Antibacterial Spectrum

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1 ANTIMICROBIAL AGENTS AND CHEMOTHERAPY, Sept. 1992, p /92/ $02.00/0 Copyright 1992, American Society for Microbiology Vol. 36, No. 9 In Vitro and In Vivo Antibacterial Activities of, a Novel Parenteral Cephalosporin with a Broad Antibacterial Spectrum KATSURA HATA,* MASAKO OTSUKI, AND TAKESHI NISHINO Department of Microbiology, Kyoto Pharnaceutical University, 5-Nakauchi-cho, Misasagi, Yamashina-ku, Kyoto 607, Japan Received 3 February 1992/Accepted 3 July 1992 is a new iijectable cephalosporin with a broad spectrum of antibacterial activity against gram-positive and gram-negative bacteria, including staphylococci and Pseudomonas aeruginosa. The in vitro activities of against clinical isolates of methicillin-susceptible Staphylococcus aureus (MIC of for 90%o of the strains tested [MIC,0], ;g/ml) and methicillin-resistant S. aureus (MIC90, plg/ml) were similar to those of cefpirome and flomoxef. Against Enterococcusfaecalis (MIC,0, 6. ;ag/ml), was the most active of the drugs tested and four times more active than cefpirome. The MIC90s of for streptococci, Haemophilus influenzae, and Neisseria gonorrhoeae ranged from to,ug/ml; was similar in activity to cefpirome. inhibited 90% of most species of the family Enterobacteriaceae at concentrations of < ilg/ml, with the exception of Serratia marcescens and Proteus vulgaris (,ug/ml). The activity of against P. aeruginosa (MIC90, 6. ;Lg/ml) was comparable to that of ceftazidime. In vivo activity was evaluated with systemic infections in mice. showed a protective effect against systemic infections by gram-positive or gram-negative bacteria, as reflected by its in vitro activity. The protective effects of were higher than those of cefpirome against S. aureus and P. aeruginosa infections and similar to those of cefpirome against other bacterial infections. Morphological studies using differential interference and phase-contrast microscopy showed that low concentrations of caused swelling of S. aureus and spheroplast and bulge formation in P. aeruginosa. In general, the antibacterial profile of is similar to that of cefpirome. The newer cephalosporin antibiotics used in the treatment of bacterial infections, such as ceftazidime, cefuzonam, and flomoxef, possess broad antibacterial spectra. However, infections caused by methicillin-resistant Staphylococcus aureus (MRSA) and Pseudomonas aeruginosa still cause major clinical problems. Accordingly, there has been continued interest in producing cephalosporins with increased activity against MRSA or P. aeruginosa, such as cefpirome (12), cefepime (5), and E1040 (14). {7,B-[2-(5-amino- 1,2,4-thiadiazol-3-yl)-(Z)-2-fluoromethoxyiminoacetamido]- 3 - [(E) (carbamoylmethyl) ethylmethylammonio propenyl] cephem carboxylate} is a new parenteral cephalosporin synthesized by Eisai Co., Ltd., Tokyo, Japan. It contains a unique side chain, a propenylammonium moiety at the 3 position, and a monofluoromethoxyimino group in the 71 side chain of the cephalosporin nucleus and has a broad antibacterial spectrum (4). In this study, we compared the in vitro and in vivo antibacterial activities of with those of cefpirome (12), ceftazidime (15), cefuzonam (2), cefotaxime (9), and flomoxef (8) and examined the morphological changes in S. aureus and P. aeruginosa induced by. MATERIALS AND METHODS Antibiotics. was provided by Eisai Co., Ltd. was provided by Hoechst Japan, Tokyo, Japan. The following other antibiotics were obtained commercially: ceftazidime (Tanabe Pharmaceutical Co., Osaka, Japan), * Corresponding author cefuzonam (Takeda Chemical Industries, Osaka, Japan), cefotaxime (Chugai Pharmaceutical Co., Tokyo, Japan), and flomoxef (Shionogi Pharmaceutical Co., Osaka, Japan). Organisms. The bacterial strains used in this study were distinct clinical isolates obtained from various hospitals in Japan between 1985 and All isolates were maintained as stock cultures in our laboratory. Determination of MICs. MICs were determined by the agar dilution method recommended by the Japan Society of Chemotherapy (1). Sensitivity test agar (Eiken) was used for all organisms except the following: streptococci (sensitivity test agar supplemented with 10% defibrinated horse blood), Haemophilus influenzae (sensitivity test agar supplemented with 5% Fildes enrichment), Branhamella catarrhalis (chocolate sensitivity test agar supplemented with 5% defibrinated horse blood), and Neisseria gonorrhoeae (chocolate sensitivity test agar supplemented with 10% defibrinated horse blood). Fresh cultures of the bacterial strains were diluted, and 5 pl of each bacterial suspension, corresponding to about 104 CFU, was spotted (Microplanter; Sakuma Seisakusho, Tokyo, Japan) onto agar plates that contained twofold serial dilutions of antibiotics. The MIC was the lowest concentration of an antibiotic that completely inhibited visible growth on agar plates after incubation for 18 h at 37 C. For N. gonorrhoeae, incubation was carried out in a candle jar. The MIC and MIC90 were the concentrations of a drug required to inhibit % and 90% of the strains, respectively. Differential interference and phase-contrast microscopy. S. aureus Smith and P. aeruginosa E-2 were incubated in sensitivity test broth for 3 h at 37 C and then incubated on sensitivity test agar plates containing different concentra-

