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The prevalence of colonization with drug-resistant pneumococci among adult workers in children's daycare.

Abstract

We conducted a study to determine if employment at a children's daycare facility increases an adult's risk of carrying Streptococcus pneumoniae in general and antibiotic-resistant S pneumoniae in particular. From January through March 2003, we obtained nasopharyngeal and oropharyngeal specimens from 63 adult workers at 6 daycare facilities and 65 similarly aged controls; all but 2 controls were nonclinical employees at our tertiary care center. Culture and sensitivity data were obtained from all specimens, and written questionnaires were used to gather information on each daycare worker, control, and daycare center. The vaccination records of children at 5 of the 6 daycare centers were reviewed. Odds ratios with 95% confidence intervals were calculated to compare the rates of colonization with S pneumoniae in the daycare workers and controls. Multinomial logistic regression analysis was used to compare different daycare centers and to identify risk factors for S pneumoniae carriage. Analysis of the results revealed that the prevalence of S pneumoniae colonization among daycare workers (3/63 [4.76%]) and controls (3/65 [4.62%]) was nearly identical. Whereas no S pneumoniae isolate from a daycare worker displayed multiple drug resistance, all 3 isolates from the controls did; however, this difference was not statistically significant. We conclude that employment at a children's daycare facility in our community did not increase an adult's risk of carrying S pneumoniae. In fact, daycare workers may be even less likely to carry antibiotic-resistant S pneumoniae because of the widespread and successful use of the heptavalent pneumococcal vaccine in young children.

Introduction

Over the course of time, Streptococcus pneumoniae has accounted for more morbidity and mortality among humans than any other bacterium. (1) This bacterium poses the greatest threat to young children, to patients with underlying debilitating medical conditions, and to the elderly. (2) The spectrum of diseases caused by Spneumoniae ranges from otitis media to pneumonia, sepsis, and meningitis. However, even in the case of otitis media, Spneumoniae is the most virulent of the various causative organisms. (3)

Pneumococcal resistance to penicillin was not documented in humans until 1965, and it remained uncommon in the United States until 1987. (4) From 1979 through 1986, 0.2% of invasive pneumococcal isolates displayed high-level resistance to penicillin. By 1997, that figure had increased to 49.7% of isolates in children younger than 2 years. (2.5-8)

Multiple-drug-resistant pneumococci were first reported in South Africa in 1977. (2,4) (The term "multiple drug resistance" applies to a serotype that is resistant or intermediately susceptible to 3 or more antimicrobials.) In the 1980s, multiple-drug--resistant strains began to appear in the U.S., most likely imported from Europe. In addition to penicillin, multiple-drug--resistant strains may be resistant to macrolide, cephalosporin, and fluoroquinolone antibiotics. (2,5-8) By 1994, the incidence of multiple-drug-resistant strains had reached 13.1%. The most recent data from the Tracking Resistance in the United States Today (TRUST) surveillance program (7) indicate that between 1999 and 2002, the overall prevalence of:

* penicillin resistance increased from 14.7 to 18.4%

* azithromycin resistance increased from 22.7 to 27.5%

* ceftriaxone resistance increased from 1.2 to 1.7%

* levofloxacin resistance increased from 0.3 to 0.9%

Children were the focus of much of the attention that was paid to Spneumoniae for good reason. Pneumococcal disease most frequently strikes between birth and 24 months of age. Pneumococci are responsible for approximately 50% of cases of acute otitis media in children and for 13 to 38% of cases of community-acquired pneumonia in children. Children are also the principal vectors of S pneumoniae transmission, which occurs via either direct contact or aerosolization. Approximately 44% of healthy American children 6 years of age and younger carry pneumococci in the nasopharynx; in other countries, such carriage rates are as high as 60%. For children in daycare, this figure jumps as high as 60 to 80%. The carriage rate peaks at preschool age before subsiding. Risk factors for colonization by resistant strains of S pneumoniae in children include age younger than 2 years, frequent antibiotic use, use of antibiotics within the previous year, use of prophylactic antibiotics, participation in group daycare, previous hospitalization, underlying disease, an absence of breast-feeding during infancy, white race, suburban residence, two or more recent episodes of otitis media, and sustained exposure to cold weather. (2,5,6,9-15)

