel U., Ohlsen K., Strommenger B., Walther B., Wieler L., Witte W. Emergence of methicillin-resistant Staphylococcus aureus (MRSA) in different animal species. Int. J. Med. Microbiol. 2010;300:109–117. doi: 10.1016/j.ijmm.2009.11.002. [DOI] [PubMed] [Google Scholar]
  • 44.Wolk D.M., Struelens M.J., Pancholi P., Davis T., Della-Latta P., Fuller D., Picton E., Dickenson R., Denis O., Johnson D., et al. Rapid detection of Staphylococcus aureus and methicillin-resistant S. aureus (MRSA) in wound specimens and blood cultures: Multicenter preclinical evaluation of the Cepheid Xpert MRSA/SA skin and soft tissue and blood culture assays. J. Clin. Microbiol. 2009;47:823–826. doi: 10.1128/JCM.01884-08. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 45.Whitby M., McLaws M.L., Berry G. Risk of death from methicillin-resistant Staphylococcus aureus bacteraemia: A meta-analysis. Med. J. Aust. 2001;175:264–267. doi: 10.5694/j.1326-5377.2001.tb143562.x. [DOI] [PubMed] [Google Scholar]
  • 46.Thampi N., Showler A., Burry L., Bai A.D., Steinberg M., Ricciuto D.R., Bell C.M., Morris A.M. Multicenter study of health care cost of patients admitted to hospital with Staphylococcus aureus bacteremia: Impact of length of stay and intensity of care. Am. J. Infect. Control. 2015;43:739–744. doi: 10.1016/j.ajic.2015.01.031. [DOI] [PubMed] [Google Scholar]
  • 47.Fortuin-de Smidt M.C., Singh-Moodley A., Badat R., Quan V., Kularatne R., Nana T., Lekalakala R., Govender N.P., Perovic O., for GERMS-SA Staphylococcus aureus bacteraemia in Gauteng academic hospitals, South Africa. Int. J. Infect. Dis. 2015;30:41–48. doi: 10.1016/j.ijid.2014.10.011. [DOI] [PubMed] [Google Scholar]
  • 48.Antonanzas F., Lozano C., Torres C. Economic features of antibiotic resistance: The case of methicillin-resistant Staphylococcus aureus. Pharmacoeconomics. 2015;33:285–325. doi: 10.1007/s40273-014-0242-y. [DOI] [PubMed] [Google Scholar]
  • 49.Rupp M.E., Archer G.L. Coagulase-negative staphylococci: Pathogens associated with medical progress. Clin. Infect. Dis. 1994;19:231–243. doi: 10.1093/clinids/19.2.231. quiz 244–245. [DOI] [PubMed] [Google Scholar]
  • 50.Banerjee S.N., Emori T.G., Culver D.H., Gaynes R.P., Jarvis W.R., Horan T., Edwards J.R., Tolson J., Henderson T., Martone W.J. Secular trends in nosocomial primary bloodstream infections in the United States, 1980-1989. National Nosocomial Infections Surveillance System. Am. J. Med. 1991;91:86S–89S. doi: 10.1016/0002-9343(91)90349-3. [DOI] [PubMed] [Google Scholar]
  • 51.Otto M. Coagulase-negative staphylococci as reservoirs of genes facilitating MRSA infection: Staphylococcal commensal species such as Staphylococcus epidermidis are being recognized as important sources of genes promoting MRSA colonization and virulence. Bioessays. 2013;35:4–11. doi: 10.1002/bies.201200112. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 52.Feng Y., Chen C.J., Su L.H., Hu S., Yu J., Chiu C.H. Evolution and pathogenesis of Staphylococcus aureus: Lessons learned from genotyping and comparative genomics. FEMS Microbiol. Rev. 2008;32:23–37. doi: 10.1111/j.1574-6976.2007.00086.x. [DOI] [PubMed] [Google Scholar]

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