JOURNAL OF CLINICAL MICROBIOLOGY, May 2007, p. 1551–1555
Copyright © 2007, American Society for Microbiology. All Rights Reserved.
Vol. 45, No. 5
Surveillance Cultures and Duration of Carriage of Multidrug-Resistant
Dror Marchaim,1* Shiri Navon-Venezia,1David Schwartz,2Jalal Tarabeia,1Iris Fefer,1
Mitchell J. Schwaber,1and Yehuda Carmeli1
Division of Epidemiology, Tel-Aviv Sourasky Medical Center, 6 Weizmann St., Tel-Aviv 64239, Israel,1and
Clinical Microbiology Laboratory, Tel-Aviv Sourasky Medical Center, 6 Weizmann St., Tel-Aviv 64239, Israel2
Received 2 December 2006/Returned for modification 22 January 2007/Accepted 12 February 2007
Isolating carriers of multidrug-resistant (MDR) Acinetobacter baumannii is the main measure to prevent its
spread. Identification of carriers accompanied by contact precautions is essential. We aimed to determine the
appropriate surveillance sampling sites and the duration of carriage of MDR A. baumannii. We studied
prospectively two groups of patients from whom MDR A. baumannii was previously isolated: (i) those with
recent clinical isolation (<10 days) and (ii) those with remote clinical isolation (>6 months). Screening for
carriage was conducted from six sites: nostrils, pharynx, skin, rectum, wounds, and endotracheal aspirates.
Strains recovered concurrently from different sites were genotyped using pulsed-field gel electrophoresis.
Twelve of 22 with recent clinical isolation of MDR A. baumannii had >1 positive screening culture, resulting
in a sensitivity of 55% when six body sites were sampled. Sensitivities of single sites ranged from 13.5% to 29%.
Among 30 patients with remote clinical isolation, screening cultures were positive in 5 (17%), with a mean
duration of 17.5 months from the last clinical culture. Remote carriers had positive screening cultures from the
skin and pharynx but not from nose, rectum, wounds, or endotracheal aspirates. Eleven strains from five
patients were genotyped. In all but one case, isolates from different sites in a given patient were clonal. Current
methodology is suboptimal to detect MDR A. baumannii carriage. The sensitivity of surveillance cultures is low,
even when six different body sites are sampled. The proportion of individuals with previous MDR A. baumannii
isolation who remain carriers for prolonged periods is substantial. These data should be considered when
designing measures to limit the spread of MDR A. baumannii.
In the past decade, multidrug-resistant (MDR) Acineto-
bacter baumannii has emerged as a major nosocomial pathogen
in many parts of the world, resulting in devastating outcomes in
terms of morbidity, mortality, and costs (1, 2, 11, 14, 18, 26).
Therapeutic options are often scarce, and in many instances
there is not a single drug to administer against this pathogen
(1, 11, 13, 14, 17–20). The International Network for the Study
and Prevention of Emerging Antimicrobial Resistance defined
the emergence of carbapenem resistance in Acinetobacter bau-
mannii infections as a “global sentinel event” warranting
prompt epidemiological and microbiological interventions
The most effective measures reported thus far to reduce the
burden of MDR A. baumannii infections in hospitals are strict
contact precautions, cohorting, application of a routine surveil-
lance program in order to identify silent carriers, intense
cleansing of the carrier’s environment, appropriate manage-
ment of infections, and attempts at decolonization (of ques-
tionable value) (2, 14, 23). These interventions, though cost-
effective in the long run, pose a vast burden on hospital
resources and personnel (2, 7, 9, 10, 13, 17, 23, 25, 26, 28).
Acinetobacter species are widely distributed in the environ-
ment and may be common commensals in humans (14). Rates
of skin colonization as high as 25 to 40% for healthy ambula-
tory volunteers and up to 75% for hospitalized patients are
reported (1–3, 26). The bacteria colonize the pharynx inter-
mittently in 7% of the general population and in addition can
be isolated from sputum, urine, stool, and vaginal discharges
(2, 14, 26). In contrast, MDR A. baumannii is primarily a
nosocomial pathogen acquired in the health care setting, and
its carriage and natural history have not been well studied (14).
