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Antimicrobial Agents and Chemotherapy logoLink to Antimicrobial Agents and Chemotherapy
. 2003 Jun;47(6):1963–1967. doi: 10.1128/AAC.47.6.1963-1967.2003

In Vitro Activities of Telithromycin and 10 Oral Agents against Aerobic and Anaerobic Pathogens Isolated from Antral Puncture Specimens from Patients with Sinusitis

Ellie J C Goldstein 1,2,*, Diane M Citron 1, C Vreni Merriam 1, Yumi Warren 1, Kerin L Tyrrel 1, Helen Fernandez 1
PMCID: PMC155841  PMID: 12760875

Abstract

A study of the comparative in vitro activity of telithromycin, a new ketolide, against 155 aerobic and 171 anaerobic antral sinus puncture isolates showed it to be active against a broad range of sinus pathogens. All pneumococci, including erythromycin-resistant strains, were susceptible to telithromycin at ≤0.5 μg/ml; all Haemophilus influenzae and Eikenella corrodens strains were inhibited by ≤4 μg of telithromycin/ml; all Moraxella spp. and beta-lactamase-producing Prevotella species strains were inhibited by ≤0.25 and 0.5 μg of telithromycin/ml, respectively. Among all anaerobes tested, 94% (160 of 171 strains) were susceptible to ≤4 μg of telithromycin/ml; however, 8 of 17 (47%) Fusobacterium strains, 2 Veillonella strains, and 1 Peptostreptococcus micros strain required >4 μg of telithromycin/ml for inhibition. Telithromycin may offer a therapeutic alternative for sinus infections, including those due to erythromycin-resistant pneumococci.


Bacterial sinusitis affects ca. 30 million Americans annually (22, 25). Macrolides have commonly been used to treat acute bacterial maxillary sinusitis with targeted activity against pneumococci, Haemophilus spp., and Moraxella catarrhalis; however, there is increasing resistance to these and other antimicrobials (14, 15, 18, 24), with sinus isolates being possibly more resistant than their general respiratory counterparts (6). Anaerobic bacteria, which are important pathogens in chronic sinusitis (11, 17), are often ignored by clinicians and their in vitro susceptibilities are infrequently reported by most respiratory or sinus studies (1, 3, 8).

Telithromycin is a new ketolide agent with a broad spectrum of activity, including activity against macrolide-resistant pathogens and many anaerobic bacteria (1, 7, 12, 16). In order to evaluate the potential efficacy of telithromycin in the therapy of sinusitis, we determined its comparative in vitro activity against 326 recent aerobic and anaerobic clinical isolates from patients with sinusitis.

Strains were isolated from antral puncture specimens obtained from adult patients between 1994 and 2002 and were identified by standard criteria (19, 23). As controls, Streptococcus pneumoniae ATCC 49619, Haemophilus influenzae ATCC 49247, Staphylococcus aureus ATCC 29213, Escherichia coli ATCC 25922, Eubacterium lentum ATCC 43055, Bacteroides fragilis ATCC 25285, and Bacteroides thetaiotaomicron ATCC 29741 were tested simultaneously with the appropriate plates and environments. The numbers and species of clinical isolates tested are given in Table 1.

TABLE 1.

Comparative in vitro activities of telithromycin against aerobic and anaerobic bacteria isolated from patients with sinusitis

