JAC Advance Access originally published online on November 6, 2007
Journal of Antimicrobial Chemotherapy 2008 61(1):26-38; doi:10.1093/jac/dkm416
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Systematic review |
Does antibiotic exposure increase the risk of methicillin-resistant Staphylococcus aureus (MRSA) isolation? A systematic review and meta-analysis
Department of Infectious Diseases, Catholic University, Rome, Italy
* Corresponding author. Tel: +39-06-30155527; Fax: +39-06-3054519; E-mail: etacconelli{at}rm.unicatt.it
Received 23 July 2007; returned 4 October 2007; revised 23 August 2007; accepted 8 October 2007
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Abstract |
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Background: Current evidence does not provide a clear definition of the association between methicillin-resistant Staphylococcus aureus (MRSA) isolation and previous antibiotic use. A systematic review was performed to determine whether antibiotic exposure is a risk factor for the isolation of MRSA.
Methods: MEDLINE and EMBASE databases were searched to identify studies published between 1976 and 2007 on the role of antibiotics as a risk factor for MRSA isolation in adult patients. The outcome of interest was MRSA isolation. Summary statistics were risk ratios (RR) comparing MRSA-positive patients to those without S. aureus isolation or with methicillin-susceptible S. aureus isolation.
Results: Seventy-six studies, including a total of 24 230 patients, met the inclusion criteria. Antibiotic exposure was determined in the 126 ± 184 (mean ± SD) days preceding MRSA isolation. The risk of acquiring MRSA was increased by 1.8-fold [95% confidence interval (CI), 1.7–1.9; P < 0.001] in patients who had taken antibiotics. The RR for single classes of antibiotics was 3 (95% CI, 2.5–3.5) for quinolones, 2.9 (95% CI, 2.4–3.5) for glycopeptides, 2.2 (95% CI, 1.7–2.9) for cephalosporins and 1.9 (95% CI, 1.7–2.2) for other β-lactams. Significant heterogeneity was detected among studies. A regression analysis revealed that the heterogeneity was linked to the length of time in which antibiotic exposure was detected before MRSA isolation (more or less than 180 days).
Conclusions: This meta-analysis shows a clear association between exposure to antibiotics and MRSA isolation. This information may be useful for researchers in designing future studies and for policy decision-making on the appropriate management of antibiotic therapies.
Keywords: antibiotic resistance , Gram-positive , antimicrobials
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Introduction |
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Nosocomial infections pose a significant threat to patients worldwide. Zhan and Miller1 reported excess mortality of 4% for infections due to medical care and 23% of mortality due to post-operative septicaemia. Antibiotic-resistant bacteria cause the majority of these nosocomial infection-related deaths. In 2005, the European Antimicrobial Resistance Surveillance System, a wide network of national surveillance systems, observed percentages of methicillin resistance ranging from no observation in Iceland to 60% of Staphylococcus aureus strains in Romania.2 In the same year, data from The Surveillance Network-USA (TSN), an electronic surveillance network that collects microbiology data from 300 clinical microbiology laboratories across the USA, reported that methicillin-resistant S. aureus (MRSA) rates were 59%, 55% and 48% for strains from non-intensive care unit (ICU) inpatients, ICU and outpatients, respectively.3
The epidemiology of nosocomial acquisition of MRSA is well described in numerous studies.4,5 Risk factors include the use of antimicrobials, underlying diseases, prior hospitalization, surgery, duration of hospitalization, central venous catheterization and endotracheal intubation, enteral feeding, admission to ICU, nursing staff workload and compliance with hand disinfection procedures.4–6 A 1 year study, carried out in an ICU, showed that urgent admission, values of APACHE II score at 24 h, bronchoscopy and days of staff deficit were all independent risk factors for nosocomial MRSA acquisition. Fitting a simple stochastic model, staff deficit was the only factor that was significantly associated with cross-transmission. It was predicted that a 12% improvement in adherence to hand hygiene might have compensated for staff shortage and prevented transmission during periods of overcrowding, shared care and high workload.5 The risk for patients, in terms of nosocomial transmission of MRSA, also seems to be significantly influenced by the proportion of patients with colonization at ICU admission, regardless of the size of the ICU.7