This study had two principal aims: (i) to examine the sensi-
tivity of culturing various body site samples to detect carriage
of MDR A. baumannii among patients with recent MDR A.
baumannii clinical isolation, assuming that this group of pa-
tients continues to carry the organism at the time of surveil-
lance; and (ii) to evaluate the long-term carriage of MDR A.
baumannii among patients with a remote MDR A. baumannii
clinical isolation who are readmitted.
MATERIALS AND METHODS
Setting. Tel-Aviv Sourasky Medical Center (TASMC) is a 1,200-bed tertiary-
care teaching hospital comprising 45 wards, with 84,000 admissions and over
87,500 clinical cultures processed annually. Hospital computerized databases
record patients with previously isolated MDR A. baumannii presenting to the
emergency rooms, and “flagging” of a patient in the system results in the imme-
diate application of contact precautions. Israeli hospitals over the past decade
have been considered an environment where MDR A. baumannii is hyperen-
demic, with a rate of detection of 1 per 140 hospital admissions of medical or
surgical patients (1, 23).
Acinetobacter isolates were identified to the species level by use of the Vitek 2
system (bioMe ´rieux, Hazelwood, MO). In order to differentiate the genomic
patterns of the Acinetobacter species identified, PCR of the 16S-23S rRNA
intergenic spacer (internal transcribed spacer) was carried out for the study
isolates according to an established protocol (8). Antimicrobial susceptibility
testing was performed using the Vitek 2 AST GN09 card, and susceptibilities to
* Corresponding author. Mailing address: Division of Epidemiology,
Tel-Aviv Sourasky Medical Center, 6 Weizmann St., Tel-Aviv 64239,
Israel. Phone: 972-52-3591739. Fax: 972-3-6974052. E-mail: drormc
?Published ahead of print on 21 February 2007.
imipenem and meropenem were confirmed by disc diffusion or Etest (AB Bio-
disk, Solna, Sweden). An A. baumannii isolate was defined as MDR if it was
resistant to at least three classes of antibiotics (including penicillins, cephalospo-
rins, monobactams, ?-lactamase inhibitor combinations, aminoglycosides, and
fluoroquinolones), while susceptibilities to amikacin, ampicillin-sulbactam, imi-
penem, meropenem, and minocycline were allowed. All isolates were processed
according to Clinical and Laboratory Standards Institute (CLSI) criteria (12).
Infection control practices during the study period. Throughout the study
period, contact precautions for the duration of the hospital stay were advised for
patients from whom MDR A. baumannii was isolated. Upon admission of a
previously identified carrier, or within 24 h of initial culture of MDR A. bau-
mannii from a hospitalized patient, ward personnel received a daily e-mail list of
patients who needed to be under contact precautions and were called by infec-
tion control practitioners to confirm adherence to contact precautions. In most
cases, patients were in multipatient rooms, their beds were marked with signs
bearing the words “contact precautions,” and gowns and gloves for patient
contact as well as alcohol-based hand disinfectant were present nearby. Periodic
surveys revealed that the material required for contact precautions was present
over 90% of the time; however, compliance with use was not systematically
Study design. Prospective surveillance was conducted from 1 June 2006 to 31
August 2006. Hospitalized adults (?18 years of age) who had positive clinical
cultures of MDR A. baumannii isolated between 1 December 2002 and 31
August 2006 were considered for inclusion. Two groups of patients were in-
cluded. The first group consisted of patients from whom MDR A. baumannii was
isolated from a clinical specimen in the preceding 10 days. We considered these
patients with a recent positive clinical isolation to be carriers by definition. This
group was studied to determine and compare the sensitivities of surveillance
from six different body locations. The second group consisted of patients with a
positive clinical isolation during previous admissions ?6 months prior to study
Each patient was approached by infection control personnel, who after ob-
taining consent cultured patient specimens from four different surveillance sites:
the nose (nostrils, bilaterally), the pharynx, the skin (the swab was premoistened
in the transport media; the same swab was then used to culture the axillae, the
antecubital fossae, and the groin bilaterally, in that order), and the rectum. Two
additional sites were sampled for subsets of patients: wounds, if a draining ulcer
was present; and endotracheal aspirates, if the patient was intubated.
