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of Internal Medicine
Emergence of Multidrug-Resistant, Community-Associated,
Methicillin-Resistant Staphylococcus aureus
Clone USA300 in Men
Who Have Sex with Men
Binh An Diep, PhD; Henry F. Chambers, MD; Christopher J. Graber, MD, MPH; John D. Szumowski, MD, MPH; Loren G. Miller, MD, MPH;
Linda L. Han, MD; Jason H. Chen, BA; Felice Lin, BA; Jessica Lin, BA; Tiffany HaiVan Phan, BA; Heather A. Carleton, MPH;
Linda K. McDougal, MS; Fred C. Tenover, PhD; Daniel E. Cohen, MD; Kenneth H. Mayer, MD; George F. Sensabaugh, DCrim; and
Franc¸oise Perdreau-Remington, PhD

Background: Infection with multidrug-resistant, community-associ-
contiguous ZIP codes with a higher proportion of male same-sex ated, methicillin-resistant Staphylococcus aureus (MRSA) has been couples. Male–male sex was a risk factor for multidrug-resistant USA300 infection (relative risk, 13.2 [CI, 1.7 to 101.6]; P Ͻ 0.001)independent of past MRSA infection (relative risk, 2.1 [CI, 1.2 to Objective: To determine the incidence of a multidrug-resistant
3.7]; P ϭ 0.007) or clindamycin use (relative risk, 2.1 [1.2 to 3.6]; MRSA clone (USA300) in San Francisco, and to determine risk P ϭ 0.007). The risk seemed to be independent of HIV infection. In San Francisco, multidrug-resistant USA300 manifested most often Design: Population-based survey and cross-sectional study using
as infection of the buttocks, genitals, or perineum. In Boston, the infection was recovered exclusively from men who have sex withmen.
Setting: 9 hospitals in San Francisco (population-based survey) and
2 outpatient clinics in San Francisco and Boston (cross-sectional
Limitations: The study was retrospective, and sexual risk behavior
Patients: Persons with culture-proven MRSA infections in 2004 to
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 pop- Measurements: Annual incidence, spatial clustering, and risk fac-
ulation. Further research is needed to determine whether existing tors for multidrug-resistant USA300 infection. Pulsed-field gel elec- efforts to control epidemics of other sexually transmitted infections trophoresis, polymerase chain reaction assays, and DNA sequencing can control spread of community-associated, multidrug-resistant were used to characterize MRSA isolates.
Results: The overall incidence of multidrug-resistant USA300 infec-
tion in San Francisco was 26 cases per 100 000 persons (95% CI,
Ann Intern Med. 2008;148:249-257.
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16 to 36 cases per 100 000 persons); the incidence was higher in 8 For author affiliations, see end of text.
Infections caused by community-associated, methicillin- Diep and colleagues (28) described a multidrug-resistant
resistant Staphylococcus aureus (MRSA) have become a USA300 isolate that had accumulated multiple resistance major public health threat. A single clone of community- genes, rendering it resistant to ␤-lactams, fluoroquinolo- associated MRSA, USA300, was not seen before 2000 but nes, tetracycline, macrolide, clindamycin, and mupirocin.
is now widely disseminated in 38 U.S. states, Canada, and Two of the resistance genes from this isolate, ermC and 9 European Union countries (1–17). It can cause unusually mupA—which determine constitutive resistance to macro- severe human diseases, including necrotizing fasciitis, sep- lides, clindamycin, and mupirocin—are carried on a large sis, endocarditis, and pneumonia (18 –23). Infections oc- conjugative plasmid called pUSA03 (28). Researchers have cur predominantly among healthy, community-dwellingpersons who lack traditional risk factors for MRSA (9, 18,24 –26).
Whereas hospital-associated MRSA strains are resistant to multiple antimicrobial classes, USA300 and other com- Editors’ Notes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 250 munity-associated MRSA strains are typically resistant to Summary for Patients . . . . . . . . . . . . . . . . . . . . . . . . . 2 -lactams and 1 or 2 other drug classes. Older generic Editorial comment. . . . . . . . . . . . . . . . . . . . . . . . . . 302 antimicrobials, such as clindamycin, tetracycline, or tri-methoprim–sulfamethoxazole, are recommended for treat- Web-Only
ing less serious community-associated MRSA infections, such as uncomplicated skin and soft tissue infections (3, 27). However, increased use of these antimicrobials could drive the emergence of new subclones of community- associated MRSA that are multidrug resistant. Recently, 2008 American College of Physicians 249
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Emergence of Multidrug-Resistant MRSA Clone USA300 pital beds; the medical center that did not participate in the survey operates 59 licensed hospital beds. The partici- Researchers have recently identified USA300, a clone of pating medical centers initiated routine specimen collec- community-acquired, methicillin-resistant Staphylococcus tion between February and September 2004 and collected aureus (MRSA) that is resistant to multiple antibiotics.
