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P

EDIATRICS

Feb 1999 VOL. 103 NO. 2 zzz zzz zzz zzz zz

Parents, Physicians, and Antibiotic Use

Howard Bauchner, MD; Stephen I. Pelton, MD; and Jerome O. Klein, MD

ABSTRACT. Background. Emergence of resistant bac-terial pathogens has increased concerns about antibiotic prescribing patterns. Parent expectations and pressure may influence these patterns.

Objective. To understand how parents influence the prescribing patterns of physicians and what strategies physicians believe are important if we are going to re-duce inappropriate use of oral antimicrobial agents.

Designs and Methods. One thousand pediatricians who are members of the American Academy of Pediatrics were asked to complete a semi-structured questionnaire. The physicians were chosen randomly by the American Academy of Pediatrics.

Results. Nine hundred fifteen pediatricians were el-igible and 610 surveys were analyzable, for a response rate of 67%. The majority of respondents were male (56%), worked in a group practice (51%), saw an average of 114 patients per week and were in practice for 14 years. Forty percent of the pediatricians indicated that 10 or more times in the past month a parent had requested an antibiotic when the physician did not feel it was indi-cated. Forty-eight percent reported that parents always, most of the time, or often pressure them to prescribe antibiotics when their children are ill but antibiotics are not indicated. In follow-up questions, approximately one-third of physicians reported they occasionally or more frequently comply with these requests. Seventy-eight percent felt that educating parents would be the single most important program for reducing inappropri-ate oral antibiotic use and 54% indicinappropri-ated that parental pressure, in contrast to concerns about legal liability (12%) or need to be efficient in practice (19%), contrib-uted most to inappropriate use of oral antibiotics.

Conclusions. Pediatricians acknowledge prescribing antimicrobial agents when they are not indicated. Pedi-atricians believe educating parents is necessary to pro-mote the judicious use of antimicrobial agents.Pediatrics

1999;103:395– 401;antibiotics, antimicrobials, parents, pe-diatricians.

ABBREVIATIONS. AOM, acute otitis media; AAP, American Academy of Pediatrics.

O

ver the past decade, decreasing susceptibility of Streptococcus pneumoniae to antimicrobial agents has been increasingly reported around the world.1–3S pneumoniaeis the most common caus-ative bacterial agent for meningitis, pneumonia, bac-teremia, acute otitis media (AOM), and sinusitis, and this pattern of resistance has profound implications for pediatrics.4 Some investigators have suggested that the emerging resistance among pneumococci is a result of increased use of antimicrobial agents.

In 1980, 4 206 000 prescriptions were written for amoxicillin for the treatment of AOM.5 In 1992, the number had grown to 12 381 000 —an increase of 194%. In 1980, 876 000 prescriptions for cephalospo-rins were recorded for the treatment of AOM; in 1992 the number was 6 892 000 —an increase of 687%. Based on these data, we estimate that in 1999, 30 000 000 prescriptions will be written for the treat-ment of AOM. The increase in prescriptions written for the treatment of AOM is attributable to at least three factors, including increase in real disease, due in part to widespread day care attendance, improved access to care, and overprescription of antimicrobial agents.6

The relationship between increased use of antimi-crobial agents and bacterial resistance is controver-sial, although many experts believe that use of inap-propriate antibiotics must be curtailed if we are going to reduce the prevalence of bacterial resis-tance.7–9In addition, previous antimicrobial use is a risk factor for bacterial disease caused by resistantS pneumoniae.10 –12The Centers for Disease Control and Prevention has announced a national plan to reduce the occurrence of bacterial resistance.13 The plan in-cludes community monitoring of resistance, limiting use of antimicrobial agents for diseases likely to be From the Divisions of General Pediatrics and Infectious Diseases, Boston

Medical Center, Boston University School of Medicine, Boston, Massachu-setts.

Received for publication Dec 5, 1997; accepted Jul 1, 1998.

Reprint requests to (H.B.) Boston Medical Center/Maternity 415, 818 Har-rison Ave, Boston, MA 02118.

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attributable to viruses, and encouraging clinicians to use narrow spectrum antimicrobials.

