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Table 1. 
Characteristics of MRSA Carriers*
Characteristics of MRSA Carriers*
Table 2. 
Characteristics of Patients Who Acquired MRSA*
Characteristics of Patients Who Acquired MRSA*
Table 3. 
Comparison of Patients With MRSA Infection and Colonization*
Comparison of Patients With MRSA Infection and Colonization*
1.
Moreno  FCrisp  CJorgensen  JHPatterson  JE Methicillin-resistant Staphylococcus aureus as a community organism. Clin Infect Dis. 1995;211308- 1312Article
2.
Panlilio  ACulver  DHGaynes  RP  et al.  Methicillin-resistant Staphylococcus aureus in U.S. hospitals, 1975-1991. Infect Control Hosp Epidemiol. 1992;13582- 586Article
3.
Collège de Bactériologie-Virologie-Hygiéne du Centre Hospitalier Universitaire de Paris, Surveillance des staphylocoques dorés et klebsielles multi-résistants à l'Assistance Publique-hôpitaux de Paris (1993-96). Bull Epidemiol Hebdo. 1998;1041- 43
4.
Richet  HWiesel  MLe Gallou  FAndré-Richet  BEspaze  E Methicillin-resistant Staphylococcus aureus control in hospitals: the French experience. Infect Control Hosp Epidemiol. 1996;17509- 511Article
5.
Lowy  FD Staphylococcus aureus infections. N Engl J Med. 1998;339520- 532Article
6.
Wakefield  DSHelms  CMMassanari  RMMori  MPfaller  M Cost of nosocomial infection: relative contributions of laboratory, antibiotic, and per diem costs in serious Staphylococcus aureus infections. Am J Infect Control. 1988;16185- 192Article
7.
Mulligan  MEMurray-Leisure  KARibner  BS  et al.  Methicillin-resistant Staphylococcus aureus: a consensus review of the microbiology, pathogenesis, and epidemiology with implications for prevention and management. Am J Med. 1993;94313- 328Article
8.
Jarlier  V Surveillance en France: klebsielles et staphylocoques multirésistants: stratégie de prévention à l'AP-HP. Bull Epidemiol Hebdo. 1993;42192- 193
9.
Ayliffe  GAJ Recommendations for the Control of Methicillin-Resistant Staphylococcus aureus (MRSA).  Geneva, Switzerland World Health Organization1996;1- 28
10.
Bradley  SFTerpenning  MSRamsey  MA  et al.  Methicillin-resistant Staphylococcus aureus: colonization and infection in a long-term care facility. Ann Intern Med. 1991;115417- 422Article
11.
Coello  RGlynn  JRGaspar  CPicazo  JJFereres  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;3739- 46Article
12.
Bradley  SF Methicillin-resistant Staphylococcus aureus in nursing homes: epidemiology, prevention and management. Drugs Aging. 1997;10185- 198Article
13.
Garner  JSJarvis  WREmori  TGHoran  TCHughes  JM CDC definitions for nosocomial infections, 1988. Am J Infect Control. 1988;16128- 140Article
14.
Acar  JBergogne-Bérézin  EChabbert  Y  et al.  Communiqué 1992 du Comité de l'Antibiogramme de la Société Française de Microbiologie. Pathol Biol (Paris). 1992;40741- 748
15.
Casewell  MW Epidemiology and control of the "modern" methicillin-resistant Staphylococcus aureusJ Hosp Infect. 1986;7(suppl A)1- 11Article
16.
Girou  EWolkenstein  POppein  F  et al.  Suivi d'une politique de lutte contre les staphylocoques dorés méticilline-résistants dans une unité de soins intensifs de dermatologie. Ann Dermatol Venereol. 1996;123(suppl 1)S16- S17
17.
Rodier  Lde Wit  D MRSA colonization rates of readmitted patients previously colonized or infected with MRSA. J Hosp Infect. 1997;35161- 163Article
18.
Girou  EPujade  GLegrand  PCizeau  FBrun-Buisson  C Selective screening for control of methicillin-resistant Staphylococcus aureus (MRSA) in high-risk hospital areas with a high level of endemic MRSA. Clin Infect Dis. 1998;27543- 550Article
19.
Maguire  GPArthur  ADBoustead  PJDwyer  BCurrie  BJ Clinical experience and outcomes of community-acquired and nosocomial MRSA in a northern Australian hospital. J Hosp Infect. 1998;38273- 281Article
20.
Hansson  C Microbial flora in venous leg ulcers and choice of treatment. Treatment of Ulcers. Oslo, Norway Sandberg AS1995;139- 148
21.
Nathan  DM Long-term complications of diabetes mellitus. N Engl J Med. 1993;3281676- 1684Article
22.
Bonten  MJMWeinstein  RA The role of colonization in the pathogenesis of nosocomial infections. Infect Control Hosp Epidemiol. 1996;17193- 200Article
23.
Boyce  JM Methicillin-resistant Staphylococcus aureus in hospitals and long-term care facilities: microbiology, epidemiology, and preventive measures. Infect Control Hosp Epidemiol. 1992;13725- 737Article
Study
June 2000

