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Risk Factors for Colonization with Methicillin-Resistant Staphylococcus aureus (MRSA) in Patients Admitted to an Urban Hospital: Emergence of Community-Associated MRSA Nasal Carriage

  1. Alicia I. Hidron1,
  2. Ekaterina V. Kourbatova1,
  3. J. Sue Halvosa2,
  4. Bianca J. Terrell1,
  5. Linda K. McDougal3,
  6. Fred C. Tenover3,
  7. Henry M. Blumberg1,2, and
  8. Mark D. King1,2
  1. 1Division of Infectious Diseases, Department of Medicine, Emory University School of Medicine, Atlanta, Georgia
  2. 2Epidemiology Department, Grady Memorial Hospital, Atlanta, Georgia
  3. 3Centers for Disease Control and Prevention, Atlanta, Georgia
  1. Reprints or correspondence: Dr. Henry M. Blumberg, Div. of Infectious Diseases, Emory University School of Medicine, 49 Jesse Hill Dr., Atlanta, GA 30303 (henry.m.blumberg{at}emory.edu).
 
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Abstract

Background. Surveillance cultures performed at hospital admission have been recommended to identify patients colonized with methicillin-resistant Staphylococcus aureus (MRSA) but require substantial resources. We determined the prevalence of and risk factors for MRSA colonization at the time of hospital admission among patients cared for at a public urban hospital.

Methods. Anterior nares cultures were obtained within 48 h after admission during a 1-month period. A case-control study and molecular typing studies were performed.

Results. A total of 53 (7.3%) of 726 patients had a nares culture positive for MRSA, and 119 (16.4%) had a nares culture that was positive for methicillin-susceptible S. aureus. In multivariate analysis, risk factors for MRSA colonization included antibiotic use within 3 months before admission (odds ratio [OR], 2.5; 95% confidence interval [CI], 1.2–5.0), hospitalization during the past 12 months (OR, 4.0; 95% CI, 2.0–8.2), diagnosis of skin or soft-tissue infection at admission (OR, 3.4; 95% CI, 1.5–7.9), and HIV infection. A total of 47 (89%) of 53 case patients colonized with MRSA had at least 1 of these independent risk factors, in contrast to 343 (51%) of 673 control patients (OR, 7.5; 95% CI, 3.2 –17.9). Molecular typing demonstrated that 16 (30%) of 53 MRSA nares isolates (2.2% of the 726 isolates) belonged to the USA300 community-associated MRSA (CA-MRSA) genotype.

Conclusion. The prevalence of MRSA colonization at the time of patient admission was high (>7%). Limiting surveillance cultures to patients with ⩾1 of the identified risk factors may allow for targeted screening. The emergence of CA-MRSA colonization represents a new, unrecognized reservoir of MRSA within hospitals, potentially increasing the risk for horizontal transmission.

Methicillin-resistant Staphylococcus aureus (MRSA) infections have become increasingly problematic in both health care and community settings. Data from the Centers for Disease Control and Prevention's (CDC's) National Nosocomial Infections Surveillance network have shown that MRSA represent >50% of S. aureus strains causing nosocomial infections in patients in intensive care units [1]. Data from the SENTRY Antimicrobial Surveillance Program have confirmed increasing rates of methicillin-resistance among S. aureus isolates worldwide, in both hospital-acquired and community-onset infections [2]. Furthermore, recent reports have noted the emerging problem of community-associated MRSA (CA-MRSA) infections [3–10].

Recognition and isolation of persons either colonized or infected with MRSA is recommended for minimizing the spread of MRSA within hospitals. Recent guidelines published by the Society for Healthcare Epidemiology of America (SHEA) recommend surveillance cultures at the time of hospital admission for patients at high risk for MRSA carriage [11]. Risk factors associated with an increased risk of nosocomial acquisition of MRSA are well recognized [12, 13]. A limited number of studies have attempted to determine risk factors for colonization with MRSA at admission to the hospital [14–16] but were conducted primarily in tertiary care centers and before the widespread emergence of CA-MRSA infections. It is unclear whether risk factors for MRSA colonization are homogeneous across different populations or whether CA-MRSA colonization is associated with a different set of risk factors than those described elsewhere.

