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Antimicrobial Agents and Chemotherapy, December 2001, p. 3504-3508, Vol. 45, No. 12
Department of Microbiology, Toronto Medical
Laboratories and Mount Sinai Hospital,1 and
Department of Laboratory Medicine and Pathobiology,
University of Toronto,2 Toronto, Canada
Received 23 March 2001/Returned for modification 23 June
2001/Accepted 22 September 2001
Macrolide resistance has been demonstrated in group B streptococcus
(GBS), but there is limited information regarding mechanisms of
resistance and their prevalence. We determined these in GBS obtained
from neonatal blood cultures and vaginal swabs from pregnant women. Of
178 isolates from cases of neonatal GBS sepsis collected from 1995 to
1998, 8 and 4.5% were resistant to erythromycin and clindamycin,
respectively, and one isolate showed intermediate penicillin resistance
(MIC, 0.25 µg/ml). Of 101 consecutive vaginal or rectal/vaginal
isolates collected in 1999, 18 and 8% were resistant to
erythromycin and clindamycin, respectively. Tetracycline resistance was
high (>80%) among both groups of isolates. Of 32 erythromycin-resistant isolates, 28 possessed the erm
methylase gene (7 ermB and 21 ermTR/ermA) and 4 harbored the mefA gene; one isolate harbored both
genes. One isolate which was susceptible to erythromycin but resistant to clindamycin (MIC, 4 µg/ml) was found to have the
linB gene, previously identified only in
Enterococcus faecium. The mreA gene was
found in all the erythromycin-resistant strains as well as in 10 erythromycin-susceptible strains. The rate of erythromycin resistance
increased from 5% in 1995-96 to 13% in 1998-99, which coincided
with an increase in macrolide usage during that time.
Group B streptococcus (GBS),
although a normal commensal of the gastrointestinal and genitourinary
tracts, is capable of causing invasive infections in neonates, pregnant
women, and persons with underlying medical conditions
(26). Between 15 and 35% of pregnant women are
asymptomatic carriers of GBS, and in the early 1990s 0.2 to 0.8% of
neonates had GBS bacteremia (26). With the advent of
consensus guidelines for intrapartum antibiotic prophylaxis in the
United States, early-onset disease decreased by 65% from 1993 to 1998 (25). Further declines are predicted if compliance with
prophylaxis can be improved (6). However, the increased use of antimicrobials for prophylaxis has raised concerns regarding the
emergence of resistance. In addition, increased resistance may have an
impact on the efficacy of prophylaxis itself.
Penicillin is the drug of choice for prophylaxis and treatment of GBS
disease, and so far, resistance to this agent has not been reported
(1, 2, 10, 16, 20, 30, 31). However, macrolides are the
recommended second-line agents and the first alternative in mothers
with a penicillin allergy. Allergy to penicillin has been reported in
12% of pregnant women in the United States (22). Several studies have
reported increasing resistance of GBS to macrolides. The SENTRY
surveillance study found that 25 and 14% of neonatal bloodstream
isolates in the United States and Canada, respectively, were resistant
to erythromycin, with 7% resistant to clindamycin (2). In
a U.S. study of vaginal isolates, prevalence of erythromycin resistance
rose from 1% from 1980 to 1993 to 18% in 1997-98 (19).
Resistance rates have also been found to vary with geographical
location. High rates have been noted in California (32 and 12% to
erythromycin and clindamycin, respectively), with lower rates in
Florida (9 and 2%, respectively) (16). In Canada, a study
of invasive isolates collected from several provinces in 1996 revealed
that 7% were resistant to erythromycin and 4% were resistant to
clindamycin (30).