Methicillin-Resistant Staphylococcus aureus Nosocomial Acquisition and Carrier State in a Wound Care Center

Author Affiliations

From the Unité d'Hygiène (Dr Kac and Ms Hérisson), Laboratoire de Microbiologie (Dr Buu-Hoï), and Service de Rééducation Vasculaire (Ms Biancardini and Dr Debure), Hôpital Broussais, Paris, France.

Arch Dermatol. 2000;136(6):735-739. doi:10.1001/archderm.136.6.735
Abstract

Objective  To assess methicillin-resistant Staphylococcus aureus (MRSA) nosocomial acquisition and carrier state in a wound care center.

Design and Setting  The results of an intervention to control MRSA were compared with those of historical controls at the wound care center of university-based Hôpital Broussais, Paris, France.

Patients  Patients admitted for specific care of chronic ulcers and surgical wounds.

Main Outcome Measures  Incidence rates of MRSA carriers and acquisition in wounds.

Results  Of 88 patients admitted during a 3-month preintervention period in 1993, 18 (21%) were MRSA carriers. Of 334 patients admitted in 1994 and 395 in 1996, 65 (19.5%) and 81 (20.5%) were MRSA carriers, respectively (P=.80). In 1993, 6 (9%) of 70 patients without MRSA acquired MRSA wound infections; the corresponding numbers were 6 (2.2%) of 269 in 1994 and 3 (0.9%) of 314 in 1996. Despite that the number of MRSA carriers remained stable at admission to the wound care center, the rate of MRSA infections in wounds per 100 noncarriers decreased significantly between the preintervention period and subsequent years: 1994 (P=.02) and 1996 (P=.002).

Conclusions  Although our results are limited by the use of historical controls, they showed that simple infection control measures, such as the use of soap and water and barrier precautions associated with staff education, seemed to significantly reduce MRSA infection rates in patients with chronic skin breaks.

METHICILLIN-resistant Staphylococcus aureus (MRSA) is increasingly common in hospitals worldwide and has recently spread to community populations.1,2 In 1993-1996 in French hospitals, the proportion of S aureus resistant to methicillin was 40%,3 and the infection rate was 0.45% in a recent multicenter survey.4 The high endemicity of MRSA poses a problem for drug therapy because of the possible development of resistance to glycopeptides, which could lead to untreatable infections.5 In addition, MRSA is a financial burden on the health care system.6 As this organism can spread easily from person to person, MRSA is introduced into hospitals by the admission of a patient with infection or colonization who serves as a reservoir.7 The control of MRSA requires the implementation of infection control measures, particularly inside high-risk wards, including rapid detection of MRSA by screening every patient at risk at admission, identifying MRSA carriers using specific labeling, rigorous hand washing by staff, isolation of patients with colonization and infection, and MRSA eradication, if possible, by the use of antiseptic agents.8,9

Open wounds, particularly when they are chronic, provide a portal of entry for MRSA to the underlying tissues, which can readily lead to local or generalized infection. In addition, the presence of wounds in geriatric patients is a risk factor for MRSA colonization at any other site.10 Recently, pressure ulcers and surgical wounds were found to be independently associated with an increased rate of subsequent MRSA infection in general hospital populations.11 The epidemiology of MRSA colonization and infection in wounds has been studied in the elderly,12 but no data are available for large cohorts of patients with miscellaneous wounds. The aim of this study was to assess the MRSA nosocomial acquisition and carrier state in a large cohort of patients admitted to a ward for treatment of chronic ulcers and postoperative wounds. The effect of an intervention to control MRSA was assessed by comparing the results before (historical controls) and after the intervention.

