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Colonization with antibiotic-susceptible strains protects against methicillin-resistant Staphylococcus aureus but not vancomycin-resistant enterococci acquisition: a nested case-control study

Critical Care volume 15, Article number: R210 (2011) Cite this article

Abstract

Introduction

Harboring sensitive strains may prevent acquisition of resistant pathogens by competing for colonization of ecological niches. Competition may be relevant to decolonization strategies that eliminate sensitive strains and may predispose to acquiring resistant strains in high-endemic settings. We evaluated the impact of colonization with methicillin-sensitive Staphylococcus aureus (MSSA) and vancomycin-sensitive enterococci (VSE) on acquisition of methicillin-resistant Staphylococcus aureus (MRSA) and vancomycin-resistant enterococci (VRE), respectively, when controlling for other risk factors.

Methods

We conducted a nested case-control study of patients admitted to eight ICUs performing admission and weekly bilateral nares and rectal screening for MRSA and VRE, respectively. Analyses were identical for both pathogens. For MRSA, patients were identified who had a negative nares screen and no prior history of MRSA. We evaluated predictors of MRSA acquisition, defined as a subsequent MRSA-positive clinical or screening culture, compared to those with a subsequent MRSA-negative nares screen within the same hospitalization. Medical records were reviewed for the presence of MSSA on the initial MRSA-negative nares screen, demographic and comorbidity information, medical devices, procedures, antibiotic utilization, and daily exposure to MRSA-positive patients in the same ward. Generalized linear mixed models were used to assess predictors of acquisition.

Results

In multivariate models, MSSA carriage protected against subsequent MRSA acquisition (OR = 0.52, CI: 0.29, 0.95), even when controlling for other risk factors. MRSA predictors included intubation (OR = 4.65, CI: 1.77, 12.26), fluoroquinolone exposure (OR = 1.91, CI: 1.20, 3.04), and increased time from ICU admission to initial negative swab (OR = 15.59, CI: 8.40, 28.94). In contrast, VSE carriage did not protect against VRE acquisition (OR = 1.37, CI: 0.54, 3.48), whereas hemodialysis (OR = 2.60, CI: 1.19, 5.70), low albumin (OR = 2.07, CI: 1.12, 3.83), fluoroquinolones (OR = 1.90, CI: 1.14, 3.17), third-generation cephalosporins (OR = 1.89, CI: 1.15, 3.10), and increased time from ICU admission to initial negative swab (OR = 15.13, CI: 7.86, 29.14) were predictive.

Conclusions

MSSA carriage reduced the odds of MRSA acquisition by 50% in ICUs. In contrast, VSE colonization was not protective against VRE acquisition. Studies are needed to evaluate whether decolonization of MSSA ICU carriers increases the risk of acquiring MRSA when discharging patients to high-endemic MRSA healthcare settings. This may be particularly important for populations in whom MRSA infection may be more frequent and severe than MSSA infections, such as ICU patients.

Introduction

Methicillin-resistant Staphylococcus aureus (MRSA) and vancomycin-resistant enteroccoci (VRE) cause substantial morbidity and mortality in hospitalized populations [1–6]. Patients acquiring MRSA or VRE incur significant risks of subsequent infection. Up to 11% of MRSA-colonized in-patients develop MRSA disease during their hospital stay, and this risk can approach 30% in the critically ill [7–9]. Similarly, 19% of VRE-colonized patients in the intensive care unit (ICU) develop VRE infection during hospitalization, and this risk can approach 32% in those with transplants or cancer [10–12]. Risks of MRSA and VRE infection after colonization also extend into the post-discharge setting. We previously found that 29% of MRSA carriers and 8% of VRE carriers developed invasive disease within 18 months, with post-discharge MRSA and VRE infections often requiring readmission [13–15].

Importantly, compared to MSSA colonization, MRSA colonization is associated with a four-fold increase in infection risk [16]. Even after controlling for host risk factors, it has been shown that MRSA colonized-patients are more likely to develop subsequent infection compared to MSSA-colonized patients [17]. These differential risks of infection following colonization are important since MRSA bacteremia is associated with greater attributable morbidity and mortality compared to MSSA bacteremia [2, 3, 18]. Moreover, the increased mortality associated with MRSA versus MSSA extends up to three months after hospital discharge [19].

Given these risks, many studies have evaluated predictors of MRSA and VRE acquisition to improve infection prevention methods. Most predictors of MRSA acquisition have related to host comorbidities, hospital factors, and antimicrobial use. For instance, diabetes, hemodialysis, ulcers, trauma, ICU stays, admission to surgical ICUs, and antibiotic exposure are known to predispose to MRSA colonization [20–26]. Although VRE carriage more commonly occurs in the critically ill, similar risk factors exist for VRE acquisition including immunosuppression, neutropenia, hematologic malignancies, ICU admission, and antibiotic exposure [27–32]. Environmental contamination has also been associated with MRSA and VRE acquisition [33–39].

