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Journal of Clinical Microbiology, August 2000, p. 2985-2988, Vol. 38, No. 8
Laboratoire de Microbiologie Médicale, Hôpital
Broussais,1 and Laboratoire de Recherche
Moléculaire sur les Antibiotiques, UFR Broussais-Hôtel
Dieu et Pitié-Salpétrière,2
Université Paris VI, Paris, France
Received 9 February 2000/Returned for modification 18 March
2000/Accepted 27 May 2000
Epidemiological relationships were investigated between 40 methicillin-resistant Staphylococcus aureus (MRSA) strains
with decreased glycopeptide susceptibility isolated from November 1998 to March 1999 from 39 patients (17 infected and 22 colonized patients) in nine wards of the Broussais Hospital, Paris, France. Reduced glycopeptide susceptibility was readily detected on brain heart infusion (BHI) agar containing 6 µg of teicoplanin per ml and on
gradient plates, but not by the standard disk diffusion method. The
MICs of vancomycin and teicoplanin, determined on BHI agar, were 4 and
8 to 32 µg/ml, respectively (standard antibiotic dilution), and 4 to
8 and 8 to 32 µg/ml, respectively (E-test). All strains were
resistant to macrolides, aminoglycosides, tetracycline, rifampin, sulfonamides, and pefloxacin, showed reduced susceptibility to fusidic
acid and fosfomycin, and were susceptible to trimethoprim and
chloramphenicol. Pulsed-field gel electrophoresis and lysotyping revealed that a multidrug-resistant MRSA clone with decreased susceptibility to glycopeptides has been discretely endemic since at
least 1996 in our institution, where it was responsible for an outbreak
in November and December 1998.
Methicillin-resistant
Staphylococcus aureus (MRSA) is among the most important
pathogens responsible for nosocomial infections. The glycopeptides
vancomycin (VAN) and teicoplanin (TEC) are the drugs of choice for the
treatment of infections due to MRSA. The MICs of these drugs for MRSA
are generally 2 µg/ml or less (14). While reduced
susceptibility to TEC (MICs, 8 to 16 µg/ml) in isolates of S. aureus has been reported since 1990 (2, 8, 9), clinical
isolates of S. aureus with reduced susceptibility to VAN
(MICs, 8 µg/ml) have occasionally been observed since 1996 (6,
11, 12). In these strains, reduced susceptibility to VAN is
frequently associated with reduced susceptibility to TEC, which is then
somewhat easier to detect (6, 11). To our knowledge, the
dissemination of MRSA strains with reduced glycopeptide susceptibility has been documented only rarely, possibly due to the lack of ease of
their detection. However, a high rate of occurrence of such strains was
reported in university hospitals throughout Japan (7) and in
one university hospital in Spain (1). Here, we describe an
outbreak caused by an MRSA strain with reduced glycopeptide susceptibility which has been cryptically endemic in our hospital for
several years and which is also present in other Parisian hospitals.
Patients.
From October 1998 through April 1999, 39 patients
(13 women, 26 men) from nine wards of Broussais Hospital, predominantly from two intensive care units and one cardiology unit, were infected (n = 17) or colonized (n = 22) with
MRSA strains with decreased susceptibility to glycopeptides (see Table
1).
Strains.
All S. aureus strains studied except
reference strain ATCC 25923 and strain 46063 were isolated at Broussais
Hospital. We analyzed a total of 58 strains (see Table 1): 2 were
susceptible to oxacillin and glycopeptides, 10 were
glycopeptide-susceptible MRSA strains isolated during the study period,
and the remaining 46 strains were homogeneously resistant MRSA and
showed decreased susceptibility to glycopeptides. Among the last group
of 46 strains, 40 were isolated during the 6-month study period, 5 were
isolated either in 1996 or 1997, and 1 (strain 46063) was isolated in
1992 at Saint Joseph Hospital, Paris (9).
Antibiotics.
Antibiotic disks were from Sanofi Diagnostics
Pasteur (Marnes-La Coquette, France). Standard reference powders of VAN
and TEC were obtained from Lilly (Saint-Cloud, France) and Marion Merrell Dow (Levallois-Perret, France), respectively.
Antimicrobial susceptibility testing.