Organism (n)a and agent In vitro activity of telithromycin (μg/ml)
Range MIC50 MIC90
Haemophilus spp.b (29)
    Telithromycin 1-8 2 4
    Erythromycin 2-8 8 8
    Azithromycin 1-8 4 8
    Clarithromycin 4-16 8 16
    Roxithromycin 4-32 16 32
    Penicillin G 0.125->16 1 >16
    Amoxicillin-clavulanate ≤0.06-4 0.5 2
    Cefuroxime ≤0.06->32 0.5 2
    Levofloxacin ≤0.008-0.03 0.015 0.015
    Moxifloxacin ≤ 0.008-0.25 0.03 0.125
    Gatifloxacin ≤0.008-0.03 ≤0.008 0.03
Moraxella catarrhalis (11)
    Telithromycin 0.06-0.125 0.06 0.125
    Erythromycin 0.06-0.25 0.125 0.125
    Azithromycin 0.06-0.125 0.06 0.06
    Clarithromycin 0.06-0.125 0.06 0.125
    Roxithromycin 0.125-0.5 0.25 0.25
    Penicillin G 0.03->16 8 16
    Amoxicillin-clavulanate ≤ 0.015-0.25 0.03 0.25
    Cefuroxime 0.25-2 1 1
    Levofloxacin 0.015-0.03 0.03 0.03
    Moxifloxacin 0.015-0.06 0.06 0.06
    Gatifloxacin 0.015-0.03 0.03 0.03
Staphylococcus aureus (28)
    Telithromycin 0.06->16 0.125 0.25
    Erythromycin 0.125->32 0.5 >32
    Azithromycin 1->32 4 >32
    Clarithromycin 0.125->32 0.25 >32
    Roxithromycin 0.25->32 1 >32
    Penicillin G 0.03->16 16 >16
    Amoxicillin-clavulanate 0.03-16 1 2
    Cefuroxime 0.25->32 1 2
    Levofloxacin 0.06->16 0.25 0.5
    Moxifloxacin 0.015-8 0.06 0.125
    Gatifloxacin 0.03-8 0.125 0.25
Streptococcus pneumoniae (30)
    Telithromycin ≤0.008-0.5 ≤0.008 0.03
    Erythromycin ≤ 0.015->32 0.06 4
    Azithromycin 0.125->32 0.25 >32
    Clarithromycin ≤ 0.015->32 0.03 2
    Roxithromycin 0.03->32 0.06 32
    Penicillin G ≤0.015-2 ≤0.015 1
    Amoxicillin-clavulanate ≤0.015-2 ≤0.015 0.5
    Cefuroxime ≤0.015-32 ≤0.015 4
    Levofloxacin 0.5-8 1 1
    Moxifloxacin 0.06-2 0.125 0.125
    Gatifloxacin 0.125-4 0.25 0.25
Eikenella corrodens (12)
    Telithromycin 0.5-4 2 2
    Erythromycin 4-32 8 32
    Azithromycin 2-32 8 16
    Clarithromycin 4-16 4 16
    Roxithromycin 8->32 16 32
    Penicillin G 0.25-2 1 2
    Amoxicillin-clavulanate 0.25-1 0.5 0.5
    Cefuroxime 2-16 8 16
    Levofloxacin ≤0.008-0.03 0.015 0.015
    Moxifloxacin 0.015-0.125 0.03 0.06
    Gatifloxacin ≤ 0.008-0.03 0.015 0.03
Enterobacteriaceae spp.c (23)
    Telithromycin 4->16 16 >16
    Erythromycin 32->32 >32 >32
    Azithromycin 4->32 16 >32
    Clarithromycin 32->32 >32 >32
    Roxithromycin >32 >32 >32
    Penicillin G 16->16 4 >16
    Amoxicillin-clavulanate 0.5->16 4 >16
    Cefuroxime 0.5->32 4 >32
    Levofloxacin 0.015-2 0.03 0.25
    Moxifloxacin 0.03-4 0.06 0.25
    Gatifloxacin 0.015-2 0.03 0.25
Miscellaneous GNBd (21)
    Telithromycin 0.25->16 16 >16
    Erythromycin 2->32 >32 >32
    Azithromycin 0.5->32 >32 >32
    Clarithromycin 0.25->32 >32 >32
    Roxithromycin 1->32 >32 >32
    Penicillin G 2->16 >16 >16
    Amoxicillin-clavulanate 1->16 >16 >16
    Cefuroxime 0.5->32 >32 >32
    Levofloxacin 0.06->16 1 8
    Moxifloxacin 0.015->16 1 8
    Gatifloxacin 0.03-16 1 8
Fusobacterium spp.e (17)
    Telithromycin 0.125-16 4 16
    Erythromycin 0.25-64 32 32
    Azithromycin 0.06-1 0.5 1
    Clarithromycin 0.125->32 16 >32
    Roxithromycin 0.125->32 32 >32
    Penicillin G ≤0.015-1 ≤0.015 1
    Amoxicillin-clavulanate ≤0.015-0.5 0.03 0.25
    Cefuroxime ≤0.03-1 0.06 0.5
    Levofloxacin 0.06-2 0.5 1
    Moxifloxacin 0.06-2 0.25 0.5
    Gatifloxacin ≤0.03-4 0.25 0.5
Prevotella melaninogenica groupf (16)
    Telithromycin ≤0.015-1 0.25 0.5
    Erythromycin 0.03-64 1 32
    Azithromycin 0.06-32 0.25 8
    Clarithromycin ≤0.015-1 0.06 1
