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Adverse Events Associated With Methicillin-Resistant Staphylococcus aureus in a Nursing Home
Paul Drinka, MD;
J. Todd Faulks, RPh;
Cathy Gauerke, MT;
Brian Goodman, PhD;
Mary Stemper, MT;
Kurt Reed, MD
Arch Intern Med. 2001;161:2371-2377.
ABSTRACT
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Background Methicillin-resistant Staphylococcus aureus
(MRSA) generates concern in nursing homes. Restrictive isolation precautions
may be applied for indefinite periods. Adverse events driving these concerns
include transmission and infection.
Methods The 721-bed Wisconsin Veterans Home in King performs approximately 645
cultures annually. The site, severity, and number of MRSA infections were
determined for 69 months. Pulsed-field gel electrophoresis was performed on
all initial isolates, followed by a statistical cluster analysis looking for
evidence of transmission.
Results Sixty-seven MRSA infections were identified (1.6 per 100 residents per
year); many were polymicrobial, and it was difficult to determine the proportionate
role of MRSA in morbidity or mortality. There was an episode of rapidly fatal
MRSA septicemia in which empiric antibiotic therapy was ineffective. Twenty-one
genetic strains were encountered. Statistical analysis identified 13 clusters
of genetically identical strains clustered in time and space (P<.05).
Conclusions Infections with MRSA were identified at relatively low rates; however,
the etiology of many serious nursing home infections is not determined, especially
pneumonia. Statistical analysis revealed clustering and evidence of transmission.
Nursing home practitioners should consider MRSA when applying empiric treatment
to serious infections. We recommend a program including (1) judicious use
of antibiotics, including topical agents, to reduce selection of resistant
organisms; (2) obtaining and tracking cultures of infectious secretions to
diagnose MRSA infections and focus antibiotic therapy; (3) universal standard
secretion precautions because any resident could be a carrier; and (4) a detailed
assessment and care plan for the carrier that maximizes containment of secretions
and independence in activities. However, basic hygiene cannot be maintained
in communal areas by some residents without restriction of activities of daily
living.
INTRODUCTION
METHICILLIN-resistant Staphylococcus aureus
(MRSA) has generated concern and confusion among nursing home practitioners.
The potential adverse events driving these concerns include transmission and
infection, as well as regulatory deficiencies and malpractice litigation.
Methicillin-resistant S aureus might cause outbreaks
or infections rendered lethal by misguided empiric antibiotic therapy.1-3 Previously, some nursing
homes refused to admit patients with MRSA because the elaborate and restrictive
isolation precautions used by hospitals were considered necessary for indefinite
periods. The indefinite application of restrictive isolation precautions is
labor intensive and might be a personal hardship for the resident. In a longitudinal
study, Terpenning et al4 found that gram-negative
rods resistant to gentamicin and/or ceftriaxone therapy were less prevalent
colonizers than MRSA but posed a greater infection risk to residents. These
organisms, however, do not engender the same level of concern. More information
is needed to assist nursing home staff in the management of MRSA.
The 4-building, 721-bed Wisconsin Veterans Home in King has an on-site
laboratory that performs approximately 645 routine clinical cultures annually
and has performed pulsed-field gel electrophoresis (PFGE) on all isolates
of MRSA since August 1994. In this article, we present a statistical analysis
of the distribution of each isolate type, looking for clustering and evidence
of transmission, as well as a description of MRSA infections. This retrospective
analysis was undertaken to refocus or possibly redirect our infection control
program.
