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Journal of Clinical Microbiology, September 2001, p. 3147-3155, Vol. 39, No. 9
0095-1137/01/$04.00+0 DOI: 10.1128/JCM.39.9.3147-3155.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Group G Beta-Hemolytic Streptococcal Bacteremia Characterized
by 16S Ribosomal RNA Gene Sequencing
Patrick C. Y.
Woo,1
Ami M. Y.
Fung,1
Susanna K. P.
Lau,1
Samson S. Y.
Wong,1 and
Kwok-Yung
Yuen1,2,*
Department of Microbiology, The University of
Hong Kong, Queen Mary Hospital,1 and
HKU-Pasteur Research Centre,2 Hong Kong
Received 10 May 2001/Returned for modification 1 July 2001/Accepted 5 July 2001
 |
ABSTRACT |
Little is known about the relative importance of the four species
of Lancefield group G beta-hemolytic streptococci in causing bacteremia
and the factors that determine the outcome for patients with group G
beta-hemolytic streptococcal bacteremia. From 1997 to 2000, 75 group G
beta-hemolytic streptococcal strains were isolated from the blood
cultures of 66 patients. Sequencing of the 16S rRNA genes of the group
G beta-hemolytic streptococci showed that all 75 isolates were
Streptococcus dysgalactiae subspecies equisimilis. The API system (20 STREP) and Vitek system
(GPI) successfully identified 65 (98.5%) and 62 (93.9%) isolates,
respectively, as S. dysgalactiae subspecies
equisimilis with >95% confidence, whereas the ATB
Expression system (ID32 STREP) only successfully identified 49 isolates
(74.2%) as S. dysgalactiae subspecies
equisimilis with >95% confidence. The median age of
the patients was 76 years (range, 33 to 99 years). Fifty-six patients
(85%) were over 60 years old. All patients had underlying diseases. No
source of the bacteremia was identified (primary bacteremia) in 34 patients (52%), whereas 17 (26%) had cellulitis and 8 (12%) had bed
sore or wound infections. Fifty-eight patients (88%) had
community-acquired group G streptococcal bacteremia. Sixty-two patients
(94%) had group G Streptococcus recovered in one blood
culture, whereas 4 patients (6%) had it recovered in multiple blood
cultures. Fifty-nine patients (89%) had group G
Streptococcus as the only bacterium recovered in their
blood cultures, whereas in 7 patients other bacteria were recovered
concomitantly with the group G Streptococcus in the
blood cultures (Staphylococcus aureus in 3, Clostridium perfringens in 2, Citrobacter
freundii in 1, and Bacteroides fragilis in 1).
Overall, 10 patients (15%) died. Male sex, diagnosis other than
cellulitis, hospital-acquired bacteremia, and multiple positive blood
cultures were associated with mortality {P < 0.005 (relative risk [RR] = 7.6), P < 0.05 (RR = 3.7), P < 0.005 (RR = 5.6), and P < 0.05 (RR = 5.6), respectively}. Unlike
group C beta-hemolytic streptococcal bacteremia, group G beta-hemolytic
streptococcal bacteremia is not a zoonotic infection in Hong Kong.
| |
INTRODUCTION |
Lancefield groups A, B, C, and G
streptococci are the major groups of beta-hemolytic streptococci that
cause bacteremia. The major reservoir for group A and B streptococci is
humans, whereas most group C beta-hemolytic streptococcal bacteremias
in Hong Kong are of animal origin (28). The group G
beta-hemolytic streptococci consist of Streptococcus
dysgalactiae subspecies equisimilis, S. milleri, S. canis, and S. intestinalis.
The reservoirs of S. dysgalactiae subspecies
equisimilis and S. milleri are humans, whereas those of S. canis and S. intestinalis are
dogs and pigs, respectively. In one study, group G streptococci were
shown to be the most common cause of beta-hemolytic streptococcal
bacteremia (16). It has been reported that diabetes
mellitus (DM), malignancy, cardiovascular disease, bone and joint
diseases, and cirrhosis are the major underlying diseases in patients
with group G beta-hemolytic streptococcal bacteremia (2, 8, 10,
16, 19). However, little is known about the relative importance
of the various species and thus the source of bacteria causing
bacteremia, the usefulness of commercial kits in identifying the
species, and the factors that determine the outcome for patients with
group G beta-hemolytic streptococcal bacteremia.
