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Universal Surveillance for Methicillin-Resistant Staphylococcus aureus in 3 Affiliated Hospitals

Ari Robicsek, MD; Jennifer L. Beaumont, MS; Suzanne M. Paule, BS; Donna M. Hacek, BS; Richard B. Thomson Jr., PhD; Karen L. Kaul, MD, PhD; Peggy King, RN, MBA; and Lance R. Peterson, MD
[+] Article and Author Information

From Evanston Northwestern Healthcare and Northwestern University Feinberg School of Medicine, Evanston, Illinois.


Acknowledgment: The authors thank Judson Vosburg and the Evanston Northwestern Healthcare administration for their support, Toni-Marie Gonzalzles for chart review, and Ilana Segal and Michael Klompas for thoughtful comments on the manuscript.

Potential Financial Conflicts of Interest:Consultancies: R.B. Thomson (GlaxoSmithKline), K.L. Kaul (Roche). Honoraria: A. Robicsek (Becton Dickinson), S.M. Paule (Becton Dickinson), R.B. Thomson (Becton Dickinson), K.L. Kaul (Roche, Becton Dickinson), L.R. Peterson (Becton Dickinson). Grants received: K.L. Kaul (Roche), L.R. Peterson (Becton Dickinson, Cepheid, 3M, Roche, Nanosphere). Grants pending: A. Robicsek (Becton Dickinson), L.R. Peterson (Becton Dickinson, Cepheid, 3M, Roche).

Reproducible Research Statement:Study protocol: Available from Dr. Peterson (e-mail, lancer@northwestern.edu). Statistical code: Available from Dr. Robicsek (e-mail, ari.robicsek@gmail.com). Data set: Available from Dr. Robicsek (e-mail, ari.robicsek@gmail.com).

Requests for Single Reprints: Lance R. Peterson, MD, Department of Pathology and Laboratory Medicine, Evanston Northwestern Healthcare, 2650 Ridge Avenue, Evanston, IL 60201; e-mail, lancer@northwestern.edu.

Current Author Addresses: Dr. Robicsek: Department of Medicine, Division of Infectious Diseases, Evanston Northwestern Healthcare, 2650 Ridge Avenue, Evanston, IL 60201.

Ms. Beaumont: Center on Outcomes, Research, and Education, Evanston Northwestern Healthcare, 2650 Ridge Avenue, Evanston, IL 60201.

Ms. Paule and Ms. Hacek: Department of Pathology and Laboratory Medicine, Division of Microbiology, Evanston Northwestern Healthcare, 2650 Ridge Avenue, Evanston, IL 60201.

Drs. Thompson, Kaul, and Peterson: Department of Pathology and Laboratory Medicine, Evanston Northwestern Healthcare, 2650 Ridge Avenue, Evanston, IL 60201.

Ms. King: Department of Risk Management, Evanston Northwestern Healthcare, 2650 Ridge Avenue, Evanston, IL 60201.

Author Contributions: Conception and design: A. Robicsek, S.M. Paule, D.M. Hacek, R.B. Thomson, K.L. Kaul, P. King, L.R. Peterson.

Analysis and interpretation of the data: A. Robicsek, J.L. Beaumont, S.M. Paule, D.M. Hacek, R.B. Thomson, K.L. Kaul, P. King, L.R. Peterson.

Drafting of the article: A. Robicsek, J.L. Beaumont, L.R. Peterson.

Critical revision of the article for important intellectual content: J.L. Beaumont, S.M. Paule, D.M. Hacek, R.B. Thomson, P. King, L.R. Peterson.

Final approval of the article: J.L. Beaumont, S.M. Paule, D.M. Hacek, R.B. Thomson, K.L. Kaul, P. King, L.R. Peterson.

Statistical expertise: J.L. Beaumont.

Obtaining of funding: P. King.

Administrative, technical, or logistic support: S.M. Paule, D.M. Hacek, R.B. Thomson, K.L. Kaul, L.R. Peterson.

Collection and assembly of data: S.M. Paule, K.L. Kaul, L.R. Peterson.


Ann Intern Med. 2008;148(6):409-418. doi:10.7326/0003-4819-148-6-200803180-00003
Text Size: A A A

Background: The effect of large-scale expanded surveillance for methicillin-resistant Staphylococcus aureus (MRSA) on health care–associated MRSA disease is not known.

