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Journal of Clinical Microbiology, December 1999, p. 3912-3916, Vol. 37, No. 12
Division of Quality Health Care, Department
of Internal Medicine, Medical College of Virginia Campus of
Virginia Commonwealth University, Richmond, Virginia
Received 14 April 1999/Returned for modification 2 July
1999/Accepted 1 September 1999
To investigate the dissemination of vancomycin-resistant
Enterococcus faecium (VREF) in a 728-bed tertiary-care
hospital, all clinical VREF isolates recovered from June 1992 to June
1997 were typed by pulsed-field gel electrophoresis, and the transfer histories of the patients were documented. A total of 413 VREF isolates
from urine (52%), wounds (16%), blood (11%), catheter tips (6%),
and other sites (15%) were studied. VREF specimens mostly came from
patients on wards (66%) but 34% came from patients in an intensive
care unit. The number of VREF isolates progressively increased over
time, with higher rates of isolation during the winter months and lower
rates in the late summer months. Four distinct banding patterns were
detected by pulsed-field gel electrophoresis among 316 samples (76%).
Strain A (122 samples; 30%) appeared in June 1992 as the first VREF
strain and was found until December 1994 throughout the entire
hospital. Type B (92 samples; 22%) was initially detected in January
1994 and disappeared in November 1996. Strain C (10 samples; 2%) was
limited to late 1996 and early 1997. Strain D (92 samples; 22%) showed
two major peaks during March 1996 to August 1996 and January 1997 to
February 1997. Unrelated strains (97 samples; 24%) appeared 1 year
after the appearance of the first VREF isolate, and the numbers
increased slightly over the years. Nosocomial acquisition (i.e., no
known detection prior to admission and first isolation from cultures
performed with samples retrieved Enterococci are the second leading
cause of nosocomial urinary tract infections and the third leading
cause of nosocomial wound and bloodstream infections (19).
Resistance to environmental conditions such as heat or desiccation
allow prolonged survival, and poor compliance with hand-washing
procedures by health care workers results in the rapid spread of
enterococci in hospitals (26, 42, 45, 66). Moreover, strains
of enterococci have acquired resistance to essentially all
antimicrobial agents over the past three decades (16, 65).
The prevalence of vancomycin resistance in enterococci has dramatically
increased in the last few years. In 1989, less than 0.4% of
enterococci were resistant to vancomycin in general wards and intensive
care units (ICUs). Eight years later, 15% of enterococcal isolates in
wards and 23% in ICUs were resistant to vancomycin (36).
Therefore, the increasing rate of spread of vancomycin-resistant
enterococci (VRE) within hospitals in the United States and the
especially high rates in ICUs indicate that VRE are some of the most
important pathogens today and illustrate the need for effective
infection control measures (28, 52).
The present study was initiated to investigate the relatedness of
clinical VRE isolates collected in a 728-bed tertiary-care hospital
from June 1992 to June 1997 by molecular biotyping methods and the
hospital transfer histories of the patients.
(This study was presented at the 8th Annual Meeting of the Society for
Healthcare Epidemiology of America, April 1998, Orlando, Fla. [abstr.
S 44, p. 48].)
Setting.
The study was performed at the Medical College of
Virginia Hospitals, a 728-bed tertiary-care, teaching facility located
in the city of Richmond, Va. The hospital houses nine specialized ICUs
with a total of 104 beds.
Study design.
The present study comprised a retrospective
analysis of all new clinical, vancomycin-resistant Enterococcus
faecium (VREF) isolates collected between June 1992 and June 1997.
Sample preparation.
Bacterial isolates were stored at
Genotype analysis.
Pulsed-field gel electrophoresis (PFGE)
(CHEF DR III; Bio-Rad Laboratories, Richmond, Calif.) was performed in
a 1% agarose gel for all isolates after digestion of total DNA with
SmaI (GIBCO BRL, Grand Island, N.Y.), as described
previously (37). The electrophoresis lasted 22 h, with
the pulse time ramped from 1 to 35 s. The restriction profiles in
ethidium bromide-stained gels were visually analyzed by one observer
and were photographed. The images of the gels were also digitized for
further investigation. For evaluation of epidemic isolates, the
restriction patterns were compared according to previously published
guidelines (62): isolates were considered indistinguishable
if there was no band difference or closely related if they differed by
two to three banding patterns, which indicated changes consistent with
a single genetic event. Two independent genetic events indicated that
isolates were possibly related to the outbreak strain. An isolate was
defined as unrelated to an outbreak strain when its PFGE pattern
differed from those of the outbreak strains by three or more
independent genetic events.
