What Proportion of Hospital Patients Colonized With Methicillin‐Resistant Staphylococcus aureus Are Identified by Clinical Microbiological Cultures?
Background. Most hospitals in the United States do not perform active surveillance cultures and, thus, rely on clinical microbiological cultures (CMCs) to identify patients colonized with methicillin‐resistant Staphylococcus aureus (MRSA). We sought to determine what proportion of patients who are colonized with MRSA at admission are identified by CMCs during hospitalization.
Methods. From February 1998 through November 2002, patients found to be colonized with MRSA at admission by use of active surveillance cultures were identified. The proportion of colonized patients who had a CMC that was positive for MRSA, the number of CMCs performed and their type (ie, according to the anatomical site from which specimens were obtained for culture), and the number and type of CMCs that were positive for MRSA were calculated.
Results. Four hundred thirty‐seven patients were found to be colonized with MRSA at admission, and 98 of 1,238 CMCs (7.9%; 95% confidence interval, 6.5%‐9.6%) performed for 66 of these patients (15%; 95% confidence interval, 11.9%‐18.8%) were positive for MRSA. The number of nonisolated days that would have occurred by relying on CMCs to identify MRSA‐colonized patients was 3,247 (mean, 7.4 days per patient). Among the anatomical sites from which specimens were obtained for CMC, wounds demonstrated the highest sensitivity (30.2%) for identifying MRSA‐colonized patients.
Conclusions. CMCs failed to identify 85% of MRSA‐colonized patients, because, in part, CMCs identified only a small proportion of colonized patients. Because many studies have shown a decrease in the transmission of MRSA from colonized patients for whom contact precautions, rather than standard precautions, are used, the findings of this study suggest that failure to identify colonized patients and to use contact precautions may be an important reason for the increasing rate of nosocomial MRSA infection in hospitals in the United States.
Received May 17, 2005; accepted August 23, 2005; electronically published February 8, 2006.
Methicillin‐resistant Staphylococcus aureus (MRSA) is an important cause of nosocomial infection in US hospitals; compared with patients who acquire methicillin‐susceptible S. aureus infection, patients who acquire MRSA infection have higher mortality rates and stay in the hospital longer, resulting in significantly increased costs.1‐3 The proportion of S. aureus strains that are resistant to methicillin has continued to increase over the past 25 years, and, according to the most recent National Nosocomial Infection Surveillance System report from the Centers for Disease Control and Prevention, 59.5% of S. aureus strains causing nosocomial infections in intensive care units (ICUs) are resistant to methicillin.4
Nosocomial transmission of MRSA is thought to be largely the result of patient‐to‐patient transmission of the organism via the contaminated hands, clothing, and equipment of healthcare workers. To control the transmission of epidemiologically important organisms, including MRSA, the Centers for Disease Control and Prevention guideline for isolation precautions in hospitals recommended contact isolation (ie, placing the patient in a private room and requiring that healthcare providers entering the room wear gowns and gloves) for patients who are known or suspected to be colonized or infected with these organisms.5
Patients known to have clinical MRSA infection contribute to the nosocomial reservoir for transmission of the organism, but a much larger proportion of this reservoir consists of patients who are merely colonized with the organism. Healthcare facilities may identify patients colonized with MRSA by use of routinely performed cultures sent to the clinical microbiology laboratory to identify causes of infection or by active surveillance cultures. A recent guideline from the Society for Healthcare Epidemiology of America emphasizes the importance of identifying the reservoir for nosocomial transmission by use of active surveillance cultures,6 but most US healthcare facilities do not perform active surveillance cultures and, thus, primarily rely on clinical microbiological cultures (CMCs) to identify MRSA‐colonized patients. We sought to determine the effectiveness of using CMCs for identifying MRSA‐colonized patients in a hospital where active surveillance cultures were being performed to identify the nosocomial reservoir of MRSA.
Methods
Study Setting and Surveillance Program
The University of Virginia Health System (Charlottesville, VA) includes a 600‐bed, tertiary‐care academic hospital that cares for patients from western and central Virginia. The hospital offers all medical and surgical subspecialty services, including solid‐organ and bone‐marrow transplantation. In 1998, to identify patients colonized with MRSA, our hospital began performing active surveillance cultures (the anatomical sites sampled were the anterior nares, the perirectum, and nonintact skin). Culture specimens were obtained in the following instances: (1) at admission, for patients admitted to any medical or surgical ward or ICU who were transferred from another healthcare facility (acute or long‐term care) and who were not previously known to have been colonized or infected with MRSA; and (2) at the time of intrafacility transfer to a general medicine ward or medical ICU, for patients who were already admitted to our hospital. Patients found to be colonized with MRSA were cared for using contact precautions.