Objective: To examine the effect of 2 expanded surveillance interventions on MRSA disease.

Design: Observational study comparing rates of MRSA clinical disease during and after hospital admission in 3 consecutive periods: baseline (12 months), MRSA surveillance for all admissions to the intensive care unit (ICU) (12 months), and universal MRSA surveillance for all hospital admissions (21 months).

Setting: A 3-hospital, 850-bed organization with approximately 40 000 annual admissions.

Intervention: Polymerase chain reaction–based nasal surveillance for MRSA followed by topical decolonization therapy and contact isolation of patients who tested positive for MRSA.

Measurements: Poisson and segmented regression models were used to compare prevalence density of hospital-associated clinical MRSA disease (bloodstream, respiratory, urinary tract, and surgical site) in each period. Rates of bloodstream disease with methicillin-susceptible S. aureus were used as a control.

Results: The prevalence density of aggregate hospital-associated MRSA disease (all body sites) per 10 000 patient-days at baseline, during ICU surveillance, and during universal surveillance was 8.9 (95% CI, 7.6 to 10.4), 7.4 (CI, 6.1 to 9.0; P = 0.15 compared with baseline), and 3.9 (CI, 3.2 to 4.7; P < 0.001 compared with baseline and ICU surveillance), respectively. During universal surveillance, the prevalence density of MRSA infection at each body site had a statistically significant decrease compared with baseline. The methicillin-susceptible S. aureus bacteremia rate did not statistically significantly change during the 3 periods. In a segmented regression model, the aggregate hospital-associated MRSA disease prevalence density changed by −36.2% (CI, −65.4% to 9.8%; P = 0.17) from baseline to ICU surveillance and by −69.6% (CI, −89.2% to −19.6%]; P = 0.03) from baseline to universal surveillance. During universal surveillance, the MRSA disease rate decreased during hospitalization and in the 30 days after discharge; no further reduction occurred thereafter. Surveillance with clinical cultures would have identified 17.8% of actual MRSA patient-days, and ICU-based surveillance with polymerase chain reaction would have identified 33.3%.

Limitation: The findings rely on observational data.

Conclusion: The introduction of universal admission surveillance for MRSA was associated with a large reduction in MRSA disease during admission and 30 days after discharge.

Figures

Grahic Jump Location
Figure 1.
Intervention timeline.

ICU = intensive care unit; MRSA = methicillin-resistant Staphylococcus aureus.

Grahic Jump Location
Grahic Jump Location
Figure 2.
Adherence to methicillin-resistant Staphylococcus aureus admission testing during intensive care unit surveillance (August 2004 to August 2005) and universal surveillance (August 2005 to April 2007).
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Grahic Jump Location
Figure 3.
Segmented Poisson regression model: aggregate hospital-associated methicillin-resistant Staphylococcus aureus prevalence density throughout the study time frame.

Intensive care unit surveillance was initiated on 1 August 2004, and universal admission surveillance was initiated on 1 August 2005. “Hospital-associated” is defined as infection occurring >48 hours after admission and ≤30 days after discharge.

Grahic Jump Location
Grahic Jump Location
Figure 4.
Timing of methicillin-resistant Staphylococcus aureus infections relative to admission during the 3 study periods.

All intra-admission differences are statistically significant, as are the differences between universal surveillance and the other periods at 1 to 30 days. ICU = intensive care unit.

Grahic Jump Location

Tables

References

Letters

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Comments

Submit a Comment
Universal surveillance for MRSA: polymerase chain reaction tests VS. culture-based assays
Posted on March 20, 2008
Liu Hong
Institute of Digestive Diseases, Xijing Hospital, Fourth Military Medical University
Conflict of Interest: None Declared

To the editor:

We read with interest the article by Robicsek and colleagues (1). They have described the first large-scale, universal-admission MRSA surveillance program in the United States, and clearly show that the program is associated with a large reduction in MRSA disease during admission and 30 days after discharge.

The intervention is based on polymerase chain reaction tests, which have better sensitivity but may yield more false-positive results (2), as compared to culture-based assays. Furthermore, polymerase chain reaction tests may not identify all the subgenus of MRSA. Although previous work suggests that culture-based assays identifies low percentage of patients with MRSA infection (3), but they show high specificity. However, the authors don't explain why they use polymerase chain reaction tests separately as intervention, instead of a combination of culture-based assays. Could the authors comment on the application dominance of polymerase chain reaction tests as compared to culture-based assays, including specificity and cost effectiveness? Clinicians will need to know which assay is recommended for wide clinical application.

