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JAC Advance Access published online on September 11, 2008
Journal of Antimicrobial Chemotherapy, doi:10.1093/jac/dkn388
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© The Author 2008. Published by Oxford University Press on behalf of the British Society for Antimicrobial Chemotherapy. All rights reserved. For Permissions, please e-mail: journals.permissions@oxfordjournals.org

Original research

Molecular characterization of erythromycin-resistant Streptococcus agalactiae strains

Anne-Sophie Domelier1,2,*, Nathalie van der Mee-Marquet1,2, Laurence Arnault2, Laurent Mereghetti1,{dagger}, Philippe Lanotte1, Agnès Rosenau1, Marie-Frédérique Lartigue1,2 and Roland Quentin1,2

1 Université François-Rabelais de Tours, UFR de Médecine, EA 3854 ‘Bactéries et risque materno-fœtal’, Institut Fédératif de Recherche 136 ‘Agents Transmissibles et Infectiologie’, 37032 Tours Cedex, France 2 Service de Bactériologie et Hygiène Hospitalière, Hôpital Trousseau, CHU de Tours, 37044 Tours, France

* Correspondence address. Service de Bactériologie-Hygiène, CHRU Trousseau, 37044 Tours cedex 9, France. Tel: +33-2-47-47-81-13; Fax: +33-2-47-47-85-30; E-mail: as.domelier{at}chu-tours.fr

Received 28 April 2008; returned 14 June 2008; revised 13 August 2008; accepted 19 August 2008


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Objectives: The aim of this study is to identify the molecular characteristics of erythromycin-resistant (Ermr) Streptococcus agalactiae strains and to correlate with the clinical origin of strains.

Methods: From 711 S. agalactiae strains, 119 Ermr strains (17%) were collected, serotyped and screened for macrolide resistance genes. The genetic relationship between strains was established by the PFGE analysis. Strains were tested for the group II intron GBSi1 downstream of the scpB gene, IS1548 in the hylB gene, four prophage DNA fragments and a lineage defined by multilocus sequence typing as ST-17.

Results: Erythromycin resistance involved 8% of serotype Ia, 15% of serotype Ib, 9% of serotype II, 16% of serotype III, 31% of serotype IV and 35% of serotype V. The prevalence of Ermr strains was higher among strains isolated from the gastric fluid of neonates (33%) than in those isolated from bacteraemia and meningitis during early-onset disease (EOD) or late-onset disease (7% and 11%) (P = 0.001). In serotype III, Ermr strains were more frequent in vaginal carriage (22%) and colonized neonates (18%) than in EOD (0%) (P = 0.03). The mef(A) gene was the most common in serotype Ia (55%), the erm(A) gene in serotype Ib (75%) and the erm(B) gene in the other serotypes (56% to 75%). All resistant strains with IS1548 also had the erm(B) gene. Ermr strains were not randomly distributed in the different PFGE genogroups, and 11% had the GBSi1 intron, 37% had at least one prophage DNA fragment and 7% belonged to ST-17.

Conclusions: Erythromycin resistance varied according to the clinical origin, serotype and molecular characteristics of S. agalactiae strains.

Key Words: group B streptococcus , macrolide , resistance genes , virulence , molecular markers , infectious diseases


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Streptococcus agalactiae, a bacterial pathogen frequently carried in the normal faecal and/or vaginal flora, is the main cause of neonatal infection. This bacterium has recently been recognized as an increasingly common pathogen in non-pregnant adults, in whom sepsis, pneumonia and infections of the urinary tract, skin and soft tissue have been reported.1 Several clinical studies have suggested a lower level of macrolide resistance in invasive strains than in non-invasive S. agalactiae strains.2–5

