TY - JOUR
AU - USA, Helen B. Viscount, MS
AB - ABSTRACT Mupirocin is an antibiotic used for eradication and infection control of methicillin-resistant Staphylococcus aureus (MRSA). Mupirocin binds to the bacterial isoleucyl tRNA synthetase, thus disrupting bacterial protein synthesis. Four hundred nine MRSA clinical isolates collected in 2006 and 2007 at Madigan Army Medical Center were screened for mupirocin resistance by E test and polymerase chain reaction; 7 MRSA isolates (1.7%) were found to be fully resistant to mupirocin (minimum inhibitory concentration [MIC] by E test: >1,024 µg/mL), 10 isolates (2.4%) had MIC values of 1 to 32 µg/mL, while 392 MRSA isolates (95.9%) had MIC values of <1 µg/mL. No trend of increased mupirocin resistance was found when compared with subsequent years. These results show that mupirocin remains a valid infection control measure due to its unique mechanism of action and the high susceptibility rate of MRSA isolates. In addition, rapid screening by polymerase chain reaction of MRSA shows promise in assessing the fully resistant mupirocin phenotype. INTRODUCTION Methicillin-resistant Staphylococcus aureus (MRSA) infection presents most commonly as relatively minor skin and soft tissue infections, but severe invasive disease, including necrotizing pneumonia, necrotizing fasciitis, severe osteomyelitis, and a sepsis syndrome with increased mortality have also been described in children and adults. Community-acquired MRSA (CA-MRSA) refers to a family of related strains of S. aureus (designated by the Centers for Disease Control and Prevention as “USA 300”) originally derived from ST8, a methicillin-sensitive strain (MSSA). The epidemic strain of CA-MRSA in the United States is clonal; it produces the Panton-Valentine leukocidin and has the type IV, staphylococcal chromosome cassette (SCC) mec element that confers methicillin resistance. These properties are rare in the USA 100 and 200 strain families, which have historically accounted for most nosocomial infections. However, recent data show that the USA 300 strains now account for an increasing portion of health care-associated infections as well,1 thereby leading to a blurring of the distinction between the USA 300 strains as “community-acquired” and USA 100/200 as “nosocomial” or “health care associated.” CA-MRSA has become an epidemic problem of serious concern in the United States and much of the world. The prevalence of MRSA colonization and infection in the surrounding community may therefore affect the selection of strategies for MRSA control in health care settings. When patients with MRSA have been compared to patients with MSSA, MRSA-colonized patients more frequently developed symptomatic infections and higher case fatality rates have been observed for certain MRSA infections, including bacteremia, poststernotomy mediastinitis, and surgical site infections. In addition, some hospitals have observed an increase in the overall occurrence of staphylococcal infections following the introduction of MRSA into a hospital or special care unit and some studies have reported an association between MRSA infections and increased length of stay, and health care costs.2 Mupirocin (Bactroban; GlaxoSmithKline, Research Triangle Park, North Carolina) is a topical antibiotic isolated from Pseudomonas fluorescens which first became commercially available in 1985 and has been available for the elimination of staphylococcus nasal carriage since 1988. It has a unique mechanism of action among antimicrobials, binding to isoleucyl tRNA synthetase, thereby preventing incorporation of isoleucine into proteins and arresting protein synthesis. It has shown no cross-resistance with other classes of antimicrobial agents. Mupirocin is bactericidal at concentrations achieved by topical administration. However, the minimum bactericidal concentration against relevant pathogens is generally 8- to 30-fold higher than the minimum inhibitory concentration (MIC). Mupirocin has been shown to be active against most strains of S. aureus and Streptococcus pyogenes, both in vitro and in clinical studies.3 Mupirocin is also active against most strains of Staphylococcus epidermidis and Staphylococcus saprophyticus. It is used in treating superficial skin infections and in controlling spread of MRSA during outbreaks and in high-risk populations such as those in nursing