References:

1 Robicsek A, Beaumont JL, Paule SM, Hacek DM, Thomson RB Jr, Kaul KL, et al. Peterson LR. Universal Surveillance for methicillin-resistant Staphylococcus aureus in 3 affiliated hospitals. Ann Intern Med. 2008;148(6):409-18.

2 Paule SM, Hacek DM, Kufner B, Truchon K, Thomson RB Jr, Kaul KL, et al. Performance of the BD GeneOhm methicillin-resistant Staphylococcus aureus test before and during high-volume clinical use. J Clin Microbiol. 2007;45:2993-8.

3 Salgado CD, Farr BM. What proportion of hospital patients colonized with methicillin-resistant Staphylococcus aureus are identified by clinical microbiological cultures? Infect Control Hosp Epidemiol. 2006;27:116-21.

Conflict of Interest:

None declared

MRSA versus MSSA Rates
Posted on March 24, 2008
Rodney B. Nelson
none
Conflict of Interest: None Declared

03/24/2008

Dear Dr. Sox:

Two aspects of the "Surveillance for MRSA in 3 Affiliated Hospitals" study (1) concern me.

First, no mention is made of IRB approval or of informed consent from the experimental subjects. Being identified as a carrier of MRSA has many practical (and potentially harmful) influences on the hospital care of a patient, and for options for post hospital care. "Harming through Protection?" has recently been discussed in the context of studies of this type.(2) The Office for Human Research Protections has backed off from its recent position that these studies require full review. However, a thrombocytopenic patient who suffers a significant, transfusion requiring, nose bleed as a result of "de-colonization" triggered by his unwitting participation in a study might view the situation differently than OHRP.

Second, the authors of the MRSA study make these two statements: "To control for the possibility that the reduction in MRSA disease was due to an unrecognized co intervention, we compared changes in prevalence density of hospital-associated MRSA bacteremia with those of hospital- associated MSSA bacteremia." "The methicillin-susceptible S. aureus bacteremia rate did not statistically significantly change during the 3 periods."

Notwithstanding the questionable validity of doing such probabilistic testing in the absence of randomization, the reasoning behind the comparison might be flawed. If comparisons between reductions is of interest, a yard stick to measure the randomness of these differences is what is needed. If the treatment (i.e., preventive interventions in this case) is beneficial, then the treatment should be significantly better than no treatment compared to a suitable control. The rates of both MRSA and MSSA fell from identical baseline rates of 2.14. MRSA rates fell to 1.09 (49% reduction) and MSSA to 1.60 (25% reduction).

A significant difference in the reduction rates for MRSA and MSSA may not actually exist, since considerable overlap in the confidence intervals for the two exists (see Table 2). (Note: there may be a trivial error in this table since -0.54, not -0.55 is the reduction for MSSA. One suspects the baseline numbers (2.14 for both) might be a misprint. To get exactly the same confidence intervals (measured in hundredths) as well as rates, the actual numerators and denominators would have to be essentially identical).

A back of the envelope estimate based on 17.28 "10,000 patient days" (roughly a year of observation) for both periods is that there were about 37 MRSA and 37 MSSA bacteremias per year in the baseline period and about 19 MRSA and 28 MSSA per 17.28 "10,000 patient days" or per year during the third observation period. Using a simple Poisson calculator (stattrek.com) and using the average rate of both infections of 23, the cumulative Poisson probability is high that the difference in mrsa and mssa reductions (49% versus 25%) are not significant (~0.24). This seems to me the most logical null hypothesis, and it cannot be rejected.

Using the authors' dual null hypotheses and my same assumptions that the baseline average rate of mrsa and mssa is identical at 37 per year absent intervention, the probability of finding 19 in a year by chance alone is only 0.0008 (i.e., < 0.004) as reported. However, the probability of finding 28 MSSA absent intervention using my crude estimates is also relatively unlikely (~0.08) not 0.30 as reported. Thus the authors' rejection of their second MSSA null hypothesis seems tenuous. Absence of proof is not proof of absence.