The objective of our study was to determine the prevalence of and risk factors for MRSA colonization among patients admitted to a large urban public hospital during a period in which CA-MRSA infection was increasingly prevalent. Additionally, we sought to determine the prevalence of nasal carriage of CA-MRSA strains.

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Methods

Study population and data collection. The study was conducted at Grady Memorial Hospital, a 1000-bed, public inner-city hospital in Atlanta, Georgia. The study was approved by the Emory University Institutional Review Board and the Grady Research Oversight Committee. During the first 2 weeks of both June and July 2003, specimens from the anterior nares of all patients admitted to the hospital on Sunday, Tuesday, or Thursday (except for patients admitted to the psychiatry service or the burn unit) were obtained for culture within 48 h after hospital admission.

Data on demographic characteristics, medical history, previous hospitalizations or clinic visits, antibiotic use within the past year, previous infection with MRSA, type of housing, and history of incarceration within the past year were obtained from hospital, pharmacy, and microbiology records or directly from patients. Data on antibiotic use were obtained from computerized pharmacy records and from patient interviews. Patients who described themselves as living in a house or apartment were classified as living in residential housing, whereas patients who were living in personal-care homes, nursing homes, long-term care facilities, correctional facilities, or other hospitals or who were homeless were classified as living in alternative housing.

Nares cultures. Samples were obtained for culture from anterior nares using Culturette swabs (Becton-Dickinson). Swabs were plated on mannitol salt plates (Becton-Dickinson) at 35°C for 24 h. Yellow colonies were streaked on blood agar plates (Becton-Dickinson) and incubated at 35°C for 24 h. Golden hemolytic cultures were identified as S. aureus by means of the Staphyloslide agglutination test (Becton-Dickinson). Oxacillin susceptibility was performed by assessing growth on Mueller-Hinton agar with 4% NaCl and 6µg/mL oxacillin at 35°C for 24 h in accordance with NCCLS guidelines [17, 18].

Molecular typing studies. PFGE was performed on all MRSA isolates as described by Bannerman et al. [19]. Restriction was performed with SmaI (Roche Molecular Biochemicals). Gel photographs were digitized and saved as a .tiff file for analysis with BioNumerics Software (Applied Maths). Cluster analysis was performed using unweighted pair-group methodology based on Dice coefficients. Pulsed-field type (PFT) clusters were defined using a coefficient of similarity of 80%. For visual strain analysis, isolates were considered to be different if PFGE patterns differed by >3 bands [19]. MRSA isolates were defined as having CA-MRSA genotypes if PFGE demonstrated either USA300 or USA400 PFTs according to the method described by McDougal et al. [20]. MRSA isolates with other PFTs were considered to have health care—associated genotypes (HA-MRSA).

SCC mec typing and Panton-Valentine leukocidin (PVL) gene analysis. The SCCmec type was determined by PCR typing of the mec gene complex, as described by Okuma et al. [21]. The presence of PVL genes in MRSA was assessed using PCR, as described by Lina et al. [22].

Antimicrobial susceptibility testing. In vitro antimicrobial susceptibility testing was done using the disk diffusion method in accordance with NCCLS standards [17].

Case-control study. A case-control study was performed to identify risk factors for colonization with MRSA. Cases were defined as patients for whom results of nasal culture revealed colonization with MRSA. Controls were defined as patients who were not colonized with MRSA (i.e., they were either colonized with methicillin-susceptible S. aureus [MSSA] or had negative results of culture).