    Roxithromycin 0.06-16 0.25 16
    Penicillin G 0.03->16 2 16
    Amoxicillin-clavulanate 0.03-2 0.25 1
    Cefuroxime 0.125->32 16 >32
    Levofloxacin 0.5->8 1 >8
    Moxifloxacin 0.25->8 1 8
    Gatifloxacin 0.25-4 0.5 4
Prevotella spp., nonpigmentedg (19)
    Telithromycin ≤0.015-0.5 0.06 0.25
    Erythromycin 0.06-32 0.5 2
    Azithromycin 0.03-32 0.25 2
    Clarithromycin ≤0.015-1 0.06 0.25
    Roxithromycin 0.06-8 0.25 1
    Penicillin G 0.03->16 0.125 >16
    Amoxicillin-clavulanate 0.03-1 0.06 1
    Cefuroxime 0.125->32 4 >32
    Levofloxacin ≤0.03-4 1 4
    Moxifloxacin 0.06-8 0.5 4
    Gatifloxacin 0.25-4 0.25 2
Propionibacterium acnes (14)
    Telithromycin ≤0.015-0.03 ≤0.015 ≤0.015
    Erythromycin ≤0.015-0.06 0.03 0.03
    Azithromycin 0.06-0.125 0.06 0.125
    Clarithromycin ≤0.015-0.03 ≤0.015 ≤0.015
    Roxithromycin 0.06-0.125 0.06 0.125
    Penicillin G ≤0.015-0.125 0.03 0.06
    Amoxicillin-clavulanate 0.03-0.5 0.06 0.125
    Cefuroxime 0.06-0.5 0.125 0.25
    Levofloxacin 0.25-0.5 0.25 0.5
    Moxifloxacin 0.125-0.25 0.125 0.25
    Gatifloxacin 0.125-0.25 0.25 0.25
Propionibacterium spp.h (14)
    Telithromycin ≤0.015 ≤0.015 ≤0.015
    Erythromycin ≤0.03-0.06 ≤0.03 0.06
    Azithromycin 0.03-0.125 0.06 0.125
    Clarithromycin ≤0.015-0.03 ≤0.015 ≤0.015
    Roxithromycin 0.06 0.06 0.06
    Penicillin G ≤0.015-0.125 0.06 0.125
    Amoxicillin-clavulanate 0.03-0.25 0.06 0.25
    Cefuroxime 0.06-1 0.5 1
    Levofloxacin 0.125-0.5 0.25 0.5
    Moxifloxacin 0.125-0.25 0.125 0.25
    Gatifloxacin 0.125-0.25 0.125 0.25
Peptostreptococcus magnus (40)
    Telithromycin ≤0.015-4 0.06 0.06
    Erythromycin 2-32 4 4
    Azithromycin 1-32 2 4
    Clarithromycin 1-32 2 2
    Roxithromycin 4-32 4 8
    Penicillin G 0.03-0.25 0.125 0.125
    Amoxicillin-clavulanate 0.06-0.25 0.125 0.25
    Cefuroxime 0.25-8 2 8
    Levofloxacin 0.125->8 0.25 0.5
    Moxifloxacin 0.06-8 0.125 0.25
    Gatifloxacin 0.06->8 0.125 0.25
Peptostreptococcus micros (17)
    Telithromycin ≤0.015->32 0.03 0.03
    Erythromycin 0.5-128 1 2
    Azithromycin 0.5->32 1 2
    Clarithromycin 0.25->32 0.5 0.5
    Roxithromycin 1->32 2 2
    Penicillin G ≤0.015-0.125 ≤0.015 0.06
    Amoxicillin-clavulanate ≤0.015-2 0.06 1
    Cefuroxime 0.06-2 0.25 1
    Levofloxacin 0.25-4 0.5 1
    Moxifloxacin 0.125-2 0.25 0.5
    Gatifloxacin 0.125-2 0.25 0.5
Peptostreptococcus spp.i (14)
    Telithromycin ≤0.015-1 0.03 0.06
    Erythromycin ≤0.015->128 1 128
    Azithromycin 0.06->32 1 >32
    Clarithromycin ≤0.015->32 0.5 >32
    Roxithromycin 0.06->32 4 >32
    Penicillin G ≤0.015-2 0.125 0.5
    Amoxicillin-clavulanate ≤0.01-4 0.06 0.25
    Cefuroxime 0.06-32 0.25 8
    Levofloxacin 0.25-4 2 4
    Moxifloxacin 0.125-1 0.25 1
    Gatifloxacin 0.125-1 0.5 1
Veillonella spp. (16)
    Telithromycin ≤0.015-8 2 8
    Erythromycin 1-32 8 32
    Azithromycin 0.5-16 2 8
    Clarithromycin 0.5-32 4 32
    Roxithromycin 4->32 32 >32
    Penicillin G 0.03-8 2 8
    Amoxicillin-clavulanate ≤0.015-4 2 4
    Cefuroxime 0.25-16 4 16
    Levofloxacin 0.06-4 0.5 4
    Moxifloxacin ≤0.03-4 0.06 2
    Gatifloxacin 0.06-2 0.125 2
Other anaerobesj (9)
    Telithromycin 0.03-4 0.5
    Erythromycin 0.125-32 1
    Azithromycin 0.03-16 1
    Clarithromycin 0.06-16 0.5
    Roxithromycin 0.25->32 2
    Penicillin G 0.03->16 1
    Amoxicillin-clavulanate 0.03-2 0.5
    Cefuroxime ≤0.015->32 2
    Levofloxacin ≤0.03->8 1
    Moxifloxacin ≤0.03->8 0.5
    Gatifloxacin <0.03->8 0.5
a

