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* HMO Research Network Centers for Education and Research on Therapeutics
Department of Ambulatory Care and Prevention, Harvard Medical School and Harvard Pilgrim Health Care, Boston, Massachusetts
Division of General Pediatrics, Children’s Hospital Boston, Boston Massachusetts
|| Meyers Primary Care Institute and Department of Pediatrics, University of Massachusetts Medical School, Worcester, Massachusetts
¶ HealthPartners Research Foundation, Minneapolis, Minnesota
# Group Health Cooperative and Departments of Pediatrics and Epidemiology, Schools of Medicine and Public Health, University of Washington, Seattle, Washington
** Clinical Research Unit, Kaiser Permanente of Colorado, Denver, Colorado
Kaiser Permanente Georgia Region, Atlanta, Georgia
Division of Research, Kaiser Permanente Northern California, Oakland, California
|||| Kaiser Permanente Center for Health Research, Portland, Oregon
¶¶ Henry Ford Health System, Detroit, Michigan
## Channing Laboratories, Brigham and Women’s Hospital, Boston, Massachusetts
*** Harvard School of Public Health, Boston, Massachusetts
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ABSTRACT |
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 TOP ABSTRACT METHODSRESULTSDISCUSSIONREFERENCES |
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Objective. We sought to assess changes in the rate of antibiotic prescribing from 1996–2000 in 9 US health plans, patterns of diagnosis and treatment responsible for these trends, and changes in the use of first-line antimicrobial agents.
Design/Methods. We analyzed claims data for dispensed medications and physician visits from 9 health plans. Each provided data on 25 000 children aged 3 months to <18 years enrolled between September 1, 1995, and August 31, 2000. Antibiotic dispensings were linked with an ambulatory visit claim to assign diagnosis. Antibiotic dispensings per person-year (antibiotics/p-y) were calculated for the age groups 3 months to <3 years, 3 years to <6 years, and 6 years to <18 years. The contribution of each diagnosis to changes in the overall rate of antibiotic use was determined. Generalized linear mixed models were used to test for trend and assess differences in rates by site.
Results. From 1996–2000, antibiotic rates for children 3 months to <3 years decreased from 2.46 to 1.89 antibiotics/p-y (24%); for children 3 years to <6 years from 1.47 to 1.09 antibiotics/p-y (25%); and for children 6 to <18 years from 0.85 to 0.69 antibiotics/p-y (16%). The reduction varied among health plans from 6% to 39% for children 3 months to <3 years. A decrease in prescriptions for otitis media accounted for 59% of the total decrease, and was primarily accounted for by a decrease in the rate of diagnosis of this condition. The proportion of first-line penicillins increased from 49% to 53%, with health plans with the lowest initial rates increasing most.
Conclusions. Antibiotic prescribing decreased significantly between 1996 and 2000, concurrent with decreased frequency of diagnosis of potential bacterial infections, especially otitis media. Attention by public health and professional organizations and the news media to antibiotic resistance may have contributed to changes in diagnostic thresholds, resulting in more judicious prescribing.
Key Words: antibiotics • otitis media • upper respiratory infection
Abbreviations: CDC, Centers for Disease Control and Prevention • URI, upper respiratory infection • NAMCS, National Ambulatory Medical Care Survey • HMO, Health Maintenance Organization • CERTs, Centers for Education and Research on Therapeutics • NDC, National Drug Code • ICD-9, International Classification of Diseases, Ninth Revision • OME, otitis media with effusion • p-y, person-years
Antibiotic resistance is considered a public health crisis in the United States.1–3 National estimates of nonsusceptibility to penicillin of Streptococcus pneumoniae, for example, increased from 16% in 19944 to 24% in 1998,5 with rates well over 50% reported from some child care settings.6–8 A multiagency federal action plan recently recommended decreasing unnecessary antibiotic prescribing as critical to combatting antimicrobial resistance.2 Because children have the highest rates of antibiotic use,9 the Centers for Disease Control and Prevention (CDC) has, since 1998, promoted a campaign to encourage judicious antibiotic prescribing for children, and has engaged the American Academy of Pediatrics, the American Academy of Family Physicians, state health departments, and health plans in this effort.10
Increasing antibiotic use in children from 1977 through the early 1990s is well-documented.9,11 This coincided with increases in the proportion of children in group child care12 and increases in the incidence of diagnosed otitis media,13 the most frequent condition associated with antibiotic prescriptions for children.14 Some studies suggest high rates of prescribing for viral diagnoses such as viral upper respiratory infection (URI) or bronchitis,15 but health plan-based analyses suggest that clearly inappropriate indications account for only a small minority of prescriptions written.14
A study based on the National Ambulatory Medical Care Survey (NAMCS) recently reported a substantial downward trend in antibiotic use for children, especially for otitis media.16 A separate NAMCS analysis17 showed a decrease in prescribing among children diagnosed with viral URIs from 1995–1998, but the fraction treated by pediatricians (38%) still far exceeds that reported elsewhere.14 The NAMCS monitors practice for 1-week periods in specified medical practices, selected to be representative of US medical care. Although these estimates have been extrapolated to the entire US population, NAMCS does not measure directly the patient denominator of reported rates. These office-based data do not include antibiotics prescribed without an office visit (eg, after a telephone encounter) or refills of an existing prescription.
