Journal of Hospital Infection
(2002)
51: 21±26
doi:10.1053/jhin.2002.1186, available online at http://www.idealibrary.com on
Management of an outbreak of
Enterobacter
cloacae
in a neonatal unit using simple
preventive measures
Y. v. Dijk *, E. M. Bik
y, S. Hochstenbach
-
Vernooijy, G. J. v. d. Vlistz
P. H. M. Savelkoul
x, J. A. Kaank
and R. J. A. Dieperslootk
*Department of Infection Control, Diakonessen Hospital, Utrecht,
yDepartment of Microbiology and Immunology,
St. Antonius Hospital, Nieuwege
in,
zDepartment of Paediatrics, Diakonessen Hospital, Utrecht,
xDepartment of
Microbiology and Infection Prevention, VU Medical Center, Amsterdam, and
kDepartment of Microbiology and
Immunology, Diakonessen Hospital, Utrecht, The Netherlands
Summary:
Enterobacter cloacae
is becoming an increasingly important nosocomial pathogen. Outbreaks of
E. cloacae
in intensive care units and burns units have been described frequently. In December 1999, a
neonate
with line sepsis was transferred from a university
hospital to the neonatal unit of the Diakonessen Hospital.
Blood culture yielded
E. cloacae. An outbreak of
E. cloacae
was occurring in the university hospital at that
time.
In February 2000, a second neonate in our hospital developed line sepsis caused
by
E. cloacae. Direct
measures
taken included cohorting of infected children, disinfection of incubators, thermometers and wards, and
screening patients. Of nine neonates, seven were colonized with
E. cloacae. Despite these measures, the
out
-
break con
tinued. Forty
-
one patients were screened; 15 were colonized. Environmental searches yielded
E. cloacae
in a sink and on two thermometers. Sixteen isolates were typed by arbitrarily primed PCR using
four
primers. All the patient isolates and the two isola
tes from thermometers were identical. The strain isolated
from the sink was unrelated. Amplified fragment length polymorphism typing showed that the outbreak clone
was identical to that in the university hospital. After the introduction of disposable
thermometer covers,
E. cloacae
colonization slowly decreased.
&
2002 The Hospital Infection Society
Keywords: Enterobacter cloacae; neonatal unit; thermometer; transmission; genotyping.
Introduction
Enterobacter
species, particularly
Enterobacter
clo
acae, are commensals of the gastrointestinal tract
in healthy adults, and rarely cause primary human
disease. However,
E. cloacae
is becoming an
increasingly important nosocomial pathogen.
1
It
is frequently cultured form body substances of
hospitalize
d patients, particularly those treated with
antibiotics.
2
Colonization has been associated
with blood, wound, respiratory and urinary tract
infections.
3
It has been suggested that colonization
and infection may arise endogenously and that
cross
-
infect
ion is relatively uncommon.
1
Never
-
theless, outbreaks of infections have been reported
in neonatal intensive care units (NICUs),
4±6
surgical
wards
7
and burns units,
8
mediated by factors such
as contaminated pharmaceutical products,
9,10
cross
-
contamination by healthcare workers' hands,
11
and
medical equipment.
12
Outbreaks often continue for
Received 20 June 2001; revised manuscript accepted
15 January 2002.
Author for correspondence: Dr Y. v. Dijk, Diakonessen Hospital
Utrecht, Department
of Infection Control, Bosboomstraat 1,
3582 KE Utrecht, The Netherlands. E
-
mail: yvdijk@diakhuis.nl
0195
-
6701/02/010021
1
06 $35.00/0
&
2002 The Hospital Infection Society
months
and
require
radical
measures,
such
as
ward
closure
or
changing
antibiotic
policy.
13
Here
we
report
an
outbreak
of
cross
-
colonization
and
infec
-
tion
by
E.
cloacae
with
resistance
to
third
-
generation
cephalosporins,
among
patients
in
a
neonatal
care
unit,
and
describe
the
ability
of
relatively
simple
infection
control
proced
ures
to
stop
the
outbreak.
Patients
and
methods
Characteristics
of
the
ward
The
outbreak
occurred
in
the
Diakonessen
Hospital
in
Utrecht,
The
Netherlands,
a
teaching
hospital
of
370
beds.