In the daycare setting, the carriage rate of Spneumoniae increases gradually and the proportion of resistant serotypes increases markedly in direct proportion to the number of children enrolled. (10) In 1988, Henderson et al reported that pneumococci recovered from children in daycare were far more likely to be resistant to trimethoprim/sulfamethoxazole (TMP/SMX) and to beta-lactam antibiotics than were organisms recovered from patients at a tertiary care university hospital. (16) Huebner et al reported that as many as 30% of such children will carry multiple serotypes. (17) According to Boken et al, one factor that might facilitate the spread of resistant pneumococci in the daycare setting is colonization of the daycare staff. (18)

Since the 1970s, we have known that antibiotics do not eradicate nasopharyngeal carriage of pneumococci, prevent reinfection, or prevent acquisition in infection-free children. (13) Therefore, the development of a vaccine represented a major step forward in the prevention of pneumococcal disease. The pneumococcal vaccine available to adults is an unconjugated, 23-valent product. For children, the seven-valent pneumococcal conjugate vaccine was approved by the U.S. Food and Drug Administration (FDA) in February 2000, and in the autumn of that year, the FDA recommended that it be universally administered to American children younger than 2 years. This vaccine includes seven serotypes: 4, 6B, 9V, 14, 18C, 19F, and 23F. These polysaccharides are combined with a nontoxic, mutant protein of diphtheria toxin. This conjugate vaccine thus increases the likelihood of an adequate antibody response in children younger than 2 years. Children in this age group tend to have a limited antibody response to T-cell--independent antigens such as bacterial polysaccharides. This may explain the relative increase in the pathogenicity of pneumococci in young children. In early trials, this heptavalent vaccine proved to be highly efficacious in children. An 89.1% reduction in total invasive pneumococcal disease burden was noted in children who received at least one dose of the vaccine. Also, children who received the vaccine were 20.1% less likely to require pressure equalization tubes. (2,5,18-20)

More than 90 capsular types of pneumococci exist, and any of them can develop antimicrobial resistance. (19) Prior to the FDA's approval of the heptavalent vaccine, the seven most common pneumococcal serotypes in children younger than 6 years were, in order of decreasing prevalence, 14, 6B, 19F, 18C, 23F, 4, and 9V. These seven accounted for 78.4% of all infections with S pneumoniae; the first three of these serotypes (14, 6B, and 19F) accounted for more than half. At the same time, three serotypes (14, 6B, and 23F) accounted for 75% of infections with multiple-drug-resistant pneumococci.

Beyond 2 years of age, serotype distribution in children becomes increasingly like the distribution observed in adults. The six most common serotypes among patients 6 years and older are, in descending order, 4, 14, 23F, 9V, 12F, and 6B. Meanwhile, a report from Spain indicated that serotypes 6, 9, 14, 15, 19, and 23 were the most likely to be highly resistant to penicillin (minimum inhibitory concentration [MIC]: [greater than or equal to] 2.0 [micro]g/ml). Likely the most important effect of the heptavalent vaccine is not that it decreases the overall carriage rate of S pneumoniae, but that it decreases the carriage rate of resistant serotypes of S pneumoniae. (2,8,11,13,20)

One factor that complicates treatment is that acute otitis media resolves spontaneously in more than 70% of cases. (21) However, while S pneumoniae is the most common cause of acute otitis media worldwide, it is also the least likely to resolve without antibiotic treatment. Meanwhile, more than 10% of cases of acute otitis media in children do not improve even with antibiotic treatment, and in countries with low antibiotic prescription rates, the rate of suppurative complications of otitis media is twice that of other countries. (8,11) Some methods that have been proposed to control the spread of resistant pneumococci include withholding antibiotic treatment in mild cases of acute otitis media, shorter antibiotic courses for upper respiratory infections, and the use of the pneumococcal vaccine in children. (18)

Adult workers in children's daycare centers may be at increased risk of acquiring pneumococci. Furthermore, these adults may facilitate the spread of S pneumoniae from one child to another. The aim of the present study was to determine if employment at a children's daycare facility in Texas increased an adult's risk of carrying S pneumoniae in general and antibiotic-resistant S pneumoniae in particular.

Patients and methods

This cross-sectional prevalence study was conducted at 6 children's daycare centers in Galveston, Tex., and at the University of Texas Medical Branch at Galveston.

A total of 63 adults employed at the daycare centers were tested for colonization by Spneumoniae from January through March 2003. During the same period, 65 adult controls who had not been employed in children's daycare were also tested for Spneumoniae. The control group was made up of 63 subjects who worked at the University of Texas Medical Branch at Galveston in a nonclinical setting (i.e., none was involved in direct patient contact), 1 housewife, and 1 elementary school teacher.

