Brief Communication
Urinary tract infection caused by Enterococcus isolates: aetiology and antimicrobial resistance patterns Qing-Yong Wang, Rong-Hai Li, Xiao-Hong Shang Department of Clinical Laboratory, Xiyuan Hospital, China Academy of Chinese Medical Sciences, Beijing, China The purpose of this study was to analyse the data on resistance in Enterococcus faecalis and E. faecium isolated from urine samples of inpatients from January 2010 to December 2013. Compared to E. faecalis, E. faecium isolates were significantly more resistant to ampicilin, nitrofurantoin, and ciprofloxacin in the antimicrobial agents evaluated. Both species showed higher resistance to high-level gentamicin. The rate of vancomycin-resistant enterococci (VRE) in E. faecium was higher as compared to that of E. faecalis, and we found that apparent increase in the frequency of VRE E. faecalis clinical isolates in the 4-year study period. In our study, analysis of the antimicrobial resistance trends showed resistance to linezolid and vancomycin were ,30.2% and ,20.3% in both species, respectively. Of noteworthy is the high rate of MDR in two species from inpatients. This study highlights that it is of importance for clinicians to promote rational drug utilization and delay the emergence of resistant organisms. Keywords: Antimicrobial resistance, Enterococcus spp., Urinary tract infection
Enterococcus faecium and Enterococcus faecalis are the most frequently occurring enterococcal bacteria isolated from urinary tract infections. Treatment of enterococcal infections is often difficult due to their inherent resistance to several antimicrobial agents and their tendency to acquired resistance.1 Many Enterococcus species have acquired resistance to commonly prescribed anti-enterococcal antibiotics such as beta-lactams, vancomycin, and aminoglycosides.2 Therefore, surveillance of enterococcal species distribution and determination of drug resistance patterns are paramount to empirical therapy strategies in clinical settings. We retrospectively reviewed the computerized database generated by the Clinical Microbiology Laboratory. Records from January 2010 to December 2013 were searched for patient urine samples that tested positive for enterococcal species (§104 colony forming units/ml). Bacterial identification and susceptibility to different antimicrobial agents were performed using the BD Phoenix Automated Microbiology System. The combination panel of the BD Phoenix Automated Microbiology System comprises an identification component and an antimicrobial susceptibility testing (AST) component. The AST component contains 84
Correspondence to: X.-H. Shang, Department of Clinical Laboratory, Xiyuan Hospital, China Academy of Chinese Medical Sciences, Beijing 100091, China. Email: [email protected]
ß 2015 Edizioni Scientifiche per l’Informazione su Farmaci e Terapia DOI 10.1179/1973947814Y.0000000192
wells with dried antimicrobial panels and one growth control well. Drug sensitivities were assayed with a broth-based microdilution test. Twenty-five microlitres of the standardized identification broth suspension was transferred to the AST broth followed by one freefalling drop of a redox (AST) indicator, yielding a final concentration. The detection of organism growth in the presence of an antimicrobial agent is carried out by the indicator in the system. Additional tests were conducted if the BD Phoenix Automated Microbiology System yielded results with ,90% confidence. E. faecalis ATCC 29212 and Staphylococcus aureus ATCC 29213 were used as quality control strains. Seven antimicrobial agents were examined: ampicillin, ciprofloxacin, gentamicin, linezolid, nitrofurantoin, tetracycline, and vancomycin. Multidrug resistance (MDR) was defined as non-susceptibility to at least one agent in three or more antimicrobial categories.3 Between 2010 and 2013, 252 E. faecalis isolates and 265 E. faecium isolates were identified in inpatient urine samples. The median ages of E. faecalis-positive inpatients were 71.5, 70.1, 71.1, and 69.6 years by treatment year, respectively, while the median ages of E. faecium-positive inpatients were 76.2, 73.2, 75.6, and 74.3 years. Yearly resistance rates of E. faecalis and E. faecium isolates to different antimicrobial agents are shown in Table 1. E. faecalis isolates and E. faecium isolates