PATIENTS AND METHODS
The Wisconsin Veterans Home, administered by the state of Wisconsin,
is a skilled nursing facility that serves veterans and their spouses. During
this study, the average daily census was 721. Seventy-nine percent of the
residents were men (mean age, 74 ± 10 years); there was an average
of 240 hospitalizations per year and average annual mortality of 18%. Ninety
percent of hospitalizations were in community hospitals and only 10% were
in Veterans Affairs medical centers. Care is provided in 4 separate buildings
on 14 floors or nursing units. One unit is a physically separated "wandering
unit." The census on nursing units varies between 50 and 60. The home has
an on-site bacteriology laboratory that is open 45 hours per week. Most cultures
are performed during those hours. The laboratory enforces strict policies
for specimen collection and will not plate a wound or sputum culture unless
collected within the previous hour. Urine culture samples are refrigerated
immediately. During this study, a mean of 645 cultures were obtained each
year for clinical purposes. Beginning in August 1994, any initial isolate
from a resident infected or colonized with MRSA underwent PFGE at Marshfield
Laboratories, Marshfield, Wis (M.S. and K.R.). Chromosomal DNA was prepared
using the method described by Maslow et al.5
Restriction endonuclease digestion of the DNA was done using SmaI (Promega Corp, Madison, Wis). Electrophoresis was performed in
a 1% gel at 200 V for 20 hours in a CHEF-DRIII system (Bio-Rad Laboratories,
Hercules, Calif). Pulse time was increased from an initial time of 5 seconds
to a final time of 40 seconds. The PFGE profiles were analyzed using Multi-Analyst
Fingerprinting Plus software (Bio-Rad). Interpretation of the patterns was
based on guidelines established by Tenover et al.6
During this study, the Wisconsin Veterans Home had policies and procedures
that required modified "contact precautions" for residents colonized or infected
with MRSA, with the addition of "droplet precautions" in the presence of an
active respiratory tract infection with splatter into the environment.7 Precautions also included use of dedicated equipment
and hand hygiene with chlorhexidine gluconate. The care plan for MRSA carriers
was individualized to take into account mobility, hygiene, ability to contain
potentially infectious secretions, and any infection tracking reports suggesting
that the individual might be transmitting MRSA. The Centers for Disease Control
and Prevention guidelines for contact and droplet precautions were modified
for each individual based on this assessment, with resident quality of life
given strong consideration. When a resident was newly discovered to be infected
with MRSA, small numbers of focused surveillance culture specimens were sometimes
obtained to determine whether that individual might be part of a cluster of
transmission. These culture specimens could include wounds, Foley catheters,
tracheostomies, and gastrostomies of those on the same nursing unit, as well
as cultures of respiratory secretions (chronic cough or rhinorrhea), hand
dermatitis, or the anterior nares of roommates or close social contacts (tight
circle). If this system suggested that transmission was occurring, infection
control procedures were upgraded.
CLINICAL STUDY
In July 2000, we used our bacteriology database to generate a listing
of all individuals with MRSA isolates and all subsequent cultures on those
individuals. We reviewed the medical charts of affected residents until June
30, 2000, to determine the proportion of patients with MRSA who had infections
and to characterize the site and severity of infections (vancomycin use, hospitalization,
or death).
STATISTICAL ANALYSIS
We identified 71 individuals with MRSA isolates in 69 months (August
1, 1994, to June 30, 2000). There were 21 PFGE strains. Tenover et al6 proposed that a 3-band difference or less between
epidemiologically related strains probably indicates a common source, whereas
a 4- to 6-band difference possibly indicates a common source. Three-band differences
typically result from a single genetic event. This criterion is recommended
for outbreaks of 1 to 3 months.6 More genetic
variability between related bacteria is anticipated during longer durations.
