JAC Advance Access originally published online on February 11, 2003
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Journal of Antimicrobial Chemotherapy (2003) 51, 639-649
© 2003 The British Society for Antimicrobial Chemotherapy
Activity of daptomycin against susceptible and multidrug-resistant Gram-positive pathogens collected in the SECURE study (Europe) during 2000–2001
1 Focus Technologies, 13665 Dulles Technology Drive, Suite 200, Herndon, VA 20171-4603; 2 Focus Technologies, Franklin, TN 37064, USA; 3 Focus Technologies, Koninginneweg 11, 1217 KP Hilversum, The Netherlands
Received 27 August 2002; returned 3 December 2002; revised 17 December 2002; accepted 20 December 2002
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Abstract |
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Antibiotic resistance was prevalent in Gram-positive pathogens collected from 40 sites in 15 European countries during 2000–2001. Among Staphylococcus aureus, 27.3% of all isolates submitted were resistant to oxacillin and ranged from 0% of isolates from the Netherlands to 36.9% of isolates from Portugal. The overall prevalence of vancomycin-resistant Enterococcus faecium was 25.1%, with Italy submitting the largest percentage of resistant isolates (60.6%). For Streptococcus pneumoniae, 9.4% of all isolates collected were resistant to penicillin with variation by country from 0% in the Netherlands to 20.7% in Portugal. Multidrug resistance (MDR), defined as concurrent resistance to three or more antimicrobials of different chemical classes, was observed in 24.6% of S. aureus, 19.6% of E. faecium and 3.6% of S. pneumoniae. The directed spectrum agents daptomycin, linezolid and quinupristin–dalfopristin were active in vitro against all isolates regardless of their resistance to other agents. Daptomycin and quinupristin–dalfopristin (MIC90s 0.5 mg/L) were equally active against oxacillin-resistant S. aureus compared with linezolid (MIC90 2 mg/L). The activities of daptomycin, quinupristin–dalfopristin and linezolid were not affected by resistance to vancomycin in E. faecium (MIC90s of 4, 2 and 2 mg/L, respectively). Daptomycin was more active against penicillin-resistant S. pneumoniae (MIC90 0.25 mg/L) than was quinupristin–dalfopristin (MIC90 0.5 mg/L) or linezolid (MIC90 2 mg/L). Daptomycin was highly active against clinically important Gram-positive pathogens, including those that were multiply resistant to currently available agents. The results of this study provide a benchmark of the activity of daptomycin against contemporary European isolates and will serve as a baseline to monitor future changes in the susceptibility of these organisms to daptomycin.
Keywords: daptomycin, Gram-positive pathogens, multidrug-resistant
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Introduction |
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The last two decades have seen the emergence and spread of resistant Gram-positive cocci and increased concern regarding the lack of new agents that are effective against these organisms.1–3 In many countries, oxacillin-resistant Staphylococcus aureus, vancomycin-resistant enterococci and penicillin-resistant Streptococcus pneumoniae are already prevalent and resistance continues to increase. Multi-resistant Gram-positive pathogens represent a hurdle for the pharmaceutical industry to overcome in terms of developing new agents that maintain activity against key pathogens and have the ability to evade existing resistance mechanisms. In recent years, a number of new directed spectrum agents such as daptomycin, quinupristin–dalfopristin and linezolid have been developed that are active against Gram-positive cocci. Quinupristin–dalfopristin and linezolid are approved for use in several countries for the therapy of infections caused by resistant Gram-positive organisms. Daptomycin is a cyclic lipopeptide that is currently in Phase III clinical trials for the treatment of serious Gram-positive infections in hospitalized patients.3 The agent has already been shown to be effective in the treatment of skin and soft tissue infections and bacteraemia in Phase II studies.4,5 Daptomycin has a unique chemical structure and a novel mode of action5 that enables it to target organisms that are resistant or multiply resistant to other classes of agents.4,6–9 The objective of the current study was to determine the activity of daptomycin against contemporary Gram-positive pathogens from 40 sites in 15 different European countries, including isolates that were susceptible, resistant and multi-resistant to currently marketed agents. The study will serve as a benchmark for the activity of daptomycin before its commercial introduction in various European countries and will provide a baseline for studies to monitor future changes in susceptibility to daptomycin.