The Health Maintenance Organization (HMO) Research Network Center for Education and Research on Therapeutics (CERTs) is a coalition of 9 geographically dispersed health plans that collaborate in research.18 Analysis of health plan enrollment files allows precise determination of population denominators, and pharmacy claims identify all antibiotics dispensed, whether prescribed by telephone, office visit, or dispensed as refills. Dispensing events after an office visit can be linked to the diagnosis given at that encounter.14 We used these data linkage capacities to study changes in antibiotic prescribing patterns for children from 1996–2000. In particular, we sought to assess the overall trends in antibiotics received, trends in use of particular antibiotic classes, and the fraction of the change in prescribing attributable to common respiratory tract illness diagnoses. We focused on patterns of antibiotic use among infants and children younger than 3 years in whom the rates of antibiotic use are highest.
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METHODS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
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Trends in prescribing and differences among health plans were analyzed for statistical significance using generalized linear mixed models20 for Poisson regression on the rates of use. This was done to account for the clustering of observations across time within each health plan. The results are presented in terms of the actual measured rates in each health plan and the sample overall. The percentage decline over the 5-year period is reported, accounting for clustering and assuming a linear trend. All analyses were conducted using SAS statistical software, version 8 (SAS Institute, Cary, NC). The study was approved by Institutional Review Boards of each of the 9 participating sites.
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RESULTS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
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We present population-based rates of each condition for the 5-year study period overall (Fig 1), excluding dispensings not linked to a visit (20%) or with no diagnosis provided (3%). Among children 3 months to <3 years, otitis media (including acute otitis media and OME) was responsible for the majority 1.22 antibiotics/p-y (antibiotic dispensings per person-year) (68%) of antibiotic dispensings. Other respiratory tract conditions were, together, responsible for an additional 0.33 antibiotics/p-y (18)%: sinusitis, 0.08 antibiotics/p-y (4%); pharyngitis, 0.07 antibiotics/p-y (4%); pneumonia, 0.05 antibiotics/p-y (3%); bronchitis, 0.04 antibiotics/p-y (2%); and cold/URI 0.09, antibiotics/p-y (5%). An additional 0.19 antibiotics/p-y (9%) of prescriptions were associated with nonspecific viral or noninfectious diagnoses or with well-child care visits. Soft tissue infections, urinary tract infections, and rare, but more serious, bacterial infections were all represented in these data, but account for a small minority (0.05 antibiotics/p-y [3%]) of antibiotic prescriptions among young children, and are grouped under "other-bacterial." The distributions of diagnoses associated with antibiotic dispensings for children aged 3 to <6 years and those aged 6 to <18 years are also provided (Fig 1). The rate of antibiotic use was dramatically lower in older age groups with 0.47 antibiotics/p-y (46%) and 0.12 antibiotics/p-y (22%) accounted for by otitis media in children 3 to <6 years and children 6 to <18 years, respectively. Not surprisingly, pharyngitis and sinusitis accounted for increasing proportions of antibiotics in older children. Combined prescribing for cold/URI and bronchitis accounted for 7%, 8%, and 9% of antibiotics in the 3 age groups, respectively.
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There were few notable trends in the proportion of cases treated within each diagnosed condition. For example, the proportions of otitis media (76%), sinusitis (84%), and pneumonia (62%) treated with an antibiotic remained constant. (These estimates include follow-up visits for these conditions, so they are lower than would be expected for new episodes only.) The proportion of those diagnosed with bronchitis, considered an inappropriate indication for antibiotics, who were treated with antibiotics decreased from 72% to 67% among all age groups combined and from 61% to 56% among children 3 months to 3 years. The proportion of visits with a cold/URI diagnosis associated with a prescription also decreased from 15% to 10% overall, and from 12% to 8% in the youngest age group.