homes, intensive care unit settings, dialysis units, and cardiothoracic surgery wards. Unfortunately, mupirocin resistance was described shortly after it became commercially available.4,5 Mechanisms of both low- and high-level mupirocin resistance among MRSA and MSSA isolates have been described. Resistance occurs in S. aureus and coagulase-negative staphylococci either due to point mutations in the chromosomal ileS gene or the presence of a second, usually plasmid-encoded ItRS (ileS-2 or mup-A), which retains its activity in the presence of mupirocin and can be acquired through plasmid exchange.6,–8 Prevalence of mupirocin resistance rates among MRSA and MSSA isolates in hospitals in Europe, New Zealand, Australia, Korea, Canada, Brazil, and the United States have been described with wide variability from 0 to 65% of isolates demonstrating resistance.9,–13 Rates of resistance have been shown to correlate with increased use.14 Considering the usage of mupirocin in the treatment of MRSA infection in the Western Regional Medical Command area and its potential of use in MRSA decolonization and infection control, this work aimed to determine the prevalence and trend of mupirocin resistance in MRSA clinical isolates at Madigan Army Medical Center (MAMC) by using a traditional antibiotic screening method (E test) and a laboratory developed real-time polymerase chain reaction (PCR) assay. METHODS Clinical Isolates Two hundred fifty-four MRSA isolated between January 1 and 30, 2006 and 155 MRSA isolated between January 1 and July 27, 2007 in the Microbiology Laboratory at MAMC were included in this study (Table I). Bacteria were isolated from skin/wounds (327 isolates); trachea/sputum/nasopharyngeal/lower respiratory tract; 33 nares; 19 body fluids, i.e., blood, urine, synovial fluid, etc. (27); and catheter tips/PEG tubes (3). All isolates were coagulase positive and yielded positive latex slide test results. The MRSA phenotype was confirmed using the Vitek 2 (bioMerieux, Marcy l'Etoile, France) identification and susceptibility testing cards for Gram-positive bacteria. All isolates were stored at −70°C and cultured for 24 hours on blood agar (BBL trypticase soy agar with 5% sheep blood; BD Biosciences, Cockeysville, Maryland) before E test and PCR screening. TABLE I Specimen Type and Numbers of Yearly MRSA Isolates Tested Specimen Type  2006 No. of Isolates  2007 No. of Isolates  Total  Skin/wounds  202  125  327  Trachea/sputum/nasopharyngeal/lower respiratory tract  23  10  33  Nares  10  9  19  Body fluids, i.e., blood, urine, synovial fluid, etc.  17  10  27  Catheter tips/PEG tubes  2  1  3  Total  254  155  409  Specimen Type  2006 No. of Isolates  2007 No. of Isolates  Total  Skin/wounds  202  125  327  Trachea/sputum/nasopharyngeal/lower respiratory tract  23  10  33  Nares  10  9  19  Body fluids, i.e., blood, urine, synovial fluid, etc.  17  10  27  Catheter tips/PEG tubes  2  1  3  Total  254  155  409  View Large TABLE I Specimen Type and Numbers of Yearly MRSA Isolates Tested Specimen Type  2006 No. of Isolates  2007 No. of Isolates  Total  Skin/wounds  202  125  327  Trachea/sputum/nasopharyngeal/lower respiratory tract  23  10  33  Nares  10  9  19  Body fluids, i.e., blood, urine, synovial fluid, etc.  17  10  27  Catheter tips/PEG tubes  2  1  3  Total  254  155  409  Specimen Type  2006 No. of Isolates  2007 No. of Isolates  Total  Skin/wounds  202  125  327  Trachea/sputum/nasopharyngeal/lower respiratory tract  23  10  33  Nares  10  9  19  Body fluids, i.e., blood, urine, synovial fluid, etc.  17  10  27  Catheter tips/PEG tubes  2  1  3  Total  254  155  409  View Large Antibiotic Susceptibility Testing of S. aureus A Vitek 2 system (bioMerieux) has been used for identification and antibiotic susceptibility testing of Gram-positive cocci including S. aureus, according to the manufacturer's instructions. Clindamycin results were confirmed by proximity testing with a macrolide to rule out inducible resistance (two 2-µg clindamycin disks placed precisely 15 and 20 mm, edge-to-edge, from a 15-µg erythromycin disk on Mueller- Hinton plates; blunting of the zone of inhibition around the clindamycin disk after 18–24 hours of incubation was interpreted as positive for inducible macrolide-lincosamide-streptogramin resistance). The results are listed in Table II. TABLE II Antibiotic Susceptibility of S. aureus Isolates