PATIENTS AND METHODS
SETTING AND PATIENTS

The wound care center (WCC) of university-based Hôpital Broussais, Paris, France, is a vascular rehabilitation ward with 51 beds and 350 to 400 admissions per year. It is dedicated to the care of chronic ulcers (venous ulcers, arterial ulcers, and neurotrophic ulcers) and wounds due to vascular surgery (distal amputation and bypass graft). The study population was composed of all patients admitted in 1994 and 1996, with a mean length of stay of 35 days.

STUDY DESIGN

We conducted a 3-month incidence survey from September 1, 1993, to November 30, 1993, consisting of systematic recording of wound infections acquired in the ward. The cohort included 88 patients, of whom 14 patients (16%) acquired wound infections due to various microorganisms. Of these 88 patients, 70 did not have MRSA at admission. Of these 70 patients, 6 (9%) acquired MRSA wound infections during their stay.

From January 1, 1994, to December 31, 1994, a program to control MRSA was implemented, including specific control measures and a continuous 12-month survey to assess the incidence of both MRSA carrier state in wounds and nosocomial acquisition. A second 12-month survey was conducted from January 1, 1996, to December 31, 1996, using the same methods to assess the medium-term efficacy of the control program.

DEFINITIONS

Methicillin-resistant S aureus carrier was defined as a patient with MRSA in wound cultures obtained less than 48 hours after admission. Methicillin-resistant S aureusacquisition was defined as the isolation of MRSA in samples taken 48 hours after admission from former noncarriers. According to the Centers for Disease Control criteria,13 wound infection was defined as the presence of 2 of the following clinical signs (localized pain or tenderness, swelling, and redness or heat) and isolation of MRSA in pure culture. If both clinical and microbiological criteria were not met, the presence of MRSA in wound cultures was considered colonization.

SURVEILLANCE METHODS

A standard form was used to collect data for the inpatients. The information gathered included date of admission, age, admission category, underlying diseases (eg, diabetes mellitus), type of wound, site of acquisition, and clinical and microbiological features of infection. Each month, all cases involving MRSA (carrier at admission or acquisition) were evaluated by the WCC staff and the infection control team. The classification of patients (MRSA carriers or patients with MRSA acquisition) depended on the date that cultures positive for MRSA were obtained (at admission or 48 hours after admission). The time to acquisition was noted. All nosocomial wound infections (including bacteria other than MRSA) were also recorded during the study period. All results were reported monthly by the infection control team to the WCC staff.

SPECIFIC CONTROL MEASURES

Before the intervention, the systematic management of wounds consisted of regular attention to changes in the appearance of wounds and regular care with Vaseline gauze dressings. Since January 1, 1994, infection control measures have been implemented in the ward.

For management of all wounds, we implemented the following measures: (1) the revision of nursing procedures, including proper and rigorous hand washing using soap and water, (2) the use of gloves and gowns by personnel who have direct contact with wounds, (3) the systematic use of disposable devices, and (4) the washing of the extremities with soap and water during dressing changes.

In addition, for specific management of wounds with MRSA, the following measures were implemented: (1) the staff of the microbiology laboratory labeled patients' laboratory results and charts when a culture was positive for MRSA, (2) the staff were educated about the risk of cross-transmission, (3) regular feedback was given to the staff about new cases of MRSA, and (4) when changing dressings, patients with MRSA were treated after patients without MRSA.

Strict patient isolation was not possible because there are only 11 single rooms in the ward.

MICROBIOLOGICAL METHODS

Samples were obtained using cotton-tipped swabs from all skin wounds at admission and all wounds during the stay, if clinical worsening occurred. The samples were delivered to the microbiology laboratory, placed on blood agar plates, and incubated at 37°C for 72 hours. Using standard laboratory procedures, MRSA was isolated and identified. The detection of methicillin resistance was performed according to the methods recommended by the Comité de l'Antibiogramme de la Société Française de Microbiologie.14

CASE-CONTROL STUDY

A case-control study was conducted to identify specific risk factors for MRSA wound infections. Cases were patients infected with MRSA and controls, patients with MRSA colonization during the same period.

