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Eradication of Methicillin-Resistant Staphylococcus aureus Carriage: A Systematic Review

  1. Heidi S. M. Ammerlaan1,
  2. Jan A. J. W. Kluytmans3,4,
  3. Heiman F. L. Wertheim5,6,
  4. Jan L. Nouwen5, and
  5. Marc J. M. Bonten1,2
  1. 1Department of Medical Microbiology, University Medical Centre Utrecht, Amsterdam
  2. 2Julius Center for Health Sciences and Primary Care, Utrecht
  3. 3Department of Medical Microbiology and Infection Control, VU University Medical Center, Amsterdam
  4. 4Laboratory for Microbiology and Infection Control, Amphia Hospital Breda, Breda
  5. 5Department of Medical Microbiology and Infectious Diseases, Erasmus Medical Centre, Rotterdam, The Netherlands
  6. 6Oxford University Clinical Research Unit, National Institute of Infectious and Tropical Diseases, Bach Mai Hospital, Hanoi, Vietnam
  1. Reprints or correspondence: Dr. H. S. M. Ammerlaan, Heidelberglaan 100, 3584 CX Utrecht, The Netherlands (H.Ammerlaan{at}umcutrecht.nl).
 
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Abstract

A systematic review was performed to determine the effectiveness of different approaches for eradicating methicillin-resistant Staphylococcus aureus carriage. Twenty-three clinical trials were selected that evaluated oral antibiotics (7 trials), topically applied antibiotics (12 trials), or both (4 trials). Because of clinical heterogeneity, quantitative analysis of all studies was deemed to be inappropriate, and exploratory subgroup analyses were performed for studies with similar study populations, methods, and targeted bacteria. The estimated pooled relative risk of treatment failure 1 week after short-term nasal mupirocin treatment, compared with placebo, was 0.10 (range, 0.07–0.14). There was low heterogeneity between study outcomes, and effects were similar for patients and healthy subjects, as well as in studies that included only methicillin-susceptible S. aureus carriers or both methicillin-susceptible S. aureus and methicillin-resistant S. aureus carriers. The development of drug resistance during treatment was reported in 1% and 9% of patients receiving mupirocin and oral antibiotics, respectively. Short-term nasal application of mupirocin is the most effective treatment for eradicating methicillin-resistant S. aureus carriage, with an estimated success of rate of 90% 1 week after treatment and ∼60% after a longer follow-up period.

Colonization is an important step in the pathogenesis of Staphylococcus aureus infection and is instrumental in the nosocomial epidemiology of these bacteria. Approximately 20% of the general population is persistently colonized with S. aureus, most frequently in the anterior nares, although other body sites, such as the perineum and throat, may also be colonized. Another 30% of the general population is intermittently colonized, and the remaining 50% appear not to be susceptible, for unknown reasons, to S. aureus carriage [1]. Methicillin-resistant S. aureus (MRSA) has become endemic in health care institutions worldwide, with up to 70% of invasive S. aureus infections having resistance [2–5], and most patients who develop drug-resistant S. aureus infection will have been colonized prior to infection. The half-life of MRSA carriage has been reported to be as long as 40 months in individuals who do not receive treatment [6].

Eradication of S. aureus carriage may serve 2 purposes: prevention of infection and prevention of transmission. Several eradication strategies have been evaluated, but studies have differed markedly in their design, study population, targeted bacteria (methicillin-susceptible S. aureus [MSSA] and/or MRSA), and duration of follow-up. Furthermore, guidelines and reviews have differed in their selection of studies (only those evaluating mupirocin [7] or excluding studies that involved MSSA [8–11] or health care workers [8]), or they have been narrative rather than systematic [7, 10–12].

Therefore, we performed a systematic review to determine the most effective approach for eradicating MRSA carriage. Importantly, the literature search was not restricted to studies that addressed eradication of MRSA alone but included studies evaluating MSSA eradication, provided that eradication was pursued with agents that had presumed antibacterial activity against MRSA.

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Methods

Data sources. We searched PubMed from 1966 through October 2008, Embase from 1966 through October 2008, and Web of Science from 1988 through October 2008 using the terms “Staphylococcus aureus,” “eradication,” “treatment,” “decolonization,” “decolonisation,” “elimination,” “carrier(s),” “carriage,” “carriership,” “colonization,” and “colonisation” to identify articles reporting on the effectiveness of treatment of MRSA or MSSA carriage. In addition, the bibliographies of selected articles were searched in an attempt to identify additional studies. We established inclusion and exclusion criteria before reviewing abstracts and articles.

