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Journal of Clinical Microbiology, July 1999, p. 2337-2342, Vol. 37, No. 7
0095-1137/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Dissemination of a Chloramphenicol- and
Tetracycline-Resistant but Penicillin-Susceptible Invasive Clone of
Serotype 5 Streptococcus pneumoniae in
Colombia
Mónica
Tamayo,1,2
Raquel
Sá-Leão,1
Ilda
Santos
Sanches,1,3
Elizabeth
Castañeda,2 and
Hermínia
de
Lencastre1,3,4,*
Instituto de Tecnologia Química e
Biológica, Universidade Nova de Lisboa,
Oeiras,1 and Faculdade de Ciências
e Tecnologia, Universidade Nova de Lisboa, Monte da
Caparica,3 Portugal; Grupo de
Microbiología, Instituto Nacional de Salud, Santa Fe de
Bogotá, Colombia2; and The
Rockefeller University, New York, New York4
Received 28 December 1998/Returned for modification 18 February
1999/Accepted 24 March 1999
 |
ABSTRACT |
A national surveillance conducted in Colombia between 1994 and 1996 identified serotype 5 Streptococcus pneumoniae as the second most frequent cause of invasive disease in children younger than
5 years of age. All 43 serotype 5 isolates collected during this period
were shown to be susceptible to penicillin, erythromycin, cefotaxime,
and vancomycin, but most (38 of 43, or 88%) were highly resistant to
chloramphenicol. In order to clarify a possible genetic relatedness
among these isolates, additional microbiological and molecular
characterizations were performed. Most (40 of 43, or 93%) of the
isolates were found to be resistant to tetracycline. Pulsed-field gel
electrophoresis (PFGE) patterns of chromosomal DNAs revealed that all
the 43 isolates were closely related and that 38 of the 43 isolates
were representatives of a "Colombian clone" of S. pneumoniae isolates which were recovered throughout the 3-year
surveillance period from patients in 13 hospitals located in five
Colombian cities. Isolates belonging to this Colombian clone were
resistant to chloramphenicol and tetracycline, hybridized with the
cat and tetM DNA probes in the same 340-kb
SmaI fragment, and had identical PFGE patterns after both
SmaI and ApaI digestions.
| |
TEXT |
Streptococcus pneumoniae
is the leading bacterial cause of childhood pneumonia in the developing
world (10). It is estimated that more than 1 million
children die each year from pneumococcal pneumonia; approximately
one-half of them are less than 1 year old (15). The high
incidence of pneumococcal infections and the increasing emergence of
drug-resistant isolates are the major reasons for the establishment of
surveillance programs.
Since 1994, an epidemiological surveillance study has been conducted in
six Latin American countries in order to identify S. pneumoniae causing invasive disease in children less than 5 years
old (10, 21). The study is part of an initiative (Regional System of Vaccines) by the Pan American Health Organization (PAHO). The
study has already provided important information on the distribution of
invasive pneumococcal serotypes among children less than 5 years old,
on antibiotic susceptibility patterns (21), and on the
genetic relationships among the isolates with diminished susceptibility to penicillin (36). In particular, the work conducted with
324 Colombian pneumococcal isolates showed that the most invasive serotypes in children were, in decreasing order of frequency, 14, 5, 23F, 1, and 6B (5). Diminished susceptibility to penicillin was found in 12% of the isolates and was associated with serotypes 23F
(53.8%), 14 (25.6%), 6B (7.7%), 9V (5.1%), 19F (5.1%), and 34 (2.6%) (5). Pulsed-field gel electrophoresis (PFGE)
analysis of these isolates identified multidrug-resistant epidemic
international clones associated with serotypes 23F and 14, among others
(6). Interestingly, all 43 of the serotype 5 isolates
collected during this period and representing the second most prevalent
group of pneumococci causing invasive disease in Colombian children
were susceptible to penicillin.
The aim of the follow-up study described here was to characterize the
Colombian serotype 5 isolates for epidemiological and genetic
relatedness. The study was carried out at the Instituto de Tecnologia
Química e Biológica as part of a collaborative project
between the Instituto Nacional de Salud in Colombia and the Center for
Molecular Epidemiology in Portugal (35).
Bacterial isolates.