clinical MRSA specimens from unique patients (n ϭ 3929)for 12 consecutive months. If a specimen was submitted Contribution
from a patient for whom a sample was cultured earlier in The authors demonstrate that the incidence of multidrug- the study period, we used the first specimen. We excluded resistant USA300 MRSA is highest in the areas of San 103 isolates because they came from patient nares and did Francisco where more male same-sex couples reside. The not represent active infection. Of the remaining 3826 infection frequently manifests as an abscess or cellulitis in MRSA specimens, 2495 were from patients residing in San the buttocks, genitals, or perineum, and male–male sex Francisco. The 3826 MRSA specimens were stratified by the medical center of origin and then by the month of specimen collection, and we used a random-number gen- Data were passively reported or retrospectively collected erator to select up to 8 MRSA specimens from each stra- tum. The stratified random sample comprised 801 nondu-plicated MRSA specimens, and of these, 532 were Implication
recovered from patients residing in San Francisco. We cal- Multidrug-resistant USA300 MRSA infection is especially culated the incidence of multidrug-resistant USA300 infec- common among men who have sex with men. It might be tion in each city ZIP code on the basis of the 532 cases, sexually transmitted in this population.
and we used 2000 U.S. Census data (33) to test the asso-ciation between disease incidence estimates and the pro- portion of male same-sex couples living in those ZIP codes.
HIV Clinic–Based Study
identified clusters of infections due to multidrug-resistant We conducted a retrospective chart review of consec- USA300 in San Francisco and Boston (29, 30), which utive patients (n ϭ 183) who had MRSA cultured from an could complicate disease management and contribute to infection site from January 2004 through June 2006 at the development of persistent or recurrent community-associ- San Francisco General Hospital (SFGH) Positive Health Program, an outpatient HIV clinic that provides special- We report the incidence of multidrug-resistant ized HIV and AIDS care in San Francisco, California. Of USA300 in San Francisco and Boston among men who the 183 specimens, 83 were collected between 1 February have sex with men, and we describe factors associated with 2004 and 31 January 2005 as part of the population-based its spread in this high-risk population, on the basis of 4 survey; these 83 specimens represented a subset of 1014 studies: a population-based survey to estimate the inci- unique MRSA isolates identified from all SFGH sites in dence and spatial clustering of multidrug-resistant USA300 the population survey. Using a standardized instrument, in San Francisco; 2 clinic-based, cross-sectional studies to we abstracted information about patients’ demographic identify risk factors for multidrug-resistant USA300 infec- characteristics, male homosexual behavior, HIV viral load, tion; and a post hoc analysis of multidrug-resistant CD4ϩ cell count, past culture-proven MRSA infection, USA300 isolates previously collected from emergency de- past clinical presentation, and site of infection from med- ical records. We collected information about male homo-sexual behavior from the patient’s clinic intake form (typ- ically administered by a social worker), in which the Population-Based Survey
patient was asked for self-identification of sexual behavior.
We characterized MRSA isolates previously collected If the clinic intake form was incomplete or missing, we in a population-based survey of MRSA infections at 9 of classified a male patient as a man who has sex with men if the 10 medical centers serving San Francisco in 2004 to an anal Papanicolaou (Pap) smear was performed at any 2005 (Liu C, Graber CJ, Karr M, Diep BA, Basuino L, time during his history at the clinic in the absence of in- Schwartz BS, et al. A population-based study of the inci- dications other than anal receptive intercourse (screening dence and molecular epidemiology of methicillin-resistant- anal Pap smear). Eight patients had missing sexual behav- Staphylococcus aureus disease in San Francisco, 2004-5. In ior data and no history of anal Pap smears; we classified preparation). The medical centers used passive surveillance them as men who do not have sex with men. Seven of these for MRSA; physicians submitted cultures to laboratories men had non–multidrug-resistant USA300 infection, and for identification of pathogens when patients presented 1 had a non-USA300 infection. Our estimates of risk for with a disease that, in the physician’s opinion, required multidrug-resistant USA300 with male–male sex did not culture. The 9 medical centers operate 4368 licensed hos- change meaningfully when these 7 patients with non–mul- 250 19 February 2008 Annals of Internal Medicine Volume 148 • Number 4
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Emergence of Multidrug-Resistant MRSA Clone USA300 Article tidrug-resistant USA300 infection were reclassified as oc-curring in men who have sex with men or when they were Figure. Annual incidence of multidrug-resistant USA300 and
percentage of male same-sex couples, by San Francisco ZIP

excluded from analyses (data not shown).
We also compared the proportion of patients with multidrug-resistant USA300 infection in the HIV clinicwith a subset of 91 MRSA cases randomly selected fromthe 1014 MRSA isolates identified from SFGH in the pop-ulation-based study.