Study selection and data extraction. Three independent reviewers (H.S.M.A., H.W., and J.N.) performed the search and screened titles and abstracts for relevant studies. The identified titles and abstracts were screened without blinding to authors and journal. Potentially relevant studies were obtained, and the full text was examined. Studies were included if they were written in English or Dutch and involved human subjects. Studies were excluded for the following reasons: (1) intervention with β-lactam antibiotics, (2) duration of follow-up <1 week, (3) no randomization, and (4) evaluation of treatment of MRSA infections without evaluation of the effect on carriage. For each study, the following characteristics were extracted: year of study, study design, study size, total number of patients in the treatment and control groups with corresponding success rates, study population, MRSA or MSSA carriage, culture sites, and length of follow-up. The validity of the included studies was assessed by determining the following criteria: generation of allocation sequence, reporting of baseline imbalances, blinding, and follow-up (we defined adequate follow-up as including 80% of study participants) [8].

Data synthesis and analysis. The meta-analysis was performed using Review manager software, version 4.2.8 (The Cochrane Collaboration). We used the random-effects model to calculate pooled relative risks (RR>p) of failure of treatment versus placebo or no treatment and 95% CIs, because this model best accounts for statistical heterogeneity between study results. The pooled RRs at end of treatment (if available) and at end of follow-up are presented. I-squares (I>2) are provided, which describe the percentage of variability in point estimates that is attributable to statistical heterogeneity rather than to sampling error and which are defined to be low (<25%), moderate (25%–75%), or high (>75%) [13]. Because of clinical heterogeneity among study populations, culture methods, culture sites, interventions, and durations of follow-up, a quantitative analysis of all included studies by means of a random-effects model was deemed to be inappropriate. Therefore, exploratory subgroup analyses were performed of studies with similar study populations (healthy volunteers [including health care workers] vs. patients), methods (effectivity determined by nasal cultures only vs. cultures of multiple body sites), and targeted bacteria (MSSA vs. MRSA and MSSA vs. MRSA and MSSA combined).

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Results

Selected studies. Initially, 2388 articles were identified in PubMed, 1161 were identified in Embase, and 876 were identified in the Web of Science. Of these, 342 articles met the inclusion criteria, 319 of which were excluded on the basis of the defined exclusion criteria (the most common reasons being missing data on the effect of treatment on carriage, a follow-up duration of <1 week, or no control group). Five studies were excluded because β-lactam antibiotics were evaluated. Twenty-three studies, all of which were published from March 1977 through October 2008, remained; they involved a total of 2114 subjects, 1831 of whom were evaluated until the end of the follow-up period, with a mean of 80 subjects per study (table 1) [14–36].

Table 1
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Table 1

Study characteristics of 23 selected studies.

Interventions. Different interventions were evaluated, including topically applied antimicrobial agents (mupirocin [17, 19, 21, 22, 25, 26, 28–30, 32, 34, 36], bacitracin nasal ointment [30], and tea tree oil [34]), systemic (orally administered) antibiotics (tetracyclines [24], fusidic acid [31], macrolides [14, 15, 33], ciprofloxacin [20], rifampin [20, 23, 24], and trimethoprim-sulfamethoxazole [20, 23]), and combinations of both [16, 18, 27, 35]. Interventions were most often used for 7 days (range, 3–14 days), with eradication rates determined for MSSA [14–19, 22, 25, 26, 29, 33], MRSA [20, 23, 24, 27, 28, 31, 34–36], or both [21, 30, 32].

Study quality. There was large variation in the methodological quality of included studies (tables 2 and 3; online only). The method of allocation was described in 12 studies only; there were no statistically significant differences in the baseline characteristics reported in 7 of these 12 studies [21, 23, 26, 28, 32, 35, 36], differences in baseline characteristics were not explicitly mentioned in 4 studies [18, 19, 33, 34], and there was a statistically significant difference in extranasal carriage between both study groups in 1 study [27]. Most studies were blinded. All studies that compared mupirocin with placebo were double-blinded [17, 19, 21, 25, 26, 28–30, 32, 36], as were 4 [14, 15, 23, 33] of 11 studies that compared systemic treatment with placebo or another treatment. One of these studies was single-blinded [20], and the remaining 6 studies were not blinded [16, 18, 24, 27, 31, 35]. Follow-up of >80% of study subjects was achieved in 16 studies; the percentage of subjects with follow-up could not be determined from the published data in 3 studies [22, 31, 33] and was <80% (range, 51%–77%) in 4 studies [18, 27, 32, 35].