Forty-three Colombian S. pneumoniae serotype 5 invasive isolates were recovered between
March 1994 and December 1996 from children less than 5 years old. The
isolates were selected on the basis of the uniform criteria established
in the PAHO epidemiological surveillance study conducted in six Latin
American countries, including Colombia (5). Most of the
S. pneumoniae isolates were collected in hospitals located
in the three most developed cities in the country, based on the
infrastructure of their health services: 14 isolates were recovered
from 13 hospitals located in Bogotá, 10 isolates were from 3 hospitals in Medellín, and 15 isolates were from 3 hospitals in
Cali. Two provincial towns, Manizales and Pereira, yielded two isolates
each. The pneumococcal isolates were recovered from 40 patients, 33 with pneumonia and 7 with meningitis. All isolates were from sterile
sites: blood (27 isolates), pleural fluid (9 isolates), and
cerebrospinal fluid (7 isolates). From three patients diagnosed with
pneumonia, S. pneumoniae was isolated from both blood and
pleural fluid.
Eight other serotype 5 isolates were also included in the study for
comparison: three isolates from Argentina and four isolates from Brazil
were resistant only to trimethoprim-sulfamethoxazole (TMP-SMZ); the
single isolate from the United States was susceptible to all
antibacterial agents tested.
Antimicrobial susceptibility testing.
MICs of penicillin G,
ceftriaxone, and TMP-SMZ were determined by the broth microdilution
method with cation-adjusted Mueller-Hinton broth (BBL Microbiology
Systems, Cockeysville, Md.) containing 3% lysed horse blood
(26). Mueller-Hinton agar (Difco Laboratories, Detroit,
Mich.) containing 5% sheep blood was used to determine MICs of
chloramphenicol and erythromycin by the E test (20) and to
determine sensitivity to tetracycline and vancomycin by the Kirby-Bauer
disk diffusion method (26). MICs and inhibition zones were
interpreted according to National Committee for Clinical Laboratory
Standards guidelines (26). S. pneumoniae ATCC
49619 was used as the control strain.
PFGE.
Chromosomal DNA was prepared according to a published
procedure (33). Chromosomal DNA was digested with 20 U of
SmaI or 20 U of ApaI (New England Biolabs,
Beverly, Mass.) and PFGE was performed with a CHEF DR-II apparatus
(Bio-Rad, Birmingham, United Kingdom) for 23 h. The assay
parameters were as follows: initial pulse, 5 s; final pulse,
35 s; voltage, 6 V/cm; and temperature, 13°C. Standard
methodologies were used for staining and photographing the gels
(30). Strain R6 of S. pneumoniae and a PFGE
lambda marker (New England Biolabs) were used as molecular weight
standards. The macrorestriction profiles were analyzed by visual
inspection of the patterns by use of the criteria of Tenover et al.
(34): isolates showing six or fewer fragment differences
were considered subtypes of a major pattern.
Southern hybridization with chloramphenicol and tetracycline
probes.
Gels were transferred to Hybond N+ membranes
(Amersham International, Little Chalfont, United Kingdom) by use of a
vacuum blotter (VaguGene XL; Pharmacia, Uppsala, Sweden) as previously
described (8). A 338-bp conserved region internal to the
cat genes belonging to both catpC194
and catpC221 classes and a 1,080-bp region
internal to the tetM gene were prepared as previously
described (24, 25, 27). For probe labeling and
hybridization, an enhanced chemiluminescence nonradioactive labeling
kit (RPN3001; Amersham, Birmingham, United Kingdom) was used according
to the manufacturer's instructions.
Table 1 summarizes the relevant
characteristics of the Colombian isolates, including isolation date,
geographic origin, antibiotic susceptibility patterns, PFGE patterns,
and results of hybridization of SmaI-digested DNA from PFGE
gels with DNA probes. An earlier study (5) had already
established that of the 43 serotype 5 invasive pneumococcal isolates,
all were susceptible to penicillin, erythromycin, cefotaxime, and
vancomycin; the majority (88%) showed resistance to chloramphenicol.
Chloramphenicol is one of the antimicrobial agents of choice for the
treatment of invasive diseases in children in Colombia (5).
Additional susceptibility testing demonstrated that most of the 43 isolates, including the 38 chloramphenicol-resistant isolates, were
also resistant to tetracycline, and a variable proportion were
resistant to TMP-SMZ. Three of the serotype 5 isolates (CLB 32, CLB 33, and CLB 35) were susceptible to all antimicrobial agents tested, and
two isolates (CLB 34 and CLB 43) were resistant only to tetracycline
and not to chloramphenicol. Differences in resistance to TMP-SMZ among
the serotype 5 isolates listed in Table 1 may reflect differences in
local antibiotic use. A single Ile 100-to-Leu mutation in dihydrofolate
reductase is known to be sufficient for trimethoprim resistance in
S. pneumoniae (1), and evidence for the rapid
emergence of resistance upon the introduction of TMP-SMZ into clinical
use has been described (17).
