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Journal of Clinical Microbiology, November 1999, p. 3769-3773, Vol. 37, No. 11
Microbiology Laboratory,
Received 16 February 1999/Returned for modification 26 April
1999/Accepted 22 July 1999
During 1994, 10 isolates of extended-spectrum
The incidence of infections caused
by salmonellae other than Salmonella typhi has increased
considerably in many countries (7, 44). The most common
serotypes, isolated from human and animal sources, in the United States
(21, 44), France (10, 27, 30, 42), and Tunisia
(2, 20), are Salmonella enteritidis, Salmonella typhimurium, and Salmonella wien,
respectively. The most prevalent serotypes in Casablanca, Morocco, are
S. typhimurium and S. enteritidis (unpublished
results). In recent years, S. typhimurium strains were
responsible for outbreaks in pediatric units and were often resistant
to multiple antibiotics, including aminopenicillins, gentamicin,
tetracycline, chloramphenicol, and sulfonamides (9, 10, 27,
44).
From February to September 1994, 10 distinct isolates of
extended-spectrum The 12 isolates of S. typhimurium were identified by Gram
stain, by determining biochemical characteristics with the API 20E system (Biomérieux), and by serological identification of somatic (O) and flagellar (H) antigens with commercial antisera (Sanofi Diagnostics Pasteur) according to the Kauffman-White serotyping scheme
(25). All strains were stored frozen at Antibiotic susceptibility testing was performed by a disk diffusion
method on Mueller-Hinton agar and interpreted in accordance with
criteria of the National Committee for Clinical Laboratory Standards
(34). The strains were screened for their resistance to the
following antibiotics (Sanofi Diagnostics Pasteur): ampicillin, amoxicillin-clavulanic acid, cephalothin, imipenem, cefotaxime, ceftazidime, aztreonam, gentamicin, amikacin, netilmicin, tobramycin, chloramphenicol, tetracycline, and trimethoprim-sulfamethoxazole. The
double-disk synergy test was performed with cefotaxime, ceftazidime, aztreonam, and clavulanic acid plus amoxicillin on Mueller-Hinton agar
(24). Escherichia coli ATCC 25922 was used as a
reference strain.
Conjugation experiments were carried out in Luria broth supplemented
with 0.5% sucrose by mixing equal volumes (1 ml) of exponentially growing cultures of donors (S. typhimurium) and the
recipient E. coli K-12 J53-2 resistant to rifampin.
After incubation at 37°C overnight with slow shaking (3),
transconjugants of E. coli were selected on MacConkey agar
supplemented with cefotaxime (1 µg/ml) and rifampin (100 µg/ml).
Extended-spectrum Phage typing was done, as previously described, at the French National
Center for Enteric Molecular Typing (Pasteur Institute, Paris, France)
(15).
Bacterial strains were screened for plasmid DNA by a modification of
the Birnboim-Doly and Ish-Horowicz Bruke extraction procedure (40). Extracted plasmid DNA was electrophoresed on an 0.7%
horizontal agarose gel containing 0.5 µg of ethidium bromide solution
per ml and analyzed under UV illumination.
For ribotyping, total S. typhimurium DNA was extracted as
described by Picard-Pasquier (36). DNA (2 to 5 µg) was
digested with four different endonucleases: PvuII,
BglII, SmaI, and EcoRI (Boehringer
GmbH, Mannheim, Germany) and analyzed by electrophoresis on submarine
ethidium bromide-containing 0.8% agarose gels. Genomic restriction
digests were subjected to Southern blotting on Hybond-N nylon membranes
(Amersham) by the classical procedure of Southern (43).
Ribosomal 16+23S RNA from E. coli (Boehringer) was used as a
probe (16) and was cold-labeled by random oligopriming with
a mixture of hexanucleotides (Pharmacia, Uppsala, Sweden) and cloned
Moloney murine leukemia virus reverse transcriptase (Bethesda Research
Laboratories, Gaithersburg, Md.) in the presence of 0.35 mM DiG-II-dUTP
(digoxigenin-II-deoxyuridine 5'-11 triphosphate; Boehringer).