Swabs (CE0373; MEUS, Piove di Sacco, Italy) were inoculated within 1 h in
enriched brain heart infusion broth and incubated for 24 h at 35°C. Samples were
then streaked on selective MacConkey agar plates (Novamed Ltd.; Jerusalem,
Israel) containing 2 ?g/ml amphotericin B and 8 ?g/ml ceftazidime. Quality
control of the selective plates was performed on a regular basis, using Escherichia
coli ATCC strain 25922 as a susceptible strain and a ceftazidime-resistant E. coli
clinical isolate as a resistant strain. In a preliminary study, the enrichment
method showed sensitivity superior to that obtained by the direct plating of swabs
onto selective media when performed in parallel (unpublished data). Represen-
tative colonies of each morphotype were picked in duplicate and transferred to
Enterotubes (Enterotest; Hy Laboratories Ltd., Rehovot, Israel). Oxidase-neg-
ative nonfermentors were further identified by use of the Vitek 2 system to the
species level, and the antimicrobial susceptibility profiles were determined. Iso-
lates were stored at ?70°C for further workup.
Epidemiologic data collection. Epidemiologic data were collected via patient
interviews and chart reviews. Parameters assessed included demographics (age
and sex), microbiological parameters of previous clinical isolations, medical
diagnosis at the current admission, long-term care facility residency, functional
status, level of consciousness, comorbidities (including calculation of the Charl-
son comorbidity index ), severity of illness (according to the McCabe score
), use of chronic invasive devices, recent invasive procedures, recent use of
antibiotics, chronic medications, tobacco or alcohol use, recent immunosuppres-
sive treatment (glucocorticoids or oncologic chemotherapy), malignant diseases,
renal function, nutritional status, and time intervals from most recent hospital-
izations and/or intensive care unit stays.
PFGE. Patients with ?2 positive cultures from different body sites were geno-
typed and classified into genetic clusters by use of pulsed-field gel electrophoresis
(PFGE). Since the initial isolates from previous admissions of the remote car-
riers were not available, we could not compare the PFGE patterns of previous
and current isolations. MDR A. baumannii was cultured on MacConkey agar and
afterwards in brain heart infusion broth for 18 h. Agarose discs of genomic DNA
were prepared as previously described (21, 24). DNA was then cleaved using 20
U of the restriction enzyme ApaI endonuclease (New England Biolabs, Beverly,
MA) for 3 h at 25°C (15, 21, 24). Electrophoresis was performed in a 1% agarose
gel (BMA Products) prepared and run in 0.5? Tris-borate-EDTA buffer on a
CHEF-DR III apparatus (Bio-Rad Laboratories, Richmond, CA). The initial
switch time was 5 seconds, the final switch time was 35 seconds, and the run time
was 23 h at 6 V/cm. Gels were stained with ethidium bromide, destained in
distilled water, and photographed by using a Bio-Rad GelDoc 2000 camera.
DNA patterns were analyzed visually and by using Diversity software (Bio-Rad).
PFGE DNA patterns were compared and interpreted according to an estab-
lished protocol (6, 24, 27).