Prevention strategies have been developed involving intrapartum chemoprophylaxis using penicillin or amoxicillin and have been applied to pregnant women with vaginal S. agalactiae or with risk factors, the aim being to reduce the incidence of early-onset disease (EOD) in newborns.6,7 Erythromycin is recommended as the second-line drug for patients who are allergic to β-lactams.6,7 However, increasing macrolide resistance rates have been reported in recent years.8 There are two mechanisms of resistance: one based on the modification of the ribosome by a methylase encoded by erm genes and the other involving increased drug efflux due to a hydrophobic membrane-bound protein encoded by the mef gene. The presence of an Erm methylase confers resistance to erythromycin and inducible or constitutive resistance to lincosamides and streptogramin B, whereas the presence of an Mef pump confers resistance only to 14- and 15-membered macrolides (M phenotype).9,10

In this study, we determined the molecular characteristics of erythromycin-resistant (Ermr) strains collected during two national epidemiological studies performed to survey antibiotic susceptibility of strains from various clinical origins.11,12 Ermr strains were serotyped and screened for erythromycin resistance genes. The genetic relationship between strains was established by PFGE. Genetic markers, previously described as markers of highly virulent clones of S. agalactiae strains, were investigated by PCR.13–21 Our findings showed that the prevalence of Ermr strains and the nature of the erythromycin resistance genes varied according to the clinical origin of strains, serotypes and molecular characteristics of strains.


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Bacterial strains

We have performed two national epidemiological studies to survey antibiotic resistance of S. agalactiae in France since 2003.11,12 From the 711 French S. agalactiae strains collected with the help of a network of laboratories across the country (Table 1), 119 strains (17%) were Ermr and were isolated from the following sites: 55 vaginal strains from 35–37 week pre-natal screening, 17 from the gastric fluid of neonates without infection but sampled for risk factor as recommended by ANAES,6 1 from the cerebrospinal fluid of newborn, 1 from newborn blood culture and 4 from the cerebrospinal fluid of newborns aged more than 15 days. Forty-one Ermr strains were isolated from non-pregnant adults aged over 18 years: 6 strains from genital infections (3 from endometritis and 3 from orchiditis), 1 from a catheter, 3 from respiratory tract infections, 12 from urinary tract infections, 11 from cutaneous lesions, 7 from bacteraemia and 1 strain from meningitis.


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  		Table 1. Serotype distribution and resistance to erythromycin of S. agalactiae strains isolated from various clinical circumstances

 
Strains were serotyped with a commercial latex agglutination kit (Pastorex Strepto BI, BII and BIII; Bio-Rad Laboratories) and by a previously reported PCR serotype identification method,22 with minor modifications as described recently.23 MICs of antibiotics,11,12 including erythromycin (Abbott, France) and clindamycin (Pfizer), were determined by an agar dilution method in Mueller–Hinton medium supplemented with 5% defibrinated sheep blood (bioMérieux) in 5% CO2 at 37°C, as recommended by the CA-SFM (Comité de l'Antibiogramme de la Société Française de Microbiologie).24 The strains were stored at –80°C with the Cryobeads system (AES Laboratories, France).

Determination of macrolide–lincosamide–streptogramin B (MLSB) phenotype

MLSB phenotype was determined by a disc diffusion method in Mueller–Hinton medium supplemented with 5% defibrinated sheep blood (bioMérieux) at 37°C in 5% CO2.25 Clindamycin discs (Bio-Rad Laboratories) were placed 23 and 30 mm from a central erythromycin disc, and the induction of clindamycin resistance was assessed. The constitutive MLSB phenotype is associated with high resistance to erythromycin and clindamycin. The inducible MLSB phenotype is associated with resistance to erythromycin and susceptibility to clindamycin, with antagonism between the erythromycin and clindamycin discs. The M phenotype (efflux) is determined by resistance to erythromycin, susceptibility to clindamycin and no antagonism between the two discs.

