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Journal of Clinical Microbiology, March 1999, p. 758-761, Vol. 37, No. 3
0095-1137/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Spread of Amikacin Resistance in
Acinetobacter baumannii Strains Isolated in Spain Due to an
Epidemic Strain
Jordi
Vila,1,*
Joaquim
Ruiz,1
Margarita
Navia,1
Berta
Becerril,2
Isabel
Garcia,3
Sofia
Perea,4
Inmaculada
Lopez-Hernandez,5
Isabel
Alamo,6
Frederic
Ballester,7
Anna M.
Planes,8
Jesus
Martinez-Beltran,9 and
Teresa Jimenez
De Anta1
Department de Microbiologia, Institut d'
Investigació Biomèdica August Pi i Sunyer, Hospital
Clínic, Facultat de Medicina, Universitat de Barcelona, 08036 Barcelona,1
Servicio de
Microbiología, Hospital Virgen del Rocio, 41013 Seville,2
Servicio de
Microbiología, Hospital de la Princesa, 28006 Madrid,3
Servicio de Microbiologia,
Hospital 12 de Octubre, 28041 Madrid,4
Departamento de Microbiología y Epidemiología
Infecciosa, Hospital Virgen Macarena, 41008 Seville,5
Servicio de
Microbiología, Hospital Nuestra Señora del Pino, 35005 Las Palmas, Grand Canary Islands,6
Servicio de Microbiología, Hospital de Sant Joan de
Reus, 43201 Reus, Tarragona,7
Servicio
de Microbiología, Hospital del Valle Hebrón, 08035 Barcelona,8 and
Servicio de
Microbiología, Hospital Ramón y Cajal, 28034 Madrid,9 Spain
Received 29 April 1998/Returned for modification 2 July
1998/Accepted 8 December 1998
 |
ABSTRACT |
Sixteen amikacin-resistant clinical Acinetobacter
baumannii isolates from nine different hospitals in Spain were
investigated to determine whether the high incidence of
amikacin-resistant A. baumannii was due to the
dissemination of an amikacin-resistant strain or to the spread of an
amikacin resistance gene. The epidemiological relationship studied by
repetitive extragenic palindromic PCR and low-frequency restriction
analysis of chromosomal DNA showed that the same clone was isolated in
eight of nine hospitals, although other clones were also found. The
strains were studied for the presence of the aph(3')-VIa
and aac(6')-I genes, which encode enzymes which inactivate
amikacin, by PCR. All 16 clinical isolates had positive PCRs with
primers specific for the amplification of the aph(3')-VIa
gene, whereas none had a positive reaction for the amplification of the
aac(6')-I gene. Therefore, the high incidence of amikacin
resistance among clinical A. baumannii isolates in Spain
was mainly due to an epidemic strain, although the spread of the
aph(3')-VI gene cannot be ruled out.
| |
INTRODUCTION |
Several outbreaks of nosocomial
infections caused by amikacin-resistant Acinetobacter
baumannii have been documented (3, 4, 11, 20). The most
frequent cause of resistance to aminoglycosides in A. baumannii is the modification of hydroxyl or amino groups of the
antibiotic by aminoglycoside-modifying enzymes (1, 5-7, 14, 15,
21), although other mechanisms such as diminished permeability or
alteration of the binding sites have been suggested (21).
Until recently, amikacin remained the most active aminoglycoside in the
treatment of infections caused by Acinetobacter spp. The 6'-aminoglycoside-acetylating enzyme found in Acinetobacter
spp. inactivates amikacin (13); however, the most frequently
found amikacin-modifying enzyme in A. baumannii is
aminoglycoside-3'-phosphotransferase VI [APH(3')-VI], a type of
3'-O-phosphotransferase which also inactivates amikacin
(8). Buisson et al. (3) found a significant correlation between amikacin consumption and the emergence of amikacin
resistance mediated by APH(3')-VI in Acinetobacter species. The main purpose of this study was to develop a PCR method for the
detection of the aph(3')-VIa gene and to determine if the spread of amikacin resistance in A. baumannii strains
isolated in nine Spanish hospitals was due to an epidemic strain
carrying the aph(3')-VIa or aac(6')-I gene.
| |
MATERIALS AND METHODS |
Bacterial strains.