Previous antibiotic use is frequently reported as a risk factor for MRSA isolation. A recent review by Monnet8 underlined the importance of a dose–effect association, supporting a causal relationship between MRSA and antimicrobial drug use. Crossley et al.9 and Hershow et al.10 reported that patients with MRSA infections had a significantly longer hospitalization before infection and were more likely to have received antimicrobial therapy. Studies that analysed antimicrobial classes separately often identified both cephalosporins and fluoroquinolones as risk factors for MRSA.11 Our group documented that the use of quinolones was an independent risk factor for the development of healthcare-associated MRSA bacteraemia.12 Quinolone use was a risk factor for MRSA, but not for methicillin-susceptible S. aureus (MSSA).13 However, several studies could not find a significant association between MRSA isolation and previous use of antibiotics.14,15
The purpose of this meta-analysis is to provide information on the strength of the association between antibiotic exposure and MRSA isolation in adult subjects and to explore any underlying sources of heterogeneity including place of acquisition (hospital/long-term care facilities versus community), definition of cases (infected versus colonized) and classes of antibiotics.
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Materials and methods |
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Article identification
Studies conducted on humans concerning the role of antimicrobial therapy as a risk factor for MRSA colonization or infection were identified through computerized literature searches using free text searching, MEDLINE (National Library of Medicine Bethesda MD) and EMBASE and by reviewing the references of the retrieved articles. Index search terms included the Medical Subjects Heading ‘methicillin-resistant Staphylococcus aureus’ or ‘risk factor’ or ‘resistance’ or ‘antimicrobial therapy’ or ‘antibiotic therapy’. The search was restricted to full articles published from December 1976 (publication date of the first study identified by the research) to June 2007. No language restriction was applied. No attempt was made to obtain information on unpublished studies. Reviewed articles were maintained in a master log, and any reason for exclusion from analysis was documented in the rejected log.
Inclusion and exclusion criteria
Studies were considered eligible if they included adult patients (>16 years of age) and if they presented data pertaining to the relationship between antibiotic use and MRSA colonization or infection. Reviews, letters, editorials and case reports were excluded.
Extraction of data was performed independently by two investigators (G. D. A. and E. P.). Each investigator was blinded to the other investigator's data extraction. In the case of disagreement between the two reviewers, a third reviewer was consulted (E. T.). Data from each trial were entered into standardized forms, verified for consistency and accuracy, and entered into a computerized database. Abstracted information included author, year of study and publication, country where the study was conducted, study design, sampling frame for inclusion (population-based, hospital-based or mixed), definition of cases (colonized versus infected) and of controls (MSSA-positive or S. aureus-negative), number of patients enrolled, population characteristics (age, presence of underlying illness and presence of central catheter), previous antimicrobial treatment and, if specified, class of antibiotic used. Data were extrapolated from tables when not available in the text. Primary outcome was the number of patients who underwent previous antibiotic therapy among patients with MRSA colonization or infection and among controls. If a study had two control groups (i.e. MSSA-positive and S. aureus-negative), data were extrapolated from the S. aureus-negative group.16
A systematic review was conducted by combining and analysing the risk ratio (RR) and computing a summary RR of the effects with 95% confidence interval (95% CI). The analysis was performed using the inverse variance fixed effects method as fixed and random models computed the same overall estimate and 95% CI, showing the absence of ‘extra’ variability across combined studies. We explored potential sources of heterogeneity through subgroup and sensitivity analyses. The subgroup analysis was performed through meta-regression, which tests whether trial attributes are associated with the study results. The subgroup analysis was performed by stratifying sampling frame for inclusion, definition of case subjects and controls, study design, geographic area of the study, presence of adjustment of covariates and length of time in which antibiotic exposure was detected. The Q statistic for homogeneity and the I2 test were calculated to assess whether results varied no more than might have been expected by the play of chance (random sampling). The Q statistic was compared with the 
2 distribution with k–1 DF, where k was the number of studies. A significant hetergeneity was considered for P < 0.10 and I2 > 50%. The small study bias was measured by Begg's funnel plot17 and by the Egger test.18
Analysis was performed using the software program Intercooled Stata (Stata Statistical Software; release 8.0, College Station, TX, USA).