The
neonatal
unit
is
a
12
-
bed
unit
divided
into
a
large
room
and
one
smaller
room,
and
has
250
admissions
per
year.
Premature
neonates
<30
gestational
weeks
or
with
severe
organ
dysfunction
are
transferred
to
the
intensive
care
unit
of
a
university
hospital
for
life
-
support
treatment
and
are
returned
to
our
unit
when
stabilized.
Nurses
assigned
to
the
unit
work
in
all
the
rooms.
Nurses,
staff
and
visitors
wear
gowns
whenever
children
are
taken
out
of
the
incubator.
Nurses
and
(para
-
)
medical
personnel
are
instructed
to
disinfect
their
hands
prior
to
each
contact.
The
children
are
not
routinely
screened
for
bacterial
colonization.
First
-
line
therapy
for
suspected
sepsis
is
amoxicillin
in
combination
with
gentamicin.
Case
definition
A
case
was
defined
as
a
child
admitted
to
the
neonatal
unit,
who
had
E.
cloacae
identified
in
an
isolate
from
any
site.
Criteria
for
infection
were
as
defined
by
the
Centers
for
Disease
Control.
14
Isolates
from
speci
-
mens
not
associated
with
infection
were
classified
as
colonization.
Bacteriological
cultures
During
the
outbreak,
specimens
for
surveillance
culture
were
obtained
once
a
week
from
the
naso
-
pharynx
and
rectum
from
all
children
in
the
neonatal
unit.
Samples
were
also
obtained
from
environ
-
mental
sites,
including
sinks,
hand
basins,
bedrails,
ventilators,
thermometers,
oil
tissues,
solutions,
and
incubators.
Specimens
were
cultured
on
5%
sheep
blood
agar
and
Colombia
CNA
agar
(bioMeÂ
rieux,
Marcy
-
l'Etoile,
France)
and
incubated
at
37
?
C.
The
bacterial
isolates
were
identified
to
species
level
using
standard
methods,
and
tested
for
susceptibility
to
amoxicillin,
amoxillin/clavulanate,
gentamicin,
amikacin,
cotrimoxazole,
ceftazidime,
ceftriaxone,
ciprofloxacin
and
imipenem.
All
the
isolates
were
stored
at
?
70
?
C,
and
were
tested
for
the
presence
of
extended
-
spectrum
b
-
lactamase
using
the
E
-
test
system
(AB
-
Biodisk,
Solna,
Sweden).
Epidemiological
typing
of
bacterial
isolates
To
examine
the
relatedness
between
different
E.
cloacae
isolates,
two
molecular
typing
methods
were
used.
First,
13
patient
isolates
and
three
environmental
strains
(two
from
thermometers
and
one
from
a
hand
basin)
were
typed
using
arbi
-
trarily
primed
PCR
(AP
-
PCR).
Chromosomal
DNA
was
extracted
from
bacterial
cultures
on
sheep
agar
plates
using
the
QIAamp
DNA
mini
kit
(QIAgen,
Westburg,
The
Netherlands).
AP
-
PCR
was
performed
in
25
mL
reaction
volumes
using
primers
ERIC1,
ERIC2,
RW3A
and
AP1.
15±17
Each
reaction
mixture
contained
10
m
M
Tris
-
HCl
(pH
9.0),
50
m
M
KCl,
2.5
m
M
MgCl,
0.1%
Triton
X
-
100,
0.01%
(w/v)
gelatin,
200
m
M
of
each
of
the
four
deoxynucleotide
triphosphates,
40
pmol
primer,
0.75
U
of
SuperTaq
polymerase
(HT
Biotechnology
Ltd.,
Cambridge,
UK)
and
50
ng
of
chromosomal
DNA.
A
Perkin
Elmer
PE9600
thermocycler
was
used
for
amplifi
-
cation.
Cycling
conditions
consisted
of
the
following
steps:
5
min
at
95
?
C,
35
cycles
of
1
min
at
95
?
C,
1
min
at
25
?
C,
and
2
min
at
72
?
C,
followed
by
a
7
-
min
extension
at
72
?
C.