Sixteen amikacin-resistant clinical
isolates of A. baumannii were collected from nine Spanish
hospitals (Hospital Clinic, Barcelona; Hospital Valle Hebrón,
Barcelona; Hospital de Sant Joan de Reus, Reus, Tarragona; Hospital
Virgen del Rocio, Seville; Hospital Clinico, Seville; Hospital de La
Princesa, Madrid; Hospital 12 de Octubre, Madrid; Hospital Ramón
y Cajal, Madrid; and Hospital Nuestra Señora [Ntra. Sra.] del
Pino, Las Palmas, Grand Canary Islands). The identification of A. baumannii was performed by standard biochemical reactions by
following the criteria of Bouvet and Grimont (2). Moreover,
all the strains analyzed in this study were causing pneumonia in
patients in the intensive care units of each hospital.
Susceptibility testing.
Susceptibility testing was performed
by using an agar dilution method in accordance with the guidelines
established by the National Committee for Clinical Laboratory Standards
(16). Approximately 104 CFU of each isolate was
inoculated onto freshly prepared media containing serial dilutions of
amikacin (Bristol-Myers Laboratories, Hounslow, United Kingdom) with a
multipoint replicator.
REP-PCR and low-frequency restriction analysis of chromosomal DNA
(PFGE).
The repetitive extragenic palindromic PCR (REP-PCR) was
performed with the primers and under the conditions described
previously (22). Samples (5 µl) of each PCR end product
were analyzed by polyacrylamide gel electrophoresis with Genephor
precast 12.5% polyacrylamide gels run at 600 V and 25 mA. After that,
the gel was stained with silver. The analysis of chromosomal DNA by
digestion with low-frequency-of-cleavage restriction enzymes and
separation of the fragments by pulsed-field gel electrophoresis (PFGE)
was performed with the ApaI enzyme under the conditions
mentioned elsewhere (12).
PCR amplification of the aph(3')-VIa and
aac(6')-I genes.
Two oligonucleotide primers were
designed on the basis of the nucleotide sequence of the
aph(3')-VIa gene in comparison with the sequences of
different phosphotransferases in an attempt to find specific sequences
of this gene which do not anneal with the other genes. These primers
were 5'-ATACAGAGACCACCATACAGT-3' (from nucleotides 140 to
159) and 5'-GGACAATCAATAATAGCAAT-3' (from nucleotides 355 to
374) (Genosys Biotechnologies, Cambridge, United Kingdom). The PCR was
performed as follows. One colony grown on MacConkey agar was
resuspended in 25 µl of sterile distilled water and boiled for 10 min. After a centrifugation step at 15,000 × g for 1 min, 25 µl of the reaction mixture containing 20 mM Tris-HCl (pH
8.8), 100 mM potassium chloride, 3.0 mM magnesium chloride, 0.1%
(wt/vol) gelatin, 400 µM deoxynucleoside triphosphates, and 1 µM
(each) primer was added, together with 2.5 U of Taq
polymerase (BRL, Life Technologies Inc., Gaithersburg, Md.). Each
reaction mixture was overlaid with mineral oil and amplified with the
following temperature profiles: 30 cycles of 94°C for 1 min, 55°C
for 1 min, and 72°C for 1 min. Amplification was performed in a DNA thermal cycler (model 480; Perkin-Elmer Cetus). The amplified DNA
products were resolved by electrophoresis in 1.5% NuSieve and 1%
agarose gels. In order to confirm that the amplified product belongs to
the aph(3')-VIa gene, the fragment was recovered from the
reaction mixture with the QIAquick Spin PCR purification kit (Qiagen,
Chatsworth, Calif.) and processed with a DNA sequencing kit (Taq
DyeDeoxy Terminator Cycle Sequencing Kit; Applied Biosystems, Foster
City, Calif.) and analyzed in an automatic DNA sequencer (model 373A;
Applied Biosystems).
Eight clinical isolates carrying the genes for other aminoglycoside
phosphotransferases were used as controls; they were Escherichia coli carrying the gene for APH(3')-I, E. coli carrying
the gene for APH(3')-II, Enterobacter cloacae carrying the
gene for APH(3')-II, Staphylococcus epidermidis carrying the
gene for APH(3')-II, E. cloacae carrying the gene for
APH(3')-III, Staphylococcus aureus carrying the gene for
APH(3')-IV, and Enterococcus faecalis carrying the gene for
APH(3')-IV.
