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Journal of Clinical Microbiology, February 2001, p. 591-595, Vol. 39, No. 2
Department of Medicine1 and
Department of Microbiology,2
Faculty of Medicine, Siriraj Hospital, Mahidol University,
Bangkok, and Department of Medicine, Khon Kaen Hospital, Khon Kaen,
Thailand3 and Department of
Bacteriology, Faculty of Medicine, Juntendo University,
Tokyo,4 Japan
Received 10 July 2000/Returned for modification 2 October
2000/Accepted 27 November 2000
To investigate whether there are methicillin-resistant
Staphylococcus aureus (MRSA) strains with reduced
susceptibility to vancomycin in Thailand, a total of 155 MRSA strains
isolated from patients hospitalized between 1988 and 1999 in university
hospitals in Thailand were tested for glycopeptide susceptibility. All
the strains were classified as susceptible to vancomycin and
teicoplanin when judged by NCCLS criteria for glycopeptide
susceptibility using the agar dilution MIC determination. Vancomycin
MICs at which 50 and 90% of the isolates tested were inhibited
(MIC50 and MIC90, respectively) were 0.5 and 1 µg/ml, respectively, with a range of 0.25 to 2 µg/ml. For
teicoplanin, MIC50 and MIC90 were 2 µg/ml,
with a range of 0.5 to 4 µg/ml. However, one-point population analysis identified three MRSA strains, MR135, MR187, and MR209, which
contained subpopulations of cells that could grow in 4 µg of
vancomycin per ml. The proportions of the subpopulations were 2 × 10 Vancomycin is a useful antibiotic
against gram-positive pathogens. However, with an increased use of the
antibiotic, resistance has been noticed in various species of bacteria
such as enterococci (18, 19), Staphylococcus
haemolyticus (27), and Staphylococcus epidermidis (9). In 1996, the first
Staphylococcus aureus strain with reduced susceptibility to
vancomycin, designated VRSA for vancomycin-resistant S. aureus (13) or GISA for glycopeptide-intermediate S. aureus (26), was isolated from a Japanese
patient who contracted vancomycin-refractory surgical incision site
infection (4). Subsequently, a total of five similar
strains were reported from the United States (5, 6),
France (23), and Korea (16). The vancomycin
MIC for these strains is 8 µg/ml. Vancomycin therapy was unsuccessful
with all of these infected patients. The emergence and spread of such
resistant strains are expected to raise the morbidity and mortality
rates of nosocomial infection significantly. Fortunately, so far only a
few isolates have been reported in the world. However, the putative
precursor strains for vancomycin resistance, designated hetero-VRSA
(13) or hetero-VISA for heterogeneously vancomycin-intermediate S. aureus (7), are
reported to be disseminated not only in Japan but also in various other
countries in the world (2, 10, 11, 13-15, 17, 24, 29; Z. Gulay, T. Atay, M. Kucukguven, and N. Yulug, Abstr. 38th Intersci.
Conf. Antimicrob. Agents Chemother., abstr. C-136, 1998).
Heterogeneously resistant (heteroresistant) strains spontaneously
generate mutants with reduced susceptibilities to vancomycin at a
frequency of 1 in 1 million or more (13). In this study,
the status of the glycopeptide susceptibility of Thai
methicillin-resistant S. aureus (MRSA) strains was analyzed
as the initiation step of an annual surveillance program for the
emergence of glycopeptide resistance in Thai S. aureus
clinical isolates.
Three hetero-VRSA strains (MR135, MR187, and MR209) were isolated
from the following clinical patients. The first two patients were
hospitalized in the same urban hospital in Bangkok but in different
wards at different periods of time. The third patient was admitted to
the medical ward of a regional hospital of Thailand. These two
hospitals were separated from each other by about 600 km.
Case 1 (strain MR135).
The case 1 patient was a 68-year-old
woman who was a resident of Bangkok. She had diabetes and developed a
long-term surgical-site MRSA infection at her knee after her second
total knee replacement operation in March 1998. The patient was
continuously treated with vancomycin from 14 May to 27 July (75 days)
and with teicoplanin for 7 days from 29 July to 4 August 1998. However,
MRSA was repeatedly isolated from synovial fluid in her knee seven
times during the time period from 6 May to 31 July. MR135 was isolated
from the synovial fluid taken on the third day of teicoplanin therapy
(31 July 1998). The patient became febrile and developed a purulent discharge from the surgical site at her knee. The patient expired on 7 August 1998.
Case 2 (strain MR187).
