Broth Microdilution and Disk Diffusion Tests for Susceptibility Testing of Pasteurella Species Isolated from Human Clinical Specimens
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微生物临床杂志 2005年第5期
R. M. Alden Research Laboratory, Santa Monica, California 90404
University of California, Los Angeles, School of Medicine, Los Angeles, California 90095
ABSTRACT
Broth microdilution and disk diffusion susceptibility testing were performed on 73 strains of Pasteurella species isolated from human infections and on five American Type Culture Collection strains of Pasteurella species. Both methods appear reliable for testing susceptibilities of Pasteurella species.
TEXT
Routine antimicrobial susceptibility determinations for Pasteurella species have not been previously recommended by the Clinical and Laboratory Standards Institute (CLSI; formerly NCCLS) for clinical laboratories, since resistance to commonly used agents was thought to be rare in human infections (1-4). However, poor in vitro activities of erythromycin, aminoglycosides, oxacillin, cephalexin, cefaclor, cefadroxil, and clindamycin have been previously reported (5). Moreover, there have been case reports on treatment failures of erythromycin and cephalexin against Pasteurella infections (7, 10). Increases in the incidence of tetracycline resistance (8) and beta-lactamase production by respiratory isolates of Pasteurella species (11) have recently been noted, and there have also been reports of plasmids carrying resistance genes found in cattle and turkey strains of Pasteurella multocida, which could potentially reach companion animals or directly cause human infection (9, 18). Consequently, it has been recognized that there is a need to test Pasteurella and other unusual organisms (12); therefore, the CLSI has undertaken development of a new document, M45-P, that will address susceptibility testing methods for such "orphan" organisms. The data generated in this study will be provided for that document.
Pasteurella species are isolated from many different animals as both commensals and pathogens. When Pasteurella is isolated from humans, its presence is usually associated with a cat or dog bite wound infection; occasionally, though, there are infections associated with nontraumatic animal contact, such as when patients with open wounds are exposed indirectly to a companion animal's oral secretions. Our laboratory has a large collection of Pasteurella strains isolated from animal bite wounds in humans. P. multocida subsp. multocida was the most frequently isolated strain, followed in descending order of frequency by P. multocida subsp. septica, P. canis, P. dagmatis, and P. stomatis (6, 17). We have performed agar dilution susceptibility testing on many of these strains and found them to be susceptible to many but not all the agents (1-5). In order to provide guidance to laboratories that need to determine susceptibility patterns of Pasteurella strains, we tested 12 antimicrobial agents against 73 of our most recent clinical isolates (collected from 1995 to the present) and five American Type Culture Collection (ATCC) strains by using both broth microdilution and disk diffusion methods, according to CLSI standards (14, 15), since these procedures are more likely to be used by the clinical lab for routine testing than is the agar dilution method.
Clinical strains were isolated from a variety of bite wounds, identified by standard methods (13), and stored at –70°C in 20% skim milk. ATCC strains included in the study were P. canis ATCC 43326T, P. dagmatis ATCC 43325T, P. multocida subsp. multocida ATCC 12947, P. multocida subsp. septica ATCC 51688, and P. stomatis ATCC 43327T. Strains were taken from the freezer and transferred twice on tryptic soy agar supplemented with 5% sheep blood (blood agar plate [BAP]; Hardy Diagnostics, Santa Maria, CA). Prior to testing, requirements for CO2 were determined by inoculation of each strain onto duplicate BAPs and incubation at 36°C for 18 h, one BAP in ambient air and the other in 5 to 7% CO2.
