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. 1999 Jun;43(6):1469–1474. doi: 10.1128/aac.43.6.1469

Linezolid Activity Compared to Those of Selected Macrolides and Other Agents against Aerobic and Anaerobic Pathogens Isolated from Soft Tissue Bite Infections in Humans

Ellie J C Goldstein 1,2,*, Diane M Citron 1, C Vreni Merriam 1
PMCID: PMC89299  PMID: 10348773

Abstract

Linezolid was tested against 420 aerobes and anaerobes, including 148 Pasteurella isolates, by an agar dilution method. Linezolid was active against all Pasteurella multocida subsp. multocida and P. multocida subsp. septica isolates and most Pasteurella canis, Pasteurella dagmatis, and Pasteurella stomatis isolates. The MIC was ≤2 μg/ml for staphylococci, streptococci, EF-4b, Weeksella zoohelcum, Fusobacterium nucleatum, other fusobacteria, Porphyromonas spp., Prevotella spp., peptostreptococci, and almost all Bacteroides tectum isolates.

Approximately 5 million Americans are bitten annually by animals (2, 21, 23), and infectious complications result (3, 7, 15, 20) due to a wide variety of isolates (1, 4, 12, 17). Linezolid, (S)-N-[[3-[3-fluoro-4-(4-morpholinyl)phenyl]-2-oxo-5-oxazo-lidinyl]methyl]acetamide, a new oxazolidinone, is active against Streptococcus pyogenes, Staphylococcus aureus, and Staphylococcus epidermidis (5, 13, 14, 25), but limited information exists about its activity against anaerobes (24). It works by binding mRNA during the start of translation and therefore does not exhibit cross-resistance with currently available antimicrobial agents (5). Linezolid has shown activity in an animal model of skin and soft tissue infections (6) and is undergoing clinical trials for the therapy of skin and soft tissue infections. Scant data is available to evaluate its potential as therapy for cellulitis due to bite wounds, since the spectrum of bite wound isolates is varied and unique (3, 7, 8). We compared the susceptibilities of 420 recent bite wound isolates to linezolid, selected macrolides, and other agents.

The strains were isolated from bite wounds (Table 1) between 1990 and 1997 and were identified by standard criteria (11, 16, 17, 22). The sources (n) were dog bites (146), cat bites (208), human bites (23), and other (24). Seven American Type Culture Collection (ATCC) strains, 5 control strains, and 12 bovine respiratory strains (especially Pasteurella haemolytica) were included for comparative purposes.

TABLE 1.

In vitro activities of linezolid, azithromycin, clarithromycin, erythromycin, amoxicillin-clavulanate, vancomycin, teicoplanin, and clindamycin against 420 aerobic and anaerobic animal and human bite wound pathogens