The case 2 patient was a 16-year-old
woman who resided in Bangkok. From 13 May to 9 September in 1996, the
patient had chronic retroperitoneal infection with MRSA. Multiple MRSA
strains were isolated from various body sites before vancomycin
treatment was given: they were isolated from her sputum on 2 June with
Pseudomonas aeruginosa, from a blood specimen on 5 June, and
from an exploration biopsy sample from her abdomen on 14 June. The
patient subsequently received long-term treatment with vancomycin (for
49 days, from 21 June to 9 August). However, MRSA was repeatedly
isolated from the drainage of her intra-abdominal abscess during the
course of vancomycin therapy. MR187 was isolated on 4 July (14 days
after the initiation of vancomycin therapy). Vancomycin treatment was discontinued, and laparoscope-assisted surgical excisions of the intra-abdominal abscess with removal of necrotic tissue and drainage of
pus were performed several times in August. The drainage fluid from her
abdomen became sterile on 6 September, and the recovered patient was
discharged from the hospital.
Case 3 (strain MR209).
MR209 was isolated on 17 June 1999 from
the sputum of a 61-year-old man in Khon Kaen, in the northern part of
Thailand, who developed nosocomial pneumonia with
Acinetobacter sp., Klebsiella pneumoniae, and
MRSA. The patient had diabetes melitus, liver cirrhosis, hepatic
encephalopathy, and cerebral infarction as underlying diseases. He was
treated with cefotaxime for 5 days from 17 to 21 June but was not
treated with any glycopeptide antibiotic. His condition deteriorated,
and he died at home shortly after he was discharged from the hospital.
Bacterial strains and antibiotics.
S. aureus
strains for which the oxacillin MIC was 4 µg/ml or above were defined
as MRSA according to the National Committee for Clinical Laboratory
Standards (NCCLS) (20). A total of 155 MRSA strains
isolated from the patients hospitalized between 1988 and 1999, including the three strains MR135, MR187, and MR209, were analyzed: 148 strains, including MR135 and MR187, were from the urban university
hospital, and 7 strains, including MR209, were from the regional
hospital. They were isolated from the respiratory tract (85 strains),
pus or exudative fluids (62 strains), blood (6 strains), and urine (2 strains).
0095-1137/01/$04.00+0 DOI: 10.1128/JCM.39.2.591-595.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
First Report of Methicillin-Resistant
Staphylococcus aureus with Reduced Susceptibility to
Vancomycin in Thailand
ABSTRACT
Top
Abstract
Introduction
Case Report
Materials and Methods
Results
Discussion
References
4, 1.5 × 106, and 4 × 107, respectively. The subsequent performance of a
complete population analysis and testing for the emergence of mutants
with reduced susceptibility to vancomycin (MIC 
8 µg/ml)
confirmed that these strains were heterogeneously resistant to
vancomycin. Two of these strains caused infection that was refractory
to vancomycin therapy. Pulsed-field gel electrophoresis showed that the
two strains had identical SmaI macrorestriction patterns
and that they were one of the common types of MRSA isolated in the
hospital. This is the first report of heterogeneous resistance to
vancomycin in Thailand and an early warning for the possible emergence
of vancomycin resistance in S. aureus in Southeast Asia.
INTRODUCTION
Top
Abstract
Introduction
Case Report
Materials and Methods
Results
Discussion
References
CASE REPORT
Top
Abstract
Introduction
Case Report
Materials and Methods
Results
Discussion
References
MATERIALS AND METHODS
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Abstract
Introduction
Case Report
Materials and Methods
Results
Discussion
References
Screening of MRSA with reduced susceptibility to
glycopeptides.
The screening was performed by one-point population
analysis (13), as follows. Overnight culture in brain
heart infusion (BHI) broth was adjusted to an optical density at 578 nm
of 0.3 (about 108 CFU/ml) and then diluted 10-fold (about
107 CFU/ml). One hundred microliters of the cell suspension
was spread onto a BHI agar plate containing 4 µg of vancomycin per
ml. The plate was incubated at 37°C for 48 h, and cell growth
was inspected at 24 and 48 h. The strain was judged to be
susceptible to vancomycin if the cell growth was not apparent within
48 h. The strain was judged to be a possible VRSA if confluent
cell growth was seen within 24 h and a possible heteroresistant
strain if a countable number of colonies was apparent within 48 h.
Confirmation of vancomycin resistance of the strain was based on the
vancomycin MIC being equal to or greater than 8 µg/ml, and that of
heteroresistance was based on a lower MIC (
4 µg/ml), a population
curve with a heterogeneous pattern, and a positive result in a
resistant mutant emergence test (13).