I concede that my probability estimate methods are much cruder than the sophisticated methods employed by the authors. Still, caution is required before accepting the notion that a difference of 9 cases per year of two types of bacteremia lends support to the surveillance and treatment methods described in the report.

Sincerely,

1) Robicsek A, Beaumont JL, et al: Universal Surveillance for Methicillin-Resistent Staphylococcus aureus in 3 Affiliated Hospitals. Ann Intern Med 2008; 148:409-418

2) Bailey MA: Harming through Protection. N Eng J Med 358:768-769, 2008.

Conflict of Interest:

None declared

Universal Surveillance for MRSA Control: Accentuating the Positives, Ignoring the Negatives?
Posted on March 25, 2008
Daniel J. Diekema
University of Iowa Carver College of Medicine
Conflict of Interest: None Declared

To the Editor,

I read with interest the ambitious and informative study by Robicsek, et al. The study authors have clearly articulated the positive impact of their MRSA control strategy. In the process, they ignore the potential unintended consequences of this approach to MRSA control.

First, the title of the study is misleading, because this intervention involved much more than universal MRSA surveillance (1). A key component of their second intervention period was decolonization with mupirocin and chlorhexidine. Among several reasons that routine decolonization of asymptomatic MRSA carriers is not recommended, the emergence of mupirocin resistance is among the most important. Indeed, a recent publication in the Annals describes the emergence of a community- associated MRSA strain bearing the plasmid pUSA03, which carries a gene conferring high level resistance to mupirocin (2). Widespread use of mupirocin will likely facilitate the rapid spread of this resistance determinant. Did the authors monitor their MRSA strains for mupirocin resistance during the course of this study?

Secondly, the universal surveillance intervention increased the use of contact isolation dramatically (from ~2000 patient-days to over 11,000 patient-days in MRSA isolation). However, the authors do not mention the accumulating literature suggesting that contact isolation may be hazardous to patients (3, 4), nor did they include non-infectious adverse outcomes among the measures they reported. The potential negative impact on patient safety of a dramatic increase in the use of contact isolation must be assessed whenever a hospital decides to expand MRSA surveillance (3). Did the authors monitor non-infectious adverse outcomes among isolated (versus non-isolated) patients during their study?

Finally, the authors point to an unchanged rate of methicillin- susceptible S. aureus infection as evidence in favor of the effectiveness of their intervention, yet this finding is also an important indictment of "MRSA-based" interventions. After all, "susceptible" S. aureus can also kill patients, as can Pseudomonas, Escherichia coli, Klebsiella, Candida, and many other pathogens. Since MRSA causes fewer than 1 in 10 hospital infections, investing infection control resources in interventions that target all pathogens, not simply MRSA, will have a much greater impact on patient safety. Other academic health care centers have been able to reduce MRSA rates using approaches that avoid the expenses and hazards of universal MRSA surveillance, while also reducing infection rates due to other nosocomial pathogens (5).

References:

1. Robicsek A, Beaumont JL, Paule SM, Hacek DM, Thomson RB Jr, Kaul KL, King P, Peterson LR. Universal surveillance for methicillin-resistant Staphylococcus aureus in 3 affiliated hospitals. Ann Intern Med. 2008;148:409-18.

2. Diep BA, Chambers HF, Graber CJ, Szumowski JD, Miller LG, Han LL, et al. Emergence of multidrug-resistant, community-associated, methicillin -resistant Staphylococcus aureus clone USA300 in men who have sex with men. Ann Intern Med. 2008;148:249-57.

3. Diekema DJ, Edmond MB. Look before you leap: Active surveillance for multidrug-resistant organisms. Clin Infect Dis 2007;44:1101-7.

4. Stelfox HT, Bates DW, Redelmeier, DA. Safety of patients isolated for infection control. JAMA 2003;290:1899-905.

5. Edmond MB, Ober JF, Bearman G. Active surveillance cultures are not required to control methicillin-resistant Staphylococcus aureus in the critical care setting. Am J Infect Control 2008;(in press).