Data Collection and Statistical Analysis
Patients found to be colonized with MRSA by use of a surveillance culture performed at admission to the hospital (to any medical or surgical ward or ICU) between February 1998 and November 2002 were identified by computer records, and the following values were calculated: (1) the proportion of patients who had 1 or more CMCs performed during their hospital stay, (2) the proportion of patients who had a CMC that was positive for MRSA, (3) the proportion of patients who had a CMC of a specimen from a particular anatomical site or medical device (eg, blood, sputum, urine, central venous catheter tip, stool, and wounds) that was positive for MRSA, (4) the proportion of CMCs of specimens obtained from a particular anatomical site that were MRSA positive, and (5) the number of days that an MRSA‐colonized patient would not have been in contact isolation if CMCs had been relied on to identify them as being colonized by MRSA. It was assumed that contact precautions would have been instituted for the patient on the day that the positive culture result was known. For example, if a patient's CMC was known to be positive for MRSA on day 5 after admission, the number of nonisolated days would have been considered to be 5, and, if a patient had a CMC negative for MRSA (or never had one performed), the number of nonisolated days would have equaled their length of stay in the hospital. Patients found to be colonized with MRSA at the time of intrafacility transfer were not included.
The effectiveness of using CMCs to identify MRSA‐colonized patients was measured by the proportion of patients known to be MRSA‐colonized for whom at least 1 CMC was positive for MRSA. The sensitivity of CMCs performed with specimens taken from a particular anatomical site (eg, wounds) was defined as the proportion of CMCs that were positive for MRSA among colonized patients. A subgroup analysis of 50 patients was conducted to evaluate the effect that antimicrobial therapy active against the patient’s MRSA strain could have had on the effectiveness of CMCs for identifying MRSA‐colonized patients. The antimicrobial susceptibility pattern for each patient’s MRSA isolate was recorded and correlated with the antibiotics the patient had received during that hospital stay. If the patient was or had been receiving an antibiotic to which the MRSA isolate was susceptible, this was considered to be a possible explanation for the failure of the CMC to detect the presence of MRSA, if a CMC was performed.
Proportions and 95% confidence intervals (95% CIs) were calculated using Epi Info 2002 (Centers for Disease Control and Prevention). Proportions were compared using the χ2 test (Epi Info 2002), and continuous variables were compared using the Student’s t test (S‐Plus Statistical Computing Package; Mathsoft).
Laboratory Methods
Specimens for surveillance culture were collected with sterile, cotton‐tipped swabs and were transported to the epidemiology laboratory where they were directly plated onto trypticase soy agar with 5% sheep blood and mannitol salt agar (BBL). Colonies were identified as S. aureus by standard microbiologic methods.7 Resistance to methicillin was measured using disk diffusion, according to NCCLS standards.8 Clinical specimens sent to the clinical microbiology laboratory were handled according to specimen type, and methods used for determining resistance to methicillin were also those recommended by the NCCLS.7,8 The results of the surveillance cultures became available, on average, 2‐3 days after the specimens were collected.
Results
Entire Patient Population
During the study period, 437 patients were found to be colonized with MRSA by surveillance cultures performed at admission to the hospital. Of these, 306 patients (70%) had 1,238 CMCs performed during their hospital stay. Ninety‐eight CMCs (7.9%; 95% CI, 6.5%‐9.6%) from 66 patients (15%; 95% CI, 11.9%‐18.8%) were positive for MRSA. CMCs were not performed for 131 patients (30%).
Patient Population Admitted to a General Hospital Ward
Three hundred twenty‐five patients were found to be colonized with MRSA at admission to a general hospital ward, and 223 (68.6%) of these patients had 733 CMCs performed during their hospital stay. Fifty‐four CMCs (7.4%; 95% CI, 5.6%‐9.5%) from 42 patients (12.9%; 95% CI, 9.5%‐17.1%) were positive for MRSA. CMCs were not performed for 102 patients (31.4%).
Patient Population Admitted to an ICU
One hundred‐twelve patients were found to be colonized with MRSA at admission to an ICU, and 83 (74.1%) of these patients had 505 CMCs performed during their hospital stay. Forty‐four CMCs (8.7%; 95% CI, 6.4%‐11.5%) from 24 patients (21.4%; 95% CI, 14.2%‐30.2%) were positive for MRSA. CMCs were not performed for 29 patients (25.9%). Compared with patients who were admitted to a general hospital ward, the proportion of patients with a CMC positive for MRSA was significantly higher among patients admitted to an ICU (12.9% vs 21.4%; 
); however, the effectiveness of using CMCs to identify MRSA‐colonized patients did not differ significantly between the 2 patient populations (8.7% vs 7.4%; 
).