Combining the 21 PFGE types for this analysis was not attempted because of
the existence of more than 200 comparisons between strains. We hypothesized
that if transmission was not occurring within our facility, each of the 10
PFGE strains with more than 1 isolate should be distributed randomly in time
among 14 nursing units. A model that captures only clustering of organisms
with no band differences is robust and, if anything, will underestimate the
degree of transmission within the facility. We performed a cluster analysis
that included 3 characteristics: PFGE type, unit location, and date of first
isolate from all initial MRSA events. We used a single linkage method and
a euclidean distance measure to determine how the distance between 2 clusters
would be defined. The final partition was determined by specifying a similarity
level of 95%. The level of similarity (S) between 2 clusters (ij) was given
by the equation Sij = 100(1 - dij)/dmax,
where dij is a distance measure calculated between all observations
in cluster i against all observations in cluster j and dmaxis the
maximum distance measure computed in the original distance matrix. Methicillin-resistant S aureus events that share a greater than 95% similarity
among their 3 common characteristics were identified as a single cluster.8
RESULTS
CLINICAL STUDY
The clinical study comprised 71 individuals, including 4 staff members,
with nasal isolates; 95% were sensitive to trimethoprim-sulfamethoxazole and
95% to tetracycline hydrochloride. Only 6 isolates were sensitive to ciprofloxacin
hydrochloride and erythromycin base. All these isolates were from the same
building and varied by 3 or 4 bands on PFGE (patients 42, 43, 47, 56, 57,
and 59) (Table 1). Among the 67
initial isolates in residents, 50 were from infected secretions. There were
10 cases in which MRSA was isolated from asymptomatic residents when surveillance
was performed around an index case (5 nasal, 4 wound, and 1 sputum). In addition,
there were 7 cases in which MRSA was isolated after abnormal findings on screening
urinalysis. Some individuals had more than 1 episode of infection. During
the 69 months of study, 67 clinical infections were identified in which MRSA
was isolated, including 14 symptomatic urinary tract infections associated
with catheterization (9 polymicrobial and 5 single isolates), 6 symptomatic
urinary tract infections without Foley catheterization (1 polymicrobial and
5 single isolates), and 3 cases of MRSA sepsis. In addition, there were 14
respiratory tract infections (8 polymicrobial and 6 single isolates). There
were 19 isolates from infected peripheral vascular wounds (13 polymicrobial
and 6 single isolates) and 11 from infected nonvascular wounds (8 polymicrobial
and 3 single isolates).
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Initial MRSA Isolates on Each Nursing Unit, August 1, 1994, Through
June 30, 2000*
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The 67 infections in which MRSA was isolated led to 21 courses of vancomycin
therapy and were associated with 19 hospitalizations, including 5 amputations.
Methicillin-resistant S aureus was also associated
with 3 deaths from pneumonia in which MRSA had been isolated, 1 from septicemia,
and 1 from transitional bladder carcinoma with polymicrobial urinary tract
infection. Two of 3 bacteremias occurred among the 4 A10 isolates. The third
bacteremic isolate, an A2 strain, varied by 4 bands from A10. There were 2
deaths related to peripheral vascular disease in which MRSA had been isolated
in mixed culture. It was difficult to determine how much of the burden of
hospitalization and mortality associated with MRSA isolation was specifically
related to MRSA rather than severe underlying disease or polymicrobial flora.
There were also 4 deaths from pneumonia or lung cancer in residents unable
to produce sputum with current MRSA colonization at other sites.
Fourteen isolates were discovered during screening in a tight circle
around an index case (10 residents and 4 staff) (see the "Patients and Methods"
section). In 9 isolates the secondary cases were genetically identical, in
1 there was 3 bands of difference, and in 4 they were unrelated (>7 bands
of difference) (patients 13, 38, 58, and 69). Patient 38 developed a wound
infection, with MRSA isolated 20 months after the initial nasal isolate. In
2 situations, nasal cultures of roommates yielded MRSA: one was of an identical
PFGE profile (patient 37) and the second was unrelated (patient 69).
CLUSTER ANALYSIS
Pulsed-field gel electrophoresis was performed on all 71 MRSA isolates
initially isolated between August 1, 1994, and June 30, 2000. Two of the 14
nursing units had no isolates, including the physically isolated "Alzheimer"
unit. Twenty-seven of the PFGE profiles were of an identical type noted as
"A" (Table 1). Patients are numbered
in the temporal order of isolation in the facility. Twenty-three additional
isolates had PFGE patterns that differed by no more than 6 bands from the
main A profile, designated A1 through A12. There were 10 additional PFGE strains
that included 20 cases. Table 1
lists each isolate, including the genetic characterization, sites of isolation,
timing, and room number. Table 1
groups strains of identical PFGE on each nursing unit.