The decrease in treatment of otitis media accounted for 59% of the total decrease in antibiotics prescribed among children 3 months to 3 years (Table 2). The proportions of the decrease in prescribing attributable to other respiratory tract infections were smaller in this age group. Eight percent of the decrease was attributable to prescribing for cold/URI, 6% for pharyngitis, and 3% and 4% for sinusitis and bronchitis, respectively. Also in this age group, 14% of the decrease was accounted for by a decrease in antibiotics not associated with an ambulatory encounter in the prior 3 days. Among children 3 to <6 years and 6 to <18 years, otitis media also accounted for substantial proportions of the decrease in antibiotics (47% and 31%, respectively), although the absolute rates of prescribing are lower than in younger children. With increasing age, a larger proportion of the decrease in antibiotic use was attributable to less treatment of pharyngitis, accounting for 13% and 30% of the decrease in the 3- to <6- and 6- to <18-year-old age groups. The decrease in antibiotic use overall in the 2 older age groups was partially attributable to bronchitis (6% and 11%) and sinusitis (10% and 16%). Decreased prescribing for cold/URI accounted for only 5% of the decrease in overall antibiotic use in children 3 to <6 and 6 to <18 years.
Despite increasing antibiotic resistance, most authorities continue to recommend amoxicillin as the agent of choice for community-acquired upper respiratory tract infections in children. Among children 3 to <3 years, first-line penicillin use, as a proportion of antibiotics dispensed, rose slightly from 48% (range among health plans: 35%–58%) of all antibiotic dispensings in 1996% to 53% (range among health plans: 43%–60%) in 2000. Prescribing of trimethoprim-sulfamethoxizole decreased most dramatically from 19% to 10% of dispensings over the same period. The largest percentage increase was for broad-spectrum macrolides, which increased from 2% to 8% concurrent with the introduction of clarithromycin and azithromycin. Patterns of use according to drug class were similar in the older age groups. By 2000, first-line penicillins accounted for 59% of antibiotics among children 3 to <6 years and those 6 to <12 years. Among children 12 to <18 years, first-line penicillins accounted for only 34%, primarily because of increased proportions of tetracyclines (23%) and macrolides (15%).
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DISCUSSION |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
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225 000 children from 9 health plans across the United States. The results show that antibiotic use in children has decreased markedly from 1996–2000. Although decreases were found in all 9 health plans and across all age groups, there was substantial variation among the health plans in rates of antibiotic use and in the magnitude of decrease. Linking each dispensing to a primary diagnosis allowed us to analyze the changes in antibiotics prescribed for a range of common conditions. Although otitis media continues to account for the majority of antibiotic use in children, a decrease in the number of cases accounts for most of the decrease in antibiotic use overall. The percent of diagnosed cases of otitis media, bronchitis, and sinusitis treated with antibiotics remained relatively constant over this same period. Finally, there is evidence for some increase in the use of first-line penicillins, as recommended by national guidelines.21 A recent report using the NAMCS reported a downward trend of 40% in antibiotic use for children and adolescents over the decade of the 1990s.16 The NAMCS collects data on ambulatory visits for a 1-week period in selected practices. Statistical techniques are then used to estimate population-based rates. In contrast, our study uses direct estimates of the denominator of enrolled children who both did and did not have medical care contact during a period of interest. Health plan data also capture antibiotics dispensed without an office visit, such as patient-initiated refills and prescriptions made by clinicians after evaluation of a patient by telephone. That these 2 studies, using different methods, show similar results is strong evidence that these trends are real. Confidence in the results is further bolstered by the consistency observed across the 9 distinct populations studied here.
The increase in antibiotic use in the 1980s9 occurred in concert with a rapid increase in the rate of diagnosis of otitis media.13,22 Whether this represented the use of lower diagnostic thresholds for this potential bacterial infection or an actual increase in its incidence is difficult to assess. Increased use of group child care may have led to more infectious illness in young children23–25 but probably does not explain the entire increase. Pressure on clinicians to see patients more quickly has also been raised as a contributing factor.26 Finally, parental pressure or antibiotic demand is cited by clinicians as an important driver of antibiotic overprescribing.26 Gaps in parental knowledge regarding appropriate indications for antibiotic use have been documented,27 although such parental pressure to prescribe may be overestimated.28,29
Competing explanations likewise exist for the observed decrease in antibiotic use. A decrease in population-based rates of use may reflect: 1) lower rates of care-seeking for acute illness by the population; 2) lower rates of diagnosis of potential bacterial infections when care is sought; or 3) less frequent treatment of infections presumed to be bacterial (eg, using a watchful waiting approach for some cases of acute otitis media). These data show a small decrease in visit rates overall, which may account for a portion of the observed reduction in antibiotic use. However, reduced prescribing is primarily accounted for by lower rates of diagnosis of bacterial infections, most notably otitis media in younger children (accounting alone for 59% of the decrease in prescribing) and a combination of otitis media, pharyngitis, and sinusitis in older children (accounting for 78% of the decrease in those 6 to <18 years). It is unlikely that changes in the epidemiology of disease account for the lower proportion of acute illness visits given a bacterial diagnosis. Haemophilus influenzae vaccine was introduced well before this study period, and pneumococcal conjugate vaccine was introduced only at the very end, so neither can account for the trends observed. Therefore, we conclude that the change in these patterns likely reflects changes either in likelihood of parents seeking care for these conditions, or in the criteria or thresholds clinicians use for assigning bacterial diagnoses.
