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Antimicrobial Agents and Chemotherapy, March 2002, p. 892-895, Vol. 46, No. 3
0066-4804/02/$04.00+0     DOI: 10.1128/AAC.46.3.892-895.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

In Vitro Activities of Tigecycline (GAR-936) against Recently Isolated Clinical Bacteria in Spain

Carmen Betriu,^1* Iciar Rodríguez-Avial,¹ Blas Ali Sánchez,¹ María Gómez,¹ Juan Álvarez,² Juan J. Picazo, and Spanish Group of Tigecycline

Department of Clinical Microbiology, Hospital Clínico San Carlos,¹ Scientific Department, Wyeth Farma, Madrid, Spain²

Received 3 August 2001/ Returned for modification 15 October 2001/ Accepted 3 December 2001

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The antimicrobial activities of tigecycline (GAR-936) were compared with those of other agents against 1,087 strains recently isolated in 12 Spanish medical centers. Tigecycline showed activity against a wide spectrum of aerobic and anaerobic bacteria, including strains such as methicillin-resistant Staphylococcus aureus, coagulase-negative staphylococci, penicillin-resistant Streptococcus pneumoniae, Enterococcus faecium, Acinetobacter baumannii, and Stenotrophomonas maltophilia.

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Tigecycline (formerly GAR-936), the 9-t-butylglycylamido derivative of minocycline, is a member of the new group of antibiotics, the glycylcyclines. Previous studies (3, 5-7, 9, 17) have shown that tigecycline exhibits potent activity against a broad spectrum of aerobic and anaerobic bacteria, including those containing the two major determinants of tetracycline resistance, ribosomal protection and active efflux. In vivo, tigecycline had a protective effect against acute lethal infections in mice caused by Escherichia coli, Staphylococcus aureus, and Streptococcus pneumoniae (20). The efficacy of tigecycline has also been proved in a rat model of experimental endocarditis involving both methicillin-resistant S. aureus and vancomycin-susceptible and -resistant Enterococcus faecalis isolates (13). Although tigecycline, like other derivatives of tetracycline, demonstrated bacteriostatic activity, Hoellman et al. (9) showed that it was bactericidal for S. pneumoniae after 24 h, with significant killing rates at earlier time periods. The pharmacokinetics of tigecycline in healthy volunteers were linear. After administration of an intravenous dose of 300 mg, the maximum concentration in serum was 2.8 µg/ml and the half-life was 36 h (G. Muralidharan, J. Getsy, P. Mayer, I. Paty, M. Micalizzi, J. Speth, B. Wester, and P. Mojaverian, Abstr. 39th Intersci. Conf. Antimicrob. Agents Chemother., abstr. F-416, p. 303, 1999).

The present study was performed to evaluate the in vitro activities of tigecycline compared with those of other agents against a wide range of recent clinical isolates. A total of 1,087 clinical strains from the 14 different species groups listed in Tables 1, 2, and 3 were tested. Twelve medical centers located throughout Spain were asked to collect consecutive isolates during January and February 2001. Each participating laboratory performed routine identification to the species level and susceptibility testing on all organisms. These were then sent to the coordinating laboratory, Hospital Clinico San Carlos, Madrid, Spain, in transport medium (Culturette and Anaerobic Culturette; Becton Dickinson Microbiology Systems, Sparks, Md.). Only one isolate per species per patient was included in this study. Upon receipt at the coordinating laboratory, the isolates were subcultured onto blood agar or brucella blood agar to ensure purity. Their identities were confirmed with the following commercial systems: Slidex Staph, Slidex-pneumo, Rapid ID 32 STREP, ID 32 STAPH, ID 32 GN, and Rapid ID 32A (bioMérieux, Marcy l'Etoile, France). Isolates were frozen at -70°C until processing.