The cluster analysis identified 13 statistically significant clusters
of identical PFGE initial isolates that included 53% of the 71 initial isolates.
The clusters involved 2 to 10 individuals clustered in time (1-9 months) and
space. Most (n = 10) involved a single nursing unit and 3 involved 2 or 3
units in a single building. Hospitalizations within 1 year of the initial
isolate were examined for each cluster. No pattern emerged except that both
individuals in cluster 12 had been admitted to the hospital that accepts 80%
of our admissions within 3 months of the first isolate.
There were additional examples of clustering within nursing units including
cases that varied by 3 or fewer bands from prevailing strains. Patient 59
had profile K isolated on December 24, 1999, which varied by 3 bands from
the endemic A10 strain. Finally, only 2 of 14 units had any A1, A2, and L
isolates. A1 differs from A2 by 2 bands and from L by 3 bands. These 3 genetically
related strains were clustered on 2 nursing units. In other cases, unusual
PFGE types were encountered on separate nursing units clustered in time. For
example, during the 69 months of study, only 4 individuals with profile F
were identified. Three were identified from 3 separate buildings between December
22, 1997, and March 19, 1998 (patients 38, 39, and 41). We did not identify
an epidemiologic link, although the clustering of this unusual PFGE type in
time suggests a common source.
The total number of individuals who had MRSA isolated during a given
year (initial or repeated) remained stable at 13 to 15 from 1995 through 1999.
The rate of MRSA infection also remained stable at approximately 1 per month.
Throughout the study, we viewed the 50- to 60-bed nursing unit as the most
likely site of transmission and therefore primarily looked for transmission
within nursing units. There were 7 clusters in which genetically identical
MRSA infections were noted on the same unit within 30 days.
COMMENT
The data demonstrate that apparent endemic MRSA isolates, indistinguishable
by PFGE, were clustered in defined areas over discrete periods. The plausible
mechanism for the clusters is transmission within a common living space with
shared caregivers. Our findings blur the distinction between "outbreak" strain
(which includes incidence higher than the baseline and linkage in time and
space with a plausible common source) and "endemic" strain.6
Endemic strains can also be statistically linked in time and space with a
plausible common source. It is no surprise that MRSA can be slowly transmitted
within a nursing home and slowly discovered by culturing infected secretions.
Our large study includes 4146 resident-years of surveillance. Smaller facilities
that seldom perform cultures and track MRSA isolates over a short period could
be experiencing similar infection rates without drawing attention (ie, 1.6
infections per year in a 100-bed facility). A number of Veterans Affairs and
community investigators studied MRSA colonization and performed time-sequenced
surveillance cultures in nursing homes. Transmission of MRSA might be inferred
by the acquisition of colonization within the nursing home. The rate of acquisition
partially depends on background colonization rates ("colonization pressure").1 Bradley et al9 reported
that 10% of 341 individuals acquired new colonization (multiple sites sampled)
in a study with mean follow-up of 3.6 months and background colonization rates
of 23%. New colonization has also been reported1-2,10-12
at rates of 2% to 9% per year. Without subtyping, the relationship of new
cases to specific preexisting cases is tenuous. In general, MRSA does not
seem to be highly contagious, but acquisition does occur within the nursing
home.
Many individuals carry S aureus in their nose
for long periods and never develop infections. Infection might subsequently
develop after an aspiration event, a break in the skin, or a bladder obstruction.
An MRSA surveillance system that completely depends on cultures of infected
secretions would be expected to allow considerable transmission to occur before
detection. Infection control experts who advise nursing homes might have no
idea how few routine cultures are performed in nursing homes compared with
hospitals. Because of the slow and uncertain relationship between transmission
and infection, we often performed surveillance cultures in a tight circle
around index cases, followed by PFGE, and determined that transmission was
occurring. Not all MRSA isolates from the tight circle were genetically related.