The American Academy of Pediatrics (AAP), The Centers for Disease Control and Prevention, and the American Society of Microbiology14recently released a pamphlet to educate parents about antibiotics. It emphasizes differences between viruses and bacte-ria, describes how resistant bacteria emerge, reviews appropriate indications for antibiotics, and counsels parents that all infections do not require antibiotics. Before we can change use of inappropriate oral antimicrobial agents, we need to understand what parents and physicians believe about their indica-tions. Recently we reported parents’ views about antibiotics.6 In a survey of 400 parents, approxi-mately one-half of the parents interviewed were con-cerned about the effect of antibiotics on the immune system. Many misunderstood appropriate indica-tions for antibiotics. Twenty percent had given anti-biotics to their children without consulting a physi-cian. As part of that study, we surveyed a small number of Massachusetts pediatricians about their experiences with parents about antibiotics. Using that survey as the basis for the current project, we have surveyed a national sample of pediatricians. The objective was to understand how parents influ-ence the prescribing patterns of physicians and what strategies physicians believe are important if we are going to reduce inappropriate use of oral antimicro-bial agents.

METHODS

A semi-structured questionnaire (see “Appendix”), previously piloted and then modified, was mailed to a random sample of 1000 pediatricians in the United States. Modifications included 1): an additional question about the pressure pediatricians feel to dispense antibiotics; 2) a change in the quantitative ranges that physicians could select as an answer to a number of the questions; and 3) a change in the choices about what physicians feel contrib-utes most to inappropriate oral antibiotic use and what they think is important to curtail such use. The pressure that pediatricians feel to dispense inappropriate oral antibiotics was asked twice, using two different time frames: 1) by quantifying how often this had happened in the past month; and 2) by describing how often this happens when children are ill (see “Appendix”). Following these two inquires (question 10 and question 16) follow-up ques-tions regarding how often the physician complied with these requests were asked. Quantitative ranges, so-called anchors, were provided for each descriptive term (see “Appendix”). These ranges were chosen during the piloting of the questionnaire.

The list of pediatricians was provided by the AAP. Resident fellows, emeritus fellows, and subspecialty fellows were excluded from the list in an attempt to focus solely on pediatricians in practice. After the initial mailing, a second and then a third mail-ing of the survey was sent to nonresponders 6 weeks to 2 months after the previously mailing. Retired and specialist pediatricians who responded to the questionnaire were considered ineligible.

Thex2statistic was used to describe differences in responses for

gender (male versus female), length of time in practice (,or$14 years), type (group versus solo versus other), location of practice (community health center versus staff model health maintenance organization versus urban noninner-city versus urban inner-city) and number of patients seen weekly (,or$the 114). The length of time in practice and number of patients seen weekly were used as a proxy for comparing experienced to less experienced physi-cians. Responses examined included the pressure parents exert on physicians to dispense antibiotics inappropriately (questions 10) and what program (question 19) and which issue (question 20) physicians believe most impacts on inappropriate antibiotic use. Multiple regression was used to simultaneously evaluate all the

potential confounding variables. The study was approved by the Human Investigation Committee of the Boston Medical Center.

RESULTS

Six hundred and eighty-seven surveys were re-turned, of which 77 were excluded from analysis because the physicians were retired (n530), special-ists (n 5 43), refused (n 5 1), or the address was unknown (n 5 3), leaving a final sample of 610. Assuming that the ineligibility rate was similar in those returned (73 out of 687) and not returned (n5 313) the final sample size of 610 represents a re-sponse rate of 67%.15

The majority of responders were male (56%), worked in a group practice (51%), saw an average of 114 patients per week and were in practice for 14 years (Table 1). Overall, 22% felt that most or many parents were worried about the number of antibiot-ics their children were receiving.

Ninety-six percent of pediatricians had parents re-quest antibiotics during the previous month when they were not indicated (Table 2). Forty percent re-ported that this occurred 10 or more times, 16% reported 7 to 9 times, 19% reported 4 to 6 times, and 20% reported 1 to 3 times. Forty-eight percent re-ported that parents always, most of the time, or often put pressure on them to prescribe antibiotics when their children are ill, but antibiotics are not clearly indicated (Table 2). In follow-up questions, approxi-mately one-third of the respondents reported that they occasionally or more frequently comply with the inappropriate request (Table 2).