Chemiluminescence detection procedures were done as described by the
manufacturer (Boehringer) by incubating the membranes in the presence
of an antidigoxigenin antibody linked to alkaline phosphatase and its
substrate, chemiluminescence substrate phenyl-phosphate disodium (CSPD;
Boehringer). Filters were autoradiographed by exposure to X-Omat AR 5 film (Kodak) for 3 h at room temperature. Isolates which differed
by one fragment were considered to be different strains. Each distinct
combination of patterns was used to define a ribotype.
For PFGE, chromosomal DNA was prepared by using the Chef Genomic DNA
Plug kit (Bio-Rad Laboratories, Hercules, Calif.). Chromosomal DNA was
digested overnight at 37°C with 30 U of XbaI in a 250-µl reaction volume. The resulting restriction fragments were then analyzed
on 14- by 20-cm 0.8% agarose gels (CHEF Mapper electrophoresis system;
Bio-Rad Laboratories), stained with ethidium bromide, and visualized by
UV transillumination. Isolates which differed by no more than three
restriction fragment positions were considered to represent subtypes of
a common epidemic strain (45).
Bacterial DNA was also studied by a RAPD procedure, which was adapted
from the method of Williams et al. (51) by using the in-house-synthesized PCR primers 217 d2 (5'GCCCCCAGGGGCACAGT 3'), A3 (5'AGTCAGCCAC 3'), and B1 (5'GTTTCGTCC 3').
The reaction took place in 50 µl of 100 mM Tris-HCI buffer (pH
8.3) containing 50 mM KCl, 4 mM MgCl2, 0.4 mM
deoxynucleoside triphosphate, 3 µM primer, 50 ng of DNA, and 2.5 U of
Taq DNA polymerase (Beckman, Fullerton, Calif.).
Amplification was performed in a DNA thermal cycler (Perkin-Elmer
Cetus, Norwalk, Conn.) programmed for 35 cycles of 1 min at 94°C, 1 min at 36°C, and 2 min at 72°C. Amplification products were
resolved by electrophoresis in a 2% agarose gel and were detected by
staining with ethidium bromide. Isolates which differed by two or more
prominent bands were considered sufficiently divergent to warrant
separate strain designations. Profiles differing from one another by
only one major band or by one or two weak bands were considered minor
variant types representing subtypes of a common epidemic strain
(5, 26).
In the present study, the enzymatic resistance to oxyimino- The combined results of antigenic, biochemical typing and antibiotyping
demonstrated the existence of the same Salmonella strain
with API profile 6704552, serotype 4,5,12:i-1,2, and the same
antibiotype characterized by the production of ESBL and resistance to
gentamicin and trimethoprim-sulfamethoxazole but susceptibility to
chloramphenicol, tetracycline, and quinolones (Table 1). In other
countries, the resistance of Salmonella to several
antibiotics was more worrisome. In the United States, 32% of the 282 human S. typhimurium isolates tested at the Centers for
Disease Control in 1996 were multidrug resistant, including isolates
with a recently emerged resistance to quinolones (23). In
England and Wales, in 1995, 27% of human S. typhimurium
isolates were multidrug resistant and 6% were also resistant to
ciprofloxacin (48).
Another powerful phenotypic typing technique for Salmonella
species is phage typing (13, 44, 50). It has been reported that this technique was the most useful marker for distinguishing clonal groups of S. typhimurium when compared to plasmid
analysis, biotyping, and antibiotic susceptibility pattern
(29). In our study, phage typing discriminated two groups
(Table 1). For most isolates (10 of 12), phage typing correlated with
biotyping and antibiotyping. However, phage typing may be problematic
in ruling out reinfection because of the high prevalence of one or a
few phage types of S. typhimurium in a community. Phage type
may also be modified by type phage-determining plasmids because
acquisition of a plasmid may partially restrict the susceptibility to
the typing bacteriophage (13). Furthermore, the use of this
technique is limited to a few specialized centers. Of the traditional
techniques most accessible to clinical laboratories, i.e., biotyping,
serotyping, and antibiograms, we found that antibiograms worked well in
discriminating between strain S124, the unrelated strain isolated in
1992, and the 12 outbreak-related isolates of S. typhimurium, so an antibiogram can be used as an initial screen to
determine strain relatedness.