Statistical analysis. Continuous variables were compared between groups by
use of an unpaired t test and a paired t test within each group. Categorical
variables were compared by use of the Pearson ?2test. For small samples,
analysis of variance and the Fisher exact test were used to analyze continuous
and categorical variables, respectively. Statistical analyses were conducted using
SPSS (version 13.0; SPSS Inc., Chicago, IL) and Stata (version 9.0; Stata Corp.,
College Station, TX). P values of ?0.05 were considered significant.
Surveillance sensitivity study. Twenty-two patients with a
recent clinical isolation of MDR A. baumannii (?10 days)
were considered “carriers” by definition. These patients were
surveyed. Sixteen of the patients were men (73%), the mean
age was 68 years (range, 29 to 88), and the mean number of
days since the last positive MDR A. baumannii isolation was 6
(range, 3 to 10). The index clinical cultures of MDR A. bau-
mannii were obtained from endotracheal aspirates (seven pa-
tients), from wounds (six patients), from urine specimens
(three patients), from intravascular catheter tips (three pa-
tients), and from blood specimens (three patients).
Of the 22 patients studied, 12 had at least one positive
surveillance isolation (range, 1 to 4). Therefore, the overall
sensitivity of the multisite surveillance approach was 55%. The
surveillance site and clinical site cultures are depicted in Table
1. No statistical difference between the various sites in terms of
yield was found (P ? 0.36). The clinical syndrome and the
number of days since the previous MDR A. baumannii isola-
tion were not significantly associated with surveillance culture
The clinical culture location most correlated with positive
surveillance isolation was the endotracheal aspirate, followed
by a wound: five of seven patients (71%) with a positive clinical
culture from the endotracheal aspirate and four of six patients
(67%) with a positive clinical culture from a wound had a
positive surveillance isolation at any site. Other sites of positive
clinical culture—urine, intravascular catheter tip, and blood—
were less predictive of positive surveillance isolation, with a
correlation of one of three patients (33%) for each site.
TABLE 1. Sensitivities of surveillance cultures from different body
sites among patients with recent clinical culture of MDR
A. baumannii (?10 days)
No. of patients
No. with MDR
aOnly discharging wounds were cultured.
bEndotracheal aspirates were obtained only from intubated patients.
1552MARCHAIM ET AL.J. CLIN. MICROBIOL.
Duration of carriage study. During the 3-month study pe-
riod, 30 of 36 patients who had a previous remote clinical
isolation (?6 months prior) of MDR A. baumannii and were
readmitted to TASMC agreed to participate in the study. One
hundred forty samples were obtained from these patients. For
five patients (17%), at least one surveillance isolation yielded
MDR A. baumannii. The mean duration from the first MDR
A. baumannii isolation from a clinical culture was 20 months
(range, 8 to 42), and that from the last isolation was 16 months
(range, 1 to 39). The durations from the last clinical isolation
were similar between those found to be long-term carriers and
those with negative surveillance cultures (Table 2). Risk fac-
tors for prolonged carriage were a bedridden functional state,
disorientation at admission, and status after coronary bypass
surgery, as depicted in Table 2. Other risk factors, including
recent use of immunosuppressants, did not reach significance.
The source of the previous positive isolation and the current
admission diagnosis did not affect the duration of carriage.
Among the cohort of remote clinical MDR A. baumannii
isolations, 7 of 140 sites sampled yielded the organism, i.e.,
three patients had 1 site positive and two patients had 2 sites
positive for MDR A. baumannii. The skin was the source for
four of the isolates, and the pharynx for three. No MDR A.
baumannii was isolated from the nostrils or rectum (30 samples
obtained from each site). The clinical sites that were surveyed,
wounds (17 samples) and endotracheal aspirates (3 samples),
also had no positive isolations.
Genotyping. Among the 52 patients studied (the two cohorts
combined), 7 of the 17 patients with positive surveillance iso-
lations had ?2 positive sites, yielding a total of 16 strains.
