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Mupirocin Prophylaxis to Prevent Staphylococcus aureus Infection in Patients Undergoing Dialysis: A Meta-analysis

  1. Evelina Tacconelli1,
  2. Yehuda Carmeli1,5,
  3. Anthony Aizer2,
  4. Gabriela Ferreira3,
  5. Marilyn G. Foreman4, and
  6. Erika M. C. D'Agata1
  1. 1Division of Infectious Diseases, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, Massachusetts
  2. 2Zena and Michael A. Wiener Cardiovascular Institute, Mount Sinai School of Medicine, New York, New York
  3. 3Division of Medicine, Robert Wood Johnson University Hospital, New Brunswick, New Jersey
  4. 4Division of Pulmonary and Critical Care, Morehouse School of Medicine, Atlanta, Georgia
  5. 5Division of Infectious Diseases, Tel-Aviv Sourasky Medical Center, Tel Aviv, Israel
  1. Reprints or correspondence: Dr. Evelina Tacconelli, Div. of Infectious Diseases, Beth Israel Deaconess Medical Center and Harvard Medical School, Kennedy 6, 330 Brookline Ave., Boston, MA 02215 (etaccone{at}bidmc.harvard.edu).
 
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Abstract

A systematic review of the English-language literature was performed to determine the overall benefit of mupirocin therapy in reducing the rate of Staphylococcus aureus infection among patients undergoing hemodialysis (HD) or peritoneal dialysis (PD). Included studies met the following criteria: they were randomized clinical trials or cohort studies; cohorts consisted of adults (age, ⩾18 years) requiring HD or PD; mupirocin therapy was administered to the treatment group, and placebo or no therapy was administered to the control group; and the primary outcome of interest was the difference in the number of S. aureus infections among mupirocin-treated and -untreated patients. Ten studies described in 9 articles were analyzed. A total of 2445 patients were included in the analysis. Use of mupirocin reduced the rate of S. aureus infections by 68% (95% confidence interval [CI], 57%–76%) among all patients undergoing dialysis; risk reductions were 80% (95% CI, 65%–89%) among patients undergoing HD and 63% (95% CI, 50%–73%) among patients undergoing PD. When data were stratified by type of infection, S. aureus bacteremia was found to be reduced by 78% among patients undergoing HD, and peritonitis and exit-site infections were found to be reduced by 66% and 62%, respectively, among patients undergoing PD. Mupirocin prophylaxis substantially reduces the rate of S. aureus infection in the dialysis population. Optimal regimens that minimize the emergence of mupirocin resistance need to be explored.

Infections are the second most common cause of death among patients requiring renal replacement therapy and contribute to >300 hospitalizations per 1000 patient-years [1]. Staphylococcus aureus is implicated in the majority of these infections, with mortality rates approaching 25% [2, 3]. The emergence and rapid spread of S. aureus strains that are resistant to multiple antibiotics has limited the therapeutic options available to treat these infections [2]. In the year 2000, 71% of dialysis units reported having ⩾1 patient with an infection caused by a methicillin-resistant S. aureus (MRSA) isolate [4]. Of even more concern are the recent reports of recovery of S. aureus isolates that are resistant to vancomycin and linezolid from patients undergoing long-term hemodialysis [5, 6]. Therefore, prevention of S. aureus infection is of paramount importance in this patient population.

Colonization with S. aureus is a necessary prerequisite for subsequent infection [7]. Mupirocin is a topical antibacterial ointment with demonstrated benefit in eradicating colonization with S. aureus [8–10]. Its efficacy for preventing S. aureus infection, however, remains controversial, especially for prevention of postoperative S. aureus infection [10–13]. There are also concerns about the emergence of mupirocin resistance among S. aureus isolates [14]. These factors may explain the lack of a general consensus on the role of mupirocin therapy in clinical practice.

Numerous studies evaluating the efficacy of intranasal or cutaneous mupirocin in the dialysis population have been performed [15–29]. The majority of studies demonstrate a risk reduction in the rate of S. aureus bacteremia among mupirocin-treated patients, although the magnitude of effect varies considerably among different studies. Trials that address the efficacy of mupirocin for prevention of S. aureus exit-site infections or peritonitis, however, have conflicting conclusions [17, 18]. Discordant results among published studies and varying estimates of the risk reduction may be due to differences in study design and patient population, including type of dialysis modality, mupirocin regimen, or type and definition of infection. Studies that did not show that mupirocin therapy was beneficial might also have been limited by sample sizes that were too small for detection of a statistically significant difference among treated and untreated groups.

