JAC Advance Access published online on June 4, 2007
Journal of Antimicrobial Chemotherapy, doi:10.1093/jac/dkm137
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Systematic review |
Daptomycin for endocarditis and/or bacteraemia: a systematic review of the experimental and clinical evidence
1 Alfa Institute of Biomedical Sciences (AIBS), Athens, Greece 2 Department of Medicine, Tufts University School of Medicine, Boston, MA, USA
* Correspondence address. Alfa Institute of Biomedical Sciences (AIBS), 9 Neapoleos Street, 151 23 Marousi, Greece. Tel: +30-694-611-0000; Fax: +30-210-683-9605; E-mail: m.falagas{at}aibs.gr
Received 8 February 2007; returned 21 March 2007; revised 30 March 2007; accepted 11 April 2007
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Abstract |
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Background: Endocarditis and bacteraemia are devastating infections with high mortality. Gram-positive cocci are the most commonly isolated pathogens. In an era of multidrug-resistant pathogens, the evaluation of new treatment options is important. Daptomycin is a cyclic lipopeptide that is active against most of these pathogens. Furthermore, it is a bactericidal antibiotic, a factor that is frequently considered in the choice of treatment of patients with bacteraemia and endocarditis.
Methods: We performed a systematic review of the evidence for the effectiveness of daptomycin in the treatment of patients and animals with endocarditis and/or bacteraemia. We searched PubMed and Scopus databases for relevant studies. Case reports, case series, controlled trials, randomized controlled trials and comparative studies using experimental animal models were included.
Results: The most reliable information comes from the single multicentre randomized controlled trial conducted on this issue, which showed that daptomycin is a promising antibiotic for the treatment of patients with Staphylococcus aureus bacteraemia and endocarditis. The experimental models indicate that the combination of daptomycin with rifampicin or gentamicin can improve outcomes further. Finally, in several of the published relevant case reports daptomycin was administered in patients with haematological malignancies.
Conclusions: Daptomycin is a promising antibiotic that has been already approved for the treatment of patients with right-sided endocarditis and bacteraemia. However, the available clinical evidence is limited and further evaluation of the antibiotic is warranted. The commonly reported de novo development of resistance is a major concern that may limit its use. More controlled trials are needed, especially for patients infected with multidrug-resistant Gram-positive cocci, comparing daptomycin with other available treatment options, including glycopeptides and oxazolidinones.
Key Words: lipopeptides , antibiotics , treatment
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Introduction |
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Endocarditis and bacteraemia are devastating infections associated with considerable mortality, which reaches 16% to 25% of the affected individuals.1–4 Their microbiology includes both Gram-positive and Gram-negative bacteria as well as fungi. Among the Gram-positive microbes, the highly resistant staphylococcal and enterococcal species are of extreme importance because they are related with more severe disease and higher mortality.5
Antibiotics with bactericidal activity have been considered the gold standard for the treatment of patients with deep tissue infections such as endocarditis and bacteraemia. Daptomycin, a fermentation product produced by Streptomyces roseosporus, is a cyclic lipopeptide antibiotic with potent bactericidal activity against most Gram-positive organisms, including multiple antibiotic-resistant strains.6 The activity of daptomycin depends on the presence of physiological levels of free calcium. Daptomycin has a novel mechanism of action—insertion into and disruption of the functional integrity of the Gram-positive plasma membrane—which results in rapid loss of membrane potential, cessation of macromolecular synthesis and cell death.7 It has been approved for the treatment of patients with skin and soft tissues infections. Although it has been recently approved for the treatment of patients with bacteraemia and right-sided endocarditis, the available evidence to date for its effectiveness for the treatment of such patients is limited. Thus, we sought to review systematically the available evidence, including animal and human studies, regarding the effectiveness and safety of daptomycin for the treatment of endocarditis and bacteraemia.