Analysis of resistant subpopulations of bacteria (population analysis). Population analysis was performed by spreading 100 µl of the starting cell suspension (made by adjusting an overnight culture in BHI broth to an optical density at 578 nm of 0.3 [about 108 CFU/ml] with fresh BHI broth) and 10-fold dilutions of this suspension onto BHI agar plates containing various concentrations of vancomycin (13, 21). After incubation at 37°C for 48 h, the number of colonies grown on each plate was counted. The number of resistant cells contained in 100 µl of the starting cell suspension was calculated and plotted on a semilogarithmic graph. Population analysis was performed with both vancomycin and teicoplanin.
Genotyping. Genotypes of hetero-VRSA and related MRSA strains were analyzed by PFGE (28). PFGE was performed for 22 h using a contour-clamped homogeneous electric field apparatus DRII (Bio-Rad) with a pulse time of 5 to 40 s. SmaI macrorestriction patterns of the three heteroresistant strains (MR135, MR187, and MR209) and nine related vancomycin-susceptible MRSA strains were compared. PFGE patterns were compared by visual examination and interpreted as follows. Isolates with no difference in banding patterns of chromosomal fragments were defined as indistinguishable, those with three or fewer fragment differences were defined as closely related, and those with four or greater fragment differences were defined as different (25).
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RESULTS |
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Top
Abstract
Introduction
Case Report
Materials and Methods
Results
Discussion
References
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Glycopeptide susceptibility of Thai strains.
Based on the
NCCLS criteria and routine clinical laboratory testing, all the
isolates were judged to be susceptible to vancomycin (MIC 4 µg/ml) and teicoplanin (MIC 8 µg/ml). Vancomycin MICs at
which 50 and 90% of the isolates were inhibited (MIC50 and MIC90, respectively) were 0.5 and 1 µg/ml, respectively,
with a range of 0.25 to 2 µg/ml. The teicoplanin MIC50
and MIC90 were both 2 µg/ml, with a range of 0.5 to 4 µg/ml.
Analysis of glycopeptide-resistant subpopulations of the three MRSA
strains.
With an inoculum size of 107 CFU, one strain,
MR135, exhibited confluent growth of cells on BHI agar containing 4 µg of vancomycin per ml within 24 h. Two other strains, MR187
and MR209, showed positive growth on the screening agar plate within
48 h, with formation of 15 and 4 colonies, respectively. All three
strains had glycopeptide MICs in the susceptible range: a vancomycin
MIC of 1 µg/ml for all the strains and teicoplanin MICs of 2 µg/ml for MR135, 1 µg/ml for MR187, and 4 µg/ml for MR209, respectively. Figure 1 illustrates the population
analysis curves of MR135, MR187, and MR209 in comparison with those of
Mu3, Mu50, MR126 (one of the glycopeptide-susceptible Thai strains),
and S. aureus type strain FDA209A: Figure 1A shows
population curves for resistance to vancomycin. The sizes of the
subpopulations of the three Thai strains that were resistant to 2 to 5 µg of vancomycin per ml were smaller than those of Mu50 and were
comparable to those of Mu3. Strain MR135 had greater resistant
subpopulations than Mu3 to 2 to 5 µg of vancomycin per ml (Fig. 1A).
MR187 and MR209 were more susceptible to vancomycin than Mu3, but both
isolates also contained resistant subpopulations of cells that could
grow in the presence of 4 and 5 µg of vancomycin per ml. All three
Thai strains had smaller sizes of subpopulations resistant to 6 to 9 µg of vancomycin ml than those of Mu3.
|
7 to
104 fractions of the populations grew in the Thai strains.
Genotypes of the three heteroresistant strains.
PFGE banding
patterns of MR135, MR187, and MR209 are shown in Fig.
2 in comparison with those of
vancomycin-susceptible S. aureus strains and Mu3. The Thai
heteroresistant strains (lanes 2 to 4) and the related
vancomycin-susceptible MRSA strains isolated from the same ward and
during overlapping time periods (lanes 5 to 13) had very similar PFGE
banding patterns. The Thai heteroresistant strains, however, had at
least seven band differences from Mu3, a Japanese isolate (lane 14).
Strains MR135 (lane 2) and MR187 (lane 3) were isolated from different
units of the urban hospital in different years (MR135 from a surgery
unit in 1998 and MR187 from an intensive care unit in 1996), but they
had identical SmaI macrorestriction patterns. The
vancomycin-susceptible MRSA strains (lanes 5 to 13) had either
identical (lanes 8 to 12) or very similar PFGE banding patterns
compared with those of MR135 (lane 2) and MR187 (lane 3). The other
heteroresistant strain, MR209 (lane 4), isolated from the regional
hospital, had a different PFGE banding pattern than those of the other
two strains, but it was noticed that it had a pattern similar to that
of one of the vancomycin-susceptible MRSA strains in the urban hospital
(lane 6).
