Skip to main content
  • ASM
    • Antimicrobial Agents and Chemotherapy
    • Applied and Environmental Microbiology
    • Clinical Microbiology Reviews
    • Clinical and Vaccine Immunology
    • EcoSal Plus
    • Eukaryotic Cell
    • Infection and Immunity
    • Journal of Bacteriology
    • Journal of Clinical Microbiology
    • Journal of Microbiology & Biology Education
    • Journal of Virology
    • mBio
    • Microbiology and Molecular Biology Reviews
    • Microbiology Resource Announcements
    • Microbiology Spectrum
    • Molecular and Cellular Biology
    • mSphere
    • mSystems
  • Log in
  • My alerts
  • My Cart

Main menu

  • Home
  • Articles
    • Current Issue
    • Accepted Manuscripts
    • COVID-19 Special Collection
    • Archive
    • Minireviews
  • For Authors
    • Submit a Manuscript
    • Scope
    • Editorial Policy
    • Submission, Review, & Publication Processes
    • Organization and Format
    • Errata, Author Corrections, Retractions
    • Illustrations and Tables
    • Nomenclature
    • Abbreviations and Conventions
    • Publication Fees
    • Ethics Resources and Policies
  • About the Journal
    • About AAC
    • Editor in Chief
    • Editorial Board
    • For Reviewers
    • For the Media
    • For Librarians
    • For Advertisers
    • Alerts
    • AAC Podcast
    • RSS
    • FAQ
  • Subscribe
    • Members
    • Institutions
  • ASM
    • Antimicrobial Agents and Chemotherapy
    • Applied and Environmental Microbiology
    • Clinical Microbiology Reviews
    • Clinical and Vaccine Immunology
    • EcoSal Plus
    • Eukaryotic Cell
    • Infection and Immunity
    • Journal of Bacteriology
    • Journal of Clinical Microbiology
    • Journal of Microbiology & Biology Education
    • Journal of Virology
    • mBio
    • Microbiology and Molecular Biology Reviews
    • Microbiology Resource Announcements
    • Microbiology Spectrum
    • Molecular and Cellular Biology
    • mSphere
    • mSystems

User menu

  • Log in
  • My alerts
  • My Cart

Search

  • Advanced search
Antimicrobial Agents and Chemotherapy
publisher-logosite-logo

Advanced Search

  • Home
  • Articles
    • Current Issue
    • Accepted Manuscripts
    • COVID-19 Special Collection
    • Archive
    • Minireviews
  • For Authors
    • Submit a Manuscript
    • Scope
    • Editorial Policy
    • Submission, Review, & Publication Processes
    • Organization and Format
    • Errata, Author Corrections, Retractions
    • Illustrations and Tables
    • Nomenclature
    • Abbreviations and Conventions
    • Publication Fees
    • Ethics Resources and Policies
  • About the Journal
    • About AAC
    • Editor in Chief
    • Editorial Board
    • For Reviewers
    • For the Media
    • For Librarians
    • For Advertisers
    • Alerts
    • AAC Podcast
    • RSS
    • FAQ
  • Subscribe
    • Members
    • Institutions
Mechanisms of Resistance

Methicillin-Resistant and -Susceptible Staphylococcus aureus Strains of Clonal Lineages ST398 and ST9 from Swine Carry the Multidrug Resistance Gene cfr

Corinna Kehrenberg, Christiane Cuny, Birgit Strommenger, Stefan Schwarz, Wolfgang Witte
Corinna Kehrenberg
1Institute of Farm Animal Genetics, Friedrich-Loeffler-Institute, Neustadt-Mariensee, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • For correspondence: corinna.kehrenberg@fli.bund.de stefan.schwarz@fli.bund.de
Christiane Cuny
2Robert Koch Institute, Wernigerode Branch, 38855 Wernigerode, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Birgit Strommenger
2Robert Koch Institute, Wernigerode Branch, 38855 Wernigerode, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Stefan Schwarz
1Institute of Farm Animal Genetics, Friedrich-Loeffler-Institute, Neustadt-Mariensee, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • For correspondence: corinna.kehrenberg@fli.bund.de stefan.schwarz@fli.bund.de
Wolfgang Witte
2Robert Koch Institute, Wernigerode Branch, 38855 Wernigerode, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
DOI: 10.1128/AAC.01376-08
  • Article
  • Figures & Data
  • Info & Metrics
  • PDF
Loading

