Original Article
Resistance to Erythromycin in Group A Streptococci
N Engl J Med 1992; 326:292-297January 30, 1992
- Abstract
- Abstract
Background.
The use of erythromycin in Finland nearly tripled from 1979 to 1989. In 1988, we observed an unusually high frequency of resistance to erythromycin in group A streptococci in one geographic region. Because routine testing does not detect the sensitivity of these organisms to antibiotics, we initiated a national study to evaluate the extent of this resistance.
Methods.
We studied 272 isolates of group A streptococci obtained from blood cultures from 1988 through 1990. In 1990 we collected from six regional laboratories 3087 consecutive isolates from throat swabs and 1349 isolates from pus samples. Resistance was indicated by growth on blood agar containing 2 μg of erythromycin per milliliter after incubation in 5 percent carbon dioxide. We also evaluated the clinical importance of erythromycin resistance in a retrospective study of consecutive patients with pharyngitis.
Results.
The frequency of resistance to erythromycin in group A streptococci from blood cultures increased from 4 percent in 1988 to 24 percent in 1990. From January to December 1990, the frequency of resistance in isolates from throat swabs increased from 7 percent to 20 percent, and resistance in isolates from pus increased from 11 percent to 31 percent. In four communities within 50 km of each other, the frequency of erythromycin resistance ranged from 2 to 5 percent to 26 to 44 percent. Several distinct DNA restriction profiles and serotypes were found among resistant isolates from the same area, suggesting a multiclonal origin. The treatment of pharyngitis with erythromycin failed in 9 of 19 patients infected with erythromycin-resistant group A streptococci, as compared with 1 of 26 patients with erythromycin-susceptible isolates (47 percent vs. 4 percent, P = 0.008).
Conclusions.
In Finland since 1988 there has been a rapid and substantial increase in resistance to erythromycin in group A streptococci. The extent of this resistance is particularly serious since there are only a few alternative antibiotics available for peroral treatment of group A streptococcal infections. (N Engl J Med 1992;326: 292–7.)
Media in This Article
Figure 1
Sales of Erythromycin in Finland from 1978 to 1989, Expressed as the Defined Daily Dose per 1000 Inhabitants per Day (DDD/1000/day).Figure 2
Frequency of Resistance to Erythromycin in 3087 Throat-Swab Isolates of Group A Streptococci (Panel A) and 1349 Isolates from Pus Samples (Panel B) in Finland in 1990.Article Activity
- Article
IN the past five years, the importance of group A streptococcal infections has increased in North America and Europe as well as in other parts of the world.1 In Northern Europe, the number of life-threatening infections caused by group A streptococci has increased and caused considerable concern.2 , 3 All group A streptococci are susceptible to penicillin, and the majority are also susceptible to erythromycin and clindamycin. For patients who are allergic to penicillin, erythromycin has been the drug of choice for treating these infections.
Although erythromycin often has gastrointestinal side effects,4 , 5 the drug has been an effective and very safe antimicrobial agent. This experience, combined with the increasing importance of Mycoplasma pneumoniae and Chlamydia pneumoniae as respiratory-tract pathogens,6 7 8 9 has contributed to the increasing use of erythromycin. The sale of erythromycin in Finland increased from 1.1 defined daily doses per 1000 inhabitants per day in 1979 to 3.2 in 1988 (the defined daily dose is 1 g of erythromycin); in 1989 the corresponding figure was 3.0 defined daily doses (Fig. 1Figure 1
Sales of Erythromycin in Finland from 1978 to 1989, Expressed as the Defined Daily Dose per 1000 Inhabitants per Day (DDD/1000/day).).10 11 12 In 1988, erythromycin accounted for 15 percent of the total consumption of antibiotics, and its use was exceeded only by that of tetracyclines (28 percent) and penicillin V (phenoxymethylpenicillin) (21 percent).In 1988 we observed an unexpectedly high frequency of erythromycin-resistant group A streptococcal isolates from throat swabs obtained in the area of Turku, on the southwestern coast of Finland.13 Because clinical-microbiology laboratories do not usually assay the susceptibility of group A streptococci to antibiotics, we postulated that a similar increase might be more widespread but unnoticed. We therefore decided to conduct a nationwide study of erythromycin resistance in group A streptococcal isolates.
