Real‐Time Polymerase Chain Reaction Detection of Methicillin‐Resistant Staphylococcus aureus: Impact on Nosocomial Transmission and Costs
Objectives. To assess the impact of real‐time polymerase chain reaction (PCR) detection of methicillin‐resistant Staphylococcus aureus (MRSA) on nosocomial transmission and costs.
Design. Monthly MRSA detection rates were measured from April 1, 2000, through December 31, 2005. Time series analysis was used to identify changes in MRSA detection rates, and decision analysis was used to compare the costs of detection by PCR and by culture.
Setting. A 1,200‐bed, tertiary care hospital in Canada.
Patients. Admitted patients at high risk for MRSA colonization. MRSA detection using culture‐based screening was compared with a commercial PCR assay.
Results. The mean monthly incidence of nosocomial MRSA colonization or infection was 0.37 cases per 1,000 patient‐days. The time‐series model indicated an insignificant decrease of 0.14 cases per 1,000 patient‐days per month (95% confidence interval, −0.18 to 0.46) after the introduction of PCR detection (
). The mean interval from a reported positive result until contact precautions were initiated decreased from 3.8 to 1.6 days (
). However, the cost of MRSA control increased from Can$605,034 to Can$771,609. Of 290 PCR‐positive patients, 120 (41.4%) were placed under contact precautions unnecessarily because of low specificity of the PCR assay used in the study; these patients contributed 37% of the increased cost. The modeling study predicted that the cost per patient would be higher with detection by PCR (Can$96) than by culture (Can$67).
Conclusion. Detection of MRSA by the PCR assay evaluated in this study was more costly than detection by culture for reducing MRSA transmission in our hospital. The cost benefit of screening by PCR varies according to incidences of MRSA colonization and infection, the predictive values of the assay used, and rates of compliance with infection control measures.
Received January 19, 2007; accepted April 26, 2007; electronically published August 10, 2007.
Methicillin‐resistant Staphylococcus aureus (MRSA) is responsible for increasing numbers of healthcare‐ and community‐acquired infections,1,2 adding to the total burden of illness and healthcare costs attributable to S. aureus.3‐9 Since 85%‐90% of patients with MRSA are asymptomatic carriers who can serve as a silent reservoir for further transmission,10 screening to detect MRSA carriage and the use of contact precautions have become the cornerstone of national guidelines on MRSA control.11,12 Furthermore, several studies have demonstrated the effectiveness13‐16 and cost‐effectiveness of these measures.12,16‐20
The main limitation of MRSA screening is the 2‐ to 4‐day delay between specimen collection and availability of the result. Molecular tests have recently become available that allow for detection of MRSA in less than 1 hour and possibly an increase in the sensitivity of detection.21 Although these tests are more expensive than culture,22 modeling studies suggest that reducing the reporting time for a positive MRSA result can reduce both the rate of nosocomial MRSA transmission23 and the number of patient isolation‐days.24 The objective of this study was to assess the effectiveness and cost of using a commercially available real‐time polymerase chain reaction (PCR) assay for MRSA detection with the goal of reducing nosocomial MRSA transmission.
Methods
This study was conducted at the Ottawa Hospital, a 1,200‐bed, multiple‐campus, tertiary care hospital with 5 critical care units. Real‐time PCR for MRSA detection was introduced in November 2004 at 1 inpatient campus and in February 2005 at the other 2 inpatient campuses. The monthly incidence of cases of nosocomial MRSA colonization or infection per 100,000 patient‐days was recorded before, during, and after implementation of PCR detection, from April 2000 through December 2005.
Throughout this period, screening criteria and infection control measures remained constant. These measures involved screening on admission for high‐risk patients (defined as patients directly transferred from another healthcare facility, patients hospitalized within the previous 6 months, and patients with a history of MRSA colonization or infection) and screening of roommates of any patient who tested positive for MRSA. Screening swab specimens were obtained from the anterior nares, rectum, open skin lesions, and catheter exit sites. Preemptive isolation of patients was not used. Patients who tested positive for MRSA were placed under contact precautions until hospital discharge or documented eradication of MRSA. Patients colonized or infected with MRSA who were in multiple‐bed rooms were moved to private rooms, and use of the other beds was blocked until the roommates’ screening results were available. After the introduction of PCR screening, patients who tested positive for MRSA by PCR were placed under contact precautions, pending confirmation by culture. Contact precautions were discontinued if the subsequent culture results were negative.