Conflict of Interest:

None declared

Universal Screening for Control of MRSA?
Posted on March 31, 2008
Margreet C Vos
Erasmus University Medical Center Rotterdam, the Netherlands
Conflict of Interest: None Declared

To the editor,

We agree with Robicsek et al (1) that active detection and isolation (ADI) reduced MRSA 70% while another recent study by Harbarth and colleagues failed (2) because Robicsek more closely approximated the goal of ADI enunciated by the 2003 SHEA guideline,(3) to identify and isolate all colonized patients (adjusting screening criteria for each facility because situations vary and criteria required in Chicago in 2008 may exceed those needed in the Netherlands or in Peoria, or in Chicago in 2018). We also agree that confining ADI to ICUs for MRSA or VRE control may be suboptimal (as suggested by multiple studies for over a decade).(3) While obvious to Northern European infection control specialists, it bears mention that 30% of an already high American MRSA rate is still far too high, thus more should be done to achieve optimal control. Examples of unmet opportunities for prevention in Robicsek's study include: 1) Robicsek's "universal admission screening" swabbed only noses. Nasal screening with culture had 78% to 93% sensitivity for detecting MRSA- colonized patients in 4 prior studies.(4) Robicsek used a PCR less sensitive than culture and actually screened only 84.4% of admissions implying that 30% to 41% of all MRSA-colonized admissions were neither found nor isolated. 2) Finding all colonized admissions wouldn't directly or promptly find and control the MRSA strains already circulating inside the hospital, so the SHEA guideline(3) recommended "periodic (eg, weekly) screening for patients remaining in the hospital at high risk for [acquiring ] MRSA because of location, antibiotic therapy, underlying disease, and/or duration of stay." If spread continues despite finding and isolating all patient reservoirs, the possibility of healthcare worker carriage should be addressed. 3) Because transmission occurs throughout the healthcare system, the SHEA guideline recommended that ADI "be implemented in all types of facilities throughout the healthcare system,"(3) but this wasn't done by the vast majority of Illinois acute and long term healthcare facilities, swelling the reservoir requiring identification, and making control by Robicsek more difficult. Lautenbach's belief that it's "premature" for all healthcare facilities to use ADI to find and isolate all colonized patients (5) reflects comfort with an unacceptable status quo. ADI was used to help control nosocomial SARS, smallpox and tuberculosis based on far less data than the over 100 studies showing MRSA control with ADI.(4) Demanding randomized trials before ADI implementation for MRSA but not for other nosocomial pathogens represents a hypocritical double standard. References: 1) Robicsek A, Beaumont JL, Paule SM, Hacek DM, Thomson RB, Kaul KL, MD, Peggy King P, and Peterson LR,. Universal surveillance for methicillin- resistant Staphylococcus aureus in 3 affiliated hospitals. Ann Intern Med 2008;148:409-418. 2) Harbarth S, Fankhauser C, Schrenzel J, Christenson J, Gervaz P, Bandiera-Clerc C, Renzi G, Vernaz N, Sax H, Pittet D. Universal screening for methicillin-resistant Staphylococcus aureus at hospital admission and nosocomial infection in surgical patients. JAMA 2008;299(10):1149-57. 3) Muto CA, Jernigan JA, Ostrowsky BE, Richet HM, Jarvis WR, Boyce JM et al. SHEA guideline for preventing nosocomial transmission of multidrug- resistant strains of Staphylococcus aureus and Enterococcus. Infect Control Hosp Epidemiol 2003;24(5):362-386. 4) Farr BM. Doing the right thing (and figuring out what that is). Infect Control Hosp Epidemiol 2006;27:999-1003. 5) Lautenbach E. Expanding the universe of methicillin-resistant Staphylococcus aureus prevention. Ann Intern Med 2008;148: 474-476.

Conflict of Interest:

None declared

When Universal does not mean All
Posted on April 3, 2008
William R. Jarvis
Jason and Jarvis Associates and Emory University School of Medicine
Conflict of Interest: None Declared