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were resistant to ampicillin (9.9 and 84.9%, respectively), nitrofurantoin (11.6 and 97%, respectively), linezolid (25.8 and 20%, respectively), tetracycline (83.3 and 35.8%, respectively), and ciprofloxacin (62.7 and 92.8%, respectively). Of the antimicrobial agents evaluated, high-level resistance to gentamicin was observed in 57.5% of E. faecalis isolates and 60% of E. faecium isolates. Vancomycin had the lowest resistance rates (4.8% of E. faecalis isolates and 15.8% E. faecium isolates). MDR rates were observed for both enterococcal species in the urine of hospital inpatients (50% total for E. faecalis isolates and 92.5% total for E. faecium isolates). Approximately 31.7% of these E. faecalis isolates and 21.5% of E. faecium isolates were nonsusceptible to three classes of antimicrobial agents, 12.3% of E. faecalis isolates and 40.4% of E. faecium isolates were non-susceptible to four classes of antimicrobial agents, and 6% of E. faecalis isolates and 30.6% of E. faecium isolates were non-susceptible to more than five classes of antimicrobial agents. Interestingly, vancomycin resistance in E. faecalis isolates increased gradually from 2010 to 2013. In recent years, Enterococcus species have become increasingly important in clinical microbiology. This is owing to their ability to cause healthcare-associated infections and their increasing resistance to different antibiotics. E. faecium and E. faecalis are considered the most clinically significant enterococci. In this study, we report no significant difference between the proportion of E. faecalis and E. faecium isolates identified from urine samples of hospital inpatients. However, these data are not consistent with previous studies.4–6 This discrepancy may be ascribed to patients being in poor physical condition at the time of sampling, and therefore, more prone to opportunistic infection than the general population. Interestingly, we also determined that the median age of inpatients with E. faecium infection was higher
than that of E. faecalis-positive inpatients in each of the study years. Mobile genetic elements are important for the propagation and persistence of antimicrobial resistance in E. faecalis and E. faecium.3 In this study, we found that the antimicrobial resistance exhibited by these two enterococcal bacteria did not change significantly over the analysis period. Exceptions were slightly increased frequencies of vancomycin resistance in E. faecalis and tetracycline resistance in E. faecium from 2010 to 2013. In addition, E. faecium isolates were significantly more resistant to ampicillin, nitrofurantoin, and ciprofloxacin, but more susceptible to tetracycline, compared with E. faecalis isolates. Based on these findings, nitrofurantoin (only for uncomplicated urinary tract infections) and ciprofloxacin (only if susceptible and as part of a combination regimen) might be suitable antibiotic options for the treatment of ampicillin- and vancomycin-resistant enterococcal infections.2 MDR rates were .50% in E. faecalis isolates and .92.5% in E. faecium isolates analysed in this current study, and this may be related to widespread antibiotic use in the hospital. In particular, many of the MDR isolates were resistant to vancomycin. Vancomycin-resistant enterococci (VRE) were first reported in 1988, and have since emerged as an increasingly common clinical problem worldwide.7 In our study, the rate of vancomycin resistance in E. faecium isolates (15.8%) was higher than that of the E. faecalis isolates (4.8%). In addition, three (25%) E. faecalis isolates and eight (21.6%) E. faecium isolates showed intermediate resistance to vancomycin (data not shown). To decrease nosocomial transmission, VRE carriers should be identified and isolated upon admission, and infection control practices should be optimized.8 Moreover, it is important that clinicians obtain accurate information about Enterococcus clinical isolates that are resistant to aminoglycosides.