Microbiological Testing
Before the introduction of real‐time PCR to the hospital, MRSA screening was performed using a selective broth enrichment culture method.25 Up to 3 swab specimens per patient were pooled into a single tube of selective broth, which was incubated at 35°C overnight and subcultured in 5% sheep blood agar. Blood agar plates with no growth or with colonies other than staphylococci were reported as negative for MRSA. Isolates of S. aureus (confirmed by tube coagulase testing) were screened for methicillin resistance using oxacillin (6 μg/mL) salt agar screening plates. Methicillin resistance was confirmed by detection of the modified penicillin binding protein 2a by latex agglutination. Pulsed‐field gel electrophoresis of MRSA isolates was performed as described elsewhere.26
When real‐time PCR testing was introduced, the IDI‐MRSA assay (GenOhm) was used for MRSA detection as described elsewhere.27 Swab specimens were inoculated into selective broth as described above and were incubated overnight at 35°C. A 50‐μL aliquot of the overnight broth culture was transferred into the sample reagent buffer provided with the assay kit. PCR was then performed according to the manufacturer’s instructions using a SmartCycler II device (Cepheid). Culture confirmation was considered necessary, because this assay will also detect methicillin‐susceptible S. aureus.27 During our initial evaluation, we found this assay had a sensitivity of 96%, a specificity of 96%, a positive predictive value of 90%, and a negative predictive value of 98%, compared with culture. However, during the postimplementation period, the positive predictive value decreased to 65%. Therefore, PCR‐positive broth samples were subcultured onto blood agar plates, and S. aureus isolates were confirmed to be methicillin‐resistant as described above.
Evaluation of Effectiveness
The incidence of nosocomial MRSA colonization or infection per 1,000 patient‐days was compared before and after the introduction of real‐time PCR. A patient with nosocomial MRSA colonization or infection was defined as any patient in whom MRSA was detected from a screening swab specimen or clinical specimen obtained 48 hours or more after admission. In addition, patients who had MRSA detected at admission were considered to have nosocomial MRSA colonization or infection if they were hospitalized in our facility within the past 2 months and had no history of admission to another healthcare facility during that 2‐month period. The MRSA transmission rate was calculated as the ratio of patients with nosocomial MRSA colonization or infection to the number of patients admitted with MRSA colonization or infection, divided by the average length of hospitalization for patients admitted with MRSA colonization or infection.17 We measured the interval from when the screening swab specimen was obtained until contact precautions were initiated. We also compared the number and size of outbreaks of nosocomial MRSA colonization and infection that occurred before and after the introduction of PCR screening. An outbreak was defined as a cluster of 2 or more patients with MRSA colonization or infection that was epidemiologically linked to the same unit who had identical strains isolated, as determined by pulsed‐field gel electrophoresis. Finally, point‐prevalence studies were performed to evaluate the rate of compliance with admission screening for MRSA and to estimate the prevalence of MRSA among S. aureus isolates.
Statistical Analysis
The effect of using PCR screening on the rate of nosocomial MRSA colonization or infection was analyzed using interventional, autoregressive, integrated, moving average time‐series modeling. Time‐series analysis was used, because rates of MRSA colonization or infection were significantly autocorrelated, which means that values at time x were significantly affected by values at time 
. This approach makes the error terms of these observations dependent and therefore violates the assumptions of classic linear regression and standard inferential testing. In our models, the MRSA screening method used was represented by a dummy series (with 0 representing traditional methods and 1 representing PCR methods) that was cross‐correlated with the outcome time series. Autocorrelation function plots were reviewed to determine the presence of moving average parameters and the need for differencing; partial autocorrelation function plots were reviewed to identify autoregressive parameters. If the t ratio for the screening method in the best‐fitting model had a 2‐sided 
, we determined that PCR methods had a statistically significant effect on the rate of MRSA colonization and infection. SAS statistical software, version 9.1.3 (SAS Institute) was used for all analyses.