The most frequently encountered macrolide resistance mechanisms in
streptococci are ribosomal modification by a methylase encoded by an
erm gene (33) and drug efflux by a
membrane-bound protein encoded by a mef gene
(17). Presence of the Erm methylase confers resistance to
erythromycin and inducible or constitutive resistance to lincosamides
and streptogramin B (macrolide-lincosamide-streptogramin B [MLS]
phenotype), whereas presence of the Mef pump confers resistance only to
14- and 15-membered macrolides (M phenotype). A second efflux
mechanism, encoded by the mreA gene, has been described for
GBS (7). However, susceptible GBS strains have also been shown to possess the mreA gene, and it might function as a
housekeeping gene (G. Clarebout and R. Leclercq, 39th Intersci. Conf.
Antimicrob. Agents Chemother. abstr. 840, p. 115, 1999). Although
several previous studies have documented the prevalence of macrolide
resistance in GBS (2, 10, 16, 19, 22, 30), few have
identified the mechanisms of resistance or have compared the prevalence
of resistance in early- and late-onset neonatal sepsis or
contemporaneous neonatal sepsis and maternal vaginal isolates. The
relative contribution of the presence of the erm and
mef genes in contributing to a resistance phenotype may have
important implications for therapy, since there are differences in drug
susceptibility depending on the mechanism of resistance. In this study
we report the prevalence and mechanisms of macrolide-lincosamide
resistance in neonatal sepsis GBS isolates collected from 1995 to 1998 and vaginal isolates from pregnant women collected in 1999.
Strains.
A total of 279 GBS strains were screened for
antimicrobial susceptibility. Strains were obtained from cases of
neonatal sepsis (n = 179) as well as from pregnant
women (n = 101). Neonatal sepsis isolates were
collected from 1995 to 1998 through the Toronto Invasive Bacterial
Diseases Network, a population-based surveillance system for invasive
bacterial diseases, including GBS, in the metropolitan Toronto and Peel
region (population, 3.5 million in 1996). All hospitals and the three
largest private laboratories serving residents of the population area
reported sterile site isolates of GBS to the central study office.
Clinical data were obtained from attending physicians and infection
control practitioners. Lab audits were conducted semiannually to ensure
complete reporting. Vaginal isolates were collected from screening
vaginal or combined vaginal and rectal swabs in pregnant women in March
1999 by the largest private laboratory serving an estimated 60% of
physician offices in metropolitan Toronto and the surrounding area. All isolates were confirmed to be GBS by standard methodology.
Susceptibility testing.
Strains were tested against
penicillin, amoxicillin, cefuroxime, cefotaxime, ceftriaxone,
erythromycin, clindamycin, tetracycline, gentamicin, and
chloramphenicol by broth microdilution following NCCLS guidelines
(21). In order to distinguish between macrolide (M) and
MLS or macrolide-lincosamide (ML) phenotypes, clindamycin discs were
placed on plates at 12 and 22 mm from a central erythromycin (15-µg)
disk and incubated overnight at 37°C in 5%
CO2. Blunting of the growth between clindamycin
and erythromycin discs and no inhibition around the clindamycin disk
indicated inducible MLS resistance (MLS I). Constitutive resistance
(MLS C) was defined as growth inhibition zones of Detection of resistance genes.
PCR was used to detect
erm and mef genes in the erythromycin- and
clindamycin-resistant isolates as described previously
(9). Primers for detection of the mreA gene
were based on GenBank accession no. U92073 (8) as follows:
MREA (bp 291 to 314), 5'-3' AGA CAC CTC GTC TAA CCT TCG CTC; and MREB
(bp 706 to 684), 5'-3' TCC ATG TAC TAC CAT GCC ACA GG. Cycling was
carried out using 5 µl of template (9) in a 25-µl
reaction mixture in a 9600 Perkin-Elmer Thermocycler as follows:
initial denaturation at 94°C for 4 min followed by denaturation at
93°C for 30 s, annealing at 50°C for 30 s, and elongation
at 72°C for 1 min for a total of 30 cycles. A final extension step
was carried out at 72°C for 5 min. Primers and PCR conditions for
detection of the linB gene were as described previously
(5). PCR products were resolved on 1% agarose gels.