Specimens were obtained from both the nasopharynx and the oropharynx of each participant. All specimen collection was performed in a standardized fashion at each participant's place of employment. Nasopharyngeal specimens were collected on a calcium alginate swab attached to a flexible aluminum wire by one of two methods: either transnasally with the assistance of a nasal speculum or transorally with a curved swab slid behind and above the soft palate as described elsewhere. (14) Oropharyngeal specimens were obtained on a sterile calcium alginate swab under direct vision assisted by a headlight and a wooden tongue blade. Of note, the transoral route was far better tolerated by the participants.

All specimens were deposited at the same microbiology laboratory for immediate processing. Identification of S pneumoniae was based on colony morphology, Gram's staining, alpha hemolysis, and P-disk. Antibiotic sensitivities were determined for penicillin, cefotaxime, erythromycin, levofloxacin, vancomycin, clindamycin, and TMP/SMX.

The E test was used to determine susceptibility to penicillin:

* Isolates with an MIC of less than 0.125 [micro]g/ml were considered to be penicillin-susceptible.

* Isolates with an MIC of 0.125 to 1.0 [micro]g/ml were considered to be intermediately susceptible to penicillin.

* Isolates with an MIC greater than 1.0 [micro]g/ml were considered to be penicillin-resistant.

The laboratory also reported the presence of clinically relevant pathogens when grown from culture. They included beta-hemolytic streptococci, Staphylococcus aureus, Moraxella catarrhalis, and mold. Serotyping of Spneumoniae was not performed.

Written questionnaires were used to collect data on each study participant and each daycare center. Information was recorded on each participant's sex, age, antibiotic use during the previous year and the previous 2 months, history of vaccination with the 23-valent pneumococcal vaccine, all sites of current employment, and the duration of employment in children's daycare. Data were also gathered on the number of children at home and their ages, as well as each child's participation in daycare and history of vaccination with the heptavalent pneumococcal vaccine. For each daycare center, information was recorded on the number of children enrolled, their age range, the cost of enrollment, and the number of adult employees.

Odds ratios and associated 95% confidence intervals were calculated to compare colonization with any of the previously mentioned pathogens between daycare workers and controls. Multinomial logistic regression analysis was performed with SPSS software to compare the daycare centers and to identify general risk factors for S pneumoniae carriage among both the daycare subjects and controls.

The study was approved by the Institutional Review Board of the University of Texas Medical Branch at Galveston. Written informed consent was obtained from all participants.

Results

The daycare worker population was made up of 59 women and 4 men, aged 18 to 62 years (mean: 35), and the control group included 46 women and 19 men, aged 21 to 65 years (mean: 36) (table 1). The only statistically significant difference between the two groups was the sex distribution (p = 0.000748). No differences were seen with respect to age, antibiotic use, history of vaccination with the 23-valent pneumococcal vaccine, or the number of children at home.

Only 3 of the 63 adult daycare workers (4.76%) were colonized with S pneumoniae at the time of the study. Of these 3 patients, 2 grew Spneumoniae from their nasopharynx only, and 1 grew S pneumoniae from the oropharynx only (table 2). Two of the 3 isolates were sensitive to all antibiotics tested; the other demonstrated resistance to penicillin (MIC: 2.0 [micro]g/ml) and TMP/SMX. Two of the three isolates came from the same daycare center.

Beta-hemolytic streptococci were isolated from 12 of the daycare workers (19.05%), S aureus from 9 (14.29%), and M catarrhalis from 2 (3.17%) (table 3).

Only 3 of the 65 controls (4.62%) were colonized with S pneumoniae at the time of the study; 2 grew Spneumoniae from the nasopharynx only and the other grew Spneumoniae from the oropharynx only (table 4). All 3 of these isolates demonstrated multiple drug resistance. One demonstrated intermediate susceptibility to penicillin (MIC: 0.25 [micro]g/ml) and resistance to erythromycin and clindamycin. Another demonstrated intermediate susceptibility to penicillin (MIC: 1.0 [micro]g/ml) and resistance to erythromycin and TMP/SMX. The third demonstrated resistance to penicillin (MIC: 2.0 [micro]g/ml), intermediate susceptibility to cefotaxime (MIC: 2.0 [micro]g/ml), and resistance to TMP/SMX.