Cost Analysis
The cost of MRSA control were analyzed for the 6 months before implementation of PCR screening (ie, period 1, April through September 2004) and the 6 months after (ie, period 2, April through September 2005). Cost data were obtained from the hospital’s finance, admission, laboratory, and housekeeping departments and represented hospital costs for 2005, computed in Canadian dollars. Screening costs were applied to all admission screening specimens; subsequent testing of patients known to carry MRSA was excluded. Screening costs included nursing time to obtain, label, and transport specimens (6 minutes per patient at Can$30.00 per hour),19 the cost of disposable laboratory supplies (Can$20.26 for cultures with positive results, Can$2.12 for cultures with negative results, and Can$15.00 for each PCR test), and laboratory labor costs to process the specimens (Can$23.45 for cultures with positive results, Can$13.15 for cultures with negative results, and Can$5.32 for each PCR test). The initial cost of Can$80,000 to purchase PCR equipment and train technologists was not included in the analysis.
The cost of contact precautions was calculated only for patients who were placed under contact precautions during their stay, because 10% of patients had been discharged when their test result positive for MRSA became available. The nursing costs related to contact precautions were estimated as 1 minute to don and remove gloves, mask, and gown (at Can$30.00 per hour) multiplied by 50 patient contacts per day, on the basis of data from comparable Canadian hospitals.19,23,28 Supply costs included the cost of gloves (Can$0.14), gowns (Can$0.46), and masks (Can$0.12) per patient contact. Hand hygiene costs were not included, because these were presumed to apply to all patients, regardless of the use of contact precautions. The cost of lost revenue because of private room use or blocked beds was obtained by multiplying daily revenue lost by the number of patient‐days under contact precautions or the number of blocked‐bed days (4 days in period 1 and 2 days in period 2). Lost revenue because of private room use was incurred in 40% of cases.
Housekeeping costs included the cost of supplies used and time required for cleaning and supervision. Two types of cleaning were performed. An isolation room cleaning required 114 minutes at Can$24.04 per hour plus Can$8.84 in material costs. A regular room cleaning required 62 minutes at Can$24.04 per hour plus Can$7.61 of material costs. The supervision time was 15 minutes at Can$26.52 per hour for both types of cleaning. An isolation room cleaning was performed each time an MRSA‐positive result was reported, on transfer of the patient from a multiple‐bed room to a private room, and again at the time of patient discharge from the private room. For patients with culture‐confirmed MRSA, the cost difference between an isolation room and a regular room cleaning was used in the calculation. For patients PCR‐positive but culture‐negative for MRSA, the cost of a regular room cleaning was used. Infection control costs reflected the time required to review each new case and ensure that the necessary precautions were in place.
Decision Analysis
It is necessary to compare the costs of a culture‐based strategy for MRSA detection with a strategy with the cost of PCR testing, assuming similar incidence rates. Thus, we created a decision tree populated with the cost data described here (Table 1). For PCR testing, the decision tree used the observed sensitivity (96%), positive predictive value (65%), and rate of compliance with screening (61%), with a baseline incidence of 5%. We assumed culture was 100% sensitive and 100% specific, in order to err on the conservative side. Analysis focused on the expected costs for each strategy, and sensitivity analysis focused on the impact of incidence, sensitivity, specificity, and screening compliance on the results.
Results
Evaluation of Effectiveness
From April 1, 2000, through December 31, 2005, the mean incidence of nosocomial MRSA colonization or infection was 0.37 cases per 1,000 patient‐days per month (range, 0‐1.3), with an average of 29,323 patient‐days per month. The monthly incidence of nosocomial MRSA colonization or infection is presented in Figure 1. Gross examination of the time series shows no obvious shift in the rate of MRSA colonization or infection after the introduction of PCR screening. The time‐series model indicated that introduction of PCR screening was associated with an insignificant decrease of 0.14 cases of nosocomial MRSA colonization or infection per 1,000 patient‐days per month (95% confidence interval [CI], −0.18 to 0.46; 
). The time‐series models fit the data well, with a lag 6 Q statistic of 0.68 and a lag 12 Q statistic of 0.72.
Figure 1. Monthly incidence of nosocomial methicillin‐resistant Staphylococcus aureus colonization and infection at the Ottawa Hospital, April 1, 2000, through December 31, 2005. Each square represents the value for a single month.
The mean time from screening of the patient to initiation of contact precautions decreased significantly, from 3.8 days in the 6 months before the introduction of PCR screening to 1.6 days in the 6 months after introduction (
). In 2005, MRSA accounted for 19% of all clinical S. aureus isolated at the Ottawa Hospital and 13% of all blood cultures that yielded S. aureus. A point prevalence survey to evaluate compliance with admission screening included 779 patients who met the criteria for admission screening; 267 (34.3%) were screened within 24 hours after admission and 475 (61.0%) were screened during their hospital stay. This compliance rate remained stable over time.