Macrolide consumption.
Data on macrolide usage in the
province of Ontario were obtained through IMS HEALTH, Montreal, Canada.
The GBS neonatal sepsis cases identified from 1995 to 1998 comprised 163 cases of early-onset disease (illness during the first
week of life) and 33 cases of late-onset disease (illness from days 7 to 90). A statistically significant decrease in incidence of invasive
disease (P = 0.001; chi-square test for trend) was noted over the period of the study (Fig.
1). Isolates were available for 178 cases, of which 153 were early-onset disease and 25 were late-onset
disease.
0066-4804/01/$04.00+0 DOI: 10.1128/AAC.45.12.3504-3508.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Prevalence and Mechanisms of Macrolide Resistance
in Invasive and Noninvasive Group B Streptococcus Isolates from
Ontario, Canada
ABSTRACT
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
INTRODUCTION
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
15 mm around both
the clindamycin and erythromycin disks. Heteroresistance to clindamycin
was defined as inhibition zones of 
15 mm around the clindamycin disk
but with resistant colonies growing within this zone. The M phenotype was characterized by resistance to erythromycin and susceptiblity to clindamycin.
RESULTS
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
View larger version (26K):
[in a new window]
FIG. 1.
Prevalence of early-onset and late-onset GBS disease
among neonates from 1995 to 1998.
Susceptibility testing revealed that none of the isolates were
resistant to 
-lactam drugs or vancomycin, although one neonatal sepsis isolate showed intermediate susceptibility to penicillin (MIC,
0.25 µg/ml). This isolate, although susceptible to ceftriaxone, was
less so than other strains (MIC, 0.5 µg/ml for this isolate versus
0.125 µg/ml for other strains). The majority of neonatal sepsis
strains (87%) showed resistance to tetracycline, and a few (2.8%)
were resistant to chloramphenicol. Erythromycin resistance was present
in 8% of strains, with 4.5% of these also resistant to clindamycin. A
single isolate was susceptible to erythromycin but resistant to
clindamycin (MIC, 4 µg/ml). Although the incidence of invasive
disease decreased over the period of the study, the rate of
erythromycin resistance increased from 5% in 1995-96 to 13% in
1998-99 (P = 0.06; chi-square test). Macrolide usage
in Ontario increased from 11.8 to 14.3 prescriptions/100 persons between 1992 and 1997. There was no difference in clinical severity or
outcome in cases associated with macrolide resistance, and these cases
were not clustered geographically within the surveillance area.
Of the 101 consecutive vaginal and rectal and vaginal isolates collected in 1999, 18% were resistant to erythromycin and 8% were constitutively or inducibly resistant to clindamycin. Isolates were susceptible to penicillin and chloramphenicol, but as noted with the neonatal sepsis isolates, resistance to tetracycline was high (82% resistant). In total, 11.5% of erythromycin-resistant strains were identified among neonatal sepsis and vaginal isolates combined.
The association of resistance mechanisms with erythromycin and
clindamycin MICs is shown in Table 1.
For only one M phenotype strain
(mef+) was the erythromycin MIC high (16
µg/ml); for the other three, the MIC was 4 µg/ml. The majority of
erythromycin-resistant strains with constitutive or inducible
clindamycin resistance possessed the ermTR gene, an allele
of ermA (24) (Table 1 and Fig.
2). All of the ermB strains
were constitutively resistant, with one strain showing heteroresistance
to clindamycin. By comparison, only 38% of strains with
ermTR/ermA showed constitutive resistance and one of these
also possessed a mef gene (erythromycin and clindamycin MICs
were each 16 µg/ml). Clindamycin had a MIC of 16 mg/liter for all
the ermTR/ermA constitutively resistant strains but only for
three of seven ermB strains. Inducibly resistant strains
appeared to have a susceptible clindamycin MIC by broth microdilution
and single-disk diffusion.