Table 2 (online only)
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Table 2 (online only)

Efficacy of studied treatments.

Table 3 (online only)
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Table 3 (online only)

Adverse events and quality assessment of studies included in the review.

Populations studied. Different populations were studied, including healthy carriers [14, 15, 17, 22, 36], health care workers [16, 19, 21, 25, 26, 30], hospitalized patients and patients visiting outpatient clinics [18, 20, 28, 29, 31, 33–35], nursing home patients [24, 32], and health care workers and patients combined [23, 27].

Topical treatment. The efficacy of topical mupirocin was evaluated in 13 studies (table 1). Mupirocin was compared with placebo in 8 studies. In addition, mupirocin was compared with chlorhexidin-neomycin nasal ointment [22] and with fusidic acid nasal ointment combined with trimethoprim-sulfamethoxazole [27]. In 2 other studies, mupirocin was compared with bacitracin [30] and tea tree oil [34]. Chlorhexidin was part of the intervention in 3 studies; however, it was always administered to both groups, which allowed determination of the effect of mupirocin [22, 27, 28].

The effects of mupirocin, compared with placebo, on carriage 1 week after treatment could be quantified for 6 studies (total number of subjects studied, 626) (table 4) [17, 19, 21, 26, 29, 32]. The efficacy of mupirocin was comparable among studies that included only MSSA carriers or included both MRSA and MSSA carriers, and efficacy was also comparable among studies that included patients or healthy subjects. As a result, the estimated pooled RRs of treatment failure with mupirocin, based on these 6 studies, was 0.10 (range, 0.07–0.14; I>2, 0%). The absence of heterogeneity in outcomes, as represented by the low I>2 value, allowed us to conclude that mupirocin eradicates MRSA and MSSA carriage 11 times more effectively than no treatment, with successful eradication in 94% of carriers (424 of 453 carriers) 1 week after treatment.

Table 4
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Table 4

Pooled relative risks (RR>p) of treatment failure 1 week after treatment and at the end of the follow-up period.

The effects of mupirocin, compared with placebo, on carriage at the end of follow-up could be quantified for 8 studies (total number of subjects studied, 902) (table 4) [17, 19, 21, 25, 26, 28, 29, 32, 36]. The duration of follow-up ranged from 16 days through 365 days. In contrast with the results at 1 week of follow-up, there was considerable heterogeneity in the results of studies with longer follow-up periods, which reduced the accuracy of the effect size. In general, however, mupirocin appeared to be effective, with estimated pooled RRs of treatment failure of 0.44 (range, 0.39–0.50; I>2, 90.2%). Eradication had been successful in 65% (range, 25%–90%) of carriers (402 of 622 carriers) after a follow-up period of at least 14 days [17, 19, 21, 22, 25–30, 32, 34, 36]. Overall, the efficacy of mupirocin was comparable among studies that included only MSSA carriers and studies that included both MRSA and MSSA carriers (including the 2 studies that involved only patients with MRSA carriage), with pooled RRs at the end of follow-up of 0.52 (range, 0.43–0.64; I>2, 76.8%) [17, 19, 25, 26, 29] and 0.40 (range, 0.34–0.48; I>2, 95.6%) (data not shown) [21, 28, 32, 36], respectively. Efficacy of mupirocin nasal ointment appeared to be lower in studies that included multiple body sites for evaluation (pooled RRs, 0.60; range, 0.49–0.74; I>2, 92.3%) [25, 28, 32], compared with studies that only tested for nasal carriage (pooled RRs, 0.38; range, 0.32–0.45; I>2, 78.5%) (data not shown) [17, 19, 21, 26, 29, 36].

Acquisition of mupirocin resistance during treatment was reported in 3 studies [28, 32, 35] and was found in 6 (1%) of 714 total subjects evaluated in 12 studies [17, 19, 21, 22, 25–29, 32, 34–36]. Reported adverse events attributable to mupirocin use were mild and did not lead to discontinuation of therapy (table 3; online only).