Community Health Clinic–Based Study
We conducted retrospective chart reviews of 130 con- secutive patients with MRSA infection treated at FenwayCommunity Health, Boston, Massachusetts, from April2004 through March 2006. Fenway Community Health isa community-based organization that provides primarycare to more than 10 000 patients annually (34). Reportshave noted that a large proportion of MRSA isolates recov-ered from skin and soft tissue infection sites of patientsseen at Fenway Community Health were resistant to mul-tiple antimicrobial agents (30, 31). Using the same stan-dardized instrument developed for the SFGH HIV clinicstudy, we abstracted clinical data from medical records of each patient at Fenway Community Health.
Among these patients, 3 with missing data on sexual behavior and no history of screening anal Pap smears were classified as men who do not have sex with men; these 3patients had non–multidrug-resistant USA300 infections.
We genotyped the multidrug-resistant USA300 isolate of 1 The legend indicates the annual incidence of multidrug-resistant clinic patient who reported male–male sex and frequent USA300 per 100 000 persons. The number within each ZIP code is thepercentage of male same-sex couples, calculated by dividing the number travel to and from the Castro District in San Francisco to of male same-sex, unmarried-partner households by the number of cou- see whether frequent travel by men who have sex with men pled (married and unmarried) households for each ZIP code, based on between the East and West coasts facilitates the clonal 2000 U.S. Census (Summary File 3) data (33). The asterisk indicates thelocation of the San Francisco General Hospital HIV clinic.
spread of multidrug-resistant USA300.
Emergency Department–Based Study
method in accordance with Clinical and Laboratory Stan- Because the spread of multidrug-resistant USA300 is a potential public health threat, we investigated the distribu- Molecular Analysis
tion of multidrug-resistant USA300 in the general popula- We genotyped isolates by using pulsed-field gel elec- tion of patients with community-associated MRSA infec- trophoresis after SmaI-macrorestriction digest of chromo- tions. To this end, we conducted a post hoc analysis of 212 somal DNA (36), spa typing of the polymorphic repeat USA300 isolates collected by Moran and colleagues (1) in regions of protein A (37), and multilocus sequence typing August 2004 from emergency departments in 11 U.S. cit- of fragments of 7 housekeeping genes (38). We further defined USA300 by the presence of Panton–Valentine leu- The study was approved by the University of Califor- kocidin genes (lukF-PV and lukS-PV) and the arginine cat- nia, San Francisco, Committee on Human Research and abolic mobile element by using polymerase chain reaction the institutional review board of Fenway Community assays (28). We defined multidrug-resistant USA300 by Health; the institutions waived the informed consent pro- its carriage of the multiresistance conjugative plasmid cess because the study involved retrospective chart reviews.
pUSA03, which was assessed by using polymerase chain Antimicrobial Susceptibility Testing
reaction assays and whole plasmid DNA sequencing, as We tested isolates for susceptibility to oxacillin, cipro- described in the Appendix (available at www.annals.org).
floxacin, erythromycin, tetracycline, clindamycin, tri- Statistical Analysis
methoprim–sulfamethoxazole, gentamicin, vancomycin, We analyzed the population-based survey data by linezolid, and mupirocin and interpreted the results in ac- weighting each of the 532 cases originating from patients cordance with the Clinical and Laboratory Standards Insti- residing San Francisco by the inverse of the probability of tute guidelines (35). We performed inducible clindamycin being included in the sample, so that the results reflect resistance (D-zone test) by using the agar disk diffusion estimates for the entire population of San Francisco (39).
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Emergence of Multidrug-Resistant MRSA Clone USA300 On the basis of each patient’s ZIP code of residence, we estimated the number of new cases for each San Francisco Population-Based Survey
ZIP code by using the Stata subroutine svytab, which ac- On the basis of a stratified random sample of 532 counted for the stratified random sampling design (Stata, (21%) of 2495 San Francisco residents who had a culture- version 9, College Station, Texas). By using ZIP code– proven MRSA infection that was treated at 9 of 10 medical derived population estimates from the 2000 U.S. Census centers serving San Francisco, we estimated the annual in- (Summary File 3 [33]), we calculated the annual incidence cidence of USA300 infection in San Francisco to be 275 rates for San Francisco as a whole and for each of its 26 cases per 100 000 persons (CI, 256 to 295 cases per ZIP codes. We used Epimap (version 3.2.2, Centers for 100 000 persons). The annual incidence of multidrug- Disease Control and Prevention, Atlanta, Georgia) to dis- resistant USA300 infection containing multiresistance con- play the distribution of the ZIP code–specific incidence jugative plasmid pUSA03 was 26 cases per 100 000 per- rates, with boundary files obtained from the Family Health sons (CI, 16 to 36 cases per 100 000 persons). Eight Outcomes Project (40). In the 2 cross-sectional studies, we contiguous San Francisco ZIP codes had an average inci- used 2-sided chi-square or Fisher exact tests to evaluate dence of multidrug-resistant USA300 of 59 cases per100 000 persons (CI, 36 to 82 cases per 100 000 persons) associations between multidrug-resistant USA300 infec- (Figure), compared with 4 cases per 100 000 persons (CI, F1
tions and demographic or clinical characteristics, and we 0 to 8 cases per 100 000 persons) for the other 18 ZIP used the Cochran–Mantel–Haenszel procedure to calculate codes (relative risk, 16.1 [CI, 9.8 to 26.5]). According to unadjusted and adjusted relative risks for multidrug-resis- 2000 U.S. Census data (33), 10.3% (4896 of 47 664) of tant USA300 infection with associated 95% CIs (Stata, couples in the 8 ZIP codes with high incidence of multi- drug-resistant USA300 were male same-sex couples, com-pared with 2.2% (1771 of 81 141) in the other 18 ZIP Role of the Funding Sources
codes (P Ͻ 0.001). The Castro District (ZIP code 94114), Centers for Disease Control and Prevention; Univer- which had the highest percentage (25.7%) of male same- sity of California, Berkeley and San Francisco; and Pfizer sex couples of any ZIP code in the United States, had an funded this study. The funding sources had no role in the incidence of multidrug-resistant USA300 of 170 cases per study design, data collection, data analysis, data interpreta- 100 000 persons (CI, 41 to 299 cases per 100 000 persons) (Figure). Taken together, the data suggest that men who
have sex with men may be at increased risk for infection
with multidrug-resistant USA300.