Methods
The group A streptococcal isolates from throat-swab and pus samples were collected from the regional microbiologic laboratories of six areas of Finland. After the first signs of increased erythromycin resistance,13 we collected about 50 consecutive throat-swab isolates containing group A streptococci from the six areas in November and December of 1988 and 1989. During 1990, all isolates of group A streptococci from routine throat-swab and pus samples were collected, for a total of 4436 isolates. Beta-hemolytic colonies were identified with commercial latex-agglutination techniques (Streptex, Wellcome, Dartford, United Kingdom, and Phadebact, Pharmacia, Solna, Sweden). Group A streptococcal isolates were then cultured on Müller-Hinton agar (Oxoid, Basingstoke, United Kingdom) containing 5 percent sheep's blood and 2 μg of erythromycin per milliliter and were incubated in an atmosphere containing 5 percent carbon dioxide. In our experience, group A streptococcal isolates can be better classified as resistant or susceptible in such an atmosphere, because the difference between susceptible and resistant populations of organisms at their minimal inhibitory concentration (MIC) is wider and more distinct in carbon dioxide than in ambient air (data not shown). Erythromycin resistance was indicated by growth on a blood-agar plate with an erythromycin concentration of 2 μg per milliliter or more. When cultures are incubated in 5 percent carbon dioxide, this cutoff point correlates well with an MIC of more than 0.5 μg per milliliter on incubation in ambient air; this concentration is recommended as the cutoff point between susceptible and moderately susceptible bacteria by the National Committee for Clinical Laboratory Standards.14
The MIC values were determined with plates whose concentration of erythromycin or clindamycin ranged from 0.12 to 16 μg per milliliter. Incubation was carried out in an atmosphere containing 5 percent carbon dioxide. The bacterial inoculum was prepared according to the guidelines of the National Committee for Clinical Laboratory Standards14 and placed on plates by means of a multipoint inoculator. Staphylococcus aureus American Type Culture Collection (ATCC) 29213, Enterococcus faecalis ATCC 29212, Escherichia coli ATCC 25922, and Streptococcus pyogenes ATCC 10389 were used as controls for testing susceptibility.
Group A streptococci from blood cultures were collected nationwide by the Department of Bacteriology of the National Public Health Institute from 1988 through 1990. Of the 293 isolates, 6 to 9 per year were not received from the regional laboratories; thus, 272 isolates were available for the determination of MIC plate-dilution susceptibility to erythromycin and clindamycin. The erythromycin MICs of isolates from throat swabs and pus samples growing on the blood-agar plates containing erythromycin (2 μg per milliliter) were also determined; 94 percent of the 578 isolates tested were resistant to erythromycin. The clindamycin MICs of 500 pharyngeal group A streptococcal isolates from the Turku area were also determined; the cutoff point used for determining clindamycin resistance was also 2 μg per milliliter or more.
While screening for erythromycin resistance, we followed the local spread of erythromycin-resistant group A streptococci in the Turku area, using a commercial disk-diffusion method (Rosco, Taastrup, Denmark). The plates were incubated in an atmosphere containing 5 percent carbon dioxide. The isolates were defined as resistant or susceptible (the term "susceptible" included isolates that were moderately susceptible) according to the guidelines of the manufacturer. The relevance of the disk test was also determined. Of 228 pharyngeal isolates shown to be susceptible by the disk test, 96 percent were also shown to be susceptible by the MIC plate-dilution test. Similarly, 96 percent of the 75 resistant isolates were resistant according to the MIC plate-dilution test.