Beta-hemolytic streptococci were isolated from 10 (15.38%) of the controls, S aureus from 7 (10.77%), and M catarrhalis from 1 (1.54%) (table 3). Seven of the controls (10.77%) had at least 1 child in daycare; none of these 7 was colonized with S pneumoniae. However, isolates from 3 of these 7 subjects (42.86%) did grow beta-hemolytic streptococci. There was no significant difference in beta-hemolytic streptococcal colonization between the daycare workers and the controls who had children in daycare, according to the chi-square test (p = 0.28). None of the controls had been vaccinated with the 23-valent pneumococcal vaccine.

The number of children attending the 6 daycare centers ranged from 60 to 285 (median: 81.5), and the number of employees ranged from 11 to 53 (median: 13.5). The cost of enrollment for the youngest children accepted at each daycare center ranged from $100 to $525 per month (mean: $350.42).

Vaccination records were submitted by 5 of the 6 daycare centers; the exception was the same center that had 2 employees with Spneumoniae. Between 16.36 and 56.76% of children at the 6 daycare centers were 3 years of age or younger (mean: 38.42%). Of these younger children, between 61.76 and 100% (mean: 82.97%) had received the heptavalent pneumococcal vaccine at least once.

Odds ratios were calculated to estimate the relative risk of colonization with S pneumoniae, penicillin-resistant S pneumoniae, multiple-drug-resistant S pneumoniae, beta-hemolytic streptococci, S aureus, and M catarrhalis among daycare workers as compared with the controls. Odds ratios were also calculated for colonization with S pneumoniae and penicillin-resistant S pneumoniae in the nasopharynx as compared with the oropharynx. None of the differences in these comparisons achieved statistical significance based on 95% confidence intervals.

Multinomial logistic regression analysis was performed to identify any correlations between colonization with S pneumoniae and sex, age, antibiotic history during the previous 2 months, antibiotic history during the previous year, having at least 1 child at home, having at least 1 child in daycare, the number of children enrolled in daycare, the length of time employed in daycare, the number of employees at a daycare center, and the cost of daycare. Again, no statistically significant relationships were found. (The cost of enrollment in daycare was taken as a rough estimate of the socioeconomic status of enrollees at a given daycare center. Of note, the least expensive daycare center had the highest number of isolates positive for S pneumoniae [2].)

Discussion

In the present study, the prevalence of colonization with Spneumoniae among adult workers in children's daycare and control subjects was nearly identical--4.76% and 4.62%, respectively. Among the daycare workers, 1 of the 3 isolates demonstrated antibiotic resistance, and this was to penicillin and TMP/SMX. Among the controls, all 3 isolates demonstrated resistance to three different antibiotics and were therefore classified as multiply drug-resistant. Nevertheless, none of these differences was statistically significant.

On the basis of these data and data from other reports, it is apparent that the prevalence of colonization with Spneumoniae among adults is much lower than the prevalence of colonization among children. In a study at a children's daycare center in Ohio, Reichler et al found that only 2 of 26 staff members (8%) grew S pneumoniae from the nasopharynx, compared with 134 of 250 children (54%). (14) While the nasopharynx likely represents the primary site of colonization for S pneumoniae in children, evidence suggests that oropharyngeal sampling may be a more sensitive means of detecting colonization in adults. (1,22) The study by Reichler et al involved sampling from the nasopharynx only, so some adults colonized with S pneumoniae were likely missed. (14)

Even so, pneumococcal colonization among adults--even daycare workers in the pre-heptavalent vaccine era--is low. It is true that exposure to young children at home significantly increases carriage rates in adults; Hendley et al reported that a parent in a household with 1 or more preschool-aged children has a 1-in-4 chance of carrying Spneumoniae at some point, while that likelihood falls to 2% for parents whose children are in junior high school? Sibling-to-sibling spread is more common than child-to-adult spread, (23) and susceptibility to the acquisition of S pneumoniae decreases as age increases. (15)

Similarities do exist between adults and children in that (1) the presence of a viral upper respiratory infection increases the likelihood of acquiring S pneumoniae as a carrier, and (2) the mean duration of carriage is 9 weeks in children and 10 weeks in adults. (1,13,21) However, Gray et al reported relatively high concentrations of serum antibodies to colonizing types in adults, whereas children--particularly those younger than 2 years--had low or undetectable levels. (13) This finding likely explains why young children are both more likely to carry S pneumoniae and more susceptible to pneumococcal disease.