at MAMCa Antibiotic  % Susceptible Isolates  Oxacillin/methicillin  52  Erythromycin  41  Clindamycin  83  Levofloxacin  66  Trimethoprim/sulfa  80–90  Nitrofurantoin  99  Tetracycline  95  Gentamicin  99  Vancomycin  100  Rifampin  100  Linezolid  100  Quinupristin/dalfopristin  100  Antibiotic  % Susceptible Isolates  Oxacillin/methicillin  52  Erythromycin  41  Clindamycin  83  Levofloxacin  66  Trimethoprim/sulfa  80–90  Nitrofurantoin  99  Tetracycline  95  Gentamicin  99  Vancomycin  100  Rifampin  100  Linezolid  100  Quinupristin/dalfopristin  100  a Table lists percent susceptible isolates, remainder are nonsusceptible, resistant, or intermediate. A total of 1,160 S. aureus isolates (individual patients) was screened between January 1 and December 31, 2006. Data include 378 newly isolated MRSA. Oxacillin: class drug for cloxacillin and nafcillin. Oxacillin- resistant staphylococci are considered resistant to all cephalosporins, carbapenems, and β-lactams. Clindamycin results are confirmed by proximity testing with a macrolide to rule out inducible resistance. View Large TABLE II Antibiotic Susceptibility of S. aureus Isolates at MAMCa Antibiotic  % Susceptible Isolates  Oxacillin/methicillin  52  Erythromycin  41  Clindamycin  83  Levofloxacin  66  Trimethoprim/sulfa  80–90  Nitrofurantoin  99  Tetracycline  95  Gentamicin  99  Vancomycin  100  Rifampin  100  Linezolid  100  Quinupristin/dalfopristin  100  Antibiotic  % Susceptible Isolates  Oxacillin/methicillin  52  Erythromycin  41  Clindamycin  83  Levofloxacin  66  Trimethoprim/sulfa  80–90  Nitrofurantoin  99  Tetracycline  95  Gentamicin  99  Vancomycin  100  Rifampin  100  Linezolid  100  Quinupristin/dalfopristin  100  a Table lists percent susceptible isolates, remainder are nonsusceptible, resistant, or intermediate. A total of 1,160 S. aureus isolates (individual patients) was screened between January 1 and December 31, 2006. Data include 378 newly isolated MRSA. Oxacillin: class drug for cloxacillin and nafcillin. Oxacillin- resistant staphylococci are considered resistant to all cephalosporins, carbapenems, and β-lactams. Clindamycin results are confirmed by proximity testing with a macrolide to rule out inducible resistance. View Large E Test The mupirocin E test from AB Biodisk (MIC range, 0.064– 1024 µg/mL) was used according to the manufacturer's instructions on Mueller-Hinton agar. Briefly, a single E test strip was applied to each plate; following incubation at 37°C for 24 hours, the MIC was determined as the point of intercept of the zone of inhibition; quality control range of MICs was tested with S. aureus ATCC 29213 (MIC, 0.064–0.25 µg/mL) and Enterococcus faecalis ATCC 29212 (MIC, 16–64 µg/mL). Real-Time PCR DNA was extracted from 3 to 5 MRSA colonies using a Roche MagNA Pure Compact System (Somerville, New Jersey). The real-time PCR assay was performed on the Light- Cycler PCR platform (Roche) using primers designed based on the published sequence of the ileS-2 gene and literature data15,16 and was custom ordered from Sigma Genosys (The Woodlands, Texas): Mup-F (5′-TAATGGGAAAATGTCTC- GAGTAGA-3′) and Mup-R (5′-AATAAAATCAGCTGGAA- AGTGTTG-3′) primers and Mup-P probe (5′-CTCTATGC- CGTTTGCTCAGCATCAT). A fully mupirocin-resistant MRSA clinical isolate with MIC > 1,024 µg/mL was used as a positive control upon cloning of PCR product and subsequent sequencing (data not shown). An IDI-MRSA assay was performed according to the manufacturer's instructions (GenOhm, San Diego, California) as previously described17 by using a SmartCycler II device (Cepheid, Sunnyvale, California); primers for also detecting the mupirocin resistance as described above were included with a SmartMix HM PCR master mix (Cepheid). RESULTS E test results showed that among the MRSA isolates collected in 2006, 242 (95.28%) had very low levels of mupirocin resistance (MIC <1 µg/mL), 7 had MIC values between 3 and 32 µg/mL (2.75%), and 5 (1.97%) were fully mupirocin resistant (MIC > 1,024 µg/mL) (Fig. 1A). Similar results were obtained for MRSA isolates collected in 2007: 150 isolates with MIC <1 µg/mL (96.76%), 3 with MIC values between 3 and 32 µg/mL (1.95%), and 2 (1.29%) fully mupirocin-resistant (MIC >1,024 µg/mL) (Fig. 1B). The fully mupirocin-resistant MRSA showed no growth inhibition zone around the E test strip (Fig. 2). FIGURE 1 View largeDownload slide Distribution