PCR
products
were
separated
by
electrophoresis
on
a
1%
agarose
gel,
stained
with
ethidium
bromide
and
visualized
by
UV
light.
Sec
-
ondly,
isolates
from
different
hospitals
were
com
-
pared
by
amplified
fragment
length
polymorphism
(AFLP),
using
restriction
enzymes
EcoR1
and
Mse1
as
described
previously.
18
Control
strains
from
unrelated
patients
were
included
in
both
typing
techniques.
Infection
control
measures
At
the
start
of
the
outbreak
(February
2000),
the
infection
control
measures
on
the
unit
were
reviewed
and
personnel
were
urged
to
be
careful
in
their
use,
and
incubators
and
materials
were
disinfected
(hypochlorite
300
ppm
or
70%
ethyl
alcohol).
All
infected
and
colonized
children
were
cohorted.
Cohorting
of
the
personnel
was
impossible
because
of
shortage
of
nurses.
Gloves
were
worn
to
handle
22
Y.
v.
Dijk
et
al.
colonized
children.
Contaminated
objects
and
surfaces
were
routinely
disinfected
with
hypochlo
-
rite
300
ppm
or
70%
ethyl
alcohol.
A
three
-
day
observational
study
was
conducted
to
monitor
the
infection
prevention
practice
of
healthcare
workers
and
parents.
The
results
of
the
interventions
were
discussed
during
weekly
meetings
with
representa
-
tives
of
the
neonatal
care
unit
and
the
Department
of
Infection
Prevention
to
watch
over
the
progress.
Results
Description
of
the
outbreak
In
December
1999,
a
neonate
(patient
1)
was
transferred
from
the
NICU
of
a
university
hospital
to
our
neonatal
care
unit.
The
neonate
developed
line
-
associated
sepsis
the
following
day.
Blood
culture
yielded
E.
cloacae
(Figure
1).
In
February
2000,
a
second
neonate
(patient
2)
developed
(line
-
associated)
sepsis
caused
by
E.
cloacae
(Figure
1).
At
the
time,
an
outbreak
of
E.
cloacae
involving
32
patients
was
occurring
at
the
NICU
of
the
university
hospital
from
which
the
index
chi
ld
was
transferred.
We
immediately
screened
all
neonates
by
specimen
collection
from
the
nasopharynx
and
rec
-
tum.
Of
the
nine
children
screened,
seven
were
colonized
with
E.
cloacae.
All
those
who
had
been
in
the
neonatal
unit
for
at
least
two
days
were
colonized.
Environmental
cultures
yielded
E.
cloacae
from
a
hand
basin
and
two
thermometers.
No
other
environmental
samples
were
found
to
harbour
the
organism.
Measures
In
our
weekly
meetings
with
the
neonatal
unit,
we
discussed
our
first
interventions.
All
sinks
and
hand
basins
were
disinfected
daily
with
hypochlorite
(300
ppm).
Disinfection
of
thermometers
changed
from
a
quick
rinse
with
70%
ethyl
alcohol
to
10
min
immersion
in
70%
ethyl
alcohol.
Other
measures
included
cohorting
of
the
colonized
and
infected
children,
disinfection
of
the
incubator
beds
and
wards,
reinforcement
of
handwashing
practice,
and
weekly
bacterial
screening
of
all
patients.
Observation
of
the
healthcare
workers'
handwashing
practice
indicated
good
compliance.
The
parents
turned
out
to
regularly
take
new
universal
oil
tissues
with
contaminated
hands.
Although
no
micro
-
organisms
were
isolated
from
tissues,
it
was
decided
to
give
each
child
their
own
tissues.
During
the
observation,
no
other
possible
route
of
transmission
was
noticed.
Despite
these
preventive
measures,
the
outbreak
continued.
A
total
of
41
patients
were
screened,
of
whom
15
were
colonized
with
E.
cloacae
(Figure
1).
No
other
child
developed
an
infection.
Despite
the
extended
disinfection
time,
Gram
-
negative
micro
-
organisms
were
still
isolated
from
the
thermometers.
Therefore,
all
thermometers
were
replaced
and
disposable
covers
were
introduced.