Although predictors of MRSA and VRE colonization have been well documented, less is known about protective factors. It has been hypothesized that methicillin-sensitive Staphylococcus aureus (MSSA) and other antibiotic-sensitive bacteria may protect against MRSA acquisition by competing for colonization of the anterior nares [40]. Competition may be relevant to decolonization strategies that may eliminate MSSA and predispose to MRSA acquisition in high endemic settings such as ICUs and nursing homes. Therefore, we assessed whether MSSA or vancomycin-sensitive enterococci (VSE) colonization reduces the risk of MRSA and VRE acquisition, respectively.

Materials and methods

We conducted a retrospective nested case-control study of patients admitted to eight adult ICUs between 1 September 2003 and 30 April 2005 at a 750-bed academic medical center in Boston, Massachusetts, who were not previously known to have MRSA or VRE and who had MRSA-negative or VRE-negative surveillance cultures upon ICU admission. All ICUs performed high-compliance admission and weekly surveillance bilateral nares cultures for MRSA and rectal cultures for VRE, providing a systematic method to distinguish between imported and incident cases during endemic conditions. ICUs included medical, cardiac, general surgery, burn/trauma, cardiac surgery (two units), thoracic surgery, and neurosurgery units, and each had a 10-bed capacity. This study was approved by the Institutional Review Board at the Brigham and Women's Hospital. A waiver of informed consent was granted.

We report details regarding the MRSA cohort, but data collection and analyses were performed identically for MRSA and VRE. We obtained census information detailing ICU patients and occupancy dates during the study period. We identified all patients who had an MRSA-negative bilateral nares screening culture and no prior history of MRSA using microbiology laboratory and infection control records dating back to 1987. We then identified patients who had either (1) a subsequent MRSA-negative bilateral nares screening culture (control) or (2) a subsequent MRSA-positive clinical or screening culture (case) within the same hospital stay (Figure 1). Subsequent MRSA screening generally reflected routine ICU protocol for weekly screening of ICU patients on a predetermined weekday. From this cohort, we selected all cases and a random sample of controls, and variables associated with MRSA acquisition were evaluated. All MRSA-negative surveillance cultures were routinely evaluated for the presence of MSSA, thereby enabling the systematic identification of MSSA colonization among cases and controls.

Figure 1
figure 1

Identification of methicillin-resistant Staphylococcus aureus (MRSA) cases and controls following intensive care unit (ICU) admission. All patients were required to have an initial MRSA-negative bilateral nares screening culture. Controls had a subsequent MRSA-negative screening culture (Interval A) whereas cases had a subsequent MRSA-positive screening or clinical culture (Interval B).

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For all MRSA and VRE cases and controls, we collected demographic and comorbidity information based on International Classification of Diseases, Ninth Revision, Clinical Modification codes from same-hospital admissions within one year prior to the initial negative surveillance culture. Measured comorbidities included diabetes, end-stage renal disease, end-stage liver disease, solid cancers, and hematologic malignancies, which were confirmed by medical chart review. Malignancies were recorded only if there was evidence of treatment in the preceding year. We also identified risk factors for MRSA and VRE infection during the two weeks prior to the initial negative surveillance culture through the period encompassing the subsequent negative or positive surveillance or clinical culture. Risk factors included active wounds and rashes, recent surgery, and non-surgical procedures including intubation, bronchoscopy, and the placement of central lines, drains, or tubes. During this time, we additionally collected laboratory indicators of renal insufficiency (creatinine > 2) and poor nutrition (albumin < 2). For the period of time encompassing two months prior to the initial negative surveillance culture until the time of the subsequent negative or positive surveillance or clinical culture, we also recorded antibiotic administration data from the following classes: narrow and broad-spectrum penicillins, first, second and third generation cephalosporins, fluoroquinolones, carbapenems, aminoglycosides, macrolides, and anti-MRSA (vancomycin, linezolid, synercid, daptomycin, tigecycline), other MRSA (doxycycline, bactrim, rifampin), anti-VRE (linezolid, synercid, daptomycin, tigecycline), or other VRE (doxycycline, nitrofurantoin)antibiotics. Time from ICU admission to the initial MRSA-negative culture was also assessed.

Additionally, we assessed colonization pressure, defined as the sum of the daily number of same ward MRSA-positive or VRE-positive patients to which patients were exposed between the initial negative culture and the subsequent positive or negative culture for MRSA or VRE. In addition to evaluating colonization pressure as a total number of daily exposures, we additionally evaluated colonization pressure as a density of exposures divided across the number of days spanned by the initial negative culture and the subsequent positive or negative culture for MRSA or VRE.

Potential predictors of MRSA or VRE acquisition were initially assessed using χ2 bivariate tests. Variables significant in bivariate testing at a level of α < 0.2 were entered into multivariate generalized linear mixed models (GLIMMIX, version 9.1; SAS, SAS Institute, Cary, NC, USA). All bivariate and multivariate analyses accounted for clustering by ICU ward. The primary independent variables of MSSA and VSE carriage were forced into the final model. All other final model variables were retained at α = 0.05.

Results

Across a 20-month period, a total of 8,203 patients had 11,528 ICU room stays. Among them, 809 patients and 658 patients were already MRSA and VRE carriers on ICU admission, leaving 7,629 and 7,806 patients eligible for MRSA and VRE acquisition, respectively. Of these, 244 and 227 patients acquired MRSA and VRE based upon a positive culture in patients with a negative surveillance culture and no prior history of MRSA or VRE, respectively. Cases were compared to a random sample of 250 controls for each pathogen. Medical records for two controls were unavailable, resulting in a total of 248 MRSA-negative controls and 248 VRE-negative controls.