2 VOL. 36, 1992 IN VITRO AND IN VIVO ACTIVITIES OF 1895 TABLE 1. Antibacterial activities of and reference compounds against clinical isolates Organism Antibacterial MIC (ILg/ml) (no. of strains) agent Range % 90% Methicillin-susceptible Staphylococcus aureus (91) MRSA (132) Staphylococcus epidermidis (67) Streptococcus pneumoniae (33) Streptococcus pyogenes (52) Enterococcus faecalis (40) Neisseria gonorrhoeae (31) Haemophilus influenzae (52) Branhamella catarrhalis (52) > -> - - -> -> -> - < < ! : , < < f : Continued on following page

3 1896 HATA ET AL. ANTIMICROB. AGENTS CHEMOTHER. Escherichia coli (40) Kiebsiella pneumoniae (40) Enterobacter cloacae (39) TABLE 1-Continued Organism Antibacterial MIC (,Lg/ml) (no. of strains) agent Range % 90% Enterobacter aerogenes (39) Citrobacterfreundii (34) Serratia marcescens (39) Proteus mirabilis (38) Proteus vulgaris (40) Morganella morganii (40) ' Continued on following page

4 VOL. 36, 1992 IN VITRO AND IN VIVO ACTIVITIES OF 1897 TABLE 1-Continued Organism Antibacterial MIC (,ug/ml) (no. of strains) agent Range % 90% Providencia rettgeri (36) ' Pseudomonas aeruginosa () > -> > -> > > Acinetobacter calcoaceticus (32) tions of. After 3 h of incubation, morphological changes of cells were examined by differential interference microscopy for S. aureus and by phase-contrast microscopy for P. aeruginosa. Systemic infection in mice. The protective effect of against systemic infections in mice was determined as described previously (3). Male ddy strain mice weighing 18 to 20 g were used. The bacterial strains, except for Streptococcuspneumoniae type III, were cultured overnight at 37 C in nutrient broth (Nissui). For S. pneumoniae, broth was supplemented with 10% horse serum. Challenge organisms were prepared in nutrient broth and 3% hog mucin (Orthana Kemisk Fabrik A/S) in sterile water. The mice were injected intraperitoneally with 0.5 ml of the bacterial suspension. The challenge inoculum was sufficient to kill % of untreated control mice within 48 h postinfection, with the exception of Downloaded from on November 14, 2018 by guest FIG. 1. Differential interference micrographs of S. aureus Smith exposed to for 3 h. Panels: A, untreated control; B,,ug/ml; C, 0.1 plg/ml; D, pg/ml; E,.g/ml; F, 6.,g/ml.