Determination of erythromycin resistance genes

All Ermr strains were screened for erythromycin resistance genes. The erm(B), erm(A) and mef(A) genes were detected by PCR amplification with previously described primers, with minor modifications,26 and the nature of the PCR products was checked by sequencing. Briefly, PCR was carried out in a final volume of 25 µL containing PCR buffer, 0.2 mM of each deoxynucleoside triphosphate, 0.5 µM of each primer, 2 IU of Taq polymerase and 25 ng of template DNA. The cycling conditions were as follows: initial denaturation at 94°C for 2 min, followed by 35 cycles of 94°C for 1 min, 55°C for 1 min and 72°C for 1 min (additional 10 min at 72°C for the final extension). The products were separated by electrophoresis in a 1.6% agarose gel in TBE (8.9 mM Tris, 8.9 mM boric acid, 0.25 mM EDTA; pH 8.0) buffer. Streptococcus pyogenes CIP107003, S. pyogenes CIP107002 and S. agalactiae 03-226 (this study) were used as positive controls for erm(B), erm(A) and mef(A) genes, respectively.

PFGE

The genetic relationship between Ermr strains was determined by PFGE. Genomic DNA was extracted from the isolates and digested with SmaI. It was then subjected to PFGE, as described previously.20 PFGE patterns were detected by ethidium bromide staining and UV transillumination, digitized and analysed with the Taxotron package (Taxolab; Institut Pasteur, Paris, France). The relationships between pulsotypes were determined by unweighted pair group analysis (UPGMA) using average linkages and the Adanson pulsogrouping program (dissimilarity). A dendrogram was drawn with Dendrograf (Taxolab; Institut Pasteur).

PCR detection of GBSi1 intron, IS1548, prophage DNA fragments F3, F5, F7, F10 and the ST-17 lineage position of strains

The presence in the genome of strains of the group II intron GBSi1 downstream of the C5a-peptidase gene scpB,17 the insertion sequence IS1548 in the hylB gene encoding hyaluronate lyase18 and four prophage DNA fragments named F3, F5, F7, F1019 and belonging to the lineage defined as ST-17 by multilocus sequence typing15,21,27 were genetic characteristics previously recognized as markers of highly virulent clones of S. agalactiae strains, on the basis that strains possessing these markers are significantly more frequently associated with neonatal meningitis or endocarditis. Previously described primers and methods were used to test for the group II intron GBSi1,17 IS154817 and the prophage DNA fragments F5, F7 and F10.19 The prophage DNA fragment F319 was detected by PCR amplification in a final volume of 25 µL containing PCR buffer, 0.2 mM of each deoxynucleoside triphosphate, 0.5 µM of each primer F3R (5'-AGT TTC CCG AGA TGC CTT TT-3') and F3L (5'-GGG TGT CCA AGA ATG GAA TG-3'), 2 IU of Taq polymerase and 25 ng of template DNA. The cycling conditions were as follows: 30 cycles of 94°C for 30 s, 45°C for 30 s and 72°C for 1 min (additional 7 min at 72°C for the final extension). The products were separated by electrophoresis in a 1.6% agarose gel in TBE buffer. The positive control strains for PCR were S. agalactiae L24 (GBSi1), L10 (IS1548) and L37 (F3, F5, F7 and F10), as described previously.14,19

The ST-17 lineage position of strains was identified by real-time PCR assay as described previously,27 with minor modifications as also recently described.23 The positive and negative control strains for PCR were S. agalactiae L24 and S. agalactiae CIP107950, respectively.14,27

Statistical analysis

The {chi}2 test and Fisher's exact test were used for statistical analysis.


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Erythromycin resistance according to clinical origin and serotypes of strains

One hundred and nineteen strains were found to be resistant to erythromycin (MIC > 1 mg/L). The origins and serotypes of strains are reported in Table 1. The frequency of the Ermr strains differed according to the clinical condition of isolation. For cases of materno-fetal and neonatal diseases, erythromycin resistance was frequent among strains isolated from gastric fluids (17/52, 33%), less frequent among vaginal strains (55/340, 16%) (P = 0.007) and least common among strains isolated from EOD and late-onset disease (LOD) (6/67, 9%) (P = 0.001). The proportion of Ermr strains from adult infections (17% to 25%) was similar to that of strains from the vagina (16%).