Genotype determination.
The isolation of bacterial DNA and
the amplification of a 377-bp fragment of the vanA gene by
PCR were performed as described previously (31). For
amplification of a vanB gene fragment (289 bp), the same PCR
solutions used for vanA were used, but the cycles were
modified (cycle 1 was 94°C for 6 min, 56°C for 1 min, and 72°C
for 1 min and cycles 2 to 31 were 94°C for 1 min, 56°C for 1 min,
and 72°C for 1 min; cycle 32 was 72°C for 2 min) and the following
primers were used: vanB-I (5'-CAT CGC CGT CCC CGA ATT TCA AA-3') and
vanB-II (5'-GAT GCG GAA GAT ACC GTG GCT-3'). The PCR products were
detected in a 1.4% agarose gel (type II) (Medium EEO; Sigma Chemicals,
St. Louis, Mo.).
Infection control measures.
In March 1994 an "antibiotic
resistant precautions" infection control policy was introduced. This
policy required the use of gloves and gowns upon entering the room of a
patient colonized or infected with VRE. The gown requirement was
modified in September 1994 to the use of gowns only if close contact or
potential contamination of clothing was anticipated. No interventions
were introduced to influence health care worker compliance with
infection control policies.
Definition of community-acquired and nosocomial infections.
For each patient, admission and discharge dates from each hospital unit
were documented. To estimate the annual rate of occurrence of VREF
isolates in our hospital, the total number of new clinical isolates was
divided by the total number of patient admissions. The definition of
nosocomial acquisition was no known colonization or infection prior to
admission and first isolation of VREF from cultures performed with
samples retrieved at least 2 days after hospitalization or previous
hospitalizations within the prior 2 months and cultures positive for
VREF within 48 h after the current admission. Patients who were
infected or colonized with VREF and who did not fulfill these criteria
were defined as having community-acquired cases of infection.
Patients and materials.
A total of 413 patients colonized or
infected with VREF were studied. From 1992 to 1997 the rate of
isolation of VREF increased from 1.1 per 1,000 to 3.3 per 1,000 patient
admissions. Clinical isolates were obtained mostly from urine (52%),
followed by wounds (16%), blood (11%), catheter tips (6%), and other
sites (15%).
PFGE results.
PFGE of 413 isolates revealed four distinct
banding patterns (patterns A, B, C, and D) for 316 (77%) specimens
(Fig. 1; Table 1). Ninety-seven (24%) isolates were not
related to these strain types or to each other. Strains with the
predominant pattern, pattern A, were found in 122 (30%) samples,
strains with pattern B were found in 92 (22%) samples, strains with
pattern C were found in 10 (2%) samples, and strains with pattern D
were found in 92 (22%), respectively.
0095-1137/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Molecular Epidemiology of Vancomycin-Resistant
Enterococcus faecium in a Large Urban Hospital over a
5-Year Period
ABSTRACT
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
2 days after hospitalization) was
found for 316 (91%) of 347 patients. Despite the implementation of
Centers for Disease Control and Prevention guidelines, the proportion of related strains and high number of nosocomial cases of infection indicate a high transmission rate inside the hospital. The results imply an urgent need for stringent enforcement of more effective infection control measures.
INTRODUCTION
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
MATERIALS AND METHODS
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
70°C in medium containing 15% glycerol. For the present study, 411 VREF isolates were thawed, and the species identification was confirmed
with the RAPID ID 32STREP system (bioMérieux sa, Marcy l'Etoile,
France). Susceptibility to ampicillin, gentamicin (Ratiopharm GmbH&Co,
Ulm, Germany), streptomycin (Merck AG, Darmstadt, Germany), vancomycin,
teicoplanin, and the experimental antibiotic LY 333328 (Eli Lilly & Co,
Indianapolis, Ind.) was determined by the broth microdilution method.
RESULTS
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
View larger version (114K):
[in a new window]
FIG. 1.
PFGE of SmaI-digested genomic DNA from 12 vanA-containing E. faecium strains. Lanes: B, H,
and N, bacteriophage lambda ladder molecular mass standard; A, C, E, G,
J, K, and M, outbreak isolates of pattern D; D, F, L, and O, outbreak
isolates of pattern C; I, unrelated isolate.
TABLE 1.
Frequency of VREF strains, van genotypes,
ampicillin and aminoglycoside susceptibilities, and detection periods
Resistance patterns of strains.