All 38 serotype 5 strains showing resistance to both tetracycline and
chloramphenicol represented a "Colombian clone": a homogeneous
group of
S. pneumoniae isolates which were susceptible to
penicillin
and erythromycin, had a common PFGE pattern (X1) after
SmaI restriction
(Fig.
1A),
and hybridized with the
tetM and
cat DNA probes
in
a common 340-kb DNA fragment (Fig.
1B and C). A conjugative
transposon,
Tn
5253, containing the
cat and
tetM genes has been described for
S. pneumoniae
and may explain the colocalization of the two genes
in the same
SmaI fragment (
2). The same PFGE pattern (X1) was
also identified in isolate CLB 34, which was resistant only to
tetracycline and not to chloramphenicol (lane 16 in Fig.
1A).
The 38 tetracycline- and chloramphenicol-resistant isolates and
isolate CLB 34 also had a common PFGE pattern after restriction
of their chromosomal
DNAs with the endonuclease
ApaI (data not
shown). Table
1
shows that the serotype 5 isolates classified
as the Colombian clone
were widely dispersed in Colombia: they
were recovered in 13 hospitals
located in five cities and were
prevalent throughout the surveillance
period from early 1994 until
late 1996.
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FIG. 1.
PFGE illustrative of the clonal dissemination of the
serotype 5 S. pneumoniae invasive isolates in Colombia. The
restriction enzyme used was SmaI. (A) PFGE subtypes X1 to
X4. Lanes 1 and 20 contain a lambda ladder; lanes 2, 13, and 19 contain
reference strain R6 used as a molecular weight marker. Numbers at left
show molecular sizes in kilobases. Lane 3, CLB 12 (X1); lane 4, CLB 30 (X1); lane 5, CLB 29 (X1); lane 6, CLB 2 (X1); lane 7, CLB 4 (X1); lane
8, CLB 5 (X1); lane 9, CLB 37 (X1); lane 10, CLB 38 (X1); lane 11, CLB
7 (X1); lane 12, CLB 8 (X1); lane 14, CLB 32 (X2); lane 15, CLB 33 (X3); lane 16, CLB 34 (X1); lane 17, CLB 35 (X2); lane 18, CLB 43 (X4).
(B) Hybridization of the same gel with the cat probe.
Chloramphenicol-resistant isolates are in lanes 3 to 12;
chloramphenicol-susceptible isolates are in lanes 14 to 18. (C)
Hybridization of the same gel with the tetM probe.
Tetracycline-resistant isolates are in lanes 3 to 12, 16, and 18;
tetracycline-susceptible isolates are in lanes 14, 15, and 17.
|
|
Because of the genetic homogeneity of the 38 isolates representing the
Colombian clone, a group of additional serotype 5
S. pneumoniae isolates with different antibiotic susceptibility
profiles
and different geographic origins were also examined by PFGE
after
digestion of the chromosomal DNAs with
SmaI and
ApaI. This group
of serotype 5 pneumococci included four
Colombian isolates (CLB
32, CLB 33, CLB 35, and CLB 43), which are
listed in Table
1,
four isolates from Brazil, three isolates from
Argentina, and
one isolate from the United States. Three of the four
Colombian
isolates (CLB 32, CLB 33, and CLB 35) were susceptible to
both
chloramphenicol and tetracycline, while isolate CLB 43 was
resistant
to tetracycline only (Table
1). The four Brazilian and three
Argentinian isolates were susceptible to both chloramphenicol
and
tetracycline but were resistant to TMP-SMZ; the U.S. isolate
was
susceptible to all antimicrobial agents
tested.
A comparison of the PFGE patterns of these additional serotype 5 isolates to the uniform PFGE pattern characteristic of the
Colombian
clone is shown for
SmaI digestion in Fig.
1 (for Colombian
isolates only) and for
ApaI digestion in Fig.
2 (for serotype
5 isolates from several
countries). After
ApaI digestion, all
38 isolates of the
Colombian clone had a common PFGE pattern (Y1),
which is illustrated by
a single representative isolate in lane
2 of Fig.
2. CLB 35 (and CLB
32; data not shown) in lane 3 of
Fig.
2 (PFGE pattern Y2), CLB 33 in
lane 4 (PFGE pattern Y3),
and CLB 43 in lane 5 (PFGE pattern Y4)
differed from the Colombian
clone in three, one, and two DNA bands,
respectively. The three
Argentinian isolates (lanes 6, 7, and 8 of Fig.
2) and three of
the four Brazilian isolates (lanes 11, 12, and 13) had
an identical
and unique PFGE pattern which differed in five bands from
that
of the Colombian clone. The last of the four Brazilian serotype
5 isolates (ST 204 in lane 10 of Fig.