After
this
and
the
introduction
of
individual
oil
tissues,
the
number
of
new
cases
of
E.
cloacae
slowly
decreased.
One
month
and
six
months
after
the
outbreak,
all
neonates
were
screened
again.
In
July
2000,
no
E.
cloacae
was
found.
In
October
2000,
E.
cloacae
16
Jul
1
Month
P
a
t
ie
n
t
n
um
b
e
r
Dec
1999
Oct
Nov
Jan
2000
Feb
Mar
Apr
May
Jun
2
3
4
5
6
7
8
9
10
11
12
13
14
15
Figure
1
Patients
colonized
with
E.
cloacae
strains
(
bfd
)
admission
on
the
neonatal
unit;
(
l
fl
)
culture
with
E.
cloacae.
E.
cloacae
in
neonatal
unit
23
was
isolated
from
the
rectum
of
one
neonate
(patient
16).
Sensitivity
and
typing
All
the
E.
cloacae
strains
isolated
during
the
outbreak
displayed
similar
antibiograms.
All
were
resistant
to
amoxicillin,
amoxicillin/clavunalate,
ceftazidime
and
ceftriaxone.
An
extended
-
spectrum
b
-
lactamase
was
demonstrated
in
all
isolates.
Sixteen
E.
cloacae
strains
isolated
from
patients
and
environmental
sites
in
the
Diakonessen
Hospital
were
typed
genetically
using
AP
-
PCR
with
four
different
primers.
The
result
from
the
ERIC1
PCR
fingerprinting
is
shown
in
Figure
2.
Four
control
strains
(lanes
1±4)
could
all
be
distinguished
from
each
other,
confirming
the
reso
-
lution
of
this
technique.
All
E.
cloacae
strains
isolated
from
patients
2±15
from
February
to
April
2000,
and
the
two
isolates
from
thermometers
showed
identical
fingerprints
with
each
of
the
primers,
confirming
the
suspected
cluster,
and
linking
it
to
the
thermometers.
In
contrast,
the
isolate
from
the
hand
basin
and
the
strain
from
patient
16
which
was
isolated
in
October
2000,
six
months
after
the
outbreak,
both
displayed
unique
fingerprint
patterns,
indicated
that
their
genotypes
were
unrelated
(Figure
2,
lanes
19
and
20,
respectively).
AFLP
typing
showed
that
the
E.
cloacae
outbreak
strain
was
identical
to
the
outbreak
strain
at
the
university
hospital
from
which
the
index
child
was
transferred
(Figure
3).
1000 bp
Patient
16
500 bp
Thermo
-
meters
Sink
Patients
Control
strains
M
C
C C
C
2
4
5
6
7 8
9
10 11
12
13
15
T
T
S
16
N
C
Figure
2
ERIC1
PCR
-
fingerprinting
of
E.
cloacae
strains.
100
60
Outbreak strain university hospital
Outbreak strains
Diakonessenhuis
Control strain 1
Control strain 2
70
80
90
Figure
3
AFLP
typing
of
E.
cloacae
strains.
24
Y.
v.
Dijk
et
al.
Discussion
In
this
study,
we
describe
an
outbreak
of
E.
cloacae
colonization
in
a
neonatal
unit.
Newborns
are
known
to
be
at
risk
for
colonization
of
Enterobacter
spp.
19
While
neonates
initially
have
a
sterile
gastrointestinal
tract,
bacterial
colonization
occurs
rapidly
in
hospital,
the
result
of
selective
antibiotic
pressure
and
nosocomial
spread
through
inadequate
hygiene.
20
Interestingly,
the
NICU
that
transferred
the
index
case
to
our
hospital
used
a
third
-
generation
cephalosporin,
ceftriaxone,
as
routine
therapy
for
neonatal
sepsis.
In
some
hospitals,
children
become
rapidly
colonized.
In
a
multicentre
study,
Fryklund
et
al.
found
a
colonization
rate
in
various
neonatal
care
units
of
0±78%.
2
Intestinal
colonization
appears
to
be
a
precursor
of
the
widespread
colonization
and
the
invasive
infection
which
occurs
in
only
a
small
proportion
of
colonized
children.