Descriptive characteristics of MRSA and VRE cases and controls are shown in Tables 1 and 2, respectively. Patient characteristics were similar across MRSA and VRE cohorts, with half being over 65 years old, nearly one-third having diabetes and one-quarter with a solid cancer. The vast majority had recent surgeries or non-surgical procedures. Compared to controls, MRSA cases had a significantly longer mean time from ICU admission to initial MRSA-negative swab (mean 4.9 versus 1.4 days, P < 0.001). Similar results were found for VRE (5.5 versus 1.3 days, P < 0.001).

Table 1 Bivariate assessment of characteristics associated with methicillin-resistant Staphylococcus aureus (MRSA) acquisition among cases and controls
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Table 2 Bivariate assessment of characteristics associated with vancomycin-resistant enterococcus (VRE) acquisition among cases and controls
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Table 1 further lists variables associated with MRSA acquisition in bivariate testing. Harboring MSSA was protective, while increased time from ICU admission to initial MRSA-negative swab, intubation, presence of a central line, fluoroquinolone utilization, and anti-MRSA antibiotic utilization were significantly associated with MRSA acquisition. In generalized linear mixed models, only MSSA carriage, intubation, fluoroquinolone utilization, and time from ICU admission to initial MRSA-negative swab remained associated with MRSA acquisition (Table 3).

Table 3 Variables associated with methicillin-resistant Staphylococcus aureus (MRSA) and vancomycin-resistant enterococcus (VRE) acquisition
Full size table

Variables associated with VRE acquisition in bivariate testing are shown in Table 2. Similar to MRSA, increased time from ICU admission to initial VRE-negative swab, intubation, presence of a central line, and fluoroquinolone utilization were significantly associated with VRE acquisition. Several other factors were also associated with VRE acquisition in bivariate testing, including end-stage renal disease, wounds, rashes, low albumin, elevated creatinine, colonization pressure and macrolide, aminoglycoside, third-generation cephalosporin and carbapenem utilization. Many of these variables remained associated with VRE acquisition in multivariate testing using generalized linear mixed models (Table 3). However, in contrast to MRSA, VSE carriage was not associated with VRE acquisition.

Discussion

Among ICU patients from a tertiary care medical center, we show that MSSA carriage results in a 50% reduced odds of MRSA acquisition when extensively accounting for other risk factors. These results support the concept that various S. aureus strains compete for occupancy of the anterior nares [40]. In this case, the protective nature of MSSA likely arises from being the initial occupant of the niche. It is likely that the presence of MRSA would similarly prevent the establishment of MSSA in the anterior nares. Thus, the presence or absence of the mec A gene alone is used as a surrogate means to distinguish S. aureus strains, rather than to suggest a competitive advantage in the absence of beta-lactam antibiotics.

However, regardless of the mechanism for competition between strains, evidence for competition supports the need to be judicious in applying decolonization regimens to eradicate the S. aureus reservoir. In particular, MSSA carriage may be preferable to the chance for re-colonization with an MRSA strain in certain high risk patient populations since it has been suggested in several studies that MRSA infections produce greater morbidity, mortality, and cost compared to MSSA infections in case mix-adjusted patient populations [2, 3, 16–18, 41, 42].

These results are relevant to decolonization strategies that are increasingly used and have been shown to successfully reduce MSSA and MRSA infections among carriers in high-endemic settings, including intensive care units and patients undergoing surgical procedures [43–51]. Currently, cardiac surgeons have a national guideline for pre-operative screening and decolonization of S. aureus to reduce S. aureus surgical site infections [43–45]. Increasingly, chlorhexidine and mupirocin are being routinely applied to MRSA carriers in hospitals to reduce healthcare-associated MRSA infection [46, 49, 52, 53].

The large body of evidence demonstrating substantial benefits of decolonization should be weighed against the potential of increased MRSA acquisition risk due to a vacated anterior nares niche. Studies are needed to evaluate whether decolonization of MSSA carriers increases the risk of acquiring MRSA when discharging patients to high-endemic MRSA healthcare settings. On the other hand, we recognize this risk may be mitigated by decolonization which could reduce the prevalence and transmission of MRSA in post-discharge healthcare settings.

Consistent with prior reports, we found that patients who acquired MRSA and VRE had longer ICU lengths of stay [35, 54, 55]. We controlled for comorbidities and procedures that may have accounted for this and identified mechanical ventilation, fluoroquinolone exposure, and increased ICU duration prior to the initial negative swab as independent predictors of MRSA acquisition [21, 35, 56–58]. We also assessed other previously defined risk factors, but we highlight the protective nature of MSSA when performing a comprehensive evaluation of potential factors associated with MRSA acquisition. Our work indicates that interactions between colonizing S. aureus strains should be considered when evaluating patient-level predictors of MRSA acquisition, particularly in the setting of decolonization therapy.