ABSTRACT

Methicillin-resistant Staphylococcus aureus clonal lineage ST398 and methicillin-susceptible lineage ST9 strains have their main reservoir in swine but can colonize and cause infections in humans. The phenicol/lincosamide/oxazolidinone/pleuromutilin/streptogramin A multidrug resistance gene cfr was detected in isolates of both clonal lineages, rendering a spread to humans with exposure to swine farming possible.

Methicillin-resistant Staphylococcus aureus (MRSA) is an important pathogen that causes health care- and community-associated infections in humans worldwide (2, 7, 18). Recent reports indicated that MRSA isolates of multilocus sequence type ST398 have their main reservoir in swine (4, 9, 25). MRSA strains of clonal lineage ST398 but also methicillin-susceptible S. aureus (MSSA) strains of other clonal lineages are able to colonize and cause infections in various other animal species and humans (14, 20, 24, 28-30). Currently, the colonization of persons with exposure to swine farming and subsequent infections in humans are a matter of worldwide concern (9, 27, 30, 31).

Due to the common multiresistance phenotype displayed by MRSA ST398 strains, therapeutic options are limited. Among the antimicrobial agents considered the most-promising therapeutics, oxazolidinones play a dominant role in the treatment of MRSA infections (5). In addition, pleuromutilins, represented by the recently FDA-approved retapamulin, are important drugs for the therapy of S. aureus skin infections (10). However, transferable oxazolidinone and pleuromutilin resistance mediated by the gene cfr has been reported recently in staphylococci from animals in Germany and Denmark (11, 12) and from humans in Colombia and the United States (17, 22). The gene cfr codes for a methyltransferase that targets A2503 in 23S rRNA. The Cfr-mediated resistance phenotype includes—besides oxazolidinones and pleuromutilins—phenicols, lincosamides, and streptogramin A antibiotics, all of which share overlapping binding sites in close proximity to A2503 (15).

To date, very little is known about the dissemination of the gene cfr among S. aureus strains from animals. The aim of the present study was to investigate S. aureus strains of porcine origin for the presence of this and other antibiotic resistance genes and to further characterize cfr-positive strains. For this, nasal swabs were taken from 846 swine from 367 farms all over Germany during 2007 and investigated at the National Reference Laboratory for Staphylococci in Germany at the Robert Koch Institute (RKI). A total of 110 porcine S. aureus isolates were identified. Studies at the Institute of Farm Animal Genetics of the Friedrich-Loeffler-Institute (FLI) included the screening of 90 porcine coagulase-positive and coagulase-variable staphylococci collected all over Germany from diseased swine in the BfT-GermVet study 2004-2006 (19) and 56 nonrelated porcine S. aureus strains provided by veterinary diagnostic laboratories from all over Germany and collected mainly in 2008. In total, two staphylococcal strains of porcine origin, one from the RKI study and the other from the FLI study, displayed a resistance phenotype indicative of the presence of cfr (Table 1). Both strains originated from swine farms in different geographic areas of northern Germany, were isolated in 2004 and 2007, respectively, and carried the gene cfr, as confirmed by PCR analysis and sequencing of the amplicons. One of these strains showed an oxacillin MIC of ≥32 μg/ml and was classified as a MRSA strain. The mecA gene and staphylococcal cassette chromosome mec type V were detected by multiplex PCR assays (13). The species identification of both strains as S. aureus was confirmed biochemically with the ID32Staph system (bioMérieux, Nürtingen, Germany). The further characterization of these strains included multilocus sequence typing (MLST) (6) and spa typing (http://spaserver2.ridom.de/index.shtml ). The cfr-carrying MRSA strain belonged to the clonal lineage ST398 with the MLST allelic profile 3-35-19-2-20-26-39. This isolate was characterized by spa typing as t034. In contrast, the cfr-carrying MSSA strain exhibited spa type t3198 and was assigned to the MLST type ST9 based on its allelic profile, 3-3-1-1-1-1-10.