21
A
case
record
study
of
Acoled
et
al.
showed
an
association
between
Enterobacter
septicaemia
and
short
gestation,
low
birthweight,
longer
period
of
endotracheal
intuba
-
tion,
and
length
of
hospital
stay.
22
This
might
explain
why
only
two
of
the
children
in
our
study
developed
an
E.
cloacae
infection.
Both
(patients
1
and
2;
Figure
1)
were
premature
(32
weeks
4
days
and
30
weeks
6/7
days)
and
had
low
birthweights,
1065
g
and
1140
g,
respectively.
Before
the
outbreak,
isolation
of
E.
cloacae
bac
-
teria
on
our
neonatal
ward
occurred
rarely.
The
high
increase
in
E.
cloacae
colonized
children
during
the
first
months
of
2000
raised
the
suspicion
of
an
out
-
break.
Indeed
molecular
fingerprinting
using
AP
-
PRC
and
AFLP
showed
that
all
the
E.
cloacae
strains
from
the
15
colonized
patients
were
geneti
-
cally
identical
(Figures
2
and
3).
Immediately
after
the
discovery
of
a
large
number
of
colonized
children,
the
factors
that
may
have
contributed
to
this
outbreak
were
investigated.
Previous
reports
documented
that
transmission
of
E.
cloacae
from
patient
to
patient
was
attri
buted
to
hospital
personnel,
or
use
of
contaminated
medical
devices.
5,12
In
our
hospital,
cross
-
transmission
by
hospital
personnel
was
unlikely,
since
there
was
a
strict
handwashing
routine.
Despite
an
intensive
environmental
search,
E.
cloacae
was
only
found
in
a
hand
basin
and
on
two
thermometers.
Of
these,
the
thermometers
were
colonized
with
the
outbreak
strain,
as
shown
by
DNA
fingerprinting
(Figure
2).
This
strongly
suggested
that
thermometers
were
the
routes
of
transmission.
Our
findings
correspond
to
those
from
another
Dutch
hospital
in
which
the
involvement
of
thermometers
in
an
E.
cloacae
out
-
break
in
a
NICU
is
described.
23
Outbreaks
involv
-
ing
other
micro
-
organisms
related
to
thermometers
have
also
been
published.
24
In
neonatal
units,
the
body
temperature
is
often
measured
by
rectal
thermometers.
In
contrast
with
other
units,
disposable
covers
were
not
used,
since
the
edges
of
the
standard
covers
may
harm
the
anal
sphincter
of
neonates.
Instead,
before
the
outbreak,
every
child
received
a
personal
thermometer.
After
use,
the
thermometer
was
wiped
with
gauze
soaked
in
70%
ethyl
alcohol
and
stored
in
a
personal
plastic
basket.
After
discharge
of
the
child,
the
same
disinfection
procedure
was
followed.
For
twins,
frequently
only
one
thermometer
was
used.
The
iso
-
lation
of
E.
cloacae
from
two
thermometers
shows
that
disinfection
was
inadequate.
Van
den
Berg
et
al.
also
showed
that
after
disinfection
with
80%
ethyl
alcohol,
one
out
of
10
thermometers
remained
contaminated
with
E.
cloacae.
23
Even
after
prolonged
incubation
of
thermometers
in
ethyl
alcohol,
our
outbreak
continued,
indicating
that
such
disinfection
is
inadequate.
Special
disposable
thermometer
covers
for
neonates
without
sharp
edges
are
available
(Uni
-
Instrumenten,
The
Netherlands).
When
we
introduced
these
on
the
unit,
contamination
of
the
thermometers
and
the
outbreak
stopped.
The
genetic
unrelatedness
of
the
strain
from
patient
16
(isolated
six
months
after
outbreak)
to
the
outbr
eak
clone
indicates
that
after
April
2000,
no
further
patient
-
to
-
patient
transmission
occurred,
and
that
the
use
of
disposable
thermometer
covers
and
the
other
measures
were
finally
vindicated.
Most
likely,
the
E.
cloacae
found
in
this
patient
was
coincidental.
The
E.
cloacae
outbreak
strain
was
probably
introduced
into
the
neonatal
care
unit
of
our
hospital
by
the
transfer
of
a
colonized
child.