ANALYSIS OF DATA

The carrier incidence rates were calculated by dividing the number of MRSA carriers by the number of admissions to the ward; it was expressed per 100 admissions.

The acquisition incidence rates were expressed in 2 different ways. The rate was first calculated by dividing the number of patients who acquired MRSA at the hospital by the number of patients without MRSA at admission and expressed per 100 noncarriers It was also calculated by dividing the number of patients who acquired MRSA at the hospital by the total length of stay of all patients admitted to the ward during the period; it was expressed per 1000 resident-care days.

Incidence data were compared using the χ2 test or Fisher exact test. In the risk factor analysis, qualitative data were compared using Fisher exact test, and quantitative data using the t test. All tests were 2-tailed; P≤.05 was considered significant.

RESULTS
CARRIERS

Of 334 admitted patients in 1994, 65 (19.5%) were MRSA carriers; of 395 admitted patients in 1996, 81 (20.5%) were MRSA carriers (P=.80). The characteristics of MRSA carriers in 1994 and 1996 were similar with respect to age, prevalence of diabetes mellitus, admission category, and type of skin breaks (Table 1). The characteristics were also comparable to those of all patients admitted to the ward during the same period (data not shown).

ACQUISITION

Of 269 patients without MRSA in 1994, 12 patients (4.5%) acquired MRSA, including 6 with colonization (2.2%) and 6 with infection (2.2%); the colonization and infection rates were 0.39 per 1000 resident-care days. Of 314 patients without MRSA in 1996, 11 patients (3.5%) acquired MRSA, including 8 with colonization (2.5%) and 3 with infection (0.9%); the colonization and infection rates were 0.61 and 0.23 per 1000 resident-care days, respectively. The ages, prevalence of diabetes mellitus, and type of skin breaks in patients who acquired MRSA were similar in 1994 and 1996 (Table 2).

There was a significant decrease in the rate of MRSA wound infections per 100 noncarriers between the preintervention period in 1993 (6 [9%] of 70) and the postintervention period in 1994 (6 [2.2%] of 269; P=.02) and 1996 (3 [0.9%] of 314; P=.002).

RISK FACTORS FOR INFECTION VS COLONIZATION

The 9 patients with infection were compared with the 14 patients with colonization (Table 3), and the patients with infection were similar to those with colonization. There was no statistically significant difference between the 2 groups in terms of age, prevalence of diabetes mellitus, nature, number and duration of wounds, wound grafts, frequency of antibiotic therapy before hospitalization, presence of simultaneous infectious sites, presence of invasive devices, and prior hospital admissions. Many of the members of both the group with infection and the group with colonization had previously received antibiotics (78% vs 86%) and had been hospitalized before their present admission (100% vs 79%).

NOSOCOMIAL WOUND INFECTIONS

A total of 34 wound infections (23 in 1994 and 11 in 1996) were acquired by the patients in the WCC, with the isolation of 37 microorganisms. Staphylococcus aureus was the main causative bacterium, with the isolation of 21 microorganisms (57%), and MRSA was responsible for 9 episodes (27% of all nosocomial wound infections). The other organisms were Streptococcus agalactiae (n=7), Pseudomonas aeruginosa (n=5), Streptococcus pyogenes (n=2), Proteus mirabilis (n=1), and Corynebacterium species (n=1). Pseudomonas aeruginosa and methicillin-sensitive S aureus were responsible for 2 mixed infections.

COMMENT

By comparing the 2 survey periods, our study revealed that the rate of MRSA carriers (20%) at admission remained stable. This percentage confirms that patients admitted to the WCC were at particularly high risk for MRSA acquisition, probably because they had a combination of several known risk factors, such as old age, previous and prolonged hospital stays, previous antibiotic treatment, and diabetes mellitus (some patients), and had undergone invasive procedures.15 Girou et al16 studied samples from the nose and/or wounds and/or perineum in a subgroup of patients with generalized dermatoses in a dermatological intensive care unit in Paris. They reported a similar rate of MRSA carriers at admission (18%). Our results are consistent with data obtained from 9 studies in nursing homes from 1982 to 1996 cited by Bradley,12 who reported rates of MRSA carriers at admission of 10% to 54%. Because the MRSA carrier state often lasts several months, patients with MRSA frequently have colonization at readmission.17 In our ward, 40% to 50% of the patients are readmitted for care of chronic wounds and are often transferred during their hospital stay between various wards. Because of cost and personnel considerations, selective screening of MRSA carriers in French university hospitals is required. However, the way of selecting the population to be screened has not been determined.18 Our data suggest that patients with chronic ulcers and postoperative wounds should be identified, screened, and isolated in all wards. Other subpopulations need to be defined as well. Such targeted strategies could prevent the spread of MRSA within hospitals and also possibly in the community where MRSA emerged recently.19