Among adults, one would expect workers at children's daycare centers to carry antibiotic-resistant strains of S pneumoniae more frequently than do other adults. However, this was not the case in our study, and the reason is likely attributable to the widespread and successful use of the heptavalent conjugate pneumococcal vaccine in young children. This vaccine has not been found to decrease the overall carriage of S pneumoniae, but it has been found to decrease the carriage of resistant serotypes. In our study, the mean S pneumoniae vaccination rate among children aged 3 years and younger in the 5 reporting daycare centers was 82.97%. Therefore, exposure to antibiotic-resistant serotypes was likely lower among the daycare workers than among the controls. Prior to the introduction of the heptavalent conjugate pneumococcal vaccine, eradication of nasopharyngeal carriage of resistant strains of S pneumoniae proved to be extremely difficult in daycare populations. (14) That story may now be changing.

Based on work done in the 1970s, Gray et al (13) reported several key findings:

* The mean age of patients at the acquisition of S pneumoniae was 6 months (range: 4 days to 18 mo).

* The acquisition rate of Spneumoniae was highest from January through March (the same time of year that we conducted our study).

* The younger a child was at the time of acquisition, the longer he or she was likely to carry a given strain.

* Prolonged nasopharyngeal carriage of a single strain was common, but infection secondary to such a strain was uncommon.

* In approximately 75% of cases, the disease-causing serotype was newly acquired.

As previously mentioned, the nasopharynx is believed to be the site most often colonized with S pneumoniae in children, while the oropharynx is the most common site in adults. However, in our study of adults, 4 of the 6 isolates came from the nasopharynx and the other 2 from the oropharynx. Furthermore, no subject was colonized in both the nasopharynx and oropharynx. Our findings suggest that adults actually may not differ from children with respect to the site of colonization and that one should sample both sites when seeking S pneumoniae colonization in adults.

The association between TMP/SMX resistance and a decreased susceptibility to penicillin is common in several countries. 15 We noted the same pattern in our study, in which 3 of the 4 isolates that demonstrated antibiotic resistance displayed decreased susceptibility to both penicillin and TMP/SMX.

In the present study, colonization with other clinically relevant organisms--beta-hemolytic streptococci, S aureus, and M catarrhalis--was slightly more common among the daycare workers than the controls, but the differences were not statistically significant. Beta-hemolytic streptococci are rarely a cause of acute otitis media in children younger than 2 years, but they have become a relatively common cause of acute otitis media in children older than 5 years. (8) This organism was encountered more frequently than S pneumoniae in our study, and it may merit further study in the daycare setting.

Note should be made that not all daycare centers in the Galveston area were involved in this study. However, we did make an effort to include daycare centers of various sizes and socioeconomic characteristics. Furthermore, not all employees at each daycare center were willing to volunteer for specimen collection. Thus, a self-selection bias might have existed.

Conclusions

The prevalence of colonization with Spneumoniae among adult workers in children's daycare centers and controls in the Galveston area was nearly identical. Surprisingly, antibiotic-resistant strains were more common in the control group. Therefore, adult daycare workers in Galveston do not appear to have a higher risk of colonization with S pneumoniae in general or antibiotic-resistant Spneumoniae in particular.

The prevalence of S pneumoniae carriage is higher in children than in adults, and young children are more susceptible to pneumococcal disease than are healthy adults. This may be attributable to the presence of higher levels of serum antibodies to pneumococci in adults. Even so, the widespread and successful use of the heptavalent conjugate pneumococcal vaccine in young children in Galveston may already be decreasing the carriage rates of antibiotic-resistant Spneumoniae in the daycare setting among not only children, but also adults.

One should sample both the nasopharynx and oropharynx when seeking S pneumoniae colonization in adults.

Finally, in our study, beta-hemolytic streptococci were more common than pneumococci in the pharynx.

Acknowledgment

The authors acknowledge Chad W. Putman, MD, for his contribution to this project.

References

(1.) Hendley JO, Sande MA, Stewart PM, Gwaltney JM Jr. Spread of Streptococcus pneumoniae in families. I. Carriage rates and distribution of types. J Infect Dis 1975;132:55-61.

(2.) Breiman RF, Butler JC, Tenover FC, et al. Emergence of drug-resistant pneumococcal infections in the United States. JAMA 1994;271:1831-5.