Surveillance cultures might be especially helpful if the index case is independently
mobile and if restriction of activities of daily living is being considered.
Theoretically, this practice offers the infection control practitioner an
earlier indication of transmission than would be provided by routine cultures
of infected secretions. The efficacy and cost-effectiveness of this procedure
are unknown.
We identified 67 MRSA infections in 69 months (1.6 per 100 residents
per year) and determined adverse associations (ie, vancomycin therapy in 21,
hospitalization in 19, and death). We do not know what proportions of outcomes
were related to methicillin resistance vs underlying disease. We did not find
high rates of MRSA infection, although the bacterial cause of many serious
nursing home infections is not determined.1
Sputum specimens are not obtained during many episodes of terminal pneumonia.
(Pneumonia is noted as a factor on 32% of death certificates at the Wisconsin
Veterans Home.) Rahimi10 reported no deaths
or hospitalizations attributed to MRSA infection in 1 year in 87 nursing home
patients. Feingold et al11 reported a similar
experience in a 60-bed nursing home. It is unlikely that any intervention
could improve on the results of these small nonintervention studies (infection
rates, <1.1 per 100 residents per year). Similar prospective studies,1-2,4, 9, 13
however, have demonstrated MRSA infection–related deaths or hospitalizations.
Diabetes mellitus, dialysis, and peripheral vascular disease have been identified
as risk factors for MRSA infection.4, 13
Methicillin-resistant S aureus infection rates (infections
per bed per year) have been reported to be 0% to 6.3%,9-12,14
with higher rates in known carriers.1, 9, 12-14
Muder et al13 reported an infection rate of
15% in 32 known carriers in 100 days, with dialysis as a significant risk
factor. Prospective surveillance to identify carriers will not identify some
individuals who subsequently develop MRSA infections.1-2,12-14
Methicillin-resistant S aureus bacteremia can be
lethal, especially if initial antibiotic therapy is misguided.1, 4
Individuals known to carry MRSA who present with serious infection syndromes
should be covered for MRSA until appropriate cultures return. Infections with
MRSA might be associated with lethal outcomes in nursing home residents.
Staphylococcus aureus is a common cause of
skin infections, pneumonia, and bacteremia in hospitals. At any given time,
it colonizes the nose of approximately 30% of humans, and it is one of the
heartiest non–spore-forming bacteria and can survive in the environment.15 During this study, 24% of S aureus isolates at the Wisconsin Veterans Home were resistant to methicillin
therapy, a percentage similar to that in hospitals throughout the United States.16 During the relatively brief period humans have been
using antibiotics, Staphylococcus has adapted with
the emergence of antibiotic resistance. Nursing home residents are frequently
hospitalized and frequently treated with antibiotics. At any given point,
6% to 8% of residents are being subjected to antibiotic treatment within close
quarters, where mobility, socialization, and group activities are encouraged.17 The scene is set for the introduction, selection,
and transmission of MRSA. As stated at the beginning of this article, our
purpose was to determine the burden of transmission and infection and to refocus
or redirect our infection control program. We recommend that MRSA be dealt
with in the context of an infection control program with 4 components:
1. The judicious use of all antibiotics, including topical agents, to
reduce the emergence of resistant bacteria.
2. Implementation of a system that encourages performing cultures of
infected secretions. As long as MRSA infection is recognized, recovery should
not be compromised, except in severe infections in which effective antibiotic
choice is limited. The importance of this point cannot be overemphasized.
