Previous Article | Next Article 
Journal of Clinical Microbiology, October 1999, p. 3384-3386, Vol. 37, No. 10
Microbiology Department,
Received 17 March 1999/Returned for modification 5 June
1999/Accepted 27 June 1999
The relationship between resistance to antibiotics on the part of
Streptococcus pneumoniae and Streptococcus
pyogenes was studied by comparing different prevalences of
resistance among hospitals obtained from a recent microbiological
surveillance of community-acquired respiratory tract infections. A high
correlation for erythromycin resistance was found between S. pneumoniae isolates from lower respiratory tract infections and
S. pyogenes isolates collected from pharyngeal swabs.
Although the reason for the link
between drug prescription practices and antimicrobial resistance has
not been established (2), this phenomenon has been studied
in the context of the geographical association of macrolide resistance
in Streptococcus pneumoniae (3) and longtime
antibiotic consumption and the increase in macrolide resistance in
Streptococcus pyogenes (8). This link was
confirmed by the decrease in macrolide resistance by S. pyogenes following restrictions on macrolide prescriptions in
Finland (12).
In Spain, the consumption of antibiotics has increased in areas where
high resistance to S. pneumoniae has been reported
(9). The increased resistance of S. pyogenes to
macrolides in Spain may be explained in part by the confirmed increase
in macrolide use (1, 4). As the association between
consumption and resistance is ecologically related, it seems logical to
study the relationship between the antimicrobial resistances of two
species of the genus Streptococcus (S. pneumoniae
and S. pyogenes) that are respiratory pathogens and members
of respiratory flora. If the rise in the consumption of antimicrobial
agents increases resistance patterns for both S. pyogenes
and S. pneumoniae, the prevalence of resistance in both
species may be related, despite the different macrolide resistance
phenotypes, constitutive for S. pneumoniae (5)
and phenotype M (presumed efflux) for S. pyogenes
(4).
This article explores the relationship of the prevalence of
erythromycin resistance between S. pneumoniae and S. pyogenes by means of data obtained from a survey carried out with
S. pneumoniae and S. pyogenes isolates between
May 1996 and April 1997 in 11 Spanish hospitals (4, 5).
A total of 914 beta-hemolytic streptococci and 1,113 S. pneumoniae isolates were isolated from community-acquired
respiratory tract infections in 14 Spanish hospitals (4, 5).
Only 11 hospitals which obtained more than 10 S. pyogenes
and 10 S. pneumoniae strains were included in this study, so
787 S. pneumoniae and 786 S. pyogenes isolates
were evaluated (Table 1). In accordance with National Committee for
Clinical Laboratory Standards (NCCLS) breakpoints, S. pyogenes and S. pneumoniae penicillin resistances were
defined as MICs of Statistical analysis was carried out by using SPPS for Windows version
7.5. The Spearman nonparametric correlation coefficient between the
prevalences of resistance to erythromycin on the part of S. pneumoniae and S. pyogenes was calculated for each hospital.
As erythromycin resistance is strongly associated with pediatric
samples in S. pneumoniae (5), and some hospitals
do not have pediatric wards, the crude prevalence was adjusted. For
this purpose, prevalences were adjusted by a direct method
(10). First, a hypothetical standard hospital was designed,
with the total S. pneumoniae population studied used as a
standard, and was distributed into four wards as follows: internal
medicine, intensive care unit, pediatrics, and other (mainly
emergencies). Secondly, crude specific prevalences
(ps) of erythromycin resistance were calculated
for each hospital ward. A specific weight (ws) was calculated for each hospital ward by means of the proportion of
isolates belonging to each ward. For each hospital ward, adjusted specific prevalence was calculated by using the formula
ws × ps. Finally, the adjusted
prevalence for each hospital was defined as the sum of the four
adjusted specific prevalences.