Both strains, MRSA ST398 and MSSA ST9, carried the cfr gene on ca. 36-kb plasmids, as confirmed by protoplast transformation into S. aureus RN4220 (12). The transformants exhibited the elevated MICs of phenicols, lincosamides, oxazolidinones, pleuromutilins, and streptogramin A antibiotics, which confirmed the functional activity of the gene cfr (Table 1). Both plasmids were indistinguishable by their BglII restriction patterns from the previously described cfr-carrying plasmid pSCFS3 (12). The cfr-containing BglII fragments obtained from the S. aureus RN4220 transformants were cloned into the BamHI site of vector pBluescript II SK+ (Stratagene, Amsterdam, The Netherlands). A sequence analysis of the cfr gene regions confirmed the assignment of both plasmids to the pSCFS3 type (12). This plasmid type carries the multidrug resistance gene cfr as well as the phenicol exporter gene fexA. The latter is usually part of transposon Tn558, and the fexA reading frame is completely retained on plasmid pSCFS3. In contrast, the Tn558-associated transposase genes tnpA and tnpB are deleted in plasmid pSCFS3 by the insertion of a 4,674-bp segment. This segment carries the cfr gene and a copy of the insertion sequence IS21-558, which is supposed to be involved in the mobility of cfr (11).

Although plasmid pSCFS3 is not conjugative, it was shown to be transferable into another staphylococcal recipient strain which then expressed the cfr-associated resistance phenotype. When entering a new host cell, plasmid pSCFS3 may undergo recombinational events with plasmids already residing in new host cells. In this regard, it should be noted that a pSCFS3-analogous cfr gene region was recently found on a 55-kb plasmid in a cfr-carrying MSSA isolate detected during the 2007 LEADER program in the United States (17). Although our results indicated that the cfr-carrying plasmids in the two porcine strains harbored only the resistance genes cfr and fexA, PCR analysis (12, 21) revealed that both strains also carried a macrolide, lincosamide, and streptogramin B resistance gene, erm(A) in MRSA ST398 and erm(C) in MSSA ST9, and that the MRSA isolate was also resistant to tetracyclines via a tet(M) gene. These observations point toward further limited therapeutic options in the control of these cfr-carrying strains.

Previous studies suggested that there is a high risk for swine farmers, veterinarians, or people with exposure to swine farming to be colonized with S. aureus strains of sequence types ST398 or ST9 (1, 23). As in other European countries, MRSA ST398 is widely disseminated as a nasal colonizer among pigs in Germany (16) and represented 0.22% of all MRSA strains from human infections in Germany in 2006/2007 (3). MRSA ST398 was also detected in outpatients or inpatients with ventilator-associated pneumonia in central Europe (30) and was assumed to have already entered the food chain (26). Among the 655 MRSA ST398 strains from pigs as well as from colonization and infections in humans that have been tested to date at RKI and FLI, only the single strain described in this study carried the gene cfr. In addition, S. aureus ST9 strains have been shown to be frequently disseminated among swine in France and have not been reported so far from other animal species (1). However, MSSA ST9 strains have occasionally been isolated from healthy human carriers (8). This sequence type seems to be rare among S. aureus isolates from infections in humans in Germany: in a study conducted by RKI and comprising 2,353 strains collected from various infections in humans all over Germany in 2007, only a single ST9 strain was identified.