Statistical analysis. Data were entered into Microsoft Access 2000 software (Microsoft Corporation) and exported into SAS software, version 8.2 (SAS Institute), which was used for data analyses. Identification of potential risk factors for MRSA colonization was initially determined by means of univariate analysis. Variables statistically significantly associated with MRSA colonization in univariate analysis were entered into a multivariate unconditional logistic regression model controlling for age, sex, and race. The final model was derived by incorporating a stepwise backward-elimination approach. Interaction between covariates was tested using 2-way interaction terms, and colinearity was assessed. Goodness of fit of the final model was assessed using the Hosmer-Lemeshow goodness of fit test. A P value of ⩽.05 was defined as statistically significant.

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Results

Prevalence of nasal MRSA colonization. Nares specimens were obtained for culture from 728 (78%) of 937 patients admitted to the hospital during the study period (figure 1). Of the 728 cultures, 2 were excluded because of mislabeled swabs, yielding 726 nares cultures. Of the 209 patients for whom samples were not cultured, 34 were admitted to services excluded from our study design, 10 patients declined to participate, and the remaining 165 patients were not available for nares culture within 48 h after admission because of hospital discharge or absence from their room for procedures or diagnostic studies. Of the 726 nares cultures, 53 (7.3%) were positive for MRSA, 119 (16.3%) were positive for MSSA, and 554 (76.3%) were culture negative (figure 1). MRSA accounted for 53 (31%) of 172 S. aureus isolates. Among 81 HIV-infected patients, the prevalence of MRSA colonization was 17% (14 of 81), in contrast to 6% (39 of 645) among HIV-seronegative persons (OR, 3.2; 95% CI, 1.7–6.3; P < .001) (figure 1). Only 7 (13%) of 53 cases colonized with MRSA were admitted with or developed a laboratory-confirmed MRSA infection during hospitalization; 5 of these 7 had bacteremia. A total of 11 of 53 cases had a diagnosis of a skin and soft-tissue infection (i.e., 4 culture confirmed and 7 with a clinical diagnosis), as noted in table 1.

Figure 1
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Figure 1

A, Study eligibility, enrollment, and prevalence of nasal colonization with methicillin-resistant Staphylococcus aureus (MRSA). The 3 predominant pulsed-field types (PFTs) recovered from nasal isolates are shown, with USA300 accounting for 30%, USA100 for 40%, and USA500 for 19% of all MRSA isolates from nares specimens (other PFTs accounted for the remaining 11%). B, Prevalence of nasal colonization with MRSA, stratified according to HIV infection status. CA-MRSA, community-acquired MRSA. MSSA, methicillin-susceptible S. aureus.

Figure 2
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Figure 2

Association between number of independent risk factors present and colonization with methicillin-resistant Staphylococcus aureus (P < .001, by the χ2 test for liner trend in proportions).

Figure 3
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Figure 3

Dendrogram (left) of representative pulsed-field types (PFTs) for methicillin-resistant Staphylococcus aureus (MRSA) isolates from cultures of nares specimens obtained from patients admitted to Grady Memorial Hospital in Atlanta, Georgia (lanes 1, 2, 4, 6, and 8), and for representative MRSA standard type strains previously published by the Centers for Disease Control and Prevention (lanes 3, 5, and 7) [20]. Three predominant PFTs were observed in the isolates recovered from nares cultures. The predominant PFTs were USA300 (16 [30%] of 53 isolates; lanes 1 and 2), USA100 (21 [40%] of 53; lane 4), and USA500 (10 [19%] of 53; lanes 6 and 8).

Table 1
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Table 1

Characteristics of patients admitted to Grady Memorial Hospital (Atlanta, GA) and results of univariate analysis of risk factors for nasal colonization with methicillin-resistant Staphylococcus aureus (MRSA).

Risk factors for nasal colonization with MRSA. Comparative demographic and clinical characteristics are shown in table 1. In univariate analysis, patients with MRSA colonization were similar to patients without MRSA colonization with respect to age, race, sex, presence of diabetes, and number of clinic visits during the previous year (table 1). Risk factors for colonization with MRSA in univariate analysis are shown in table 1.

