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Antimicrobial Agents and Chemotherapy, December 2001, p. 3334-3340, Vol. 45, No. 12
Microbiology Department, Hospital Donostia,
San Sebastián,1 Microbiology
Department, Residencia Marqués de Valdecilla,
Santander,2 Medical Department,
GlaxoSmithKline, Tres Cantos,3
Microbiology Department, Hospital General Universitario
Gregorio Marañón,4 and
Microbiology Department, Hospital Ramón y
Cajal,6 Madrid, and Instituto Valenciano
de Microbiología, Valencia,5 Spain
Received 27 September 2000/Returned for modification 30 April
2001/Accepted 26 July 2001
A nationwide multicenter susceptibility surveillance study
which included 1,684 Streptococcus pneumoniae and 2,039 S. pyogenes isolates was carried out over 1 year in order
to assess the current resistance patterns for the two most important
gram-positive microorganisms responsible for community-acquired
infections in Spain. Susceptibility testing was done by a broth
microdilution method according to National Committee for Clinical
Laboratory Standards M100-S10 interpretative criteria. For
S. pneumoniae, the prevalences of highly resistant strains
were 5% for amoxicillin and amoxicillin-clavulanic acid; 7% for
cefotaxime; 22% for penicillin; 31% for cefuroxime; 35% for
erythromycin, clarithromycin, and azithromycin; and 42% for cefaclor.
For S. pyogenes, the prevalence of erythromycin resistance
was 20%. Efflux was encountered in 90% of S. pyogenes and
5% of S. pneumoniae isolates that exhibited erythromycin
resistance. Erythromycin resistance was associated with
clarithromycin and azithromycin in both species, regardless of
phenotype. Despite the different nature of the mechanisms of
resistance, a positive correlation (r = 0.612) between
the two species in the prevalence of erythromycin resistance was found
in site-by-site comparisons, suggesting some kind of link with
antibiotic consumption. Regarding ciprofloxacin, the MIC was Antibiotic agents can select
resistant microorganisms (18), and clinically
important bacteria involved in respiratory tract infections are rapidly
developing resistance to common therapeutic options, as is the case for
Streptococcus pneumoniae (13) and S. pyogenes (24). Decreased susceptibility to macrolides
in S. pyogenes (2) and to In addition to links between macrolide consumption and erythromycin
resistance in S. pyogenes (11, 24) and
consumption of Our group has undertaken several studies in which we have described the
pattern of resistance of S. pneumoniae and S. pyogenes to different antibiotics commonly used in Spain (2,
3) and reported the ecological relationship of the erythromycin
resistance rates for both species (9). In this study, we
report the current rates of resistance and further explore inter- and
intraspecies ecological relationships, in light of new S. pneumoniae breakpoints.
Surveillance studies play a key role in tailoring antibiotic
prescriptions in screened geographical areas. They are even more important when there is a need to provide awareness of recent changes
in breakpoints based on pharmacokinetic and pharmacodynamic data for
S. pneumoniae (19, 20) and how they affect its
prevalence of resistance.
Consecutive clinical isolates collected between November 1998 and October 1999 from patients with community-acquired respiratory infections (namely, acute pharyngitis caused by S. pyogenes
and acute otitis media, acute exacerbations of chronic bronchitis, and
pneumonia caused by S. pneumoniae) were collected by 17 university hospitals selected on the basis of population and
geographical location in Spain. The demographic information submitted
for each isolate included specimen collection date, specimen source,
hospital ward, and unit of care.
