Context Overuse of antibiotics has contributed to microbial resistance, compromising
the treatment of bacterial infections. Very high levels (>50%) of antibiotic
resistance among invasive Streptococcus pneumoniae
have been documented in Knox County, Tennessee.
Objective To determine the effectiveness of a community-wide intervention aimed
at reducing inappropriate antibiotic use among children.
Design, Setting, and Participants The Knox County Health Department led a multifaceted year-long campaign
(May 1997 through April 1998) aimed at decreasing unnecessary antibiotic use
among children. Tennessee's 3 other major urban counties (Shelby, Hamilton,
and Davidson) did not conduct similar campaigns and served as controls. Evaluation
included white and black children (aged <15 years) enrolled in Tennessee's
Medicaid Managed Care Program in the 4 study counties, representing 36% of
the study counties' children (464 200 person-years observed).
Intervention Educational efforts were directed toward health care practitioners (primarily
via peer leader presentations) and to the parents of young children and the
public (primarily via printed materials).
Main Outcome Measure The intervention-attributable effect on antibiotic use, defined as the
excess percentage change in oral antibiotic prescription rates in Knox County
between the 12-month preintervention and postintervention periods, relative
to that of control counties.
Results Antibiotic prescription rates declined 19% and 8% among Knox County
and control county children, respectively, yielding an 11% intervention-attributable
decline (95% confidence interval, 8%-14%; P<.001).
The intervention-attributable decrease in prescription rates was greatest
among children aged 1 to less than 5 years (among white children, 8% [P<.001]; among black children, 18% [P<.001]).
Conclusions A community-wide educational intervention reduced antibiotic prescription
levels among children in Knox County.
Increasing resistance to antibiotics is compromising treatment of Streptococcus pneumoniae and other serious bacterial infections.1,2 "Antibiotic pressure," the use and
misuse of large quantities of antibiotics, is the driving force behind the
worldwide resistance phenomenon.3,4
Concern regarding this problem has motivated a review of antibiotic prescribing
patterns and treatment guidelines.5-10
Children represent a population of particular concern because they have
the highest rates of antibiotic use and infection with antibiotic-resistant
pathogens.2,11,12
By the early 1990s, US children younger than 15 years were receiving an average
of almost 1 oral antibiotic prescription per year, primarily for the treatment
of respiratory infections.11 A substantial
proportion of this prescribing is thought to be unnecessary.13,14
Responsible antimicrobial use as a means to curtail drug resistance has been
broadly promoted by the Centers for Disease Control and Prevention (CDC),
the American Academy of Pediatrics, and other groups and institutions.5,15 In the United States, reductions in
antibiotic prescribing have been demonstrated in targeted primary care practices16 and in 2 relatively isolated rural populations.17,18 However, little is known about the
effectiveness of broader community- or state-level campaigns.5,19
Tennessee had the highest rate of prescription utilization in the United
States during 1998, based on capitated retail sales data.20
Similarly, utilization rates for penicillins, cephalosporins, and trimethoprim-sulfamethoxazole
in Tennessee were at least 20% higher than national averages.20
Within Tennessee, strains of S pneumoniae isolated
from invasive infections have demonstrated a high prevalence of penicillin
resistance (35%)2; the highest resistance levels
(>50%) were reported for Knox County (1998 population, 375 00021; county seat: Knoxville).22
In response to this problem, and stimulated by a recent multidrug-resistant
pneumococcal meningitis outbreak in a nearby county,23
the Knox County Health Department (KCHD) conducted a multifaceted educational
intervention. In this article, we evaluate the intervention's effect on pediatric
antibiotic prescribing.
The KCHD led a year-long community-wide intervention (May 1997 through
April 1998) to decrease unnecessary antibiotic use among children. In 1997,
KCHD created the East Tennessee Drug Resistance Task Force, with representatives
of state, regional, and county health departments, a university medical center,
a commercial laboratory, a managed care organization, and the CDC, to develop
and implement the intervention. The campaign was directed at 3 main audiences:
(1) 250 key health care providers (eg, pediatricians and family physicians)
who provided most routine health care services to Knox County children; (2)
parents of young children; and (3) the general public.