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A single isolate which was susceptible to erythromycin but resistant to clindamycin was found to have the linB gene. The mreA gene was present in all the erythromycin-resistant strains as well as in 10 randomly selected erythromycin-susceptible strains from patients with neonatal sepsis.
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DISCUSSION |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
|
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In this study, a marked increase in prevalence of erythromycin resistance in invasive isolates occurred between 1995 and 1997 and this increase was reflected in the vaginal and rectal isolates collected in 1999, of which 18% were erythromycin resistant. There was a temporal increase in macrolide usage in the province of Ontario between 1994 and subsequent years, which could account for the increase in resistance.
High rates of tetracycline resistance were noted, as has been described in other studies (3, 4, 11, 31), and this is likely due to the presence of the tetM gene (27). tetM can be readily transferred via conjugative transposons (29), which may account for its spread under selective pressure. However, the reason for its high prevalence in GBS is unclear since tetracycline is not used prophylactically or therapeutically in pregnant women or in the pediatric population.
Most studies on antimicrobial susceptibility of GBS strains have found uniform susceptibility to penicillin (1, 2, 10, 16, 19, 22, 30, 31), although increased resistance to ampicillin, in particular as a result of ante- and intrapartum treatment with this agent, has been described (18). However, Vermillion et al. (32), in a study of 574 GBS isolates collected from an obstetric population in the United States in 1998, reported 1.8% of strains with nonsusceptibility to penicillin; MIC levels were not reported. In our study one neonatal sepsis strain showed intermediate penicillin resistance (MIC, 0.25 µg/ml). Emergence of resistance to penicillin should be monitored since this is the first-line agent for prophylaxis.
Erythromycin resistance was found to be predominantly due to the
presence of an Erm methylase and the ermTR/ermA gene was most prevalent (75% of MLS strains). An ermTR/ermA gene was
identified in a strain collected as far back as 1995. The
ermTR/ermA gene has been identified in group A
streptococcus (GAS) strains from different geographical locations
(9, 11, 13, 14), in Group C and G streptococci (15,
28), and in Peptostreptococcus strains
(23). In these studies, the ermTR/ermA strains
rarely, if ever, possessed a constitutive phenotype. Our previous study of GAS strains identified only 1 of 19 ermTR/ermA strains
with constitutive resistance. The number of constitutively resistant ermTR/ermA strains identified in this study suggests that
this phenotype is more highly associated with GBS than with GAS. In addition, a high clindamycin MIC (16 mg/liter) was associated with
all of the constitutively resistant ermTR/ermA
strains but with only 42% of ermB strains with this
phenotype. Interestingly, inducibly resistant ermTR/ermA
strains showed a susceptible clindamycin MIC by broth microdilution as
well as by single disk diffusion and based on these tests alone, they
would be phenotypically indistinguishable from mef-positive
strains. In a routine clinical diagnostic laboratory, it would be
important to carry out a double-disk diffusion test as described here
to verify clindamycin resistance.
Bozdogan et al. in 1999 described a novel lincosamide-inactivating nucleotidyltransferase encoded by the linB gene in Enterococcus faecium (5). Our studies demonstrate its presence in GBS. It will be interesting to see whether, or more likely how soon, this gene spreads to other GBS strains or indeed to other streptococcal species.
The low prevalence of the mef gene (16% of erythromycin-resistant strains) is in contrast to erythromycin-resistant GAS strains isolated in Ontario, where 70% of strains possessed this gene (9). Among pneumococcal strains collected from across Canada, 55% were mef positive (12). The mef gene has been shown to be mobile in a variety of gram-positive bacteria (17), and its low incidence in GBS is surprising, although the potential for spread is presumably high. A second efflux mechanism, encoded by the mreA gene, has been reported to be associated with macrolide resistance in GBS (8). However, all strains tested (both resistant and susceptible) possessed this gene, which adds weight to its questionable role as a cause of macrolide resistance (Clarebout and Leclercq, 39th ICAAC).