Isolates were tested
by the disk diffusion method on Mueller-Hinton (MH) agar
(bioMérieux, Marcy l'Etoile, France) by following the zone size
criteria described by the Antibiogram Committee of the French Society
of Microbiology (5). The antibiotics tested included
penicillin G (PEN), oxacillin (OXA), rifampin (RIF), erythromycin
(ERY), lincomycin (LIN), tetracycline (TET), streptomycin (STR),
kanamycin (KAN), gentamicin (GEN), amikacin (AMK), tobramycin
(TOB), sulfonamides (SUL), trimethoprim (TMP), chloramphenicol
(CHL), fusidic acid (FUA), pefloxacin (PEF), fosfomycin (FOF), VAN, and
TEC. The MICs of VAN and TEC were determined on MH and brain heart
infusion (BHI) agar (Difco, Detroit, Mich.) with a Steers replicator
device with an inoculum of ca. 104 CFU/spot and on BHI agar
by the E-test (AB Biodisk, Dammartin sur Tigeaux, France) with an
inoculum equivalent to 2 standard McFarland units. Each test was
carried out at least three times. In the framework of this study, an
isolate was considered to have decreased susceptibility if the MICs of
VAN and TEC for the isolate were PFGE.
Pulsed-field gel electrophoresis (PFGE) was carried
out with a CHEF DRII apparatus (Bio-Rad Laboratories, Ivry-sur-Seine, France) as described previously (13). SmaI- and
SacII-digested DNA was separated for 24 h at 14°C and
200 V with pulse times of 5 to 35 and 2 to 20 s and at an angle of
120°.
Lysotyping.
The strains were phage typed at the National
Reference Center for Staphylococci, Institut Pasteur, with the
international set of S. aureus phages together with some
experimental phages.
Analysis of the antimicrobial susceptibilities of the MRSA strains
with decreased susceptibility to glycopeptides.
The resistance
markers for the strains studied are listed in Table
1. All 46 strains with decreased
susceptibility to glycopeptides showed a particular multidrug
resistance phenotype: resistance to PEN, OXA, RIF, ERY, LIN, TET, STR,
KAN, GEN, AMK, TOB, SUL, and PEF and decreased susceptibility to FOF
and FUA. The strains remained susceptible only to TMP and CHL. On the
standard antibiogram, they yielded inhibition zones around the VAN and
TEC disks with diameters of
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Outbreak of Methicillin-Resistant Staphylococcus
aureus with Reduced Susceptibility to Glycopeptides in a
Parisian Hospital
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
4 µg/ml (3).
Susceptibility to glycopeptides was also determined with BHI agar
plates with VAN and TEC gradients from 0 to 16 µg/ml and by
population analysis on BHI agar as described previously (7,
12).
RESULTS
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
17 mm; however, two strains (BE06 and
DE18) had diameters of ca. 15 mm around the TEC disks. With respect to
the MICs for the 12 fully susceptible strains including the American Type Culture Collection (ATCC) reference strain (Table 1), the MICs of
VAN for the 46 strains under study were increased twofold on BHI agar,
while the MICs of TEC were increased 4- to 16-fold. When the E-test was
used, similar increases were observed and reduced susceptibilities to
both glycopeptides were obvious when the multidrug-resistant MRSA
strains were grown on gradient plates (data not shown). Ninety-seven
percent of these strains grew on BHI agar containing 6 µg of TEC per
ml.
TABLE 1.
Characteristics of S. aureus strains analyzed
7 to
105, while the susceptible strains were fully inhibited
by 2 µg/ml (Fig. 1A). Further population analysis of the
subpopulations that grew in the presence of VAN at a concentration of 4 µg/ml showed that they remained heterogeneous (data not shown).
Similar results were obtained with TEC, but the frequencies were
somewhat higher (Fig. 1B). These strains might then be called
hetero-VAN-resistant S. aureus (hetero-VRSA), as proposed by
Hiramatsu et al. (7), or hetero-glycopeptide-resistant
S. aureus (hetero-GRSA).
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Epidemiological markers of the MRSA strains with decreased
susceptibility to glycopeptides.
Table 1 summarizes the results of
the analysis of the PFGE banding patterns and the lysotypes of all
strains included in this study. Ninety-three percent of the 40 strains
with reduced glycopeptide susceptibility isolated during the 6-month
study period had identical patterns. The remaining 7% of the strains had banding patterns similar to the predominant pattern, with differences concerning no more than four bands and indicating a close
relationship between the strains (13). Five strains isolated
at Broussais Hospital in 1996 and 1997, and one strain, 46063, isolated
in 1992 at Saint Joseph Hospital (9) yielded the predominant
banding pattern (Fig. 2). By contrast,
differences in at least seven bands were consistently observed for the
fully glycopeptide-susceptible MRSA strains (Fig. 2). As for the phage types, all typeable strains with reduced susceptibility to
glycopeptides except strain 46063 had identical lysotypes and were
susceptible only to phage 54, a lysotype uncommon in fully
glycopeptide-susceptible strains in France (N. El Solh, personal
communication).