The educational campaign stressed that (1) antibiotics should be used
only for bacterial infections; (2) colds and most coughs and sore throats
are caused by viruses and should not be treated with antibiotics; and (3)
when antibiotics are prescribed, they should be narrow spectrum. Major components
of the campaign were as follows.
Provider education consisted of (1) lectures by a CDC physician to 150
of the key providers; (2) presentations at hospital staff meetings, grand
rounds, continuing medical education seminars, resident conferences, and targeted
primary care clinics; (3) distribution of new prescribing guidelines for pediatric
respiratory infections6 to the 250 key providers;
and (4) related articles published in the KCHD quarterly newsletter mailed
to all 1500 Knox County physicians.
Parent education consisted of (1) distribution of 40 000 pamphlets
to parents of all children in day care and grades K-3; (2) distribution of
patient education materials to the 250 key providers; and (3) distribution
of pamphlets to the parents of every newborn (incorporated with informational
mailings regarding childhood immunizations).
Public education consisted of (1) distribution of 30 000 pamphlets
to hospitals, clinics, and dental offices; (2) communication of information
through television, radio, and newspaper coverage and public service announcements;
(3) distribution of 38 000 pamphlets to families receiving influenza
vaccine; and (4) distribution of 53 000 pamphlets to pharmacy clients.
One of the KCHD staff members, a medical epidemiologist, managed the campaign
and performed the majority of the educational presentations. The majority
of the educational materials (eg, pamphlets entitled "Antibiotics and Your
Child") distributed in the campaign were developed by and are available from
the CDC.24,25
Study Design and Rationale
Because there have been both general and localized efforts to promote
the appropriate use of antibiotics,25 the impact
of the Knox County intervention was evaluated by comparing outcomes with suitable
control counties. Tennessee's 3 other urbanized counties were selected; these
counties and their respective county seats were Shelby (Memphis), Davidson
(Nashville), and Hamilton (Chattanooga). The control counties are geographically
distant from Knox County and did not conduct similar community-wide interventions.
Prescription of oral antibiotics to children was compared between the intervention
county and control counties during the 12-month periods before, during, and
after the intervention. The intervention-attributable effect was defined as
the excess percentage reduction in prescription rates in Knox County relative
to the control counties. The study also examined rates of outpatient visits
for respiratory illnesses, ratios of prescriptions to respiratory illness
visits, and antibiotic resistance among pneumococcal isolates from invasive
infections. Because the absolute rate of antibiotic use was of interest, prescriptions
were not linked to specific office visits and diagnoses, thus avoiding problems
or omissions associated with mistakes or shifts in coding,26
and prescriptions resulting from telephone consultations or emergency department
visits.
The study population included children younger than 15 years who were
residents of 4 counties (Knox, Davidson, Hamilton, and Shelby) and who were
enrolled in the Tennessee Medicaid Managed Care Program (TennCare). On January
1, 1994, Medicaid was supplanted in Tennessee by TennCare, a managed care
system that extended health insurance coverage to approximately 50% more persons
than were eligible for Medicaid and shifted the care of enrollees to physicians
in private practice.27 The TennCare enrollment
file identifies persons who are eligible to receive benefits; the specific
dates of coverage; and the sex, race, date of birth, and county of residence
of the enrollees. Children entered the study on the first day after May 1,
1996, on which they met the inclusion criteria, which were enrollment in TennCare
within 30 days of birth or for 1 year, age younger than 15 years, and residence
in 1 of the 4 study counties. Children were followed until loss of coverage
by TennCare, age 15 years, death, or April 30, 1999. Person-time as a hospital
inpatient was excluded. Children not designated as either white or black represented
a small proportion (4%) of the eligible population and were also excluded.
Person-time contributed by children included in the study was expressed in
person-years and grouped according to age (<1 year, 1 to <5 years, and
5 to <15 years), county of residence, and race.