In contrast to the association between MSSA and MRSA colonization, VSE was not protective against VRE acquisition. This latter finding is consistent with the abundance of microbial flora in the gut reservoir, where antibiotic-susceptible and resistant strains are not mutually exclusive for intestinal colonization. Similar to prior papers, we identified several risk factors associated with VRE acquisition including end-stage renal disease, active wounds, and low serum albumin levels [59, 60].

Our study has important limitations. First, this study was restricted to ICU patients from a tertiary care hospital, and nearly 90% of our study population underwent surgery. Due to differences in patient populations, our findings may not be generalizable to other hospitals or non-ICU settings. Second, our work was often reliant on either nares or rectal screening alone to determine MRSA or VRE acquisition, respectively. If the sensitivity of these single-site screening tests was low, some of our controls may have actually harbored MRSA or VRE, and some of our cases may have actually been long term carriers. Nevertheless, this would have reduced the differences found between the groups. Finally, our results may not be generalizable to MRSA clones that do not predominantly colonize the anterior nares. While this has been suggested for community-associated clones, other research has found no difference in the strain-specific distribution of body site carriage among nursing home residents [61].

Conclusions

We found that MSSA nasal carriage conferred a 50% reduction in the odds of MRSA acquisition among ICU patients. In contrast, no protective effect was observed for VSE. These findings are important for decolonization regimens that may eliminate MSSA and predispose to MRSA acquisition in high-endemic settings, such as ICUs, nursing homes, and rehabilitation centers. Additional studies are needed to better understand the degree to which MSSA is protective and the long-term impact of decolonization relative to subsequent healthcare exposures.

Key messages

  • MSSA carriage significantly protects against MRSA acquisition in ICUs.

  • In contrast, VSE carriage does not protect against VRE acquisition in ICUs.

  • Studies are needed to evaluate whether decolonization of MSSA ICU carriers increases the risk of acquiring MRSA when discharging patients to high-endemic MRSA healthcare settings.

Abbreviations

ICU:

intensive care unit

VSE:

vancomycin-sensitive enterococcus.

References

  1. Klein E, Smith DL, Laxminarayan R: Hospitalizations and deaths caused by MRSA, United States, 1999-2005. Emerg Infect Dis 2007, 13: 1840-1846.

    Article  PubMed Central  PubMed  Google Scholar 

  2. Cosgrove SE, Sakoulas G, Perencevich EN, Schwaber MJ, Karchmer AW, Carmeli Y: Comparison of mortality associated with methicillin-resistant and methicillin-susceptible Staphylococcus aureus bacteremia: a meta-analysis. Clin Infect Dis 2003, 36: 53-59. 10.1086/345476

    Article  PubMed  Google Scholar 

  3. Cosgrove SE, Qi Y, Kaye KS, Harbarth S, Karchmer AW, Carmeli Y: The impact of methicillin resistance in Staphylococcus aureus bacteremia on patient outcomes: mortality, length of stay, and hospital charges. Infect Control Hosp Epidemiol 2005, 26: 166-174. 10.1086/502522

    Article  PubMed  Google Scholar 

  4. National Nosocomial Infections Surveillance System: National Nosocomial Infections Surveillance (NNIS) System Report, data summary from January 1992 through June 2004, issued October 2004. Am J Infect Control 2004, 32: 470-485. 10.1016/j.ajic.2004.10.001

    Article  Google Scholar 

  5. Patel R: Clinical impact of vancomycin-resistant enterococci. J Antimicrob Chemother 2003, 51: iii13-iii21.

    Article  CAS  PubMed  Google Scholar 

  6. Pelz RK, Lipsett PA, Swoboda SM, Diener-West M, Powe NR, Brower RG, Perl TM, Hammond JM, Hendrix CW: Vancomycin-sensitive and vancomycin-resistant enterococcal infections in the ICU: attributable costs and outcomes. Intensive Care Med 2002, 28: 692-697. 10.1007/s00134-002-1276-8

    Article  PubMed  Google Scholar 

  7. Asensio A, Guerrero A, Quereda C, Lizán M, Martinez-Ferrer M: Colonization and infection with methicillin-resistant Staphylococcus aureus : associated factors and eradication. Infect Control Hosp Epidemiol 1996, 17: 20-28. 10.1086/647184

    Article  CAS  PubMed  Google Scholar 

  8. Coello R, Glynn JR, Gaspar C, Pacazo JJ, Fereres J: Risk factors for developing clinical infection with methicillin-resistant Staphylococcus aureus (MRSA) amongst hospital patients initially only colonized with MRSA. J Hosp Infect 1997, 37: 39-46. 10.1016/S0195-6701(97)90071-2

    Article  CAS  PubMed  Google Scholar 

  9. Pujol M, Pena C, Pallares R, Ayats J, Ariza J, Gudiol F: Risk factors for nosocomial bacteremia due to methicillin-resistant Staphylococcus aureus . Eur J Clin Microbiol Infect Dis 1994, 13: 96-102. 10.1007/BF02026134

    Article  CAS  PubMed  Google Scholar 

  10. Muto CA, Jernigan JA, Ostrowsky BE, Richet HM, Jarvis WR, Boyce JM, Farr BM, SHEA: SHEA guideline for preventing nosocomial transmission of multidrug-resistant strains of Staphylococcus aureus and enterococcus . Infect Control Hosp Epidemiol 2003, 24: 362-386. 10.1086/502213