The clinical effects of erythromycin and penicillin on the outcome of pharyngitis caused by erythromycin-resistant and erythromycin-susceptible group A streptococci were surveyed at the Pöytyä and Parainen health centers (penicillin was used as a control factor). In Finland, medical care is free of charge and the majority of the population is treated at local health centers. We collected the medical records of all patients from 1988 through 1990 with erythromycin-resistant or erythromycin-susceptiblc group A streptococcal isolates from throat-swab samples (as determined by the disk test). In this study, treatment was considered to have failed clinically or bacteriologically (or both clinically and bacteriologically) if symptoms of infection persisted or the throat culture was still positive for group A streptococci two days after treatment began or three days after it was completed.
To obtain an impression of how widely erythromycin-resistant group A streptococci had spread in Pöytyä, we collected throat-swab samples from children at the local primary school and daycare center who had no symptoms of infection. The samples were cultured immediately on plates with 5 percent sheep's-blood agar, and the MICs of beta-hemolytic streptococcal isolates were determined with the MIC plate-dilution method described above.
The clonal similarity of the group A streptococci was determined by using DNA restriction endonucleases for total digestion of 95 throat-swab or pus isolates randomly chosen from the six laboratories. The DNA was prepared and digested with HindIII (Boehringer–Mannheim, Oriola, Espoo, Finland) as described by Skjold et al.15 and Cleary et al.16 The serotypes of these 95 isolates were also determined. The T type of each isolate was identified by slide agglutination of trypsin-digested suspensions of washed bacterial cells in the presence of type-specific antiserums (Institute of Sera and Vaccines, Sevac, Prague, Czechoslovakia). The types were further identified with the serum opacity reaction of Maxted and Widdowson.17
Figures for the sales of erythromycin in each area were obtained from data based on the Finnish Statistics on Medicines 18 or, for Pöytyä, directly from the local pharmacy.
Fisher's exact test and the chi-square test were used for statistical analysis. A P value below 0.05 was considered to indicate statistical significance.
Results
Resistance of Group A Streptococci to Erythromycin
Blood Cultures
Of the 272 blood-culture isolates available for susceptibility testing, 56 were collected in 1988, 116 in 1989, and 100 in 1990. The frequency of resistance to erythromycin was 4 percent in 1988, 7 percent in 1989, and 24 percent in 1990; the increase in resistance was significant (7 percent vs. 24 percent, P = 0.004). Only two of the blood-culture isolates obtained in 1990 were resistant to clindamycin.
Throat-Swab and Pus Samples
We collected 296 group A streptococcal isolates from throat-swab samples from the six laboratories in November and December 1988 and 310 during the same months in 1989. In 1988 5.4 percent of the isolates were resistant to erythromycin according to the MIC-plate dilution test, and in 1989 4.2 percent. There was no marked variation according to geographic area or year in the frequency of resistance in these samples.
In 1990, 590 of 4436 isolates of group A streptococci from throat-swab or pus samples (13 percent) were found to be resistant to erythromycin; 11 percent of the 3087 isolates from throat swabs were resistant, and 19 percent of the 1349 isolates from pus — a significant difference (P<0.0001) (Table 1Table 1
Erythromycin Resistance of Group A Streptococci Isolated from Throat-Swab and Pus Samples in Six Areas in Finland in 1990.). The monthly frequency of erythromycin resistance among the 3087 pharyngeal isolates ranged from 6.2 to 8.2 percent in the period January to June, to 10 to 20 percent in the period July to December (Fig. 2AFigure 2Frequency of Resistance to Erythromycin in 3087 Throat-Swab Isolates of Group A Streptococci (Panel A) and 1349 Isolates from Pus Samples (Panel B) in Finland in 1990.). Among the 1349 isolates from pus, the frequency of resistance ranged from 9.0 to 11 percent in the period January to March to 12 to 32 percent in the period April to December (Fig. 2B). Resistance to clindamycin was not detected in the 500 pharyngeal isolates studied, all of which were collected from the Turku area.The highest incidence of resistance was found in the Kuopio area, where 29 percent of the throat-swab isolates and 54 percent of the isolates from pus samples were erythromycin-resistant (Table 1); among the 50 isolates studied in 1988 and the 50 studied in 1989, 0 percent and 8 percent, respectively, were erythromycin-resistant. In the southern part of Finland (the areas of Helsinki, Turku, and Tampere), the frequency of resistance in 1990 was intermediate and ranged from 7.7 to 16 percent in isolates from throat-swab samples and from 11 to 12 percent in pus samples. In western and northern Finland (Seinäjoki and Oulu areas), resistance was notably less frequent — i.e., 2.3 to 2.5 percent in throat-swab samples and 2.3 to 8.5 percent in pus samples.