Our study shows that although the incidence of invasive neonatal GBS disease is decreasing in association with increasing use of intrapartum antimicrobial prophylaxis, macrolide resistance in GBS strains appears to be increasing. The clinical relevance of macrolide-resistant GBS in women treated with macrolides for intrapartum prophylaxis needs to be assessed.
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ACKNOWLEDGMENT |
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This work was supported by a grant from the Canadian Bacterial Diseases Network.
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FOOTNOTES |
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* Corresponding author. Mailing address: Mount Sinai Hospital, 600 University Ave., Room 1483, Toronto ON M5G 1X5, Canada. Phone: (416) 586-8459. Fax: (416) 586-8746. E-mail: jdeazavedo{at}mtsinai.on.ca.
Present address: The Samuel Lunenfeld Research Institute of Mount
Sinai Hospital, Toronto ON M5G 1X5, Canada.
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Antimicrobial Agents and Chemotherapy, December 2001, p. 3504-3508, Vol. 45, No. 12
0066-4804/01/$04.00+0 DOI: 10.1128/AAC.45.12.3504-3508.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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(2007). A composite transposon associated with erythromycin and clindamycin resistance in group B Streptococcus. J Med Microbiol
56: 947-955
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Amezaga, M. R., McKenzie, H.
(2006). Molecular epidemiology of macrolide resistance in {beta}-haemolytic streptococci of Lancefield groups A, B, C and G and evidence for a new mef element in group G streptococci that carries allelic variants of mef and msr(D). J Antimicrob Chemother
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Zeng, X., Kong, F., Wang, H., Darbar, A., Gilbert, G. L.
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50: 204-209
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Marimon, J. M., Valiente, A., Ercibengoa, M., Garcia-Arenzana, J. M., Perez-Trallero, E.
(2005). Erythromycin Resistance and Genetic Elements Carrying Macrolide Efflux Genes in Streptococcus agalactiae. Antimicrob. Agents Chemother.
49: 5069-5074
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Dogan, B., Schukken, Y. H., Santisteban, C., Boor, K. J.
(2005). Distribution of Serotypes and Antimicrobial Resistance Genes among Streptococcus agalactiae Isolates from Bovine and Human Hosts. J. Clin. Microbiol.
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Woo, P. C. Y., Tse, H., Wong, S. S. Y., Tse, C. W. S., Fung, A. M. Y., Tam, D. M. W., Lau, S. K. P., Yuen, K.-y.
(2005). Life-Threatening Invasive Helcococcus kunzii Infections in Intravenous-Drug Users and ermA-Mediated Erythromycin Resistance. J. Clin. Microbiol.
43: 6205-6208
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Achard, A., Villers, C., Pichereau, V., Leclercq, R.
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49: 2716-2719
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von Both, U., Buerckstuemmer, A., Fluegge, K., Berner, R.
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Gonzalez, J. J., Andreu, A., the Spanish Group for the Study of Perinatal Infec,
(2005). Multicenter Study of the Mechanisms of Resistance and Clonal Relationships of Streptococcus agalactiae Isolates Resistant to Macrolides, Lincosamides, and Ketolides in Spain. Antimicrob. Agents Chemother.
49: 2525-2527
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Klaassen, C. H. W., Mouton, J. W.
(2005). Molecular Detection of the Macrolide Efflux Gene: To Discriminate or Not To Discriminate between mef(A) and mef(E). Antimicrob. Agents Chemother.
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Duarte, R. S., Bellei, B. C., Miranda, O. P., Brito, M. A. V. P., Teixeira, L. M.
(2005). Distribution of Antimicrobial Resistance and Virulence-Related Genes among Brazilian Group B Streptococci Recovered from Bovine and Human Sources. Antimicrob. Agents Chemother.
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Desjardins, M., Delgaty, K. L., Ramotar, K., Seetaram, C., Toye, B.