    Article  PubMed  Google Scholar 

  11. Matar MJ, Tarrand J, Raad I, Rolston KVI: Colonization and infection with vancomycin-resistant Enterococcus among patients with cancer. Am J Infect Control 2006, 34: 534-536. 10.1016/j.ajic.2006.04.205

    Article  PubMed  Google Scholar 

  12. McNeil SA, Malani PN, Chenoweth CE, Fontana RJ, Magee JC, Punch JD, Mackin ML, Kauffman CA: Vancomycin-resistant enterococcal colonization and infection in liver transplant candidates and recipients: a prospective surveillance study. Clin Infect Dis 2006, 42: 195-203. 10.1086/498903

    Article  PubMed  Google Scholar 

  13. Huang SS, Platt R: Risk of methicillin-resistant Staphylococcus aureus infection after previous infection or colonization. Clin Infect Dis 2003, 36: 281-285. 10.1086/345955

    Article  PubMed  Google Scholar 

  14. Datta R, Huang SS: Risk of postdischarge infection with vancomycin-resistant enterococcus after initial infection or colonization. Infect Control Hosp Epidemiol 2010, 31: 1290-1293. 10.1086/657332

    Article  PubMed Central  PubMed  Google Scholar 

  15. Datta R, Huang SS: Risk of infection and death due to methicillin-resistant Staphylococcus aureus in long-term carriers. Clin Infect Dis 2008, 47: 176-181. 10.1086/589241

    Article  PubMed Central  PubMed  Google Scholar 

  16. Safdar N, Bradley EA: The risk of infection after nasal colonization with Staphylococcus aureus . Am J Med 2008, 121: 310-315. 10.1016/j.amjmed.2007.07.034

    Article  PubMed  Google Scholar 

  17. Honda H, Krauss MJ, Coopersmith CM, Kollef MH, Richmond AM, Fraser VJ, Warren DK: Staphylococcus aureus nasal colonization and subsequent infection in intensive care unit patients: does methicillin-resistance matter? Infect Control Hosp Epidemiol 2010, 31: 584-591. 10.1086/652530

    Article  PubMed Central  PubMed  Google Scholar 

  18. Blot SI, Vandewoude KH, Hoste EA, Colardyn FA: Outcome and attributable mortality in critically ill patients with bacteremia involving methicillin-susceptible and methicillin-resistant Staphylococcus aureus . Arch Intern Med 2002, 162: 2229-2235. 10.1001/archinte.162.19.2229

    Article  PubMed  Google Scholar 

  19. Wolkewitz M, Frank U, Philips G, Schumacher M, Davey P: Mortality associated with in-hospital bacteraemia caused by Staphylococcus aureus : a multistate analysis with follow-up beyond hospital discharge. J Antimicrob Chemother 2011, 66: 381-386. 10.1093/jac/dkq424

    Article  CAS  PubMed  Google Scholar 

  20. Gorwitz RJ, Kruszon-Moran D, McAllister SK, McQuillan G, McDougal LK, Fosheim GE, Jensen BJ, Killgore G, Tenover FC, Kuehnert MJ: Changes in the prevalence of nasal colonization with Staphylococcus aureus in the United States, 2001-2004. J Infect Dis 2008, 197: 1226-1234. 10.1086/533494

    Article  PubMed  Google Scholar 

  21. Salangsang JA, Harrison LH, Brooks MM, Shutt KA, Saul MI, Muto CA: Patient-associated risk factors for acquisition of methicillin-resistant Staphylococcus aureus in a tertiary care hospital. Infect Control Hosp Epidemiol 2010, 31: 1139-1147. 10.1086/656595

    Article  PubMed  Google Scholar 

  22. Warren DK, Guth RM, Coopersmith CG, Merz LR, Zack JE, Fraser VJ: Epidemiology of methicillin-resistant Staphylococcus aureus colonization in a surgical intensive care unit. Infect Control Hosp Epidemiol 2006, 27: 1032-1040. 10.1086/507919

    Article  PubMed  Google Scholar 

  23. Marshall C, Harrington G, Wolfe R, Fairley CK, Wesselingh S, Spelman D: Acquisition of methicillin-resistant Staphylococcus aureus in a large intensive care unit. Infect Control Hosp Epidemiol 2003, 24: 322-326. 10.1086/502215

    Article  PubMed  Google Scholar 

  24. Huang SS, Rifas-Shiman SL, Warren DK, Fraser VJ, Climo MW, Wong ES, Cosgrove SE, Perl TM, Pottinger JM, Herwaldt LA, Jernigan JA, Tokars JL, Diekema DJ, Hinrichsen VL, Yokoe DS, Platt R, Centers for Disease Control and Prevention Epicenters Program: Improving methicillin-resistant Staphylococcus aureus surveillance and reporting in intensive care units. J Infect Dis 2007, 195: 330-338. 10.1086/510622

    Article  PubMed  Google Scholar 

  25. Aizen E, Ljubuncic Z, Ljubuncic P, Aizen I, Potasman I: Risk factors for methicillin-resistant Staphylococcus aureus colonization in a geriatric rehabilitation hospital. J Gerontol A Biol Sci Med Sci 2007, 62: 1152-1156.

