Previous Article | Next Article 
Journal of Clinical Microbiology, January 2001, p. 8-13, Vol. 39, No. 1
Department of Clinical Microbiology and
Infection Control, University Hospital Vrije Universiteit, 1007 MB
Amsterdam, The Netherlands
Received 9 May 2000/Returned for modification 27 July 2000/Accepted 18 October 2000
Forty-eight clinical Acinetobacter isolates with
different epidemic behavior were investigated for the presence of
integrons and plasmids and for antibiotic susceptibility. Integrons
were demonstrated in 50% of the strains by an integrase gene PCR.
Epidemic strains of Acinetobacter baumannii were found to
contain significantly more integrons than nonepidemic strains. Also,
the presence of integrons was significantly correlated with
simultaneous resistance to several antibiotics. Plasmids were detected
in 42% of the strains. However, there was no significant correlation
between the numbers of plasmids and integrons in
Acinetobacter species strains, no significant difference in
the number of plasmids between epidemic and nonepidemic A. baumannii strains, and no significant correlation between the
presence of plasmids and antibiotic resistance. Hence, it is likely
that integrons play an important role in antibiotic resistance and
thereby in the epidemic behavior of A. baumannii. Because
the integrase gene PCR identified almost three-quarters of the epidemic
A. baumannii isolates (17 of 23), this seems to be a rapid
and simple technique for the routine screening and identification of
clinical A. baumannii isolates with epidemic potential.
Acinetobacter baumannii
is an important opportunistic pathogen responsible for severe
nosocomial infections, especially in intensive-care-unit (ICU) patients
(3). The majority of infections are of epidemic origin,
and treatment has become difficult because many strains are resistant
to a wide range of antibiotics, including broad-spectrum In recent years, a novel mechanism of resistance gene dissemination
among bacteria has been described (25). This mechanism is
based on the location of these genes on integrons. Integrons are
conserved, transposon-like DNA elements which have the ability to
capture and mobilize gene cassettes. Insertion and excision of these
cassettes occur via a site-specific recombinase that belongs to the
integrase family. A distinguishing feature of an integron is the
presence of three components within the conserved 5' region: (i) an
integrase gene (intI) encoding the IntI integrase, (ii) a
gene (attI) encoding the cassette integration site, and (iii) one or more promoters responsible for the expression of gene
cassettes if present. Based on the sequence of their intI genes, four classes of integrons have been described, three of which
(classes 1 to 3) contain antibiotic resistance gene cassettes. At
present, approximately 60 different gene cassettes have been identified, most of which encode resistance to antibiotics (6, 8,
17, 25). Class 1 integrons are predominantly associated with a
sulI gene as part of a 3'-conserved segment
(25). Integrons of class 2 include transposon
Tn7 and relatives (9, 16). In class 3 only one
integron has been described (2, 21). The majority of
integrons belong to class 1 and have been found predominantly in
clinical isolates of gram-negative bacteria, including
Acinetobacter species (14, 18, 19, 23; M. E. Jones, E. Peters, A. M. Weersink, A. Fluit, and J. Verhoef,
Letter, Lancet 349:1742-1743, 1997). A. baumannii strains may vary considerably in their epidemiological
potential, and those strains that have been known to spread widely and
rapidly among hospitalized patients have been designated epidemic
A. baumannii strains. Antibiotic resistance has been shown
to be one of the factors which can influence the nosocomial
dissemination of A. baumannii (5). In this
study the presence of integrons and plasmids was investigated in a
collection of unrelated epidemic and sporadic Acinetobacter
isolates from different parts of the world. In addition, the
association of integrons and plasmids with antibiotic resistance and
epidemic behavior was determined.
Strains.
The Acinetobacter strains used in the
present study comprise two sets of isolates. The first set consisted of
25 isolates recovered from patients from 25 independent hospital
outbreaks in 11 countries (Table 1).
Acinetobacter strains from The Netherlands were obtained
from recognized nosocomial outbreaks, and strains from other countries
were obtained from reported outbreaks. These epidemic strains were each
isolated from at least three different patients. The second set
consisted of 25 Acinetobacter species strains that were
isolated only once from patients in each outbreak hospital; these
strains were defined as nonepidemic, or sporadic.