Table 1 shows the number of strains and
the prevalence of erythromycin resistance corresponding to each
hospital center. Phenotype M is the most prevalent phenotype in
S. pyogenes (93%), with 6 and 1% of constitutive and
inducible MLSB phenotype, respectively, whereas for
S. pneumoniae the constitutive mechanism was the most common
(99.6%), with only 0.4% presenting inducible MLSB
phenotype and no strains with M phenotype. All S. pyogenes
isolates included in this study were from pharyngeal swabs, and 61.8%
of samples were collected in pediatric wards. With respect to S. pneumoniae, 84.8% of strains were collected from adult patients,
and 91.9% were collected from lower respiratory tract samples. Overall
resistance to erythromycin was 34.1% for S. pneumoniae and
26.7% for S. pyogenes, with maximal erythromycin resistance
prevalences for S. pneumoniae and S. pyogenes of
59 and 70%, respectively, whereas minimal prevalences were 23 and 5%,
respectively.
No relation was found between penicillin resistance in either species
(0% for S. pyogenes and 37.2% for S. pneumoniae), but hospitals exhibiting a high prevalence of
S. pneumoniae resistance to erythromycin also exhibited a
high prevalence of S. pyogenes resistance to erythromycin.
The relationship between both species' erythromycin is shown by
hospital in Fig. 1. A high correlation coefficient was found (r = 0.75, P < 0.01).
0095-1137/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Is There an Ecological Relationship between Rates
of Antibiotic Resistance of Species of the Genus
Streptococcus?
ABSTRACT
Top
Abstract
Text
References
TEXT
Top
Abstract
Text
References
4 µg/ml and 2 µg/ml, respectively
(9a). Resistance to erythromycin was defined as a MIC of 1
µg/ml for both species (9a). Antibiotic susceptibility was
determined by using a semiautomated microdilution method according to
the NCCLS guidelines, and the mechanism of resistance to erythromycin was evaluated by using a double diffusion disk test with erythromycin (15 µg) and clindamycin (2 µg) disks placed 20 mm apart as
described elsewhere (11, 13).
TABLE 1.
Susceptibility to macrolides of 786 S. pyogenes isolates and 787 S. pneumoniae isolates by
Spanish hospital
View larger version (17K):
[in a new window]
FIG. 1.
Relationship between erythromycin resistance in S. pneumoniae and S. pyogenes by Spanish hospital.
Hospitals: 1, Reina Sofía (Córdoba); 2, Virgen de las
Nieves (Granada); 3, Virgen de la Macarena (Sevilla); 4, Basurto
(Bilbao); 5, La Fe (Valencia); 6, Gregorio Marañón
(Madrid); 7, La Paz (Madrid); 8, Clínico (Salamanca); 9, Xeral
(Santiago de Compostela); 10, Infanta Cristina (Badajoz); 11, Clínico (Zaragoza).
The problem of increased resistance to antibiotics on the part of
community respiratory pathogens is well known. In Spain, penicillin
resistance in S. pneumoniae has increased since 1989 from
44% (7) to 60% in 1996 to 1997 (5). Similarly,
erythromycin resistance increased from 10% in 1985 (7) to
33.7% in 1996 to 1997 (5). Data for S. pyogenes
show an increase in erythromycin resistance from 3% in 1991 to 1992 (6) to 27% in 1996 to 1997 (4), due in part to
the increase of highly resistant strains (MIC, 8 µg/ml). This
increase was attributed to the spread of the M phenotype
(4), and an ecological relation with macrolide consumption
has been described previously (8). The existence of this
type of relationship was also suggested for S. pneumoniae (9). Based on this phenomenon, a relationship between
macrolide resistance in S. pyogenes and S. pneumoniae is suspected.
Despite the ecological nature of the present study, a high correlation between macrolide resistance in S. pyogenes and S. pneumoniae both was found. S. pyogenes isolates are mainly of pediatric origin, from upper respiratory tract infections (pharyngeal swabs), and from a self-limited disease (streptococcal pharyngitis), and exhibit a high prevalence of M phenotype resistance to macrolides. In contrast, S. pneumoniae strains are of adult origin, from lower respiratory tract infections (i.e., sputum and bronchial aspirate) and lung infections (pneumonia and acute exacerbation of chronic bronchitis), and show a high prevalence of constitutive phenotype. Thus, the ecological relation between consumption and resistance seems to warrant further study.
| |
ACKNOWLEDGMENTS |
|---|
This study was supported by a grant from SmithKline Beecham S.A. Spain.