AFLP
typing
showed
that
the
E.
cloacae
outbreak
clone
was
closely
related
to
that
of
the
NICU
of
the
university
hospital
from
which
the
index
case
was
transferred
(Figure
3).
To
our
knowledge,
this
is
the
first
report
on
hospital
-
to
-
hospital
transmission
of
an
E.
cloacae
strain.
The
fact
that
this
caused
outbreaks
in
at
least
two
neonatal
units
suggests
that
it
possesses
certain
specific
virulence
factors,
which
enables
it
to
cause
epidemic
spread.
Not
much
is
known
about
epidemic
E.
cloacae,
and
this
finding
deserves
more
investi
-
gation.
Probably
the
difference
in
their
predilection
E.
cloacae
in
neonatal
unit
25
for
survival
in
the
human
or
in
the
environment
plays
an
important
role.
20,21
In
conclusion,
an
outbreak
caused
by
E.
cloacae
in
a
neonatal
unit
was
recognized,
and
confirmed
by
molecular
fingerprinting.
Infected
thermometers
were
found
to
be
the
most
important
vector.
When
an
outbreak
of
this
kind
occurs,
stopping
further
admission
is
an
accepted
intervention.
23
Our
results
show
that
a
strict
regime
of
simple
infection
control
procedures
in
combination
with
regular
feedback
can
be
a
worthwhile
alternative.
References
1.
Sanders
WE
Jr,
Sanders
CC.
Enterobacter
spp:
pathogens
poised
to
flourish
at
the
turn
of
the
century.
Clin
Microbiol
Rev
1997;
10:
220±241.
2.
Fryklund
B,
Tullus
K,
Burman
LG.
Epidemiology
of
enteric
bacteria
in
neonatal
unitsÐinfluence
of
procedures
and
patient
variables.
J
Hosp
Infect
1991;
18:
15±21.
3.
Jarvis
WR,
Martone
WJ.
Predominant
pathogens
in
hospital
infections.
J
Antimicrob
Chemother
1992;
29(Suppl.
A):
19±34.
4.
Peters
SM,
Bryan
J,
Cole
MF.
Enterobacterial
repetitive
intergenic
consensus
polymerase
chain
reaction
typing
of
isolates
of
Enterobacter
cloacae
from
an
outbreak
of
infection
in
a
neonatal
intensive
care
unit.
Am
J
Infect
Control
2000;
28:
123±12
9.
5.
Verweij
PE,
Belkum
van
A,
Melchers
WJG
et
al.
Interrepeat
fingerprinting
of
third
-
generation
cephalosporin
-
resistant
Enterobacter
cloacae
isolated
during
an
outbreak
in
a
neonatal
intensive
care
unit.
Infect
Control
Hosp
Epidemiol
1995;
16:
25±29.
6.
Nierop
van
WH,
Duse
AG,
Stewart
RG
et
al.
Molecular
epidemiology
of
an
outbreak
of
Enterobacter
cloacae
in
the
neonatal
intensive
care
unit
of
a
provincial
hospital
in
Gauteng,
South
Africa.
J
Clin
Microbiol
1998;
36:
3085±3087.
7.
Andersen
BM,
Sorlie
D,
Hotvedt
R
et
al.
Multiply
beta
-
lactam
resistant
Enterobacter
cloacae
infections
linked
to
the
environmental
flora
in
a
unit
for
cardiothoracic
and
vascular
surgery.
Scand
J
Infect
Dis
1989;
21:
181±191.
8.
Markowitz
SM,
Smith
SM,
Williams
DS.
Retro
-
spective
analysis
of
plasmid
patterns
in
a
study
of
burn
unit
outbreaks
of
infection
due
to
Enterobacter
cloacae.
J
Infect
Dis
1983;
148:
18±23.
9.
Archibald
LK,
Ramos
M,
Arduino
MJ
et
al.
Entero
-
bacter
cloacae
and
Pseudomonas
aeruginosa
poly
-
microbial
bloodstream
infections
traced
to
extrinsic
contamination
of
dextrose
multidose
vial.
J
Pediatr
1998;
133:
640±644.
10.
Tresoldi
AT,
Padoveze
MC,
Trabasso
P
et
al.