Organism (no. of isolates) Agent MIC (μg/ml)
Range 50% 90%
Aerobes
 Pasteurella multocida subsp. multocida (30) Linezolid 1–2 2 2
Azithromycin 0.125–1 0.5 1
Clarithromycin 0.125–4 2 2
Erythromycin 0.125–4 2 2
Amoxicillin-clavulanate 0.06–0.25 0.25 0.25
Vancomycin >32 >32 >32
Teicoplanin >32 >32 >32
Clindamycin 8–>32 32 >32
 Pasteurella multocida subsp. septica (43) Linezolid 1–2 2 2
Azithromycin 0.125–1 0.5 1
Clarithromycin 0.25–4 2 2
Erythromycin 0.25–4 2 2
Amoxicillin-clavulanate 0.06–0.5 0.25 0.5
Vancomycin >32 >32 >32
Teicoplanin 32–>32 >32 >32
Clindamycin 8–>32 32 >32
 Pasteurella canis (21) Linezolid 1–8 2 2
Azithromycin 0.125–0.25 0.25 0.25
Clarithromycin 1–2 1 2
Erythromycin 0.5–2 1 1
Amoxicillin-clavulanate 0.03–0.25 0.125 0.25
Vancomycin 8–>32 >32 >32
Teicoplanin 16–>32 >32 >32
Clindamycin 4–>32 32 32
 Pasteurella dagmatis (11) Linezolid 0.5–4 2 4
Azithromycin ≤0.03–0.5 0.125 0.5
Clarithromycin 0.125–2 1 2
Erythromycin 0.125–1 0.5 1
Amoxicillin-clavulanate 0.06–0.25 0.125 0.25
Vancomycin 8–>32 >32 >32
Teicoplanin >32 >32 >32
Clindamycin 2–32 32 32
 Pasteurella stomatis (19) Linezolid 1–16 4 8
Azithromycin 0.06–0.5 0.25 0.5
Clarithromycin 0.5–2 1 2
Erythromycin 0.25–2 0.5 1
Amoxicillin-clavulanate 0.06–0.25 0.125 0.25
Vancomycin >32 >32 >32
Teicoplanin 16–>32 >32 >32
Clindamycin 2–>32 32 32
 Pasteurella haemolytica (7) Linezolid >32 >32
Azithromycin 0.5–1 1
Clarithromycin 1–4 2
Erythromycin 1–4 2
Amoxicillin-clavulanate 0.06–0.25 0.06
Vancomycin >32 >32
Teicoplanin >32 >32
Clindamycin 2–16 16
 Pasteurella speciesa (17) Linezolid 1–>32 2 32
Azithromycin 0.25–1 0.5 1
Clarithromycin 1–4 2 2
Erythromycin 1–2 1 2
Amoxicillin-clavulanate 0.06–0.25 0.25 0.25
Vancomycin >32 >32 >32
Teicoplanin >32 >32 >32
Clindamycin 2–32 32 32
 Actinobacillus-Haemophilus speciesb (9) Linezolid ≤0.03–>32 4
Azithromycin ≤0.03–4 0.25
Clarithromycin ≤0.03–>4 1
Erythromycin ≤0.03–4 1
Amoxicillin-clavulanate ≤0.016–0.5 0.03
Vancomycin ≤1–>32 32
Teicoplanin ≤1–>32 8
Clindamycin ≤0.03–>32 4
 Moraxella catarrhalis (11) Linezolid 4–32 8 8
Azithromycin 0.06–0.5 0.125 0.25
Clarithromycin 0.125–1 0.25 1
Erythromycin 0.25–1 0.25 0.5
Amoxicillin-clavulanate 0.03–0.5 0.06 0.5
Vancomycin 4–>32 4 16
Teicoplanin 4–>32 4 32
Clindamycin 4–16 8 8
 Moraxella speciesc (12) Linezolid 4–16 4 8
Azithromycin 0.03–0.5 0.06 0.5
Clarithromycin 0.06–1 0.125 0.5
Erythromycin 0.06–1 0.125 1
Amoxicillin-clavulanate ≤0.016–0.5 0.25 0.5
Vancomycin 2–16 8 8
Teicoplanin 2–32 8 32
Clindamycin 2–16 4 8
 Neisseria weaveri (13) Linezolid 4–16 8 16
Azithromycin 0.125–0.25 0.125 0.25
Clarithromycin 0.125–0.5 0.25 0.5
Erythromycin 0.125–1 0.5 1
Amoxicillin-clavulanate 0.125–0.25 0.125 0.25
Vancomycin 4–16 8 8
Teicoplanin 4–16 8 16
Clindamycin 4–32 16 32
 Neisseria speciesd (10) Linezolid 8–32 16 16
Azithromycin 0.125–2 0.25 2
Clarithromycin 1–8 1 8
Erythromycin 0.5–4 0.5 4
Amoxicillin-clavulanate 0.125–1 0.5 1
Vancomycin 2–>32 4 32
Teicoplanin 2–>32 8 16
Clindamycin 4–>32 8 16
 EF-4b (13) Linezolid 8–16 8 8
Azithromycin 0.125–0.25 0.25 0.25
Clarithromycin 0.5–2 0.5 1
Erythromycin 0.25–1 0.5 0.5
Amoxicillin-clavulanate 0.06–0.5 0.25 0.5
Vancomycin 2–32 8 32
Teicoplanin 2–32 8 8
Clindamycin 2–8 8 8
 Eikenella corrodens (20) Linezolid 4–16 8 16