Therefore, a systematic review of the English-language literature was performed to determine the overall benefit of mupirocin therapy in reducing the rate of S. aureus infection among patients requiring chronic hemodialysis (HD) and peritoneal dialysis (PD). By combining the results of different studies into a single meta-analysis, improvement in the estimates of the size of the effect of mupirocin and an increase in the statistical power for primary end point and subgroup analysis, including different dialysis modalities, mupirocin regimens, and types of S. aureus infections (peritonitis or bacteremia), could be achieved.

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Methods

Literature search. Published human studies of the efficacy of mupirocin for prevention of S. aureus infection in the dialysis population were identified through computerized literature searches using MEDLINE, the Science Citation Index, and the Cochrane Database and by reviewing the references of retrieved articles. Index search terms included the medical subject heading terms “dialysis,” “mupirocin,” “bactroban,” and "Staphylococcus aureus." The search was restricted to English-language trials published from January 1980, when mupirocin became available for clinical use, through June 2002. No attempt was made to obtain information about unpublished studies. Reviewed articles were maintained in a master log, and any reason for exclusion from analysis was documented in the rejection log.

Inclusion and exclusion criteria. The following criteria were used in selecting studies for inclusion: (1) the study population consisted of adults (age, ⩾18 years) requiring HD or PD; (2) the study was a randomized, controlled clinical trial (RCT) or a cohort study; (3) mupirocin therapy was administered to the treatment group, and placebo or no therapy was administered to the control group; and (4) the primary outcome was a difference in the rate of S. aureus infection (bacteremia, exit-site infection, or peritonitis) among mupirocin-treated and -untreated patients undergoing dialysis. Studies comparing the efficacy of mupirocin with that of other antibiotics were excluded. Reviews, letters, editorials, abstracts, and case reports were also excluded.

Data extraction. Extraction of data was performed independently by 3 investigators (E.T., M.G.F., and G.F.). Relevant abstracts were identified, and manuscripts were reviewed in detail if they could not be excluded on the basis of an abstract review. Each investigator was blinded to the other investigators' data extraction. Data from each trial were entered onto standardized forms, verified for consistency and accuracy, and entered into a computerized database. Information abstracted included year of publication, location of trial, study design, number of patients enrolled, population characteristics (age, sex, and percentage of nasal carriers of S. aureus), dialysis modality (HD or PD), intervention (dosage, frequency, duration, and site of application of mupirocin), and duration of follow-up. The quality of the RCTs was determined using Jadad's quality assessment score [30].

The outcomes abstracted were the number of exit-site infections, cases of peritonitis, and cases of bacteremia caused by S. aureus in treated and untreated patients. The criteria for each of these outcomes were those used in each individual trial. Discrepancies in data extraction were identified, and resolution required consent from all reviewers. Potential heterogeneity between studies was evaluated for type of study design (historical controls vs. randomized controls); type of dialysis modality (HD vs. PD); treatment arms (administration of mupirocin only to patients who were nasal carriers of S. aureus vs. administration of mupirocin to all patients); dosage, duration, and site of application of mupirocin; and duration of follow-up.

Statistical analysis. The principal measures of effect were the number of S. aureus infections among mupirocin-treated and -untreated populations and the corresponding incidence rates of infection. These results were combined and analyzed by calculating the relative risk (RR) and computed summary estimates with 95% CIs.

Analysis was performed using the DerSimonian and Laird random effects model [31]. We applied this model to all of the studies and, separately, to stratified subsets of trials for which the population type (patients undergoing HD vs. those undergoing PD) and type of infection (exit-site infection, bacteremia, and peritonitis) defined the stratification.

The Q test of homogeneity (heterogeneity) was calculated using the inverse-variance weights method [31]. For each outcome, publication bias (i.e., zero effect studies have a smaller chance of being published than do statistically significant studies) was assessed by the Begg funnel plot [32] and the Egger test [33]. The test for homogeneity assessed whether the distribution of the effect sizes was compatible with the assumption that interstudy differences were attributable to random sampling alone. We considered heterogeneity to be statistically significant if P < .10.