Other topical agents were investigated less often. Bacitracin nasal ointment only eradicated carriage in 10 (29%) of 34 MRSA and MSSA carriers at 1 week after treatment (range, 13%–44%) [16, 30], and tea tree oil eliminated MRSA carriage in 46 (44%) of 110 carriers at 2 weeks after treatment [34]. Compared with mupirocin, estimated pooled RRs of treatment failure of bacitracin and tea tree oil at the end of treatment was 1.88 (range, 0.57–6.15; I>2, 79.9%) (data not shown). Fusidic acid nasal ointment and chlorhexidin washings have only been studied in combination with other topical or systemic medication, and the effectiveness of these components could not be determined.

Systemic treatment. The efficacy of oral antibiotics was evaluated in 11 studies (table 1). In all studies, eradication was evaluated for either MRSA or MSSA. Only 6 studies compared systemic treatment with receipt of placebo or no treatment; 3 of these studies involved patients [24, 31, 33], and 3 involved healthy subjects [14–16]. Of these 6 studies, 4 addressed MSSA carriage [14–16, 33], and 2 addressed MRSA carriage [24, 31]). The results were pooled in the random-effects model (table 4). Different regimens were compared in the other 5 studies. The overall pooled RRs of treatment failure of oral antibiotics, compared with placebo or no treatment, was 0.47 (range, 0.39–0.57; I>2, 3.2%) 1 week after treatment [14–16, 24, 31] and 0.54 (range, 0.33–0.87; I>2, 91.9%) at the end of the follow-up period [14–16, 24, 31, 33]. The high level of heterogeneity in the second analysis, however, indicates that the effect estimate should be interpreted with caution. Efficacies at the end of the follow-up period appeared to be comparable in studies that included only MSSA carriers [14–16, 33] or only MRSA carriers [24, 31]. In contrast with the results of mupirocin studies, the efficacy of systemic treatment, when compared with that of placebo or no treatment, was not higher in studies that determined eradication by means of nasal cultures only (pooled RRs, 0.74; range, 0.65–0.85; I>2, 57.9%) [14–16], compared with those using cultures samples from multiple body sites (pooled RRs, 0.40; range, 0.11–1.42; I>2, 90.3%) (data not shown) [24, 31, 33].

More specifically, trimethoprim-sulfamethoxazole in combination with rifampin or nasal fusidic acid eradicated MRSA carriage in 48 (62%) of 78 subjects (range, 40%–95%) in 3 studies [20, 23, 27]. Of the macrolides, monotherapy with clarithromycin reduced nasal MSSA carriage in 43 (88%) of 49 subjects at the end of 8 weeks of follow-up, but it was also associated with a rapid and prolonged increase in macrolide resistance in oropharyngeal nonstaphylococcal flora [33]. Combined treatment with doxycycline, rifampin, mupirocin, and chlorhexidin was associated with MRSA eradication in 64 (74%) of 87 patients after 3 months, with >50% of patients being MRSA free up to 8 months later [35]. In 1 study, ciprofloxacin was compared with trimethoprim-sulfamethoxazole (with rifampin added to the treatment regimen in both study groups), but this randomized trial was terminated prematurely because of clonal spread of a ciprofloxacin-resistant MRSA strain in the hospital [20]. Rifampin as part of combination therapy with other oral and/or topical antibiotics was associated with eradication of MRSA in 138 (62%) of 221 carriers (after a follow-up period of at least 14 days) [20, 23, 24, 35]. Acquisition of resistance to the oral antibiotics used for eradicating MSSA and MRSA carriage was reported in 5 studies [18, 20, 23, 24, 31], in 39 (9%) of 443 total subjects evaluated in 10 studies [14–16, 18, 20, 23, 24, 27, 31, 35]; acquisition of resistance was especially common among patients who received fusidic acid and rifampin monotherapy [18, 24, 31]. Reported adverse events were mild and led to discontinuation of therapy in 4 patients in 2 studies (table 3; online only) [20, 23].

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Discussion

Short-term (4–7 days in duration) topical nasal application of mupirocin is the most effective treatment for eradicating MRSA, with an estimated success probability of ∼90% 1 week after treatment and ∼60% after a longer follow-up period, ranging from 14 days through 365 days in different studies. The reported effectiveness of mupirocin is comparable amogn MSSA carriers and MRSA carriers, but it is higher among healthy carriers than among patients. Estimated successful eradication with oral antibiotics was achieved in ∼60% of subjects 1 week after treatment and in ∼50% of subjects after longer follow-up periods. For oral antibiotics, the reported effectiveness was comparable among MRSA carriers and MSSA carriers and among patients and healthy carriers. Of note, MSSA eradication efficacy at the end of follow-up was higher in the 1 study that involved patients [33] than it was in the 3 studies with healthy carriers [14–16]. No explanation could be found for this difference.