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TABLE 1. In vitro activities of tigecycline and other antimicrobial agents against gram-positive isolates

Antimicrobial agents tested were obtained from their respective manufacturers. The group of antimicrobial agents tested varied according to the bacterial species. For S. pneumoniae susceptibility was tested by the agar dilution method with Mueller-Hinton agar supplemented with 5% sheep blood. Susceptibility testing for the remaining isolates was performed by the agar dilution method in accordance with the guidelines of the National Committee for Clinical Laboratory Standards (NCCLS) (14-16). Production of ß-lactamase was tested with nitrocefin disks (Cefinase; Becton Dickinson Microbiology Systems). Appropriate quality control was performed with E. coli ATCC 25922, E. coli ATCC 35218, S. aureus ATCC 29213, E. faecalis ATCC 29212, E. faecalis ATCC 51229, S. pneumoniae ATCC 49619, Pseudomonas aeruginosa ATCC 27853, Bacteroides fragilis ATCC 25285, and Bacteroides thetaiotaomicron ATCC 29741. The data were analyzed with Epi Info 2000 software (version 1.1).

Table 1 summarizes the antimicrobial activities of tigecycline and the comparator agents against the gram-positive aerobic isolates tested. Among the 102 S. pneumoniae isolates included in the study, 62.7% were intermediate and 37.3% were highly resistant to penicillin. More than half (54.9%) were resistant to erythromycin. For three (2.9%) isolates levofloxacin MICs were 8 to 32 µg/ml. The emergence of resistance to fluoroquinolones in S. pneumoniae has already been reported (4, 8, 10). The MICs of tigecycline for all pneumococci, irrespective of their susceptibilities to ß-lactams or macrolides, ranged from 0.06 to 0.125 µg/ml. These results are similar to those obtained by Petersen et al. (20). For all staphylococci tested tigecycline MICs were 0.5 µg/ml, and both the MIC at which 90% of strains are inhibited (MIC₉₀) and the range of MICs for tigecycline were slightly lower than those previously reported by Patel et al. (17) and Boucher et al. (3). Among the enterococci, tigecycline was equally active against Enterococcus faecium and E. faecalis. The activity of tigecycline against vancomycin-resistant enterococci could not be studied because the enterococcal isolates included in this study were all susceptible to vancomycin and teicoplanin. In Spain, the prevalence of vancomycin resistance among enterococcal isolates is very low (19), in contrast to reports from the United States, where the prevalence of vancomycin resistance is about 17% (12). The MIC₅₀s and MIC₉₀s of tigecycline for enterococcal isolates ranged from 0.125 to 0.25 µg/ml. These values are similar to those reported previously (3, 6, 20). None of the E. faecium strains produced ß-lactamase, although for 74.5% of these organisms ampicillin MICs were 64 µg/ml. High levels of resistance to gentamicin (MICs, >500 µg/ml) and streptomycin (MICs, >2,000 µg/ml) were more common among E. faecium isolates (21.6 and 62.7%, respectively) than among E. faecalis isolates (11.5 and 44.2%, respectively).

Tigecycline activities against members of the family Enterobacteriaceae and nonfermentative gram-negative bacilli are shown in Table 2. The tigecycline MIC₉₀s for all members of the family Enterobacteriaceae tested ranged from 0.5 to 2 µg/ml. Data from the SENTRY antimicrobial surveillance program study, recently performed in Europe (21), showed a high prevalence of quinolone resistance among E. coli strains isolated in Spain. The MICs of tigecycline were similar for ciprofloxacin-resistant and -susceptible E. coli strains, whereas the rate of resistance to gentamicin was significantly (P < 0.01) higher among ciprofloxacin-resistant E. coli (24.1%) strains than among ciprofloxacin-susceptible E. coli strains (5.4%).

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TABLE 2. In vitro activities of tigecycline and other antimicrobial agents against gram-negative isolates

Against Acinetobacter baumannii, an important cause of nosocomial infections, the rank order of activity of all agents tested determined by using MIC₅₀s and MIC₉₀s was as follows: polymyxin B > tigecycline > sulbactam > levofloxacin > ampicillin-sulbactam > imipenem > cefepime > piperacillin-tazobactam > gentamicin. Resistance to imipenem was detected in 28.1% of all A. baumannii isolates tested, and more than 90% of A. baumannii strains were inhibited by tigecycline at 8 µg/ml. Gales and Jones (6) reported an MIC₉₀ of tigecycline for Acinetobacter sp. isolates of 2 µg/ml. However, they studied a smaller number of isolates (n = 30) than we did and included different species of Acinetobacter in their study.