The following reference standard-grade antimicrobials were obtained: penicillin G, chloramphenicol, and doxycycline (Sigma, St. Louis, MO); amoxicillin (GlaxoSmithKline, Research Triangle Park, NC); levofloxacin (RW Johnson PRL, Springhouse, PA); moxifloxacin (Bayer Corp., West Haven, CT); tetracycline (Bristol-Myers Squibb, Syracuse, NY); erythromycin and cephalothin (Eli Lilly & Co., Indianapolis, IN); azithromycin (Pfizer Inc., Groton, CT); and trimethoprim-sulfamethoxazole and ceftriaxone (Roche Pharmaceuticals, Nutley, NJ). They were reconstituted according to the manufacturers' instructions, serially diluted in cation-adjusted Mueller-Hinton broth, and dispensed into microdilution panels with a Quick-Spense (Sandy Spring Instrument Co., Germantown, MD) multichannel reagent dispenser. After preparation, the panels were stored at –70°C until needed. The same antimicrobials were used for disk diffusion testing except that ampicillin was substituted for amoxicillin, since they have been found to have the same activity (16). Disks were manufactured by Becton Dickinson, Sparks, MD.
In preparation for testing, the strains were grown overnight on BAPs at 36°C. A bacterial suspension equal to a McFarland standard of 0.5 was prepared in 0.85% saline by using a turbidity meter (Dade International Inc., West Sacramento, CA) and further diluted in cation-adjusted Mueller-Hinton broth with 5% laked horse blood (LHB) to a concentration of approximately 106 CFU/ml. Fifty microliters of this suspension was inoculated into the wells of the panels, which also contained 50 μl of the antimicrobials at double strength, giving a final inoculum of approximately 5 x 105 CFU/ml or 5 x 104 CFU/well and a final concentration of 2.5% LHB. Since none of the strains required CO2 for growth, incubation was carried out at 36°C in ambient air for 18 to 20 h. The same saline suspension was used within 15 min to inoculate plates containing Mueller-Hinton agar supplemented with 5% sheep blood (MHB; Hardy Diagnostics) for antimicrobial disk diffusion testing; colony counts were performed for selected isolates to verify inoculum concentration. After application of the disks, the plates were incubated at 36°C in ambient air for 18 to 20 h.
After incubation, the growth in the panels was read and the MICs recorded (14). The MIC was determined to be the lowest concentration that completely inhibited growth of the organism; zone diameters on MHB were measured and recorded (15). If, as in some instances, the zones were very large and overlapped neighboring zones, the radius of each zone was measured and doubled to obtain the diameter.
Quality control was performed according to standard methods (14, 15, 16), using Streptococcus pneumoniae (ATCC 49619) and Staphylococcus aureus (ATCC 29213) for broth microdilution and Escherichia coli (ATCC 25922) and S. aureus (ATCC 25923) for disk diffusion. Because the Pasteurella strains were inoculated onto MHB, quality control for the antimicrobial disks was carried out with both plain Mueller-Hinton agar and MHB agar. Broth microdilution tests were also compared, with and without LHB, for S. aureus ATCC 29213.
The MIC ranges and the modal MICs, as well as the corresponding zone diameter ranges and modal zone diameters, are presented in Table 1. Although the drugs were diluted to very low concentrations, endpoints were not reached for all strains because of their very susceptible nature. This was especially true for trimethoprim-sulfamethoxazole, which was tested at concentrations as low as 0.03 (trimethoprim) and 0.6 (sulfamethoxazole) μg/ml, and for ceftriaxone, which was tested at 0.015 μg/ml. P. canis, P. dagmatis, and P. stomatis strains were even more susceptible to all agents than either P. multocida subsp. multocida or P. multocida subsp. septica strains.
According to Goldstein et al. (5), erythromycin resistance is fairly widespread among P. multocida strains, and there is at least one report where erythromycin failure led to P. multocida meningitis and sepsis in a cat bite victim (10). In our present study, erythromycin does have the highest range of MICs (0.5 to 4 μg/ml) among the agents tested, but there are as yet no CLSI guidelines by which to interpret these results; however, azithromycin ranges were consistently 3 dilutions lower than erythromycin ranges for all strains tested. Reports of beta-lactamase-producing strains in humans have been limited to respiratory isolates thought to have acquired resistance from beta-lactamase-producing strains of Haemophilus influenzae present in the respiratory tract (11). The amoxicillin MIC in that report, 8 μg/ml, was reduced to 0.25 μg/ml when tested with amoxicillin-clavulanic acid, and the nitrocefin beta-lactamase test was positive.