Table 1 Yearly resistance rates (%) exhibited by E. faecium and E. faecalis isolates to different antimicrobial agents 2010
Antibiotic
2011
2013
2010–2013
E. faecalis E. faecium E. faecalis E. faecium E. faecalis E. faecium E. faecalis E. faecium E. faecalis E. faecium (n553) (n562) (n571) (n581) (n553) (n543) (n575) (n579) (n5252) (n5265)
Ampicillin 7.5 85.5 Nitrofurantoin 9.4 95.2 Linezolid 30.2 27.4 Tetracycline 84.9 19.4 Ciprofloxacin 54.7 93.5 Vancomycin 0 19.4 Gentamicin* 52.8 58.1 Multidrug resistance (non-susceptibility 3 18.9 17.7 4 11.3 45.2 §5 7.5 27.4 MDR (§3) 37.7 90.3
15.5 81.5 7.5 79.1 8.0 91.1 9.9 12.7 98.8 11.3 93.0 12.0 98.7 11.6 22.5 12.3 28.3 20.9 24.0 21.5 25.8 78.9 33.3 84.9 46.5 85.3 45. 6 83.3 66.2 92.6 49.1 90.7 74. 7 93.7 62.7 2.8 9.9 3.8 14.0 10.7 20.3 4.8 52.1 65.4 54.7 46.5 68.0 63.3 57.5 to three or more classes of the antimicrobial agents tested in this study) 35.2 22.2 26.4 25.6 41.3 21.5 31.7 8.5 45.7 11.3 27.9 17.3 38 12.3 7.0 24.7 3.8 32.6 5.3 38.0 6.0 50.7 92.6 41.5 86.0 64 97.5 50
Note: *High-level gentamicin resistance. MDR: multidrug resistance.
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We observed no significant difference in E. faecalis and E. faecium resistance to high-level gentamicin treatment over the study period. If enterococcal strains are resistant to high-level gentamicin treatment, however, increased resistance to vancomycin might also occur.9 Of the antimicrobial agents evaluated, non-susceptibility rates to linezolid were 25.8 and 20% for E. faecalis isolates and E. faecium isolates, respectively. However, 82.5% of E. faecalis isolates and 61.5% of E. faecium isolates were in the intermediate range. Therefore, we recommend that AST be performed before commencement of therapy. Linezolid is currently approved by the United States Food and Drug Administration for treatment of infections caused by VRE. Nonetheless, sporadic resistance to linezolid has been reported.2,10,11 In conclusion, the antimicrobial resistance reported in this study highlights the need for accurate identification of enterococci species owing to their significant differences in resistance profiles. This study also concurs with previous reports which demonstrate that the BD Phoenix Automated Microbiology System rapidly identifies enterococci and accurately analyses AST in a clinical laboratory setting.12,13 Our results further support the promotion of rational drug use to delay the emergence of resistant organisms, and emphasize the importance of monitoring multidrugresistant E. faecalis and E. faecium isolates in a clinical setting. However, except for age of the outpatients, we concede that this report is limited because no other clinical characteristics were analysed. In a follow-up study, we wish to evaluate the association (if any) between enterococci-related urinary tract infections and sex distribution, type (cystitis, urethritis, or pyelonephritis), or the presence of asymptomatic or symptomatic episodes. It is also worth examining the history of antibiotic use for each patient, and whether antibiotics were indeed necessary for treatment of the documented bacteriuria.
Disclaimer Statements Contributors Qing-Yong Wang: Conception and design of study, data analysis and/or interpretation, drafting of manuscript and/or critical revision, and approval of final version of manuscript. Rong-Hai Li:
Antimicrobial resistance of enterococci
Acquisition of data. Xiao-Hong Shang: Conception and design of study, data analysis and/or interpretation, and approval of final version of manuscript. Funding None. Conflicts of interest None declare. Ethics approval None.