n = number of isolates tested.

b

Includes H influenzae (n = 2) and H. paraphrophilus (n = 3).

c

Includes Eschericiha coli (n = 6), Citrobacter koseri (n = 2), Enterobacter aerogenes (n = 2), Enterobacter cloacae (n = 3), Hafnia alvei (n = 1), Klebsiella oxytoca (n = 3), Klebsiella pneumoniae (n = 1), Pantoea agglomerans (n = 1), Proteus mirabilis (n = 1), Serratia liquefaciens, (n = 2), and Serratia marcescens (n = 1).

d

Includes Achromobacter xylosoxidans (n = 2), Pseudomonas aeruginosa (n = 9), Acinetobacter baumannii (n = 1), Acinetobacter lwoffi (n = 1), Bordetella bronchiseptica (n = 1), Flavobacterium sp. strain IIb (n = 3), and Stenotrophomonas maltophilia (n = 3).

e

Includes F nucleatum (n = 14), F. necrophorum (n = 2), and F. naviforme (n = 1).

f

Includes P. intermedia (n = 1) and P. melaninogenica (n = 15).

g

Includes P. bivia (n = 2), P. buccae (n = 8), and P. oris (n = 4).

h

Includes P. avidum (n = 6), P. granulosum (n = 5), and Propionibacterium spp. (n = 3).