Even if our initial studies do not allow us to estimate the prevalence of the gene cfr in S. aureus strains from swine, we report here the first two porcine S. aureus isolates of sequence types ST398 and ST9 that carry the multidrug resistance gene cfr on a plasmid. As there is obviously no pronounced host specificity with respect to the colonization of pigs and humans, the transfer of cfr-carrying S. aureus ST398 or ST9 from swine to humans and a further spread of human-adapted S. aureus strains cannot be excluded.

View this table:
  • View inline
  • View popup
TABLE 1.

MICs of the cfr-carrying MRSA ST398 and MSSA ST9 strains and their pSCFS3-carrying S. aureus RN4220 transformants

ACKNOWLEDGMENTS

We thank Vera Nöding for excellent laboratory assistance.

We also thank the Deutsche Forschungsgemeinschaft for supporting the study with grant SCHW382/6-3.

FOOTNOTES

    • Received 14 October 2008.
    • Returned for modification 6 November 2008.
    • Accepted 24 November 2008.
  • Copyright © 2009 American Society for Microbiology

REFERENCES

  1. 1.↵
    Armand-Lefevre, L., R. Ruimy, and A. Andremont. 2005. Clonal comparison of Staphylococcus aureus isolates from healthy pig farmers, human controls, and pigs. Emerg. Infect. Dis.11:711-714.
    OpenUrlCrossRefPubMedWeb of Science
  2. 2.↵
    Boucher, H. W., and G. R. Corey. 2008. Epidemiology of methicillin-resistant Staphylococcus aureus. Clin. Infect. Dis.46(Suppl. 5):344-349.
    OpenUrl
  3. 3.↵
    Cuny, C., and W. Witte. 2008. Importance of the spread of methicillin-resistant Staphylococcus aureus (MRSA) in fattened pigs for humans? MMW Fortschr. Med.150(Suppl. 2):65-67.
    OpenUrlPubMed
  4. 4.↵
    de Neeling, A. J., M. J. van den Broek, E. C. Spalburg, M. G. van Santen-Verheuvel, W. D. Dam-Deisz, H. C. Boshuizen, A. W. van de Giessen, E. van Duijkeren, and X. W. Huijsdens. 2007. High prevalence of methicillin resistant Staphylococcus aureus in pigs. Vet. Microbiol.122:366-372.
    OpenUrlCrossRefPubMedWeb of Science
  5. 5.↵
    Diekema, D. J., and R. N. Jones. 2001. Oxazolidinone antibiotics. Lancet358:1975-1982.
    OpenUrlCrossRefPubMedWeb of Science
  6. 6.↵
    Enright, M. C., N. P. Day, C. E. Davies, S. J. Peacock, and B. G. Spratt. 2000. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J. Clin. Microbiol.38:1008-1015.
    OpenUrlAbstract/FREE Full Text
  7. 7.↵
    Enright, M. C., D. A. Robinson, G. Randle, E. J. Feil, H. Grundmann, and B. G. Spratt. 2002. The evolutionary history of methicillin-resistant Staphylococcus aureus (MRSA). Proc. Natl. Acad. Sci. USA99:7687-7692.
    OpenUrlAbstract/FREE Full Text
  8. 8.↵
    Grundmann, H., S. Hori, M. C. Enright, C. Webster, A. Tami, E. J. Feil, and T. Pitt. 2002. Determining the genetic structure of the natural population of Staphylococcus aureus: a comparison of multilocus sequence typing with pulsed-field gel electrophoresis, randomly amplified polymorphic DNA analysis, and phage typing. J. Clin. Microbiol.40:4544-4546.
    OpenUrlAbstract/FREE Full Text
  9. 9.↵
    Huijsdens, X. W., B. J. van Dijke, E. Spalburg, M. G. van Santen-Verheuvel, M. E. Heck, G. N. Pluister, A. Voss, W. J. Wannet, and A. J. de Neeling. 2006. Community-acquired MRSA and pig-farming. Ann. Clin. Microbiol. Antimicrob.5:26.
    OpenUrlCrossRefPubMed
  10. 10.↵
    Jacobs, M. R. 2007. Retapamulin: a semisynthetic pleuromutilin compound for topical treatment of skin infections in adults and children. Future Microbiol.2:591-600.