Azithromycin 2–4 4 4
Clarithromycin 4 4 4
Erythromycin 2–4 4 4
Amoxicillin-clavulanate 0.06–0.5 0.5 0.5
Vancomycin 32–>32 32 >32
Teicoplanin 8–32 32 32
Clindamycin 16–>32 32 >32
 Weeksella zoohelcum (10) Linezolid 0.25–2 1 2
Azithromycin 0.5–2 1 2
Clarithromycin 0.125–0.5 0.25 0.5
Erythromycin 0.25–1 0.25 0.5
Amoxicillin-clavulanate ≤0.016–0.125 0.06 0.06
Vancomycin ≤1–16 4 8
Teicoplanin ≤1–8 4 8
Clindamycin ≤0.03–0.06 ≤0.03 ≤0.03
 Staphylococcus aureus (12) Linezolid 0.125–2 0.125 0.25
Azithromycin 2 2 2
Clarithromycin 0.125–0.5 0.125 0.125
Erythromycin 0.06–0.25 0.125 0.126
Amoxicillin-clavulanate 0.25–1 0.25 0.5
Vancomycin 0.5–1 0.5 1
Teicoplanin 0.25–0.5 0.5 0.5
Clindamycin ≤0.03–0.125 ≤0.03 0.06
 Staphylococcus speciese (23) Linezolid 0.125–2 0.5 1
Azithromycin 0.25–>32 1 >32
Clarithromycin 0.06–>32 0.25 >32
Erythromycin 0.06–>32 0.125 >32
Amoxicillin-clavulanate 0.06–1 0.125 0.5
Vancomycin 0.5–2 1 1
Teicoplanin 0.125–2 0.5 2
Clindamycin ≤0.03–>32 0.06 >32
 Streptococcus speciesf (27) Linezolid ≤0.03–1 1 1
Azithromycin ≤0.03–16 0.125 8
Clarithromycin ≤0.03–4 ≤0.03 2
Erythromycin ≤0.03–4 ≤0.03 1
Amoxicillin-clavulanate ≤0.016–0.5 0.06 0.25
Vancomycin ≤0.06–0.5 0.5 0.5
Teicoplanin ≤0.06–0.125 ≤0.06 0.125
Clindamycin ≤0.03–0.25 0.06 0.25
Anaerobes
 Bacteroides tectum (21) Linezolid 1–4 2 2
Azithromycin 0.5–4 1 1
Clarithromycin 0.125–0.5 0.125 0.125
Erythromycin 0.25–1 0.5 0.5
Amoxicillin-clavulanate 0.03–0.5 0.03 0.06
Vancomycin 8–>16 16 >16
Teicoplanin 8–>16 >16 >16
Clindamycin ≤0.03–1 ≤0.03 ≤0.03
 Fusobacterium nucleatum (18) Linezolid ≤0.03–1 0.5 1
Azithromycin 0.5–32 2 32
Clarithromycin 4–>32 32 >32
Erythromycin 4–>32 16 >32
Amoxicillin-clavulanate ≤0.016–0.125 0.03 0.125
Vancomycin >16 >16 >16
Teicoplanin >16 >16 >16
Clindamycin ≤0.03–0.125 0.06 0.125
 Fusobacterium speciesg (10) Linezolid 0.125–1 0.5 0.5
Azithromycin 0.125–16 0.5 2
Clarithromycin 1–>32 4 32
Erythromycin 1–>32 2 16
Amoxicillin-clavulanate ≤0.016–0.25 0.125 0.125
Vancomycin 8–>16 >16 >16
Teicoplanin >16 >16 >16
Clindamycin ≤0.03–0.125 ≤0.03 0.06
 Peptostreptococcus speciesh (10) Linezolid 0.5–2 1 2
Azithromycin 0.25–>32 0.5 32
Clarithromycin 0.06–>32 0.06 >32
Erythromycin 0.06–>32 0.125 >32
Amoxicillin-clavulanate ≤0.016–0.5 0.125 0.5
Vancomycin 0.125–1 0.25 0.5
Teicoplanin ≤0.06–0.25 ≤0.06 0.25
Clindamycin ≤0.03–0.5 ≤0.03 0.25
 Porphyromonas speciesi (25) Linezolid 0.25–2 1 2
Azithromycin 0.06–0.5 0.25 0.5
Clarithromycin ≤0.03–0.125 0.06 0.125
Erythromycin 0.06–0.25 0.125 0.25
Amoxicillin-clavulanate ≤0.016–0.06 ≤0.016 0.06
Vancomycin ≤1–>16 8 >16
Teicoplanin ≤1–2 ≤1 2
Clindamycin ≤0.03 ≤0.03 ≤0.03
 Prevotella heparinolytica (13) Linezolid 2 2 2
Azithromycin 1–2 2 2
Clarithromycin 0.06–0.125 0.125 0.125
Erythromycin 0.25 0.25 0.25
Amoxicillin-clavulanate 0.06–0.25 0.125 0.25
Vancomycin 8–>16 16 16
Teicoplanin 16–>16 16 >16
Clindamycin ≤0.03 ≤0.03 ≤0.03
 Prevotella speciesj (15) Linezolid 1–2 2 2
Azithromycin ≤0.03–8 2 4
Clarithromycin ≤0.03–0.125 0.06 0.125
Erythromycin 0.06–1 0.25 0.5
Amoxicillin-clavulanate ≤0.016–0.5 0.125 0.5
Vancomycin 2–>16 >16 >16
Teicoplanin ≤1–>16 8 >16
Clindamycin ≤0.03–0.06 ≤0.03 ≤0.03
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a