We found a 3.5% to 4.5% acquisition rate in patients with chronic skin breaks. These results are consistent with Girou et al,16 who found a 3.6% MRSA acquisition rate in patients with various skin diseases and an 8.5% rate among patients with generalized dermatoses. Our methods differed from those of Girou et al, who considered both true infections and colonizations without clinical signs. We performed bacterial cultures only if clinical worsening occurred, which did not allow us to calculate precisely the total MRSA colonization rates (with and without clinical signs) and thus underestimated the true rate of MRSA acquisition. Only systematic screening, for instance weekly, could provide information about true MRSA colonization rates. A cost-benefit analysis would be required to assess whether this is warranted.

In many patients with skin breaks, it is doubtful whether there is a clinical wound infection because local signs are misleading, especially if they are not found in combination with other symptoms20 that justify bacterial sample analysis. Among 23 patients with clinical signs, only 9 (39%) with the isolation of MRSA were related to a true local infection according to the Centers for Disease Control criteria,13 which led to a possible systemic treatment. Despite the limitations of the risk factor analysis due to the small numbers of patients in the 2 groups, the failure to identify a specific factor for infection (Table 3), particularly diabetes mellitus, which is a known risk factor for wound infection,21 was an unexpected finding in our study. In wounds, colonization and infection may be 2 stages of the same pathological process, the infection state resulting from an imbalance between the pathogen's virulence and the host's defense factors.22

As S aureus is part of the commensal flora and no normal microbial flora in leg ulcers can be established,20 optimal therapy for such wounds with MRSA colonization has not been defined. In our ward, careful local care, mainly based on washing and wound cleaning, seems to be beneficial enough to avoid the need for systemic antibiotics when wounds have MRSA colonization. A regular and particular vigilance for the development of new local signs in patients with skin breaks is essential for the early detection of such pathogenic colonizations.

This study showed a significant decrease in the incidence of infection between the period before the implementation of the control program and subsequent years, 1994 (P=.02) and 1996 (P=.002). Many measures have been recommended for controlling the spread of MRSA in hospitals. However, there is controversy regarding which measures should be preferentially implemented. Our intervention to control MRSA consisted of systematic wound management associated with the strict application of simple barrier precautions, such as using gloves and gowns and regularly washing the hands and skin with soap and water. These simple measures could be applied in most long-term care or rehabilitation facilities with high MRSA incidence. Other proposed measures,23 such as cohort nursing or placing all MRSA patients in single rooms or in separate wards, are not easily applicable in most facilities.

Although the results of our study are limited by the use of historical controls, they showed that simple infection control measures, such as the use of soap and water and barrier precautions associated with staff education, seemed to significantly reduce MRSA infection rates in patients with chronic skin breaks.

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Article Information

Accepted for publication November 4, 1999.

Presented in part at the Fifth International Conference on the Prevention of Infection, Nice, France, May 6, 1998.

The authors thank Gilles Chatellier, MD, for the helpful suggestions on statistical analysis.

Corresponding author: Guillaume Kac, MD, Unité d'Hygiène, Service de Microbiologie, Hôpital Broussais, 96 rue Didot, 75014 Paris, France (e-mail: guillaume.kac@brs.ap-hop-paris.fr).