0095-1137/01/$04.00+0 DOI: 10.1128/JCM.39.1.8-13.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Identification of Epidemic Strains of
Acinetobacter baumannii by Integrase Gene PCR
ABSTRACT
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
INTRODUCTION
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
-lactams,
aminoglycosides, and fluoroquinolones (13, 20, 24, 27).
Studies of antibiotic resistance mechanisms in A. baumannii
have demonstrated the presence of specific genes located on
transferable plasmids and transposons (1, 22, 26). Natural
transformation has been described in Acinetobacter calcoaceticus, but its role in the genetic spread of antibiotic resistance within clinical A. baumannii isolates has yet to
be defined (15).
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
TABLE 1.
Epidemiological data and results of integron and plasmid
analysis of 50 clinical Acinetobacter species strains used
in this study
Identification of strains. Presumptive identification of the isolates was performed by the analytical profile index procedure (API 20NE system; bioMérieux, Marcy l'Etoile, France). Species identification was confirmed by amplified fragment length polymorphism (AFLP), as described previously (11). All strains belonged to the A. calcoaceticus-A. baumannii complex (A. calcoaceticus [n = 1], A. baumannii [n = 40], Acinetobacter genospecies 3 [n = 5], Acinetobacter genospecies 13 [n = 3]), except for two (1N and 14N) which could not be identified at the species level and were therefore excluded from the final results (Table 1). Of all 25 epidemic strains, 23 were identified as A. baumannii.
Genomic DNA isolation.
DNA was prepared from fresh overnight
cultures grown on Luria-Bertani (LB) agar plates (Difco Laboratories,
Detroit, Mich.) as described previously (4). Extracted DNA
was resolved in 100 µl of TE buffer (10 mM Tris, 1 mM EDTA [pH
8.0]) supplemented with 10 µg of RNase (Sigma, St. Louis, Mo.).
Purified DNA was aliquoted and stored at 
20°C.
PCR amplification. PCR amplifications were carried out in 20-µl volumes containing 5 µl of template DNA, 0.2 mM (each) deoxynucleoside triphosphate (dNTP), 2 µl of 10× PCR buffer, 1 U of Taq polymerase (Perkin-Elmer [PE] Applied Biosystems, Foster City, Calif.), 1.5 mM MgCl2, and 1.25 µM each primer. PCR amplification was performed with the GeneAmp PCR System 9700 thermal cycler (PE Applied Biosystems). Amplification products were resolved by electrophoresis at 120 V for 2 h on 2% agarose gels with 0.5× Tris-borate-EDTA buffer containing ethidium bromide and were visualized under UV light. All PCR amplifications were performed in duplicate.
PCR amplification for the detection of class 1 integron cassettes (integron PCR) was performed with primers 5'CS and 3'CS, as described previously (12). For PCR detection of the IntI1 and IntI2 integrase genes (integrase gene PCR), oligonucleotide primers based on the intI1 and intI2 genes were designed (Table 2). Primers IntIF and IntIR were used to amplify a 160-bp fragment of the intI1 gene. The combination of primers Int2F and Int2R amplified a fragment of 288 bp, specific for the intI2 gene. The positions of the primers relative to the integron are indicated in Fig. 1. PCR amplification of integrase gene type 1 and type 2 was performed simultaneously for 35 cycles: 30 s of denaturation at 94°C, 30 s of annealing at 55°C, and 30 s of extension at 72°C.
|
|
DNA sequencing of PCR products. Template PCR products were purified with the Qiaquick PCR Purification kit (Qiagen, Chatsworth, Calif.). Purified PCR products were sequenced with dye terminators on an ABI 377 automatic sequencer (Applied Biosystems). DNA sequences were compared to the National Center for Biotechnology Information (NCBI) database.