The proportion of cases treated within each diagnosis was relatively stable. Attention has recently focused on the modest benefit of antibiotic treatment on a number of common conditions30–32; adoption of a watchful waiting approach for otitis media has been advocated by some.33,34 The data reported here show little change in clinicians’ treatment under each diagnostic label. This suggests that it may be more difficult to persuade clinicians to withhold treatment for minor infections than to adjust their diagnostic thresholds toward more judicious antibiotic use. Given this, one might expect to see the rates of OME increase as an alternative diagnosis to acute otitis media.35 We observed no such increase, suggesting that clinicians may be currently considering tympanic membranes normal that they previously would have diagnosed as having acute infection.
The diagnoses of cold/URI and bronchitis deserve special mention. Previous studies using NAMCS data have reported very high rates of antibiotic prescribing for cold/URI, which are considered inappropriate indications for antibiotic treatment.15,17 In previous health plan-based studies and in these data as well, the proportion of children with these viral diagnoses receiving antibiotics is much smaller.14 This does not prove that clinicians in these health plans do not prescribe for colds; rather, it shows that their assignment of diagnoses is more consistent with the treatment chosen. Cough illness, even characterized by deep cough, is generally viral.36 However, physicians in practice (and patients) use the diagnosis of bronchitis as an indication for antibiotics. The proportion of children with this diagnosis who received antibiotic treatment remains >60%—against current expert recommendations. If physicians become convinced that bronchitis is not an appropriate indication for antibiotic treatment, they may use competing diagnoses with overlapping symptoms, such as sinusitis, for which antibiotics are indicated according to recent guidelines.37
The strengths of health plan data for epidemiologic analyses have been described elsewhere,38 but these results must be interpreted with a number of caveats. First is the concern that the patients and physicians represented in data from these health plans are not representative of general medical care in the United States. The consistency of the findings across geographic regions and delivery system type, however, argues for generalizability across these features. Many of the clinicians represented in the data of 5 of the included health plans provide care to patients of many insurers within their geographic areas. We drew random samples of 25 000 members from each plan. This number allowed us to determine very precise estimates of rates of prescribing, while simplifying data management processes and giving equal weight in our analysis to each of the represented health plans. Though Medicaid members are represented in the data of 6 of these plans, they represent a small minority of enrollees. Therefore, we cannot make reliable inferences about care for low-income children or for those without health insurance. Finally, we lack information on any drugs that were not billed to the health plans. These account for a small proportion of antibiotics overall, but would include drug samples given in the office or those paid for completely out-of-pocket or billed to a second insurer. Furthermore, we have no reason to believe that the fraction of antibiotics dispensed in these ways changed over the period of study.
The substantial decrease in antibiotic prescribing is rightfully hailed as a victory for public health campaigns, but is also likely a reflection of increased patient and clinician awareness of antibiotic overuse and resistance from other sources. Our data highlight how changing diagnostic patterns are intimately connected with current and presumably future antibiotic use rates among children. For example, it may be more fruitful to ask clinicians to use stricter criteria for the somewhat subjective diagnosis of acute sinusitis than to ask them to recommend symptomatic care alone for diagnosed cases, as recommended in guidelines for adults.39,40 As we achieve the goal of reducing unnecessary antibiotic exposure for children, it will be critical to continue to monitor changes in patterns of resistance of common pathogens such as S pneumoniae in the community to gauge the benefit of decreased prescribing. Conversely, it will be critical to carefully monitor rates of mastoiditis and other rare complications of common bacterial infections as clinicians and parents raise their thresholds for using antibiotics. Such ongoing assessment will allow a more fully informed consideration of the risks and benefits of antibiotic use by children in an era of increasing resistance.
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ACKNOWLEDGMENTS |
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We are indebted to Courtney Adams for her tireless work in coordinating the project; Parker Pettus for his meticulous analysis of the data; and the data analysts at each of the participating health plans, without whom this work could not have gone forward.
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FOOTNOTES |
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Address correspondence to Jonathan A. Finkelstein, MD, MPH; Department of Ambulatory Care and Prevention, Harvard Medical School and Harvard Pilgrim Health Care, 133 Brookline Ave, 6th Floor, Boston, MA 02215. e-mail: jonathan_finkelstein{at}hphc.org
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