of the E test MIC values of MRSA clinical isolates from 2006 (A) and 2007 (B). FIGURE 1 View largeDownload slide Distribution of the E test MIC values of MRSA clinical isolates from 2006 (A) and 2007 (B). FIGURE 2 View largeDownload slide Representative example of the E test results on Mueller- Hinton agar showing the growth inhibition zone on mupirocin-sensitive MRSA (A); no growth inhibition was observed on seven MRSA isolates (B). FIGURE 2 View largeDownload slide Representative example of the E test results on Mueller- Hinton agar showing the growth inhibition zone on mupirocin-sensitive MRSA (A); no growth inhibition was observed on seven MRSA isolates (B). The ileS-2 gene conferring resistance to mupirocin was detected by real-time PCR on the LightCycler platform only in the seven fully resistant isolates (Fig. 3). Since in the present study there were no isolates with MIC values >32 µg/mL but < 1,024 µg/mL, it is unclear whether the ileS-2 gene is also present in isolates in that MIC range. FIGURE 3 View largeDownload slide Representative example of real-time PCR results on LightCycler PCR platform for detection of the ileS-2 gene for mupirocin resistance of MRSA. FIGURE 3 View largeDownload slide Representative example of real-time PCR results on LightCycler PCR platform for detection of the ileS-2 gene for mupirocin resistance of MRSA. Since rapid detection of the MRSA genotype by PCR can be performed directly from nasal specimens with the IDI-MRSA assay (targets MRSA-specific SCCmec gene), we also modified this assay so that the same specimen can be tested for mupirocin resistance (detection of ileS-2 gene) (Fig. 4). FIGURE 4 View largeDownload slide Detection of mupirocin-resistant/sensitive MRSA/MSSA using an IDI-MRSA assay on the SmartCycler II PCR platform. The customized IDI-MRSA assay exemplified here specifically detects the MRSA- specific SCCmec gene and the mupirocin resistance ileS-2 gene in the same run. Mup-R, mupirocin fully resistant; Mup-S, mupirocin sensitive; and Kit PC, IDI-MRSA-positive control. FIGURE 4 View largeDownload slide Detection of mupirocin-resistant/sensitive MRSA/MSSA using an IDI-MRSA assay on the SmartCycler II PCR platform. The customized IDI-MRSA assay exemplified here specifically detects the MRSA- specific SCCmec gene and the mupirocin resistance ileS-2 gene in the same run. Mup-R, mupirocin fully resistant; Mup-S, mupirocin sensitive; and Kit PC, IDI-MRSA-positive control. DISCUSSION Because MRSA infections have been associated with increased morbidity, mortality, and prolonged hospitalization, reliable infection control measures and rapid detection methods are currently the focus of attention in civilian and military health care settings. Mupirocin is the active ingredient in Bactroban Ointment and Bactroban Cream (GlaxoSmithKline) and is frequently used in the treatment of superficial MRSA infections and in infection control protocols designed to reduce MRSA colonization. Each gram of Bactroban Ointment (mupirocin ointment) contains 2% (20 mg) mupirocin in a bland water miscible ointment base (polyethylene glycol ointment, N.F.) consisting of polyethylene glycol 400 and polyethylene glycol 3350. A paraffin-based formulation—Bactroban Nasal (mupirocin calcium ointment; GlaxoSmithKline)—is also available for intranasal use. Colonization with S. aureus may be transient or last for years. The nasal carriage rates have been reported in the literature as 25 to 30% for the general population and 10 to 40% for outpatient population or on admission (with MRSA representing >50% of hospital-acquired S. aureus in some North American hospitals).1 In the Western Regional Medical Command, Bactroban Ointment and Bactroban Cream (GlaxoSmithKline) have been widely prescribed: 4,256 tubes containing a total of 93,968 g of mupirocin formulation from March 1, 2006 through February 28, 2007. However, mupirocin is not prescribed in our institution for MRSA decolonization. Despite intensive usage, our study shows that the mupirocin resistance levels in MRSA isolates remain very low (below 2% in 2006–2007) and have not changed significantly from 1 year to the next (1.97% fully resistant isolates in 2006 versus 1.29% in 2007); these data are in contrast to recently reported higher rates of mupirocin resistance (13.2%) in a surgical intensive care unit despite low levels of in-hospital mupirocin