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Antimicrobial Agents and Chemotherapy, June 1998, p. 1493-1494, Vol. 42, No. 6
0066-4804/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.

Different Erythromycin Resistance Mechanisms in Group C and Group G Streptococci

Janne Kataja,1,* Helena Seppälä,1,2 Mikael Skurnik,3 Hannu Sarkkinen,4 and Pentti Huovinen1

Antimicrobial Research Laboratory, National Public Health Institute,1 Department of Ophthalmology, University of Turku,2 and Turku Centre for Biotechnology, University of Turku and Åbo Akademi University,3 Turku, and Central Hospital of Päijät-Häme, Lahti,4 Finland

Received 10 November 1997/Returned for modification 21 January 1998/Accepted 25 March 1998

    ABSTRACT
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Different mechanisms of erythromycin resistance predominate in group C and G streptococcus (GCS and GGS, respectively) isolates collected from 1992 to 1995 in Finland. Of the 21 erythromycin-resistant GCS and 32 erythromycin-resistant GGS isolates, 95% had the mefA or mefE drug efflux gene and 94% had the ermTR methylase gene, respectively.

    TEXT
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Lancefield group C and G streptococci (GCS and GGS, respectively) may cause pharyngitis and a variety of severe infections in humans (9, 19). For penicillin-allergic patients, erythromycin has long been a good alternative in the treatment of streptococcal infections. Resistance to erythromycin in group A streptococci (GAS) has been reported from a number of countries (6, 11, 15), but there are few reports of erythromycin resistance in GCS and GGS (1, 20).

The two presently recognized mechanisms for resistance to macrolide antibiotics in streptococci are target-site modification and active-drug efflux. Target-site modification is mediated by an erythromycin resistance methylase (erm) that reduces binding of macrolide, lincosamide, and streptogramin B (MLS) antibiotics to the target site in the 50S ribosomal subunit (5). The phenotypic expression of MLS resistance can be inducible (IR) or constitutive (CR). In active-drug efflux, the protein encoded by the mefA or mefE (macrolide efflux) gene causes resistance to 14- and 15-membered macrolide compounds only (3, 18). This phenotype is called the M phenotype (17).

In the present study, we investigated the susceptibilities of GCS and GGS to erythromycin and three other antimicrobials and determined the erythromycin resistance mechanism in the isolates resistant to erythromycin.

From January 1992 through December 1995, a total of 579 clinical isolates of GCS and 911 clinical isolates of GGS were collected from throat swab and pus samples in the microbiological laboratory of the Central Hospital of Pohjois-Karjala in Joensuu, Finland, and sent to the Antimicrobial Research Laboratory of the National Public Health Institute, Turku, Finland. Identification of beta -hemolytic isolates was performed by a commercial latex-agglutination technique (Streptex; Wellcome, Dartford, England). The MICs of erythromycin, clindamycin, tetracycline, and penicillin (Sigma Chemical Co. Ltd., St. Louis, Mo.) were determined by the plate dilution method according to the recommendations of the National Committee for Clinical Laboratory Standards (8) as described previously (12). The breakpoints for resistance were as follows: erythromycin and clindamycin, >= 1 µg/ml (8); penicillin, >= 4 µg/ml (8); and tetracycline, >= 8 µg/ml (8). The control strains were those described previously (11).

The IR, CR, and M phenotypes of erythromycin-resistant GCS and GGS isolates were determined by the double-disk test by using erythromycin and clindamycin disks as described previously (12).

For the detection of different erythromycin resistance genes in the genomes of GCS and GGS by PCR, DNA was extracted as described previously (14). The DNAs of the erythromycin-resistant isolates were amplified with primers specific for the ermA, ermB, ermC, and mefA or -E genes; PCR conditions for the primer sets were as described previously (16, 3). Primers used for the detection of the ermTR gene were designed on the basis of the sequence of ermTR (13) as follows: 5'-ATAGAAATTGGGTCAGGAAAAGG-3' (TR1) and 5'-TTGATTTTTAGTAAAAAG-3' (TR2). The PCR mixture was as described previously (13). A total of 35 cycles were carried out with a thermal reactor (model HB-TR1; Hybaid Ltd., Middlesex, United Kingdom) as follows: denaturation at 94°C for 30 s, annealing at 42°C for 60 s, and elongation at 72°C for 90 s. To confirm that TR1 and TR2 had amplified the ermTR gene, the PCR products obtained by using these primers were digested with HinfI endonuclease (Promega Co., Madison, Wis.) under conditions recommended by the manufacturer. The DNAs containing erythromycin resistance genes from Staphylococcus aureus RN2864 (7), Clostridium perfringens CP592 (2), Staphylococcus aureus IHT 62242, Streptococcus pyogenes A200 (13), and S. pyogenes A569 were used as positive controls in the PCR-based detection of the ermA, ermB, ermC, ermTR, and mefA or -E genes, respectively. After the amplification, the detection and visualization of the PCR products were performed as described previously (10). Amplification of the DNAs from the positive controls with the corresponding primers produced PCR products of expected sizes; ermA, ermB, and ermC were 640 bp, ermTR was 530 bp, and mefA or -E was 1.4 kb. Digestion of the PCR products obtained with the TR1 and TR2 primers from the control strain produced bands with lengths of 355, 128, and 54 bp, as expected.