Several studies have shown the stability of plasmid profile analysis of
Salmonella species. Thus, plasmid analysis appears to be the
more effective method for grouping strains with the same serotype
obtained from a single outbreak (7, 49). Holmberg et al.
(22) compared plasmid profiles, phage types, and
antibiotypes in the investigation of 20 outbreaks of S. typhimurium infections. In 17 of these 20 outbreaks, a correlation
was found between these three techniques. The most discriminatory
method was plasmid profile analysis in two outbreaks and phage typing
in one outbreak (22). Several investigators reported that
resistance to different antimicrobial agents was mediated by a large
plasmid (2, 7, 13, 20, 31). This plasmid was found in all
our strains (data not shown); the only difference in the plasmid
profiles was the absence of one small plasmid in the isolates from
nurses. However, this may not exclude an epidemiological relationship
between all isolates because plasmids are unstable genetic elements
that can be readily lost or acquired.
Ribotyping has been used for the study of many bacterial species
responsible for nosocomial infections (6, 11) and also for
different species of the genus Salmonella (12, 19, 30, 35). In our study, ribotyping revealed an identical pattern (Fig.
1; Table 2)
for all isolates, including the unrelated strain, S124, by four
different restriction endonucleases, including EcoRI, an
enzyme which has been suggested to be the most discriminative and as
having the most easily defined banding distribution (12, 49). These results suggest that ribotyping is of limited value in
the epidemiological analysis of these Salmonella species.
However, ribotyping with hybridization with the IS200 probe
was more sensitive than phage typing or ribotyping for discriminating
between S. typhimurium isolates because of the wide
diversity of IS200 profiles among S. typhimurium
isolates (30). Our findings also suggest, as reported by
others researchers (12, 33, 35), that ribotyping should be
used in parallel with phage typing, antibiotyping, and plasmid
analysis.
0095-1137/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Characterization of Extended-Spectrum
-Lactamase-Producing Salmonella typhimurium by Phenotypic
and Genotypic Typing Methods
ABSTRACT
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Abstract
Text
References
-lactamase-producing Salmonella typhimurium were
recovered from children transferred to our hospital from two different
centers. Two additional isolates were recovered from two nurses from
one of these centers. The aim of this study was to determine if there
is any relationship between these isolates. The characterization was
done by phenotypic and genotypic methods: biotyping, phage typing,
antibiotic susceptibility pattern determination, plasmid analysis,
ribotyping (by the four endonucleases EcoRI,
SmaI, BglII, and PvuII),
pulsed-field gel electrophoresis (PFGE) of genome macrorestriction
patterns with XbaI, and randomly amplified polymorphic DNA
(RAPD) pattern determination (with the three primers 217 d2, B1, and
A3). The same biotype, the same serotype, and an identical antibiotype
were found. All isolates were resistant to oxyimino--lactams,
gentamicin, tobramycin, and sulfamethoxazole-trimethoprim. All isolates
showed an indistinguishable pattern by ribotyping and very similar
patterns by PFGE and RAPD. The overall results indicated the spread of
a closely related strain of S. typhimurium in children and nurses.