Ten outbreaks occurred that involved 38 patients in period 1, and 8 outbreaks occurred that involved 20 patients in period 2. This difference was not statistically significant (0.23 vs 0.14 cases per 1,000 patient‐days per outbreak; relative risk [RR], 1.5 [95% CI, 0.90 to 2.88]; 
).
Cost Analysis
The costs associated with MRSA control are given in Table 2. In period 1, a total of 107 newly identified cases of MRSA colonization or infection occurred, of which 59 (55.1%) were considered nosocomial. In period 2, a total of 112 new culture‐confirmed cases occurred, of which 55 (49.1%) were considered nosocomial. Comparison of periods 1 and 2 found no significant differences in the rate of MRSA colonization or infection at admission (8.84 vs 9.36 cases per 1,000 admissions; RR, 0.94 [95% CI, 0.82 to 1.08]), the rate of nosocomial MRSA colonization or infection (0.35 vs 0.39 cases per 1,000 patient‐days; RR, 0.96 [95% CI, 0.66‐1.40]), or the rate of MRSA transmission (0.015 vs 0.012 cases per 1,000 patient‐days; 
). Previously known MRSA carriers who were readmitted represented 47.5% of patients with MRSA detected at admission (198 of 417) and accounted for 45.9% of the contact precautions–days in both periods (2,655 of 5,788).
The total cost of MRSA control increased from Can$605,034.60 for screening by culture to Can$771,609.33 for screening by PCR (Table 2). The mean cost per patient with MRSA colonization or infection increased from Can$2,937.06 to Can$3,656.92. Revenue lost because of private room use represented the largest cost, accounting for more than 30% of MRSA control costs in both study periods. A significant increase occurred in the number of patients placed under contact precautions in period 2, compared with period 1 (12.9 vs 8.2 patients per 1,000 admissions; RR, 1.57 [95% CI, 1.40 to 1.77]). In period 2, there were 290 patients placed under contact precautions, of whom 120 (41.4%) had a positive PCR result but a negative culture result and were considered to have had a false‐positive PCR result. These patients contributed 380 additional contact precaution–days and Can$83,925.80 in cost, accounting for 50% of the cost increase in period 2. Because of the low positive predictive value of PCR testing, all positive PCR results needed to be confirmed by culture, increasing the laboratory cost for a positive MRSA result from Can$43.71 in period 1 to Can$64.03 in period 2.
Decision Analysis
Our baseline analysis found that the PCR‐based strategy was more costly than the culture‐based strategy for MRSA detection (Can$96 vs Can$67 per patient, for a cost difference of Can$29). Cost differences decreased with higher rates of sensitivity and specificity of PCR detection but increased with higher rates of screening. For example, the cost difference was Can$20 if 100% sensitivity and 100% specificity were assumed for PCR detection. Conversely, the cost difference increased to Can$48 if the admission screening compliance rate improved to 90%. Cost differences were most sensitive to changes in the incidence of MRSA colonization and infection: the incremental cost of PCR testing was Can$45 for an incidence of 10% (Figure 2).
Figure 2. Impact of the incidence of methicillin‐resistant Staphylococcus aureus colonization and infection on the incremental cost of screening with polymerase chain reaction (PCR), based on the following assumptions: PCR sensitivity, 96%; PCR positive predictive value, 65%; and rate of compliance with admission screening, 61%.
Discussion
Rapid methods for detection of MRSA should reduce the rate of nosocomial transmission and facilitate control of MRSA.21,29 We found that implementing real‐time PCR detection was associated with a significant reduction in delays to initiate contact precautions for MRSA‐positive patients but an insignificant reduction in rate of nosocomial MRSA colonization and infection. Although modeling studies predict that rapid detection methods will be cost‐effective,23,24 results were mixed in one study30 and negative in our study. Our study contributes important clinical data to inform future modeling studies.22 Considering the cost difference of Can$166,000 between the 2 MRSA control strategies and the cost of Can$14,000 to treat a single MRSA infection,28 we estimate that 12 MRSA infections would need to be prevented during a 6‐month period for PCR to be cost neutral in our hospital.