Pasteurella species include (n) Pasteurella multocida subsp. gallicida (4), Pasteurella pneumotropica (1), Pasteurella multocida (2), and other Pasteurella species (10). 

b

Actinobacillus-Haemophilus species include (n) Actinobacillus actinomycetemcomitans (1) other Actinobacillus species (2), Haemophilus parainfluenzae (4), and other Haemophilus species (2). 

c

Moraxella species include all isolates not identified to the species level. 

d

Neisseria species include (n) Neisseria subflava (2), Neisseria elongata subsp. nitroreducens (1), Neisseria cinerea-N. flavescens (1), Neisseria canis (1), and other Neisseria species (5). 

e

Staphylococcus species include (n) Staphylococcus epidermidis (7), Staphylococcus warneri (7), Staphylococcus sciuri-S. lentus (2), Staphylococcus hyicus (1), Staphylococcus simulans (1), and Staphylococcus intermedia (5). 

f

Streptococcus species include (n) Streptococcus constellatus (1), Streptococcus intermedius (4), Streptococcus mitis (10), Streptococcus mutans (10), Streptococcus sanguis I (1), and Streptococcus sanguis II (1). 

g

Fusobacterium species include (n) Fusobacterium gonidiaformans (1), Fusobacterium necrophorum (1), Fusobacterium russii (6), and other fusobacteria (2). 

h

Peptostreptococcus species include (n) Peptostreptococcus anaerobius (6), Peptostreptococcus asaccharolyticus (1), Peptostreptococcus magnus (1), and other Peptostreptococcus species (2). 

i

Porphyromonas species include (n) Porphyromonas cangingivalis (2), Porphyromonas canoris (5), Porphyromonas gingivalis (8), Porphyromonas circumdentaria (2), and Porphyromonas macacae (8). 

j

Prevotella species include (n) Prevotella bivia (3), Prevotella buccae (2), Prevotella intermedia (4), Prevotella denticola (1), Prevotella loeschii (1), Prevotella melaninogenica (2), and Prevotella zoogleoformans (2). 

Laboratory powders were supplied as follows: linezolid and clindamycin, Pharmacia & Upjohn Co., Kalamazoo, Mich.; azithromycin, Pfizer Inc., New York, N.Y.; clarithromycin, Abbott Laboratories, Abbott Park, Ill.; amoxicillin-clavulanate, SmithKline Beecham Pharmaceuticals, Philadelphia, Pa.; erythromycin and vancomycin, Eli Lilly & Co., Indianapolis, Ind.; and teicoplanin, Hoechst Marion Roussel, Cincinnati, Ohio.

Susceptibility testing was performed by use of National Committee for Clinical Laboratory Standards methods (18, 19). Brucella agar supplemented with hemin, vitamin K1, and 5% laked sheep blood was the basal medium used for anaerobic species and for Eikenella corrodens, Weeksella zoohelcum, and Capnocytophaga spp. Mueller-Hinton agar was used for staphylococci, and Mueller-Hinton agar supplemented with 5% sheep blood was used for the remainder of the organisms. Serial twofold dilutions of antimicrobial agents were reconstituted according to the manufacturers’ instructions on the day of the test and added to the media at various concentrations.