Eleven isolates from five patients were genotyped (Fig. 1);
three distinct clones were detected, all known nosocomial
clones that are commonly associated with MDR A. baumannii
infections at TASMC (1). For each of the five patients for
whose samples genotyping was performed, the same clone was
found at two sites; for one patient, an additional clone at a
third site was also found (patient 517) (Fig. 1).
In this surveillance study, we focused on two questions which
are cardinal in limiting the spread of MDR A. baumannii:
which body site should be cultured in order to detect carriage
of MDR A. baumannii, and what is the duration of carriage?
We found that culturing a single body site has very low sensi-
tivity, not higher than 30%, and that even when multiple sites
are sampled the sensitivity of detecting carriers of MDR A.
baumannii reaches only 55%. Sampling multiple body sites is
time-consuming and costly, and it is not suitable for routine use
by clinicians and clinical laboratories. The low sensitivity of
single-site surveillance for MDR A. baumannii is in contrast to
the much higher sensitivities of single-site screening for other
MDR pathogens, e.g., rectal cultures for the detection of car-
riers of vancomycin-resistant enterococci and nasal cultures to
detect carriers of methicillin-resistant Staphylococcus aureus
(16, 29). We also found that MDR A. baumannii may be
carried for long durations, up to 42 months, and that prolonged
carriage affects at least 17% of patients with previous clinical
isolations of MDR A. baumannii. This proportion of long-term
carriers is likely an underestimate due to the limited sensitivity
of surveillance in the detection of carriers (55%) and implies
that prolonged carriage of MDR A. baumannii may affect 30%
of patients with remote clinical isolations.
A combination of several factors may explain the low sensi-
tivity of surveillance cultures. First, it was assumed that all
FIG. 1. Distribution of PFGE clones among patients with ?2 pos-
itive isolates. Lanes: 1, lambda ladder molecular size marker; 2 and 3,
clone H, patient 11, with isolates recovered from pharynx and skin,
respectively; 4 and 5, clone D, patient 502, with isolates recovered from
skin and rectum, respectively; 6 and 7, clone C, patient 515, with
isolates recovered from skin and rectum, respectively; 8 to 10, patient
517, with isolates recovered from sputum (clone D), nose (clone C),
and rectum (clone D), respectively; 11 and 12, clone C, patient 518,
with isolates recovered from pharynx and nose, respectively.
TABLE 2. Several epidemiological parameters and their association
with MDR A. baumannii prolonged carriage in univariate analysis
(n ? 5)
(n ? 25)
Mean age (yr)
No. of male sex
Mo from last MDR
A. baumannii isolation
No. resident at LTCFa
No. with disoriented
Mean Charlson comorbidity
Mean McCabe severity of
No. with recent use of
No. with permanent invasive
No. with recent surgerye
No. with recent invasive
No. taking antibiotics on
No. with indicated status post-
coronary bypass surgery
No. taking chronic insulin
No. receiving chronic
78 ? 12
17.5 ? 16
69 ? 18
16 ? 8.5
aLTCF, long-term care facility.
dIncluding glucocorticoids and anticancerous chemotherapy in the previous
ePrevious 6 months.
VOL. 45, 2007PROLONGED DURATION OF CARRIAGE OF MDR A. BAUMANNII1553
patients from whom MDR A. baumannii was isolated from
clinical cultures within the last 10 days were carriers, and this
may not have been true in all cases, i.e., certain patients may
have had MDR A. baumannii at the infection site only. This is
likely the explanation in very few cases, since both surveillance
sites and clinically relevant sites (draining wounds and endo-
tracheal aspirates from intubated patients) were sampled. Sec-
ond, patients may have received an appropriate antimicrobial
therapy against MDR A. baumannii, which may have eradi-
cated the pathogen prior to our sampling. However, among our
cohort, only two had received such a regimen, as one patient
received cefepime (for which the in vitro results have a ques-
tionable significance if an extended-spectrum-?-lactamase-
producing organism is present), and the second patient re-
ceived, for only 1 day prior to culture, colistin. Therefore, we
believe that this factor did not considerably bias our results.