Seventeen percent, 15%, and 24% of pediatricians, had parents request a specific antibiotic or a different one than they were going to prescribe 10 or more, 7 to 9 times, and 4 to 6 times during the previous month, respectively. Thirty percent of respondents had parents request antibiotics over the telephone 10 or more times in the previous month. The vast ma-jority (79%) rarely or never complied with this re-quest.

Educating parents was cited by 78% of respon-dents as the single most important program for re-ducing inappropriate oral antibiotic use (Table 3). This was in contrast to developing more careful di-agnostic criteria (15%), and reducing legal liability (4%) or drug detailing (,1%). Consistent with those

TABLE 1. Characteristics of Physicians Participating in Anti-biotic Survey (n5610)

Gender (% male) 56

Years in practice (median, range) 14 (1–66) Location of practice (%)

Urban, inner city 14

Urban, noninner city 23

Suburban 46

Rural 15

Other 2

Description of practice (%)

Solo, or two physicians 24

Group 51

Staff model health maintenance organization 6

Community health center 5

Hospital outpatient clinic 7

Other 7

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responses, 54% indicated that parent pressure con-tributed the most to inappropriate use of oral antibi-otics (Table 3).

Differences in responses did emerge with respect to certain sociodemographic factors and selected out-comes. Physicians who see more patients ($114 per week) were more likely to report that parents pres-sured them 101 times in the previous month to dispense antibiotics (51% vs 31%, P , .001). The same was true for physicians who practice in a rural setting (56%) versus those in suburbia (43%), urban noninner-city (36%) or urban inner-city (26%, P , .001); and those in group practice (49%) versus solo (36%) or other (28%,P,.001). No sociodemographic factor impacted on either single most important pro-gram for reducing antibiotic use or which issue con-tributes most to inappropriate antibiotic use. Less experienced physicians (,14 years in practice) were more likely to cite parent education as the single most important program for reducing inappropriate antibiotic use (81% vs 73%,P5.08). Similar findings emerged from multiple regression analysis, with busier physicians (P , .001), those practicing in a rural setting (P5 .001), and those in group practice (P 5 .026) more likely to report that parents pres-sured them 101 times in the previous month to dispense antibiotics inappropriately. In addition, in the multiple regression, females (80%) listed parent education as more important than males (75%, P 5 .035).

DISCUSSION

In this survey, physicians responded that they ac-quiesce to parent pressure and prescribe

antimicro-bial agents when they are not indicated. The physi-cians believe that parents must be reeducated if inappropriate antimicrobial use is to decline. Physi-cians did not report that more careful diagnostic criteria, reducing drug detailing, or legal liability or the need to be efficient in practice were nearly as important as educating parents. In a recent editorial, Edwards16commented that in a era of managed care and an emphasis on efficiency in practice, sufficient time may not be available to discuss issues about antibiotics.

Changing antimicrobial prescribing habits is likely to be easier in the hospital then in the outpatient setting. The use of restricted formularies and the need to obtain previous approval in the hospital limits antimicrobial choice. These restrictions are less available in the ambulatory setting. To reduce use of inappropriate antimicrobial agents in the ambulatory setting we need to alter patient-physician communi-cation.

This study has a number of limitations. We relied on physician self-report. It is possible that there are differences between what physicians report and what actually occurs. However, it is unlikely that physicians prescribe inappropriate antimicrobials less than reported, although it is possible that they misinterpret parent expectations. Second, in any sur-vey, there is always concern whether the nonre-sponders differ from the renonre-sponders. We have no information on the nonresponders, although the re-sponse rate approached 70%. In addition, the demo-graphic characteristics of the responders are similar to AAP periodic surveys of its membership,17 sug-gesting that this sample is representative of pediatri-cians who are members of the AAP.