Severe MRSA infections must be identified by culture. Culture and sensitivity
data also have many institutional benefits: (a) They allow determination of
the proportion of MRSA isolates from various sites. Clinicians should be aware
of the relative probability of MRSA at their institution and include it in
the early differential diagnosis of serious clinical infections so that proper
antibiotic therapy is not delayed. This latter circumstance is the reason
we fear MRSA. (b) They allow identification of outbreaks. (c) They might allow
clinicians to substitute narrow-spectrum antibiotics such as amoxicillin for
broad-spectrum antibiotics such as cephalosporins or quinolones that give
MRSA a selective advantage (ie, prevention of MRSA). The Infectious Disease
Society of America recommends "pathogen-directed therapy based on in vitro
susceptibility test results" for the treatment of community-acquired pneumonia
because of concerns that empirical selection of drugs will drive microbial
resistance.18
3. Implementation of universal standard secretion precautions. It is
likely that when transmission occurs, it is because of lapses in basic standard
secretion precautions. In the absence of screening, there are probably many
unrecognized carriers of antibiotic-resistant bacteria. These unrecognized
carriers probably pose a greater risk of transmission than the resident with
"MRSA" emblazoned on his chart. Staff must be reminded that any resident could
be a carrier. This is analogous to bloodborne pathogens.
4. Performance of an individual assessment of residents with MRSA that
includes mobility, comprehension, hygiene, ability to contain colonized secretions,
and any bacteriologic data implicating the resident in transmission. This
will allow formulation of an individual care plan to isolate colonized secretions
and maximize activities of daily living. The MRSA carrier state creates a
conflict between 2 powerful principles of nursing home practice, ie, maintaining
a safe environment and maximizing independence in activities of daily living.
This conflict is greatest in a colonized resident with poor hygiene who is
independently mobile. Control measures used in hospitals should not automatically
be extrapolated into nursing homes. Contact secretion precautions should be
applied, especially if secretions were poorly contained and close contact
was required. A SHEA position paper on antimicrobial resistance in long-term
care recommended that residents colonized with resistant pathogens not be
restricted from group activities unless they are shedding large numbers of
organisms and the resident was epidemiologically linked to infection in other
residents.19 Unfortunately, there may be a
delay between transmission and the discovery of transmission by culturing
infected secretions. In addition, some mobile carriers not implicated in transmission
are observed to be contaminating the common environment during independent
activity. Nursing home staff have great difficulty reconciling this observation
with their own efforts to contain secretions. We, therefore, believe that
physical separation that is well tolerated should be implemented without evidence
of transmission. If the resident leaves his or her room, colonized sites should
be secured and covered and assisted hand washing and possibly clean clothes
provided. Personal items and equipment could be left behind, with regular
decontamination of surfaces frequently touched by the resident. The care plan
must be individualized and will be limited by the facility resources. Unfortunately,
basic hygiene in common areas cannot be maintained in some residents without
some restriction of activities of daily living. This step requires significant
attention to the resident's psychosocial adaption. If antibiotic treatment
of MRSA is administered because of infection or transmission, the sites of
colonization should be fully characterized to optimize therapy. Consider the
presence of such things as foreign bodies, devitalized tissue, ischemia, sinusitis,
bronchiectasis, elevated postvoid residua, and osteomyelitis. If an underlying
substrate is not addressed mechanically, decolonization is especially unlikely.
Management recommendations for known carriers will continue to evolve. Perhaps
residents, surrogates, and the public should be informed that nursing homes,
like child day care facilities, care for individuals who have received multiple
courses of antibiotics and might carry antibiotic-resistant bacteria. Residents
socialize and interact with one another and can exchange bacteria during social
interactions.
The fear of MRSA should be harnessed to improve universal standard secretion
precautions and to obtain culture specimens for targeting antibiotic treatment.
AUTHOR INFORMATION
Accepted for publication March 14, 2001.
Corresponding author: Paul Drinka, MD, Medical Director, Wisconsin
Veterans Home, N2665 County Rd QQ, King, WI 54946-0620 (e-mail: Paul.Drinka{at}dva.state.wi.us).
From the Wisconsin Veterans Home, King (Dr Drinka, Mr Faulks, and Ms
Gauerke); the Veterans Affairs Medical Center, Madison, Wis (Dr Goodman);
the Microbiology Section, Marshfield Laboratories (Ms Stemper), and the Marshfield
Medical Research Foundation (Dr Reed), Marshfield, Wis.
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