At each center, isolates kept at Susceptibility testing was performed using double dilutions by a
semiautomated microdilution method with custom-dried 96-well trays
(Sensititre; Trek Diagnostics Inc., Westlake, Ohio) and Mueller-Hinton
broth supplemented with 3% lysed horse blood according to the
guidelines of the National Committee for Clinical Laboratory Standards
(NCCLS) (20) and with a final inoculum of 5 × 105 CFU/ml. Cultures were incubated for 24 h at 35°C
in ambient air with 11 antimicrobial agents (penicillin, amoxicillin,
amoxicillin-clavulanate [2:1], cefaclor, cefuroxime, cefixime,
cefotaxime, erythromycin, clarithromycin, azithromycin, and
ciprofloxacin) selected on the basis of common empiric therapy options
in Spain. S. pneumoniae ATCC 49619 and Escherichia
coli ATCC 35218 were used as control strains. Breakpoints used
were those recommended by NCCLS (NCCLS document M100-S10)
(20). An arbitrary breakpoint for resistance to
ciprofloxacin of The mechanism of resistance to erythromycin was evaluated with a
double-diffusion disk test as described elsewhere (26) with erythromycin (15 µg) and clindamycin (2 µg) disks placed 20 mm
apart on 5% defibrinated horse blood agar and incubated overnight at
35°C in a 5% carbon dioxide atmosphere. After incubation, the
presence or absence of blunting in the zone of inhibition of the
clindamycin disk was recorded (22). If the clindamycin inhibition zone was blunted toward the erythromycin disk, the strain
was interpreted as clindamycin inducible. Resultant phenotype patterns
were clindamycin-sensitive strains (M phenotype) and clindamycin-resistant or -inducible strains (MLSB phenotype).
The Spearman nonparametric correlation coefficient for the prevalence
of resistance to erythromycin in S. pneumoniae and S. pyogenes and combined erythromycin and penicillin resistance in S. pneumoniae was calculated for each center. Differences in
the prevalence of resistance between different groups, together with calculation of the odds ratios (OR) and the 95% confidence intervals (CI), were assessed by the Twelve percent (201 out of 1,684) of the S. pneumoniae
isolates were from middle ear samples, whereas 88% (1,483 out of
1,684) were from patients suffering from lower respiratory tract (LRT) infections (1,169 [78.8%] from samples such as sputum, bronchial aspirate, or bronchoalveolar lavage fluid and 314 [21.2%] from blood). Eighty-three percent of the S. pneumoniae isolates
were from the adult population. All 2,039 S. pyogenes
isolates were from pharyngeal swabs; 87% were from the pediatric population.
Table 1 shows the in vitro susceptibility
of S. pneumoniae and S. pyogenes isolates.
Overall, a 50.1% prevalence of nonsusceptibility and a 21.7%
prevalence of high-level resistance to penicillin were observed for
S. pneumoniae isolates, with prevalences of resistance of 30 to 40% for macrolides and oral cephalosporins and of about 5 to 7%
for amoxicillin (with or without clavulanate) and cefotaxime. The
prevalence of intermediate resistance was below 9% for all antibiotics
except penicillin (28.3%) and cefotaxime (16.7%). From the viewpoint
of intrinsic activity, cefotaxime proved the most active agent (MIC at
which 90% of the isolates tested were inhibited [MIC90],
1 µg/ml), followed by penicillin and amoxicillin (MIC90,
2 µg/ml). Considering both parameters, the prevalence of resistance
and the MIC90 both cefotaxime and amoxicillin were the most
active agents. Table 2 shows the
percentages of isolates for which the MIC of every drug was increased.
0066-4804/01/$04.00+0 DOI: 10.1128/AAC.45.12.3334-3340.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Antimicrobial Susceptibilities of 1,684 Streptococcus
pneumoniae and 2,039 Streptococcus pyogenes
Isolates and Their Ecological Relationships: Results of a 1-Year
(1998-1999) Multicenter Surveillance Study in Spain
ABSTRACT
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Materials and Methods
Results
Discussion
Appendix
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4
µg/ml for 7% of S. pneumoniae and 3.5% of S. pyogenes isolates. Ciprofloxacin resistance (MIC, 4 µg/ml)
was significantly (P < 0.05) associated with
macrolide resistance in both S. pyogenes and S. pneumoniae and with penicillin nonsusceptibility in S. pneumoniae.