Isolation of plasmids. From each strain, plasmid DNA was prepared in duplicate, as described by Hartstein et al. (10), with minor modifications. Briefly, isolates were grown on LB agar plates at 37°C for 24 h. Cells from half of the plate were suspended in 1.5 ml of a solution containing 2.5 M NaCl-10 mM EDTA (pH 8.0), 250 µl of 0.5% alkyltrimethylammonium bromide (ATAB), 250 µl of 1% Triton X-100, and 200 µl of lysozyme (10 mg/ml). After incubation in a water bath at 56°C for 15 min, protein was extracted with phenol-chloroform-isoamyl alcohol (25:24:1), and plasmid DNA was precipitated with ice-cold isopropanol. The precipitate was collected by centrifugation and dissolved in 80 µl of TAE buffer (0.04 M Tris-acetate, 0.001 M EDTA [pH 8.2]). After addition of 1 µl of RNase (500 µg/ml), the solutions were incubated at 37°C for 30 min. Ten microliters of the samples and 5 µl of running dye were loaded onto the gel and run for 18 h at 25 V. Gels were stained with ethidium bromide and photographed under UV illumination.
Antibiotic susceptibility. MICs of selected antimicrobial agents were determined with the Vitek System (bioMérieux, Vitek, Inc., Hazelwood, Mo.). Thirteen antibiotics were tested: ampicillin, ampicillin-clavulanate, piperacillin-tazobactam, cefuroxime, cefotaxime, ceftazidime, imipenem, meropenem, gentamicin, tobramycin, amikacin, ciprofloxacin, and trimethoprim-sulfamethoxazole. MIC data were interpreted according to the guidelines of the NCCLS.
| |
RESULTS |
|---|
|
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
|
|---|
Epidemiological data for the different strains and hospital outbreaks are shown in Table 1. Almost three-quarters of the outbreaks (18 of 25) occurred in ICUs and affected 3 to more than 100 patients.
Detection of class 1 integrons by integron PCR. For the detection of complete class 1 integrons, PCR amplification was performed with primers for the 5'- and 3'-conserved segments. This PCR also permitted the determination of the size of any inserted gene cassette. Integrons with various insert sizes were found in 44% (22 of 48) of the Acinetobacter species strains. The range of inserted gene cassette sizes detected varied from 800 to 3,000 bp. Sixty-five percent (15 of 23) of epidemic A. baumannii isolates were integron positive. Strikingly, in nonepidemic Acinetobacter species isolates, the frequency of integron carriage was only 30% (7 of 23).
Detection of class 1 and class 2 integrons by integrase gene
PCR.
PCR detection of the intI1 and intI2
genes demonstrated the presence of integrons in two more strains,
compared to the integron PCR. Overall, the integrase gene PCR resulted
in a frequency of integron-positive isolates of 50% (24 of 48). All
the integrons were found in isolates of A. baumannii (24 of
40). Class 1 integrons were detected in 58% (23 of 40) of the A. baumannii isolates, whereas only one A. baumannii
strain (3O) contained a class 2 integron (Fig.
2). The correlation between the presence
of integrons, as determined by integrase gene PCR, and the epidemic
character of the Acinetobacter strains was statistically
significant (P < 0.05).
|
Sequence analysis. To confirm that primers Int1 and Int2 correctly identified the intI1 and intI2 genes, amplification products of strain 1O and 3O were sequenced. The sequences of these products were 100% identical to previously published sequences of the intI1 and intI2 genes.
Detection of plasmids. Plasmids were found in 42% (20 of 48) of the Acinetobacter strains. The distribution of plasmids in epidemic isolates was 36% (9 of 25) versus 48% (11 of 23) for nonepidemic isolates; this difference was not significant. Interestingly, only six isolates of A. baumannii contained both an integron and a plasmid.
Antibiotic susceptibility and integron carriage.
Susceptibility to 13 different antibiotics was related to the presence
or absence of an integron within the Acinetobacter strains.
Table 3 shows the antibiotic
susceptibilities of integron-positive and integron-negative isolates to
each of the antibiotics tested, expressed in terms of the MIC at which
50% of the isolates tested were inhibited (MIC50).