HIV Clinic–Based Study
Table 1. Distribution of Methicillin-Resistant Staphylococcus
The SFGH HIV clinic is located in a ZIP code with aureus Genotypes and Antimicrobial Resistance Profiles at
the San Francisco General Hospital HIV Clinic

high prevalence of multidrug-resistant USA300 (Figure).
The 183 consecutive patients with MRSA infection treated
Resistance, %
at the SFGH HIV clinic were predominantly male (85%),white (54%), and men who have sex with men (69%) and Multidrug-
Non–Multidrug-
Non-USA300
had a median age of 40 years (interquartile range, 34 to 47 Resistant
Resistant
Genotypes‡
USA300†
years). Most (n ϭ 179) had skin and soft tissue infections that manifested as an abscess (n ϭ 121), cellulitis (n ϭ 17), folliculitis (n ϭ 18), impetigo (n ϭ 2), ulceration (n ϭ 6), and wound infection (n ϭ 15). The remaining 4 patients had non–multidrug-resistant USA300 or non-USA300 in- fection that manifested as joint infection, acute sinusitis, bloodstream infection, and pneumonia. Forty-five (25%) patients had infections involving the buttocks, genitals, or perineum (buttocks [n ϭ 27], scrotum [n ϭ 6], penis [n ϭ 5], perianal area [n ϭ 3], pubic region [n ϭ 2], rectum [n ϭ 1], and vulva [n ϭ 1]).
* Based on 30 patients. Multidrug-resistant USA300 contains the multiresistance Of the 183 MRSA cases, 170 (93%) were USA300 and 13 (7%) were non-USA300. Of the 170 USA300 † Based on 140 patients.
‡ Based on 13 patients. Distribution of other genotypes (identified by using multi- cases, 30 were multidrug-resistant USA300 (16% of all locus sequence typing and pulsed-field gel electrophoresis): ST59:USA1000 (n ϭ MRSA cases) and 140 were non–multidrug-resistant 7); ST8:USA500 (n ϭ 4); ST5:USA100 (n ϭ 2).
§ Of the 183 isolates tested, 30 (100%) multidrug-resistant USA300 isolates, 32 USA300 (76% of all cases) (Table 1). In comparison, mul- T1
(23%) non–multidrug-resistant USA300 isolates, and 3 (23%) non-USA300 iso- tidrug-resistant USA300 accounted for only 2 of 91 (2%) lates demonstrated constitutive resistance to clindamycin; 1 non-USA300 isolatedemonstrated an inducible clindamycin-resistant phenotype (ST8:USA500).