INTRODUCTION
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Abstract
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Materials and Methods
Results
Discussion
Appendix
References
-lactams,
including parenteral broad-spectrum cephalosporins, macrolides, and
ciprofloxacin, in S. pneumoniae (3, 8) has
already been described in Spain. These facts make good-quality data a
necessity for effective interventions to counter the problem of
antimicrobial resistance (18) and to help in designing
prescription guidelines, since there is an established but complex
relationship between antibiotic consumption and prevalence of
resistance (18). This aspect is most important for
community-acquired respiratory tract infections, since up to 85 to 90%
of antibiotics are used in the community and 80% of this proportion is
prescribed to treat this type of infection (14).
-lactams and macrolides and resistance to penicillin
and erythromycin in S. pneumoniae (12),
multiresistance and coselection of resistance (8, 10; C. García-Rey, L. Aguilar, J. García-de-Lomas, and the
Spanish Surveillance Group for Respiratory Pathogens, Abstr. Proc. 3rd
Eur. Congr. Chemother. Span. J. Chemother. 13(Suppl. 2):74, abstr. T161) may also be explained by antibiotic consumption. Although several authors have reported on variations in
the prevalence of resistance in the absence of variations in antibiotic
use (27, 28), the increase in resistance to a given antibiotic (e.g., erythromycin) often relates to the consumption of
that antibiotic or of antibiotics belonging to the same group (11, 24). Because many pneumococcal strains display
multiresistance, it is no wonder that the consumption of a given
antibiotic leads to an increase in resistance to nonrelated antibiotics
(8, 10; Garcia-Rey et al., Abstr. Proc. 3rd Eur. Congr. Chemother).
MATERIALS AND METHODS
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Materials and Methods
Results
Discussion
Appendix
References
70°C were thawed once a
month, seeded onto an enriched transport medium, incubated overnight at
35 to 37°C, and shipped to a central laboratory (Instituto Valenciano
de Microbiología, Valencia, Spain), where compliance of the
isolates with the criteria for inclusion in the study was checked.
Confirmation of the identification of isolates was provided by positive
bile solubility and inhibition by optochin for S. pneumoniae
and serogroup A immunoagglutination (Streptex; Murex, Chantillon,
France) for S. pyogenes. Serogrouping of all the
pneumococcal isolates was performed at the reference central laboratory
and the Centro Nacional de Microbiología, Instituto de Salud
Carlos III, Majadahonda, Madrid, Spain, using the Quellung technique (Statens Seruminstitut, Copenhagen, Denmark) (17) and dot
blot analysis (6). Isolates were kept frozen at 70°C
in duplicate until antimicrobial susceptibility testing was performed.
4 µg/ml was used (as it has not been established for S. pneumoniae by NCCLS) as a marker to indicate the
development of quinolone resistance.
2 test with the Yates
correction when necessary. Statistical analyses were carried out using
SPSS version 8.0 for Windows and Epi-Info version 6.04.
RESULTS
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TABLE 1.
In vitro activity of antimicrobial agents against
S. pneumoniae and S. pyogenes isolates
TABLE 2.