Detection of the aac(6')-Ib and aac(6')-Ih genes
was performed by PCR by following the procedure described by Ploy et
al. (17).
| |
RESULTS |
The 16 amikacin-resistant clinical A. baumannii
isolates were epidemiologically analyzed by REP-PCR and by
low-frequency-of-cleavage restriction enzyme analysis of chromosomal
DNA and PFGE. The analysis by REP-PCR allowed the distribution of the
strains into five different groups with DNA bands ranging from 200 to
2,000 bp (Fig. 1A). Nine of the 16 strains belonged to the same type (type 1) and came from seven
different hospitals, whereas two strains each were of types 2, 3, and 4 and one strain was of type 5. The strains belonging to type 2 were
isolated in a Madrid hospital and in another hospital in Seville,
whereas strains belonging to type 4 were isolated in two different
hospitals in Seville (Table 1). The
analysis of chromosomal DNA by PFGE confirmed the results obtained by
REP-PCR (Table 1 and Fig. 1B) with one exception. The PFGE pattern of
the strain determined to be of type 5 by REP-PCR had the same PFGE
pattern as the strains determined to be of type 1 by REP-PCR;
therefore, all these strains must be considered the same type (type A
by PFGE). The results were analyzed by following the criteria described
by Tenover et al. (19).
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FIG. 1.
Patterns obtained by REP-PCR (A) and PFGE (B). The
numbers above the lanes indicate the strains. Lane M, DNA molecular
size marker (100-bp DNA Ladder; Life Technologies Inc.).
|
|
For all amikacin-resistant clinical A. baumannii isolates
tested in this study, the amikacin MIC was >32 µg/ml (Table 1). To
investigate whether the resistance was due to the synthesis of the
aminoglycoside-modifying enzyme APH(3')-VIa, a PCR for the
amplification of the aph(3')-VIa gene was used. A DNA
fragment of the expected size of 234 bp, from nucleotides 140 to 374 of the aph(3')-VIa gene, was obtained (Fig.
2A). Its nucleotide sequence showed 100%
homology with that described by Martin et al. (13). This DNA
fragment was not obtained from the other strains which carried the
genes corresponding to four different phosphotransferases (Fig. 2A),
showing that the primers were specific for aph(3')-VIa. All
the strains analyzed in our study were positive for the
aph(3')-VIa gene by PCR (Fig. 2B), whereas when primers
specific for the amplification of the aac(6')-Ib and
aac(6')-Ih genes were used, the genes were not amplified
from any of the strains.
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FIG. 2.
(A) Analysis of PCR-amplified DNA with primers specific
for amplification of aph(3')-VIa. Lanes: 1, E. coli carrying the gene for APH(3')-I; 2, E. coli
carrying the gene for APH(3')-II; 3, E. cloacae carrying the
gene for APH(3')-II; 4, S. epidermidis carrying the gene for
APH(3')-II; 5, E. cloacae carrying the gene for APH(3')-III;
6, S. aureus carrying the gene for APH(3')-IV; 7, E. faecalis carrying the gene for APH(3')-IV; 8, A. baumannii carrying the gene for APH(3')-VIa; and M, DNA molecular
mass marker VI (Boehringer Mannheim, Mannheim, Germany). (B) PCR
analysis of the aph(3')-VIa gene of the amikacin-resistant
clinical A. baumannii isolates studied. Control indicates an
amikacin-susceptible A. baumannii strain used as a negative
control. Lane M, DNA molecular size marker (100-bp DNA Ladder; Life
Technologies Inc.).
|
|
The number of beds in the hospitals from which the strains included in
this study were obtained ranged from 274 to 1,150. All hospitals but
one (Hospital San Joan de Reus, Reus, Tarragona, Spain) have both
oncology and transplant patients. The distribution of the A. baumannii isolates by clinical source was quite similar in all
hospitals, with respiratory specimens being the most common clinical
specimens containing A. baumannii, followed by wound and
urine specimens.
| |
DISCUSSION |
We studied whether the high incidence of amikacin resistance in
A. baumannii strains isolated in Spain was due to the
dissemination of the amikacin resistance gene aph(3')-VIa or
aac(6')-I or to the spread of an amikacin-resistant strain
of A. baumannii. The epidemiological relationship among the
16 selected clinical isolates of A. baumannii studied by
REP-PCR and PFGE showed that clone A (as determined by PFGE) was
isolated from patients in eight of nine hospitals. Therefore, the same
clone has spread throughout Spain, even to the Canary Islands, which
are far from the Spanish peninsula. Moreover, one clone (clone D4)
spread between two hospitals in Seville. Another clone (clone B2)
spread from a hospital in Seville to a hospital in Madrid or vice
versa. Overall, four different clones of A. baumannii were identified.