MRSA cases randomly selected from the 1014 MRSA iso- 252 19 February 2008 Annals of Internal Medicine Volume 148 • Number 4
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Emergence of Multidrug-Resistant MRSA Clone USA300 Article lates identified from throughout SFGH in the population- Health sample (Table 2). All patients in this sample who
based study (P Ͻ 0.001). Among the 118 men who have had multidrug-resistant USA300 infection were men who sex with men, the proportion of USA300 and multidrug- had sex with men, and none of the more than 3000 men resistant USA300 infections that involved the buttocks, seen at this health center annually who did not have male– genitals, or perineum was 27% (32 persons) and 11% (13 male sex had multidrug-resistant USA300 infection, sug- gesting the exclusive spread of the multidrug-resistant In bivariate analyses, having male–male sex increased USA300 clone among men who have sex with men. Infec- the risk for multidrug-resistant USA300 infection (relative tion with HIV seemed to be a risk factor (Table 2). In a
risk, 12.8 [CI, 1.8 to 91.3]) (Table 2). Twenty-nine of the
subgroup analysis involving only the 121 USA300-infected 30 patients with multidrug-resistant USA300 infection had men who have sex with men, 33 of 56 (59%) who were a history of having male–male sex, consistent with the high HIV positive had multidrug-resistant USA300 infection incidence of multidrug-resistant USA300 observed in San compared with 27 of 65 (42%) who were HIV negative Francisco ZIP codes with high percentages of male same- (relative risk, 1.4 [CI, 1.0 to 2.0]; P ϭ 0.056). We could sex couples (Figure). The proportion of multidrug-resis-
not calculate the adjusted relative risk for multidrug-resis- tant USA300 infections that involved the buttocks, geni- tant USA300 infection for men who have sex with men tals, or perineum was 30% (13 of 43 persons), whereas the after controlling for the potential confounding effects of proportion of multidrug-resistant USA300 infections that HIV infection because the 5 patients who did not have involved other sites was 14% (17 of 121 persons) (relative male–male sex also did not have multidrug-resistant risk, 2.2 [CI, 1.1 to 4.1]). Other risk factors for infection USA300 infection. Nonetheless, these data suggest that al- with multidrug-resistant USA300 were past MRSA infec- though HIV infection is a risk factor for multidrug-resis- tion (relative risk, 3.2 [CI, 1.7 to 5.9]) and past use of tant USA300 infection, having male–male sex is also a risk clindamycin (relative risk, 2.8 [CI, 1.5 to 5.3]) and tri- factor independent of HIV infection.
methoprim–sulfamethoxazole (relative risk, 2.2 [CI, 1.1 to We noted a multidrug-resistant USA300 isolate from 4.2]). In a multivariable analysis simultaneously adjusted 1 patient treated at Fenway Community Health for multi- for the 3 strongest predictors of developing multidrug- drug-resistant USA300 infection who reported having resistant USA300 infection, namely male–male sex, past male–male sex and a history of frequent travel to and from MRSA infection, and past use of clindamycin, all 3 risk the Castro District, the epicenter of multidrug-resistant factors retained their strong association with multidrug- USA300 infection in San Francisco (Figure). The isolate
resistant USA300 infection (Table 3).
has the pulsed-field gel electrophoresis subtype USA300-0114, as are the vast majority of multidrug-resistant Community Health Clinic–Based Study
USA300 isolates in San Francisco (28). The isolate also Of 130 patients with MRSA infection, 126 (97%) contained a 37136 – base pair plasmid identical in nucleo- were infected with USA300 and 4 (3%) were infected with tide sequence to the multiresistance pUSA03 found in non-USA300; of the 126 USA300 infections, 60 were multidrug-resistant USA300 isolates from San Francisco multidrug-resistant USA300 (46% of all MRSA cases) and (Appendix, available at www.annals.org) (28), indicating
66 were non–multidrug-resistant USA300 (51% of all that men who have sex with men and frequently travel cases). Compared with the 170 patients with USA300 in- between Boston and San Francisco may facilitate the clonal fection from the SFGH HIV clinic (Table 2), the 126
spread of multidrug-resistant USA300.
patients with USA300 infection from Fenway Community Emergency Department–Based Study
Health were more likely to be white (86% vs. 56%; P Ͻ In our post hoc analysis of 212 USA300 isolates col- 0.001); have male–male sex (96% vs. 69%; P Ͻ 0.001); lected in August 2004 from emergency departments in 11 and have infections involving the buttocks, genitals, or per- U.S. cities (1), 8 isolates were constitutively resistant to ineum (37% vs. 25%; P ϭ 0.026). They were also less clindamycin. We tested these 8 clindamycin-resistant likely to have HIV infection (45% vs. 100%; P Ͻ 0.001) USA300 isolates and found that only 2 carried the multi- or to have used clindamycin in the preceding 12 months drug-resistant plasmid pUSA03. One of these isolates was (1% vs. 20%; P Ͻ 0.001). The 1 Fenway Community recovered from an 81-year-old woman from New York Health patient who had used clindamycin in the preceding City, and 1 was recovered from a 37-year-old man from 12 months had multidrug-resistant USA300 infection.
Los Angeles who was identified as a man who has sex with Among the 121 men who have sex with men in the Fen- men (Talan D. Personal communication.). These findings way Community Health sample, the proportion of those suggest that multidrug-resistant USA300 is presently rare with USA300 and multidrug-resistant USA300 infections that involved the buttocks, genitals, or perineum were 39%(47 patients) and 18% (22 patients), respectively.