5 1898 HATA ET AL. ANTIMICROB. AGENTS CHEMOTHER. FIG. 2. Phase-contrast micrographs of P. aeruginosa E-2 exposed to for 3 h. Panels: A, untreated control; B, 1Lg/ml; C,,ug/ml; D, 6.,ug/ml; E,,ug/ml; F,,ug/ml. mice infected with Klebsiella pneumoniae KC-1 or P. aeruginosa 15846, which died within 3 days after challenge. The antibiotic doses were administered subcutaneously in a volume of 0.2 ml of normal saline 2 h after infection. At least five levels (serial twofold doses) of the test compounds were employed with 10 mice at each level, and the 7-day survival ratios were determined. The % effective dose (ED) was calculated by the Litchfield-Wilcoxon method (7). RESULTS Antibacterial activity. The antibacterial activities of, cefpirome, ceftazidime, cefuzonam, flomoxef, and cefotaxime against clinical isolates are shown in Table 1. was active against staphylococci. The MIC90 of for methicillin-susceptible S. aureus strains was,ug/ml, which was similar to those of cefpirome, cefuzonam, and flomoxef and 1/16 to 1/4 times those of cefotaxime and ceftazidime. The MIC and MIC90 of for MRSA strains were 6. and,ug/ml, respectively. Its MIC was similar to that of flomoxef and eight times lower than those of cefuzonam and cefpirome, and its MIC-w was similar to those of cefpirome, cefuzonam, and flomoxef. and cefotaxime were inactive against MRSA, with MICs of,ug/ml. The activity of was comparable to that of cefpirome and cefuzonam against Staphylococcus epidermidis. Against streptococci, was comparable to cefpirome and cefotaxime and 4 to 16 times more active than ceftazidime and flomoxef. However, was four times less active than cefuzonam against S. pneumoniae., with an MIC90 of 6.,ug/ml for Enterococcus faecalis, was the most potent of the compounds tested. It was four times more active than cefpirome. The other reference compounds did not inhibit most strains of E. faecalis at a concentration of,ug/ml or less. The MIC90s of for N. gonorrhoeae and H. influenzae were and,ug/ml, respectively. was 4 to 16 times more active against these species than was flomoxef and was comparable to the other compounds tested. Against B. catarrhalis,, with an MIC90 of,ug/ml, was four times more active than cefpirome but eight times less active than ceftazidime. In general, and cefpirome were more active against most members of the family Enterobacteriaceae than were the other compounds tested. The MIC90s of for Escherichia coli and K pneumoniae were and,ug/ml, respectively. was equal to or four times more active than cefpirome against these species. The MIC90s of for Enterobacter cloacae, Enterobacter aerogenes, and Citrobacter freundii were,, and jig/ml, respectively, and was equal to or four times more active than cefpirome and 64 to > 128 times more active than ceftazidime, cefuzonam, cefotaxime, and flomoxef against these species. Against Serratia marcescens, was comparable to cefpirome and eight or more times more active than the other reference compounds, with an MIC90 of,ug/ml. Against Morganella morganii and Providencia rettgeri, was equal to or 4 times more active than cefpirome and 4 to 64 times more active than ceftazidime and cefuzonam, with MIC90s of and,g/ml, respectively. was similar in activity to cefpirome, ceftazidime, and cefotaxime and four times more active than cefuzonam against Proteus mirabilis. was four or more times less active than these reference compounds against Proteus vulgaris.

6 VOL. 36, 1992 IN VITRO AND IN VIVO ACTIVITIES OF 1899 Organism TABLE 2. Staphylococcus aureus Smith Streptococcus pneumoniae type III Escherichia coli KC-14 Klebsiella pneumoniae KC-1 Citrobacterffreundii B3 Serratia marcescens T-55 Pseudomonas aeruginosa Acinetobacter calcoaceticus Ac-54 a LD, % lethal dose. Protective effects of and reference compounds against systemic infection in mice Challenge dose, CFU/mouse (no. of LDSa) 3.3 x 106 (260) 6.6 x 10 (90) 1.5 x 105 (90) 2.4 x 104 (26) 1.7 x 106 (22) 2.1 x 106 (80) 7.5 x 104 (74) 2.2 x 105 (18) Against P. aeruginosa, the activity of was similar to that of ceftazidime. The MIC and MIC90 of for P. aeruginosa were and 6.,ug/ml, respectively. The MIC of was equal to or four times lower than those of ceftazidime and cefpirome. was as active as cefpirome and ceftazidime against Acinetobacter calcoaceticus, with an MIC of,ug/ml and an MIC90 of p,g/ml. Morphological effects. The morphological changes induced by in S. aureus Smith and P. aeruginosa E-2 were examined by differential interference and phase-contrast microscopy, respectively. In S. aureus (Fig. 1), induced a little swelling at a concentration of one-fourth of the MIC and lysis above the MIC. In P. aeruginosa (Fig. 2), induced formation of filamentatous cells from nor- Test compound MIC (F±g/ml) ED, mg/kg (95% confidence limits) ( ) ( ) 9.17 ( ) 3.07 ( ) ( ) 2.18 ( ) 4.19 ( ) 37.0 ( ) 12.7 ( ) 2.78 ( ) ( ) ( ) ( ) ( ) ( ) ( ) ( ) ( ) 12.3 ( ) ( ) ( ) ( ) 16.3 ( ) ( ) ( ) 7 ( ) ( ) 3.35 ( ) 2.66 ( ) 11.7 ( ) 5.70 ( ) >200 > ( ) 9.31 ( ) 8.90 ( ) 97.1 ( ) ( ) mally rod-shaped cells at concentrations of one-fourth to four times the MIC. When P. aeruginosa cells were exposed to high concentrations of ( and,ug/ml), formation of spheroplasts and bulges and cell lysis were observed. Activity against systemic infections in mice. The in vivo activity of against systemic infections in mice is shown in Table 2. showed in vivo activity against gram-positive and gram-negative bacterial infections, as reflected by its in vitro activity. The ED of against S. aureus was mg/kg; was comparable to flomoxef, 3 times more effective than cefpirome, and 10 to 30 times more effective than cefuzonam and ceftazidime. Against S. pneumoniae infection, the activity of was comparable to those of cefpirome and flomoxef and about 5