For serotype Ia (8% erythromycin-resistant), serotype Ib (15%) and serotype II (9%), the proportions of Ermr strains did not differ significantly according to the clinical origin of the strains (Table 1). For other serotypes, no significant difference in the prevalence of erythromycin resistance was observed in adult infections. In contrast, erythromycin resistance in the serotype III strains was significantly more frequent for those isolated from vaginal carriage (30/136, 22%) and colonized neonates (gastric fluids) (3/17, 18%) than for those from EOD (0/25, 0%) (P = 0.03). Significantly fewer serotype IV strains isolated from vaginal carriage (3/16 strains, 19%) were resistant than those from gastric fluids (3/4 strains, 75%) (P = 0.03), but no serotype IV strain was found in EOD or LOD. Similarly, significantly fewer serotype V strains isolated from vaginal carriage (11/49 strains, 22%) expressed erythromycin resistance than serotype V strains isolated from the gastric fluid (6/6 strains, 100%) (P = 0.001), but serotype V strains were rarely responsible for EOD or LOD (one case).

Erythromycin resistance genes according to the origin, MLSB phenotype and serotype of strains

Seventy-six of the 119 strains (64%) had the erm(B) gene, 29 (24%) the erm(A) gene and 12 (10%) the mef(A) gene (Table 2).


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  		Table 2. MLSB phenotype and erythromycin resistance genes according to various clinical circumstances

 
No significant differences in the distribution of the three erythromycin resistance genes were found between strains of the various clinical origins, except for the erm(B) gene which was significantly more frequently found in Ermr strains from cutaneous lesions (10/11 strains, 91%) than in those of other clinical origins (16/30 strains, 53%) (P = 0.033) (Table 2).

Eighty-two percent of the strains (72/88) with a constitutive MLSB phenotype carried the erm(B) gene and 18% (16/88) the erm(A) gene. Twenty-four percent (4/17) of the strains that expressed the inducible MLSB phenotype had the erm(B) gene and 76% (13/17) the erm(A) gene. Eighty-six percent (12/14) of the strains with the M phenotype had the mef(A) gene, and the PCR tests used revealed no gene in 14% (2/14).

The distribution of erythromycin resistance genes differed significantly between serotypes (Table 3) (P = 0.0001). The mef(A) gene was the most frequently found gene in Ermr serotype Ia strains (6/11, 55%); the erm(A) gene was the most frequently found gene in Ermr serotype Ib strains (6/8, 75%) and the erm(B) gene was the most common in the other Ermr serotypes, especially in the major serotypes III (36/49, 73%) and V (24/32, 75%).


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  		Table 3. Distribution of erythromycin resistance genes according to serotype and genetic markers of virulent clones of strains

 
PFGE and molecular characterization of Ermr strains

PFGE characterization was undertaken for 111 Ermr strains, the DNA from 8 strains being consistently resistant to SmaI digestion in repeated tests. The UPGMA method performed with the PFGE patterns generated a dendrogram in which the strains were distributed into six different PFGE groups, with 60% of dissimilarity (G1–G6; Figure 1). The erythromycin resistance genes erm(B), erm(A) and mef(A) were not equally distributed among the six PFGE groups (P = 0.0013, Figure 1). The prevalence of the erm(B) gene was 79% in the PFGE group G1 (23/29), 93% in G2 (13/14), 70% in G5 (16/23) and ≤50% in the other PFGE groups. The prevalence of the erm(A) gene was 57% in the PFGE group G3 (4/7) and ≤30% in the other PFGE groups. No mef(A) gene was found in PFGE groups G1 and G2.