use.18 Consistent with the high number of skin infections (Table I), the majority of fully resistant mupirocin isolates5 were obtained from skin/wounds while the other two were cultured from trachea and sputum, respectively. The high prevalence of MRSA and the acquired resistance to multiple antibiotics is a cause for concern. Of the 1,160 S. aureus isolates screened for antibiotic resistance at MAMC in 2006, only 52% were oxacillin/methicillin susceptible and resistance to other antibiotics is on the rise (Table II). However, the low levels of MRSA resistance to mupirocin suggest that mupirocin remains a valid infection control measure of MRSA likely due to the unique mechanism of action of this antibiotic. New antimicrobial agents with alternative mechanisms of action are also in development to overcome the resistance trends both for isolates from community- or nosocomial-acquired infections.19,20 Because increasing MRSA rates place a considerable burden on hospital infection control programs with regard to logistics and costs, reliable molecular detection assays which decrease the 2- to 4-day turnaround time for isolation, identification, and confirmation of MRSA by traditional methods are becoming available. IDI-MRSA was Food and Drug Administration-approved in March 2004. Customizing such MRSA detection assays to also screen for antibiotic resistance may help physicians decide whether a targeted antibiotic such as mupirocin remains an effective agent to be used in the treatment of MRSA infection or in the eradication of nasal colonization with MRSA in adult patients and health care workers as part of a comprehensive infection control program and an effective epidemiological tool. In summary, the results of this study establish a threshold of mupirocin resistance in MRSA clinical isolates in the Western Regional Medical Command. Continued surveillance of mupirocin resistance is important to retain the usefulness of this agent for the treatment or prevention of MRSA infections. ACKNOWLEDGMENTS Thanks go to Madigan Army Medical Center staff, Ms. Haengcha Chong (Molecular Diagnostics Laboratory) for technical and logistical support with the PCR, Ms. Mary Myers and Mr. Chris Gibson (Microbiology Laboratory, MAMC, Fort Lewis, Washington) for S. aureus antibiotic susceptibility data, and COL Ricke Weickum (Department of Pharmacy, MAMC, Fort Lewis, Washington) for Bactroban utilization rate. This work was performed under the MAMC Institutional Review Board Protocol 207048 “Mupirocin resistance among S. aureus isolates at Madigan Army Medical Center.” REFERENCES 1. Seybold U, Kourbatova EV, Johnson JG et al.  : Emergence of community-associated methicillin-resistant S. aureus USA 300 genotype as a major cause of health care-associated blood stream infections. Clin Infect Dis  2006; 42: 647– 56. Google Scholar CrossRef Search ADS PubMed  2. 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Desjardins M, Guibord C, Lalonde B, Toye B, Ramotar K Evaluation of the IDI-MRSA assay for detection of methicillin-resistant Staphylococcus aureus from nasal and rectal specimens pooled in a selective broth. J Clin Microbiol  2006; 44: 1219– 23. Google Scholar CrossRef Search ADS PubMed  18. Jones JC, Rogers TJ, Brookmeyer P et al.  : Mupirocin resistance in patients colonized with methicillin-resistant Staphylococcus aureus in a surgical intensive care unit. CID  2007; 45: 541– 7. Google Scholar CrossRef Search ADS   19. Singh K, Malathum K, Murray BE In vitro activities of a new ketolide, ABT-773, against multi-drug-resistant Gram-positive cocci Antimicrob Agents Chemother  2001; 45: 3640– 3. 20. Livermore DM Tigecycline: what is it, and where should it be used? J Antimicrob Chemother  2005; 56: 611– 4. Google Scholar CrossRef Search ADS PubMed  Footnotes 1 The data of this study were partly presented in-house at the Madigan Army Medical Center Research Day, April 26, 2007, Fort Lewis, WA. Reprint & Copyright © Association of Military Surgeons of the U.S.
TI - Mupirocin Resistance Screening of Methicillin-Resistant Staphylococcus aureus Isolates at Madigan Army Medical Center
JO - Military Medicine
DO - 10.7205/MILMED.173.6.604
DA - 2008-06-01
UR - https://www.deepdyve.com/lp/oxford-university-press/mupirocin-resistance-screening-of-methicillin-resistant-staphylococcus-8bYu0avyaO
SP - 604
EP - 608
VL - 173
IS - 6
DP - DeepDyve
ER -