7 1900 HATA ET AL. to 17 times those of ceftazidime and cefuzonam. The activities of against E. coli and K pneumoniae infections, with EDs of and mg/kg, respectively, were similar to those of cefpirome and higher than those of the other reference compounds. The ED of against C. freundii was mg/kg; was similar in efficacy to cefpirome and 10 to 20 times as effective as the other reference compounds. Against S. marcescens infection, the activity of (ED, mg/kg) was comparable to those of cefpirome and ceftazidime and about 5 to 20 times those of cefuzonam and flomoxef. was also effective against P. aeruginosa infection. The activity of, with an ED of 2.66 mg/kg, was similar to that of ceftazidime and four times that of cefpirome, while cefuzonam and flomoxef were ineffective against P. aeruginosa infection. Against A. calcoaceticus infection, the activity of (ED, 4.88 mg/kg) was comparable to those of cefpirome and ceftazidime and about 20 times higher than those of cefuzonam and flomoxef. DISCUSSION is a new injectable cephalosporin, which has been described by Watanabe et al. (13), with a broad antibacterial spectrum and potent antibacterial activity. One of the antibacterial characteristics of is its activity against S. aureus and E. faecalis. The activity of against methicillin-susceptible S. aureus was comparable to those of cefpirome, cefuzonam, and flomoxef. also inhibited % and 90% of MRSA strains at concentrations of 6. and,ug/ml, respectively. Its activity was similar to that of flomoxef, which has been reported to be more active in vitro than other cephalosporins against MRSA (8). However, its activity, with an MIC90 of,ug/ml, is probably inadequate for clinical use for MRSA infections. In addition, was active against E. faecalis, which was resistant or less susceptible to most of the existing cephalosporins. The MIC90 of for E. faecalis was 6.,ug/ml, and its activity was four times that of cefpirome. The other reference compounds were inactive (MICs,,ug/ml). Kamiya et al. have suggested that the high activity of against S. aureus and E. faecalis is provided by the introduction of a quatemary ammoniopropenyl substituent at the 3 position of the cephem nucleus (4). A second characteristic of is that is very effective against most members of the family Enterobacteriaceae. In general, the activity of was comparable to that of cefpirome and higher than those of the other reference compounds against these species. In particular, the activity of was much higher (.64 times) than those of ceftazidime, cefuzonam, cefotaxime, and flomoxef against Enterobacter and Citrobacter species, which produce high levels of chromosomal,-lactamase (11). (6) and cefepime (10) have been reported to be active against these species. In this study, was four times more active than cefpirome against E. aerogenes and C. freundii. also showed higher in vivo activity against systemic infection caused by a strain of C. freundii that was resistant to the other extended-spectrum cephalosporins than did ceftazidime and cefuzonam. This activity seems to be due to the resistance of to enzymatic hydrolysis and the low affinity of the compound for 1-lactamases (13). possessed potency comparable to that of ceftazidime against P. aeruginosa, an opportunistic pathogen that is one of the major causes of life-threatening nosocomial ANTIMICROB. AGENTS CHEMOTHER. bacterial infections. The M'C and MIC90 of for P. aeruginosa were and 6.,ug/ml, respectively, and its activity was comparable to that of ceftazidime and four times higher than that of cefpirome. Watanabe et al. have reported that introduction of the aminothiadiazolyl group in