We thank Francisco Soriano and César García-Rey for critically reviewing the manuscript.
| |
FOOTNOTES |
|---|
* Corresponding author. Mailing address: Medical Department, SmithKline Beecham, C/ Valle de la Fuenfría No. 3, 3°-D, 28034 Madrid, Spain. Phone: 34-91-334 52 75. Fax: 34-91-334 51 41. E-mail: lorenzo.aguilar-alfaro{at}sb.com.
Members of the Spanish Surveillance Group for Respiratory Pathogens
are F. Baquero, Ramon y Cajal Hospital, Madrid; J. A. García-Rodríguez, Clinico Universitario Hospital,
Salamanca; E. Cercenado, Gregorio Marañón Hospital, Madrid;
M. Gobernado and N. Diosdado, La Fe Hospital, Valencia; A. García, La Paz Hospital, Madrid; M. de la Rosa and A. Martínez-Brocal, Virgen de las Nieves Hospital, Granada;
M. C. Rubio, Clinico Universitario Hospital, Zaragoza; R. Cisterna and A. Morla, Basurto Hospital, Bilbao; I. Trujillano, Clinico
Universitario Hospital, Salamanca; E. Perea and L. Martínez,
Virgen Macarena Hospital, Sevilla; C. García-Riestra and I. Rodríguez, Xeral de Galicia Hospital, Santiago de Compostela;
M. Casal and A. Ibarra, Reina Sofía Hospital, Córdoba;
A. C. Gómez-García and F. J. Blanco-Palenciano, Infanta Cristina Hospital, Badajoz; C. Gimeno and M. Bermejo, Instituto Valenciano de Microbiología, Valencia; and
R. Dal-Ré, SmithKline Beecham Pharmaceuticals, Madrid.
| |
REFERENCES |
|---|
|
Top
Abstract
Text
References
|
|---|
| 1. | Baquero, F., and the Task Force of the General Direction for Health Planning of the Spanish Ministry of Health. 1996. Antibiotic resistance in Spain: what can be done? Clin. Infect. Dis. 23:819-823[Medline]. |
| 2. |
Baquero, F.
1998.
Trends in antibiotic resistance of respiratory pathogens: an analysis and commentary on a collaborative surveillance study.
J. Antimicrob. Chemother.
38(Suppl. A):117-132 |
| 3. | Baquero, F. 1999. Evolving resistance patterns of Streptococcus pneumoniae: a link with long-acting macrolide consumption? J. Chemother. 11(Suppl. 1):35-43. |
| 4. |
Baquero, F.,
J. A. García-Rodríguez,
J. García-de-Lomas,
L. Aguilar, and the Spanish Surveillance Group for Respiratory Pathogens.
1999.
Antimicrobial resistance of 914 beta-hemolytic streptococci isolated from pharyngeal swabs in Spain: results of a 1-year (1996-1997) multicenter surveillance study.
Antimicrob. Agents Chemother.
43:178-180 |
| 5. |
Baquero, F.,
J. A. García-Rodríguez,
J. García-de-Lomas,
L. Aguilar, and the Spanish Surveillance Group for Respiratory Pathogens.
1999.
Antimicrobial resistance of 1,113 Streptococcus pneumoniae isolates from patients with respiratory tract infections in Spain: results of a 1-year (1996-1997) multicenter surveillance study.
Antimicrob. Agents Chemother.
43:357-359 |
| 6. |
Betriu, C.,
A. Sánchez,
M. Gómez,
A. Cruceyra, and J. J. Picazo.
1993.
Antibiotic susceptibility of group A streptococci: a 6-year follow up study.
Antimicrob. Agents Chemother.