MIC distribution for drugs tested against 1,684 pneumococcal isolates collected in Spain from 1998 through 1999
When the prevalence of susceptibility to each of the other antibiotics
of the S. pneumoniae isolates distributed according to their
penicillin susceptibility categories (Table
3) is considered, it can be seen that the
progressive increase in penicillin MICs has less influence on the
activity of amoxicillin (97 and 60% prevalences of susceptibility for
penicillin-intermediate and -resistant strains, respectively) than on
those of cefotaxime (85 and 11% prevalences of susceptibility for
penicillin-intermediate and -resistant isolates, respectively),
macrolides (40% prevalence of susceptibility for both
penicillin-intermediate and -resistant isolates), or oral
cephalosporins (0% prevalence of susceptibility for
penicillin-resistant isolates). Nonetheless, within the group of oral
cephalosporins, differences between cefaclor and cefuroxime are evident
for isolates exhibiting penicillin-intermediate resistance, since up to
70 and 35% of these isolates are resistant to the respective
aforementioned antibiotics. All of the -lactam nonsusceptibility and
the majority of the macrolide nonsusceptibility happen to be clustered
among the penicillin-nonsusceptible isolates. Notwithstanding, cefotaxime (and penicillin) is likely to be unfairly judged by considering raw NCCLS breakpoints rather than the proportion of isolates with progressively higher MICs. A simple glance at Table 2
shows that there are fewer isolates for which MICs of cefotaxime are
high than for which amoxicillin MICs are high. Likewise, in terms of
MICs, penicillin behaved in a manner very similar to that of
amoxicillin.
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Significant differences were found regarding erythromycin nonsusceptibility in S. pneumoniae when isolates from patients with otitis were compared to those from patients with LTR infections (46.8 versus 33.2%; OR, 1.76; CI, 1.29 to 2.39; P < 0.01). Within the latter group, isolates from blood exhibited a lower erythromycin resistance rate than isolates from the remaining LRT samples (18.8 versus 37.2%; OR, 2.57; CI, 1.88 to 3.55; P < 0.01). As far as penicillin is concerned, middle ear samples had a significantly higher rate of nonsusceptibility than samples from patients with LRT infections (57.7 versus 49.2%; OR, 1.41; CI, 1.04 to 1.92; P = 0.02); blood samples had a nonsusceptibility rate of 34.1%, and the rate for samples from the respiratory tract was 53.2%. The rank order of penicillin resistance by sample, based on NCCLS breakpoints, was middle ear (27.4%) > respiratory tract (22.4%) > blood (16.5%) (P = 0.01). Likewise, clear differences in erythromycin resistance (48.5 versus 32.2%; OR, 1.98; CI, 1.51 to 2.58; P < 0.01) and penicillin resistance (28.4 versus 20.6%; OR, 1.53; CI, 1.14 to 2.07; P < 0.01) were evident between children and adults for S. pneumoniae.
Regarding S. pyogenes isolates, rates of macrolide
resistance were about 20% (Table 1). No difference in erythromycin
resistance was observed between children and adults (20.1 versus
23.3%), contrary to what was found with S. pneumoniae. As
expected, all S. pyogenes isolates were 100% susceptible to
the -lactam drugs tested, with very low
MIC50/MIC90 values.
The distribution of phenotypes of erythromycin resistance is shown in
Table 4; 95% of the
erythromycin-resistant S. pneumoniae isolates had
constitutive MLSB phenotype, whereas the M phenotype was
predominant (90%) among erythromycin-resistant S. pyogenes isolates.
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When the relationship between erythromycin nonsusceptibility and
penicillin nonsusceptibility in S. pneumoniae was examined on a geographical basis (Fig. 1), a
strong positive correlation (r = 0.784; P < 0.05) between both rates of resistance was observed. Therefore,
centers with a high rate of erythromycin resistance also had a high
rate of penicillin nonsusceptibility.
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When the rates of erythromycin resistance for both species of the same
Streptococcus genus were analyzed from a geographical perspective, it was found that centers with a high resistance rate for
S. pneumoniae also had a high resistance rate for S. pyogenes and vice versa (Fig. 2).
Hence, a fairly good correlation (r = 0.612;
P < 0.05) between rates of erythromycin resistance for
both species was shown on a geographical basis. Interestingly, centers
in northern Spain (Santander, San Sebastián, and Bilbao) had the
lowest rates of erythromycin resistance for S. pyogenes (10, 15, and 16%, respectively) and among the lowest rates for S. pneumoniae (27, 30, and 22%, respectively).