Although the Vitek system (bioMerieux Vitek, Hazelwood,
Mo.), the API system (bioMerieux Vitek), and the ATB Expression system (bioMerieux Vitek) are commonly used for microbial identification of
beta-hemolytic streptococci in the clinical laboratory, none of these
systems contains all four group G beta-hemolytic streptococci in the
database. Since the discovery of PCR and DNA sequencing, comparisons of
the gene sequences of bacterial species have shown that the 16S rRNA
gene is highly conserved within a species and among species of the same
genus and thus can be used as the new "gold standard" for
species-level identification of bacteria. Using this new standard,
phylogenetic trees based on base differences between species are
constructed, and bacteria are classified and reclassified into new
genera (13, 14). Recently, we have reported the
application of 16S rRNA gene sequencing in the identification of
clinical isolates with ambiguous biochemical profiles (20, 21,
24, 25) and of a bacterium that was noncultivable
(7). In this study, we used 16S rRNA gene sequencing for
the species-level identification of 75 group G beta-hemolytic
streptococcal strains isolated from the blood cultures of 66 patients
in a 4-year period. The usefulness of the Vitek system (GPI), the
API system (20 STREP), and the ATB Expression system (ID32 STREP)
in identifying the isolates was compared with this gold standard. The
epidemiology, clinical diseases, and outcome for patients that
developed group G beta-hemolytic streptococcal bacteremia were also analyzed.
| |
MATERIALS AND METHODS |
Patients and microbiological methods.
The 66 patients in
this study were hospitalized at the Queen Mary Hospital in Hong Kong
during a 4-year period (1997 to 2000). All clinical data were collected
prospectively as described in our previous publications (11,
27). Clinical specimens were collected and handled according to
standard protocols. The BACTEC 9240 blood culture system (Becton
Dickinson, Sparks, Md.) was used. All suspect colonies were identified
by standard conventional biochemical methods (12).
Lancefield serogrouping was performed using Streptex (Murex Biotech
Ltd., Dartford, United Kingdom) according to the manufacturer's
instructions. In addition, the Vitek system (GPI; bioMerieux Vitek),
API system (20 STREP; bioMerieux Vitek), and ATB Expression system
(ID32 STREP; bioMerieux Vitek) were used for the identification of the
group G beta-hemolytic streptococci in this study. Multiple isolates
obtained from the same patient were counted only once in the
calculation of the usefulness of each kit for identifying group G
Streptococcus. Antimicrobial susceptibility was tested by
the Kirby-Bauer disk diffusion method and results were interpreted
according to the NCCLS criteria (3).
Extraction of bacterial DNA for 16S rRNA gene sequencing.
The bacterial DNA extraction method was modified from our
previous published protocol (23). Briefly, 80 µl
of NaOH (0.05 M) was added to 20 µl of bacterial cells suspended in
distilled water and the mixture was incubated at 60°C for 45 min,
followed by addition of 6 µl of Tris-HCl (pH 7.0) to achieve a final
pH of 8.0. The resultant mixture was diluted 100-fold, and 5 µl of the diluted extract was used for PCR.
PCR, gel electrophoresis, and 16S rRNA gene sequencing.