Analysis to Assess the Effect of Antimicrobial Therapy on the Sensitivity of CMC
Subgroup analysis for 50 patients for whom 197 CMCs were negative for MRSA revealed that 8 patients (16%) had received antibiotic therapy that could have been active against their MRSA strain (eg, vancomycin, clindamycin, or trimethoprim‐sulfamethoxazole) and, thus, could have prevented 66 (33.5%) of the CMCs for these patients from being positive for MRSA.
Nonisolated Patient Days
The total number of days that the 437 patients found to be colonized with MRSA by active surveillance cultures (at admission) would not have been in contact isolation while awaiting the results of their cultures was 874 to 1,311 days (ie, 2 to 3 days per patient). For the 66 patients (15%) with an MRSA‐positive CMC, the total number of nonisolated patient days that would have occurred before the positive culture result was known would have been 358 (average, 5.4 days per patient). For the 371 patients (85%) who had an MRSA‐negative CMC or who never had a CMC performed (and thus would have remained nonisolated throughout their entire hospitalization), the total number of nonisolated patient days would have been 2,889 (average, 7.8 days per patient). Compared with patients who had an MRSA‐positive CMC, patients who had an MRSA‐negative CMC or who never had a CMC performed would have remained nonisolated for a significantly longer mean time (5.4 days vs 7.8 days; 
). The total number of nonisolated patient days that would have occurred by relying on MRSA‐positive CMCs to identify MRSA‐colonized patients was 3,247 (average, 7.4 days per colonized patient). Thus, the number of nonisolated days prevented by using active surveillance cultures to identify MRSA‐colonized patients was 1,936 to 2,373 days (ie, 
days to 
days).
Culture Types
Among the types of cultures performed, cultures of specimens from wounds (acute or chronic) demonstrated the highest sensitivity (30.2%) for identifying MRSA‐colonized patients, followed by cultures of sputum specimens and of central venous catheter tips (Table).
Discussion
The use of active surveillance cultures to identify MRSA‐colonized patients so that transmission can be prevented with contact precautions has been controversial, in part because most available data suggest that this approach works,6,12‐32 but the approach has not yet been used routinely and consistently to control MRSA infection in the vast majority of US healthcare facilities.33 The results of this analysis suggest that relying on CMCs to identify MRSA‐colonized patients results in failure to recognize a large majority of these patients, who constitute most of the reservoir for nosocomial transmission of MRSA. Reliance on CMCs would have failed to identify 85% of this cohort of MRSA‐colonized patients (87% of patients in hospital wards and 79% of patients in ICUs). This failure occurred, in part, because CMCs were shown to identify only a small proportion of MRSA‐colonized patients. The use of antibiotics shortly before or during the period when the CMC specimen was obtained could have affected this proportion.
In a multivariate analysis, colonization pressure (ie, the ratio of the number of patient‐days for MRSA carriers to the total number of patient days) was an independent risk factor for nosocomial acquisition of the organism.9 When the weekly colonization pressure was greater than 30%, the risk of nosocomial MRSA acquisition was almost 5 times higher for patients in the medical ICU than when colonization pressure was less than 10% (relative risk, 4.9; 95% CI, 1.2‐19.9; 
).9 Furthermore, other studies have reported that a substantial proportion of patients colonized with MRSA will subsequently develop an MRSA infection.10,11 For example, in one study, the risk of developing an MRSA infection over the course of 18 months was 29% among colonized individuals. These infections were often severe and included cases of bacteremia, pneumonia, and soft‐tissue infection.10 In a meta‐analysis of 11 studies, compared with bacteremia due to methicillin‐susceptible S. aureus, bacteremia due to MRSA was associated with an almost 2‐fold higher mortality rate (relative risk, 1.8; 95% CI, 1.33‐2.69; 
) after adjustment for other predictors of death.1 Another study reported an 8‐day longer hospital stay (
)3 and a median excess of more than $17,000 in hospital costs for patients with bacteremia due to MRSA, compared with patients with bacteremia due to methicillin‐susceptible S. aureus.3 In addition, among patients who acquired a surgical site infection, a multivariable analysis found that infection with MRSA was associated with a significantly increased odds ratio of death (odds ratio, 3.4; 
) and a 1.9‐fold increase in hospital costs.2 Thus, control of MRSA transmission is a desirable goal for healthcare facilities.