Suppliers of standard laboratory powders were as follows: telithromycin and roxithromycin, Aventis-Pharma Pharmaceuticals (Romainville, France); azithromycin, Pfizer, Inc. (New York, N.Y.); clarithromycin, Abbott Laboratories (Abbott Park, Ill.; note that the 14-hydroxy clarithromycin compound was not tested along with the clarithromycin); erythromycin, Eli Lilly & Co. (Indianapolis, Ind.); amoxicillin-clavulanate and cefuroxime, Glaxo SmithKline (Philadelphia, Pa.); levofloxacin, R. W. Johnson Pharmaceutical Research Institute (Raritan, N.J.); moxifloxacin, Bayer Corp. (West Haven, Conn.); and gatifloxacin, Bristol-Myers Squibb (Princeton, N.J.).

Susceptibility testing was performed according to National Committee for Clinical Laboratory Standards (NCCLS) guidelines (20, 21). Brucella agar supplemented with hemin, vitamin K1, and 5% laked sheep blood was the basal medium used for anaerobic species. The broth microdilution method and an inoculum of ca. 5 × 104 CFU per well was used for aerobes (21), and the agar dilution method with an inoculum of 105 CFU per spot was used for anaerobes (20).

(This work was presented in part at the 40th Annual Meeting of the Infectious Diseases Society of America, Chicago, Ill., 24 to 27 October 2002.)

The proposed preliminary breakpoints for telithromycin were as follows: for pneumococci, streptococci, and staphylococci, ≤1 μg/ml is considered susceptible, 2 μg/ml is considered intermediate, and ≥4 μg/ml is considered resistant; for Haemophilus influenzae, ≤2 μg/ml is considered susceptible, 4 μg/ml is considered intermediate, and ≥8 μg/ml is considered resistant (1). Telithromycin showed very good activity in our study, with most of the typical aerobic sinus pathogens being susceptible to ≤4 μg of telithromycin/ml. The isolates requiring ≥8 μg of telithromycin/ml for inhibition were unusual aerobic gram-negative isolates that are not expected to be susceptible; this included 21 of 23 Enterobacteriaecae strains and 18 of 21 lactose-nonfermenting gram-negative rod strains, such as Pseudomonas aeruginosa, Flavobacterium sp. strain IIb, Stenotrophomonas maltophilia, Acinetobacter baumannii, and Achromobacter xylodosoxidans.

Breakpoints for anaerobic bacteria have not been established, but of the anaerobes tested, 94% (160 of 171 strains) were susceptible to ≤4 μg of telithromycin/ml. Resistant anaerobes included 8 of 17 (47%) strains of fusobacteria, 2 of 16 Veillonella strains, and 1 Peptostreptococcus micros isolate. Our study did not include any pediatric strains that may be more resistant than adult strains (6, 14).

Although macrolides have been recommended as first-line therapy in sinusitis (11), macrolide resistance among clinical Streptococcus pneumoniae isolates has been reported to range from 11.1% among Canadian isolates collected in 2000 (18) to 20.4% for invasive isolates collected in the United States in 1999 (14). Telithromycin has previously been noted to be active against erythromycin-resistant pneumococci “irrespective of their mechanism of macrolide resistance” (2, 15) and to “select for resistance less often” than the lower-level macrolides (5). In our study, telithromycin had an MIC at which 90% of the isolates tested are inhibited (MIC90) of 0.03 μg/ml against pneumococci that was much more active than the MIC90s of erythromycin (4 μg/ml), azithromycin (>32 μg/ml), and clarithromycin (2 μg/ml). Three pneumococcal sinus isolates were resistant to penicillin, whereas none were resistant to amoxicillin according to newly proposed NCCLS breakpoints. Of 30 isolates, 5 (17%) were resistant to erythromycin, as well as resistant to azithromycin, roxithromycin, and clarithromycin.