The effects of predictor variables on outcome were evaluated by meta-regression analysis on the basis of a general, linear-measures modeling procedure for least squares means. Variables that were potentially associated with mupirocin efficacy on the basis of the literature review and data availability served as covariates to the regression model. We analyzed 5 covariates: study design (RCT vs. cohort study), prevalence of S. aureus infection in the control group, drug regimen (intranasal vs. exit-site application; maintenance therapy vs. not maintenance therapy), and duration of follow-up. All reported P values were 2-tailed. A P value of <.05 was considered to be statistically significant. All statistical analysis for the meta-analysis was performed using Intercooled Stata, version 7.0 (Stata Statistical Software).

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Results

Study selection. Literature searches identified 70 studies. The review of references did not disclose any papers beyond the databases search. Thirteen articles [17–29] met the inclusion criteria. Four articles [21–23, 27] were subsequently excluded: 2 studies [23, 27] provided data presented in other articles, 1 trial [22] did not report data for the control population, and 1 trial [21] did not include the duration of follow-up. For the 2 latter studies, the authors could not provide further information because the primary outcome was different from the topic of this meta-analysis [22] or could not be contacted [21]. Both of these studies, however, reported a statistically significant reduction in the rate of S. aureus infection among mupirocin-treated patients (figure 1).

Figure 1
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Figure 1

Flow chart depicting the selection process for studies included in the meta-analysis. CTs, cohort trials; RCTs, randomized controlled trials.

Among the 9 articles included in the meta-analysis, 1 study [24] provided data from 2 different clinical trials. Thus, a total of 10 clinical studies were evaluated, with 1212 patients in the treatment groups and 1233 in the control groups. A total of 1468 patients required PD, and 977 required HD.

Study characteristics. Descriptive summary results for each study are reported in table 1. Of the 10 studies, 3 [19, 25, 28] were RCTs that used prospective controls; 2 of these studies [19, 28] were blinded. All RCTs were of medium-high methodologic quality, according to Jadad's quality score [30]. The remaining 7 trials [17, 18, 20, 24–26, 29] were prospective, nonrandomized cohort studies. These studies enrolled consecutive patients receiving mupirocin and historical control subjects (i.e., patients from the same department before mupirocin began to be used and who did not receive any prophylaxis). One trial [20] performed an intent-to-treat analysis. Six studies [17–19, 24, 29] included patients undergoing PD, and 4 [20, 25, 26, 28] included patients undergoing HD. Five studies [17–20, 26, 28] were performed in Europe, 2 [24] were performed in Canada, 2 [18, 29] were performed in the United States, and 1 [25] was performed in Brazil.

Figure 2
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Figure 2

Risk ratios and 95% CIs for mupirocin versus placebo or no prophylaxis in clinical trials of prevention of Staphylococcus aureus infection in the dialysis population.

Figure 3
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Figure 3

Risk ratios and 95% CIs for mupirocin versus placebo or no prophylaxis in clinical trials of prevention of Staphylococcus aureus bacteremia, exit-site infection, and peritonitis in the dialysis population.

Figure 4
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Figure 4

Funnel plot with pseudo 95% CIs of 9 studies included in the meta-analysis. Horizontal line, fixed-effect summary estimate (determined using inverse-variance weighting); sloping lines, expected 95% CIs for a given SE, assuming no heterogeneity between the studies.

Table 1
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Table 1

Characteristics of studies comparing mupirocin prophylaxis with no prophylaxis in dialysis populations.

Six studies [17–20, 26, 28] restricted the enrollment to patients with S. aureus nasal colonization; the remaining 4 trials [24, 25, 29] included all patients, regardless of S. aureus colonization status. One study [20] excluded patients who were colonized with MRSA or tobramycin-resistant S. aureus, because there were different treatment protocols for antimicrobial-resistant isolates at the study institution. Other studies excluded patients who received antibiotics in the month before enrollment [19, 24] or who had diabetes mellitus or tuberculosis [24]. The site, frequency, and duration of mupirocin treatment differed among the studies. In 6 studies [17–20, 26, 28], mupirocin was applied to the anterior nares 2–3 times daily for 5–14 days. Maintenance mupirocin therapy differed among these 6 studies: in 3 studies [20, 26, 28], mupirocin was readministered 1–3 times weekly for the duration of the study period; in 1 study [18], the baseline treatment regimen (3 times daily for 5 days) was repeated for 3 months; in 1 study [19], the baseline treatment was repeated every 4 weeks; and in 1 study [17], mupirocin was readministered only if additional nasal cultures revealed the presence of S. aureus. In the remaining 4 studies (1 of which [25] involved patients undergoing HD and 3 [24, 29] of which involved patients undergoing PD), mupirocin was applied to the catheter exit site.