All isolates expressed
high-level vancomycin resistance (MICs, 128 µg/ml; Table 1). Of the
strains with the four patterns, only strains with pattern B were
susceptible to teicoplanin (MICs, <1 µg/ml). Pattern B strains
contained the vanB resistance gene, whereas the strains with
the other three patterns contained vanA genes. No
vanC strain was detected. High-level resistance to the aminoglycosides gentamicin (MICs, >1,024 µg/ml) and streptomycin (MICs, >2,048 µg/ml) was demonstrated in strains with patterns B, C,
and D. Pattern A strains were resistant only to gentamicin (MICs,
>1,024 µg/ml). Ampicillin resistance was noted in the isolates. The
MIC of ampicillin was 16 µg/ml (MICs, 16 µg/ml [pattern A strains], 64 µg/ml [pattern B strains], and 128 µg/ml [pattern C and D strains]). Strains of all four patterns were susceptible to
the investigational antibiotic LY 333328 (MICs, <0.125 µg/ml).
Dissemination of strains inside the hospital. A pattern A strain appeared in June 1992 and was the first VREF isolate recovered from a patient on a ward. It was found throughout the hospital until December 1994 (Fig. 2). Eighty-six clinical isolates were obtained from patients on wards, whereas 36 isolates were obtained from patients in ICUs. Between February 1994 and April 1994 an increased rate of recovery of VREF isolates (up to eight isolates per month) was found in ICUs.
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Nosocomial cases of infection. Sixty-nine percent of all VREF isolates (284 specimens) were from patients on wards, whereas 31% (129 specimens) were from patients in ICUs. Ninety-one percent (316 specimens) met the definition for nosocomial acquisition, including 251 of 266 (94%) related strains and 65 of 81 (80%) isolates of unrelated strain types. No data were available for 66 specimens (50 infected with related strains and 16 infected with unrelated strains).
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DISCUSSION |
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Materials and Methods
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Infection or colonization with VRE results in a wide spectrum of possible deleterious effects for patients in health care settings. Studies have demonstrated that VRE can cause serious infections, and the attributable mortality of bacteremia caused by VRE has been estimated to be nearly 40% (18, 43). Control of VRE may result in a reduced quality of life for patients, since isolation measures limit social exchange. In addition to possible increased length of hospitalization, VRE carrier status makes the integration of these patients more difficult, especially in rehabilitation or long-term health care settings (14, 27, 32, 69). Overall, problems related to therapy and isolation for patients colonized or infected with VRE lead to increased health care costs (61).
First detected in Europe in 1986 (33), VRE have emerged as important pathogens in the United States. Regarding the origin of VRE, European studies demonstrated that the carriage of VRE in the community was probably caused by the use of antibiotics as growth promoters in animals (1, 13). In the United States, however, Coque et al. (11) and Silverman et al. (57) could not isolate any VRE from community volunteers or consecutively admitted patients. These findings are reinforced by the wide variety of PFGE patterns in European studies compared to the that in the United States (3, 5). Van den Braak et al. (67) hypothesized that dissemination of resistance genes might be more important than strain transfer, explaining the clonal discrepancy of strains of VRE between animals and humans in Europe. Only recently, VRE have been isolated from animal feed in a small study in the United States (56). In our study, the number of outbreak strains was limited to four. Other investigators have observed similar results (9, 11, 15, 25, 40). Only Bonten et al. (7) found polyclonality of isolates of VRE in a U.S. ICU. Therefore, the origin of VRE in the United States is still unclear, but their distribution appears to be concentrated in health care settings.
VRE are usually transmitted by contact. Noskin et al. (44) found that VRE could survive for at least 1 h on gloved and ungloved fingertips and for 5 to 7 days on environmental surfaces. Other investigators have shown that VRE can exist in stool specimens of a carrier for up to 2 years, providing a source for environmental spread (34, 35, 39, 47, 54). These characteristics can result in the wide dissemination of VRE, as demonstrated in our study. Beginning with an index strain in June 1992, one VREF strain (pattern A) circulated throughout the entire hospital for a 2-year period. Unrelated strains appeared 12 months after the appearance of the first VREF strain, indicating that there was no additional outside source for VREF at the beginning of the observation period. Rapid dissemination of VRE has also been found by other investigators (9, 11, 25, 46). Investigations of different health care facilities in the same region by Moreno et al. (40) and Fridkin et al. (22) revealed that the spread of VRE strains is not limited to one hospital.