In multivariate analysis, factors independently associated with an increased risk of MRSA colonization included hospitalization within the past 12 months (OR, 4.01; 95% CI, 1.97–8.15), the presence of a skin or soft-tissue infection at admission (OR, 3.40; 95% CI, 1.46–7.90), antimicrobial use within the 3 months before admission, and HIV-seropositive status (table 2). HIV infection was associated with an increased risk of MRSA colonization among HIV-infected persons who had not received antibiotics within 3 months before the current admission (OR, 13.81; 95% CI, 4.34–43.04), but not among HIV-seropositive persons who had received antibiotics within 3 months before admission (OR, 1.68; 95% CI, 0.63–4.43). Antimicrobial use in the 3 months before hospital admission was associated with a higher risk of MRSA colonization among HIV-seronegative persons than among HIV-seronegative persons who had not received antibiotics within 3 months before admission (OR, 2.46; 95% CI, 1.20–5.03) (table 2).

Table 2
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Table 2

Multivariate analysis of the risk factors associated with methicillin-resistant Staphylococcus aureus colonization in patients newly admitted to Grady Memorial Hospital (Atlanta, GA).

Additional analyses assessed risk factors for MRSA nares colonization on the basis of genotype. Skin and soft-tissue infection was an independent risk factor for CA-MRSA USA300 colonization (OR, 9.9; 95% CI, 3.2–30.9), whereas hospitalization in the past 12 months (OR, 8.1; 95% CI, 2.8–23.1) and antimicrobial use among HIV-seronegative patients (OR, 3.0; 95% CI, 1.2–7.2) were independent risk factors for nares colonization with HA-MRSA genotypes. HIV infection was an independent risk factor for both CA-MRSA and HA-MRSA nares colonization (data not shown).

Of the 53 cases colonized with MRSA, 47 (89%) had at least 1 of the independent risk factors identified in multivariate analysis, compared with 343 (51%) of 673 controls who were not colonized with MRSA (OR, 7.5; 95% CI, 3.2 –17.9). Cases and controls were compared to assess the impact of the number of independent risk factors on the likelihood of MRSA colonization. A significant dose-response relationship was demonstrated between MRSA colonization and the number of risk factors present (P < .001, by the χ2 test for linear trend in proportions) (figure 2).

Molecular and genetic typing. Molecular typing revealed that 47 (89%) of 53 isolates clustered into 1 of 3 PFGE patterns or PFTs (figure 3). These 3 PFTs included USA300 (16 [30%] of 53 isolates), USA100 (21 [40%] of 53), and USA500 (10 [19%] of 53). The overall prevalence of colonization with CA-MRSA with the USA300 PFT among patients admitted to our institution was 2.2% (16 of 726). SCCmec IV and PVL genes were identified in 15 (94%) of 16 USA300 isolates; the remaining USA300 isolate carried SCCmec II and lacked PVL genes.

Antimicrobial susceptibility. Antimicrobial susceptibility results for the MRSA isolates according to PFT are shown in table 3. All USA300 isolates were resistant to β-lactams and erythromycin and were susceptible to clindamycin, trimethoprim-sulfamethoxazole, rifampin, gentamicin, and vancomycin. Only 6 (35%) of 17 USA300 isolates were susceptible to ciprofloxacin. Susceptibilities of MRSA isolates with a health care—associated genotype (i.e., genotypes other than USA300 or USA400) are shown in table 3.

Table 3
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Table 3

Antibiotic susceptibility patterns of methicillin-resistant Staphylococcus aureus isolates recovered from nares cultures, according to pulsed-field type.

