Emergence of Multidrug-Resistant, Community-Associated, Methicillin-Resistant Staphylococcus aureus Clone USA300 in Men Who Have Sex with Men

  1. Binh An Diep, PhD;
  2. Henry F. Chambers, MD;
  3. Christopher J. Graber, MD, MPH;
  4. John D. Szumowski, MD, MPH;
  5. Loren G. Miller, MD, MPH;
  6. Linda L. Han, MD;
  7. Jason H. Chen, BA;
  8. Felice Lin, BA;
  9. Jessica Lin, BA;
  10. Tiffany HaiVan Phan, BA;
  11. Heather A. Carleton, MPH;
  12. Linda K. McDougal, MS;
  13. Fred C. Tenover, PhD;
  14. Daniel E. Cohen, MD;
  15. Kenneth H. Mayer, MD;
  16. George F. Sensabaugh, DCrim; and
  17. Françoise Perdreau-Remington, PhD
  1. From the University of California, San Francisco, San Francisco, Harbor-University of California, Los Angeles, Medical Center, Torrance, and University of California, Berkeley, Berkeley, California; Beth Israel Deaconess Medical Center, Massachusetts Department of Public Health, and The Fenway Institute of Fenway Community Health, Boston, Massachussetts; Centers for Disease Control and Prevention, Atlanta, Georgia; and Brown University and Miriam Hospital, Providence, Rhode Island.

    Abstract

    Background: Infection with multidrug-resistant, community-associated, methicillin-resistant Staphylococcus aureus (MRSA) has been reported but seems to be isolated.

    Objective: To determine the incidence of a multidrug-resistant MRSA clone (USA300) in San Francisco, and to determine risk factors for the infection.

    Design: Population-based survey and cross-sectional study using chart review.

    Setting: 9 hospitals in San Francisco (population-based survey) and 2 outpatient clinics in San Francisco and Boston (cross-sectional study).

    Patients: Persons with culture-proven MRSA infections in 2004 to 2006.

    Measurements: Annual incidence, spatial clustering, and risk factors for multidrug-resistant USA300 infection. Pulsed-field gel electrophoresis, polymerase chain reaction assays, and DNA sequencing were used to characterize MRSA isolates.

    Results: The overall incidence of multidrug-resistant USA300 infection in San Francisco was 26 cases per 100 000 persons (95% CI, 16 to 36 cases per 100 000 persons); the incidence was higher in 8 contiguous ZIP codes with a higher proportion of male same-sex couples. Male–male sex was a risk factor for multidrug-resistant USA300 infection (relative risk, 13.2 [CI, 1.7 to 101.6]; P < 0.001) independent of past MRSA infection (relative risk, 2.1 [CI, 1.2 to 3.7]; P = 0.007) or clindamycin use (relative risk, 2.1 [1.2 to 3.6]; P = 0.007). The risk seemed to be independent of HIV infection. In San Francisco, multidrug-resistant USA300 manifested most often as infection of the buttocks, genitals, or perineum. In Boston, the infection was recovered exclusively from men who had sex with men.

    Limitations: The study was retrospective, and sexual risk behavior was not assessed.

    Conclusion: Infection with multidrug-resistant USA300 MRSA is common among men who have sex with men, and multidrug-resistant MRSA infection might be sexually transmitted in this population. Further research is needed to determine whether existing efforts to control epidemics of other sexually transmitted infections can control spread of community-associated, multidrug-resistant MRSA.

    Article and Author Information

    • Acknowledgment: The authors thank Dr. David A. Talan for providing isolates and clinical data.

    • Grant Support: By U.S. Public Health Service grant R01/CCR923381 (Dr. Chambers); University of California, Berkeley, Faculty Research Grant (Dr. Sensabaugh); unrestricted grant from Pfizer (Dr. Perdreau-Remington); Microbial Pathogenesis and Host Defense Postdoctoral Fellowship (5T32AI060537-02) (Dr. Diep) and HIV Translational Research Fellowship (5T32AI060530-02) (Dr. Graber) from the University of California, San Francisco; and U.S. Public Health Service grant R01/CCR923419 (Dr. Miller).

    • Potential Financial Conflicts of Interest: None disclosed.

    • Reproducible Research Statement: Study protocol, statistical code, and portions of deidentified data are available from Dr. Diep (e-mail, bdiep{at}epi-center.ucsf.edu).

    • Requests for Single Reprints: Binh An Diep, PhD, Department of Medicine, University of California, San Francisco, San Francisco General Hospital, 1001 Potrero Avenue, Building 30, Room 3300, San Francisco, CA 94110; e-mail, bdiep{at}epi-center.ucsf.edu.

    • Current Author Addresses: Drs. Diep, Chambers, Graber, and Perdreau-Remington; Ms. Phan; and Ms. Carleton: University of California, San Francisco, San Francisco General Hospital, 1001 Potrero Avenue, Building 30, Room 3300, San Francisco, CA 94110.

    • Dr. Szumowski: Beth Israel Deaconess Medical Center, Deaconess 311, 330 Brookline Avenue, Boston, MA 02215.

    • Dr. Miller: Harbor-UCLA Medical Center, 1000 West Carson Street, Box 466, Torrance, CA 90509.

    • Dr. Han: State Laboratory Institute, 305 South Street, Jamaica Plain, MA 02130.

    • Mr. Chen, Ms. F. Lin, Ms. J. Lin, and Dr. Sensabaugh: School of Public Health, MC#7360, University of California, Berkeley, CA 94720.

    • Ms. McDougal and Dr. Tenover: Centers for Disease Control and Prevention, 1600 Clifton Road, Atlanta, GA 30333.

    • Dr. Cohen: Fenway Community Health, 7 Haviland Street, Boston, MA 02115.

    • Dr. Mayer: Brown University/Miriam Hospital, 164 Summit Avenue, Providence, RI 02906.

    • Author Contributions: Conception and design: B.A. Diep, C.J. Graber.

    • Analysis and interpretation of the data: B.A. Diep, C.J. Graber, J.D. Szumowski, L.G. Miller, L.L. Han, F.C. Tenover, D.E. Cohen, K.H. Mayer, G.F. Sensabaugh, F. Perdreau-Remington, H.F. Chambers.

    • Drafting of the article: B.A. Diep.

    • Critical revision of the article for important intellectual content: B.A. Diep, C.J. Graber, H.F. Chambers, G.F. Sensabaugh, F. Perdreau-Remington, J.D. Szumowski, L.G. Miller, L.L. Han, J.H. Chen, F. Lin, J. Lin, T.H. Phan, H.A. Carleton, L.K. McDougal, F.C. Tenover, D.E. Cohen, K.H. Mayer.

    • Final approval of the article: B.A. Diep, H.F. Chambers, C.J. Graber, J.D. Szumowski, L.G. Miller, L.L. Han, J.H. Chen, F. Lin, J. Lin, T.H. Phan, H.A. Carleton, L.K. McDougal, F.C. Tenover, D.E. Cohen, K.H. Mayer, G.F. Sensabaugh, F. Perdreau-Remington.

    • Provision of study materials or patients: H.F. Chambers, F. Perdreau-Remington, L.G. Miller, L.L. Han, D.E. Cohen, K.H. Mayer.

    • Statistical expertise: B.A. Diep, C.J. Graber, L.G. Miller.

    • Obtaining of funding: H.F. Chambers, G.F. Sensabaugh, F. Perdreau-Remington.

    • Collection and assembly of data: B.A. Diep, C.J. Graber, J.D. Szumowski, J.H. Chen, F. Lin, J. Lin, T.H. Phan, H.A. Carleton, L.K. McDougal, L.L. Han.

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