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Materials and methods |
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Organism collection and identification
During 2000–2001, 5948 Gram-positive isolates were collected from patient specimens at 40 hospitals distributed throughout Europe. In total, 1222 S. aureus, 1040 coagulase-negative staphylococci, 1840 Enterococcus faecalis, 454 Enterococcus faecium, 160 Enterococcus species (defined as non-E. faecalis and non-E. faecium), 865 S. pneumoniae and 367 Streptococcus agalactiae were collected. Isolates were transported using Amies swabs (Technical Consultants Ltd, Lancashire, UK) to our laboratory (Focus Technologies, Herndon, VA, USA) for in vitro antimicrobial susceptibility testing. Upon receipt, isolates were subcultured on to 5% sheep blood agar and their identities confirmed. S. aureus were confirmed using the slide coagulase test; coagulase-negative staphylococci were confirmed by the tube coagulase test and Vitek (bioMérieux, Hazelwood, MO, USA). All enterococci were confirmed using the PYR test and speciated using Vitek. Enterococci with unique phenotypes (e.g. quinupristin–dalfopristin-resistant E. faecium) were verified through either supplemental biochemical testing or PCR using D-Ala-D-Ala ligase gene (ddl) primers specific for E. faecalis and E. faecium.10 S. pneumoniae were confirmed using optochin disc testing and S. agalactiae were confirmed by the observation of ß-haemolysis and the PathoDx Strep Grouping agglutination test (Remel, Lenexa, KS, USA).
Antimicrobial testing
All isolates were tested by broth microdilution according to NCCLS guidelines.11 Isolates were subcultured on to 5% sheep blood agar and grown overnight (20–24 h). Previously frozen Sensititre microdilution panels manufactured by TREK Diagnostics (Westlake, OH, USA) were used with wells containing daptomycin supplemented to physiological levels (50 mg/L) of Ca2+. MICs were interpreted as susceptible, intermediate or resistant according to NCCLS guidelines,12 where available. S. aureus ATCC 29213, E. faecalis ATCC 29212 and S. pneumoniae ATCC 49619 were tested daily as quality control organisms.
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Results |
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The results in Table 1 show the activities of daptomycin and comparator agents against Gram-positive clinical isolates collected from 15 countries in Europe during 2000–2001. The results compare the activities of all the agents tested against isolates that were susceptible and resistant to agents commonly used to stratify resistance, such as oxacillin for staphylococci, vancomycin for enterococci and penicillin for streptococci.
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Activity against staphylococci
Resistance to oxacillin among the 1222 isolates of S. aureus collected from the 15 countries was 27.3%. Resistance to oxacillin also resulted in cross-resistance to many other agents including ciprofloxacin, erythromycin, clindamycin and gentamicin. The activities of daptomycin and linezolid were not affected by resistance to oxacillin since the MIC90s of those agents were the same for both oxacillin-susceptible and -resistant isolates. Daptomycin and quinupristin–dalfopristin (MIC90 0.5 mg/L) were the most active agents against oxacillin-resistant S. aureus compared with linezolid (MIC90 2 mg/L). Among coagulase-negative staphylococci, the overall oxacillin resistance rate was even higher (53.3%) than for S. aureus. Oxacillin-resistant coagulase-negative staphylococci were also cross-resistant to many other agents such as erythromycin, gentamicin, ciprofloxacin and co-trimoxazole. For the oxacillin-resistant coagulase-negative staphylococci, quinupristin–dalfopristin, daptomycin and linezolid had MIC90s of 0.25, 0.5 and 2 mg/L, respectively.