There have been a number of studies that have addressed the issue of patient expectations for anti-microbial agents, although the majority have focused on adults. Recently, Macfarlane18reported in a study of 787 adults with lower respiratory tract illness, that they often believe that infection is the problem and antibiotics are the answer. Even when the doctor judges that antibiotics are not indicated, patients’ expectations increase the likelihood that antibiotics will be prescribed.18 Vinson and Lutz19 asked clini-cians to indicate, after a visit with families, if they sensed that parents of acutely ill children wanted an antibiotic. In a study of 1398 patients, they found that TABLE 2. Percentage of Physicians Experiencing Parent

Request for Unnecessary Antibiotics and How Often They Com-plied With Request

Number of times in past month parents requested unnecessary antibiotics

0 — 4%

1–3 — 20%

4–6 — 19%

7–9 — 16%

101 — 40%

Frequency that physicians complied with request

Always — 1%

Most of the time — 2%

Often — 7%

Occasionally — 24%

Rarely — 44%

Never — 22%

Frequency that parents pressured physicians to dispense antibiotics when child ill, but antibiotics not indicated

Always — 1%

Most of the time — 9%

Often — 38%

Occasionally — 38%

Rarely — 13%

Never — 1%

Frequency that physicians complied with request

Always — ,1%

Most of the time — 1%

Often — 6%

Occasionally — 23%

Rarely — 46%

Never — 24%

TABLE 3. Factors Cited by Pediatricians as Influencing Inappropriate Oral Antibiotic Use

Single most important program for reducing inappropriate oral antibiotic use

Develop more careful diagnostic criteria — 15%

Reduce drug detailing — ,1%

Reduce legal liability — 4%

Educate parents about appropriate indications — 78%

Other — 4%

Issue that contributes most to inappropriate oral antibiotic use

Concerns about legal liability — 12% Need to be efficient in practice — 19%

Parent pressure — 54%

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physician perception of parental expectations for an-tibiotics was associated with a diagnosis of bronchitis and prescribing an antibiotic.19 Hamm et al20 found that 65% of 113 adult patients with respiratory infec-tions expected antibiotics. Physicians had some abil-ity to perceive this expectation and frequently pre-scribed antibiotics for patients who expect them. Interestingly, no association was found between a prescription for antibiotics and patient satisfaction.

The physicians who responded to this survey cited parent pressure has the most important issue that impacts on the use of inappropriate oral antibiotics. There are data that suggest that clinicians do not always follow diagnostic criteria carefully and indi-cations for antimicrobials. Recently, Schwartz and colleagues21 reported that many pediatricians and family practitioners dispense antibiotics for rhinor-rhea lasting only a couple of days. Gonzales and others,22 in an analysis from the National Ambula-tory Medical Care Survey, reported that office visits for colds, upper respiratory tract infections, and bronchitis resulted in;12 million antibiotic prescrip-tions to adults.21It is likely that this also occurs in the pediatric population. It is not clear when physicians dispense antimicrobials for reasons that are not con-sidered appropriate by some clinicians if they are responding to patient pressure, issues related to sat-isfaction, their beliefs that antimicrobials help in these circumstances, legal liability, need to be effi-cient in practice, or misunderstand diagnostic criteria and indications for antimicrobials. It is likely that all these issues contribute to the use of inappropriate oral antimicrobial agents.

Changing physician behavior is complex. Davis and others23 reported in a metaanalysis of 99 trials that four strategies: reminders, patient-mediated in-terventions, outreach visits, and opinion leaders were effective in changing physician behavior. Of these, patient-mediated strategies are particularly ef-fective when physicians are ready to change their practice. Pathman and colleagues24 found that phy-sicians who disagreed with indications for hepatitis B vaccine or varicella vaccine, nevertheless adminis-tered the vaccines if parents requested them. These data and those reported in this survey suggest that educating parents about appropriate indications for antimicrobials must be part of any comprehensive plan to reduce inappropriate oral antibiotic use. It is possible that if parents are educated about appropri-ate indications for oral antimicrobials, they may not only pressure physicians less to dispense antibiotics, but also influence physician behavior by appropri-ately questioning the role that antibiotics play in the treatment of some medical conditions.

Pediatricians need to promote the judicious use of antimicrobial agents. We believe that the approach to the problem of inappropriate oral antimicrobial use must be balanced: parents must be reeducated, either directly by clinicians or through public health cam-paigns; and physicians need to sharpen their diag-nostic skills and become more familiar with specific indications for antibiotic.25,26

ACKNOWLEDGMENTS

This work was supported in part with grants from the Bureau of Health Professions (Faculty Development Award and Institu-tional NaInstitu-tional Research Service Award).