Word count = 397

To the editor,

We read with interest the study by Robicsek et al (1) and accompanying editorial (2). Congratulations to Robicsek et al for their successful intervention (70% MRSA infection reduction) using MRSA active detection and isolation (ADI). It is troubling that the editorialist failed to recognize this achievement. Instead of focusing on what should be done (use of MRSA Prevention Bundles), he offers excuses for why this hasn't/shouldn't occur. We believe the editorial requires comment. First, the editorialist states there is a "lack of rigorous scientific evidence" on how to limit MRSA. This is more applicable to a number of the Centers for Disease Control and Prevention (CDC) recommendations (e.g., outlawing false/long fingernails, maximum barrier precautions, etc.) with far less supporting evidence, yet never is. He discounts >150 quasi-experimental studies reporting MRSA control after MRSA Bundle (including ADI) implementation (3). Second, Lautenbach opines that several states' legislation "mandate uniform surveillance for MRSA", i.e., "one-size fits all". Perhaps the term "uniform" should be clarified. The Maryland bills and Illinois and Pennsylvania laws mandate active MRSA screening of facility-specific high-risk patients coupled with effective control measures (i.e., the SHEA Guideline approach [4]). MRSA high-risk patients exist at virtually every U.S. healthcare facility, so maybe this, like many CDC Guideline recommendations (Influenza prevention) should only come in one size. CDC lists groups for influenza immunization, without similar concerns voiced. Third, Lautenbach states that "screening for MRSA reduces MRSA infections---is not necessarily correct". We agree. MRSA screening alone will not reduce MRSA infections. Reductions require screening coupled with appropriate control measures. However, no study (quasi-experimental or randomized) has shown sustained 70% MRSA reductions without ADI inclusion.

Fourth, Lautenbach thinks it is "premature" to apply Robicsek's MRSA prevention bundle. Does he not believe that nearly 100,000 MRSA infections and 20,000 deaths annually require action? The MRSA Bundle works. We shouldn't be wasting time (and lives) debating the meritorious weight of each Bundle element (which has not been done with CVC-BSI, SSI or VAP Bundles). Fifth, Lautenbach states that "failure to act decisively"¦"¦.has resulted largely from the lack of rigorous scientific evidence". Au contraire, the failure of MRSA control results from hospitals choosing to continue to follow traditional infection control practices (e.g., isolating only culture-positive patients) despite a significant and growing body of evidence supporting a more aggressive approach. If prevention is primary, then implementing effective measures, like MRSA Bundles with ADI are, essential. Sincerely, William R. Jarvis, M.D. Carlene A. Muto, M.D., M.S. Jason and Jarvis Associates Division of Infectious Diseases Hilton Head Island, South Carolina 29928 University of Pittsburgh School of Medicine

3471 Fifth Street

1215 Kaufmann Building

Pittsburgh, PA 15213

References:

1) Robicsek A, Beaumont JL, Paule SM, Hacek DM, Thomson RB, Kaul KL, MD, Peggy King P, and Peterson LR,. Universal surveillance for methicillin- resistant Staphylococcus aureus in 3 affiliated hospitals. Ann Intern Med. 2008;148:409-418.

2) Lautenbach E. Expanding the universe of methicillin-resistant Staphylococcus aureus prevention. Ann Intern Med. 2008;148: 474-476.

3) Farr BM. Doing the right thing (and figuring out what that is). Infect Control Hosp Epidemiol 2006;27:999-1003.

4) Muto CA, Jernigan JA, Ostrowsky BE, Richet HM, Jarvis WR, Boyce JM et al. SHEA guideline for preventing nosocomial transmission of multidrug- resistant strains of Staphylococcus aureus and Enterococcus. Infection Control & Hospital Epidemiology 24(5):362-386, 2003. http://www.shea- online.org/Assets/files/position_papers/SHEA_MRSA_VRE.pdf

Conflict of Interest:

None declared

Question to Authors
Posted on April 25, 2008
Belinda K Ireland
BJC HealthCare, Washington University
Conflict of Interest: None Declared

Robicsek and colleagues' paper has received considerable attention for their findings, and some for their methods. I'd like to request the authors provide a bit more clarity on their analytic methods. In their section on statistical analysis for computing rates of MRSA infection, the authors state that for both models, they exclude infections that occur during the first month of each intervention surveillance period, presumably as an adjustment for lag time of the effect of intervention, but this is not so stated. The authors also neglect to state that they removed the corresponding person-time from their rates. This is important, because failing to do so artificially reduces infection rates for the intervention periods, creating a time during which individuals contribute to the denominator but cannot contribute to the numerator as infection cases. Would the authors please clarify their methods, so that we can exclude analytic error as a possible reason for their findings?