References 1 Murray BE. The life and times of the Enterococcus. Clin Microbiol Rev. 1990;3:46–65. 2 Arias CA, Contreras GA, Murray BE. Management of multidrug-resistant enterococcal infections. Clin Microbiol Infect. 2010;16:555–62. 3 Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, et al. Multidrug-resistant, extensively drugresistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012;18:268–81. 4 Protonotariou E, Dimitroulia E, Pournaras S, Pitiriga V, Sofianou D, Tsakris A. Trends in antimicrobial resistance of clinical isolates of Enterococcus faecalis and Enterococcus faecium in Greece between 2002 and 2007. J Hosp Infect. 2010;75:225–7. 5 Wang JT, Chang SC, Wang HY, Chen PC, Shiau YR, Lauderdale TL. High rates of multidrug resistance in Enterococcus faecalis and E. faecium isolated from inpatients and outpatients in Taiwan. Diagn Microbiol Infect Dis. 2013;75:406–11. 6 Hidron AI, Edwards JR, Patel J, Horan TC, Sievert DM, Pollock DA, et al. NHSN annual update: antimicrobialresistant pathogens associated with healthcare-associated infections: annual summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2006–2007. Infect Control Hosp Epidemiol. 2008;29:996–1011. 7 Uttley AH, Collins CH, Naidoo J, George RC. Vancomycinresistant enterococci. Lancet. 1988;1:57–8. 8 Cohen MJ, Adler A, Block C, Gross I, Minster N, Roval V, et al. Acquisition of vancomycin-resistant enterococci in internal medicine wards. Am J Infect Control. 2009;37:111–6. 9 Adhikari L. High-level aminoglycoside resistance and reduced susceptibility to vancomycin in nosocomial enterococci. J Glob Infect Dis. 2010;2:231–5. 10 Arias CA, Vallejo M, Reyes J, Panesso D, Moreno J, Castaneda E, et al. Clinical and microbiological aspects of linezolid resistance mediated by the cfr gene encoding a 23S rRNA methyltransferase. J Clin Microbiol. 2008;46:892–6. 11 Gonzales RD, Schreckenberger PC, Graham MB, Kelkar S, DenBesten K, Quinn JP. Infections due to vancomycin-resistant Enterococcus faecium resistant to linezolid. Lancet. 2001;357:1179. 12 Carroll KC, Borek AP, Burger C, Glanz B, Bhally H, Henciak S, et al. Evaluation of the BD Phoenix automated microbiology system for identification and antimicrobial susceptibility testing of staphylococci and enterococci. J Clin Microbiol. 2006;44:2072–7. 13 Brigante GR, Luzzaro FA, Pini B, Lombardi G, Sokeng G, Toniolo AQ. Drug susceptibility testing of clinical isolates of streptococci and enterococci by the Phoenix automated microbiology system. BMC Microbiol. 2007;7:46.
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Urinary tract infection caused by Enterococcus isolates: aetiology and antimicrobial resistance patterns Qing-Yong Wang, Rong-Hai Li, Xiao-Hong Shang Department of Clinical Laboratory, Xiyuan Hospital, China Academy of Chinese Medical Sciences, Beijing, China The purpose of this study was to analyse the data on resistance in Enterococcus faecalis and E. faecium isolated from urine samples of inpatients from January 2010 to December 2013. Compared to E. faecalis, E. faecium isolates were significantly more resistant to ampicilin, nitrofurantoin, and ciprofloxacin in the antimicrobial agents evaluated. Both species showed higher resistance to high-level gentamicin. The rate of vancomycin-resistant enterococci (VRE) in E. faecium was higher as compared to that of E. faecalis, and we found that apparent increase in the frequency of VRE E. faecalis clinical isolates in the 4-year study period. In our study, analysis of the antimicrobial resistance trends showed resistance to linezolid and vancomycin were ,30.2% and ,20.3% in both species, respectively. Of noteworthy is the high rate of MDR in two species from inpatients. This study highlights that it is of importance for clinicians to promote rational drug utilization and delay the emergence of resistant organisms. Keywords: Antimicrobial resistance, Enterococcus spp., Urinary tract infection
Enterococcus faecium and Enterococcus faecalis are the most frequently occurring enterococcal bacteria isolated from urinary tract infections. Treatment of enterococcal infections is often difficult due to their inherent resistance to several antimicrobial agents and their tendency to acquired resistance.1 Many Enterococcus species have acquired resistance to commonly prescribed anti-enterococcal antibiotics such as beta-lactams, vancomycin, and aminoglycosides.2 Therefore, surveillance of enterococcal species distribution and determination of drug resistance patterns are paramount to empirical therapy strategies in clinical settings. We retrospectively reviewed the computerized database generated by the Clinical Microbiology Laboratory. Records from January 2010 to December 2013 were searched for patient urine samples that tested positive for enterococcal species (§104 colony forming units/ml). Bacterial identification and susceptibility to different antimicrobial agents were performed using the BD Phoenix Automated Microbiology System. The combination panel of the BD Phoenix Automated Microbiology System comprises an identification component and an antimicrobial susceptibility testing (AST) component. The AST component contains 84