References
1.
Moreno  FCrisp  CJorgensen  JHPatterson  JE Methicillin-resistant Staphylococcus aureus as a community organism. Clin Infect Dis. 1995;211308- 1312Article
2.
Panlilio  ACulver  DHGaynes  RP  et al.  Methicillin-resistant Staphylococcus aureus in U.S. hospitals, 1975-1991. Infect Control Hosp Epidemiol. 1992;13582- 586Article
3.
Collège de Bactériologie-Virologie-Hygiéne du Centre Hospitalier Universitaire de Paris, Surveillance des staphylocoques dorés et klebsielles multi-résistants à l'Assistance Publique-hôpitaux de Paris (1993-96). Bull Epidemiol Hebdo. 1998;1041- 43
4.
Richet  HWiesel  MLe Gallou  FAndré-Richet  BEspaze  E Methicillin-resistant Staphylococcus aureus control in hospitals: the French experience. Infect Control Hosp Epidemiol. 1996;17509- 511Article
5.
Lowy  FD Staphylococcus aureus infections. N Engl J Med. 1998;339520- 532Article
6.
Wakefield  DSHelms  CMMassanari  RMMori  MPfaller  M Cost of nosocomial infection: relative contributions of laboratory, antibiotic, and per diem costs in serious Staphylococcus aureus infections. Am J Infect Control. 1988;16185- 192Article
7.
Mulligan  MEMurray-Leisure  KARibner  BS  et al.  Methicillin-resistant Staphylococcus aureus: a consensus review of the microbiology, pathogenesis, and epidemiology with implications for prevention and management. Am J Med. 1993;94313- 328Article
8.
Jarlier  V Surveillance en France: klebsielles et staphylocoques multirésistants: stratégie de prévention à l'AP-HP. Bull Epidemiol Hebdo. 1993;42192- 193
9.
Ayliffe  GAJ Recommendations for the Control of Methicillin-Resistant Staphylococcus aureus (MRSA).  Geneva, Switzerland World Health Organization1996;1- 28
10.
Bradley  SFTerpenning  MSRamsey  MA  et al.  Methicillin-resistant Staphylococcus aureus: colonization and infection in a long-term care facility. Ann Intern Med. 1991;115417- 422Article
11.
Coello  RGlynn  JRGaspar  CPicazo  JJFereres  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;3739- 46Article
12.
Bradley  SF Methicillin-resistant Staphylococcus aureus in nursing homes: epidemiology, prevention and management. Drugs Aging. 1997;10185- 198Article
13.
Garner  JSJarvis  WREmori  TGHoran  TCHughes  JM CDC definitions for nosocomial infections, 1988. Am J Infect Control. 1988;16128- 140Article
14.
Acar  JBergogne-Bérézin  EChabbert  Y  et al.  Communiqué 1992 du Comité de l'Antibiogramme de la Société Française de Microbiologie. Pathol Biol (Paris). 1992;40741- 748
15.
Casewell  MW Epidemiology and control of the "modern" methicillin-resistant Staphylococcus aureusJ Hosp Infect. 1986;7(suppl A)1- 11Article
16.
Girou  EWolkenstein  POppein  F  et al.  Suivi d'une politique de lutte contre les staphylocoques dorés méticilline-résistants dans une unité de soins intensifs de dermatologie. Ann Dermatol Venereol. 1996;123(suppl 1)S16- S17
17.
Rodier  Lde Wit  D MRSA colonization rates of readmitted patients previously colonized or infected with MRSA. J Hosp Infect. 1997;35161- 163Article
18.
Girou  EPujade  GLegrand  PCizeau  FBrun-Buisson  C Selective screening for control of methicillin-resistant Staphylococcus aureus (MRSA) in high-risk hospital areas with a high level of endemic MRSA. Clin Infect Dis. 1998;27543- 550Article
19.
Maguire  GPArthur  ADBoustead  PJDwyer  BCurrie  BJ Clinical experience and outcomes of community-acquired and nosocomial MRSA in a northern Australian hospital. J Hosp Infect. 1998;38273- 281Article
20.
Hansson  C Microbial flora in venous leg ulcers and choice of treatment. Treatment of Ulcers. Oslo, Norway Sandberg AS1995;139- 148
21.
Nathan  DM Long-term complications of diabetes mellitus. N Engl J Med. 1993;3281676- 1684Article
22.
Bonten  MJMWeinstein  RA The role of colonization in the pathogenesis of nosocomial infections. Infect Control Hosp Epidemiol. 1996;17193- 200Article
23.
Boyce  JM Methicillin-resistant Staphylococcus aureus in hospitals and long-term care facilities: microbiology, epidemiology, and preventive measures. Infect Control Hosp Epidemiol. 1992;13725- 737Article
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