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Results |
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Literature search identified 665 studies. Two hundred and four abstracts were read and excluded because they reported paediatric cases or because they were single case reports, reviews or letters. Three hundred and fifty-seven articles were read and excluded because studies did not investigate the relationship between antibiotic use and MRSA isolation. Twenty-six authors were contacted for further details19–44 and their studies were excluded because they did not satisfy the inclusion criteria or they did not answer. Six studies were excluded because they were duplicates.45–50 The remaining 72 studies were included in the analysis.4,7,10,13,51–118 Among them, four studies provided data from two different studies.75,82,86,99 Thus, a total of 76 clinical studies were evaluated with a total study population of 24 230 patients: 4365 MRSA-positive and 19 865 controls (Figure 1).
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Study description
A summary is reported in Table 1. Thirty studies were performed in the USA (42%), 29 in Europe (40%), 9 in Asia (13%), 2 in Brazil (3%) and 1 in Australia and in Canada, respectively (1%). Thirty-five were case–control studies (18 retrospective and 17 prospective), 34 were cohort studies (29 prospective and 5 retrospective) and 7 were prevalence surveys. All but six60,95,101,103,107,117 specified that the diagnosis of MRSA was done according to the international microbiological guidelines. Mean age of patients was reported in 56 studies [mean ± standard deviation (SD), 59 ± 15 years]. Patients with diabetes and cancer were included in 34 (45%) and 26 (34%) studies, respectively. Data on the presence of central venous catheters were reported in 24 studies (32%).
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Twenty-nine studies included MRSA-colonized patients (38%) and 38 MRSA-infected patients (50%), and 9 studies did not distinguish between MRSA infection and colonization (12%). The definition of the control group varied among studies: MSSA-positive subjects (33 studies), those with no S. aureus isolation throughout the study period (13 studies) and mixed population (30 studies).
Twenty-six studies included patients with community-acquired MRSA (34%), 35 with nosocomial or healthcare-associated MRSA (46%) and 15 with mixed isolation (20%). Eight studies were performed during an MRSA outbreak.52,59,60,64,69,88,94,97 Six studies included cohorts of community patients (from the survey practice lists, homeless and urban poor population, drug addicts, football players, US army soldiers and university students).72,76,87,90,92,97
In the majority of studies, colonized patients were sampled at nose (14 studies), nose plus skin (8 studies), nose plus wounds and/or perineum and/or catheter sites (11 studies). Studies on MRSA infections included bloodstream infections (17 studies), ventilator-associated pneumonia (3), skin infections (3), endocarditis (2), mediastinitis (1) and mixed infections (19). Two studies did not specify the type of infection included.13,58 The length of time in which antibiotic exposure was detected ranged from 7 to 1080 days (mean ± SD, 126 ± 184 days) prior to the MRSA isolation (for cases) or the inclusion in the study (for controls). Twenty-four studies did not specify the length of time in which antibiotic exposure was detected.4,10,13,51,53,54,59–61,64,66,68,69,73,83,86,95,101,103,108–110,113,118 Adjustment for covariates (age, sex, race, co-morbidities, Simplified Acute Physiology Score II, hospital ward, admission date, length of hospitalization prior to the MRSA isolation, previous hospitalizations, T lymphocyte CD4 cells count and incarceration status) was performed in 14 studies.13,51,62,67,69,87,88,94–96,101,103,113,117
Antibiotic use and MRSA isolation