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The distribution by serogroup or serotype for the S. pneumoniae isolates was as follows: ST19 (14.0%), ST6 (10.8%), ST23 (10.1%), ST14 (9.0%), ST3 (8.5%), ST9 (6.4%), and ST15 (4.2%); these values accounted for up to 65% of all isolates.
For 86 pneumococcal isolates (5%), the amoxicillin MIC was 8
µg/ml, and among these, serotype 14 was by far the predominant one
(45.9%), followed by serotypes 6 (17.6%), 9 and 23 (14% each), and
15 (5.8%). More than two-thirds of the isolates were isolated in
northern centers, and only 6% were obtained from southern Spain. Penicillin MICs for these strains were two or three twofold dilutions lower than those of amoxicillin. The prevalence of nonsusceptibility for these 86 isolates was 100% for penicillin,
amoxicillin-clavulanate, cefaclor, cefuroxime, and cefotaxime, whereas
it was 65% for macrolides; the ciprofloxacin MIC was 4 µg/ml for
11.7%. For 21 of the isolates, the amoxicillin MIC was 16 µg/ml.
With these isolates, there was again a clear geographical predominance,
as more than 90% were from northern areas.
For up to 120 pneumococcal isolates (7.1%) and 70 S. pyogenes isolates (3.4%), the ciprofloxacin MIC was 4 µg/ml.
Ciprofloxacin resistance was more prevalent among
erythromycin-nonsusceptible pneumococcal isolates than among
erythromycin-susceptible ones (9.67 versus 5.75%; OR, 1.76; CI, 1.19 to 2.60; P < 0.05). No statistically significant
association between ciprofloxacin and penicillin resistance was found,
although it was seen for penicillin-nonsusceptible isolates versus
susceptible ones (8.4 versus 5.8%; OR, 1.48; CI, 1.01 to 2.20;
P < 0.05). For S. pyogenes, clustering of
ciprofloxacin resistance also was seen for erythromycin-resistant
isolates versus susceptible ones (6.1 versus 2.7%; OR, = 2.29; CI,
1.34 to 3.88; P < 0.05). Ciprofloxacin resistance was
also more prevalent among pneumococcal isolates from adults than among
those from children (7.7 versus 4.2%; OR, 1.9; CI, 1.03 to 3.85;
P < 0.05), but it was not significant (4.1 versus 3.3%; P > 0.05) among S. pyogenes isolates.
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DISCUSSION |
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The prevalence of erythromycin resistance in S. pneumoniae currently remains at 35%, although it seems to have decreased to 20% for S. pyogenes compared to the results of a previous survey (2, 3) (33.7% for pneumococci and 26.7% for S. pyogenes). Participation in this study of three new centers in northern Spain (Santander, San Sebastián, and Bilbao) with very low rates of S. pyogenes erythromycin resistance (10 to 17%) is likely to have biased the mean rate.
With regard to high-level resistance to penicillin in S. pneumoniae, the current prevalence also has apparently decreased to 21.7%, but geographical imbalance in the proportions of resistant strains is very unlikely to have contributed significantly to this decrease.
Qualitative differences in erythromycin resistance were also observed for S. pneumoniae, since a higher rate of the M phenotype was found in Las Palmas (Canary Islands) relative to the entire study population (20 versus 5.6%). The Canary Islands are located approximately 10° south of the Spanish peninsula and close to the African coast. With this single exception, almost 95% of the erythromycin-resistant pneumococcal isolates displayed the MLSB phenotype.
From a quantitative viewpoint (i.e., prevalence of erythromycin resistance), a fairly good positive correlation (r = 0.612) was found between both species of the genus Streptococcus (Fig. 2), as already reported (9). This correlation indicates differential antibiotic consumption as a likely reason, as the species have different mechanisms of erythromycin resistance (constitutive for S. pneumoniae and efflux for S. pyogenes), different population sources (adults and children), and different pathologies (LRT infections and pharyngitis). Apart from the geographical factor, a temporal factor already has been reported in Spain, in which antibiotic consumption over time correlates well with the evolution of resistance in both S. pneumoniae and S. pyogenes (11, 12).