Third, the sampling and microbiological methods used may not
be sensitive enough to detect MDR A. baumannii bacteria,
particularly if they are present at the sampled body sites in low
concentrations. Although an enrichment method was used af-
ter its superiority to direct culturing onto selective media was
confirmed, this method may still not be sensitive enough. Re-
garding the surveillance skin samples, for example, we can only
postulate that another method which samples a skin surface
area larger than that sampled by swabbing would increase the
yield of the surveillance cultures. Fourth, MDR A. baumannii
may occupy different body sites in different patients.
One might expect that the pharynx would be the best site to
sample for carriage of MDR A. baumannii for a number of
reasons: Acinetobacter spp. were reported to be common com-
mensals in the human pharynx, pneumonia is the most com-
mon clinical syndrome of A. baumannii infections, and the
bacterium is known for its ability to rapidly colonize tracheot-
omies (2). In fact, we found that the pharynx had a low sensi-
tivity (23%) as a surveillance site. The skin was also suggested
to be appropriate site for the surveillance of MDR A. bauman-
nii (14). In our cohort of patients with remote clinical isola-
tions, four of five long-term carriers were identified by skin
sampling. However, the skin had the lowest sensitivity as a
surveillance site for patients with recent clinical isolation
(13.5%), though as we previously mentioned, the appropriate
methodology for obtaining skin samples is yet not well defined.
Isolating MDR A. baumannii from hospitalized patients de-
pends on external ecological variables and risk factors related
to the patients themselves (5). Several previous reports have
discussed the risk factors associated with the development of
MDR A. baumannii infections in hospitalized patients (2, 14,
26). As far as we know, this is the first report that investigates
the risk factors associated with prolonged MDR A. baumannii
carriage. Two of the risk factors identified, a bedridden state
and a disoriented state, were both reported in the past as being
associated with MDR A. baumannii infections in hospitalized
patients (2, 26). Small sample sizes limit the generalizability of
these results and do not allow for meaningful multivariate
analysis. In addition, due to the low sensitivity of surveillance
and the possible resultant misclassification of MDR A. bau-
mannii carriers as noncarriers, the identification of these risk
factors should be interpreted cautiously.
Another study limitation was that the previous MDR A.
baumannii strains of the remote carriers were not available for
genotyping, and therefore we can only assume that remote
carriers remained carriers of the same clone. However, when
we genotyped isolates that were colonizing concurrently differ-
ent body sites, we saw that a given clone can be isolated from
multiple sites and cause different clinical syndromes. In addi-
tion, the clones identified were all familiar, having been pre-
viously associated with MDR A. baumannii outbreaks at
TASMC (1), and therefore it is reasonable to assume that the
long-term carriers acquired the strains in the nosocomial set-
ting, continued to harbor them for several years, and probably
spread them in their local outpatient environment as well.
In conclusion, our study demonstrates that the current meth-
odology to detect MDR A. baumannii carriage is suboptimal
and that persistent carriage of MDR A. baumannii occurs in a
substantial proportion of patients. Improved methods of sur-
veillance are necessary, and long-term contact precautions for
MDR A. baumannii carriers should be considered.
We thank Keren Strauss and Rina Moskovitch for their assistance in
conducting the study.
This study did not receive any financial support.
We have no commercial association or other conflict of interest
regarding any of the products used in the study.
1. Abbo, A., S. Navon-Venezia, O. Hammer-Muntz, T. Krichali, Y. Siegman-
Igra, and Y. Carmeli. 2005. Multidrug-resistant Acinetobacter baumannii.
Emerg. Infect. Dis. 11:22–29.
2. Allen, D. M., and B. J. Hartman. 2004. Acinetobacter species, p. 2631–2635.
In G. L. Mandell, J. E. Bennett, and R. Dolin (ed.), Mandell, Douglas, and
Bennett’s principles and practice of infectious diseases, 6th ed. Churchill
Livingstone, Philadelphia, PA.