PCR
amplification and DNA sequencing of the 16S rRNA genes were performed
according to our previous publications (7, 20, 21, 22, 24,
25). Briefly, DNase I-treated distilled water and PCR master mix
(which contains deoxynucleoside triphosphates, PCR buffer, and
Taq polymerase) were used in all PCRs by adding 1 U of DNase
I (Pharmacia, Uppsala, Sweden) to 40 µl of distilled water or PCR
master mix and incubating the mixture at 25°C for 15 min and
subsequently at 95°C for 10 min to inactivate the DNase I. The
bacterial DNA extracts and controls were amplified with 0.5 µM
concentrations of the primers (LPW200,
5'-GAGTTGCGAACGGGTGAG-3', and LPW205,
5'-CTTGTTACGACTTCACCC-3') (Gibco BRL, Rockville, Md.). The
PCR mixture (50 µl) contained bacterial DNA, PCR buffer (10 mM
Tris-HCl [pH 8.3], 50 mM KCl, 2 mM MgCl2, and
0.01% gelatin), 200 µM concentrations of each deoxynucleoside
triphosphate, and 1.0 U of Taq polymerase (Boehringer,
Mannheim, Germany). The mixtures were amplified in 40 cycles of 94°C
for 1 min, 55°C for 1 min, and 72°C for 2 min, and a final
extension at 72°C for 10 min in an automated thermal cycler
(Perkin-Elmer Cetus, Gouda, The Netherlands). DNase I-treated distilled
water was used as the negative control. A 10-µl aliquot of each
amplified product was electrophoresed in a 1.0% (wt/vol) agarose gel,
with a molecular size marker (lambda DNA AvaII digest;
Boehringer) run in parallel. Electrophoresis in Tris-borate-EDTA buffer
was performed at 100 V for 1.5 h. The gel was stained with
ethidium bromide (0.5 µg/ml) for 15 min, rinsed, and photographed
under UV light illumination.
The PCR products were gel purified using the QIAquick PCR purification
kit (Qiagen, Hilden, Germany). Both strands of the PCR products were
sequenced twice with an ABI 377 automated sequencer according to the
manufacturer's instructions (Perkin-Elmer, Foster City, Calif.), using
the PCR primers LPW200 and LPW205 and additional primers designed from
the sequencing data of the first round of sequencing (LPW99,
5'-TTATTGGGCGTAAAGCGA-3', and LPW273,
5'-TTGCGGGACTTAACCCAAC-3'). The sequences of the PCR
products were compared with known 16S rRNA gene sequences in GenBank by
multiple sequence alignment using the CLUSTAL W program
(17).
Statistical analysis.
A comparison of characteristics was
made between patients who succumbed to and those who survived the group
G beta-hemolytic streptococcal bacteremia. A chi-square test was used
for categorical variables and Student's t test was used for
age analysis. Multivariate logistic analysis was not performed because
of the small sample size. A P value of <0.05 was regarded
as statistically significant.
| |
RESULTS |
16S rRNA gene sequencing.
PCR of the 16S rRNA genes of the
blood culture group G beta-hemolytic streptococci showed bands at 1,414 bp. Sequencing of the 16S rRNA genes showed that all the isolates
obtained from the same patient had the same nucleotide sequence. There
were one to four base differences between the isolates and S. dysgalactiae subspecies equisimilis (GenBank accession
number AB008926), 79 to 82 base differences between the isolates and
S. anginosus (GenBank accession number X58309), 52 to 55 base differences between the isolates and S. canis (GenBank
accession number AB002483), and 73 to 76 base differences between the
isolates and S. intestinalis (GenBank accession number
AB002519), indicating that all 75 isolates were S. dysgalactiae subspecies equisimilis (Fig.
1).
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FIG. 1.
DNA sequences of the 16S rRNA genes of the group G
beta-hemolytic Streptococcus isolate from the blood
culture of patient 1 and those of S. dysgalactiae
subspecies equisimilis (GenBank accession number
AB008926), S. anginosus (GenBank accession number
X58309), S. canis (GenBank accession number AB002483),
and S. intestinalis (GenBank accession number AB002519).
The shaded bases represent those in the various
Streptococcus species that are different from the
corresponding ones in the isolate.
|
|
Lancefield serogrouping and identification by commercial
systems.
All group G beta-hemolytic streptococci (isolated from
blood cultures and other clinical specimens) showed agglutination only with the serogroup G antiserum and not with any other antisera. All
isolates obtained from the same patient showed the same biochemical profile and hence were counted as one isolate in the calculations. The
API system (20 STREP) successfully identified 65 (98.5%) isolates as
S. dysgalactiae subspecies equisimilis with
>95% confidence. The remaining 1 (1.5%) isolate was identified
as S. dysgalactiae subspecies equisimilis with
77% confidence. The Vitek system (GPI) successfully identified 62 (93.9%) isolates as S. dysgalactiae with >95% confidence,
1 (1.5%) isolate as S. agalactiae with 81% confidence, and
3 (4.5%) isolates were "unidentified." The ATB Expression system
(ID32 STREP) only successfully identified 49 (74.2%) isolates as
S. dysgalactiae subspecies equisimilis with >95% confidence, 3 (4.5%) isolates as S. dysgalactiae
subspecies equisimilis with 83% confidence, 3 (4.5%)
isolates as S. dysgalactiae subspecies
equisimilis with 65% confidence, 1 (1.5%) isolate as Streptococcus group L with 87% confidence, and 1 (1.5%)
isolate as S. agalactiae with >95% confidence (not the
isolate that was identified by the Vitek system as S. agalactiae), and 9 (13.6%) isolates were "unidentified."