A marked increase in the frequency of erythromycin-resistant group A streptococci was observed in two areas during 1990. In the Turku and Tampere districts, the frequency of resistant throat-swab isolates increased from 7 percent in each district in January 1990 to 19 percent and 24 percent, respectively, in December. The corresponding figures for isolates from pus samples were 19 percent and 12 percent in January and 33 percent and 42 percent in December.
In 1990 we analyzed the local distribution of erythromycin-resistant pharyngeal group A streptococci in the Turku area. Of 1259 isolates, 126 were collected from the city of Turku (January 1990 only), 259 from Kaarina, 154 from Pöytyä, 262 from Parainen, and 458 from other communities. In the cities of Kaarina and Turku, the frequency of resistant isolates was 2 to 5 percent. However, in Pöytyä, 30 km north of Turku, the frequency was no lower than 44 percent, and in Parainen, 15 km south of Turku, the corresponding figure was 26 percent. In the remaining suburban areas, 9 percent of isolates were resistant.
The clonality of erythromycin-resistant group A streptococci was studied by analysis of DNA restriction profiles. Among the 95 isolates, 14 different clones were identified. In Helsinki, 4 different DNA restriction profiles were detected among the 15 isolates. In Turku, 3 profiles were found among 17 isolates; in Tampere, 3 profiles among 20 isolates; in Kuopio, 4 profiles among 22 isolates; in Seinäjoki, 1 profile among 4 isolates; and in Oulu, 3 profiles among 17 isolates. Figure 3Figure 3
DNA Restriction-Endonuclease (HindIII) Profiles of Selected Group A Streptococcal Isolates. shows the variability of the profiles among 14 erythromycin-resistant isolates selected from among the isolates in all areas studied. Although there were some identical restriction profiles among the isolates from different areas, none of the profiles predominated. The serotypes of 35 of the 95 isolates (37 percent) could not be determined. Eight serotypes were identified among the remaining 60 isolates — i.e., T4M4 (27 isolates), T11M12 (9), T28 (9), T22 (6), T12M12 (5), T1M1 (2), T11 (1), and T4 (1).To assess how widespread erythromycin-resistant group A streptococci were among healthy children in Pöytyä, we studied 239 children from a primary school and day-care center. Seven children had pharyngeal cultures that were positive for group A streptococci, and six of the isolates were erythromycin-resistant. We also found 23 isolates of group C streptococci, 9 isolates of group G streptococci, 12 isolates of group F streptococci, and 9 isolates of beta-hemolytic streptococci, none of which could be typed. Only a group G streptococcal isolate was resistant to erythromycin, with an MIC of 2 μg per milliliter.