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Methods |
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Literature search
We carried out a systematic review of the current evidence for the effectiveness of daptomycin in the treatment of patients and animals with endocarditis and/or bacteraemia. Two authors (K. P. G. and F. N.) independently searched PubMed (January 1985 to January 2007) and Scopus (1986–2006) in order to identify articles appropriate for inclusion in the review. They also searched reference lists of retrieved articles for other relevant papers. Search terms included ‘daptomycin’, ‘endocarditis’, ‘heart disease’ and ‘bacteremia’.
Study selection and data extraction
Potentially relevant studies were selected according to title and abstract review of all initially identified articles. Case reports, case series, controlled trials, randomized controlled trials (RCTs) and studies using experimental animal models were included, while review articles were excluded from this review.
Consequently, any study assessing the effectiveness and safety of daptomycin for the treatment of endocarditis or bacteraemia was eligible for inclusion in the review. Animal studies were eligible for inclusion in the review only if the studied animals were randomly assigned to each treatment group. A group of animals receiving no treatment should have been included in the study. No restriction on the studied microorganism was set. Decreases in the number of colony forming units of the vegetations or sterilization of the resected valves were the primary outcomes in these studies.
In case reports and case series, patients receiving treatment with daptomycin for endocarditis or bacteraemia were evaluable for the analysis, if age, gender, medical history, reason for daptomycin administration and/or outcome of the infection were available. All patients with endocarditis according to Duke's criteria who received daptomycin as a monotherapy or as a part of the regimen were included.8,9 Bacteraemia was defined as culture of 
1 blood sample that yielded Gram-positive cocci (2 for coagulase-negative staphylococci) and clinical profile compatible with a diagnosis of bacteraemia with one of the following findings: fever, chills, leucocytosis with prominent left shift, changes in vital signs, signs of septic shock (decreased peripheral perfusion or hypotension) and petechiae or purpura.
Case reports and case series were excluded if no data regarding the effectiveness of daptomycin for the treatment of patients with endocarditis and bacteraemia were available. Reports that used daptomycin for the treatment of infections due to microorganisms that were not susceptible to this antibiotic were excluded. In addition, case reports were excluded when the duration of daptomycin administration was not adequate for the treatment of such patients.
All controlled trials and RCTs identified through the search process were eligible for inclusion in the review. Effectiveness of treatment, adverse events due to the studied medications and mortality were the outcome measures for the trials.
The treatment outcome was defined as cure when the patient general status had improved, the blood cultures were negative, and in the cases of endocarditis the transthoracic echocardiograph (TTE) or transoesophageal echocardiograph (TEE) revealed no evidence of persistent vegetations on the infected valve according to the information provided by the authors of each case report. Treatment outcome was defined as improvement when there were no signs of persistent infection (negative blood cultures, no evidence of persistent vegetations) but the duration of the treatment period was not adequate or the infection relapsed after discharge from hospital or the patient died due to other reasons during the same hospitalization but there was evidence for resolution of the infection. Duration of treatment was considered as adequate when it lasted for a week or more. Treatment failure was defined as persistence of signs, symptoms and laboratory or imaging findings of infective endocarditis or bacteraemia despite appropriate antibiotic treatment with daptomycin, relapse of the infection or death due to infective endocarditis or bacteraemia or their complications.
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In total, 102 potentially relevant articles identified from the PubMed database; 6 additional articles were identified from the Scopus database. Thus, 108 articles were examined for potential inclusion in our review. Seventy-three studies were excluded from the review because they were not directly relevant to the focus of our study or because daptomycin administration was not appropriate. Finally, 35 studies were selected for further evaluation and are presented in the Tables below.