These data are in accord with those reported by other investigators (2, 13). Hoban et al. (13) reported telithromycin MIC90s of ≤0.12 μg/ml for both penicillin-susceptible and -intermediate pneumococci and of 0.25 μg/ml for penicillin-resistant strains isolated in Canada in 1997 and 1998. One of our macrolide-resistant isolates was also resistant to all three fluoroquinolones but susceptible to telithromycin. Doern et al. (6) noted that 39% of sinus pneumococcus isolates were resistant to penicillin compared to 26% overall resistance in general isolates and also noted that 10% of the pneumococcus strains were resistant to azithromycin, clarithromycin, and erythromycin, while Thornsberry et al. (24) reported 29% resistance among pneumococcal strains to clarithromycin.

Against Staphylococcus aureus, telithromycin had an MIC90 of 0.25 μg/ml versus erythromycin, azithromycin, and clarithromycin (without the addition of the 14-hydroxy clarithromycin), which each had an MIC90 >32 μg/ml. In our study, 54% (14 of 26) of Haemophilus influenzae strains were beta-lactamase producers. Telithromycin had an MIC90 of 4 μg/ml compared to MICs of 16 μg/ml for clarithromycin, 8 μg/ml for azithromycin and erythromycin, and 32 μg/ml for roxithromycin. Hoban et al. (13) also noted that telithromycin and clarithromycin had, respectively, MIC90s of 4 and 16 μg/ml against 1,438 Canadian isolates (obtained from 1997 to 1998) of Haemophilus influenzae. However, these authors noted azithromycin MIC90s of 2 μg/ml against beta-lactamase-negative strains and 4 μg/ml against beta-lactamase-positive strains. We did not observe a similar pattern in our strains, although the number of isolates we tested was much smaller. Thornsberry et al. (24) noted that only 67 and 58% of Haemophilus influenzae strains were amoxicillin and clarithromycin susceptible, respectively. Clinical correlation of these susceptibility results against Haemophilus species has not yet been done.

In agreement with the results of Hoban et al. (13), we also found that telithromycin had an MIC90 of 0.125 μg/ml against Moraxella catarrhalis, which was comparable to those of the macrolides studied. Telithromycin performed well against Eikenella corrodens, with an MIC90 of 2 μg/ml, compared to 16 μg/ml for clarithromycin and azithromycin and 32 μg/ml for roxithromycin and erythromycin. Levofloxacin also showed good activity against most aerobic sinus isolates, including Eikenella corrodens.

Studies of the anaerobic activity of telithromycin have focused on general and abdominal isolates, with scant information presented regarding respiratory anaerobic isolates (7, 8, 12). In our study telithromycin was quite active (MIC, ≤4 μg/ml) against 94% of the anaerobe strains tested.

Methodological differences and the effect of CO2 in the atmosphere of incubation on the pH of the medium may account for some of the variability between the studies (4, 8-10, 12), but results were remarkably similar overall. Ednie et al. (8), who used the Oxyrase method and Wilkins-Chalgren agar without CO2, reported a telithromycin MIC50 of 4 μg/ml for nine Fusobacterium nucleatum strains and an MIC90 of 0.25 μg/ml for Prevotella melaninogenica. Edlund et al. (7) reported telithromycin to have an MIC range of 0.016 to 8.0 μg/ml against 30 isolates of Fusobacterium nucleatum and of 0.016 to 1.0 μg/ml against 30 strains of Propionibacteriumacnes.

Telithromycin had its greatest activity against gram-positive aerobes and gram-positive anaerobes. Some aerobic gram-negative strains, as wells as anaerobic strains of Fusobacterium species and Veillonella species, may be resistant to telithromycin. However, compared to currently available macrolides, it exhibited overall a broader spectrum of activity against sinus pathogens, especially those resistant to erythromycin, and thus merits further evaluation as a therapeutic alternative in sinusitis.

Acknowledgments

This study was supported in part by a grant from Aventis Pharmaceuticals.

We thank Judee H. Knight and Alice E. Goldstein for assistance.

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