    OpenUrlCrossRefPubMedWeb of Science
  11. 11.↵
    Kehrenberg, C., F. M. Aarestrup, and S. Schwarz. 2007. IS21-558 insertion sequences are involved in the mobility of the multiresistance gene cfr. Antimicrob. Agents Chemother.51:483-487.
    OpenUrlAbstract/FREE Full Text
  12. 12.↵
    Kehrenberg, C., and S. Schwarz. 2006. Distribution of florfenicol resistance genes fexA and cfr among chloramphenicol-resistant Staphylococcus isolates. Antimicrob. Agents Chemother.50:1156-1163.
    OpenUrlAbstract/FREE Full Text
  13. 13.↵
    Kondo, Y., T. Ito, X. X. Ma, S. Watanabe, B. N. Kreiswirth, J. Etienne, and K. Hiramatsu. 2007. Combination of multiplex PCRs for staphylococcal cassette chromosome mec type assignment: rapid identification system for mec,ccr, and major differences in junkyard regions. Antimicrob. Agents Chemother.51:264-274.
    OpenUrlAbstract/FREE Full Text
  14. 14.↵
    Loeffler, A., A. K. Boag, J. Sung, J. A. Lindsay, L. Guardabassi, A. Dalsgaard., H. Smith, K. B. Stevens, and D. H. Lloyd. 2005. Prevalence of methicillin-resistant Staphylococcus aureus among staff and pets in a small animal referral hospital in the UK. J. Antimicrob. Chemother.56:692-697.
    OpenUrlCrossRefPubMedWeb of Science
  15. 15.↵
    Long, K. S., J. Poehlsgaard, C. Kehrenberg, S. Schwarz, and B. Vester. 2006. The Cfr rRNA methyltransferase confers resistance to phenicols, lincosamides, oxazolidinones, pleuromutilins, and streptogramin A antibiotics. Antimicrob. Agents Chemother.50:2500-2505.
    OpenUrlAbstract/FREE Full Text
  16. 16.↵
    Meemken, D., C. Cuny, W. Witte, U. Eichler, R. Staudt, and T. Blaha. 2008. Occurrence of MRSA in pigs and in humans involved in pig production—preliminary results of a study in the northwest of Germany. Dtsch. Tierärztl. Wochenschr.115:132-139.
    OpenUrlPubMed
  17. 17.↵
    Mendes, R. E., L. M. Deshpande, M. Castanheira, J. DiPersio, M. A. Saubolle, and R. N. Jones. 2008. First report of cfr-mediated resistance to linezolid in human staphylococcal clinical isolates recovered in the United States. Antimicrob. Agents Chemother.52:2244-2246.
    OpenUrlAbstract/FREE Full Text
  18. 18.↵
    Oliveira, D. C., A. Tomasz, and H. de Lencastre. 2002. Secrets of success of a human pathogen: molecular evolution of pandemic clones of methicillin-resistant Staphylococcus aureus. Lancet Infect. Dis.2:180-189.
    OpenUrlCrossRefPubMedWeb of Science
  19. 19.↵
    Schwarz, S., E. Alesík, C. Werckenthin, M. Grobbel, A. Lübke-Becker, L. H. Wieler, and J. Wallmann. 2007. Antimicrobial susceptibility of coagulase-positive and coagulase-variable staphylococci from various indications of swine, dogs and cats as determined in the BfT-GermVet monitoring program 2004-2006. Berl. Münch. Tierärztl. Wochenschr.120:372-379.
    OpenUrlPubMedWeb of Science
  20. 20.↵
    Strommenger, B., C. Kehrenberg, C. Kettlitz, C. Cuny, J. Verspohl, W. Witte, and S. Schwarz. 2006. Molecular characterization of methicillin-resistant Staphylococcus aureus strains from pet animals and their relationship to human isolates. J. Antimicrob. Chemother.57:461-465.
    OpenUrlCrossRefPubMedWeb of Science
  21. 21.↵
    Strommenger, B., C. Kettlitz, G. Werner, and W. Witte. 2003. Multiplex PCR assay for simultaneous detection of nine clinically relevant antibiotic resistance genes in Staphylococcus aureus. J. Clin. Microbiol.41:4089-4094.
    OpenUrlAbstract/FREE Full Text
  22. 22.↵