Interestingly, S. aureus ATCC 29213 tended to give slightly higher MICs with penicillin and amoxicillin when LHB was present; however, there were no significant differences noted on disk diffusion tests for the quality control strains on Mueller-Hinton agar, with or without sheep blood inclusion.
The broth microdilution MICs obtained in this study were virtually identical to those obtained by agar dilution in our previous studies (4, 5) as well as to the broth microdilution MICs obtained by Mortensen et al. (12), with the exception of azithromycin, which was determined in that study by Etest (AB Biodisk, Piscataway, NJ) incubated with CO2, predictably resulting in slightly higher MICs. Both methods appear reliable for testing susceptibilities of Pasteurella species, and the data presented here will be included in the new CLSI document, M45-P. Since resistant strains were not available for our study, we recommend that if a laboratory encounters a strain of Pasteurella species with zone diameters smaller or with MICs higher than those currently reported, that laboratory should confirm the identification of the isolate and consider sending it to a reference or research lab for verification of resistance and for further study to define the mechanism.
ACKNOWLEDGMENTS
We thank Hardy Diagnostics for providing the Mueller-Hinton agar, antimicrobial disks, and saline dilution blanks used in this study.
We thank Vreni Merriam for review of the manuscript.
REFERENCES
Goldstein, E. J. C., D. M. Citron, S. H. Gerardo, M. Hudspeth, and C. V. Merriam. 1998. Activities of HMR 3004 (RU 64004) and HMR 3647 (RU 66647) compared to those of erythromycin, azithromycin, clarithromycin, roxithromycin, and eight other antimicrobial agents against unusual aerobic and anaerobic human and animal bite pathogens isolated from skin and soft tissue infections in humans. Antimicrob. Agents Chemother. 42:1127-1132.
Goldstein, E. J. C., D. M. Citron, C. V. Merriam, K. Tyrrell, and Y. Warren. 1999. Activity of gatifloxacin compared to those of five other quinolones versus aerobic and anaerobic isolates from skin and soft tissue samples of human and animal bite wound infections. Antimicrob. Agents Chemother. 43:1475-1479.
Goldstein, E. J. C., D. M. Citron, C. V. Merriam, Y. Warren, and K. Tyrrell. 2000. Comparative in vitro activities of ABT-773 against aerobic and anaerobic pathogens isolated from skin and soft-tissue animal and human bite wound infections. Antimicrob. Agents Chemother. 44:2525-2529.
Goldstein, E. J. C., D. M. Citron, C. V. Merriam, Y. A. Warren, K. L. Tyrrell, and H. T. Fernandez. 2002. In vitro activities of garenoxacin (BMS-284756) against 170 clinical isolates of nine Pasteurella species. Antimicrob. Agents Chemother. 46:3068-3070.
Goldstein, E. J. C., D. M. Citron, and G. A. Richwald. 1988. Lack of in vitro efficacy of oral forms of certain cephalosporins, erythromycin, and oxacillin against Pasteurella multocida. Antimicrob. Agents Chemother. 32:213-215.
Goldstein, E. J. C., D. M. Citron, B. Wield, U. Blachman, V. L. Sutter, T. A. Miller, and S. M. Finegold. 1978. Bacteriology of human and animal bite wounds. J. Clin. Microbiol. 8:667-672.
Gomez-Reino, J. J., M. Shah, P. Gorevic, and R. Lusskin. 1980. Pasteurella multocida arthritis. Case report. J. Bone Jt. Surg. Am. Vol. 62:1212-1213.
Jorgensen, J. H. 2004. Need for susceptibility testing guidelines for fastidious or less-frequently isolated bacteria. J. Clin. Microbiol. 42:493-496.
Kehrenberg, C., N. T. T. Tham, and S. Schwarz. 2003. New plasmid-borne antibiotic resistance gene cluster in Pasteurella multocida. Antimicrob. Agents Chemother. 47:2978-2980.