As in the SFGH HIV clinic population, having male– DISCUSSION
male sex was a risk factor for multidrug-resistant USA300 Multidrug-resistant USA300 is the first widely dissem- infection among patients in the Fenway Community inated, community-associated, multidrug-resistant MRSA www.annals.org
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Emergence of Multidrug-Resistant MRSA Clone USA300 Table 2. Risk Factors for Multidrug-Resistant USA300 Infections among Outpatients in San Francisco and Boston*
Risk Factor
San Francisco General Hospital HIV Clinic, San Francisco†
Fenway Community Health, Boston‡
MDR USA300/
MDR USA300/
Relative Risk
MDR USA300/
MDR USA300/
Relative Risk
(95% CI)§
(95% CI)§
Infections
Infections
Infections
Infections
in Outpatients
in Outpatients
in Outpatients
in Outpatients
with Risk
without Risk
with Risk
without Risk
Factor, n/n (%)
Factor, n/n (%)
Factor, n/n (%)
Factor, n/n (%)
Site of infection
HIV infection
CD4؉ lymphocyte count
Receipt of HAART in past 12 mo
Men who have sex with men
Hospitalization in past 12 mo
MRSA infection in past 12 mo
Antimicrobial use in past 12 mo
* MDR ϭ multidrug-resistant; MRSA ϭ methicillin-resistant Staphylococcus aureus; HAART ϭ highly active antiretroviral therapy.
† There were 30 MDR USA300 and 170 USA300 infections in total at this institution.
‡ There were 60 MDR USA300 and 126 USA300 infections in total at this institution.
§ Relative risks were calculated by using the Cochran–Mantel–Haenszel procedure for the evaluation of the risk for MDR USA300 infection among patients with risk factorcompared with patients with no risk factor. These calculations excluded 13 non-USA300 infections from the San Francisco General Hospital HIV clinic, and 4 non-USA300infections from Fenway Community Health, to eliminate the potential confounding effects of heterogenous bacterial genetic backgrounds. These calculations did not includemissing data. For patients at the San Francisco General Hospital HIV clinic, 6 (4%) had missing data on antimicrobial use, 6 (4%) had missing data on site of infection, and2 (1%) had missing data on CD4ϩ cell count. For patients at Fenway Community Health, 23 (18%) had missing data on race, 1 (1%) had missing data on CD4ϩ cell count.
clone. Emergence of multidrug-resistant USA300 in the men in San Francisco and Boston and that having male– community suggests that the USA300 lineage can over- male sex seems to be a risk factor for multidrug-resistant come the presumed fitness cost of multidrug resistance.
USA300 infection independent of HIV infection. Al- Data from this study suggest that multidrug-resistant though the use of clindamycin and mupirocin, 2 antimi- USA300 has spread rapidly among men who have sex with crobial agents that can select for multidrug-resistant 254 19 February 2008 Annals of Internal Medicine Volume 148 • Number 4
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Emergence of Multidrug-Resistant MRSA Clone USA300 Article USA300 over non–multidrug-resistant USA300 strains, lated from San Francisco patients. Since the beginning of may have contributed to the spread of multidrug-resistant the AIDS epidemic, sexual contact by men who have sex USA300 in men who have sex with men in San Francisco with men from Boston with partners from New York City, (Table 1–3), the data also suggest that antimicrobial use is
Los Angeles, and San Francisco has been associated with not an a priori condition for the spread of multidrug-resis- the dissemination of infectious pathogens (49). Because tant USA300 given the infrequent use of clindamycin and travel history is not frequently documented in patients’ mupirocin among the Fenway Community Health sample.
charts, it is not clear to what extent contacts between men Spread of the USA300 clone among men who have sex who have sex with men from Boston and San Francisco with men is associated with high-risk behaviors, including could have contributed to the clonal dissemination of multi- use of methamphetamine and other illicit drugs, sex with drug-resistant USA300. However, the genotype of multi- multiple partners, participation in a group sex party, use of drug-resistant USA300 in the patient from Fenway Com- the Internet for sexual contacts, skin-abrading sex, and his- munity Health and the recent marked predominance of tory of sexually transmitted infections (41– 43). The same multidrug-resistant USA300 in Boston suggest the multi- patterns of increased sexual risk behaviors among men who drug-resistant USA300 epidemic probably started in San have sex with men—which have resulted from changes in Francisco and has been disseminated by the frequent cross- beliefs regarding HIV disease severity with the availability coastal travel of men who have sex with men. The recent of potent antiretroviral therapy— have been driving resur- emergence of multidrug-resistant, community-associated gent epidemics of early syphilis, rectal gonorrhea, and new MRSA with similar antimicrobial susceptibility profiles to HIV infections in San Francisco, Boston, and elsewhere multidrug-resistant USA300 was recently noted among (44 – 46). Our findings that 27% (32 of 118) of men who men who have sex with men in New York City (32) and have sex with men from the SFGH HIV clinic and 39% Los Angeles (Miller LG, Diep BA. Unpublished data.), (47 of 121) of those from Fenway Community Health had indicating the potential for rapid, nationwide dissemina- infections involving the buttocks, genitals, or perineum are tion of multidrug-resistant USA300 among men who have consistent with sexual transmission of USA300 in this pop- ulation. Cook and colleagues (47) recently reported MRSA The high incidence of multidrug-resistant USA300 infections involving the buttocks or genitoperineal area of among men who have sex with men has major implications heterosexual partners; these community-associated MRSA for empirical treatment of skin infections in these patients.