    Toh, S. M., L. Xiong, C. A. Arias, M. V. Villegas, K. Lolans, J. Quinn, and A. S. Mankin. 2007. Acquisition of a natural resistance gene renders a clinical strain of methicillin-resistant Staphylococcus aureus resistant to the synthetic antibiotic linezolid. Mol. Microbiol.64:1506-1514.
    OpenUrlCrossRefPubMedWeb of Science
  23. 23.↵
    van Belkum, A., D. C. Melles, J. K. Peeters, W. B. van Leeuwen, E. van Duijkeren, X. W. Huijsdens, E. Spalburg, A. J. de Neeling, H. A. Verbrugh, and Dutch Working Party on Surveillance and Research of MRSA-SOM. 2008. Methicillin-resistant and -susceptible Staphylococcus aureus sequence type 398 in pigs and humans. Emerg. Infect. Dis.14:479-483.
    OpenUrlCrossRefPubMedWeb of Science
  24. 24.↵
    Van den Eede, A., A. Martens, U. Lipinska, M. Struelens, A. Deplano, O. Denis, F. Haesebrouck, F. Gasthuys, and K. Hermans. 2009. High occurrence of methicillin-resistant Staphylococcus aureus ST398 in equine nasal samples. Vet. Microbiol.133:138-144.
    OpenUrlCrossRefPubMedWeb of Science
  25. 25.↵
    van Duijkeren, E., R. Ikawaty, M. J. Broekhuizen-Stins, M. D. Jansen, E. C. Spalburg, A. J. de Neeling, J. G. Allaart, A. van Nes, J. A. Wagenaar, and A. C. Fluit. 2008. Transmission of methicillin-resistant Staphylococcus aureus strains between different kinds of pig farms. Vet. Microbiol.126:383-389.
    OpenUrlCrossRefPubMedWeb of Science
  26. 26.↵
    van Loo, I. H., B. M. Diederen, P. H. Savelkoul, J. H. Woudenberg, R. Roosendaal, A. van Belkum, N. Lemmens-den Toom, C. Verhulst, P. H. van Keulen, and J. A. Kluytmans. 2007. Methicillin-resistant Staphylococcus aureus in meat products, the Netherlands. Emerg. Infect. Dis.13:1753-1755.
    OpenUrlCrossRefPubMedWeb of Science
  27. 27.↵
    van Loo, I., X. Huijsdens, E. Tiemersma, A. de Neeling, N. van de Sande-Bruinsma, D. Beaujean, A. Voss, and J. Kluytmans. 2007. Emergence of methicillin-resistant Staphylococcus aureus of animal origin in humans. Emerg. Infect. Dis.13:1834-1839.
    OpenUrlCrossRefPubMedWeb of Science
  28. 28.↵
    Walther, B., L. H. Wieler, A. W. Friedrich, A. M. Hanssen, B. Kohn, L. Brunnberg, and A. Lübke-Becker. 2008. Methicillin-resistant Staphylococcus aureus (MRSA) isolated from small and exotic animals at a university hospital during routine microbiological examinations. Vet. Microbiol.127:171-178.
    OpenUrlCrossRefPubMedWeb of Science
  29. 29.
    Weese, J. S., M. Archambault, B. M. Willey, P. Hearn, B. N. Kreiswirth, B. Said-Salim, A. McGeer, Y. Likhoshvay, J. F. Prescott, and D. E. Low. 2005. Methicillin-resistant Staphylococcus aureus in horses and horse personnel, 2000-2002. Emerg. Infect. Dis.11:430-435.
    OpenUrlCrossRefPubMedWeb of Science
  30. 30.↵
    Witte, W., B. Strommenger, C. Stanek, and C. Cuny. 2007. Methicillin-resistant Staphylococcus aureus ST398 in humans and animals, Central Europe. Emerg. Infect. Dis.13:255-258.
    OpenUrlCrossRefPubMedWeb of Science
  31. 31.↵
    Wulf, M., and A. Voss. 2008. MRSA in livestock animals—an epidemic waiting to happen? Clin. Microbiol. Infect.14:519-521.
    OpenUrlCrossRefPubMedWeb of Science
View Abstract
PreviousNext
Back to top
Download PDF
Citation Tools
Methicillin-Resistant and -Susceptible Staphylococcus aureus Strains of Clonal Lineages ST398 and ST9 from Swine Carry the Multidrug Resistance Gene cfr
Corinna Kehrenberg, Christiane Cuny, Birgit Strommenger, Stefan Schwarz, Wolfgang Witte
Antimicrobial Agents and Chemotherapy Jan 2009, 53 (2) 779-781; DOI: 10.1128/AAC.01376-08