Integron carriage was significantly associated with an increase in
antibiotic resistance. In addition, integron-positive A. baumannii strains showed resistance to a significantly higher number of different antibiotics compared to integron-negative isolates
(Fig. 3). Eighty percent (20 of 25) of
the epidemic strains were resistant to five or more of the antibiotics
tested. Strikingly, all integron-positive strains except one (23 of 24)
showed resistance to five or more of the antibiotics tested. Integron
detection identified 74% (17 of 23) of the epidemic A. baumannii isolates.
|
|
| |
DISCUSSION |
|---|
|
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
|
|---|
The aim of our study was to investigate the possible role of integrons and plasmids in the epidemic behavior of clinical isolates of A. baumannii. The epidemic A. baumannii isolates as well as the sporadic Acinetobacter species strains included in this study were obtained from hospitals in 11 different countries. Almost half of these strains (48%) carried integrons. Integrons, however, were found significantly more often in epidemic A. baumannii strains than in sporadic isolates. Possibly, these genetic structures play an important role in the epidemic behavior of A. baumannii.
Class 1 integrons were the most common integrons found in this collection of A. baumannii isolates. Only one clinical isolate, strain 3O, was found to contain a class 2 integron structure. Other investigators have also found predominantly class 1 integrons in Acinetobacter species (23). A survey by Gonzalez et al., however, demonstrated predominantly class 2 integrons in A. baumannii isolates from Chilean hospitals (7). Possibly the strains from the latter study were more genetically related.
In the present study, two different PCR assays were used to detect either class 1 integrons by amplification of any inserted gene cassette or class 1 and class 2 integrons by detection of the specific intI1 and intI2 genes. The integron PCR could lead to false-negative results because (i) the number of inserted genes in the cassette could exceed the PCR extension capacity, which is optimized for DNA products of less than 2.5 kb; (ii) a strain can possess an integron without a gene cassette; and (iii) class 2 integrons do not contain the sulI gene at the 5'-conserved segment (18). The integrase gene PCR, however, detects both class 1 and class 2 integrons by amplification of two products of specific small sizes irrespective of the heterogeneity of the inserted gene cassettes. The integrase gene PCR was indeed more sensitive than the integron PCR and detected integrons in two outbreak strains which were negative in the integron PCR.
Integron-positive strains were significantly associated with resistance
to multiple antibiotics. This is not surprising, since many antibiotic
resistance gene cassettes encoding resistance to a wide range of
antibiotics have been reported (6). However, this could
not explain resistance to extended-spectrum -lactams because such
integron-encoded resistance genes have never been described. Resistance
to extended-spectrum -lactams could be due to a combination of
integrons and resistance genes located on other genetic structures such
as plasmids (14). The differences in ciprofloxacin
resistance, however, cannot be explained this way, since transferable
quinolone resistance encoded by integrons or plasmids has never been
described. Most likely, changes in outer membranes of integron-positive
Acinetobacter strains, induced by transferable -lactam
resistance, are responsible for these differences. Although plasmids
were detected in a substantial number of strains, no significant
correlations between plasmid carriage and either antibiotic resistance
(data not shown) or epidemic behavior was found. These results indicate
that antibiotic resistance in clinical isolates of A. baumannii is associated particularly with the presence of
integrons. In the strains analyzed in this study, the integrons are
probably not located on plasmids, since only six of the strains
investigated harbored both integrons and plasmids.
The analysis of A. baumannii strains with known epidemic behavior demonstrates that early identification of epidemic strains may be possible by detection of integrons or multiple antibiotic resistance. The integrase gene PCR identified almost 75% of the epidemic A. baumannii strains. Multiple antibiotic resistance, defined as resistance to five or more antibiotics, showed good correlation with the presence of integrons and epidemic behavior of the strains. Susceptibility testing, however, has several disadvantages, including its laboriousness, the need for a pure bacterial culture, and subsequent overnight incubation. Also, the chosen cutoff level of five antibiotics is arbitrary and depends on the choice and the number of the antibiotics tested. PCR mapping of integrons, on the other hand, is a rapid and easy technique which can be performed on a single colony.