A summary of the available evidence regarding the effectiveness of daptomycin for the treatment of endocarditis in experimental models is shown in Table 1.10–20 Eleven reports of experimental models of aortic valve endocarditis in rats and rabbits comparing the effectiveness of daptomycin with vancomycin, teicoplanin, amoxicillin and penicillin G were conducted. Several strains of potential pathogens were used. The most common Gram-positive coccus used in these models was Staphylococcus aureus [six strains of methicillin-susceptible S. aureus (MSSA) and five strains of methicillin-resistant S. aureus (MRSA)] followed by Enterococcus spp. [three strains of vancomycin-resistant Enterococcus (VRE) and seven strains of vancomycin-susceptible Enterococcus].
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MRSA endocarditis models. In all models, the administration of daptomycin resulted in a significant reduction of the bacterial counts of the aortic vegetations in comparison with the no-treatment arm. In addition, two models reported that the addition of rifampicin in the daptomycin regimen resulted in a further significant reduction in the counts of vegetations when compared with daptomycin alone.11,12 The assumption that the administration of daptomycin twice daily could result in a better outcome than its administration in a single dose12 was not verified in other models.13 There was no significant difference in the effectiveness of daptomycin in comparison with vancomycin and teicoplanin. The number of sterile valves after administration of daptomycin varied between models (range 10% to 100%), but there was no difference between daptomycin and glycopeptides in the individual models. None of the models compared daptomycin with linezolid or quinupristin–dalfopristin.
MSSA endocarditis models. The available data from experimental models are contradictory. In one model, the administration of daptomycin twice daily (5 mg/kg every 12 h) was more effective in reducing bacterial counts of vegetations than 10 mg/kg of daptomycin once daily and vancomycin twice daily.12 In two other models, daptomycin in adequate dosage was either more effective than or at least as effective as vancomycin, depending on the strain used for infection.15,16 Finally, daptomycin was as effective as antistaphylococcal penicillins in reducing bacterial counts of aortic valve vegetations.15,18 Accordingly, more excised valves were sterilized after the administration of daptomycin than with vancomycin; on the contrary, antistaphylococcal penicillins were as effective as daptomycin on this issue.
Enterococcus spp. endocarditis models. Enterococcus faecalis was the infecting organisms in six models.10,14,17–20 In all of them, treatment with daptomycin was as effective as glycopeptides and penicillins in reducing the bacterial count of aortic valve vegetations. Daptomycin was more effective than amoxicillin or ampicillin alone when penicillin-resistant isolates were used, but this difference was eliminated when the combination of amoxicillin with gentamicin or ampicillin with sulbactam was used.
VRE endocarditis models. Two models used VRE faecium as the offending organism10,13 Daptomycin was as effective as teicoplanin for the reduction of bacterial counts of aortic valve vegetations. The combination of daptomycin with gentamicin was the single most effective regimen that resulted in a significant reduction of the bacterial counts of the vegetations as well as an increased number of sterile valves. Daptomycin was more effective than amoxicillin for the treatment of endocarditis due to VRE faecium, but it was as effective as amoxicillin for VRE faecalis endocarditis.10
Bacteraemia models. One experimental model with S. aureus bacteraemia has been conducted, in which daptomycin was compared with vancomycin.21 Two different dosage regimens were used for each antibiotic. There was no significant difference in survival in any of the four treatment groups.
Endocarditis. A summary of the evidence from published case reports and case series to date with use of daptomycin for the treatment of patients with bacterial endocarditis is shown in Table 2.22–33 A total of 19 cases were retrieved. Information regarding the demographics, clinical data, type of heart valve and other variables were not reported in a few cases, thus the denominator varies in the following proportions of cases; 47.3% (9/19) of the affected individuals were men. The median age of patients was 60.5 years (range 13–92). Prosthetic valve infective endocarditis accounted for 10.5% (2/19) of cases. Three patients had undergone bone marrow transplantation, three patients had chronic renal failure, two had coronary artery disease and two had systemic lupus erythematosus. No history was available for seven of the included patients.
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Blood cultures were performed and proved positive for all but one of the reviewed patients. S. aureus was the predominant isolated pathogen (seven isolates of MRSA and five isolates of MSSA) followed by VRE (four isolates). Vancomycin-susceptible E. faecalis, coagulase-negative Staphylococcus and Corynebacterium striatum were the remaining isolates. One of the blood cultures yielded two microorganisms (MRSA and E. faecalis).