Correspondence to: X.-H. Shang, Department of Clinical Laboratory, Xiyuan Hospital, China Academy of Chinese Medical Sciences, Beijing 100091, China. Email: [email protected]
ß 2015 Edizioni Scientifiche per l’Informazione su Farmaci e Terapia DOI 10.1179/1973947814Y.0000000192
wells with dried antimicrobial panels and one growth control well. Drug sensitivities were assayed with a broth-based microdilution test. Twenty-five microlitres of the standardized identification broth suspension was transferred to the AST broth followed by one freefalling drop of a redox (AST) indicator, yielding a final concentration. The detection of organism growth in the presence of an antimicrobial agent is carried out by the indicator in the system. Additional tests were conducted if the BD Phoenix Automated Microbiology System yielded results with ,90% confidence. E. faecalis ATCC 29212 and Staphylococcus aureus ATCC 29213 were used as quality control strains. Seven antimicrobial agents were examined: ampicillin, ciprofloxacin, gentamicin, linezolid, nitrofurantoin, tetracycline, and vancomycin. Multidrug resistance (MDR) was defined as non-susceptibility to at least one agent in three or more antimicrobial categories.3 Between 2010 and 2013, 252 E. faecalis isolates and 265 E. faecium isolates were identified in inpatient urine samples. The median ages of E. faecalis-positive inpatients were 71.5, 70.1, 71.1, and 69.6 years by treatment year, respectively, while the median ages of E. faecium-positive inpatients were 76.2, 73.2, 75.6, and 74.3 years. Yearly resistance rates of E. faecalis and E. faecium isolates to different antimicrobial agents are shown in Table 1. E. faecalis isolates and E. faecium isolates
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were resistant to ampicillin (9.9 and 84.9%, respectively), nitrofurantoin (11.6 and 97%, respectively), linezolid (25.8 and 20%, respectively), tetracycline (83.3 and 35.8%, respectively), and ciprofloxacin (62.7 and 92.8%, respectively). Of the antimicrobial agents evaluated, high-level resistance to gentamicin was observed in 57.5% of E. faecalis isolates and 60% of E. faecium isolates. Vancomycin had the lowest resistance rates (4.8% of E. faecalis isolates and 15.8% E. faecium isolates). MDR rates were observed for both enterococcal species in the urine of hospital inpatients (50% total for E. faecalis isolates and 92.5% total for E. faecium isolates). Approximately 31.7% of these E. faecalis isolates and 21.5% of E. faecium isolates were nonsusceptible to three classes of antimicrobial agents, 12.3% of E. faecalis isolates and 40.4% of E. faecium isolates were non-susceptible to four classes of antimicrobial agents, and 6% of E. faecalis isolates and 30.6% of E. faecium isolates were non-susceptible to more than five classes of antimicrobial agents. Interestingly, vancomycin resistance in E. faecalis isolates increased gradually from 2010 to 2013. In recent years, Enterococcus species have become increasingly important in clinical microbiology. This is owing to their ability to cause healthcare-associated infections and their increasing resistance to different antibiotics. E. faecium and E. faecalis are considered the most clinically significant enterococci. In this study, we report no significant difference between the proportion of E. faecalis and E. faecium isolates identified from urine samples of hospital inpatients. However, these data are not consistent with previous studies.4–6 This discrepancy may be ascribed to patients being in poor physical condition at the time of sampling, and therefore, more prone to opportunistic infection than the general population. Interestingly, we also determined that the median age of inpatients with E. faecium infection was higher