Integrons were also found in seven nonepidemic strains, which may be an indication of the epidemic potential of these strains. Another explanation for this finding could be the definition of the epidemic and nonepidemic phenotypes in terms of the capacity to spread to one or more patients. It is well known that many different circumstances, such as infection control measures, antibiotic policy, and susceptibilities of individual patients, can facilitate or prevent the dissemination of bacteria, including A. baumannii.
In conclusion, integrase gene PCR is a rapid, valuable procedure, which can be easily used in routine clinical microbiology laboratories for the detection of integrons in clinical A. baumannii isolates. It seems to be a rapid and simple tool for the routine screening of A. baumannii isolates in order to identify strains with epidemic potentials. This is important for the immediate introduction of specific infection control measures in the hospital setting in order to limit the nosocomial spread of these strains.
| |
ACKNOWLEDGMENTS |
|---|
We are indebted to our colleagues who contributed strains of Acinetobacter to this study. We also thank Nabil Atif for technical assistance.
| |
FOOTNOTES |
|---|
* Corresponding author. Mailing address: University Hospital Vrije Universiteit, P.O. Box 7057, 1007 MB Amsterdam, The Netherlands. Phone: 31-204440552. Fax: 31-204440473. E-mail: p.savelkoul{at}azvu.nl.
Present address: Sint Franciscus Gasthuis, 3004 BA Rotterdam, The Netherlands.
| |
REFERENCES |
|---|
|
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
|
|---|
| 1. |
Amyes, S. G. B., and H.-K. Young.
1996.
Mechanisms of antibiotic resistance in Acinetobacter spp. genetics of resistance, p. 185-223.
In
E. Bergogne-Bérézin, M. L. Joly-Guillou, and K. J. Towner (ed.), Acinetobacter microbiology, epidemiology, infections, management. CRC Press, Boca Raton, Fla.
|
| 2. | Arakawa, Y., M. Murakami, K. Suzuki, H. Ito, R. Wacharotayankun, S. Ohsuka, N. Kato, and M. Ohta. 1995. A novel integron-like element carrying the metallo-beta-lactamase gene blaIMP. Antimicrob. Agents Chemother. 39:1612-1615[Abstract]. |
| 3. | Bergogne-Bérézin, E., and K. J. Towner. 1996. Acinetobacter spp. as nosocomial pathogens: microbiological, clinical, and epidemiological features. Clin. Microbiol. Rev. 9:148-165[Medline]. |
| 4. |
Boom, R.,
C. J. A. Sol,
M. M. M. Salimans,
C. L. Jansen,
P. M. E. Wertheim-van Dillen, and J. van der Noordaa.
1990.
Rapid and simple method for purification of nucleic acids.
J. Clin. Microbiol.
28:495-503 |
| 5. | Dijkshoorn, L., H. Aucken, P. Gerner-Smidt, P. Janssen, M. E. Kaufmann, J. Garaizar, J. Ursing, and T. L. Pitt. 1996. Comparison of outbreak and nonoutbreak Acinetobacter baumannii strains by genotypic and phenotypic methods. J. Clin. Microbiol. 34:1519-1525[Abstract]. |
| 6. | Fluit, A. C., and F. J. Schmitz. 1999. Class 1 integrons, gene cassettes, mobility, and epidemiology. Eur. J. Clin. Microbiol. Infect. Dis. 18:761-770[CrossRef][Medline]. |
| 7. | Gonzalez, G., K. Sossa, H. Bello, M. Dominguez, S. Mella, and R. Zemelman. 1998. Presence of integrons in isolates of different biotypes of Acinetobacter baumannii from Chilean hospitals. FEMS Microbiol. Lett. 161:125-128[CrossRef][Medline]. |
| 8. |
Hall, R. M.,
H. J. Brown,
D. E. Brookes, and H. W. Stokes.
1994.
Integrons found in different locations have identical 5' ends but variable 3' ends.