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DISCUSSION |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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In our institution, a 400-bed university hospital, about 1,000 S. aureus strains are isolated annually. In 1998, 40% of the isolates were MRSA, and about one-half of these were susceptible to GEN. The observation, at an unusual frequency, of MRSA strains with a particular phenotype (resistance to GEN, RIF, ERY, LIN, TET, PEF, and SUL, reduced susceptibility to FUA, and susceptibility to TMP and CHL) in November 1998 led us to analyze these strains more closely. Forty-five MRSA strains with the particular multiple-antibiotic resistance phenotype were collected retrospectively and prospectively from October 1998 until the end of March 1999.
The glycopeptide susceptibilities of these multidrug-resistant strains were not adequately assessed by the standard antibiogram procedure, since only in some rare instances was there a marginally reduced diameter of the inhibition zone around TEC. Considering the only slightly reduced susceptibilities observed after MIC determinations by standard methods, these strains do not fall into the category of intermediate glycopeptide susceptibility according to the criteria of the National Committee for Clinical Laboratory Standards (10) and the Antibiogram Committee of the French Society of Microbiology (5). They were, however, not fully glycopeptide susceptible as were the MRSA strains with different multiple-antibiotic resistance profiles isolated in our institution during the same period. When the standard dilution procedure was carried out on BHI medium instead of MH medium, as proposed previously (7), reduced susceptibility to TEC became noticeable (Table 1). This was also the case when gradient plates or the E-test was used with BHI medium (Table 1).
Reduced glycopeptide susceptibility was not a homogeneously expressed trait. The subpopulation that grew in the presence of more than 4 µg of VAN or TEC per ml among the strains with reduced glycopeptide susceptibility (Fig. 1) was reminiscent of the previously reported subpopulation strains termed hetero-VRSA (7, 12). It would therefore be reasonable to consider the presence of such strains a possible risk factor for VAN or TEC treatment failures in patients with MRSA infections since this reduction in susceptibility might be the first step in the development of higher-level resistance.
Molecular typing and lysotyping revealed a high degree of relatedness among the strains with reduced glycopeptide susceptibility. This, in conjunction with the fact that the lysotype of these isolates was rare and the fact that the multidrug resistance phenotype was homogeneous, suggested that these strains were clonal. The identification of strains of this type among hospital strains dating back to 1996, the increase in their frequency over a 2-month period, and the persistence of scattered isolates to the present day, despite drastic measures related to hospital hygiene, are consistent with a limited outbreak of a discretely endemic strain. This persistence probably dates back to at least 1992, when MRSA strain 46063 (which has the clonal PFGE pattern; Fig. 2) was isolated in a hospital immediately adjacent to Broussais Hospital (9). When the PFGE patterns of the MRSA isolates with reduced glycopeptide susceptibility from our institution were compared with that of strain Mu50, which is related to the hetero-VRSA strains from Japan (7), it was obvious that they were not members of the same clone (Fig. 2). The same observation was made (Fig. 2) with respect to hetero-VRSA strains from Spain (1).
Four of the 40 consecutive strains isolated during the 6-month study period were isolated from patients upon admission. This indicated that the clonal isolates are not confined to our institution. In fact, MRSA isolates with indistinguishable characteristics have since been identified in at least three major hospitals in Paris (data not shown). We do not know the frequencies at which MRSA with reduced glycopeptide susceptibility occur in those institutions and whether they have constituted up to 25% of all staphylococci isolated during any given period, as was the case during the last 2 months of 1998 in Broussais Hospital.
Prospectively, all MRSA isolates should be systematically examined for reduced glycopeptide susceptibility because it may not remain confined to the multiple antibiotic-resistant clones identified so far. Clonal diversity of hetero-VRSA strains isolated in different French hospitals was recently demonstrated unambiguously (4). In the absence of broadly recognized recommendations, we now routinely screen all S. aureus strains on BHI agar containing 6 µg of TEC per ml. If reduced glycopeptide susceptibility is suspected, it is verified by the E-test with VAN and TEC. However, all S. aureus strains isolated from patients with severe infections are immediately subjected to the E-test.
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ACKNOWLEDGMENTS |
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This work was supported by the Institut National de la Santé et de la Recherche Médicale, Paris (CRI 9504).
We thank A. Morvan for lysotyping and N. El Solh and O. Chesneau for interpretation of the phage typing data and helpful discussions, K. Hiramatsu and J. Linares for the gifts of strains (Mu50 and MRSA1152, respectively), and I. Casin, V. Jarlier, and E. Varon for providing clinical isolates.
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FOOTNOTES |
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* Corresponding author. Mailing address: L.R.M.A., Université Paris VI, 15 rue de l'Ecole de Médecine, 75270 Paris Cedex 06, France. Phone: 33-1-01.42.34.68.65. Fax: 33-1-01.43.25.68.12. E-mail: ipodgla{at}ccr.jussieu.fr.
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REFERENCES |
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References
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Journal of Clinical Microbiology, August 2000, p. 2985-2988, Vol. 38, No. 8
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