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  		Figure 1. Genetic relationships between 119 Ermr strains analysed by the UPGMA method using PFGE characterization of strains. The strains were distributed into six distinct groups designated G1–G6. aNumber and proportion of Ermr strains in each PFGE group. bNumber and proportion of strains that possess each erythromycin resistance gene in each PFGE group. NR, not restricted.

 
Among the PFGE groups of Ermr strains, the distribution of markers of highly virulent clones of S. agalactiae differed (Figure 1): only 1 of the 29 Ermr strains of group G1 possessed markers of highly virulent clones; the Ermr strains that had IS1548 in the hylB gene (14 strains) were in the PFGE group G2 in 8 cases; the Ermr strains that belonged to the ST-17 lineage or that had the group II intron GBSi1 downstream of the scpB gene were frequently in the PFGE group G6 (5/9 strains of the ST-17 lineage and 7/13 strains that had the group II intron GBSi1).

The prevalence of the highly virulent clone markers found in the 119 Ermr strains is reported in Table 3. The erm(B) gene was the only erythromycin resistance gene found in the 14 Ermr strains that had IS1548 in the hylB gene. Otherwise, the other erythromycin resistance genes did not appear to be associated with the other virulence markers.


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We found a higher prevalence of Ermr strains isolated from gastric fluids than from vaginal samples that involved serotypes Ib, II, IV and V. In contrast, strains responsible for EOD, mostly of serotype III as usually described,3,5,17 were never found as resistant to erythromycin in our studied population (Table 1).

Previous studies have suggested a possible association between serotype V strains and the presence of the erm(A) gene26 or the erm(B) gene28–30 and between serotype Ia and the mef(A) gene.28 We also found such associations: the mef(A) gene was found in 55% of the Ermr serotype Ia strains, the erm(A) gene in 75% of the Ermr serotype Ib strains and the erm(B) gene in 74% of the Ermr serotype III strains and 75% of the Ermr serotype V strains (Table 3). In addition, we found that the erm(B), erm(A) and mef(A) genes were not equally distributed among strains of the PFGE genogroups (Figure 1). Therefore, differences in the capsule and/or the bacterial wall between genogroups could result in different degrees of susceptibility to transformation or transposition involved in the horizontal transfers of erythromycin resistance genes.31,32 By showing that strains possessing IS1548 in the hylB gene (Table 3) (a marker of a well-defined phylogenetic genogroup)14,16 had acquired only the erm(B) gene, we provide support for this view.

For comparison, we studied the prevalence of genetic markers of highly virulent clones of S. agalactiae strains13–21 in a population of 123 erythromycin-susceptible (Erms) strains of similar origin and serotype than those of the 119 Ermr strains studied here (A.-S. D., N. v. d. M.-M. and R. Q., unpublished data). Thirteen of the 119 Ermr strains (11%) and 33 of the 123 Erms strains (27%) possessed GBSi1 downstream of the scpB gene (P = 0.002). Forty-four of the 119 Ermr strains (37%) and 61 of the 123 Erms strains (50%) possessed at least one prophage DNA fragment (P = 0.05). Nine of the 119 Ermr strains (8%) and 18 of the 123 Erms strains (15%) were in the ST-17 clone (P = 0.05). Most of these genetic markers that were less prevalent in Ermr than in Erms strains are mobile genetic elements that mediate horizontal gene transfer, which has be hypothesized to have a key role in the emergence of pathogens from commensal bacteria.14,33,34


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This study was supported by the Ministère de l'Enseignement Supérieur et de la Recherche and by the Centre Hospitalier Universitaire de Tours.


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None to declare.


   Footnotes
 
{dagger} Present address. The Methodist Hospital Research Institute Center for Molecular and Translational Human Infectious Disease Research, 6565 Fannin Street, SM8-060, Houston, TX 77030, USA. Back


   Acknowledgements
 
We are grateful to J. Loulergue for her technical assistance.


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