3. Berlau, J., H. Aucken, H. Malnick, and T. Pitt. 1999. Distribution of Acin-
etobacter species on skin of healthy humans. Eur. J. Clin. Microbiol. Infect.
4. Bion, J. F., S. A. Edlin, G. Ramsay, S. McCabe, and I. M. Ledingham. 1985.
Validation of a prognostic score in critically ill patients undergoing transport.
Br. Med. J. (Clin. Res. Ed.) 291:432–434.
5. Bonten, M. J., S. Slaughter, A. W. Ambergen, M. K. Hayden, J. van Voorhis,
C. Nathan, and R. A. Weinstein. 1998. The role of “colonization pressure” in
the spread of vancomycin-resistant enterococci: an important infection con-
trol variable. Arch. Intern. Med. 158:1127–1132.
6. Bou, G., G. Cervero, M. A. Dominguez, C. Quereda, and J. Martinez-
Beltran. 2000. PCR-based DNA fingerprinting (REP-PCR, AP-PCR) and
pulsed-field gel electrophoresis characterization of a nosocomial outbreak
caused by imipenem- and meropenem-resistant Acinetobacter baumannii.
Clin. Microbiol. Infect. 6:635–643.
7. The Brooklyn Antibiotic Resistance Task Force. 2002. The cost of antibiotic
resistance: effect of resistance among Staphylococcus aureus, Klebsiella pneu-
moniae, Acinetobacter baumannii, and Pseudomonas aeruginosa on length of
hospital stay. Infect. Control Hosp. Epidemiol. 23:106–108.
8. Chang, H. C., Y. F. Wei, L. Dijkshoorn, M. Vaneechoutte, C. T. Tang, and T.
C. Chang. 2005. Species-level identification of isolates of the Acinetobacter
calcoaceticus-Acinetobacter baumannii complex by sequence analysis of the
16S–23S rRNA gene spacer region. J. Clin. Microbiol. 43:1632–1639.
9. Chen, H. P., T. L. Chen, C. H. Lai, C. P. Fung, W. W. Wong, K. W. Yu, and
C. Y. Liu. 2005. Predictors of mortality in Acinetobacter baumannii bacte-
remia. J. Microbiol. Immunol. Infect. 38:127–136.
10. Choi, J. Y., Y. S. Park, C. O. Kim, Y. S. Park, H. J. Yoon, S. Y. Shin, Y. A.
Kim, Y. G. Song, D. Yong, K. Lee, and J. M. Kim. 2005. Mortality risk factors
of Acinetobacter baumannii bacteraemia. Intern. Med. J. 35:599–603.
11. Cisneros, J. M., and J. Rodriguez-Bano. 2002. Nosocomial bacteremia due
to Acinetobacter baumannii: epidemiology, clinical features and treatment.
Clin. Microbiol. Infect. 8:687–693.
12. Clinical and Laboratory Standards Institute. 2006. Performance standards
for antimicrobial susceptibility testing; 16th informational supplement. Ap-
proved standard M100–S16. Clinical and Laboratory Standards Institute,
13. Coelho, J., N. Woodford, J. Turton, and D. M. Livermore. 2004. Multiresis-
tant acinetobacter in the UK: how big a threat? J. Hosp. Infect. 58:167–169.
14. Fournier, P. E., and H. Richet. 2006. The epidemiology and control of
Acinetobacter baumannii in health care facilities. Clin. Infect. Dis. 42:692–
1554MARCHAIM ET AL. J. CLIN. MICROBIOL.
15. Gouby, A., M. J. Carles-Nurit, N. Bouziges, G. Bourg, R. Mesnard, and P. J. Download full-text
Bouvet. 1992. Use of pulsed-field gel electrophoresis for investigation of
hospital outbreaks of Acinetobacter baumannii. J. Clin. Microbiol. 30:1588–
16. Hill, R. L., and M. W. Casewell. 1990. Nasal carriage of MRSA: the role of
mupirocin and outlook for resistance. Drugs Exp. Clin. Res. 16:397–402.