Enterobacter
cloacae
sepsis
outbreak
in
a
newborn
unit
caused
by
contaminated
total
parenteral
nutrition
solution.
Am
J
Infect
Control
2000;
28:
258±261.
11.
Harbarth
S,
Sudre
P,
Dharan
S
et
al.
Outbreak
of
Enterobacter
cloacae
related
to
understaffing,
overcrowding,
and
poor
hygiene
practices.
Infect
Control
Hosp
Epidemiol
1999;
20:
598±603.
12.
Thomas
A,
Lalitha
MK,
Jesudason
MV
et
al.
Trans
-
ducer
related
Enterobacter
cloacae
sepsis
in
post
-
operative
cardiothoracic
patients.
J
Hosp
Infect
1993;
25:
211±214.
13.
FinnstroÈ
m
O,
Isaksson
B,
Haeggman
S
et
al.
Control
of
an
outbreak
of
highly
beta
-
lactam
-
resistant
Enterobacter
cloacae
strain
in
a
neonatal
special
unit.
Acta
Paediatr
1998;
87:
1070±1074.
14.
Garner
JS,
Javis
WR,
Emori
TC
et
al.
CDC
definitions
for
nosocomial
infections.
Am
J
Infect
Control
1998;
16:
128±140.
15.
DelVecchio
VG,
Petroziello
JM,
Gress
MJ
et
al.
Molecular
genotyping
of
methicillin
-
resistant
Staphylococcus
aureus
via
fluorophore
-
enhanced
repetitive
-
sequence
PCR.
J
Clin
Microbiol
1995;
33:
2141±2144.
16.
Versalovic
J,
Koeuth
T,
Lupski
JR.
Distribution
of
repetitive
DNA
sequences
in
eubacteria
and
appli
-
cation
to
fingerprinting
of
bacterial
genomes.
Nucl
Acid
Res
1991;
19:
6823±6831.
17.
Belkum
van
A,
Kluytmans
J,
Leeuwen
van
W
et
al.
Multicenter
evaluation
of
arbitrary
primed
PCR
for
typing
of
Staphylococcus
aureus
strains.
J
Clin
Micro
-
biol
1995;
33:
1537±1547.
18.
Savelkoul
PHM,
Aarts
HJM,
de
Haas
J
et
al.
Ampli
-
fied
-
fragment
length
polymorphism
analysis:
the
state
of
an
art.
J
Clin
Microbiol
1999;
37:
3083±3091.
19.
Goldmann
DA.
The
bacterial
flora
of
neonates
in
intensive
care
-
monitoring
and
manipulation.
J
Hosp
Infect
1988;
11(Suppl.
A):
340±351.
20.
Acolet
D,
Ahmet
Z,
Houang
E
et
al.
Enterobacter
cloacae
in
a
neonatal
intensive
care
unit:
account
of
an
outbreak
and
its
relationship
to
use
of
third
generation
cephalosporins.
J
Hosp
Infect
1994;
28:
273±286.
21.
Tullus
K,
Berglund
B,
Fryklund
B
et
al.
Epidemiology
of
fecal
strains
of
the
family
Enterobacteriaceae
in
22
neonatal
wards
and
influence
of
antibiotic
policy.
J
Clin
Microbiol
1988;
26:
1166±1170.
22.
Fok
TF,
Hon
Lee
C,
Wong
EMC
et
al.
Risk
factors
for
Enterobacter
septicemia
in
a
neonatal
unit:
case
-
control
study.
Clin
Infect
Dis
1998;
27:
1204±1209.
23.
Berg
van
den
RWA,
Claahsen
HL,
Niessen
M
et
al.
Enterobacter
cloacae
outbreak
in
the
NICU
related
to
disinfected
thermometers.
J
Hosp
Infect
2000;
45:
29±43.
24.
Broek
van
den
PJ,
Verbakel
-
Salomons
EMA,
Franssen
A
et
al.
Thermometers
as
vehicle
of
Klebsiella
pneumoniae
producting
extended
spectrum
betalacta
-
mase.
Infect
Control
Hosp
Epidemiol
2000;
21:
134.
26
Y.
v.
Dijk
et
al.
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