Activity against enterococci
The overall rate of vancomycin resistance in E. faecium was 25.1%. However, the vancomycin-susceptible isolates were highly resistant to ampicillin and ciprofloxacin with resistance rates of 64.6% and 63.1%, respectively. Among the vancomycin-resistant E. faecium isolates, resistance to ampicillin and ciprofloxacin increased to 83.3% and 79.8%, respectively. The activity of teicoplanin was adversely affected by cross-resistance to vancomycin, as resistance increased from 0% among vancomycin-susceptible isolates to 78.1% among the vancomycin-resistant isolates. Sixteen isolates (3.5%) of E. faecium were resistant to quinupristin–dalfopristin; 10 of the isolates were vancomycin susceptible and six were vancomycin resistant. The activities of linezolid, quinupristin–dalfopristin and daptomycin were not affected by resistance to vancomycin since the MIC90s of all three agents were 2, 2 and 4 mg/L, respectively, for both vancomycin-susceptible and -resistant organisms. Among E. faecalis, the overall vancomycin resistance rate was 2.2%. Ciprofloxacin was the least effective agent against vancomycin-susceptible E. faecalis, with 521/1798 isolates (29.0%) being resistant. The vancomycin-resistant isolates of E. faecalis were also increasingly resistant to teicoplanin and ciprofloxacin with resistance rates of 85.0% and 75.0%, respectively. The activities of daptomycin and linezolid were unaffected by cross-resistance to vancomycin, and both agents demonstrated equivalent activity based on MIC90s (MIC90 2 mg/L). Amongst the other Enterococcus species, 10.6% of the isolates were resistant to vancomycin. The least effective agents were ampicillin and ciprofloxacin with resistance rates of 37.5% and 31.3%, respectively. Linezolid and daptomycin had MIC90s of 2 and 4 mg/L, respectively.
Activity against streptococci
Among the 865 isolates of S. pneumoniae tested, 619 (71.6%) were penicillin susceptible, 165 (19.1%) were penicillin intermediate and 81 (9.4%) were penicillin resistant. Penicillin resistance correlated with reduced susceptibility to the other ß-lactams (co-amoxiclav, cefuroxime, ceftriaxone), erythromycin, clindamycin and co-trimoxazole. The penicillin susceptibility status of the isolates had no effect on the activity of vancomycin, levofloxacin or the newer directed spectrum agents, daptomycin, quinupristin–dalfopristin and linezolid, as the MIC90 of each agent was the same for both penicillin-susceptible and -resistant isolates. Based on MIC90s, daptomycin was the most active agent against penicillin-resistant S. pneumoniae (MIC90 0.25 mg/L) compared with quinupristin–dalfopristin (MIC90 0.5 mg/L) and linezolid (MIC90 1 mg/L). Among S. agalactiae, clindamycin (6.5%) and erythromycin (10.4%) displayed the highest rates of resistance compared with all other agents tested. The ß-lactam agents (penicillin, co-amoxiclav, cefuroxime, ceftriaxone) were very active, with MIC90s of 
0.12 mg/L. Daptomycin and quinupristin–dalfopristin demonstrated equally potent activities against S. agalactiae (MIC90s 0.25 mg/L) compared with linezolid (MIC90 1 mg/L).
Prevalence of MDR
Table 2 shows the prevalence of multidrug-resistant (MDR; defined as concurrent resistance to three or more agents from different antimicrobial classes) phenotypes in S. aureus, E. faecium and S. pneumoniae collected in this study. Among S. aureus isolates, the most prevalent MDR phenotype included resistance to ciprofloxacin, erythromycin and oxacillin, and was demonstrated by 10.9% of the isolates tested. In addition, 10.1% of S. aureus isolates were also resistant to four agents, and 2.0% of isolates were resistant to five agents (ciprofloxacin, erythromycin, gentamicin, oxacillin, co-trimoxazole). Among the 454 isolates of E. faecium tested, 89 (19.6%) were MDR, with the most prevalent phenotype being resistance to ampicillin, ciprofloxacin and vancomycin. In S. pneumoniae, resistance to penicillin, erythromycin and co-trimoxazole was the most common MDR phenotype and was present in 3.4% of the isolates. The results in Figure 1 show that there were no major differences in the MIC distributions (modal MICs one-doubling dilution) for daptomycin against MDR and non-MDR isolates of S. aureus, E. faecalis, E. faecium and S. pneumoniae.