J. Bacteriol.
176:6286-6294 |
| 9. | Hall, R. M., and C. M. Collis. 1995. Mobile gene cassettes and integrons: capture and spread of genes by site-specific recombination. Mol. Microbiol. 15:593-600[CrossRef][Medline]. |
| 10. | Hartstein, A. I., V. H. Morthland, J. W. Rourke, Jr., J. Freeman, S. Garber, R. Sykes, and A. L. Rashad. 1990. Plasmid DNA fingerprinting of Acinetobacter calcoaceticus subspecies anitratus from intubated and mechanically ventilated patients. Infect. Control Hosp. Epidemiol. 11:531-538[Medline]. |
| 11. |
Koeleman, J. G. M.,
J. Stoof,
D. J. Biesmans,
P. H. M. Savelkoul, and C. M. J. E. Vandenbroucke-Grauls.
1998.
Comparison of amplified ribosomal DNA restriction analysis, random amplified polymorphic DNA analysis, and amplified fragment length polymorphism fingerprinting for identification of Acinetobacter genomic species and typing of Acinetobacter baumannii.
J. Clin. Microbiol.
36:2522-2529 |
| 12. | Levesque, C., L. Piche, C. Larose, and P. H. Roy. 1995. PCR mapping of integrons reveals several novel combinations of resistance genes. Antimicrob. Agents Chemother. 39:185-191[Abstract]. |
| 13. | Marques, M. B., E. S. Brookings, S. A. Moser, P. B. Sonke, and K. B. Waites. 1997. Comparative in vitro antimicrobial susceptibilities of nosocomial isolates of Acinetobacter baumannii and synergistic activities of nine antimicrobial combinations. Antimicrob. Agents Chemother. 41:881-885[Abstract]. |
| 14. |
Martinez-Freijo, P.,
A. C. Fluit,
F. J. Schmitz,
V. S. C. Grek,
J. Verhoef, and M. E. Jones.
1998.
Class I integrons in Gram-negative isolates from different European hospitals and association with decreased susceptibility to multiple antibiotic compounds.
J. Antimicrob. Chemother.
42:689-696 |
| 15. |
Palmen, R., and K. J. Hellingwerf.
1997.
Uptake and processing of DNA by Acinetobacter calcoaceticusa review.
Gene
192:179-190[CrossRef][Medline].
|
| 16. |
Radstrom, P.,
O. Skold,
G. Swedberg,
J. Flensburg,
P. H. Roy, and L. Sundstrom.
1994.
Transposon Tn5090 of plasmid R751, which carries an integron, is related to Tn7, Mu, and the retroelements.
J. Bacteriol.
176:3257-3268 |
| 17. |
Recchia, G. D.,
H. W. Stokes, and R. M. Hall.
1994.
Characterisation of specific and secondary recombination sites recognised by the integron DNA integrase.
Nucleic Acids Res.
22:2071-2078 |
| 18. | Sallen, B., A. Rajoharison, S. Desvarenne, and C. Mabilat. 1995. Molecular epidemiology of integron-associated antibiotic resistance genes in clinical isolates of Enterobacteriaceae. Microb. Drug Resist. 1:195-202[Medline]. |
| 19. | Schmitz, F. J., P. Martinez-Freijo, S. Theis, A. C. Fluit, J. Verhoef, H. P. Heinz, and M. E. Jones. 1999. Prevalence of class 1 integrons and association with decreased antibiotic susceptibility in German gram-negative blood culture isolates. Clin. Microbiol. Infect. 5:496-498[Medline]. |
| 20. |
Seifert, H.,
R. Baginski,
A. Schulze, and G. Pulverer.
1993.
Antimicrobial susceptibility of Acinetobacter species.
Antimicrob. Agents Chemother.
37:750-753 |
| 21. | Senda, K., Y. Arakawa, S. Ichiyama, K. Nakashima, H. Ito, S. Ohsuka, K. Shimokata, N. Kato, and M. Ohta. 1996. PCR detection of metallo-beta-lactamase gene (blaIMP) in gram-negative rods resistant to broad-spectrum beta-lactams. J. Clin. Microbiol. 34:2909-2913[Abstract]. |
| 22. |
Seward, R. J.,
T. Lambert, and K. J. Towner.
1998.
Molecular epidemiology of aminoglycoside resistance in Acinetobacter spp.