Susceptibility results. The proportions of the GCS and GGS isolates resistant to erythromycin (3.6 and 3.5%, respectively) and clindamycin (1.0 and 0.3%, respectively) were similar, but the proportion of GCS isolates resistant to tetracycline was clearly lower than that of GGS isolates (13 versus 43%). All isolates were susceptible to penicillin (Table 1). Tetracycline resistance was found in 2 (10%) and 16 (50%) of the 21 erythromycin-resistant GCS and 32 GGS isolates, respectively, which parallels the common tetracycline resistance level well. Hence, it seems that tetracycline resistance in GCS or GGS is not linked to erythromycin resistance.

                              
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  		TABLE 1.   MICs of four antibiotics for 579 GCS isolates and 911 GGS isolates

Published figures of the frequencies of erythromycin resistance in GCS and GGS from other countries are scarce. In England in the middle of the 1980s, erythromycin resistance was found in 1.4 and 1.6% of GCS and GGS isolates, respectively (1). In Taiwan in 1993 to 1994, resistance to erythromycin was found in 41.7 and 23.5% of GCS and GGS isolates, respectively (19).

Erythromycin resistance phenotypes and genes. Nearly all (95%) of the erythromycin-resistant GCS isolates had the M phenotype, whereas 91 and 6% of the erythromycin-resistant GGS isolates had the IR and the CR phenotype, respectively.

All isolates with the M phenotype were positive with primers specific for the mefA or -E gene. Likewise, the ermTR gene was found in all IR phenotype isolates. Of the CR phenotype isolates, one had the ermTR gene and the other had the ermB gene. Hence, 20 (95%) of the 21 erythromycin-resistant GCS isolates had the mefA or -E gene, and the mechanism conveyed by this gene has been shown to be active-drug efflux (17). As 30 (94%) of the 32 erythromycin-resistant GGS isolates had the ermTR gene and one GGS isolate had the ermB gene, altogether 31 (97%) of the 32 GGS isolates had an erm gene, and the mechanism of resistance is therefore proposed to be target-site modification.

The mefA gene was first identified in GAS (16), and we have also found it in GAS with the M phenotype (4). The ermTR gene in GAS A200 was recently characterized by us (13), and we have found it to be common in Finland among GAS with the IR phenotype (4). This study is the first to show that the ermTR gene and the mefA or -E gene may exist in other beta -hemolytic streptococcus species as well. Because the erythromycin resistance genes are the same in GCS, GGS, and GAS in Finland, it is possible that the genes have transferred among these species. Although there is an association between the active-efflux mechanism and GCS in Finland, it is possible that this association is not a universal phenomenon. In Taiwan the MIC results showed that 33.3% of the GCS isolates were resistant to clindamycin (20), which is related to MLS resistance (12).

In summary, different mechanisms of erythromycin resistance predominate in GCS and GGS isolates in Finland.

    ACKNOWLEDGMENTS

We are indebted to Minna Lamppu, Tarja Laustola, Anna-Liisa Lumiaho, and Tuula Randell for expert technical assistance and to Monica Österblad for editorial assistance.

This work was supported by the Sigrid Juselius Foundation (funds to J. Kataja and H. Seppälä), the Maud Kuistila Foundation (funds to H. Seppälä), and the Scandinavian Society for Antimicrobial Chemotherapy (funds to P. Huovinen).

    FOOTNOTES

* Corresponding author. Mailing address: Antimicrobial Research Laboratory, National Public Health Institute, P.O. Box 57, 20521 Turku, Finland. Phone: 358-2-2519255. Fax: 358-2-2519254. E-mail: janne.kataja{at}utu.fi.

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Antimicrobial Agents and Chemotherapy, June 1998, p. 1493-1494, Vol. 42, No. 6
0066-4804/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.


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