    Article  PubMed  Google Scholar 

  26. Robiczek A, Beaumont JL, Thomson RB Jr, Govindarajan G, Peterson LG: Topical therapy for methicillin-resistant Staphylococcus aureus colonization: impact on infection risk. Infect Control Hosp Epidemiol 2009, 30: 623-632. 10.1086/597550

    Article  Google Scholar 

  27. Hayden M: Insights into the epidemiology and control of infection with vancomycin-resistant enterococci. Clin Infect Dis 2000, 31: 1058-1065. 10.1086/318126

    Article  CAS  PubMed  Google Scholar 

  28. Bhorade SM, Christenson J, Pohlman AS, Arnow PM, Hall JB: The incidence of and clinical variables associated with vancomycin-resistant enterococcal colonization in mechanically ventilated patients. Chest 1999, 115: 1085-1091. 10.1378/chest.115.4.1085

    Article  CAS  PubMed  Google Scholar 

  29. Beltrami EM, Singer DA, Fish L, Manning K, Young S, Banerjee SN, Baker R, Jarvis WR: Risk factors for acquisition of vancomycin-resistant enterococci among patients on a renal ward during a community hospital outbreak. Am J Infect Control 2000, 28: 282-285. 10.1067/mic.2000.106276

    Article  CAS  PubMed  Google Scholar 

  30. Ostrowsky BE, Venkataraman L, D'Agata EM, Gold HS, DeGirolami PC, Samore MH: Vancomycin-resistant enterococci in intensive care units. Arch Intern Med 1999, 159: 1467-1472. 10.1001/archinte.159.13.1467

    Article  CAS  PubMed  Google Scholar 

  31. Suntharam N, Lankford MG, Trick WE, Peterson LR, Noskin GA: Risk factors for acquisition of vancomycin-resistant enterococci among hematology-oncology patients. Diagn Microbiol Infect Dis 2002, 43: 183-188. 10.1016/S0732-8893(02)00392-9

    Article  PubMed  Google Scholar 

  32. Carmeli Y, Eliopoulos GM, Samore MH: Antecedent treatment with different antibiotic agents as a risk factor for vancomycin-resistant Enterococcus. Emerg Infect Dis 2002, 8: 802-807.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  33. Hardy KJ, Oppenheim BA, Gossain S, Gao F, Hawkey PM: A study of the relationship between environmental contamination with methicillin-resistant Staphylococcus aureus (MRSA) and patients' acquisition of MRSA. Infect Control Hosp Epidemiol 2006, 27: 127-132. 10.1086/500622

    Article  PubMed  Google Scholar 

  34. Drees M, Snydman DR, Schmid CH, Barefoot L, Hansjosten K, Vue PM, Cronin M, Nasraway SA, Golan Y: Prior environmental contamination increases the risk of acquisition of vancomycin-resistant enterococci. Clin Infect Dis 2008, 46: 678-685. 10.1086/527394

    Article  CAS  PubMed  Google Scholar 

  35. Huang SS, Datta R, Platt R: Risk of acquiring antibiotic-resistant bacteria from prior room occupants. Arch Intern Med 2006, 166: 1945-1951. 10.1001/archinte.166.18.1945

    Article  PubMed  Google Scholar 

  36. Boyce JM, Potter-Bynoe G, Chenevert C, King T: Environmental contamination due to methicillin-resistant Staphylococcus aureus : possible infection control implications. Infect Control Hosp Epidemiol 1997, 18: 622-627. 10.1086/647686

    Article  CAS  PubMed  Google Scholar 

  37. Bhalla A, Pultz NJ, Gries DM, Ray AJ, Eckstein EC, Aron DC, Donskey CJ: Acquisition of nosocomial pathogens on hands after contact with environmental surfaces near hospitalized patients. Infect Control Hosp Epidemiol 2004, 25: 164-167. 10.1086/502369

    Article  PubMed  Google Scholar 

  38. Hayden MK, Blom DW, Lyle EA, Moore CG, Weinstein RA: Risk of hand or glove contamination after contact with patients colonized with vancomycin-resistant enterococcus or the colonized patients' environment. Infect Control Hosp Epidemiol 2008, 29: 149-154. 10.1086/524331

    Article  PubMed  Google Scholar 

  39. Martinez JA, Ruthazer R, Hansjosten K, Barefoot L, Snydman DR: Role of environemental contamination as a risk factor for acquisition of vancomycin-resistant enterococci in patients treated in a medical intensive care unit. Arch Intern Med 2003, 163: 1905-1912. 10.1001/archinte.163.16.1905

    Article  PubMed  Google Scholar 

  40. Dall'Antonia M, Coen PG, Wilks M, Whiley A, Millar M: Competition between methicillin-sensitive and -resistant Staphylococcus aureus in the anterior nares. J Hosp Infect 2005, 61: 62-67. 10.1016/j.jhin.2005.01.008