2) differed from the
Argentinian-Brazilian
group in one band only (and differed from the
Colombian clone
in six bands). The single type 5 isolate from the
United States
had a PFGE pattern unrelated to those of any of the other
serotype
5 isolates (the number of DNA band differences was greater
than
12).
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FIG. 2.
PFGE after ApaI restriction of serotype 5 S. pneumoniae invasive isolates from Colombia (CLB),
Argentina (ARG), the United States (PP), and Brazil (ST). Lane 2, CLB
34; lane 3, CLB 35; lane 4, CLB 33; lane 5, CLB 34; lane 6, ARG 30;
lane 7, ARG 314; lane 8, ARG 364; lane 9, PP 20; lane 10, ST 204; lane
11, ST 206; lane 12, ST 207; lane 13, ST 331. Lane 15 contains a lambda
ladder; lanes 1 and 14 contain reference strain R6 used as a molecular
weight marker. Numbers at right show molecular sizes in kilobases.
|
|
Serotype 5
S. pneumoniae was common in the United States and
Europe in the 1930s (
16), but since then, its frequency of
isolation has declined, leading to its virtual disappearance
(
14).
In Spain, serotype 5 pneumococci ranked 6th in order
of frequency
between 1979 and 1989 but only 13th in 1990 to 1996 (
12,
13).
Antibiotic resistance in isolates of this serotype
was seen most
often for tetracycline, sometimes associated with
resistance to
chloramphenicol or general susceptibility to all
antimicrobial
agents. Penicillin resistance has been rare among
serotype 5 isolates
(for a review, see references
13
and
22).
In contrast to the findings in Europe, the United States, and Canada,
serotype 5 (and serotype 1) remained the most frequent
pneumococcal
serotype in Africa (
3,
7,
9) and India (
19)
in
the 1980s and 1990s, and the continued importance of serotypes
5 and 1 in other developing countries, including countries in
South America,
was also documented in recent studies (
31,
32).
In
particular, serotype 5
S. pneumoniae isolates were found to
be the second most frequent causative agents of invasive disease
in
children in Argentina (
28,
29), Chile (
23), and
Uruguay
(
18) and were ranked third in Brazil (
4)
and ninth in Mexico
(
11). These observations led to the
suggestion that serotype
5 should be included in a future protein
conjugate vaccine (
21,
32).
In conclusion, the observations described demonstrate that the great
majority of serotype 5 pneumococcal isolates currently
in circulation
in Colombia represent a unique Colombian clone,
with most isolates
expressing resistance to tetracycline and chloramphenicol
but remaining
susceptible to penicillin. Since these isolates
were all from sterile
sites and also included closely related
serotype 5 bacteria susceptible
to all antimicrobial agents tested,
this
S. pneumoniae
lineage appears to carry all virulence factors
necessary to invade the
human host. It is important to determine
the degree of dispersion of
this clone throughout Latin America
and in other countries where this
serotype is frequently
isolated.
| |
ACKNOWLEDGMENTS |
Support for this work was provided by the CEM/NET initiative
(CEM/NET Project 31 from IBET, contract PRAXIS XXI-2/2.1/BIO/1154/95, and contract PECS/C/SAU/145/95 from JNICT) and by a grant from Fundação Calouste Gulbenkian awarded to H. de Lencastre. R. Sá-Leão was supported by grant BD/4259/96 from PRAXIS XXI
from Fundação para a Ciência e Tecnologia. The work
of M. Tamayo in Portugal was supported by Fundação Calouste
Gulbenkian, Lisbon, Portugal; Support for M. Tamayo in Colombia came
from PAHO, the Canadian Agency for International Development, and the
Instituto Nacional de Salud, Santa Fe de Bogotá, Colombia.
We acknowledge Clara Inês Agudelo and María Victoria
Ovalle from the Instituto Nacional de Salud and Alejandra Corso from the Instituto Nacional de Enfermedades Infecciosas, Buenos Aires, Argentina, for stimulating discussions. We express our gratitude to
Alexander Tomasz of The Rockefeller University, New York, N.Y., for
help in the interpretation of data and writing of the manuscript. Idalina Bonfim from Instituto de Tecnologia Química e
Biológica, Oeiras, Portugal, provided technical assistance in
some of the antibiotic susceptibility testing.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Laboratory of
Microbiology, The Rockefeller University, 1230 York Ave., New York, NY 10021. Phone: (212) 327-8277. Fax: (212) 327-8688. E-mail:
lencash{at}rockvax.rockefeller.edu.
| |
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Journal of Clinical Microbiology, July 1999, p. 2337-2342, Vol. 37, No. 7
0095-1137/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
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