Nevertheless, the assumption that antibiotic consumption relates to resistance in a linear way needs to be made with care. Whether other factors, such as local clonal epidemiological differences (different prevalences of certain M protein types in S. pyogenes or serogroups in S. pneumoniae) or antibiotic pressure selection of strains carrying a more suitable gene trait and consequently "hitchhiking" their remaining genomes, are involved remains to be seen. Addressing such a question is of importance in order to either undertake societal infection control measures or control inappropriate antibiotic use. Erythromycin resistance of S. pyogenes in Spain has been related to the circulation of certain clones in a given area over time (21), which might account for the geographical differences in the prevalences of resistance. Certainly, antibiotic pressure somehow affects this turnover. When the prevalence of erythromycin resistance in S. pyogenes has been traced in a given location, it has varied widely over time (22). Oscillations ranging from 10 to 30% have been common in short follow-up periods. Another example of local oscillations in the prevalence of resistance is provided by the site in Córdoba, which showed a high rate of erythromycin resistance for S. pneumoniae and S. pyogenes (60% for both species) in a previous report (9), whereas in the current surveillance the rate was 30%. In addition to natural fluctuations in the spread of resistance (28), seasonal variations in either resistance rates (2, 3) or clonal turnover also may contribute to the global picture. All these factors may be important, since despite the fact that high resistance rates have been described for areas whose antibiotic consumption has increased (16), a given lower level of resistance has not been immediately seen after a decline in antibiotic use. Mathematical modeling shows that there is a lag until a decrease is perceived, and the declining rate is lower than the ascending rate (1). In addition, the new steady state is reached after a series of temporal oscillations whose intensity, duration, and stability depend on how long this biological lag takes.
In addition to coincident geographical and temporal selection of erythromycin resistance in both species, isolates that accumulate different resistance traits may also play a key role. In this study, amoxicillin nonsusceptibility clustered only in highly penicillin-resistant S. pneumoniae isolates, whereas cephalosporin nonsusceptibility and macrolide nonsusceptibility clustered in both penicillin-intermediate and penicillin-resistant isolates. Hence, it seems that penicillin nonsusceptibility is a better driver of nonsusceptibility for macrolides and cephalosporins than for amoxicillin. The selection of coresistance also occurs on a geographical basis, as shown in Fig. 1.
The fact that amoxicillin (and amoxicillin-clavulanate) now has higher breakpoints based on pharmacodynamic and pharmacokinetic considerations has resulted in a dramatic change in what was previously considered nonsusceptibility. As an example, a study conducted 2 years ago (3) with old NCCLS breakpoints (19) reported a rate of amoxicillin resistance of 23.7%, compared to the current 5.1%. If old breakpoints were now applied, the resultant rate would be the same (24%). These new breakpoints for amoxicillin may create the impression that amoxicillin and amoxicillin-clavulanate are more active in vitro than intravenous penicillin or cefotaxime, as breakpoints for these have not been changed. In any event, there is clinical evidence that amoxicillin and ceftriaxone are useful for the treatment of penicillin- and even cephalosporin-resistant pneumococcal pneumonia (23).
Among the most striking findings were the impressive rates of ciprofloxacin resistance found in S. pneumoniae (7.1%) and S. pyogenes (3.4%), which to our knowledge are the highest rates ever published. These figures were not so surprising for S. pneumoniae in Spain, since high rates of ciprofloxacin resistance have been reported (8, 15) in recent years. In addition, the prevalence of high ciprofloxacin MICs was mainly clustered in erythromycin-nonsusceptible (8, 15) and penicillin-nonsusceptible pneumococcal strains (4, 15). More interesting are the prevalence of ciprofloxacin resistance in S. pyogenes and its association with erythromycin resistance. These associations may explain the presence of high ciprofloxacin MICs in both species in children, who are not usually given fluoroquinolones. Ciprofloxacin resistance is becoming a matter of concern, since recent reports have communicated prevalence rates that might be a warning signal for a future increase in resistance (4, 8, 15). However, ciprofloxacin is not a good indicator for resistance to newer quinolones and does not imply the same findings for all drugs within this family (4, 7).