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Discussion

Among patients admitted to a large, urban public hospital in Atlanta, 7.3% were colonized with MRSA at the time of admission, and one-third of those colonized were harboring the CA-MRSA USA300 clone. Thus, the overall prevalence of colonization with CA-MRSA USA300 was 2.2%. Persons with HIV infection were significantly more likely to be colonized with MRSA than were HIV-seronegative persons (17% vs. 6%), as were persons admitted with a diagnosis of skin and soft-tissue infection.

The prevalence of MRSA colonization at hospital admission observed in our study is higher than the prevalence published in previous reports (range, 1.3%–5.3%) [14, 15, 23–26]. Potential explanations for the higher prevalence observed in our study include differences in patient demographic characteristics, underlying medical problems, and frequency of encounters with the health care system, as well as changing temporal trends in colonization with MRSA, as exemplified by an increased contribution to the prevalence of colonization by CA-MRSA [14, 15]. In addition, the high prevalence of HIV infection in our study population (11% of all patients admitted to the hospital), coupled with a higher prevalence of MRSA colonization among HIV-positive patients, represents another possible explanation for the higher prevalence of MRSA colonization we observed.

In multivariate analysis, hospitalization within the preceding year, receipt of antibiotics within 3 months before admission, presence of a skin and soft-tissue infection at the time of admission, and HIV-seropositive status were identified as independent risk factors for MRSA colonization. To our knowledge, our study is the first that has identified HIV infection and skin and soft-tissue infection at the time of hospital admission as risk factors for colonization with MRSA. HIV-seropositive patients who were not receiving antibiotics had an increased prevalence of colonization with MRSA. We hypothesize that the lack of association for MRSA colonization among HIV-infected patients who had recently received antimicrobial therapy may be related to use of trimethoprim-sulfamethoxazole for prophylaxis against Pneumocystis carinii pneumonia, which could potentially reduce colonization with MRSA. Further studies are needed to investigate this hypothesis.

In an effort to reduce nosocomial transmission of MRSA, SHEA has recommended surveillance cultures at the time of hospital admission for patients at high risk of MRSA carriage [11]. Only 6 (11%) of 53 cases with MRSA nares colonization in our study had clinical infections with MRSA; thus, the majority of persons harboring MRSA would not be identified through surveillance of clinical cultures. Screening all patients admitted to a large institution can be logistically and financially challenging. Furthermore, the proposed revised isolation guidelines from the Healthcare Infection Control Practices Advisory Committee (HICPAC) have not included performance of surveillance cultures as a routinely recommended strategy for all patients admitted to an institution [27].

In the SHEA guidelines, a working definition of what constitutes a high risk for MRSA (i.e., one that defines patients who are to be targeted for surveillance cultures) remains unclear [11]. In our study, we have confirmed the association between MRSA colonization and previous hospitalization or antibiotic use and have also provided evidence that patients with HIV infection and patients with skin and soft-tissue infection at the time of admission are at significantly increased risk for nasal MRSA carriage. Furthermore, the likelihood of MRSA colonization increases significantly in accordance with the number of risk factors present. In our institution, performance of surveillance cultures for patients with ⩾1 of the independent risk factors identified herein may provide relatively effective surveillance while significantly reducing the number of patients requiring surveillance cultures (by approximately one-half). However, logistically, it could be difficult for some institutions to implement a risk-based surveillance program, compared with universal performance of surveillance cultures.

Recent reports have noted the emergence of CA-MRSA infections (especially skin and soft-tissue infections) and outbreaks of CA-MRSA disease among persons without traditional risk factors for MRSA [4–9]. However, reports of nasal colonization with the CA-MRSA USA300 clone have been limited [28, 29]. Among these latter reports, there was significant heterogeneity in the definition of CA-MRSA, with the majority of definitions relying on the timing of isolation of S. aureus, and molecular typing was not performed in all of the studies. In our study, we have demonstrated by molecular typing that a significant proportion (2.2%) of persons admitted to an urban hospital are colonized with the CA-MRSA USA300 clone, with most (94%) of these strains carrying PVL genes and the SCCmec IV allele.