In most cases, the reason for administration of daptomycin was treatment failure with other antibiotics (mainly vancomycin 15/19, 79%) or combinations of antibiotics. In one case, daptomycin was administered because there was increased possibility for adverse effects from linezolid administration to a patient with splenectomy and bone marrow transplantation. In another patient, daptomycin was administered empirically because a staphylococcal infection was presumed. Finally, no reason was reported for one case.
The median duration of daptomycin administration was 28 days (range 8–91). The outcome at the end of treatment was good for the majority of patients with endocarditis treated with daptomycin (11/19 cases, 57.8%). One of these patients died of co-morbidity during the follow-up period and one more due to relapse of the infection. The general status as well as the laboratory and/or imaging findings of three (15.8%) additional patients improved after the administration of daptomycin; one of these patients died after withdrawal of life support due to severe haemorrhagic pancreatitis and acute respiratory distress syndrome. Failure of treatment with daptomycin was seen in five cases (26.3%); four of these patients died. The overall mortality of the reviewed case reports was 38.9% (7/18).
Information regarding the possible adverse effects associated with daptomycin administration was available in 10 cases. Adverse effects developed in five patients (50). Increase in the levels of creatine kinase (CK) was reported in four of them; the remaining patient developed mild deterioration of renal function. Two patients discontinued treatment with daptomycin. One of these patients required intubation after the development of eosinophilic pneumonia that was attributed to the daptomycin administration. None of the treated isolates developed resistance or decreased susceptibility to daptomycin.
Bacteraemia. A summary of the evidence from published case reports and case series to date with use of daptomycin for the treatment of patients with bacteraemia is shown in Table 3.28,34–44 A total of 41 cases was retrieved. Information regarding the demographics, clinical data, type of heart valve and other variables were not reported in a few cases, thus the denominator varies in the following proportions of cases; 58.5% (24/41) of the affected individuals were men. The median age of patients was 58 years (range 18–87). Sixteen patients had haematological diseases (including acute myeloid leukaemia) and nine of them had undergone bone marrow transplantation, four patients had chronic renal failure, four had bone and joint infections, two had liver cirrhosis and two had pyelonephritis. No history was available for 12 of the included patients.
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Blood cultures were performed and proved positive for all but one of the reviewed patients. VRE (24/47 isolates, 51.1%) was the predominant isolated pathogen followed by S. aureus [12 isolates of MRSA (25.5%) and 2 isolates of MSSA (4.3%)]. Gram-negative bacteria (three isolates), coagulase-negative Staphylococcus (two isolates), vancomycin-resistant Leuconostoc mesenteroides (two isolates), vancomycin-susceptible Enterococcus durans (one isolate) and Streptococcus pneumoniae (one isolate) were the remaining isolates.
In most cases, the reason for administration of daptomycin was treatment failure with another antibiotic [mainly vancomycin (16/33, 48.5%) and linezolid (8/33, 24.2%)] or a combination of antibiotics. In 11 cases, daptomycin was administered according to a therapeutic protocol. No reason was reported for five cases.
The median duration of daptomycin administration was 14 days (range 3–56). The outcome at the end of treatment was good for the majority of patients with bacteraemia treated with daptomycin (27/41 cases, 65.9%). One of these patients died of co-morbidity during the follow-up period. Failure of treatment with daptomycin was seen in 14 cases (34.1%); 10 of these patients died. The overall mortality of the reviewed case reports was 26.8% (11/41). Adverse effects developed in six patients for whom data on this issue were available. Increase in the levels of creatinine kinase (CK) was reported in one of them; the other patients developed renal failure. Five of the treated isolates developed resistance to daptomycin during the treatment period. However, no data were available for 32 patients.