The majority of published studies of VRE have focused on ICUs. However, our investigation revealed that 66% of all VREF were found in ward areas. The VREF situation in our hospital evolved from a locally limited outbreak to a situation of endemicity affecting all units in a short time period. Therefore, hospitalwide approaches are vital to control the dissemination of VRE even at an early stage.
An interesting aspect of the dissemination of VRE in our study is the sudden disappearance of one outbreak strain followed by the appearance of another strain. Reasons for the strain shift remain unknown. Isolation and contact precaution measures cannot be considered, since another prominent strain emerged by a similar transmission route. Therefore, further studies should focus on the microbial mechanisms favoring one VRE strain over another as a cause of hospitalwide outbreaks (22).
In the last decade several approaches to preventing and limiting the spread of VRE were developed and integrated into national guidelines for hospitals (23, 29). These recommendations are based on the origin of VRE, the mechanism of transmission in the hospital environment, and the risk factors for acquisition.
Preventive measures taken to avoid selection of VRE include the restricted use of antibiotics, especially vancomycin (2, 8, 10, 12, 21, 24, 25, 30, 35, 40, 46, 48-51, 55, 58, 60, 63, 68). The Hospital Infection Control Practices Advisory Committee (HICPAC) of the Centers for Disease Control and Prevention published guidelines for the appropriate use of vancomycin in 1995 (29). These recommendations were partially implemented in our hospital. Evans and Kortas (21) reported that only 35% of 101 orders for vancomycin were consistent with the HICPAC guidelines in a university hospital. Administration of vancomycin or other antibiotics, such as cephalosporins, metronidazole, or clindamycin, can also increase the rate of skin colonization with VRE, enhancing possible transmission from patient to patient (2). Restriction of antibiotic use to an acceptable level may reduce the selection for VRE, but studies are still needed to prove the benefit of this measure.
Standard precautions should be followed for the handling of patients in the daily routine. Even if the patient is not known to be infected or colonized with a pathogen, these guidelines require the use of gloves for contact with blood, body fluids, secretions, excretions, and potentially contaminated items and hand washing after glove removal. However, measurement of compliance with hand washing by health care workers in our own facility has revealed unacceptably low hand-washing rates (4). The importance of this simple method is further strengthened by the large number of unrecognized, silent carriers of VRE (2, 6, 8, 12, 17, 25, 30, 35, 38, 40, 41, 46, 49, 53, 59, 63, 64, 66). If VRE are detected, isolation precautions should be implemented as described in Centers for Disease Control and Prevention and HICPAC guidelines (23, 29). In March 1994 "antibiotic resistant precautions" were introduced in our facility. These precautions require the use of gloves and gowns upon entering a patient's room. These interventions did not appear to have a significant impact on the spread of VREF. In summary, even if precautions are practical and useful, compliance by health care providers is a major factor for their success.
Because we collected only clinical isolates, we do not know how widespread colonization with VREF was and whether there were differences in rates of colonization with various strains. Furthermore, the outcome of infections caused by VREF depends highly on the severity of the underlying diseases. Therefore, the results of this study should be interpreted as a reflection of the potential risk for patients who acquire VREF and not as a predictive value of fatality.
In conclusion, the rapidly developing situation of endemicity in our hospital demonstrated the ability of VRE to spread, despite implementation of universal and specialized infection control measures. Control of VRE requires a multifaceted approach since existing measures seem to be inadequate and/or are not appropriately followed by health care providers.
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ACKNOWLEDGMENTS |
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We are grateful to I. Klare, Robert Koch-Institute, Wernigerode, Germany, for determination of the van genotypes of the strain isolates.
W. E. Bischoff was supported by a grant from the Walter-Marget-Society, Freiburg, Germany.
The experimental antibiotic LY 333328 was provided by Eli Lilly & Co, Indianapolis, Ind.
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FOOTNOTES |
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* Corresponding author. Mailing address: Department of Internal Medicine, Medical College of Virginia Campus of Virginia Commonwealth University, P.O. Box 980509, Richmond, VA 23219. Phone: (804) 828-9726. Fax: (804) 828-4926. E-mail: medmond{at}hsc.vcu.edu.
Present address: Institute for Medical Microbiology, Medical School
Hanover, Hanover, Germany.
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Journal of Clinical Microbiology, December 1999, p. 3912-3916, Vol. 37, No. 12
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Copyright © 1999, American Society for Microbiology. All rights reserved.
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