Definitions, Outcomes, and Data Sources
The 12-month periods before (May 1996 through April 1997), during (May
1997 through April 1998), and after (May 1998 through April 1999) the educational
intervention were categorized as years 1, 2, and 3 for this study. Computerized
TennCare files for 1996 through 1999 were used to determine the primary study
outcome, oral antibiotic prescription use, and a secondary outcome, outpatient
visits to a physician for a diagnosed respiratory illness, for enrolled children
during the 3 study years. These files contained information on medical services
reimbursed, including dates of medical services received on an outpatient
basis, associated diagnoses and procedures, and prescriptions filled. Prescriptions
were not linked with visits, and no more than 1 visit per patient per day
was counted.
Prescriptions included were those filled for antimicrobial drugs administered
orally and typically used for treatment of respiratory infections in pediatric
outpatients. Antibiotic categories included were penicillins (eg, amoxicillin
and ampicillin), cephalosporins, trimethoprim-sulfamethoxazole, and macrolides/other
(eg, erythromycin, erythromycin-sulfisoxazole, azithromycin, and clindamycin).
For the purpose of this study, respiratory illness was defined as an outpatient
diagnosis of otitis media (International Classification
of Diseases, Ninth Revision [ICD-9]28
codes 381-382), common cold (ICD-9 code 460), sinusitis
(ICD-9 codes 461, 473), pharyngitis (ICD-9 code 462), tonsillitis (ICD-9 code 463),
laryngitis/tracheitis (ICD-9 code 464), bronchitis
(ICD-9 codes 466, 490, 491); pneumonia and influenza
(ICD-9 codes 480-487); or unspecified acute respiratory
illness (ICD-9 code 465).
Data on cases of invasive S pneumoniae infections
occurring in Knox County children younger than 15 years were provided by an
ongoing, active, population-based surveillance system sponsored by the CDC
(the Active Bacterial Core Surveillance program29).
A case of invasive pneumococcal disease was defined as isolation of S pneumoniae from blood, cerebrospinal fluid, or other
usually sterile site. Isolates were tested for antimicrobial susceptibility
using the broth microdilution method by a designated reference laboratory.
Susceptibilities to penicillin, cefotaxime, trimethoprim-sulfamethoxazole,
and erythromycin were examined. Isolates were defined as resistant in this
study if they exhibited intermediate- or high-level resistance to a particular
antibiotic.
Prescription rates were calculated by dividing the number of antibiotic
prescriptions administered in ambulatory care by the person-years observed.
Prescription rates were stratified by study county, study year, race, age
group, and antibiotic category and were expressed per 100 person-years. When
stratified by race, baseline prescription rates were similar among the 3 control
counties (Table 1). For this reason,
the control counties were combined in the subsequent analyses.
Negative Binomial Regression models30
were used to estimate adjusted prescription rates, test whether a significant
intervention-attributable effect existed, and examine potential interactions
among the intervention-attributable effect with age and race. Each model included
variables representing county (Knox vs control), age group (<1 year, 1
to <5 years, and 5 to <15 years), race (white and black), and study
year (year 1, 2, and 3), as well as all relevant interaction terms. In addition,
each model included random effects to account for unobserved heterogeneity
within the counties. The intervention-attributable effect was represented
by the excess percentage change in prescription rates from year 1 to year
3 for Knox County over and above any temporal reductions observed in the control
counties. The intervention-attributable change in the crude rate was determined
by multiplying the intervention-attributable excess percentage change by the
baseline rate in Knox county and represents the estimated reduction in the
number of prescriptions in Knox county in year 3 attributable to the intervention.
Visit rates, calculated by dividing the number of outpatient respiratory
illness visits by the person-years observed, and ratios of antibiotic prescriptions
to the number of outpatient visits (ie, prescription to visit ratios) were
examined as secondary outcome variables. Both were analyzed in a similar manner
as described above for antibiotic prescription rates.
The prevalence of resistance among S pneumoniae
isolates from invasive infections occurring in Knox County was calculated
using the number of resistant isolates divided by the total number of isolates
tested; these rates were expressed as percentages and stratified by study
year and antibiotic category. P = .05 was the level
of significance; basic analyses were performed using SAS Version 8.2 (SAS
Institute Inc, Cary, NC).
The 3-year study encompassed 464 200 person-years of observation
representing 36% of all children younger than 15 years residing in the 4 study
counties (Table 1). The average
annual study population ranged from approximately 18 000 to 84 000
children per county per year. While the study populations were similar with
regard to age and sex, the racial makeup differed substantially, consistent
with underlying demographic differences among the counties; the Knox County
study population had the highest proportion of white children (73%), whereas
Shelby County had the highest proportion of black children (90%).