The average duration of follow-up for mupirocin-treated and -untreated patients was 10.68 months (range, 5.4–15.6 months) and 11.45 months (range, 4.3–19.7 months), respectively (P = .57; table 1). In 1 study [18] in which the number of S. aureus infections was reported as episodes per person-year, the total number of infections in treated and untreated patients was obtained by multiplying the incidence rate by the duration of follow-up. The overall prevalence of S. aureus infection in the combined control groups was 0.08–2.17 cases per person-year for bacteremia, 0.11–0.25 cases per person-year for peritonitis, and 0.11–9.51 cases per person-year for exit-site infection.

S. aureus infections in the dialysis population. Using the random-effects model, the summary RR of mupirocin versus placebo or no prophylaxis for S. aureus infections among all dialysis patients was 0.32 (95% CI, 0.24–0.43; P < .001; figure 2). The test result for heterogeneity across the studies was not statistically significant (Q = 14.71; P = .10).

Analysis of dialysis modality. The type of dialysis modality was analyzed separately. For studies that included only patients undergoing HD, the summary RR for all types of S. aureus infection was 0.20 (95% CI, 0.11–0.35; P < .001), with no evidence of heterogeneity (Q = 0.74; P = .86) (figure 2). When bacteremia was analyzed separately among patients undergoing HD, there was a statistically significant reduction in the number of cases in the mupirocin-treated population (summary RR, 0.22; 95% CI, 0.11–0.42; P < .001) (figure 3). Only 2 studies [25, 29] reported the number of exit-site infection infections among patients undergoing HD (summary RR, 0.19; 95% CI, 0.06–0.56; P = .003). The result of the test for heterogeneity was not statistically significant for either analysis (P > .5 for each).

Among patients undergoing PD, mupirocin therapy significantly reduced the number of all S. aureus infections, including peritonitis and exit-site infections (summary RR, 0.37; 95% CI, 0.27–0.50; P < .001), with no evidence of heterogeneity (Q = 9.09; P = .10) (figure 2). When S. aureus peritonitis and exit-site infection were analyzed separately, mupirocin prophylaxis demonstrated a risk reduction for each (RR for peritonitis, 0.34 [95% CI, 0.20–0.57; P < .001]; RR for exit-site infection, 0.38 [95% CI, 0.22–0.67; P < .001]). Tests for heterogeneity demonstrated a statistically significant Q value for the exit-site infection subgroup (Q = 9.96; P = .04) and the peritonitis subgroup (Q = 11.14; P = .05).

Publication bias. The Begg funnel plot of studies included in the meta-analysis is shown in figure 4. There was no evidence of publication bias demonstrated using either the Begg test (rank correlation method; P = 0.85) or the Egger test (weighted regression; P = .53).

Meta-regression. Factors that might explain the observed correlations between treatment effects and outcome were analyzed. Study design, maintenance versus intermittent mupirocin therapy, site of application (nasal vs. exit site), duration of follow-up, location of study, and prevalence of S. aureus infection among control subjects were taken into account to explain heterogeneity using a meta-regression analysis. For exit-site infection, only the duration of follow-up differed between case and control subjects, with a shorter duration of follow-up among treated patients who did not develop an exit-site infection (P = .009). There were no statistically significant differences in factors analyzed in the meta-regression between patients with peritonitis and control subjects.

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Discussion

This systematic review of the literature quantified the benefit of topical mupirocin therapy in preventing S. aureus infections among both patients undergoing HD and those undergoing PD. Overall, mupirocin therapy reduced the risk of developing S. aureus infection by 68% among all patients undergoing dialysis. In a subgroup analysis of different dialysis modalities, the risk reduction was 80% for patients undergoing HD and 63% for those undergoing PD. Analysis of different types of S. aureus infections, including exit-site infection, peritonitis, and bacteremia, demonstrated significant rate reductions among patients receiving mupirocin therapy. Use of maintenance versus single-application mupirocin regimens, or mupirocin treatment of all patients versus treatment of only those with S. aureus nasal colonization did not confound these findings. These pooled estimates suggest that mupirocin prophylaxis substantially reduces the likelihood of developing an S. aureus infection in this patient population.