    Article  PubMed  Google Scholar 

  41. Lauplan KB, Ross T, Gregson DB: Staphylococcus aureus bloodstream infections: risk factors, outcomes, and the influence of methicillin resistance in Calgary, Canada, 2000-2006. J Infect Dis 2008, 198: 336-343. 10.1086/589717

    Article  Google Scholar 

  42. Kang CI, Song JH, Chung DR, Peck KR, Ko KS, Yeom JS, Kim SW, Chang HH, Kim YS, Jung SI, Son JS, Hsueh PR, So TM, Lalitha MK, Yang Y, Huang SG, Wang H, Lu Q, Carlos CC, Perera JA, Chiu CH, Liu JW, Chongthaleong A, Thamlikitkul V, Van Pham H, Asian Network for Surveillance of Resistant Pathogens (ANSORP) Study Group: Clinical impact of methicillin resistance on outcome of patients with Staphylococcus aureus infection: a stratified analysis according to underlying diseases and sites of infection in a large prospective cohort. J Infect 2010, 61: 299-366. 10.1016/j.jinf.2010.07.011

    Article  PubMed  Google Scholar 

  43. Perl TM, Cullen JJ, Wenzel RP, Zimmerman MB, Pfaller MA, Sheppard D, Twombley J, French PP, Herwaldt LA: Intranasal mupirocin to prevent postoperative Staphylococcus aureus infections. N Engl J Med 2002, 346: 1871-1877. 10.1056/NEJMoa003069

    Article  CAS  PubMed  Google Scholar 

  44. Engleman R, Shahian D, Shemin R, Guy TS, Bratzler D, Edwards F, Jacobs M, Fernando H, Bridges C: The Society of Thoracic Surgeons practice guidelines series: antibiotic prophylaxis in cardiac surgery, Part II: antibiotic choice. Ann Thorac Surg 2007, 83: 1569-1576. 10.1016/j.athoracsur.2006.09.046

    Article  Google Scholar 

  45. Kallen AJ, Wilson CT, Larson RJ: Perioperative intranasal mupirocin for the prevention of surgical-site infections: systematic review of the literature and meta-analysis. Infect Control Hosp Epidemiol 2005, 26: 916-922. 10.1086/505453

    Article  PubMed  Google Scholar 

  46. Ridenour G, Lampen R, Fiderspiel J, Kritchevsky S, Wong E, Climo M: Use of intranasal mupirocin and chlorhexidine bathing and the incidence of methicillin-resistant Staphylococcus aureus colonization and infection among intensive care units patients. Infect Control Hosp Epidemiol 2007, 28: 1155-1161. 10.1086/520102

    Article  PubMed  Google Scholar 

  47. Simor AE, Phillips E, McGeer A: Randomized controlled trial of chlorhexidine gluconate for washing, intranasal mupirocin, and rifampin and doxycycline versus no treatment for the eradication of methicillin-resistant Staphylococcus aureus colonization. Clin Infect Dis 2007, 44: 178-185. 10.1086/510392

    Article  CAS  PubMed  Google Scholar 

  48. Climo MW, Sepkowitz KA, Zuccotti G, Fraser VJ, Warren DK, Perl TM, Speck K, Jernigan JA, Robles JR, Wong ES: The effect of daily bathing with chlorhexidine on the acquisition of methicillin-resistant Staphylococcus aureus , vancomycin-resistant enterococcus, and healthcare-associated bloodstream infections: results of a quasi-experimental multicenter trial. Crit Care Med 2009, 37: 1858-1865. 10.1097/CCM.0b013e31819ffe6d

    Article  CAS  PubMed  Google Scholar 

  49. Robicsek A, Beaumont JL, Thomson RB, Govindarajan G, Peterson LR: Topical therapy for methicillin-resistant Staphylococcus aureus colonization: impact on infection risk. Infect Control Hosp Epidemiol 2009, 30: 623-632. 10.1086/597550

    Article  PubMed  Google Scholar 

  50. Bode LG, Kluytmans JA, Wertheim HF, Bogaers D, Vandenbroucke-Grauls CM, Roosendaal R, Troelstra A, Box AT, Voss A, van der Tweel I, van Belkum A, Verbrugh HA, Vos MC: Preventing surgical-site infections in nasal carriers of Staphylococcus aureus . N Engl J Med 2010, 362: 9-17. 10.1056/NEJMoa0808939

    Article  CAS  PubMed  Google Scholar 

  51. van Rijen M, Bonten M, Wenzel R, Kluytmans J: Mupirocin ointment for preventing Staphylococcus aureus infections in nasal carriers. Cochrane Database Syst Rev 2008, 4: CD006216.