The total baseline (year 1) rates of antibiotic prescriptions and respiratory
illness visits reflected the racial composition of each county's study population,
with higher rates corresponding to higher proportions of white children (Table 1). For each of the 4 counties, both
prescription and outpatient visit rates among white children were approximately
twice as high as among black children. However, even when white and black
children were examined separately, Knox County's prescription and outpatient
visit rates remained elevated relative to the control sites.
Overall, antibiotic prescription rates declined 19% and 8% from year
1 to year 3 among Knox County and control county children, respectively, yielding
an 11% (95% confidence interval [CI], 8%-14%) intervention-attributable decline
(P<.001) in prescriptions (Table 2). In Knox County, prescription rates declined by 16% and
21% for white and black children respectively (Figure 1), with most of the decline occurring during year 2 when
the intervention was conducted. Among controls, the decrease in prescription
rates from year 1 to year 3 was more evident among white children (12%) than
black children (3%). The changes in Knox County's prescription rates exceeded
these secular trends for black children (P<.001)
but not white children (P = .18).
Antibiotic prescription rates in Knox County and in the control counties
decreased among all age and race groups examined (Table 2). These age-specific decreases were similar in magnitude
among white and black children in Knox County, but not in the control counties
where the decrease was more pronounced among white children. The intervention's
effect on prescription rates was significant (P<.001)
for black children in all 3 age groups (attributable decreases ranging from
16%-20%) and for white children in the 1- to less than 5-year age group (8%
attributable decrease). The intervention-attributable effects, expressed in
terms of their impact on baseline prescribing rates, were equivalent to decreases
of 18 and 25 prescriptions per 100 child-years among white and black children
aged 1 to less than 5 years, respectively.
The observed changes in prescription rates did not appear to result
from changes in respiratory illness visit rates; these rates were relatively
stable during the 3-year study period (Figure
1), and there was no evidence of an unusual respiratory illness
season among the study sites. The ratios of antibiotic prescriptions to respiratory
illness visits were also examined (Figure
1). At baseline, the prescription to visit ratios were similar when
comparing Knox County and the control sites. During the intervention year,
the prescription to visit ratio for both black and white children declined
substantially in Knox County, but not among the controls. By year 3 (postintervention),
the prescription to visit ratio in Knox County had decreased approximately
20% among both race groups; for black children the excess decline relative
to the controls was 13% (P<.001), while for white
children it was 8% (P = .06). In the 1- to 4-year
age group, the prescription to visit ratios declined significantly among both
white children (11%, P = .02) and black children
(17%, P<.001).
Use patterns for specific antibiotics were generally similar between
Knox County and the control counties and for both white and black children
(Figure 2). Overall, the majority
of antibiotic prescriptions were for penicillins, and this proportion increased
significantly (P<.001) during the study period
among black and white children in the intervention and control sites. Prescription
rates among black and white children in Knox County declined for all of the
antibiotic categories examined. These declines were consistently greater among
Knox County children than among controls except for cephalosporins, which
had a significantly greater decline in white children in the control counties.
Resistance rates among isolates of invasive S pneumoniae occurring in Knox County children remained high (≥50%) from year
1 through year 3 for all 4 antibiotic categories examined. Reductions in S pneumoniae resistance rates were not evident (Table 3).
Knox County's public health community recognized the problem of antibiotic
resistance and responded by conducting an educational intervention. Our evaluation
used Medicaid data to demonstrate that antibiotic use declined substantially
among Knox County children in concert with the campaign. When control counties
were examined, a secular downward trend in antibiotic prescription rates was
documented; this finding is in agreement with other recent reports31,32 and may reflect the impact of both
national and local efforts to promote appropriate antibiotic use. In Knox
County, the reduced antibiotic prescribing was beyond that observed in the
control counties, as demonstrated by 2 measures: population-based prescription
rates and prescription to visit ratios. Since this study was not a controlled
clinical trial, it is possible that the observed reduction in prescribing
in Knox County was due to other unmeasured factors or to the greater influence
of temporal trends in a region with high baseline prescribing. However, the
strong temporal association of the "excess reduction" in antibiotic prescribing
that occurred coincident with the intervention confirmed our a priori hypothesis
and suggests that this was indeed an effect of the intervention.