infections can progress to necrotizing fasciitis of the geni- Several important antimicrobial classes for treatment of toperineal region (Fournier gangrene) (48). It is not clear MRSA infections or eradication of colonization, including whether the behavior potentiating these infections among clindamycin, tetracycline, and mupirocin, may not be ef- men who have sex with men is anal sex (that is, dissemi- fective in this population. Resistance to trimethoprim– nation of rectal carriage of community-associated MRSA), sulfamethoxazole and rifampin remains rare among skin-abrading sexual practices, or increased frequency of USA300 isolates and was not seen in multidrug-resistant intimate skin-to-skin contact; prevention messages may USA300 in our study (Table 1). However, prophylactic
therefore need to suggest caution in each of these practices.
antimicrobial use has selected for the emergence of tri- The risk for multidrug-resistant USA300 infections in methoprim–sulfamethoxazole resistance in subclones ge- the buttocks, genitals, or perineum was 30% (13 of 43) netically related to the USA300 lineage in patients from among SFGH HIV clinic patients and 47% (22 of 47) San Francisco and New York City who were infected with among Fenway Community Health patients, suggesting a HIV (50 –52). Prudent use of these antimicrobial agents similar role of sexual contact in the rapid dissemination of for suspected MRSA disease in men who have sex with multidrug-resistant USA300. We also found that a patient men is advisable to slow the emergence of even more resis- treated at Fenway Community Health for infection with tant community-associated MRSA. The pUSA03 plasmid multidrug-resistant USA300 who had a history of frequent that determines multidrug resistance in multidrug-resistant travel to and from the Castro District in San Francisco had USA300 belongs to a highly promiscuous class of conjuga- an multidrug-resistant USA300 clone identical to that iso- tive plasmids that could readily accept transposons encod- Table 3. Adjusted Relative Risk for Multidrug-Resistant USA300 Infections among Outpatients Treated at the San Francisco
General Hospital HIV Clinic*

Characteristic
Adjusted Relative Risk (95% CI)
Methicillin-resistant Staphylococcus aureus infection in past 12 mo *Results shown for the most stable multivariable analysis. Addition to the analysis of variables for past use of mupirocin; past use of trimethoprim-sulfimethoxazole; andinfection involving buttocks, genitals, or perineum led to spurious estimates because of small numbers of events.
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Emergence of Multidrug-Resistant MRSA Clone USA300 ing resistance to aminoglycosides, trimethoprim, vancomy- Current author addresses and author contributions are available at www cin, and other antimicrobials, potentiating the emergence of even more resistant community-associated MRSA (28,53).
Our study has limitations. Our incidence estimates for References
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Grant Support: By U.S. Public Health Service grant R01/CCR923381
soft tissue infection in Italy. Euro Surveill. 2007;12:E070412.1. [PMID:17439803] (Dr. Chambers); a University of California, Berkeley, Faculty Research 14. Wannet WJ, Heck ME, Pluister GN, Spalburg E, van Santen MG, Huijs-
Grant (Dr. Sensabaugh); an unrestricted grant from Pfizer (Dr. Perd- dans XW, et al. Panton-Valentine leukocidin positive MRSA in 2003: the Dutch
reau-Remington); and a Microbial Pathogenesis and Host Defense Post- situation. Euro Surveill. 2004;9:28-9. [PMID: 15591693] doctoral Fellowship (5T32AI060537-02) (Dr. Diep) and an HIV Trans- 15. Huijsdens XW, van Santen-Verheuvel MG, Spalburg E, Heck ME, Pluister
lational Research Fellowship (5T32AI060530-02) (Dr. Graber) from the GN, Eijkelkamp BA, et al. Multiple cases of familial transmission of community-
University of California, San Francisco; and U.S. Public Health Service acquired methicillin-resistant Staphylococcus aureus. J Clin Microbiol. 2006;44: 2994-6. [PMID: 16891525]
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Potential Financial Conflicts of Interest: None disclosed.
JU. Dissemination of community-acquired methicillin-resistant Staphylococcus
aureus
clones in northern Norway: sequence types 8 and 80 predominate. J Clin
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Medicine, University of California, San Francisco, San Francisco General MRSA [Letter]. N Engl J Med. 2005;353:532-3. [PMID: 16079385] Hospital, 1001 Potrero Avenue, Building 30, Room 3300, San Fran- 18. Gonzalez BE, Martinez-Aguilar G, Hulten KG, Hammerman WA,
cisco, CA 94110; e-mail, bdiep@epi-center.ucsf.edu.