the 71 side chain of the cephem nucleus enhances antibacterial activity against P. aeruginosa (14). The in vivo activity of in systemic infection clearly reflected its in vitro activity against P. aeruginosa. Thus, has a broad antibacterial spectrum covering gram-positive bacteria, including staphylococci and E. faecalis, and gram-negative bacteria, including P. aeruginosa. The in vitro study results were generally consistent with those of Watanabe et al. (13). also showed efficacy in systemic infections with various bacteria, and this was clearly reflected by its in vitro activity. Overall, is a very promising antibacterial agent for the treatment of various bacterial infections. Further studies on pharmacokinetic and toxicological behaviors are therefore warranted. ACKNOWLEDGMENT This study was financially assisted by Eisai Co., Ltd. REFERENCES 1. Committee for Revision of MIC Determination Method Revision of minimal inhibitory concentration (MIC) determination method. Chemotherapy (Tokyo) 29: Hikida, M., M. Inoue, and S. Mitsuhashi In vitro antibacterial activity of L-105, a new cephalosporin. J. Antimicrob. Chemother. 18: Hiruma, R., M. Otsuki, M. Tashima, Y. Obana, and T. Nishino In-vitro and in-vivo antibacterial activities of E1040, a new cephalosporin with potent antipseudomonal activity. J. Antimicrob. Chemother. 26: Kamiya, T., T. Naito, Y. Kai, Y. Komatsu, M. Sasho, N. Sato, T. Nakamura, S. Negi, Y. Machida, and Y. Yamauchi Program Abstr. 30th Intersci. Conf. Antimicrob. Agents Chemother., abstr Kessler, R. E., M. Bies, R. E. Buck, D. R. Chisholm, T. A. Pursiano, Y. H. Tsai, M. Misiek, K. E. Price, and F. Leitner Comparison of a new cephalosporin, BMY 28142, with other broad-spectrum,3-lactam antibiotics. Antimicrob. Agents Chemother. 27: Kobayashi, S., S. Arai, S. Hayashi, and K. Fujimoto P-Lactamase stability of cefpirome (HR810), a new cephalosporin with a broad antibacterial spectrum. Antimicrob. Agents Chemother. 30: Litchfield, J. T., Jr., and F. Wilcoxon A simplified method of evaluating dose-effect experiments. J. Pharmacol. Exp. Ther. 96: Murakami, K., K. Nomura, M. Doi, and T. Yoshida Production of low-affinity penicillin-binding protein by low- and high-resistance groups of methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 31: Neu, H. C., N. Aswapokee, P. Aswapokee, and K. P. Fu HR756, a new cephalosporin active against gram-positive and gram-negative aerobic and anaerobic bacteria. Antimicrob. Agents Chemother. 15: Phelps, D. J., D. D. Carlton, C. A. Farrell, and R. E. Kessler Affinity of cephalosporins for P-lactamases as a factor in antibacterial efficacy. Antimicrob. Agents Chemother. 29: Sanders, C. C Chromosomal cephalosporinases responsible for multiple resistance to newer 3-lactam antibiotics. Annu. Rev. Microbiol. 41: Seibert, G., M. Limbert, I. Winkler, and T. Dick Antibacterial activity in vitro and P-lactamase stability of the new

8 VOL. 36, 1992 cephalosporin HR810 in comparison with five other cephalosporins and two aminoglycosides. Infection 11: Watanabe, N., R. Hiruma, and K. Katsu In vitro evaluation of, a new cephalosporin with a broad antibacterial spectrum. Antimicrob. Agents Chemother. 36: Watanabe, N., K. Katsu, M. Moryama, and K. Kitoh In IN VITRO AND IN VIVO ACTIVITIES OF 1901 vitro evaluation of E1040, a new cephalosporin with potent antipseudomonal activity. Antimicrob. Agents Chemother. 32: Wise, R., J. H. Andrews, and K. A. Bedford Comparison of in vitro activity of GR20263, a novel cephalosporin derivative, with activities of other beta-lactam compounds. Antimicrob. Agents Chemother. 17:

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