To our knowledge, this is the first report to demonstrate reductions
in pediatric antibiotic prescribing as a consequence of a community-wide educational
intervention in a large urbanized setting. Of note, the magnitude of the intervention-attributable
reductions in antibiotic prescription rates reported herein was similar to
decreases reported in other recent interventions targeting pediatric antibiotic
use.17,18,32
Certain aspects of the intervention were noteworthy. The intervention
was spearheaded by the local county health department and conducted on a limited
budget using existing personnel. A coalition was developed that included key
members of the local medical community. The educational efforts engaged both
medical providers and parents, while also reaching the general public. Reductions
in prescribing were sustained for at least 1 year after Knox County's campaign
ended, though the greatest effect occurred during the intervention year. Although
encouraging, this suggests that interventions might need to be maintained
over longer periods.
The evaluation was limited to TennCare enrollees, which to some degree
controlled for access to care and socioeconomic factors. The effect of the
intervention on children of higher socioeconomic status, is not known. On
the other hand, the study population was large and represented a substantial
portion of the total pediatric population. Also, the exact mechanism by which
prescription rates were lowered in Knox County could not be ascertained. Although
prescriptions were not linked to actual visits, the prescription to visit
ratio provided a measure of the likelihood that a respiratory illness encounter
resulted in an antibiotic prescription. The decreased ratios of prescriptions
to visits suggest that, as a result of the educational intervention, Knox
County physicians adopted more stringent criteria for writing antibiotic prescriptions
and/or that parents' expectations for receiving prescriptions was reduced.
The intervention effect was greater among black children, even though
their baseline antibiotic prescription rates were lower. White children received
care for respiratory illnesses approximately twice as often as black children.
Higher rates of ambulatory health care among white children for otitis media
and other respiratory conditions have been described previously.33,34
The reasons why white children received physician care for respiratory illnesses
more often than black children in our study are unknown and could not be examined
directly. Because this study included only children who were covered by TennCare,
differences in access to care should have been minimized. Antibiotic prescription
rates also were approximately twice as high among white children as black
children. Consequently, much of the observed excess in antibiotic prescribing
at the intervention site appeared to be caused by the high proportion of white
children in Knox County. Within Knox County, and among the control sites,
prescribing levels among black and white children were similar when differences
in respiratory illness visit rates were accounted for. These data indicate
a need to examine the appropriateness of different levels of antibiotic and
ambulatory care use.
Younger children have the highest rates of antibiotic use.12
For example, prescription rates among children aged 1 to less than 5 years
were approximately twice as high as among children aged 5 to less than 15
years in our study. Therefore, educational interventions should target the
parents of preschoolers, as was done in Knox County. In fact, the largest
intervention effects in Knox County were observed among children aged 1 to
less than 5 years.
The correlation between levels of ambulatory care visits and antibiotic
prescriptions identified in our study suggests that the provider visit itself
could be a driving force behind antibiotic prescribing. In other words, unnecessary
office visits might precipitate unnecessary prescriptions.35-37
Therefore, more attention should be given to the education of parents and
child care center personnel regarding the appropriate indications for seeking
physician care and antibiotic treatment for children with acute respiratory
illnesses.
Among this study population, a general decline occurred across antibiotic
categories. A primary message of this intervention was that narrow-spectrum
antibiotics should be used preferentially. Our data indicated that even before
the intervention, narrow-spectrum penicillins dominated antibiotic use and
that, during the study period, the proportion of antibiotic use accounted
for by penicillins increased. Limited data were available regarding resistance
among invasive S pneumoniae isolates among Knox County
children. There was no indication of any decrease in pneumococcal resistance
1 year after the Knox County intervention; however, the sample size limited
our ability to detect modest changes in resistance. It is likely that further
sustained reductions in antibiotic use will be required to lower the prevalence
of antibiotic resistance among S pneumoniae and other
community-acquired bacterial pathogens. Clonal spread of resistant strains
is thought to contribute to their persistence after introduction to a community,1 and substantial time lags are expected to accompany
their disappearance.38
A national action plan to address the problem of antibiotic-resistant
infections in the United States was recently developed by a governmental task
force.5,39 Educational interventions
to counter the development and spread of microbial resistance through promotion
of responsible antibiotic use were identified as essential to this plan. The
decline in antibiotic prescribing documented after the Knox County intervention
should encourage these broader efforts.