Seventy studies (92%) reported on antibiotic therapy. Specific classes of antibiotics were analysed in 18 studies4,13,53,54,69,77,79,84,85,88,93–95,98,101,112,113,118 (24%). The combined RR of MRSA isolation in patients who had been previously treated with antibiotic therapy versus non-treated patients documented an almost doubled disadvantage for previously treated patients in detecting MRSA (RR, 1.8; 95% CI, 1.7–1.9; P < 0.001) (Figure 2). Subgroup analyses stratified by classes of antimicrobial therapy (quinolones, β-lactams other than cephalosporins, glycopeptides, and cephalosporins) are shown in Figure 3. The highest risk was associated with the use of quinolones (RR, 3; 95% CI, 2.5–3.5), followed by the use of glycopeptides (RR, 2.9; 95% CI, 2.4–3.5), cephalosporins (RR, 2.2; 95% CI, 1.7–2.9) and other β-lactams (RR, 1.9; 95% CI, 1.7–2.2). The use of macrolides was not included in the subgroup analysis as only three studies reported on these data.4,77,85 Only one, among these papers, observed a statistically significant association between macrolide use and MRSA isolation in the multivariate analysis.4
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Distribution of the RR of MRSA acquisition in patients previously treated with antibiotic therapy versus non-treated patients, stratified by definition of cases, showed that the combined RR was 1.9 for infected patients (95% CI, 1.8–2; P < 0.001) and 1.6 for colonized subjects (95% CI, 1.5–1.7; P < 0.001). Both the forest plots that stratified for community (RR, 1.6; 95%CI, 1.5–1.7; P < 0.001) and nosocomial/healthcare-associated (RR, 1.7; 95% CI, 1.6–1.9; P < 0.001) isolation showed a significant disadvantage for patients who had been previously treated with antibiotic therapy. Among the studies that reported data for patients who acquired MRSA in hospital and community without dividing them into different groups, the combined RR was 2.1 (95% CI, 1.9–2.3; P < 0.001).
Analysis of heterogeneity documented a significant heterogeneity among the analysed studies (Table 2). Heterogeneity was not detected among prevalence studies (P = 0.3, I2 test = 15%). A meta-regression showed that the greatest source of heterogeneity was related to the length of time in which antibiotic exposure was detected (more or less than 180 days) (P = 0.003).
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Analysis of small study bias
Begg's funnel plot (P = 0.4) and the Egger test (P = 0.2) for small study bias indicated that there was no evidence of bias (Figure 4).
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Discussion |
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The evidence of the association between previous antibiotic therapy and colonization or infection due to antibiotic-resistant bacteria has been reported for different microorganisms including vancomycin-resistant enterococci (VRE),119,120 extended-spectrum β-lactamase-producing bacteria121 and imipenem-resistant Pseudomonas aeruginosa.122 A prediction model, aimed at identifying MRSA bacteraemia, predicted that 80% of the nosocomial and 60% of the community-acquired bacteraemia would be resistant to methicillin if patients had experienced antimicrobials prior to the onset. This model also indicated that there were no differences between antibiotics in the prediction of MRSA.85 Although many epidemiological studies which focused on MRSA reported a statistically significant association between previous antibiotic therapy and MRSA isolation, the size of this association has not been appropriately explored.
According to the Society for Healthcare Epidemiology of America (SHEA) guidelines for preventing nosocomial transmission of MRSA and VRE, the use of antimicrobial agents in US hospitals is often excessive or unnecessary.123 This large use of antibiotics can create conditions in which bacteria with mechanisms of resistance experience a competitive advantage. Therefore, one of the SHEA recommendations (number IV) underlines the need to reduce the use of antibiotics, mainly fluoroquinolones, and to help prevent the persistent carriage of MRSA.123 In 2005, revised MRSA infection-control guidelines for hospitals from the Joint Working Party of the BSAC, Hospital Infection Society and Infection Control Nurses Association included the rational use of antibiotics and an antibiotic policy among the basic infection-control measures.124 A limited use of glycopeptides, cephalosporins and fluoroquinolones was strongly recommended.124
This meta-analysis demonstrates that subjects who have been exposed to antibiotic therapy have an almost 2-fold chance of acquiring MRSA as opposed to non-exposed subjects. This risk is almost three times greater after the use of quinolones and glycopeptides.