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DISCUSSION |
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Abstract
Introduction
Case Report
Materials and Methods
Results
Discussion
References
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This is the first report of infection due to MRSA strains with reduced susceptibility to vancomycin in Thailand. Although the three isolates were heterogeneously resistant to vancomycin, this report is an early warning that S. aureus strains with full resistance to vancomycin might emerge in the future, emphasizing the importance of a laboratory capability of identifying heterogeneous vancomycin resistance. The disk diffusion method is inadequate to detect S. aureus strains with reduced susceptibilities to vancomycin (26). Although well-standardized microdilution MIC determination can detect S. aureus clinical isolates with reduced susceptibilities to vancomycin, it cannot detect heteroresistance. Based on the MICs, all three isolates reported in this study are judged to be susceptible to glycopeptide antibiotics (20). Strains MR135 and MR187, however, were isolated from patients whose MRSA infection did not respond favorably to long-term vancomycin treatment. Other researchers also reported that vancomycin treatment failure was associated with infection caused by MRSA heteroresistant to vancomycin (1, 13, 15, 17, 23, 29). Efforts to detect heteroresistant strains, therefore, may be warranted not only to monitor the progression of glycopeptide resistance acquisition by local MRSA strains, but also to predict the clinical effectiveness of glycopeptide treatment of the patients infected with MRSA.
MRSA strains with reduced susceptibilities to vancomycin in Japan and in the United States were isolated after prolonged exposure to the antibiotic (4, 12, 24), as were two Thai strains. MR135 was isolated from a patient treated with vancomycin for 75 days and with teicoplanin for 3 days, and MR187 was isolated after 14 days of vancomycin therapy. Strain MR209 was an exception. The strain was isolated from a patient who had not been treated with any glycopeptide antibiotic. In this case, the strain might have been transmitted to the patient from another patient who had undergone glycopeptide treatment of MRSA infection. This possibility may explain why the strain had the lowest vancomycin resistance of the three strains, since the vancomycin resistance phenotype is unstable in the absence of antibiotic pressure (3). MR209 was marginal with regard to heteroresistance if heteroresistance is defined as having resistant subpopulations whose number is greater than one in 106 (13).
The genotypes of three heteroresistant strains were quite distinct from that of the Japanese strain Mu3 (Fig. 2), but they were indistinguishable from the genotypes other Thai MRSA strains retaining vancomycin susceptibility. Therefore, as recently demonstrated in in vitro experiments (22), it is likely that vancomycin resistance is acquired by MRSA strains with diverse genetic backgrounds besides that of the Japanese MRSA clonotype II-A (13). In this regard, however, it was noted that Thai strains had a different pattern of resistance from that of Mu3. In contrast to Mu3, the Thai strains did not contain larger resistant subpopulations capable of growth in 6 to 9 µg of vancomycin per ml (Fig. 1A). They were also less resistant to teicoplanin than Mu3 or Mu50 (Fig. 1B). These phenotypic differences in the resistance patterns indicate that the mechanism of glycopeptide resistance in Thai strains is different from that in Japanese MRSA strains (8). Research is under way to clarify the genetic mechanism behind Thai strains expressing reduced susceptibilities to glycopeptide antibiotics.
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ACKNOWLEDGMENTS |
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This work was a part of the Nosocomial Infections and Drug-Resistant Microorganisms project, which was supported by the Core University System Exchange Programme under the Japan Society for the Promotion of Science, coordinated by the University of Tokyo Graduate School of Medicine and Mahidol University. The work was also supported by an unrestricted grant from Wyeth Lederle Japan Ltd.
We thank Rachada Sathitmathakul and Siriporn Sripalakit, Centre for Nosocomial Infection Control, Faculty of Medicine, Siriraj Hospital, Mahidol University.
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FOOTNOTES |
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* Corresponding author. Mailing address: Department of Bacteriology, Juntendo University, 2-1-1 Hongo, Bukyo-Ku, Tokyo, Japan 113-8421. Phone: 81-3-5802-1040. Fax: 81-3-5684-7830. E-mail: hiram{at}med.juntendo.ac.jp.
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References
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Journal of Clinical Microbiology, February 2001, p. 591-595, Vol. 39, No. 2
0095-1137/01/$04.00+0 DOI: 10.1128/JCM.39.2.591-595.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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Kluytmans, J., Van Griethuysen, A., Willemse, P., Van Keulen, P.
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