1.Schrag SJ, Beall B, Dowell SF. Limiting the spread of resistant pneumococci.
Clin Microbiol Rev.2000;13:588-601.Google Scholar 2.Whitney CG, Farley MM, Hadler J.
et al. Increasing prevalence of multidrug-resistant
Streptococcus
pneumoniae in the United States.
N Engl J Med.2000;343:1917-1924.Google Scholar 3.Levy SB. Antibiotic resistance: an ecological imbalance.
Ciba Found Symp.1997;207:1-9.Google Scholar 4.Wenzel RP, Edmond MB. Managing antibiotic resistance.
N Engl J Med.2000;343:1961-1963.Google Scholar 5.Bell DM. Promoting appropriate antimicrobial drug use: perspective from the
Centers for Disease Control and Prevention.
Clin Infect Dis.2001;33(suppl 3):S245-S250.Google Scholar 6.Dowell SF, Marcy SM, Phillips WR, Gerber MA, Schwartz B. Principles of judicious antimicrobial agents for pediatric upper respiratory
tract infections.
Pediatrics.1998;101:163-165.Google Scholar 7.Jernigan DB, Cetron MS, Breiman RF. Minimizing the impact of drug-resistant
Streptococcus
pneumoniae (DRSP).
JAMA.1996;275:206-209.Google Scholar 8.Schwartz B, Bell DM, Hughes JM. Preventing the emergence of antimicrobial resistance: a call for action
by clinicians, public health officials, and patients.
JAMA.1997;278:944-945.Google Scholar 9.Bauchner H, Philipp B. Reducing inappropriate oral antibiotic use.
Pediatrics.1998;102:142-145.Google Scholar 10.Gonzales R, Bartlett JG, Besser RE.
et al. Principles of appropriate antibiotic use for treatment of acute respiratory
tract infections in adults.
Ann Intern Med.2001;134:479-486.Google Scholar 11.McCaig LF, Hughes JM. Trends in antimicrobial drug prescribing among office-based physicians
in the United States.
JAMA.1995;273:214-219.Google Scholar 12.Nyquist AC, Gonzales R, Steiner JF, Sande MA. Antibiotic prescribing for children with colds, upper respiratory tract
infections, and bronchitis.
JAMA.1998;279:875-877.Google Scholar 13.Barden LS, Dowell SF, Schwartz B, Lackey C. Current attitudes regarding use of antimicrobial agents: results from
physicians' and parents' focus group discussions.
Clin Pediatr (Phila).1998;37:665-671.Google Scholar 14.Bauchner H, Pelton SI, Klein JO. Parents, physicians, and antibiotic use.
Pediatrics.1999;103:395-401.Google Scholar 15.Schwartz B. Preventing the spread of antimicrobial resistance among bacterial respiratory
pathogens in industrialized countries: the case for judicious antimicrobial
use.
Clin Infect Dis.1999;28:211-213.Google Scholar 16.Gonzales R, Steiner JF, Lum A, Barrett Jr PH. Decreasing antibiotic use in ambulatory practice.
JAMA.1999;281:1512-1519.Google Scholar 17.Petersen KL, Hennessy TW, Parkinson AJ.
et al. Provider and community education decreases antimicrobial use and carriage
of penicillin-resistant Streptococcus pneumoniae
in rural Alaska communities. Presented at: 37th Annual Meeting of the Infectious Diseases Society
of America; November 18-21, 1999; Philadelphia, Pa. Abstract 62.
18.Belongia EA, Sullivan BJ, Chyou PH, Madagame E, Reed KD, Schwartz B. A community intervention trial to promote judicious antibiotic use
and reduce penicillin-resistant
Streptococcus pneumoniae carriage in children.