TEXT
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Abstract
Text
References
-lactamase (ESBL)-producing S. typhimurium (S1 to S10) were isolated at the microbiology
laboratory of the Ibn Rochd University Hospital, Casablanca, Morocco,
from children with acute diarrhea and septicemia. These children were
transferred to our hospital from two different centers (center 1 and
center 2). In September 1994, two additional strains of S. typhimurium were isolated from stools of nurses from center 1 (S11
and S12) (Table 1). Because it was the
first time such isolates were isolated in our laboratory and this type
of resistance is rarely associated with the genus Salmonella
(8, 14), and because children are transferred between the
two centers, the aim of this study was to determine if these isolates
belong to the same or to related clones. These isolates were
characterized by phenotypic methods, including biotyping, serotyping,
phage typing, and determination of antibiotic susceptibility patterns,
and by genotypic techniques such as plasmid analysis, ribotyping,
pulsed-field gel electrophoresis (PFGE), and randomly amplified
polymorphic DNA (RAPD).
TABLE 1.
Origin and phenotypic characteristics of outbreak-related
isolates of S. typhimurium
70°C in 20% glycerol and in nutrient agar stab cultures at room temperature. The
type strain, ATCC 43971, and one nonrelated S. typhimurium strain, S124, were studied for comparison.
-lactamase production was confirmed in the
transconjugants by the double-disk diffusion test (24).
-lactam
antibiotics was reported among isolates of S. typhimurium for the first time in our laboratory. The production of ESBL is rarely
associated with the genus Salmonella (8, 14). The first such strains were detected in France in 1984 and 1987 (S. typhimurium), in Tunisia in 1988 (Salmonella wien), in
Algeria in 1990 (Salmonella mbandaka), and in Argentina in
1991 (S. typhimurium) (1, 10, 20, 37). The most
frequent types of ESBLs found in Salmonella species were
SHV-2, CTX-2, CTX-M2, TEM-27, CTX-M5, and PER-1 (1, 8, 20, 31, 37,
49).
View larger version (93K):
[in a new window]
FIG. 1.
Ribotyping profiles after digestion by EcoRI
of S. typhimurium isolates S124, S1 to S12, and type strain
ATCC 43971. Lane M contains molecular size markers.
TABLE 2.
Genotypic characteristics of outbreak-related isolates of
S. typhimurium and the type strain
Genomic macrorestriction fragment analysis by PFGE has been used successfully for many bacterial species (18, 38, 39). This is also true for S. typhi (47) and S. enteritidis (46). However, PFGE analysis of S. typhimurium was rarely done (32, 41). In the present study, an identical pattern, X1, was found for most isolates (in 9 of 12 isolates); the second pattern, X2, was very similar to X1, differing only by one weak band, and with genetic methods, such a difference is not reliable proof for concluding that isolates represent different strains (17, 28, 45) (Fig. 2; Table 2). The disadvantages of PFGE are time-consuming DNA preparation and electrophoresis, costly reagents, and requirement of specialized equipment.
|
RAPD is another powerful typing method. It has the advantages of speed and simplicity. Its stability and reproducibility have been recently reported (4). Its discriminatory power relies on the primer sequences chosen. Its usefulness for S. typhimurium typing has not been well documented. In this study, we selected primers which have been shown to differentiate clones of members of the family Enterobacteriaceae. With primer A3, all isolates (S1 to S12) and S124 yielded identical patterns, whereas with primers 217 d2 and B1, the isolates were highly related or identical, differing by only one band, and were genetically unrelated to S124 and the ATCC type strain (Fig. 3; Table 2).
|
Among phenotypic methods, plasmid analysis and antibiotyping remain interesting for use in the study of S. typhimurium. Among recent genetic methods, RAPD typing seems well adapted to situations in which a rapid comparison of bacterial strains is needed. PFGE is more discriminatory and can be used as a confirmatory method.
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FOOTNOTES |
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* Corresponding author. Mailing address: Faculté de Médecine, Laboratoire de Microbiologie, 19 rue Tarik Bnouzyad, Casablanca BP 9154, Morocco. Phone and fax: (212-2) 26-90-57. E-mail: mohamed.benbachir{at}fmp-uh2c.ac.ma.
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