Conflict of Interest:

None declared

Reply from the Authors
Posted on April 30, 2008
Lance R Peterson
Evanston Northwestern Healthcare
Conflict of Interest: None Declared

The letter by Dr. Diekema raises several items for discussion. We regret that the writer(s) found our title misleading. As indicated in the report, the program's critical and enforced aspect was universal admission surveillance. Decolonization was at the attending physician's discretion. We routinely culture all positive PCR samples for MRSA and test isolates for mupirocin resistance, which occurred in 5.6% of strains before universal surveillance began and 4.1% at the end of the program's first year (1). Additionally, to minimize the potential for resistance, we have removed mupirocin for clinical use other than for nasal decolonization.

The overall impact of isolation on patient care is an important question. A number of reports, none of which are randomized trials, have suggested possible negative impact on the isolated patient. The cited review by Diekema and colleagues (2) references the report by Stelfox et al that appears to demonstrate more adverse events in isolated patients as well as fewer acceptable process of care measures (3). However, there were unacceptably high lapses in care of patients in the control (unisolated) group as well, with 21-41% of controls having days with no vital signs recorded as ordered; 9-11% of control days with no nursing notes; and 2-24% of unisolated patients having days with no physician notes - suggesting considerable improvement in many care practices were needed at the two study sites. Importantly, all significant adverse event increases were related to the area of supportive care failures, which is consistent with lower acceptable processes of care documentation and readily monitored for any improvement intervention.

As expected, patients are placed into isolation precautions for reasons other than MRSA (e.g., undiagnosed pneumonia, other multidrug- resistant organisms, or Clostridium difficile-associated diarrhea). We found that universal MRSA surveillance only modestly increased the overall rate of patients isolated (4). A recent one-day prevalence survey at Evanston Hospital (April 29, 2008) found that 10 of 30 patients were in isolation because of the universal MRSA surveillance program. As a monitor of satisfaction/dissatisfaction with our program, following the study period we asked our service excellence department to review any patient complaints related to our MRSA control program; there were none. On the contrary, there had been spontaneous comments thanking ENH for our aggressive approach to preventing healthcare-associated infections.

Another critical issue raised was that of focus on MRSA alone. We fully concur. While not part of our report, during the time frame of our MRSA program we managed an outbreak of Acinetobacter baumanii in one of our intensive care units and a rise of Clostridium difficile-associated diarrhea across our three-hospital organization; we also developed a new program to minimize our surgical site infections from S. aureus. All of these required separate investigation and intervention initiatives that were successfully completed (5-7), illustrating that MRSA need not be the only focus of an Infection Control program. This is not a zero-sum game, in which control of one infection necessarily leads to less funds for the control of another. In our case, success with MRSA and the cost savings that resulted has in fact led to a greater willingness of our hospital administration to support other Infection Control efforts.

We do believe, as our data suggests, that preventing transmission of MRSA so that fewer patients become colonized with this pathogen is a worthwhile goal for infection control programs. Another example of this is the recent publication by Harbarth and colleagues (8). This group demonstrated targeted surveillance for MRSA in their surgical patients showed no benefit in lowering overall surgical site infections. However, they documented the important risk associated with MRSA colonization by showing that 5-13% of MRSA colonized patients developed infection in contrast to 0-0.5% of non-carriers. We cannot comment upon the Edmond paper cited as it is in press.

The second letter of commentary by Dr. Nelson raises the issue of IRB approval and questions regarding our statistical methods. IRB approval was obtained for this project and disclosed to the Annals; unfortunately mention of it was unintentionally omitted in the final publication. While decolonization was recommended by infection control, it was not enforced and was at the discretion of the attending physician, requiring a specific order for this treatment. No adverse event related to decolonization was reported during the 21-month intervention period.

Regarding the statistical methods, firstly, there were indeed 37 MRSA and 37 methicillin susceptible S. aureus (MSSA) bacteremias in the baseline time period, accounting for the identical rates and 95% confidence intervals. In view of the comments regarding our data on MRSA and MSSA infection rates, we were perhaps insufficiently clear in outlining the aim of this analysis. We did not set out to directly compare the change in MRSA bacteremia rate with that of the MSSA bacteremia rates; due to the small number of bacteremic infections, statistical power for detecting such differences was limited. However, we have re-analyzed our data in this way, and even with the limited available power, a test comparing the Period 3 MRSA and MSSA bacteremia rates based on a Poisson regression results in a p-value of 0.085. That this difference should approach statistical significance has "˜face validity'; while MRSA and MSSA bacteremia rates were identical at baseline, MSSA rates were 50% higher than MRSA rates during Period 3. We believe the letter writer(s) arrived at a different result because the "back of the envelope" estimate did not account for the differing lengths of time in Periods 1 and 3.