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National variations in the numbers of resistant organisms
The numbers of resistant isolates submitted by each European country are shown in Table 3. Oxacillin-resistant S. aureus, vancomycin-resistant enterococci and penicillin-resistant S. pneumoniae were prominent among isolates collected from most of the European countries. However, there were significant differences in the numbers of resistant isolates collected from the various countries that were used to profile the activity of daptomycin. Among S. aureus, 4.0% of the isolates collected were resistant to oxacillin in the Netherlands compared with 36.9% of the isolates from Portugal. The percentage of E. faecium isolates resistant to vancomycin ranged from 0% in Switzerland and Scandinavia (Sweden, Denmark and Finland) to 60.6% in Italy. Among S. pneumoniae, no penicillin-resistant isolates were collected from the Netherlands compared with 20.7% of isolates from Portugal. There is also considerable countrywide variation in MDR phenotypes for the different Gram-positive organisms. For example, MDR S. aureus ranges from 2.0% in the Netherlands to 36.7% in Ireland. There was little or no variation in the activity of daptomycin (based on MIC ranges and MIC90s) regardless of phenotype, national origin of isolates or varying numbers of resistant isolates per country.
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Discussion |
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This study was designed to assess the activity of daptomycin against susceptible, resistant and MDR Gram-positive pathogens collected from laboratories in 15 countries in Europe during 2000–2001. Daptomycin was highly active against all the clinically important Gram-positive pathogens, including those that were resistant to other agents. Although daptomycin is currently in Phase III clinical development,3,13 in vitro data on the drug were first reported >14 years ago.14–19 The MIC90s of daptomycin obtained in this study with contemporary isolates of staphylococci, streptococci and enterococci from Europe were in agreement with those reported in the studies conducted in 1987. These results indicate that there has been little or no change in the susceptibility of Gram-positive pathogens to daptomycin during the past 14 years, and currently marketed agents have not provided any pressure for the selection of daptomycin-resistant isolates. The activity of daptomycin in this study was also similar to the results reported for clinical isolates collected and tested in a study conducted in the USA during 1999,8 indicating that isolates from both continents were equally susceptible to daptomycin. For example, the MIC90s of daptomycin for oxacillin-resistant S. aureus, penicillin-resistant S. pneumoniae and vancomycin-resistant E. faecium were 0.5, 0.25 and 4 mg/L, respectively.8
The in vitro antimicrobial activity of daptomycin is well known to be dependent on the physiological concentration of calcium in the test medium.14,20–23 Many of the early studies to evaluate the activity of daptomycin, including one for proposed staphylococcal breakpoints,19 were conducted in cation-supplemented Mueller–Hinton broth (CSMHB) adjusted to physiological levels of Ca2+ (50 mg/L). The current medium recommended by the NCCLS is cation-adjusted Mueller–Hinton broth (CAMHB), which contains 20–25 mg/L of Ca2+. Daptomycin is typically two- to four-fold more active when tested in media supplemented to contain the physiologically relevant concentration of calcium ions. The importance of the calcium content on testing the activity of daptomycin is also proving important in proposing breakpoints that are likely to be recommended by various agencies in Europe. A recent study conducted in the UK, testing the activity of daptomycin against 328 recent clinical isolates, showed that daptomycin had an MIC90 of 1 mg/L for staphylococci and streptococci, and an MIC90 of 2 mg/L for the enterococci.24 The effect of calcium concentration on daptomycin activity was highlighted and a tentative breakpoint of 2 mg/L for staphylococci, streptococci and enterococci was proposed using the methods of the British Society for Antimicrobial Chemotherapy (BSAC). However, it is clear that the results from the clinical trials will be important in establishing the final breakpoints that are adopted, especially for organisms such as E. faecium, for which the MIC90 of daptomycin was 4 mg/L.