Treatment of Pharyngitis with Erythromycin
The medical records of 196 patients with throat-swab samples containing erythromycin-resistant group A streptococci were retrieved and studied together with the records of 333 patients with erythromycin-susceptible group A streptococci (Table 2Table 2
Frequency of Failure of Treatment of Group A Streptococcal Pharyngitis.). Erythromycin had been used to treat pharyngitis in 19 of the 196 patients with erythromycin-resistant isolates and in 26 of the 333 patients with erythromycin-susceptible isolates (Table 2). The rate of treatment failure was 47 percent in the former group (9 of 19 patients) and 4 percent in the latter (1 of 26 patients) (P = 0.0008). As a control measure, the results of penicillin treatment were also studied. Fifty-seven of 80 consecutive patients with erythromycin-resistant isolates had been treated with penicillin, with a failure rate of 9 percent, and 171 of 179 consecutive patients with erythromycin-susceptible isolates had received penicillin, with a failure rate of 3 percent (P = 0.126) (Table 2).Use of Erythromycin in Finland
In 1989, erythromycin was sold in Finland in an amount equal to 3.0 defined daily doses per 1000 inhabitants per day. The amount sold in various regions was as follows: 3.7 defined daily doses per 1000 inhabitants per day in the Helsinki area, 3.1 in the Turku area, 2.6 in the Tampere area, 2.3 in the Seinäjoki area, 3.1 in the Kuopio area, and 2.6 in the Oulu area. Regional data for the previous years were not available. In Pöytyä the consumption of erythromycin was 2.2 defined daily doses per 1000 inhabitants per day in 1989, and in the city of Turku the corresponding figure was 4.1.
Discussion
Our study shows that erythromycin-resistant strains of group A streptococci have emerged rapidly in Finland. This was evident in a study of isolates from blood cultures, as well as from pharyngeal and pus samples. During 1990 the frequency of resistant isolates increased in the Kuopio, Turku, and Tampere areas; however, in Helsinki it remained at the previous level, and in the Seinäjoki and Oulu districts resistant isolates were seen only rarely. In addition to the emergence of resistance, we found that erythromycin treatment frequently failed to cure throat infections caused by erythromycin-resistant isolates (Table 2).
As well as an overall increase in the levels of resistance to erythromycin, there was great local variation in resistance in the Turku area. In four communities within 50 km of each other, the rate of resistance to erythromycin ranged from 2 percent to 44 percent. This variation cannot be explained by differences in the use of erythromycin on the community level. The level of resistance in Turku was 5 percent, but in Pöytyä, only 30 km north, it was 44 percent, even though the use of erythromycin in Turku was almost twice that in Pöytyä. We made the same finding in the six areas we studied. Resistance was clearly highest in the Kuopio area, but the use of erythromycin there was similar to that in the Helsinki and Turku areas, where resistance was less frequent. Although the possibility of an increase in erythromycin use over time in a particular area could not be evaluated, it is hard to find any explanation for the overall increase in resistance other than the general increase in the use of this drug (Fig. 1).
Several reports of erythromycin resistance among group A streptococci have been published.19 20 21 22 23 24 25 26 27 28 29 According to these reports, the resistance of group A streptococci ranged from 1 percent to 18 percent. However, most of these studies were based on small numbers of isolates and lacked follow-up data. An increasing trend toward erythromycin resistance resembling that in the present study was reported more than a decade ago from Japan,30 , 31 where the frequency of erythromycin-resistant group A streptococci first increased to 70 to 80 percent and then decreased after the use of erythromycin was reduced.31
In this study, erythromycin resistance was found to be significantly higher among isolates from pus samples than among those from pharyngeal samples (Table 1). The most common focus of infection in Finnish patients with septicemia due to group A streptococci is the skin (unpublished data). This may explain the simultaneous increase in erythromycin resistance in group A streptococcal isolates from blood cultures and pus samples. In addition, the emergence of erythromycin resistance in group A streptococci took place at the same time as an increase in the frequency of group A streptococcal septicemia.2
The high frequency of resistance to erythromycin in group A streptococci is of major clinical concern, because only a few peroral antibiotics are useful for treating infections caused by these organisms. If treatment with erythromycin is excluded, the only drugs available for patients who cannot take penicillin are the peroral cephalosporins and clindamycin. Although resistance to erythromycin and resistance to clindamycin are often linked (the constitutive type of resistance32), we did not detect any clindamycin-resistant group A streptococci among the erythromycin-resistant throat-swab isolates. However, because of the inducible type of resistance,32 clindamycin may not be clinically effective against these isolates despite their susceptibility in vitro. Trimethoprim–sulfamethoxazole (cotrimoxazole) cannot be used because of the intrinsic resistance of group A streptococci to this drug,33 and the efficacy of the fluoroquinolones against group A streptococcal infections has not yet been established. Because of possible cross-resistance, the effect of different new macrolide antibiotics against erythromycin-resistant group A streptococci should also be evaluated.