Coss-Bu J, Avalos-Mishaan A, et al. Severe Staphylococcal sepsis in adolescents
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Current Author Addresses: Drs. Diep, Chambers, Graber, and Perd-
Obtaining of funding: H.F. Chambers, G.F. Sensabaugh, F. Perdreau- reau-Remington; Ms. Phan; and Ms. Carleton: University of California, San Francisco, San Francisco General Hospital, 1001 Potrero Avenue, Collection and assembly of data: B.A. Diep, C.J. Graber, J.D. Szu- Building 30, Room 3300, San Francisco, CA 94110.
mowski, J.H. Chen, F. Lin, J. Lin, T.H. Phan, H.A. Carleton, L.K.
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, APPENDIX
Box 466, Torrance, CA 90509.
Dr. Han: State Laboratory Institute, 305 South Street, Jamaica Plain, We tested for multiresistance conjugative plasmid pUSA03 by using polymerase chain reaction assays designed to detect Ms. J. Lin, Mr. Chen, Ms. F. Lin, and Dr. Sensabaugh: School of Public ermC, mupA, and the conjugative gene transfer genes traE and Health, MC#7360, University of California, Berkeley, CA 94720.
traI (28). These assays used the following oligonucleotides: mu- Ms. McDougal and Dr. Tenover: Centers for Disease Control and Pre- pA–F, 5'-CTTAGTTAACTCAGCATCAG-3'; mupA–R, 5'-GG vention, 1600 Clifton Road, Atlanta, GA 30333.
TTTGATAGCGGCTCTATGC-3'; ermC–F, 5'-GAAATCGG Dr. Cohen: Fenway Community Health, 7 Haviland Street, Boston, MA CTCAGGAAAAGG-3'; ermC–R, 5'-GCTATTCACTTTAGG TTTAGGATG-3'; traE-F, 5'-AACAAATGCGTACTACAGA Dr. Mayer: Brown University/Miriam Hospital, 164 Summit Avenue, CC-3'; traE–R, 5'-CCTGCTGTTGCTGTATCC-3'; traI–F, 5'- ACCGATATGAATAACACCGTC-3';traI–R,5'-AAACCTTCACAAGCAATGGAC-3'.
Author Contributions: Conception and design: B.A. Diep, C.J. Graber.
By using whole-plasmid DNA sequencing, we found that Analysis and interpretation of the data: B.A. Diep, C.J. Graber, J.D.
the pUSA03 plasmid from the Fenway Community Health pa- Szumowski, L.G. Miller, L.L. Han, F.C. Tenover, D.E. Cohen, K.H.
tient with multidrug-resistant USA300 infection who had a fre- Mayer, G.F. Sensabaugh, F. Perdreau-Remington, H.F. Chambers.
Drafting of the article: B.A. Diep.
quent history of travel to and from the Castro District was iden- Critical revision of the article for important intellectual content: B.A.
tical in nucleotide sequence to the multiresistance pUSA03 found Diep, C.J. Graber, H.F. Chambers, G.F. Sensabaugh, F. Perdreau-Rem- in multidrug-resistant USA300 isolates from San Francisco (Gen- ington, J.D. Szumowski, L.G. Miller, L.L. Han, J.H. Chen, F. Lin, J.
Bank Accession no. CP000258) (28). In brief, we prepared plas- Lin, T.H. Phan, H.A. Carleton, L.K. McDougal, F.C. Tenover, D.E.
mid DNA by using the Qiagen Plasmid Midi Kit (Qiagen, Va- lencia, California). We sequenced 250 ng of plasmid DNA Final approval of the article: B.A. Diep, H.F. Chambers, C.J. Graber, directly with 2.0 pmol of primers by using an Applied Biosystems J.D. Szumowski, L.G. Miller, L.L. Han, J.H. Chen, F. Lin, J. Lin, T.H.
96-capillary 3730xl DNA Analyzers (DNA Sequencing Facility, Phan, H.A. Carleton, L.K. McDougal, F.C. Tenover, D.E. Cohen, K.H.
Mayer, G.F. Sensabaugh, F. Perdreau-Remington.
University of California, Berkeley, California). Primers (n ϭ 86) Provision of study materials or patients: H.F. Chambers, F. Perdreau- were designed to provide complete sequence coverage of the pro- Remington, L.G. Miller, L.L. Han, D.E. Cohen, K.H. Mayer.
totypical pUSA03 nucleotide sequence (28); these primers are Statistical expertise: B.A Diep, C.J. Graber, L.G. Miller.
described in detail in the Appendix Table.
W-50 19 February 2008 Annals of Internal Medicine Volume 148 • Number 4
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Appendix Table. Primers Used in Sequencing of Multiresistance Conjugative Plasmid pUSA03
5؅ to 3؅
5؅ to 3؅
Coverage of
pUSA03 Open
Reading
Frames*

* As detailed in GenBank Accession no. CP000258 (28).
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19 February 2008 Annals of Internal Medicine Volume 148 • Number 4 W-51
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Source: http://thefenwayinstitute.org/documents/1-15-08_MRSA_early_release.pdf

Microsoft word - history_ms.doc

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