Pediatrics.2001;108:575-583.Google Scholar 19.Mainous III AG, Hueston WJ, Love MM, Evans ME, Finger R. An evaluation of statewide strategies to reduce antibiotic overuse.
Fam Med.2000;32:22-29.Google Scholar 20.Emigh RC. Novartis Pharmacy Benefit Report: 1999 Facts and
Figures. East Hanover, NJ: Novartis Pharmaceuticals Corp; 1999.
21.US Census Bureau, Population Estimates Program, Population Division. Population Estimates for Counties by Age and Sex:
Annual Time Series July 1, 1990 to July 1, 1999. Washington, DC: US Census Bureau; 2000. Document CO-99-9.
22.Perz JF, Craig AS, Jorgensen D, Hall S, Schaffner W. Evaluation of innovative surveillance for drug-resistant
Streptococcus pneumoniae. Am J Epidemiol.2001;154:1000-1005.Google Scholar 23.Craig AS, Erwin PC, Schaffner W.
et al. Carriage of multidrug-resistant
Streptococcus pneumoniae and impact of chemoprophylaxis during an outbreak of meningitis at
a day care center.
Clin Infect Dis.1999;29:1257-1264.Google Scholar 24.Belongia EA, Schwartz B. Strategies for promoting judicious use of antibiotics by doctors and
patients.
BMJ.1998;317:668-671.Google Scholar 25.Emmer CL, Besser RE. Combating antimicrobial resistance: intervention programs to promote
appropriate antibiotic use.
Infections Med.2002;19:160-173.Google Scholar 26.Arnold SR, Allen UD, Al Zahrani M.
et al. Antibiotic prescribing by pediatricians for respiratory tract infection
in children.
Clin Infect Dis.1999;29:312-317.Google Scholar 27.Mirvis DM, Chang CF, Hall CJ, Zaar GT, Applegate WB. TennCare—health system reform for Tennessee.
JAMA.1995;274:1235-1241.Google Scholar 28.World Health Organization. International Classification of Diseases, Ninth Revision
(ICD-9). Geneva, Switzerland: World Health Organization; 1977.
29.Schuchat A, Hilger T, Zell E.
et al. Active bacterial core surveillance of the Emerging Infections Program
Network.
Emerg Infect Dis.2001;7:92-99.Google Scholar 30.Cameron AC, Trivedi PK. Regression Analysis of Count Data. New York, NY: Cambridge University Press; 1998.
31.McCaig LF, Besser RE, Hughes JM. Decline in pediatric antimicrobial drug prescribing among office-based
physicians in the United States, 1989-1998. Presented at: 38th Annual Meeting of the Infectious Diseases Society
of America; September 7-10, 2000; New Orleans, La. Abstract 652.
32.Finkelstein JA, Davis RL, Dowell SF.
et al. Reducing antibiotic use in children: a randomized trial in 12 practices.
Pediatrics.2001;108:1-7.Google Scholar 33.Bondy J, Berman S, Glazner J, Lezotte D. Direct expenditures related to otitis media diagnoses: extrapolations
from a pediatric Medicaid cohort.
Pediatrics.2000;105:e72.Google Scholar 34.Freid VM, Makuc DM, Rooks RN. Ambulatory health care visits by children: principal diagnosis and
place of visit.
Vital Health Stat 13.1998;(137):1-23.Google Scholar 35.Watson RL, Dowell SF, Jayaraman M.
et al. Antimicrobial use for pediatric upper respiratory infections: reported
practice, actual practice, and parent beliefs.
Pediatrics.1999;104:1251-1257.Google Scholar 36.Pappas DE, Schwartz RH, Sheridan MJ, Hayden GF. Medical exclusion of sick children from child care centers.
South Med J.2000;93:575-578.Google Scholar 37.Skull SA, Ford-Jones EL, Kulin NA, Einarson TR, Wang EE. Child care center staff contribute to physician visits and pressure
for antibiotic prescription.
Arch Pediatr Adolesc Med.2000;154:180-183.Google Scholar 38.Austin DJ, Kristinsson KG, Anderson RM. The relationship between the volume of antimicrobial consumption in
human communities and the frequency of resistance.
Proc Natl Acad Sci U S A.1999;96:1152-1156.Google Scholar