Our restriction-profile analysis identified 14 clones among the 95 selected isolates of group A streptococci, with no single clone predominating. However, among these isolates, only eight serotypes were identified, and the serotypes of 37 percent could not be determined. Restriction-endonuclease profiles have been shown to correlate well with the M serotypes of different group A streptococci.16 We did not look for such a correlation in this study, but we found the determination of these profiles useful in showing the clonal diversity of group A streptococci. In Japan, an outbreak of infection with erythromycin-resistant group A streptococci was caused mainly by the T12 serotype.30 Our experience was more like that of Canadian investigators, who demonstrated that erythromycin-resistant isolates represented several different serotypes.19 The resistance of streptococci to erythromycin is typically plasmid-mediated,34 which could explain the rapid spread of resistance to different clones of group A streptococci (Fig. 3). More studies are in progress to determine the mechanisms of erythromycin resistance in isolates found in our country.
In Finland, the use of erythromycin in 1988 and 1989 was almost three times that in 1978 (Fig. 1). When the rates of use in Nordic countries in 1989 were compared, the rate in Finland was 50 percent higher than that in Denmark and 100 percent higher than that in Sweden and Norway.12 Furthermore, a trend toward increasing use of the drug was observed only in Finland. In 1983, erythromycin was consumed at a rate of 4.1 defined daily doses per 1000 inhabitants per day in the United States, 2.8 doses in Australia, 2.4 doses in Canada, and 2.3 doses in France.35 These figures are similar to or higher than those for Finland.
In conclusion, the increased frequency of erythromycin resistance in group A streptococci is a serious problem. We do not see any possible way to control this clinical problem except to reduce the use of erythromycin and other macrolides. We also believe that frequent determination of the susceptibility of group A streptococci to erythromycin by clinical-microbiology laboratories worldwide would be valuable to show how extensively erythromycin-resistant group A streptococci have spread and to follow changes in patterns of resistance.
Supported by the Sigrid Juselius Foundation (funds to Drs. Seppälä, S. Huovinen, and P. Huovinen), Eli Lilly S.A. (funds to Mr. Nissinen), and Lääkefarmos Orion Co. (funds to Dr. Seppälä).
We are indebted to Professor P. Helena Mäkelä for valuable advice; to Ritva Scotford, Marja-Liisa Lindman, Tarja Boman, and Ann-Sofie Hakulinen for expert technical assistance; to Mildrid Ekelund and Pirjo Saarinen for the figures on erythromycin use in the Pöytyä community; and to Dr. Robert Paul for assistance in editing.
Source Information
From the Antimicrobial Research Unit, National Institute of Public Health, Turku, Finland (H.S., H.J., S.H., P.H.); the Oulu Regional Institute, National Institute of Public Health, Oulu, Finland (E.H.); the Department of Bacteriology, National Institute of Public Health, Helsinki (A.N., M.J.); the Department of Clinical Microbiology, University of Umeå, Umeå, Sweden (S.E.H.); the health centers of Parainen (T.H.) and Pöytyä (L.P.-M.), Finland; the departments of Clinical Microbiology of Kuopio University Hospital, Kuopio, Finland (M.-L.K.), Aurora Hospital, Helsinki (S.K.), Tampere University Hospital, Tampere, Finland (O.L.), and Seinäjoki Central Hospital, Seinäjoki, Finland (S.O.); and the Research Institute for Social Security of the Social Insurance Institution, Helsinki (T.K.). Address reprint requests to Dr. Seppälä at the Antimicrobial Research Unit, National Institute of Public Health, P.O. Box 57, 20521 Turku, Finland.
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