Levin, J. M., and D. A. Talan. 1990. Erythromycin failure with subsequent Pasteurella multocida meningitis and septic arthritis in a cat-bite victim. Ann. Emerg. Med. 19:1458-1461.
Lion, C., A. Lozniewski, V. Rosner, and M. Weber. 1999. Lung abscess due to beta-lactamase-producing Pasteurella multocida. Clin. Infect. Dis. 29:1345-1346.
Mortensen, J. E., O. Giger, and G. L. Rodgers. 1998. In vitro activity of oral antimicrobial agents against clinical isolates of Pasteurella multocida. Diagn. Microbiol. Infect. Dis. 30:99-102.
Murray, P. R., E. J. Baron, J. H. Jorgensen, M. A. Pfaller, and R. H. Yolken (ed.). 2003. Manual of clinical microbiology, 8th ed. ASM Press, Washington, D.C.
National Committee for Clinical Laboratory Standards. 2003. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically, 5th ed. Approved standard M7-A6. National Committee for Clinical Laboratory Standards, Wayne, Pa.
National Committee for Clinical Laboratory Standards. 2003. Performance standards for antimicrobial disk susceptibility tests, 8th ed. Approved standard M2-A8. National Committee for Clinical Laboratory Standards, Wayne, Pa.
National Committee for Clinical Laboratory Standards. 2004. Performance standards for antimicrobial susceptibility testing, 14th informational supplement. Approved standard M100-S14. National Committee for Clinical Laboratory Standards, Wayne, Pa.
Talan, D. A., D. M. Citron, F. M. Abrahamian, G. J. Moran, E. J. C. Goldstein, and Emergency Medicine Animal Bite Infection Study Group. 1999. Bacteriologic analysis of infected dog and cat bites. N. Engl. J. Med. 340:85-92.
Wu, J. R., H. K. Shieh, J. H. Shien, S. R. Gong, and P. C. Chang. 2003. Molecular characterization of plasmids with antimicrobial resistant genes in avian isolates of Pasteurella multocida. Avian Dis. 47:1384-1392.(Diane M. Citron, Yumi A. )
University of California, Los Angeles, School of Medicine, Los Angeles, California 90095
ABSTRACT
Broth microdilution and disk diffusion susceptibility testing were performed on 73 strains of Pasteurella species isolated from human infections and on five American Type Culture Collection strains of Pasteurella species. Both methods appear reliable for testing susceptibilities of Pasteurella species.
TEXT
Routine antimicrobial susceptibility determinations for Pasteurella species have not been previously recommended by the Clinical and Laboratory Standards Institute (CLSI; formerly NCCLS) for clinical laboratories, since resistance to commonly used agents was thought to be rare in human infections (1-4). However, poor in vitro activities of erythromycin, aminoglycosides, oxacillin, cephalexin, cefaclor, cefadroxil, and clindamycin have been previously reported (5). Moreover, there have been case reports on treatment failures of erythromycin and cephalexin against Pasteurella infections (7, 10). Increases in the incidence of tetracycline resistance (8) and beta-lactamase production by respiratory isolates of Pasteurella species (11) have recently been noted, and there have also been reports of plasmids carrying resistance genes found in cattle and turkey strains of Pasteurella multocida, which could potentially reach companion animals or directly cause human infection (9, 18). Consequently, it has been recognized that there is a need to test Pasteurella and other unusual organisms (12); therefore, the CLSI has undertaken development of a new document, M45-P, that will address susceptibility testing methods for such "orphan" organisms. The data generated in this study will be provided for that document.