Only one open-label RCT45 was conducted comparing daptomycin with antistaphylococcal penicillins or vancomycin (standard therapy), in combination with gentamicin for the treatment of patients with endocarditis or bacteraemia due to methicillin-susceptible and methicillin-resistant S. aureus. Patients were randomly assigned with the use of a centralized computer-generated block randomization schedule that was designed to achieve a 1:1 ratio of patients. All data were reviewed regularly by an independent committee. Of the 246 randomized patients, 235 were eligible for the analysis of effectiveness. Overall, daptomycin and standard therapy were equally effective for the treatment of patients with endocarditis and bacteraemia (61% versus 60.9% at the end of treatment and 44.2% versus 41.7% at the test-of-cure visit 42 days after the end of treatment). Success rates favoured daptomycin over vancomycin among patients who were infected with MRSA (44.4% for daptomycin versus 31.8% for standard therapy, P = 0.28), but were higher among patients receiving standard therapy for MSSA infection (44.6% for daptomycin versus 48.6% for standard therapy, P = 0.74). The authors did not distinguish between patients with definite endocarditis and bacteraemia on this issue. In patients with baseline diagnosis of definite and possible MRSA endocarditis, daptomycin was also more effective than standard therapy, but without statistical significance (41.7% versus 28.9%). Daptomycin was as effective as standard therapy for the treatment of patients with staphylococcal (both MRSA and MSSA) definite endocarditis (32.1% versus 36.0%) and bacteraemia (47.8% versus 43.3%). Patients with MRSA bacteraemia and right-sided endocarditis showed similar success rates when treated with either daptomycin or vancomycin, suggesting that daptomycin may be considered an alternative to vancomycin in the management of these infections.
Elevated CK levels were reported in more patients treated with daptomycin (6.7% versus 0.9%, P = 0.04), while more patients receiving standard therapy had renal impairment (18.1% versus 6.7%, P = 0.009). The number of patients treated with gentamicin was higher in the standard therapy group (93% versus 0.8%). The MIC for seven isolates increased from baseline values in patients treated with daptomycin, but none of these isolates developed resistance to daptomycin; however, six of these seven patients had microbiological failure. Increase in the MIC of vancomycin was also noticed in four isolates. Finally, mortality was similar between the compared regimens (15% versus 16%).
Several limitations of this RCT should be taken into account. First, the number of enrolled patients with left-sided S. aureus endocarditis was very small and the treatment success in this group of patients was very low (11.1% versus 22.2% for daptomycin and standard therapy, respectively). Second, although not statistically significant, treatment failure due to persistent or relapsing S. aureus infection was more common in the daptomycin than the standard therapy group (15.8% versus 9.6%, P = 0.17). On the other hand, treatment failure due to discontinuation of antibiotic administration because of adverse effects (mainly impairment of renal function) was more common in the standard therapy than the daptomycin group (14.8% versus 6.7%, P = 0.06); gentamicin was administered to more patients in the standard therapy group. Third, the criteria for treatment success were very strict and consequently, the reported clinical success was very low. The authors considered as treatment failure all patients that did not have a blood culture drawn at the test-of-cure visit 42 days after the end of treatment, regardless of their clinical status. Similarly, all patients who discontinued treatment due to adverse effects associated with study antibiotics were considered as treatment failures. Finally, only patients with S. aureus infections were enrolled in this RCT.
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The available evidence regarding the treatment of patients with endocarditis and bacteraemia due to Gram-positive cocci with daptomycin is limited. The most reliable information comes from the single multicentre RCT conducted on this issue, which had some important limitations. The most important of these limitations was the small number of enrolled patients with final diagnosis of endocarditis and especially those with left-sided endocarditis. However, this RCT provides valuable information regarding patients with bacteraemia. Daptomycin seems to be an equal alternative to vancomycin and antistaphylococcal penicillins for the treatment of patients with S. aureus bacteraemia.