The use of contact precautions has been shown to decrease nosocomial transmission of MRSA.6,12‐27,30‐32 In one study, the rate of nosocomial MRSA transmission was compared between MRSA‐colonized patients being cared for using contact precautions and those being cared for using standard precautions.13 A 15.6‐fold decrease (95% CI, 5.3‐45.6) in MRSA transmission was reported for the group being cared for using contact precautions (0.009 transmissions per day vs 0.14 transmissions per day for the standard precautions group; 
).13 A study from an ICU in The Netherlands reported 38‐fold more transmissions from nonisolated patients than from isolated patients.14 A multicenter study from The Netherlands that used a more conservative analysis did not include all instances of transmission but, instead, analyzed whether one or more transmissions from a colonized patient had occurred; the study found that, of 95 nonisolated patients, 19 patients transmitted pathogens at least once, and, of 73 isolated patients, only 4 patients transmitted pathogens at least once (relative risk, 4.3; 95% CI, 1.3‐18.2).34 In the present study cohort, the performance of surveillance cultures for high‐risk patients at admission prevented 1,936‐2,373 nonisolated patient days for MRSA‐colonized patients. Taken together, these data suggest that the failure to identify MRSA‐colonized patients, who constitute the majority of the reservoir for nosocomial transmission, and the failure to use contact precautions for these patients may be an important reason for the increasing rate of nosocomial MRSA infection that has been documented in US hospitals.4
Two recent studies have concluded that surveillance cultures and contact precautions would not help to control nosocomial transmission of MRSA in an ICU.28,29 In the first study, nosocomial transmission reportedly did not occur, even though these measures were not used for 10 weeks.28 In the second study, these measures reportedly did not work to control the transmission of MRSA.29 The study by Nijssen et al.28 did not specify whether standard precautions or universal barrier precautions were used, which makes interpretation of their results difficult. A relatively brief study (10 weeks) like that by Nijssen et al.28 also provides less statistical power to detect a difference from the findings of many published studies that have shown improved control of MRSA transmission with active surveillance cultures and contact precautions. For example, a longer contemporaneous study by Marshall et al.35 showed high rates of MRSA transmission (11.4%) and explicitly stated that only standard precautions were used. Even higher rates of transmission in an ICU were suggested by Cepeda et al.29 MRSA infection rates also increased significantly in many hospital ICUs surveyed by the National Nosocomial Infection Surveillance System during the 9 years that standard precautions were required in US hospitals.4,5 Such data suggest that studies by different authors conducted among different populations would be needed to verify the finding of Nijssen et al.28 that transmission of MRSA in ICUs is now well controlled.
Cepeda et al.29 concluded that no current measures, including active surveillance cultures and contact precautions, work to control the transmission of MRSA in an ICU where it is endemic, a finding that is at variance with the results of multiple studies.15,30‐32 Cepeda et al.29 made it harder to detect a difference between the 2 study groups by redefining standard precautions as being very similar to contact precautions. They also reported that nurses showed poor compliance with handwashing and good compliance with donning gowns, but not with removing gowns (as required to prevent transmission) or with donning or removing gloves. In addition, the compliance of healthcare workers other than nurses was not mentioned, and, according to Nijssen et al.,28 these healthcare workers may be more likely to transmit MRSA because, unlike nurses, they move more frequently from patient to patient. A large proportion of isolation days were also spent without contact isolation, which biased the results of the study by Cepeda et al.29 toward the null. Given the large number of studies that have reported success in controlling the transmission of MRSA using surveillance cultures and contact precautions,6,12‐27,30‐32 the results of the study by Cepeda et al.29 also require confirmation by additional studies by other investigators.
Others have reported the proportion of MRSA‐colonized patients for whom CMCs were positive for MRSA during their hospital stay. One study from a French ICU reported that 13 of 101 patients (12.9%; 95% CI, 7.04%‐21.0%) for whom screening cultures were positive at admission had an MRSA‐positive CMC during the 3 days before or after transfer to the ICU.25 In comparison, the present study, which was conducted at a large US tertiary care center, found that 21.4% of ICU patients (95% CI, 14.2%‐30.2%) had a CMC that was positive for MRSA during their hospital stay. Another study by Lucet et al.36 found results similar to those of the present study. Compared with admission screening, clinical samples identified only 15.8% of elderly patients known to have had MRSA at admission to the hospital. In addition, 81.1% of MRSA‐positive patient days would have been spent without contact isolation if culture of clinical samples was relied on to identify MRSA‐positive patients.36 Of note, in the present study, a large majority of the newly admitted patients with MRSA colonization were in regular hospital wards, where two‐thirds of all nosocomial infections have occurred in this hospital in recent years (data not shown).
Despite many studies having documented that use of active surveillance cultures and contact precautions can control nosocomial MRSA transmission in healthcare facilities,6,12‐27,30‐32 the number of US healthcare facilities that have routinely and consistently used this approach to control transmission throughout the healthcare setting remains low.33 The details of the numerous studies reporting successful control of MRSA with these methods are beyond the scope of the present article; however, the results of the present study suggest that meaningful control of patient‐to‐patient transmission of nosocomial MRSA probably cannot be achieved by relying on CMCs to detect colonized patients, because most of the patients are missed when this strategy is used.
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Presented in part at the 13th Annual Scientific Meeting of the Society for Healthcare Epidemiology of America; April 5‐8, 2003; Arlington, VA (abstract 28).