17. Jain, R., and L. H. Danziger. 2004. Multidrug-resistant Acinetobacter infec-
tions: an emerging challenge to clinicians. Ann. Pharmacother. 38:1449–
18. Jones, R. N. 2001. Resistance patterns among nosocomial pathogens: trends
over the past few years. Chest 119:397S–404S.
19. Levin, A. S. 2002. Multiresistant Acinetobacter infections: a role for sulbac-
tam combinations in overcoming an emerging worldwide problem. Clin.
Microbiol. Infect. 8:144–153.
20. Levin, A. S. 2003. Treatment of Acinetobacter spp infections. Expert Opin.
21. Maslow, J., A. Slutsky, and R. Arbeit. 1993. Application of pulsed-field gel
electrophoresis to molecular epidemiology, p. 563–572. In D. Persing, T.
Smith, F. Tenover, and T. White (ed.), Diagnostic molecular microbiology:
principles and applications. American Society for Microbiology, Washington,
22. McGregor, J. C., P. W. Kim, E. N. Perencevich, D. D. Bradham, J. P. Furuno,
K. S. Kaye, J. C. Fink, P. Langenberg, M. C. Roghmann, and A. D. Harris.
2005. Utility of the Chronic Disease Score and Charlson Comorbidity Index
as comorbidity measures for use in epidemiologic studies of antibiotic-resis-
tant organisms. Am. J. Epidemiol. 161:483–493.
23. Paul, M., M. Weinberger, Y. Siegman-Igra, T. Lazarovitch, I. Ostfeld, I.
Boldur, Z. Samra, H. Shula, Y. Carmeli, B. Rubinovitch, and S. Pitlik. 2005.
Acinetobacter baumannii: emergence and spread in Israeli hospitals 1997–
2002. J. Hosp. Infect. 60:256–260.
24. Tenover, F. C., R. D. Arbeit, R. V. Goering, P. A. Mickelsen, B. E. Murray,
D. H. Persing, and B. Swaminathan. 1995. Interpreting chromosomal DNA
restriction patterns produced by pulsed-field gel electrophoresis: criteria for
bacterial strain typing. J. Clin. Microbiol. 33:2233–2239.
25. Theaker, C., B. Azadian, and N. Soni. 2003. The impact of Acinetobacter
baumannii in the intensive care unit. Anaesthesia 58:271–274.
26. Van Looveren, M., and H. Goossens. 2004. Antimicrobial resistance of Acin-
etobacter spp. in Europe. Clin. Microbiol. Infect. 10:684–704.
27. Vila, J., M. A. Marcos, and M. T. Jimenez de Anta. 1996. A comparative
study of different PCR-based DNA fingerprinting techniques for typing of
the Acinetobacter calcoaceticus-A. baumannii complex. J. Med. Microbiol.
28. Villegas, M. V., and A. I. Hartstein. 2003. Acinetobacter outbreaks, 1977–
2000. Infect. Control Hosp. Epidemiol. 24:284–295.
29. Weinstein, J. W., S. Tallapragada, P. Farrel, and L. M. Dembry. 1996.
Comparison of rectal and perirectal swabs for detection of colonization with
vancomycin-resistant enterococci. J. Clin. Microbiol. 34:210–212.
30. Wisplinghoff, H., T. Bischoff, S. M. Tallent, H. Seifert, R. P. Wenzel, and M.
B. Edmond. 2004. Nosocomial bloodstream infections in US hospitals: anal-
ysis of 24,179 cases from a prospective nationwide surveillance study. Clin.
Infect. Dis. 39:309–317.
VOL. 45, 2007 PROLONGED DURATION OF CARRIAGE OF MDR A. BAUMANNII1555