Surveillance data reported that the majority of MRSA strains are resistant to quinolones.125 The mechanisms of resistance to methicillin and ciprofloxacin may be unrelated, but tend to be associated. Biological mechanisms for quinolones to select methicillin-resistant S. aureus are not well explained. Fluoroquinolones have an excellent tissue diffusion that could promote the acquisition of MRSA by eradicating susceptible microorganisms such as MSSA. In vitro studies have shown that subinhibitory concentrations of ciprofloxacin induced the production of fibronectin-binding proteins and increased the adhesion to fibronectin-coated surfaces promoting host colonization.126 It has also been demonstrated that ciprofloxacin is excreted in apocrine and eccrine sweat of healthy individuals undergoing antibiotic therapy.127 Venezia et al.128 showed that growth in the presence of a fluoroquinolone resulted in >10-fold increase in the proportion of the population that grew on agar containing oxacillin. Ciprofloxacin exhibited a greater effect than moxifloxacin, levofloxacin and gatifloxacin. The increase was directly proportional to the fluoroquinolone concentration and could be detected as early as 8 h after exposure to the fluoroquinolone. The authors suggested that fluoroquinolones might influence oxacillin resistance by selective inhibition or by killing of the more susceptible subpopulations in heteroresistant S. aureus.128
One study, which was conducted in a department of Geriatric Medicine in London, documented that a restriction in the use of cephalosporins, the introduction of simple control measures such as emphasis on hand washing and 7 day time-limits on antibiotic use, reduced the MRSA incidence from 3.95 per 100 hospital admissions to 1.94.129 Schentag et al.130 showed that the ‘shift’ from MSSA to MRSA begins on the first day in hospital, when patients are given cefazolin as surgical prophylaxis. Under selective antibiotic pressure, colonizing flora changes within 24–48 h. For patients who protract their hospital stay, subsequent courses of third-generation cephalosporins further select and amplify the colonizing MRSA population.
Similar biological mechanisms might be hypothesized for glycopeptides and β-lactams in the selection of MRSA strains. By eliminating MSSA, these drugs might enhance the patient's susceptibility to MRSA colonization. In vitro, the induction of phenotypic resistance in mecA-positive MSSA was attempted by a 24 h exposure to oxacillin and cefotaxime.131 In a prospective cohort study including 864 patients starting antibiotics, the incidence of MRSA nasal colonization for 1000 days of therapy was 7.9 for carbapenems, 3.2 for glycopeptides, 3.1 for quinolones and 2.4 for third-generation cephalosporins.132
Although meta-analyses are able to provide a better assessment of the relationship between specific factors and outcomes by increasing the power to investigate the diseases, they cannot eliminate potential sources of error contained in the included studies. The main source of heterogeneity of the RR estimates between available studies must be considered before drawing final conclusions on the real strength of the association between antibiotic therapy and MRSA isolation. In this study, the most relevant source of heterogeneity was related to the length of time in which antibiotic exposure was detected, which varied greatly among studies (from 7 to 1080 days). When studies were grouped for study design (i.e. prevalence survey), no heterogeneity was detected. Another possible cause of heterogeneity among analysed studies could be the lack of data on duration of antibiotic use and dosages. Most studies did not report on association therapy. The effect of antibiotic association, for example, macrolide plus cephalosporin, should be further studied.
Despite the limitations of the study, this meta-analysis, which analyses the data of 24 230 patients, shows a clear association between exposure to antibiotics and MRSA isolation. A controlled use of antibiotics may, thus, be one of the few modifiable factors offering potential for primary prevention of MRSA colonization. Meticulous attention to infection-control practices is also of paramount importance in preventing MRSA colonization. Ultimately, future research should focus on some of the limitations of the current literature. Prospective cohort studies analysing the development of newly acquired MRSA colonization in patients undergoing antibiotic therapy need to be planned.
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No funding has been received.
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None to declare.
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References |
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