than that of E. faecalis-positive inpatients in each of the study years. Mobile genetic elements are important for the propagation and persistence of antimicrobial resistance in E. faecalis and E. faecium.3 In this study, we found that the antimicrobial resistance exhibited by these two enterococcal bacteria did not change significantly over the analysis period. Exceptions were slightly increased frequencies of vancomycin resistance in E. faecalis and tetracycline resistance in E. faecium from 2010 to 2013. In addition, E. faecium isolates were significantly more resistant to ampicillin, nitrofurantoin, and ciprofloxacin, but more susceptible to tetracycline, compared with E. faecalis isolates. Based on these findings, nitrofurantoin (only for uncomplicated urinary tract infections) and ciprofloxacin (only if susceptible and as part of a combination regimen) might be suitable antibiotic options for the treatment of ampicillin- and vancomycin-resistant enterococcal infections.2 MDR rates were .50% in E. faecalis isolates and .92.5% in E. faecium isolates analysed in this current study, and this may be related to widespread antibiotic use in the hospital. In particular, many of the MDR isolates were resistant to vancomycin. Vancomycin-resistant enterococci (VRE) were first reported in 1988, and have since emerged as an increasingly common clinical problem worldwide.7 In our study, the rate of vancomycin resistance in E. faecium isolates (15.8%) was higher than that of the E. faecalis isolates (4.8%). In addition, three (25%) E. faecalis isolates and eight (21.6%) E. faecium isolates showed intermediate resistance to vancomycin (data not shown). To decrease nosocomial transmission, VRE carriers should be identified and isolated upon admission, and infection control practices should be optimized.8 Moreover, it is important that clinicians obtain accurate information about Enterococcus clinical isolates that are resistant to aminoglycosides.
Table 1 Yearly resistance rates (%) exhibited by E. faecium and E. faecalis isolates to different antimicrobial agents 2010
Antibiotic
2011
2013
2010–2013
E. faecalis E. faecium E. faecalis E. faecium E. faecalis E. faecium E. faecalis E. faecium E. faecalis E. faecium (n553) (n562) (n571) (n581) (n553) (n543) (n575) (n579) (n5252) (n5265)
Ampicillin 7.5 85.5 Nitrofurantoin 9.4 95.2 Linezolid 30.2 27.4 Tetracycline 84.9 19.4 Ciprofloxacin 54.7 93.5 Vancomycin 0 19.4 Gentamicin* 52.8 58.1 Multidrug resistance (non-susceptibility 3 18.9 17.7 4 11.3 45.2 §5 7.5 27.4 MDR (§3) 37.7 90.3
15.5 81.5 7.5 79.1 8.0 91.1 9.9 12.7 98.8 11.3 93.0 12.0 98.7 11.6 22.5 12.3 28.3 20.9 24.0 21.5 25.8 78.9 33.3 84.9 46.5 85.3 45. 6 83.3 66.2 92.6 49.1 90.7 74. 7 93.7 62.7 2.8 9.9 3.8 14.0 10.7 20.3 4.8 52.1 65.4 54.7 46.5 68.0 63.3 57.5 to three or more classes of the antimicrobial agents tested in this study) 35.2 22.2 26.4 25.6 41.3 21.5 31.7 8.5 45.7 11.3 27.9 17.3 38 12.3 7.0 24.7 3.8 32.6 5.3 38.0 6.0 50.7 92.6 41.5 86.0 64 97.5 50
Note: *High-level gentamicin resistance. MDR: multidrug resistance.
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We observed no significant difference in E. faecalis and E. faecium resistance to high-level gentamicin treatment over the study period. If enterococcal strains are resistant to high-level gentamicin treatment, however, increased resistance to vancomycin might also occur.9 Of the antimicrobial agents evaluated, non-susceptibility rates to linezolid were 25.8 and 20% for E. faecalis isolates and E. faecium isolates, respectively. However, 82.5% of E. faecalis isolates and 61.5% of E. faecium isolates were in the intermediate range. Therefore, we recommend that AST be performed before commencement of therapy. Linezolid is currently approved by the United States Food and Drug Administration for treatment of infections caused by VRE. Nonetheless, sporadic resistance to linezolid has been reported.2,10,11 In conclusion, the antimicrobial resistance reported in this study highlights the need for accurate identification of enterococci species owing to their significant differences in resistance profiles. This study also concurs with previous reports which demonstrate that the BD Phoenix Automated Microbiology System rapidly identifies enterococci and accurately analyses AST in a clinical laboratory setting.12,13 Our results further support the promotion of rational drug use to delay the emergence of resistant organisms, and emphasize the importance of monitoring multidrugresistant E. faecalis and E. faecium isolates in a clinical setting. However, except for age of the outpatients, we concede that this report is limited because no other clinical characteristics were analysed. In a follow-up study, we wish to evaluate the association (if any) between enterococci-related urinary tract infections and sex distribution, type (cystitis, urethritis, or pyelonephritis), or the presence of asymptomatic or symptomatic episodes. It is also worth examining the history of antibiotic use for each patient, and whether antibiotics were indeed necessary for treatment of the documented bacteriuria.