Since many European countries use different susceptibility testing methods and interpretative criteria, it is often difficult to assess or compare resistance rates from studies generated and reported in different countries.25 In this study, all isolates collected in each country were tested at a central laboratory using NCCLS-recommended methodologies to compare resistance in each country. A few surveillance studies have focused on antimicrobial resistance in Gram-positive cocci in countries in Europe. Many of the European studies that have been conducted have investigated enterococcal resistance to the glycopeptides vancomycin and teicoplanin.26–28 The results of this study confirm previous observations showing that resistance to vancomycin and teicoplanin is observed more frequently among E. faecium than among E. faecalis. For S. pneumoniae, penicillin resistance varies considerably within different countries in Europe. A surveillance study conducted in 1997–1998 showed a high prevalence of penicillin-resistant S. pneumoniae in Spain and France,29 and this was also true for the isolates collected in this study conducted in 2000–2001. There is also very little data on the prevalence of MDR Gram-positive bacteria in Europe. However, reports are now beginning to appear on multi-resistant S. pneumoniae in the USA and suggest its prevalence is increasing.30,31 There is a need to monitor antimicrobial resistance in Europe since increased travel and trade within the European Union make it more likely that the dissemination of resistant pathogens will increase. This is already apparent for methicillin-resistant S. aureus, which was once primarily a nosocomial pathogen and is now being detected in the community setting.32
The results of this study show that there is significant resistance to selected agents in many clinically important Gram-positive pathogens in many of the European countries studied. Even more alarming is the fact that resistance is not restricted to a single agent but may involve resistance to multiple agents. The new directed spectrum agents are effective against clinically important pathogens. As expected, these agents are also active against organisms that are multidrug resistant, since their use is currently not widespread.33 The ability of the newer directed spectrum agents to circumvent multiple resistance mechanisms is due to their novel targets and mechanisms of action, which it is to be hoped will provide these agents with a long period of therapeutic utility. For example, the ability of daptomycin to circumvent existing resistance mechanisms is due to its novel mode of action targeting the function of the bacterial plasma membrane.5,34 Unfortunately, the evolutionary ability of microbes to develop resistance mechanisms to counteract novel pharmacophores will always exist. The results of this study have already shown that there were 16 isolates of E. faecium from seven countries (Austria, Belgium, France, Germany, Greece, Portugal and Spain) that were resistant to quinupristin–dalfopristin. Linezolid-resistant isolates were not detected in this study; however, there have been reports on linezolid-resistant isolates of S. aureus and E. faecium in the USA35–37 and recently the UK.38 In vitro studies to generate spontaneous daptomycin-resistant mutants of S. aureus, S. epidermidis, E. faecalis and E. faecium have proved unsuccessful.34 Serial passage of S. aureus in the presence of daptomycin did generate resistant mutants that had daptomycin MICs that were 8- to 32-fold higher than the parent strain; however, many resistant mutants had significant growth defects, alteration of membrane potential and reduced virulence.
Daptomycin was highly active against both MDR and non-MDR isolates of S. aureus, E. faecium and S. pneumoniae. This study confirms that resistance, including multidrug resistance, is prevalent in Gram-positive pathogens in many countries in Europe during 2000–2001. The results of the study will be important in benchmarking the antimicrobial activity of daptomycin against European isolates and will serve as a baseline for future studies to monitor changes in the susceptibility of these organisms to daptomycin following its approval and clinical use in European countries.
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Acknowledgements |
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This study was funded by Cubist Pharmaceuticals, Inc., Lexington, MA, USA.
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Footnotes |
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* Corresponding author. Tel: +1-703-480-2575; Fax: +1-703-480-2654; E-mail: jkarlowsky{at}focusanswers.com
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References |
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J. N. Steenbergen, J. Alder, G. M. Thorne, and F. P. Tally Daptomycin: a lipopeptide antibiotic for the treatment of serious Gram-positive infections J. Antimicrob. Chemother., March 1, 2005; 55(3): 283 - 288. [Abstract] [Full Text] [PDF]
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E. Senneville, L. Legout, M. Valette, Y. Yazdanpanah, F. Giraud, E. Beltrand, G. Obert, L. Dubreuil, H. Migaud, and Y. Mouton Risk factors for anaemia in patients on prolonged linezolid therapy for chronic osteomyelitis: a case-control study J. Antimicrob. Chemother., October 1, 2004; 54(4): 798 - 802. [Abstract] [Full Text] [PDF]
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B. Dvorchik, R. D. Arbeit, J. Chung, S. Liu, W. Knebel, and H. Kastrissios Population Pharmacokinetics of Daptomycin Antimicrob. Agents Chemother., August 1, 2004; 48(8): 2799 - 2807. [Abstract] [Full Text] [PDF]
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B. Dvorchik and D. Damphousse Single-Dose Pharmacokinetics of Daptomycin in Young and Geriatric Volunteers J. Clin. Pharmacol., June 1, 2004; 44(6): 612 - 620. [Abstract] [Full Text] [PDF]
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