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Malbruny, B., Werno, A. M., Anderson, T. P., Murdoch, D. R., Leclercq, R.
(2004). A new phenotype of resistance to lincosamide and streptogramin A-type antibiotics in Streptococcus agalactiae in New Zealand. J Antimicrob Chemother
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Fluegge, K., Supper, S., Siedler, A., Berner, R.
(2004). Antibiotic Susceptibility in Neonatal Invasive Isolates of Streptococcus agalactiae in a 2-Year Nationwide Surveillance Study in Germany. Antimicrob. Agents Chemother.
48: 4444-4446
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Uh, Y., Jang, I. H., Hwang, G. Y., Lee, M. K., Yoon, K. J., Kim, H. Y.
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42: 3306-3308
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Tang, P., Ng, P., Lum, M., Skulnick, M., Small, G. W., Low, D. E., Sarabia, A., Mazzulli, T., Wong, K., Simor, A. E., Willey, B. M.
(2004). Use of the Vitek-1 and Vitek-2 Systems for Detection of Constitutive and Inducible Macrolide Resistance in Group B Streptococci. J. Clin. Microbiol.
42: 2282-2284
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Acikgoz, Z. C., Almayanlar, E., Gamberzade, S., Gocer, S.
(2004). Macrolide Resistance Determinants of Invasive and Noninvasive Group B Streptococci in a Turkish Hospital. Antimicrob. Agents Chemother.
48: 1410-1412
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Hasenbein, M. E., Warner, J. E., Lambert, K. G., Cole, S. E., Onderdonk, A. B., McAdam, A. J.
(2004). Detection of Multiple Macrolide- and Lincosamide-Resistant Strains of Streptococcus pyogenes from Patients in the Boston Area. J. Clin. Microbiol.
42: 1559-1563
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Heelan, J. S., Hasenbein, M. E., McAdam, A. J.
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Bingen, E., Doit, C., Bidet, P., Brahimi, N., Deforche, D.
(2004). Telithromycin Susceptibility and Genomic Diversity of Macrolide-Resistant Serotype III Group B Streptococci Isolated in Perinatal Infections. Antimicrob. Agents Chemother.
48: 677-680
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d'Oliveira, R. E.C., Barros, R. R., Mendonca, C. R.V., Teixeira, L. M., Castro, A. C.D.
(2003). Susceptibility to antimicrobials and mechanisms of erythromycin resistance in clinical isolates of Streptococcus agalactiae from Rio de Janeiro, Brazil. J Med Microbiol
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Lopardo, H. A., Vidal, P., Jeric, P., Centron, D., Paganini, H., Facklam, R. R., Elliott, J.
(2003). Six-Month Multicenter Study on Invasive Infections Due to Group B Streptococci in Argentina. J. Clin. Microbiol.
41: 4688-4694
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Werno, A. M., Anderson, T. P., Murdoch, D. R.
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Diekema, D. J., Andrews, J. I., Huynh, H., Rhomberg, P. R., Doktor, S. R., Beyer, J., Shortridge, V. D., Flamm, R. K., Jones, R. N., Pfaller, M. A.
(2003). Molecular Epidemiology of Macrolide Resistance in Neonatal Bloodstream Isolates of Group B Streptococci. J. Clin. Microbiol.
41: 2659-2661
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Betriu, C., Culebras, E., Gomez, M., Rodriguez-Avial, I., Sanchez, B. A., Agreda, M. C., Picazo, J. J.
(2003). Erythromycin and Clindamycin Resistance and Telithromycin Susceptibility in Streptococcus agalactiae. Antimicrob. Agents Chemother.
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Poyart, C., Jardy, L., Quesne, G., Berche, P., Trieu-Cuot, P.
(2003). Genetic Basis of Antibiotic Resistance in Streptococcus agalactiae Strains Isolated in a French Hospital. Antimicrob. Agents Chemother.
47: 794-797
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