The Dr. Nelson's next set of calculations (in which a p-value of 0.08 is presented for the change in MSSA infections) erroneously treats the 37 infections at baseline as a fixed value, effectively ignoring the random error; it also uses one-sample tests to compare the universal surveillance results to this value. Our calculations used two-group comparisons, accounting for random variation in measurement for both time periods, resulting in larger p-values.

References:

1. Paule S, Robicsek A, Suseno M, Kaul KL, Peterson LR. Incidence of mupirocin resistance in methicillin-resistant Staphylococcus aureus (MRSA) during universal surveillance and decolonization [Abstract]. In: Program and Abstracts of the 46th Interscience Conference on Antimicrobial Agents and Chemotherapy, 27-30 September 2006, San Francisco, California. Abstract C2-1149. Washington, DC: American Society for Microbiology.

2. Diekema DJ, Edmond MB. Look before you leap: Active surveillance for multidrug-resistant organisms. Clin Infect Dis 2007;44:1101-7.

3. Stelfox HT, Bates DW, Redelmeier DA. Safety of patients isolated for infection control. JAMA. 2003;290:1899-905.

4. Peterson, LR, Hacek DM, Robicsek A. Case Study: An MRSA Intervention at Evanston Northwestern Healthcare. Joint Comm J Qual Pat Safety. 2007;33:732-8.

5. La Forgia C, Franke J, Hacek DM, Small M, Paule SM, O'Connor K, Thomson RB, Jr, Peterson LR. A novel environmental cleaning intervention to curtail an outbreak of MDR-Acinetobacter baumannii in an intensive care unit [Abstract]. In: Program and Abstracts of the 16th Annual Meeting of the Society of Hospital Epidemiologists of America, 18-20 March, 2006, Chicago, Illinois. Abstract 306. Arlington, VA: Society for Healthcare Epidemiology of America.

6. Hacek DM, Robicsek A, Ogle A, Fisher A, Peterson LR. Significant impact of terminal room cleaning with bleach on reducing nosocomial Clostridium difficile [Abstract]. In: Program and Abstracts of the 47th Interscience Conference on Antimicrobial Agents and Chemotherapy, 17-20 September 2007, Chicago, Illinois. Abstract K-608. Washington, DC: American Society for Microbiology.

7. Hacek DM, Robb WJ, Paule SM, Kudrna JC, Stamos VP, Peterson LR. Staphylococcus aureus nasal decolonization in joint replacement surgery reduces infection. Clin Orthop Relat Res. 2008;Mar 18; [Epub ahead of print]. 8. Harbarth S, Fankhauser C, Schrenzel J, Christenson J, Gervaz P, Bandiera-Clerc C, Renzi G, Vernaz N, Sax H, Pittet D. Universal screening for methicillin-resistant Staphylococcus aureus at hospital admission and nosocomial infection in surgical patients. JAMA. 2008;299:1149-57.

8. Harbarth S, Fankhauser C, Schrenzel J, Christenson J, Gervaz P, Bandiera-Clerc C, Renzi G, Vernaz N, Sax H, Pittet D. Universal screening for methicillin-resistant Staphylococcus aureus at hospital admission and nosocomial infection in surgical patients. JAMA. 2008;299:1149-57.

Lance R. Peterson

Jennifer L. Beaumont

Ari Robicsek

Evanston Northwestern Healthcare 2650 Ridge Avenue Evanston, IL 60201

Conflict of Interest:

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Summary for Patients

Universal Surveillance for Methicillin-Resistant Staphylococcus aureus in 3 Affiliated Hospitals

The summary below is from the full report titled “Universal Surveillance for Methicillin- Resistant Staphylococcus aureus in 3 Affiliated Hospitals.” It is in the 18 March 2008 issue of Annals of Internal Medicine (volume 148, pages 409-418). The authors are A. Robicsek, J.L. Beaumont, S.M. Paule, D.M. Hacek, R.B. Thomson Jr., K.L. Kaul, P. King, and L.R. Peterson.

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