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Print

Alerts
Sign In to Email Alerts with your Email Address
Email

Thank you for sharing this Antimicrobial Agents and Chemotherapy article.

NOTE: We request your email address only to inform the recipient that it was you who recommended this article, and that it is not junk mail. We do not retain these email addresses.

Enter multiple addresses on separate lines or separate them with commas.
Methicillin-Resistant and -Susceptible Staphylococcus aureus Strains of Clonal Lineages ST398 and ST9 from Swine Carry the Multidrug Resistance Gene cfr
(Your Name) has forwarded a page to you from Antimicrobial Agents and Chemotherapy
(Your Name) thought you would be interested in this article in Antimicrobial Agents and Chemotherapy.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Share
Methicillin-Resistant and -Susceptible Staphylococcus aureus Strains of Clonal Lineages ST398 and ST9 from Swine Carry the Multidrug Resistance Gene cfr
Corinna Kehrenberg, Christiane Cuny, Birgit Strommenger, Stefan Schwarz, Wolfgang Witte
Antimicrobial Agents and Chemotherapy Jan 2009, 53 (2) 779-781; DOI: 10.1128/AAC.01376-08
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
  • Top
  • Article
    • ABSTRACT
    • ACKNOWLEDGMENTS
    • FOOTNOTES
    • REFERENCES
  • Figures & Data
  • Info & Metrics
  • PDF

KEYWORDS

Anti-Bacterial Agents
Bacterial Proteins
Drug Resistance, Multiple, Bacterial
Genes, Bacterial
methicillin-resistant Staphylococcus aureus
Staphylococcus aureus

Related Articles

Cited By...

About

  • About AAC
  • Editor in Chief
  • Editorial Board
  • Policies
  • For Reviewers
  • For the Media
  • For Librarians
  • For Advertisers
  • Alerts
  • AAC Podcast
  • RSS
  • FAQ
  • Permissions
  • Journal Announcements

Authors

  • ASM Author Center
  • Submit a Manuscript
  • Article Types
  • Ethics
  • Contact Us

Follow #AACJournal

@ASMicrobiology

       

ASM Journals

ASM journals are the most prominent publications in the field, delivering up-to-date and authoritative coverage of both basic and clinical microbiology.

About ASM | Contact Us | Press Room

 

ASM is a member of

Scientific Society Publisher Alliance

 

American Society for Microbiology
1752 N St. NW
Washington, DC 20036
Phone: (202) 737-3600

Copyright © 2021 American Society for Microbiology | Privacy Policy | Website feedback

Print ISSN: 0066-4804; Online ISSN: 1098-6596