Several studies have also demonstrated that mupirocin prophylaxis is cost-effective in the dialysis population, with substantial reductions in health care expenditures. Bloom et al. [15] showed that both weekly mupirocin therapy for all patients undergoing dialysis and mupirocin therapy given every 3 months targeted only to patients with S. aureus nasal colonization can result in annual savings ranging from $748,000 to more than $1,000,000 per 1000 patients undergoing HD. Despite the substantial benefit of mupirocin in preventing S. aureus infections and its cost-effectiveness, prophylactic mupirocin administration in the dialysis population is not a widely accepted practice. Concern about the emergence of mupirocin resistance may be the main factor that limits its use [34, 35]. In a 625-bed teaching hospital, a marked increase in the point prevalence of MRSA infection among inpatients led to widespread mupirocin administration to all hospitalized patients in 1992 [14]. This intervention led to a rapid increase in mupirocin resistance, from 2.7% of MRSA isolates in 1990 to 65% in 1993 [14].

There are several limitations to this meta-analysis. First, because of an insufficient number of randomized, double-blind, controlled studies, other study designs were included in this analysis. A majority of these studies used historical controls and may have introduced bias. However, the marked risk reduction and the consistent beneficial results from the majority of studies strengthen the summary results of this meta-analysis. Second, the type and duration of hemodialysis access was not provided in the majority of studies. Thus, differences among case and control subjects for this potential risk factor for S. aureus bacteremia or exit-site infection could not be assessed. Third, the risk reduction for bacteremia among patients undergoing PD was not assessed, because there was a lack of studies to have addressed this outcome and that met our inclusion criteria. Fourth, trials that did not show that mupirocin prophylaxis had a benefit in decreasing the number of S. aureus infections may not have been published, thereby biasing the results towards a beneficial effect of mupirocin prophylaxis. However, standardized methods to identify the presence of publication bias were used, and the results were not significant. Last, heterogeneity was detected in subgroup analysis of both exit-site infections and peritonitis among patients undergoing PD. The meta-regression showed that heterogeneity in the analysis of exit-site infections was significantly associated with a shorter duration of follow-up among treated patients. This difference may have led to an overestimation of the benefit of mupirocin therapy in this situation, because late infections that occur after the follow-up period may not have been detected. The heterogeneity detected for the peritonitis subgroup could not be explained by the meta-regression analysis, because no variables differed significantly between case and control subjects, including type and frequency of mupirocin regimen, duration of follow-up, type of study design, and prevalence of S. aureus infection among control subjects. Despite the heterogeneity between studies, however, 5 of the 6 studies demonstrated a risk reduction in the prevalence of S. aureus infection with the use of mupirocin prophylaxis.

The great majority of studies published to date have demonstrated a benefit of mupirocin prophylaxis in reducing the rate of S. aureus infection in the dialysis population, including a recent literature synthesis focusing on the PD population [36]. The present meta-analysis further strengthens and quantifies this benefit by systematically combining the results of these studies. Nevertheless, the optimal strategy for using this topical antimicrobial and minimizing the emergence of resistance is still unclear. Because patients often become recolonized with S. aureus after receiving an initial treatment regimen, periodic screening with application of mupirocin among carriers seems to be a reasonable option. This strategy would target mupirocin to high-risk patients and limit any unnecessary use, thereby decreasing the emergence of resistance. Meticulous attention to infection-control practices during insertion and access of dialysis catheters is also of paramount importance in preventing S. aureus infection. Ultimately, future longitudinal studies need to define a mupirocin regimen that balances a reduction in the incidence of S. aureus infection with concerns about the emergence of mupirocin resistance.

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Acknowledgments

We are grateful to Michael A. Stoto for his assistance in the statistical analysis in this study.

  • Received May 5, 2003.
  • Accepted August 11, 2003.
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  1. Clin Infect Dis. (2003) 37 (12): 1629-1638. doi: 10.1086/379715
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