(3.) Musher D, Dagan R. Is the pneumococcus the one and only in acute otitis media? Pediatr Infect Dis J 2000;19:399-400.

(4.) Austrian R. Confronting drug-resistant pneumococci. Ann Intern Med 1994;121:807-9.

(5.) Giebink GS. The prevention of pneumococcal disease in children. N Engl J Med 2001;345:1177-83.

(6.) Hofmann J, Cetron MS, Farley MM, et al. The prevalence of drug-resistant Streptococcus pneumoniae in Atlanta. N Engl J Med 1995;333:481-6.

Frederick S. Rosen, MD; Matthew W. Ryan, MD

From the Department of Otolaryngology-Head and Neck Surgery, University of Texas Medical Branch at Galveston.

Reprint requests: Frederick S. Rosen, MD, Department of Otolaryngology, Children's Hospital and Research Center, 747 52nd St., Oakland, CA 94609-1809. Phone: (510) 428-3000, ext. 6844; fax: (925) 685-0917; e-mail: frosenr@yahoo.com
Table 1. Selected characteristics and findings relative to the
daycare workers (n = 63) and controls (n = 65)

 Daycare Controls
 n (%) n (%)

Women/men 59/4 (93.65/6.35) * 46/19 (70.77/29.23) *

Mean age, yr (range) 35 (18 to 62) 36 (21 to 65)

History of antibiotics 12 (19.05) 19 (29.23)
in the previous 2 mo

History of antibiotics 36 (57.14) 37 (56.92)
in the previous year

Vaccination with 23-valent 3 (4.76) 0
pneumococcal vaccine

[greater than or equal to] 19 (30.16) 15 (23.08)
1 child at home

S pneumoniae positivity 3 (4.76) 3 (4.62)

* The only statistically significant difference between the two
groups was the sex distribution (p = 0.000748).

Table 2. Antibiotic resistance and susceptibility in the 3
S pneumoniae-positive daycare workers

 Worker 1 Worker 2
 (nasopharynx) (oropharynx)

Penicillin (MIC) Resistant Susceptible
 (2.0 [micro]g/ml) (0.06 [micro]g/ml)
Cefotaxime (MIC) Susceptible Susceptible
 (1.0 [micro]g/ml) (0.12 [micro]g/ml)
Erythromycin Susceptible Susceptible
Levofloxacin Susceptible Susceptible
Vancomycin Susceptible Susceptible
Clindamycin Susceptible Susceptible
TMP/SMX Resistant Susceptible
Multiple drug resistance No No

 Worker 3
 (nasopharynx)

Penicillin (MIC) Susceptible
 (0.03 [micro]g/ml)
Cefotaxime (MIC) Susceptible
 (0.03 [micro]g/ml)
Erythromycin Susceptible
Levofloxacin Susceptible
Vancomycin Susceptible
Clindamycin Susceptible
TMP/SMX Susceptible
Multiple drug resistance No

Table 3. Other clinically relevant organisms found in
this study

 Daycare Controls
Organism n (%) n (%)

Beta-hemolytic 12 (19.05) 10 (15.38)
streptococci

S aureus 9 (14.29) 7 (10.77)

M catarrhalis 2 (3.17) 1 (1.54)

Table 4. Antibiotic resistance and susceptibility in the 3
S pneumoniae-positive controls

 Control 1 Control 2
 (oropharynx) (nasopharynx)

Penicillin (MIC) Intermediately Intermediately
 susceptible susceptible
 (0.25 [micro]g/ml) (1.0 [micro]g/ml)

Cefotaxime (MIC) Susceptible Susceptible
 (0.12 [micro]g/ml) (1.0 [micro]g/ml)

Erythromycin Resistant Resistant

Levofloxacin Susceptible Susceptible

Vancomycin Susceptible Susceptible

Clindamycin Resistant Susceptible

TMP/SMX Susceptible Resistant

Multiple drug resistance Yes Yes

 Control 3
 (nasopharynx)

Penicillin (MIC) Resistant
 (2.0 [micro]g/ml)

Cefotaxime (MIC) Intermediately
 susceptible
 (2.0 [micro]g/ml)

Erythromycin Susceptible

Levofloxacin Susceptible

Vancomycin Susceptible

Clindamycin Susceptible

TMP/SMX Resistant

Multiple drug resistance Yes
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Author:Ryan, Matthew W.
Publication:Ear, Nose and Throat Journal
Date:Jan 1, 2007
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