Pasteurella species are isolated from many different animals as both commensals and pathogens. When Pasteurella is isolated from humans, its presence is usually associated with a cat or dog bite wound infection; occasionally, though, there are infections associated with nontraumatic animal contact, such as when patients with open wounds are exposed indirectly to a companion animal's oral secretions. Our laboratory has a large collection of Pasteurella strains isolated from animal bite wounds in humans. P. multocida subsp. multocida was the most frequently isolated strain, followed in descending order of frequency by P. multocida subsp. septica, P. canis, P. dagmatis, and P. stomatis (6, 17). We have performed agar dilution susceptibility testing on many of these strains and found them to be susceptible to many but not all the agents (1-5). In order to provide guidance to laboratories that need to determine susceptibility patterns of Pasteurella strains, we tested 12 antimicrobial agents against 73 of our most recent clinical isolates (collected from 1995 to the present) and five American Type Culture Collection (ATCC) strains by using both broth microdilution and disk diffusion methods, according to CLSI standards (14, 15), since these procedures are more likely to be used by the clinical lab for routine testing than is the agar dilution method.
Clinical strains were isolated from a variety of bite wounds, identified by standard methods (13), and stored at –70°C in 20% skim milk. ATCC strains included in the study were P. canis ATCC 43326T, P. dagmatis ATCC 43325T, P. multocida subsp. multocida ATCC 12947, P. multocida subsp. septica ATCC 51688, and P. stomatis ATCC 43327T. Strains were taken from the freezer and transferred twice on tryptic soy agar supplemented with 5% sheep blood (blood agar plate [BAP]; Hardy Diagnostics, Santa Maria, CA). Prior to testing, requirements for CO2 were determined by inoculation of each strain onto duplicate BAPs and incubation at 36°C for 18 h, one BAP in ambient air and the other in 5 to 7% CO2.
The following reference standard-grade antimicrobials were obtained: penicillin G, chloramphenicol, and doxycycline (Sigma, St. Louis, MO); amoxicillin (GlaxoSmithKline, Research Triangle Park, NC); levofloxacin (RW Johnson PRL, Springhouse, PA); moxifloxacin (Bayer Corp., West Haven, CT); tetracycline (Bristol-Myers Squibb, Syracuse, NY); erythromycin and cephalothin (Eli Lilly & Co., Indianapolis, IN); azithromycin (Pfizer Inc., Groton, CT); and trimethoprim-sulfamethoxazole and ceftriaxone (Roche Pharmaceuticals, Nutley, NJ). They were reconstituted according to the manufacturers' instructions, serially diluted in cation-adjusted Mueller-Hinton broth, and dispensed into microdilution panels with a Quick-Spense (Sandy Spring Instrument Co., Germantown, MD) multichannel reagent dispenser. After preparation, the panels were stored at –70°C until needed. The same antimicrobials were used for disk diffusion testing except that ampicillin was substituted for amoxicillin, since they have been found to have the same activity (16). Disks were manufactured by Becton Dickinson, Sparks, MD.
In preparation for testing, the strains were grown overnight on BAPs at 36°C. A bacterial suspension equal to a McFarland standard of 0.5 was prepared in 0.85% saline by using a turbidity meter (Dade International Inc., West Sacramento, CA) and further diluted in cation-adjusted Mueller-Hinton broth with 5% laked horse blood (LHB) to a concentration of approximately 106 CFU/ml. Fifty microliters of this suspension was inoculated into the wells of the panels, which also contained 50 μl of the antimicrobials at double strength, giving a final inoculum of approximately 5 x 105 CFU/ml or 5 x 104 CFU/well and a final concentration of 2.5% LHB. Since none of the strains required CO2 for growth, incubation was carried out at 36°C in ambient air for 18 to 20 h. The same saline suspension was used within 15 min to inoculate plates containing Mueller-Hinton agar supplemented with 5% sheep blood (MHB; Hardy Diagnostics) for antimicrobial disk diffusion testing; colony counts were performed for selected isolates to verify inoculum concentration. After application of the disks, the plates were incubated at 36°C in ambient air for 18 to 20 h.
After incubation, the growth in the panels was read and the MICs recorded (14). The MIC was determined to be the lowest concentration that completely inhibited growth of the organism; zone diameters on MHB were measured and recorded (15). If, as in some instances, the zones were very large and overlapped neighboring zones, the radius of each zone was measured and doubled to obtain the diameter.