    PubMed  Google Scholar 

  52. Edgeworth JD: Has decolonization played a central role in the decline in UK methicillin resistant Staphylococcus aureus transmission? A focus on evidence from intensive care. J Antimicrob Chemother 2011, 66: ii41-47. 10.1093/jac/dkq325

    Article  CAS  PubMed  Google Scholar 

  53. Fraser TG, Fatica C, Scarpelli M, Arroliga AC, Guzman J, Shrestha NK, Hixson E, Rosenblatt M, Gordon SM, Procop GW: Decrease in Staphylococcus aureus colonization and hospital-acquired infection in a medical intensive care unit after institution of an active surveillance and decolonization program. Infect Control Hosp Epidemiol 2010, 31: 779-783. 10.1086/654001

    PubMed  Google Scholar 

  54. Reed SD, Friedman JY, Engemann JJ, Griffiths RI, Anstrom KJ, Kaye KS, Stryjewski ME, Szczech LA, Reller LB, Corey GR, Schulman KA, Fowler VG Jr: Costs and outcomes among hemodialysis patients with methicillin-resistant or methicillin-susceptible Staphylococcus aureus bacteremia. Infect Control Hosp Epidemiol 2005, 26: 175-183. 10.1086/502523

    Article  PubMed  Google Scholar 

  55. Song X, Srinivasan A, Plaut D, Perl TM: Effect of nosocomial vancomycin-resistant enterococcal bacteremia on mortality, length of stay and costs. Infect Control Hosp Epidemiol 2003, 24: 251-256. 10.1086/502196

    Article  PubMed  Google Scholar 

  56. Nseir S, Di Pompeo C, Soubrier S, Delour P, Lench H, Roussel-Delvallez M, Onimus T, Saulnier F, Mathieu D, Durocher A: First-generation fluoroquinolone use and subsequent emergence of multiple drug-resistant bacteria in the intensive care unit. Crit Care Med 2005, 33: 283-289. 10.1097/01.CCM.0000152230.53473.A1

    Article  CAS  PubMed  Google Scholar 

  57. Weber SG, Gold HS, Hooper DC, Karchmer AW, Carmeli Y: Fluoroquinolones and the risk for methicillin-resistant Staphylococcus aureus in hospitalized patients. Emerg Infect Dis 2003, 9: 1415-1422.

    Article  PubMed Central  PubMed  Google Scholar 

  58. Tacconelli E, De Angelis G, Cataldo MA, Pozzi E, Cauda R: Does antibiotic exposure increase the risk of methicillin-resistant Staphylococcus aureus (MRSA) isolation? A systematic review and meta-analysis. J Antimicrob Chemother 2008, 61: 26-38.

    Article  CAS  PubMed  Google Scholar 

  59. DeLisle S, Perl TM: Vancomycin-resistant enterococci: a road map on how to prevent the emergence and transmission of antimicrobial resistance. Chest 2003, 123: 504S-518S. 10.1378/chest.123.5_suppl.504S

    Article  CAS  PubMed  Google Scholar 

  60. Zhou Q, Moore C, Eden S, Tong A, McGeer A: Factors associated with acquisition of vancomycin-resistant enterococci (VRE) in roommate contacts of patients colonized or infected with VRE in a tertiary care hospital. Infect Control Hosp Epidemiol 2008, 29: 398-403. 10.1086/587187

    Article  PubMed  Google Scholar 

  61. Shurland SM, Stine OC, Venezia RA, Johnson JK, Zhan M, Furuno JP, Miller RR, Johnson T, Roghmann MC: Colonization sites of USA300 methicillin-resistant Staphylococcus aureus in residents of extended care facilities. Infect Control Hosp Epidemiol 2009, 30: 313-318. 10.1086/596114

    Article  PubMed Central  PubMed  Google Scholar 

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Acknowledgements

This study was funded by the CDC Prevention Epicenters Program (1U01CI000344, Platt) and the National Institutes of Health (K23AI64161-01, Huang).

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Authors and Affiliations

  1. Division of Infectious Diseases and Health Policy Research Institute, University of California Irvine School of Medicine, 100 Theory, Ste 110, Irvine, CA, 92697, USA

    Susan S Huang & Rupak Datta

  2. Channing Laboratory, Brigham and Women's Hospital and Harvard Medical School, 181 Longwood Avenue, Boston, MA, 02115, USA

    Susan S Huang & Richard Platt

  3. Department of Population Medicine, Harvard Pilgrim Health Care Institute and Harvard Medical School, 133 Brookline Avenue, Boston, MA, 02215, USA

    Rupak Datta, Sheryl Rifas-Shiman, Ken Kleinman, Hilary Placzek, Julie D Lankiewicz & Richard Platt

  4. Department of Clinical and Population Health Research, University of Massachusetts Medical School, 55 Lake Avenue North, Worcester, MA, 01655, USA

    Hilary Placzek

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  1. Susan S Huang
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  2. Rupak Datta
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  3. Sheryl Rifas-Shiman
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Correspondence to Susan S Huang.

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The authors declare that they have no competing interests.

Authors' contributions

JL participated in the study design and coordination. HP performed data collection and contributed to the study design. SRS and KK participated in the study conception and design and performed the statistical analysis. RD contributed to the data interpretation and manuscript preparation. SH and RP conceived of the study, contributed to its design and analysis, and critically revised the manuscript for intellectual content. All authors read and approved the final manuscript.

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Huang, S.S., Datta, R., Rifas-Shiman, S. et al. Colonization with antibiotic-susceptible strains protects against methicillin-resistant Staphylococcus aureus but not vancomycin-resistant enterococci acquisition: a nested case-control study. Crit Care 15, R210 (2011). https://doi.org/10.1186/cc10445

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  • DOI: https://doi.org/10.1186/cc10445

Keywords

Critical Care

ISSN: 1364-8535