Of the aminoglycoside-modifying enzymes detected in A. baumannii, so far, only APH(3')-VI and AAC(6')-I confer resistance to amikacin. APH(3')-VI is primarily associated with
Acinetobacter spp. and is less frequently observed in other
gram-negative bacteria (18). The aph(3')-VIa
gene, which encodes APH(3')-VI, has been cloned from A. baumannii (13). APH(3')-VI production is characterized by resistance to kanamycin, neomycin, paromomycin, ribostamycin, butirosin, and gentamicin B, as well as to amikacin and isepamicin (9). AAC(6')-I production confers resistance to amikacin,
netilmicin, sisomicin, and tobramycin. Ten genes, named
aac(6')-Ia to aac(6')-Ij, encoding AAC(6')-I
enzymes have been described (18). Of these genes,
aac(6')-Ib and Aac(6')-Ih have frequently been
found in A. baumannii (17). The resistance
determinant of AAC(6') was apparently chromosomally located
(15), although recently it has been described to be plasmid
mediated (10), and it has been suggested that the
aph(3')-VIa gene could reside on a transposon (9). These genes can therefore be easily transferred among strains carried on these genetic elements, contributing to the spread
of amikacin resistance. In this study, we have developed a PCR for the
specific detection of the aph(3')-VIa gene, and we have
detected this gene in 100% of the amikacin-resistant clinical A. baumannii isolates from different hospitals in different
geographic areas in Spain, whereas these strains did not have a
positive PCR result when primers specific for the aac(6')-Ib
and aac(6')-Ih genes were used. Our data are consistent with
the results of previous studies in which dot blot hybridization was
used (9, 18). In those studies 82.7 and 95% of
amikacin-resistant Acinetobacter strains hybridized with an
aph(3')-VIa probe (9, 18). In part, our results
agree with those of Lambert et al. (9), who showed that in
France the dissemination of amikacin resistance in
Acinetobacter spp. was due to a gene, although the
dissemination of an amikacin-resistant clone is also true in Spain.
PCR for the detection of aminoglycoside-modifying enzymes may play a
major role in delineating the types of genes involved in epidemics, may
help define their modes of transmission, and may make large studies of
the movement of specific resistance determinants during outbreaks of
nosocomial and community-acquired infections possible. In the outbreaks
caused by A. baumannii, the use of antibiotics can
contribute to the persistence and spread of the outbreak. Sometimes the
patients are only colonized with this microorganism and do not require
antimicrobial therapy; therefore, it is important to differentiate
between colonization and infection before therapy is begun. In
conclusion, our study has shown the contribution of the
aph(3')-VIa gene to the incidence of amikacin resistance in
A. baumannii studied by PCR. This, together with the
molecular epidemiological analysis of strains isolated from different
hospitals in Spain, has shown that the dissemination of amikacin
resistance was due to an epidemic strain carrying the
aph(3')-VIa gene and demonstrates how easily this
microorganism is spread from hospital to hospital.
| |
ACKNOWLEDGMENTS |
This work was supported in part by grant SAF97-0091 from Plan
Nacional I+D, Madrid, Spain, and grant FIS 98/0526.
We thank R. Gómez-Lus for supplying us with the strains used as controls.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Laboratori de
Microbiologia, Hospital Clinic, Facultat de Medicina, Universitat de Barcelona, Villarroel, 170, 08036 Barcelona, Spain. Phone:
34-3-2275522. Fax: 34-3-2275454. E-mail:
vila{at}medicina.ub.es.
| |
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Journal of Clinical Microbiology, March 1999, p. 758-761, Vol. 37, No. 3
0095-1137/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
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Abstract
Introduction