Most clinical isolates of Stenotrophomonas maltophilia are inherently resistant to several antimicrobial agents, and few therapeutic options remain for the treatment of infections caused by these organisms. In this study, the most active agent against S. maltophilia was trimethoprim-sulfamethoxazole, to which 98.1% of strains were susceptible. The rates of resistance to piperacillin-tazobactam, ceftazidime, and amikacin were >65%. Susceptibility and intermediate susceptibility to ticarcillin-clavulanate were found in 73 and 27% of S. maltophilia isolates, respectively. The MIC₉₀ of tigecycline (4 µg/ml) was at least eightfold lower than those of ticarcillin-clavulanate, piperacillin-tazobactam, ceftazidime, and amikacin and comparable to that of trovafloxacin. To our knowledge, only two other published studies (6, 20) have reported tigecycline activity against S. maltophilia isolates. Our results agree with those reported in both studies. All P. aeruginosa isolates were susceptible to cefepime, and 6.7% were resistant to imipenem. In accordance with the data published by Gales and Jones (6) and Petersen et al. (20), tigecycline showed less activity against these organisms, and its MIC₉₀ was 16 µg/ml.

The in vitro activities of tigecycline against the anaerobic isolates tested are summarized in Table 3. Members of the B. fragilis group are the anaerobic bacteria most frequently isolated from clinical infections, and resistance to several of the traditionally used antibiotics and some of the newer ß-lactam agents has increasingly been reported (1, 2, 11). Resistance to imipenem was not found, although such resistance has been detected in other Spanish studies (2, 18), but with a low incidence. The new agent tested inhibited 86.7% of all strains at 4 µg/ml, and its activity did not vary among the different species of the group. The MIC₅₀s and MIC₉₀s of tigecycline for B. fragilis were 1 dilution lower than those recently reported by Gales and Jones (6) but higher than those reported by Edlund and Nord (5). Among toxigenic Clostridium difficile isolates, tigecycline showed the lowest MIC₅₀s and MIC₉₀s of all the antibiotics evaluated. It inhibited 92.7% of strains at 0.125 µg/ml. Similar results have been reported previously (5, 6, 20).

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TABLE 3. In vitro activities of tigecycline and other antimicrobial agents against anaerobes

In the last two decades, the incidence of infections due to multidrug-resistant gram-positive cocci, such as methicillin-resistant S. aureus, vancomycin-resistant enterococci, or penicillin-resistant S. pneumoniae, has been on the increase in many parts of the world. Therefore, gram-negative bacilli such as A. baumannii and S. maltophilia, in which multidrug resistance is common, have emerged as important nosocomial pathogens. These occurrences pose a serious therapeutic challenge and underscore the need for new agents for the treatment of infections caused by multidrug-resistant gram-positive and gram-negative pathogens. The results of this study indicate that tigecycline is active against a wide variety of bacterial species including most gram-positive and gram-negative aerobic and anaerobic organisms. This new antibiotic is a promising agent which may have an important role in the therapy of infections caused by antibiotic-resistant gram-positive and gram-negative bacteria.

APPENDIX Members of the Spanish Group of Tigecycline (coordinator, Juan J. Picazo, Madrid) are as follows: J. Aznar (Seville), E. Bouza (Madrid), R. Cisterna (Bilbao), J. García de Lomas (Valencia), J. B. García Moya (Zaragoza), J. A. García-Rodríguez (Salamanca). A. Guerrero (La Coruña), M. T. Jiménez de Anta (Barcelona), E. J. Perea (Seville), M. de la Rosa (Granada), and J. Ruiz (Murcia).

 
This study was supported by a financial grant from Wyeth-Ayerst Research, Pearl River, N.Y.

 
* Corresponding author. Mailing address: Department of Clinical Microbiology, Hospital Clínico San Carlos, Plaza Cristo Rey s/n, 28040 Madrid, Spain. Phone: 34913303485. Fax: 34913303478. E-mail: cbetriu{at}efd.net.

Members of the Spanish Group of Tigecycline are listed in the Appendix.

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Antimicrobial Agents and Chemotherapy, March 2002, p. 892-895, Vol. 46, No. 3
0066-4804/02/$04.00+0     DOI: 10.1128/AAC.46.3.892-895.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

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