Patient characteristics.
The characteristics of the 66 patients with group G streptococcal bacteremia are tabulated and
summarized in Tables 1 and 2, respectively. The incidence of group G streptococcal
bacteremia was similar throughout the 4-year study period. There were
slightly more cases in the late spring and summer months (April to
August). The median age was 76 years (range, 33 to 99 years). Fifty-six patients (85%) were over 60 years old. The male/female ratio was 38:28. All patients had underlying diseases. The major underlying conditions included immobilization and/or bed sore in 19 (29%), cerebrovascular accident (CVA) in 18 (27%), malignancy in 17 (26%), hypertension (HT) in 16 (24%), DM in 13 (20%), dementia in 10 (15%),
lymphedema in 10 (15%), chronic renal failure (CRF) in 10 (15%),
cirrhosis in 5 (8%), and intravenous drug abuse (IVDA) in 5 (8%). No
source of the bacteremia was identified (primary bacteremia) in 34 patients (52%), whereas 17 (26%) had cellulitis, 8 (12%) had a bed
sore or wound infection, 2 (3%) had infective endocarditis, 2 (3%) had pneumonia, 2 (3%) had an abscess, and 1 (2%) had
septic arthritis. Fifty-eight (88%) and 8 (12%) had community- and
hospital-acquired group G streptococcal bacteremia, respectively.
Sixty-two patients (94%) had group G Streptococcus recovered in 1 blood culture, whereas 4 patients (6%) had it recovered in multiple blood cultures. Fifty-nine patients (89%) had group G
Streptococcus as the only bacteria recovered in their blood cultures, whereas in 7 patients other bacteria were recovered concomitantly with the group G Streptococcus in the blood
cultures (Staphylococcus aureus in patients 10, 48, and 54;
Clostridium perfringens in patients 28 and 56;
Citrobacter freundii in patient 21; and Bacteroides
fragilis in patient 47). Seven patients with wound infections and
two patients with cellulitis had group G Streptococcus
recovered from the wound swabs (patients 4, 12, 16, 26, 29, 39, 47, and
56) or aspirate (patient 53). One patient (patient 63) with a pelvic
abscess had group G Streptococcus recovered from the abscess
pus. The isolates recovered from 63 patients (95.5%) were sensitive to
penicillin, cephalothin, erythromycin, clindamycin, and vancomycin. Two
isolates (3.0%) were resistant to both erythromycin and clindamycin
(patients 38 and 41), and one isolate was resistant to erythromycin but
sensitive to clindamycin (patient 39). Overall, 10 patients (15%)
died.
The characteristics of patients who succumbed to and those who survived
the group G beta-hemolytic streptococcal bacteremia
were compared and
are summarized in Table
3. Male sex,
diagnosis
other than cellulitis, hospital-acquired bacteremia, and
multiple
positive blood cultures were associated with mortality
{
P < 0.005
(relative risk [RR] = 7.6),
P < 0.05 (RR = 3.7),
P < 0.005 (RR
= 5.6), and
P < 0.05 (RR = 5.6),
respectively}.
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TABLE 3.
Comparison of characteristics of patients who died of and
those who survived the group G beta-hemolytic streptococcal
bacteremiaa
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| |
DISCUSSION |
In this study, we documented that all 75 group G beta-hemolytic
streptococci were S. dysgalactiae subspecies
equisimilis by using the molecular gold standard of
bacterial species-level identification, 16S rRNA gene sequencing. With
this gold standard, the relative usefulness of the Vitek system (GPI),
the API system (20 STREP), and the ATB Expression system (ID32 STREP)
in identifying this species could be compared. The API system (20 STREP) and Vitek system (GPI) were good in identifying S. dysgalactiae subspecies equisimilis, as they were able
to confidently identify 99% and 94% of the isolates, respectively. On
the other hand, the ATB Expression system (ID32 STREP) could only
identify 74% of the isolates correctly, despite this system's
containing the largest number of biochemical reactions [32 as opposed
to 25 in the API system (20 STREP) and 30 in the Vitek system (GPI)].