Quality control was performed according to standard methods (14, 15, 16), using Streptococcus pneumoniae (ATCC 49619) and Staphylococcus aureus (ATCC 29213) for broth microdilution and Escherichia coli (ATCC 25922) and S. aureus (ATCC 25923) for disk diffusion. Because the Pasteurella strains were inoculated onto MHB, quality control for the antimicrobial disks was carried out with both plain Mueller-Hinton agar and MHB agar. Broth microdilution tests were also compared, with and without LHB, for S. aureus ATCC 29213.
The MIC ranges and the modal MICs, as well as the corresponding zone diameter ranges and modal zone diameters, are presented in Table 1. Although the drugs were diluted to very low concentrations, endpoints were not reached for all strains because of their very susceptible nature. This was especially true for trimethoprim-sulfamethoxazole, which was tested at concentrations as low as 0.03 (trimethoprim) and 0.6 (sulfamethoxazole) μg/ml, and for ceftriaxone, which was tested at 0.015 μg/ml. P. canis, P. dagmatis, and P. stomatis strains were even more susceptible to all agents than either P. multocida subsp. multocida or P. multocida subsp. septica strains.
According to Goldstein et al. (5), erythromycin resistance is fairly widespread among P. multocida strains, and there is at least one report where erythromycin failure led to P. multocida meningitis and sepsis in a cat bite victim (10). In our present study, erythromycin does have the highest range of MICs (0.5 to 4 μg/ml) among the agents tested, but there are as yet no CLSI guidelines by which to interpret these results; however, azithromycin ranges were consistently 3 dilutions lower than erythromycin ranges for all strains tested. Reports of beta-lactamase-producing strains in humans have been limited to respiratory isolates thought to have acquired resistance from beta-lactamase-producing strains of Haemophilus influenzae present in the respiratory tract (11). The amoxicillin MIC in that report, 8 μg/ml, was reduced to 0.25 μg/ml when tested with amoxicillin-clavulanic acid, and the nitrocefin beta-lactamase test was positive.
Interestingly, S. aureus ATCC 29213 tended to give slightly higher MICs with penicillin and amoxicillin when LHB was present; however, there were no significant differences noted on disk diffusion tests for the quality control strains on Mueller-Hinton agar, with or without sheep blood inclusion.
The broth microdilution MICs obtained in this study were virtually identical to those obtained by agar dilution in our previous studies (4, 5) as well as to the broth microdilution MICs obtained by Mortensen et al. (12), with the exception of azithromycin, which was determined in that study by Etest (AB Biodisk, Piscataway, NJ) incubated with CO2, predictably resulting in slightly higher MICs. Both methods appear reliable for testing susceptibilities of Pasteurella species, and the data presented here will be included in the new CLSI document, M45-P. Since resistant strains were not available for our study, we recommend that if a laboratory encounters a strain of Pasteurella species with zone diameters smaller or with MICs higher than those currently reported, that laboratory should confirm the identification of the isolate and consider sending it to a reference or research lab for verification of resistance and for further study to define the mechanism.
ACKNOWLEDGMENTS
We thank Hardy Diagnostics for providing the Mueller-Hinton agar, antimicrobial disks, and saline dilution blanks used in this study.
We thank Vreni Merriam for review of the manuscript.
REFERENCES
Goldstein, E. J. C., D. M. Citron, S. H. Gerardo, M. Hudspeth, and C. V. Merriam. 1998. Activities of HMR 3004 (RU 64004) and HMR 3647 (RU 66647) compared to those of erythromycin, azithromycin, clarithromycin, roxithromycin, and eight other antimicrobial agents against unusual aerobic and anaerobic human and animal bite pathogens isolated from skin and soft tissue infections in humans. Antimicrob. Agents Chemother. 42:1127-1132.
Goldstein, E. J. C., D. M. Citron, C. V. Merriam, K. Tyrrell, and Y. Warren. 1999. Activity of gatifloxacin compared to those of five other quinolones versus aerobic and anaerobic isolates from skin and soft tissue samples of human and animal bite wound infections. Antimicrob. Agents Chemother. 43:1475-1479.