The existence of 86 strains for which the amoxicillin MIC was 8
µg/ml and the penicillin MICs were two or three twofold dilutions lower than those of amoxicillin is also a matter of concern. As a
matter of fact, this phenomenon was recently reported in France for
strains for which the amoxicillin MIC was 4 µg/ml (5), indicating that high-level resistance to amoxicillin emerged within preexisting penicillin-resistant clones. The geographical north-south gradient in Spain and the predominance of certain serogroups, such as
14, among our amoxicillin-resistant isolates both suggest a strong
clonal relationship. A more detailed study with these isolates is in progress.
Country-based monitoring networks are of great importance in the study of local selection of resistance, coselection of resistance, selection of coresistance and resistance drivers in order to attain the appropriate level of local antibiotic consumption and/or evaluate natural clone fluctuations in the spread of resistance.
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APPENDIX |
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The members of the Spanish Surveillance Group for Respiratory Pathogens are J. Larruskain, Hospital Donostia, San Sebastián; E. Cercenado, Hospital Gregorio Marañón, Madrid; J. Barrón and L. López, Hospital de Cruces, Bilbao; T. Jiménez de Anta and F. Marco, Hospital Clinico Provincial, Barcelona; E. Perea and L. Martínez, Hospital Virgen de la Macarena, Sevilla; C. Latorre and A. Gené, Hospital Sant Joan de Déu, Barcelona; J. A. García-Rodríguez (Study Coordinator) and I. Trujillano, Hospital Clínico Universitario, Salamanca; A. García, S. García, and M. Güeni, Hospital La Paz, Madrid; J. Ruiz and E. Simarro, Hospital Virgen de la Arrixaca, Murcia; C. García-Riestra, B. Regueiro, A. Jato, and M. Prieto, Hospital Clínico Universitario, Santiago de Compostela; C. Rubio and C. García, Hospital Clínico Universitario, Zaragoza; M. de la Rosa, Hospital Virgen de las Nieves, Granada; A. M. Martín and F. Cañas, Hospital Insular, Las Palmas; D. Romero and M. González, Hospital Nuestra Señora de Alarcos, Ciudad Real; J. M. Nogueira, Hospital Dr. Peset, Valencia; M. Casal and A. Ibarra, Hospital Reina Sofia, Córdoba; A. Fenoll and J. Casal, Instituto Carlos III, Madrid; J. J. Granizo, Fundación Jiménez Diaz, Madrid; L. López and C. Gimeno, Instituto Valenciano de Microbiología, Valencia; and R. Dal-Ré, GlaxoSmithKline, Tres Cantos, Madrid.
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ACKNOWLEDGMENT |
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This study was supported by a grant from SmithKline Beecham S. A., Madrid, Spain.
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FOOTNOTES |
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* Corresponding author. Mailing address: Medical Department, GlaxoSmithKline, c/Doctor Severo Ochoa, 2, Parque Tecnologico de Madrid, 28760 Tres Cantos, Madrid, Spain. Phone: 34 91 807 5912. Fax: 34 91 807 0596. E-mail: lorenzo.aguilar-alfaro{at}gsk.com.
The members of the Spanish Surveillance Group for Respiratory
Pathogens are listed in the Appendix.
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REFERENCES |
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Antimicrobial Agents and Chemotherapy, December 2001, p. 3334-3340, Vol. 45, No. 12
0066-4804/01/$04.00+0 DOI: 10.1128/AAC.45.12.3334-3340.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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