Agar plates were inoculated with a Steers replicator (Craft Machine Inc., Chester, Pa.). The inoculum used for aerobes was 104 CFU per spot, and 105 CFU per spot was used for E. corrodens and anaerobes. Aerobic isolates were incubated at 35°C in an aerobic environment for 24 h and then examined. E. corrodens, W. zoohelcum, and streptococci were incubated in 5% CO2 for 48 h and then examined.

The control strains tested included S. aureus ATCC 29213, Enterococcus faecalis ATCC 29212, Escherichia coli ATCC 25922, Bacteroides fragilis ATCC 25285, and Eubacterium lentum ATCC 43055. In addition, P. haemolytica ATCC 33396, Pasteurella multocida subsp. gallicida ATCC 51689, P. multocida subsp. septica ATCC 51688, Pasteurella stomatis ATCC 43327, Pasteurella dagmatis ATCC 43325, Pasteurella canis ATCC 43326, and Neisseria canis ATCC 14687 were used.

The activities of linezolid and the other agents tested are shown in Table 1. The susceptibility of the control strains tested was within reference ranges. Linezolid was active against all P. multocida subsp. multocida and P. multocida subsp. septica isolates at ≤2 μg/ml. For P. canis isolates, the linezolid MIC at which 90% of the isolates were inhibited (MIC90) was 2 μg/ml. Almost all the other Pasteurella isolates were susceptible to ≤8 μg of linezolid per ml, except for 1 isolate of P. stomatis, for which the MIC was 16 μg/ml, and 4 of 16 other Pasteurella isolates (Table 1, footnote a). All P. haemolytica isolates were resistant (MIC, >32 μg/ml). Clindamycin was inactive against almost all Pasteurella isolates studied.

The staphylococci and streptococci studied were all susceptible to ≤2 μg of linezolid per ml. These results are similar to those reported by Jones et al. (13) and Jorgensen et al. (14). However, for many of our gram-negative aerobic bite wound pathogens, e.g., EF-4b, Moraxella catarrhalis, and other Moraxella species, the MIC of linezolid was ≥8 μg/ml, at the cusp of the proposed breakpoints (13). Zurenko et al. (25) studied 10 strains of M. catarrhalis and reported an MIC90 of 4 μg/ml and a range of 4 to 8 μg/ml. For E. corrodens, Neisseria weaveri, and other Neisseria species, the MIC90 was 16 μg/ml. For only one Neisseria isolate and one Haemophilus isolate was the MIC ≥32 μg/ml. The activity of the different macrolides was variable and consistent with that in prior reports (9, 10).

Vancomycin and teicoplanin were active against some of the unusual aerobic gram-negative bacilli and some of the Prevotella and Porphyromonas species. This result suggests that Gram stain characterization of these species may mask genetic relatedness to gram-positive species.

Yagi and Zurenko (24) studied a variety of common anaerobes encountered in general clinical infections, such as B. fragilis group members (MIC90, 8 μg/ml), but most of the isolates that they studied were different from our isolates. Zurenko et al. (25) studied 10 strains of B. fragilis and found a linezolid MIC90 of 4 μg/ml. All of our bite wound anaerobes were susceptible to ≤2 μg of linezolid per ml, with the exception of two Bacteroides tectum strains. For Fusobacterium nucleatum and other Fusobacterium species, the linezolid MIC was ≤1 μg/ml; this result was in sharp contrast to the absolute or relative resistance noted to all the macrolides tested. The activity of linezolid against F. nucleatum also compares favorably to that of the ketolides HMR 3004 and HMR 3647 (9). Linezolid was active against all Prevotella and Porphyromonas species at ≤2 μg/ml. Interestingly, many of the peptostreptococci were resistant to the macrolides but susceptible to clindamycin and to linezolid (MIC, ≤2 μg/ml). Yagi and Zurenko (24) and Jones et al. (13) also studied peptostreptococci and found all of them to be susceptible to ≤2 μg of linezolid per ml. The ketolides HMR 3004 and HMR 3647 were active at ≤0.5 μg/ml against a similar spectrum of bite wound pathogens (9).

Linezolid appears to be more active than the macrolides tested against staphylococci, peptostreptococci, and fusobacteria isolated from human and animal bite wounds and merits further clinical evaluation.

Acknowledgments

We thank Judee H. Knight, Alice E. Goldstein, and David Talan for various forms of assistance.

This study was funded in part by an educational grant from Pharmacia & Upjohn Co.

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