Goldstein, E. J. C., D. M. Citron, C. V. Merriam, Y. Warren, and K. Tyrrell. 2000. Comparative in vitro activities of ABT-773 against aerobic and anaerobic pathogens isolated from skin and soft-tissue animal and human bite wound infections. Antimicrob. Agents Chemother. 44:2525-2529.
Goldstein, E. J. C., D. M. Citron, C. V. Merriam, Y. A. Warren, K. L. Tyrrell, and H. T. Fernandez. 2002. In vitro activities of garenoxacin (BMS-284756) against 170 clinical isolates of nine Pasteurella species. Antimicrob. Agents Chemother. 46:3068-3070.
Goldstein, E. J. C., D. M. Citron, and G. A. Richwald. 1988. Lack of in vitro efficacy of oral forms of certain cephalosporins, erythromycin, and oxacillin against Pasteurella multocida. Antimicrob. Agents Chemother. 32:213-215.
Goldstein, E. J. C., D. M. Citron, B. Wield, U. Blachman, V. L. Sutter, T. A. Miller, and S. M. Finegold. 1978. Bacteriology of human and animal bite wounds. J. Clin. Microbiol. 8:667-672.
Gomez-Reino, J. J., M. Shah, P. Gorevic, and R. Lusskin. 1980. Pasteurella multocida arthritis. Case report. J. Bone Jt. Surg. Am. Vol. 62:1212-1213.
Jorgensen, J. H. 2004. Need for susceptibility testing guidelines for fastidious or less-frequently isolated bacteria. J. Clin. Microbiol. 42:493-496.
Kehrenberg, C., N. T. T. Tham, and S. Schwarz. 2003. New plasmid-borne antibiotic resistance gene cluster in Pasteurella multocida. Antimicrob. Agents Chemother. 47:2978-2980.
Levin, J. M., and D. A. Talan. 1990. Erythromycin failure with subsequent Pasteurella multocida meningitis and septic arthritis in a cat-bite victim. Ann. Emerg. Med. 19:1458-1461.
Lion, C., A. Lozniewski, V. Rosner, and M. Weber. 1999. Lung abscess due to beta-lactamase-producing Pasteurella multocida. Clin. Infect. Dis. 29:1345-1346.
Mortensen, J. E., O. Giger, and G. L. Rodgers. 1998. In vitro activity of oral antimicrobial agents against clinical isolates of Pasteurella multocida. Diagn. Microbiol. Infect. Dis. 30:99-102.
Murray, P. R., E. J. Baron, J. H. Jorgensen, M. A. Pfaller, and R. H. Yolken (ed.). 2003. Manual of clinical microbiology, 8th ed. ASM Press, Washington, D.C.
National Committee for Clinical Laboratory Standards. 2003. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically, 5th ed. Approved standard M7-A6. National Committee for Clinical Laboratory Standards, Wayne, Pa.
National Committee for Clinical Laboratory Standards. 2003. Performance standards for antimicrobial disk susceptibility tests, 8th ed. Approved standard M2-A8. National Committee for Clinical Laboratory Standards, Wayne, Pa.
National Committee for Clinical Laboratory Standards. 2004. Performance standards for antimicrobial susceptibility testing, 14th informational supplement. Approved standard M100-S14. National Committee for Clinical Laboratory Standards, Wayne, Pa.
Talan, D. A., D. M. Citron, F. M. Abrahamian, G. J. Moran, E. J. C. Goldstein, and Emergency Medicine Animal Bite Infection Study Group. 1999. Bacteriologic analysis of infected dog and cat bites. N. Engl. J. Med. 340:85-92.
Wu, J. R., H. K. Shieh, J. H. Shien, S. R. Gong, and P. C. Chang. 2003. Molecular characterization of plasmids with antimicrobial resistant genes in avian isolates of Pasteurella multocida. Avian Dis. 47:1384-1392.(Diane M. Citron, Yumi A. )