The epidemiology of group G beta-hemolytic streptococcal bacteremia in
Hong Kong was found to be similar to that reported in previous studies
(2, 8, 10, 16, 19). Most patients were old, with a
predominance of males. In our series, all patients had underlying
diseases, similar to the 74 to 92% rate reported in previous studies
(10, 16). The spectrum of underlying conditions was also
similar, with immobilization, CVA, HT, and malignancy being the most
important conditions (10, 16). Similar to previous studies
(i.e., rates of 70 to 75%), most cases of group G beta-hemolytic streptococcal bacteremia were community acquired (88%) (2, 16,
19). The reservoir for S. dysgalactiae subspecies
equisimilis is humans, and most infections are probably
endogenous. Unlike group C beta-hemolytic streptococcal bacteremia
(28), group G beta-hemolytic streptococcal bacteremia is
not a zoonotic infection in Hong Kong. Among the 30 patients with
documented foci of infection, the skin was the major portal of entry,
as cellulitis and bed sore or wound infections made up the majority of
the diagnoses. No clinical diagnosis was achieved for 34 patients
(52%), which was comparable to the 50% rate reported in a previous
study (16).
Cellulitis was the most common diagnosis in those patients who had
group G beta-hemolytic streptococcal bacteremia with known sources of
infection. In our recent series and in previous reports on cellulitis
complicating lymphedema, non-group A beta-hemolytic streptococci
(mostly group B and group G streptococci) constituted most of the
documented causes of cellulitis (26). Most of the patients
had lymphedema because of malignancy with surgery and/or radiotherapy.
In the present study, among the 17 patients with group G beta-hemolytic
streptococcal bacteremic cellulitis, about half had it as a
complication of lymphedema and malignancy, of which carcinoma of the
breast was the most common.
The overall mortality rate (15%) in our patients with group G
beta-hemolytic streptococcal bacteremia was similar to those reported
in previous studies (8 to 17%) (2, 6). In the previous reports, no analysis was made on the risk factors associated with mortality in patients with group G beta-hemolytic streptococcal bacteremia. In this study, we found by univariate analysis that male
gender, diagnosis other than cellulitis, hospital-acquired infection,
and multiple positive blood cultures were poor prognostic factors for
group G beta-hemolytic streptococcal bacteremia. Since there were only
10 patients who died, multivariate analyses for the identification of
independent prognostic factors was not performed.
Two S. dysgalactiae subspecies equisimilis
isolates were resistant to both erythromycin and clindamycin.
Macrolide, lincosamide, and type B streptogramin antibiotics inhibit
bacterial growth by binding to the 50S ribosomal subunits of the
bacteria and inhibiting protein synthesis. Resistance to these
antibiotics is usually due to target modification through the
acquisition of erm (erythromycin resistance methylase)
genes. These genes encode enzymes that N-6 dimethylate a specific
adenine residue of the 23S rRNA of the bacteria, leading to
cross-resistance to macrolides, lincosamides, and streptogramin B
(MLSB resistance phenotype) (1, 4, 5, 6, 9,
15, 18). We speculate that the cross-resistance to erythromycin
and clindamycin in the two S. dysgalactiae subspecies equisimilis isolates was due to an erm gene.
Further cloning and characterization of such a gene will delineate
whether it belongs to an existing class or a previously undescribed class.
| |
ACKNOWLEDGMENT |
This work was partly supported by the Committee of Research and
Conference Grants, The University of Hong Kong.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Department of
Microbiology, The University of Hong Kong, University Pathology
Building, Queen Mary Hospital, Hong Kong. Phone: (852) 28554892. Fax:
(852) 28551241. E-mail: hkumicro{at}hkucc.hku.hk.
| |
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Journal of Clinical Microbiology, September 2001, p. 3147-3155, Vol. 39, No. 9
0095-1137/01/$04.00+0 DOI: 10.1128/JCM.39.9.3147-3155.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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Abstract
Introduction