The increased costs associated with PCR detection in this study were largely due to the low positive predictive value of the test. The unnecessary use of contact precautions for patients considered to have false‐positive PCR results accounted for approximately 50% of the increased costs, and the need for culture confirmation further eliminated anticipated cost savings. Our modeling study predicted that PCR detection would be less costly if improved sensitivity eliminated the need for culture confirmation; however, many centers will continue to require some culturing for strain typing. The model suggested that although the PCR assay we used was found to be costly in our hospital, it may be cost‐effective in areas that have higher incidence rates of MRSA colonization and infection, which would improve the positive predictive value of the test and eliminate the additional costs of unnecessarily placing patients under contact precautions. In addition, the manufacturer of the PCR assay has made some modifications to this commercially available assay that may improve its positive predictive value. This PCR assay may reduce MRSA control costs in hospitals where patients are isolated on admission until MRSA screening results are available (ie, those that use preemptive isolation). A lack of private rooms prohibits the use of this control measure in our hospital. Finally, other rapid methods for MRSA detection, such as the use of chromogenic media, are becoming available and appear to have high sensitivity and specificity.31 Such methods may offer a less costly alternative to PCR for rapid detection, although they are likely not as sensitive as a PCR assay.
Our data define some of the costs and challenges associated with control of nosocomial MRSA colonization and infection. The cost of the MRSA control measures recommended by the Society for Healthcare Epidemiology of America guidelines12 was approximately Can$3,000 per patient. The incidence of newly diagnosed cases in our study (4.97 cases per 1,000 admissions) was similar to the 1999 Canadian incidence of 4.12 cases per 1,000 admissions.32 The prevalence of MRSA‐positive patients admitted to our hospital increased during the study period, reflecting an increase in the rate of MRSA colonization and infection in the Ottawa region in the years 2000 to 2005, from 14.9 to 61.8 cases per 100,000 population. In light of the increase in the number of cases in our community, any control measures are likely to be most effective if implemented on a region‐wide, rather than facility‐specific, basis. Nearly half of the patients with MRSA detected at admission were previously known MRSA carriers.
This study highlights some important considerations for healthcare facilities considering implementation of PCR for MRSA detection. First, our data demonstrate that test performance may vary significantly between the evaluation phase and routine use in a clinical setting. Our previously published data found this PCR assay to be an excellent screening test with a negative predictive value of 98%, compared with culture.27 However, the positive predictive value decreased from 90% during the evaluation phase to 65% after implementation. This decrease appeared to be largely due to the detection of certain methicillin‐susceptible S. aureus strains. Preimplementation evaluation likely failed to detect this limitation, because testing was performed on a limited number of specimens. Second, new technology is unlikely to affect MRSA transmission in the absence of good infection control measures. The major weakness in our infection control program was the low rate of compliance with admission screening: 39.0% of high‐risk patients admitted to the hospital were not screened. Failure to identify MRSA carriers and place them under contact precautions, although associated with reduced cost in our modeling study, may increase the rate of nosocomial MRSA colonization or infection between 5‐ and 45‐fold.17 Similarly, new technology is unlikely to compensate for a lack of compliance with hand hygiene and other infection control measures to reduce transmission. In one Canadian hospital, healthcare workers and visitors were compliant with MRSA transmission precautions only 28% of the time.33
In summary, in our hospital the use of the IDI‐MRSA PCR assay was more costly than use of culture for detection of MRSA with the goal of reducing the rate of MRSA transmission. The cost benefit of PCR technology will vary according to the incidence rate of MRSA colonization and infection, the predictive values of the PCR assay used, and the rate of compliance with infection control measures. Rapid testing is less likely to be effective if delays occur in obtaining the specimen or in initiating contact precautions once the test results are available. Before investing in new technology, healthcare facilities should first ensure good compliance with admission screening, hand hygiene, and contact precautions, because any potential benefits associated with new technology are less likely to be realized if compliance rates are poor.
Acknowledgments
Financial support. L.O.C. reports receiving support from the Coordenacao de Aperfeicoamento de Pessoal de Nivel Superior, Ministry of Education, Brazil.
Potential conflicts of interest. All authors report no conflicts of interest relevant to this article.
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Presented in part: 16th Annual Meeting of the Society for Healthcare Epidemiology of America; Chicago, IL; March 2006 (Abstract 59).