In the majority of the relevant case reports, daptomycin was administered when treatment of patients with endocarditis or bacteraemia with other potentially effective antibiotics (including glycopeptides and linezolid) had failed. Thus far, vancomycin and, in patients who can not tolerate vancomycin or treatment had failed, linezolid are the recommended antibiotics for the treatment of patients with endocarditis due to multidrug-resistant Gram-positive cocci according to the American Heart Association.46,47 The available data suggest that daptomycin could also be considered for the treatment of patients with endocarditis due to Gram-positive cocci, but more data are necessary.
In the published case reports, several patients receiving treatment with daptomycin for bacteraemia or endocarditis had a history of acute leukaemia or had received haemopoietic stem-cell transplantation. These patients are at higher risk for development of infections and increased mortality. Daptomycin seems to be an alternative choice for the treatment of such patients, especially when treatment with vancomycin has failed. Although linezolid can also be effective, its administration for a long period is associated with haematological adverse effects that may prohibit its use in patients with haematological abnormalities.
The available experimental models suggested that the combination of daptomycin with rifampicin or gentamicin could enhance its activity in vivo against MRSA and VRE. However, in the single RCT conducted on the issue, daptomycin was barely ever combined with any other antibiotic. On the contrary, gentamicin was added in 93% of the patients treated with vancomycin or antistaphylococcal penicillins. Whether this could explain the non-significant more treatment failures reported for daptomycin in patients with persistent S. aureus infections enrolled in the RCT should be an issue of further research. Data from animal studies can be used as a guide for future research, but should never be considered as strong evidence for treatment options in humans.
The main adverse effect noted in the studied patients was myopathy associated with an increase in CK serum levels. Animal studies have demonstrated that myopathy was specific to skeletal muscles. The skeletal myopathy was associated with minimal degeneration that was associated with inflammation at high doses; the inflammation did not further contribute to muscle damage, and there was regeneration without fibrosis.48 In one of the case reports, the authors stated that rhabdomyolysis also occurred. Others also reported cases of renal damage associated with the use of daptomycin. It should be noted that increased caution is required in treating patients with renal dysfunction because prolonged exposure to higher serum levels of daptomycin may elicit myopathy, which in turn may deteriorate renal function.
Development of resistance is among the most important issues regarding antibiotic use. There are several reports of increase in the minimal inhibitory concentration or de novo development of resistance during treatment with daptomycin. In many of these reports, these phenomena were associated with treatment failures or even death. It is noteworthy that in these reports the duration of daptomycin administration was relatively short (range 14–27 days). Future studies should try to evaluate whether the combination of daptomycin with other antibiotics effective against Gram-positive bacteria would reduce the resistance rates reported to date for daptomycin.
Further research is needed regarding the most appropriate regimen for the treatment of patients with endocarditis due to resistant Gram-positive cocci like MRSA, methicillin-resistant coagulase-negative staphylococci and VRE. The currently available antibiotics (vancomycin, teicoplanin, linezolid, daptomycin, tigecycline and dalbavancin) are promising, but RCTs comparing these agents are lacking while treatment failure and mortality remain high. Therefore, more data are also needed regarding the effectiveness of combination therapy with rifampicin and/or aminoglycosides.
In conclusion, although daptomycin has already been approved for the treatment of patients with right-sided endocarditis and bacteraemia, the available evidence is limited and further evaluation of the antibiotic is warranted. The commonly reported de novo development of resistance is a major concern that may limit its use for the treatment of life-threatening infections. The combination of daptomycin with other antibiotics active against multi-antibiotic resistant strains could result in better outcomes and fewer cases of daptomycin-resistant Gram-positive cocci. However, there are no clinical data supporting this issue. Accordingly, daptomycin should be used with caution and preferably when standard treatments have failed, in order to preserve this potentially effective drug for future use.
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None.
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TopAbstractIntroductionMethodsResultsDiscussionFundingTransparency declarationsReferences |
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None to declare.
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