37:1717-1719 |
| 7. | Fenoll, A., C. M. Burgon, R. Muñoz, D. Vicioso, and T. Casal. 1991. Serotype distribution and antimicrobial resistance of Streptococcus pneumoniae isolates causing systemic infections in Spain, 1979-1989. Rev. Infect. Dis. 13:56-60[Medline]. |
| 8. | Granizo, J., L. Aguilar, and R. Dal-Ré. 1998. Ten years Streptococcus pyogenes resistance to macrolides in Spain, in relation to macrolide consumption, p. 99. In Proceedings of the Second International Meeting on the Therapy of the Infections, Florence, Italy, 18-21 November. |
| 9. | Liñares, J., R. Pallarés, T. Alonso, J. L. Pérez, J. Ayats, F. Gudiol, P. F. Villadrich, and R. Martín. 1992. Trends in antimicrobial resistance of clinical isolates of Streptococcus pneumoniae in Bellvitge hospital, Barcelona, Spain (1979-1990). Clin. Infect. Dis. 15:99-105[Medline]. |
| 9a. | National Committee for Clinical Laboratory Standards. 1999. Performance standards for antimicrobial susceptibility testing; ninth informational supplement. M100-S9. National Committee for Clinical Laboratory Standards, Villanova, Pa. |
| 10. | Rothman, K., and S. Greenland. 1998. Measures of effect and measures of association, p. 47-66. In K. Rothman, and S. Greenland (ed.), Modern epidemiology, 2nd ed. Lippincott-Raven Publishers, Philadelphia, Pa. |
| 11. |
Seppälä, H.,
A. Nissinen,
Q. Yu, and P. Huovinen.
1993.
Three different phenotypes of erythromycin-resistant Streptococcus pyogenes in Finland.
J. Antimicrob. Chemother.
32:885-891 |
| 12. |
Seppälä, H.,
T. Klaukka,
J. Vuopio-Varkila,
A. Muotiala,
H. Helenius,
K. Lager, and P. Huovinen.
1997.
The effect of changes in the consumption of macrolide antibiotics on erythromycin resistance in group A streptococci in Finland.
N. Engl. J. Med.
337:441-446 |
| 13. | Sutcliffe, J., A. Tait-Kamradt, and L. Wondrack. 1996. Streptococcus pneumoniae and Streptococcus pyogenes resistant to macrolides but sensitive to clindamycin: a common resistance pattern mediated by an efflux system. Antimicrob. Agents Chemother. 40:1817-1824[Abstract]. |
Journal of Clinical Microbiology, October 1999, p. 3384-3386, Vol. 37, No. 10
0095-1137/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Perez-Trallero, E., Garcia-de-la-Fuente, C., Garcia-Rey, C., Baquero, F., Aguilar, L., Dal-Re, R., Garcia-de-Lomas, J., the Spanish Surveillance Group for Respiratory Pat,
(2005). Geographical and Ecological Analysis of Resistance, Coresistance, and Coupled Resistance to Antimicrobials in Respiratory Pathogenic Bacteria in Spain. Antimicrob. Agents Chemother.
49: 1965-1972
[Abstract] [Full Text] -
Garcia-Rey, C., Aguilar, L., Baquero, F., Casal, J., Martin, J. E.
(2002). Pharmacoepidemiological Analysis of Provincial Differences between Consumption of Macrolides and Rates of Erythromycin Resistance among Streptococcus pyogenes Isolates in Spain. J. Clin. Microbiol.
40: 2959-2963
[Abstract] [Full Text] -
Perez-Trallero, E., Fernandez-Mazarrasa, C., Garcia-Rey, C., Bouza, E., Aguilar, L., Garcia-de-Lomas, J., Baquero, F., The Spanish Surveillance Group for Respiratory Pat,
(2001). 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. Antimicrob. Agents Chemother.
45: 3334-3340
[Abstract] [Full Text] -
Granizo, J. J., Aguilar, L., Casal, J., Dal-Re, R., Baquero, F.
(2000). Streptococcus pyogenes resistance to erythromycin in relation to macrolide consumption in Spain (1986-1997). J Antimicrob Chemother
46: 959-964
[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»