CA-MRSA USA300 isolates were more commonly recovered from the nares of patients admitted with skin and soft-tissue infections. A potential explanation of why the CA-MRSA USA300 clone is more likely to lead to clinical infection, particularly to skin and soft-tissue infections, is the fact that USA300 strains generally contain PVL genes. Colonization with health care—associated MRSA genotypes, which generally lack PVL genes, may be less likely to result in clinically apparent infection. Among military recruits, an increased risk of developing a soft-tissue infection was observed for those colonized with CA-MRSA, compared with those colonized with MSSA [28]. In our study, 10 (63%) of the 16 patients colonized with CA-MRSA USA300 genotype in their nares did not have clinically apparent infections at the time of admission; prospective studies would be needed to delineate whether persons colonized with this clone are at increased risk of developing infections, compared with persons colonized with health care—associated genotypes.

The emergence of CA-MRSA as a common cause of staphylococcal infections [30] and nares colonization, as suggested by our findings presented in this report, presents new challenges to infection-control practitioners for reducing nosocomial transmission of MRSA. The independent risk factors for MRSA colonization identified herein were observed in 14 (88%) of 16 patients colonized with CA-MRSA USA300, suggesting that a history of health care contact is not a reliable way to differentiate between community-associated and health care—associated genotypes. However, the risk factors we identified would still allow for identification of persons colonized with MRSA, regardless of the genotype of the colonization strain.

The previous paradigm for MRSA acquisition was that it occurred in the health care setting [14]. This is no longer exclusively the case, given the emergence of CA-MRSA. Although it may continue to be the case that most patients colonized with health care—associated MRSA genotypes had acquisition in health care facilities, we suspect that acquisition of the MRSA USA300 clone is occurring both in the community and within the health care setting. Support for this hypothesis stems from the high prevalence of CA-MRSA USA300 observed in community-onset S. aureus skin and soft-tissue infections in Atlanta, which represents a focus for community acquisition [30], and from evidence that nosocomial infections are now being caused by CA-MRSA [31, 32].

Our study is subject to certain limitations. Of the patients eligible for screening, 18% were not available to have a nares culture performed within 48 h after hospital admission, which creates the potential for selection bias. We believe selection bias was minimal, because patients who did not have a nares culture performed did not differ from persons included in the study with regard to age, race, or HIV infection status. Our data was collected at a public urban hospital with a high prevalence of HIV infection. Thus, generalization of these findings to other populations should be done with caution. Finally, the temporal relationship between MRSA colonization and acquisition of the reported risk factors is unknown, because this study assessed the prevalence of colonization at a specific point in time.

In summary, we identified a high prevalence (>7%) of colonization with MRSA among patients admitted to an urban hospital. The majority of cases colonized with MRSA did not demonstrate evidence of clinical infection, indicating that clinical cultures for MRSA only represent the tip of the iceberg of the overall MRSA burden in our hospital. In our institution, limiting surveillance cultures to patients with ⩾1 of the identified risk factors may allow for targeted screening designed to maximize recognition of MRSA colonization while reducing the logistic requirements and financial resources required. Finally, we have demonstrated that a significant number of patients (2.2% of all adults admitted to the hospital) are colonized with CA-MRSA USA300 clone at the time of admission, which represents an emerging and increasingly problematic reservoir of MRSA in US hospitals.

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Acknowledgments

Financial support. Emory Medical Care Foundation (to M.D.K.), Emory Mentored Clinical Research Scholars Program, National Institutes of Health (NIH) National Center for Research Resources (grant K12 RR017643 to H.M.B. and M.D.K.), and NIH National Institute of Allergy and Infectious Diseases (grant K23 AI054371 to M.D.K.)

Potential conflicts of interest. All authors: no conflicts.

  • Received November 11, 2004.
  • Accepted February 23, 2005.
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  1. Clin Infect Dis. (2005) 41 (2): 159-166. doi: 10.1086/430910
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