J. Med. Microbiol.
47:455-462 |
| 23. | Seward, R. J., and K. J. Towner. 1999. Detection of integrons in worldwide nosocomial isolates of Acinetobacter spp. Clin. Microbiol. Infect. 5:308-318[Medline]. |
| 24. | Shi, Z. Y., P. Y. Liu, Y. Lau, Y. Lin, B. S. Hu, and J. M. Shir. 1996. Antimicrobial susceptibility of clinical isolates of Acinetobacter baumannii. Diagn. Microbiol. Infect. Dis. 24:81-85[CrossRef][Medline]. |
| 25. | Stokes, H. W., and R. M. Hall. 1989. A novel family of potentially mobile DNA elements encoding site-specific gene-integration functions: integrons. Mol. Microbiol. 3:1669-1683[Medline]. |
| 26. | Vahaboglu, H., R. Ozturk, G. Aygun, F. Coskunkan, A. Yaman, A. Kaygusuz, H. Leblebicioglu, I. Balik, K. Aydin, and M. Otkun. 1997. Widespread detection of PER-1-type extended-spectrum beta-lactamases among nosocomial Acinetobacter and Pseudomonas aeruginosa isolates in Turkey: a nationwide multicenter study. Antimicrob. Agents Chemother. 41:2265-2269[Abstract]. (Erratum, 42:484, 1998.) |
| 27. |
Vila, J.,
A. Marcos,
F. Marco,
S. Abdalla,
Y. Vergara,
R. Reig,
R. Gomez-Lus, and T. Jimenez de Anta.
1993.
In vitro antimicrobial production of beta-lactamases, aminoglycoside-modifying enzymes, and chloramphenicol acetyltransferase by and susceptibility of clinical isolates of Acinetobacter baumannii.
Antimicrob. Agents Chemother.
37:138-141 |
Journal of Clinical Microbiology, January 2001, p. 8-13, Vol. 39, No. 1
0095-1137/01/$04.00+0 DOI: 10.1128/JCM.39.1.8-13.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Zong, Z., Partridge, S. R., Iredell, J. R.
(2009). A blaVEB-1 Variant, blaVEB-6, Associated with Repeated Elements in a Complex Genetic Structure. Antimicrob. Agents Chemother.
53: 1693-1697
[Abstract] [Full Text] -
Boo, T. W., Walsh, F., Crowley, B.
(2009). Molecular characterization of carbapenem-resistant Acinetobacter species in an Irish university hospital: predominance of Acinetobacter genomic species 3. J Med Microbiol
58: 209-216
[Abstract] [Full Text] -
Peleg, A. Y., Seifert, H., Paterson, D. L.
(2008). Acinetobacter baumannii: Emergence of a Successful Pathogen. Clin. Microbiol. Rev.
21: 538-582
[Abstract] [Full Text] -
Zhang, R., Yang, L., Cai, J. C., Zhou, H. W., Chen, G.-X.
(2008). High-level carbapenem resistance in a Citrobacter freundii clinical isolate is due to a combination of KPC-2 production and decreased porin expression. J Med Microbiol
57: 332-337
[Abstract] [Full Text] -
Bhattacharjee, A., Sen, M. R., Anupurba, S., Prakash, P., Nath, G.
(2007). Detection of OXA-2 group extended-spectrum-{beta}-lactamase-producing clinical isolates of Escherichia coli from India. J Antimicrob Chemother
60: 703-704
[Full Text] -
Valenzuela, J. K., Thomas, L., Partridge, S. R., van der Reijden, T., Dijkshoorn, L., Iredell, J.
(2007). Horizontal Gene Transfer in a Polyclonal Outbreak of Carbapenem-Resistant Acinetobacter baumannii. J. Clin. Microbiol.
45: 453-460
[Abstract] [Full Text] -
Gu, B., Tong, M., Zhao, W., Liu, G., Ning, M., Pan, S., Zhao, W.
(2007). Prevalence and Characterization of Class I Integrons among Pseudomonas aeruginosa and Acinetobacter baumannii Isolates from Patients in Nanjing, China. J. Clin. Microbiol.