To include as much of the available evidence as possible, we decided not to restrict our literature search to studies of the eradication of MRSA alone but to also include studies that evaluated MSSA carriage, under the assumption that MSSA carriage has a similar response to eradication therapy if agents with activity against both MRSA and MSSA are used. On the basis of the fact that mupirocin has a similar effect on both pathogens, as indicated by our analyses, there is no reason to reject this assumption for studies that involve mupirocin. This increases the size of the included population from 718 subjects for studies including MRSA carriers alone to 2036 subjects in the current analysis. The analyses of oral antibiotics yielded similar results, although heterogeneity across studies was higher and reduced the accuracy of the effect sizes obtained.

MRSA frequently colonizes extranasal sites (e.g., throat and perineum) [6, 37, 38], which reduces the effectiveness of topical (intranasal) mupirocin treatment, as the findings of our study suggest. The estimated risk of eradication failure increased from 0.38 to 0.60 for studies that evaluated nasal colonization alone and studies that evaluated colonization of additional body sites, respectively. However, such reduced effectiveness was not found for systemic treatment. For these agents, the risk of eradication failure was actually higher in studies that evaluated nasal colonization alone (pooled RRs, 0.74), compared with studies that also evaluated extranasal sites (pooled RRs, 0.43), although the 95% CI of the latter estimate ranged from 0.14 through 1.27. In fact, reported determinants in patients who experience failure of MRSA eradication by topical treatment (mupirocin treatment, in particular) are skin lesions (e.g., wounds and eczema) [22, 23, 28] and mupirocin resistance [28, 35].

Mupirocin effectiveness decreased with a prolonged follow-up period. There are 3 biological explanations for this difference in effectiveness related to the duration of follow-up. First, this estimate was affected by the results of the 1 study that included only hospitalized MRSA carriers (98 subjects) and that failed to demonstrate a beneficial effect of mupirocin therapy [28]. Compared with patients in the other studies, patients in this study had a higher risk of comorbidity, were more likely to have multiple body sites evaluated, and had a higher risk of having a mupirocin-resistant strain at the start of treatment (found in 23 [24%] of 98 subjects). Second, a longer duration of follow-up after a short course of treatment increases the risk of recolonization from other sources, such as other patients, which may be especially relevant in hospitalized populations. Third, recolonization may also result if mupirocin therapy suppresses bacterial density, rather than completely eradicating carriage.

On the basis of the available evidence in this systematic review, intranasal administration of mupirocin ointment seems to be safe and is associated with a 1% risk of acquiring a drug-resistant strain during treatment. Recent surveillance studies, however, have reported mupirocin-resistant MRSA strains in up to 13% of patients in institutions that do not practice routine use of mupirocin and in up to 65% of patients in areas with widespread mupirocin use [39]. In such settings, tea tree oil might be an alternative treatment, because it was found to be as effective as mupirocin in 1 study [34].

Short-term nasal eradication therapy with mupirocin is highly effective during the period immediately after it is administered and would serve the purpose of presurgical eradication, as has been suggested for presurgical eradication of MSSA carriage [40]. Furthermore, because the duration of hospital stay is <1 week for most patients, such an approach would also reduce the potential burden of transmission if it was applied to control disease spread. These findings corroborate the beneficial results of rapid detection of MRSA carriage and subsequent mupirocin treatment [41]. In patients with factors that are associated with treatment failure (e.g., skin lesions, mupirocin-resistant strains, and positive results of cultures from extra-nasal sites), systemic eradication treatment (e.g., rifampin administered in combination with another oral antibiotic), in addition to mupirocin nasal ointment, is the treatment of choice.

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Acknowledgments

Financial support. The Netherlands Organization of Scientific Research (VICI NOW 918.76.611 to M.J.M.B.).

Potential conflicts of interest. M.J.M.B. has received research funding from Novartis and 3M, is a member of the speakers' bureau for Pfizer, and is a member of the advisory boards of 3M and Novartis. J.L.N. is a member of the advisory board of GlaxoSmithKline. J.A.J.W.K. has received consulting fees from 3M, Novabay, and Wyeth and has received honoraria from 3M and Becton Dickenson for lectures. H.S.M.A. and H.F.L.W.: no conflicts.

  • Received August 13, 2008.
  • Accepted November 27, 2008.
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  1. Clin Infect Dis. (2009) 48 (7): 922-930. doi: 10.1086/597291
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