Disclaimer Statements Contributors Qing-Yong Wang: Conception and design of study, data analysis and/or interpretation, drafting of manuscript and/or critical revision, and approval of final version of manuscript. Rong-Hai Li:
Antimicrobial resistance of enterococci
Acquisition of data. Xiao-Hong Shang: Conception and design of study, data analysis and/or interpretation, and approval of final version of manuscript. Funding None. Conflicts of interest None declare. Ethics approval None.
References 1 Murray BE. The life and times of the Enterococcus. Clin Microbiol Rev. 1990;3:46–65. 2 Arias CA, Contreras GA, Murray BE. Management of multidrug-resistant enterococcal infections. Clin Microbiol Infect. 2010;16:555–62. 3 Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, et al. Multidrug-resistant, extensively drugresistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012;18:268–81. 4 Protonotariou E, Dimitroulia E, Pournaras S, Pitiriga V, Sofianou D, Tsakris A. Trends in antimicrobial resistance of clinical isolates of Enterococcus faecalis and Enterococcus faecium in Greece between 2002 and 2007. J Hosp Infect. 2010;75:225–7. 5 Wang JT, Chang SC, Wang HY, Chen PC, Shiau YR, Lauderdale TL. High rates of multidrug resistance in Enterococcus faecalis and E. faecium isolated from inpatients and outpatients in Taiwan. Diagn Microbiol Infect Dis. 2013;75:406–11. 6 Hidron AI, Edwards JR, Patel J, Horan TC, Sievert DM, Pollock DA, et al. NHSN annual update: antimicrobialresistant pathogens associated with healthcare-associated infections: annual summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2006–2007. Infect Control Hosp Epidemiol. 2008;29:996–1011. 7 Uttley AH, Collins CH, Naidoo J, George RC. Vancomycinresistant enterococci. Lancet. 1988;1:57–8. 8 Cohen MJ, Adler A, Block C, Gross I, Minster N, Roval V, et al. Acquisition of vancomycin-resistant enterococci in internal medicine wards. Am J Infect Control. 2009;37:111–6. 9 Adhikari L. High-level aminoglycoside resistance and reduced susceptibility to vancomycin in nosocomial enterococci. J Glob Infect Dis. 2010;2:231–5. 10 Arias CA, Vallejo M, Reyes J, Panesso D, Moreno J, Castaneda E, et al. Clinical and microbiological aspects of linezolid resistance mediated by the cfr gene encoding a 23S rRNA methyltransferase. J Clin Microbiol. 2008;46:892–6. 11 Gonzales RD, Schreckenberger PC, Graham MB, Kelkar S, DenBesten K, Quinn JP. Infections due to vancomycin-resistant Enterococcus faecium resistant to linezolid. Lancet. 2001;357:1179. 12 Carroll KC, Borek AP, Burger C, Glanz B, Bhally H, Henciak S, et al. Evaluation of the BD Phoenix automated microbiology system for identification and antimicrobial susceptibility testing of staphylococci and enterococci. J Clin Microbiol. 2006;44:2072–7. 13 Brigante GR, Luzzaro FA, Pini B, Lombardi G, Sokeng G, Toniolo AQ. Drug susceptibility testing of clinical isolates of streptococci and enterococci by the Phoenix automated microbiology system. BMC Microbiol. 2007;7:46.
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