45: 241-243
[Abstract] [Full Text] -
Hujer, K. M., Hujer, A. M., Hulten, E. A., Bajaksouzian, S., Adams, J. M., Donskey, C. J., Ecker, D. J., Massire, C., Eshoo, M. W., Sampath, R., Thomson, J. M., Rather, P. N., Craft, D. W., Fishbain, J. T., Ewell, A. J., Jacobs, M. R., Paterson, D. L., Bonomo, R. A.
(2006). Analysis of Antibiotic Resistance Genes in Multidrug-Resistant Acinetobacter sp. Isolates from Military and Civilian Patients Treated at the Walter Reed Army Medical Center. Antimicrob. Agents Chemother.
50: 4114-4123
[Abstract] [Full Text] -
Turton, J. F., Woodford, N., Glover, J., Yarde, S., Kaufmann, M. E., Pitt, T. L.
(2006). Identification of Acinetobacter baumannii by Detection of the blaOXA-51-like Carbapenemase Gene Intrinsic to This Species.. J. Clin. Microbiol.
44: 2974-2976
[Abstract] [Full Text] -
Turton, J. F., Kaufmann, M. E., Gill, M. J., Pike, R., Scott, P. T., Fishbain, J., Craft, D., Deye, G., Riddell, S., Lindler, L. E., Pitt, T. L.
(2006). Comparison of Acinetobacter baumannii Isolates from the United Kingdom and the United States That Were Associated with Repatriated Casualties of the Iraq Conflict.. J. Clin. Microbiol.
44: 2630-2634
[Abstract] [Full Text] -
Fiett, J., Baraniak, A., Mrowka, A., Fleischer, M., Drulis-Kawa, Z., Naumiuk, L., Samet, A., Hryniewicz, W., Gniadkowski, M.
(2006). Molecular Epidemiology of Acquired-Metallo-{beta}-Lactamase-Producing Bacteria in Poland. Antimicrob. Agents Chemother.
50: 880-886
[Abstract] [Full Text] -
Bartual, S. G., Seifert, H., Hippler, C., Luzon, M. A. D., Wisplinghoff, H., Rodriguez-Valera, F.
(2005). Development of a Multilocus Sequence Typing Scheme for Characterization of Clinical Isolates of Acinetobacter baumannii. J. Clin. Microbiol.
43: 4382-4390
[Abstract] [Full Text] -
Turton, J. F., Kaufmann, M. E., Glover, J., Coelho, J. M., Warner, M., Pike, R., Pitt, T. L.
(2005). Detection and Typing of Integrons in Epidemic Strains of Acinetobacter baumannii Found in the United Kingdom. J. Clin. Microbiol.
43: 3074-3082
[Abstract] [Full Text] -
Nemec, A., Dolzani, L., Brisse, S., van den Broek, P., Dijkshoorn, L.
(2004). Diversity of aminoglycoside-resistance genes and their association with class 1 integrons among strains of pan-European Acinetobacter baumannii clones. J Med Microbiol
53: 1233-1240
[Abstract] [Full Text] -
Zarrilli, R., Crispino, M., Bagattini, M., Barretta, E., Di Popolo, A., Triassi, M., Villari, P.
(2004). Molecular Epidemiology of Sequential Outbreaks of Acinetobacter baumannii in an Intensive Care Unit Shows the Emergence of Carbapenem Resistance. J. Clin. Microbiol.
42: 946-953
[Abstract] [Full Text] -
Corvec, S., Caroff, N., Espaze, E., Giraudeau, C., Drugeon, H., Reynaud, A.
(2003). AmpC cephalosporinase hyperproduction in Acinetobacter baumannii clinical strains. J Antimicrob Chemother
52: 629-635
[Abstract] [Full Text] -
Gombac, F., Riccio, M. L., Rossolini, G. M., Lagatolla, C., Tonin, E., Monti-Bragadin, C., Lavenia, A., Dolzani, L.
(2002). Molecular Characterization of Integrons in Epidemiologically Unrelated Clinical Isolates of Acinetobacter baumannii from Italian Hospitals Reveals a Limited Diversity of Gene Cassette Arrays. Antimicrob. Agents Chemother.
46: 3665-3668
[Abstract] [Full Text]
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Copyright © 2009 by the American Society for Microbiology. For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»