The authors would like to thank Chris McElroy for her spirited views on this subject. Beth Kastner and Colleen Pearson were once again invaluable in this research endeavor.

REFERENCES

1. Friedland IR, McCracken GH Jr. Management of infections caused by antibiotic-resistantStreptococcus pneumoniae. N Engl J Med. 1994;331: 377–382

2. Tomasz A. The Pneumococcus at the gate.N Engl J Med.1995;333: 514 –515

3. Hofmann J, Cetron MS, Farley MM, et al. The prevalence of drug-resistantStreptococcus pneumoniaein Atlanta.N Engl J Med.1995;333: 481– 486

4. Barnett ED, Klein JO. The problem of resistant bacteria for the manage-ment of acute otitis media.Pediatr Clin North Am.1995;42:509 –517 5. McCaig LF, Hughes JM. Trends in antimicrobial drug prescribing

among office-based physicians in the United States.JAMA. 1995;273: 214 –219

6. Palmer D, Bauchner H. Parents’ and physicians’ views on antibiotics. Pediatrics. 1997;99(6). URL: http://www.pediatrics.org/cgi/content/ full/99/6/e6

7. Murray B. Can antibiotic resistance be controlled?N Engl J Med.1994; 330:1229 –1230

8. Tomasz A. Multiple-antibiotic-resistant pathogenic bacteria—a report on the Rockefeller University workshop.N Engl J Med. 1994;330: 1247–1251

9. Lederberg J. Infection emergent.JAMA. 1996;275:243–245

10. Arnold KE, Leggiadro RJ, Breiman RF, et al. Risk factors for carriage of drug-resistantStreptococcus pneumoniae.J Pediatr. 1996;128:757–763 11. Tan TQ, Mason EO Jr, Kaplan SL. Penicillin-resistant systemic

pneumo-coccal infection in children: a retrospective case-control study. Pediat-rics. 1993;92:761–767

12. Robins-Browne RM, Khasany ABM, Koornhof HJ. Antibiotic-resistant pneumococci in hospitalized children.J Hyg. 1984;93:9 –16

13. Berkelman RL, Pinner RW, Hughes JM. Addressing emerging microbial threats in the United States.JAMA. 1996;275:315–320

14. American Academy of Pediatrics, Centers for Disease Control and Prevention, American Society for Microbiology.Your Child and Antibi-otics. 1997

15. Council of American Survey Research Organizations.On the Definition of Response Rates; a Special Report From the CASRO Task Force on Comple-tion Rates. Port Jefferson, NY: Council of American Survey Research Organizations; 1982

16. Edwards KM. Resisting the urge to prescribe.J Pediatr.1996;128:729 –730 17. Campbell JR, Schaffer SK, Szilagyi PG, et al. Blood lead screening

practices among US Pediatricians.Pediatrics. 1996;98:372–377 18. Macfarlane J, Holmes W, Macfarlane R, Britten N. Influence of patients’

expectations on antibiotic management of acute lower respiratory tract illness in general practice: questionnaire study.Br Med J.1997;315: 1211–1214

19. Vinson DC, Lutz L. The effect of parental expectations on treatment of children with a cough: a report from ASPN.J Fam Pract.1993;37:23–27 20. Hamm RM, Kicks RJ, Bemben DA. Antibiotics and respiratory infections: are patients more satisfied when expectations are met.J Fam Pract.1996;43:56 – 62

21. Schwartz RH, Freij BJ, Ziai M, Sheridan MJ. Antimicrobial prescribing for acute purulent rhinitis in children: a survey of pediatricians and family practitioners.Pediatr Infect Dis J.1997;16:185–190

22. Gonzales R, Steiner JF, Sande MA. Antibiotic prescribing for adults with colds, upper respiratory tract infections, and bronchitis by ambulatory care physicians.JAMA.1997;278:901–904

23. Davis DA, Thomson MA, Oxman AD, Haynes B. Changing physician performance—a systematic review of the effect of continuing medical education strategies.JAMA.1995;274:700 –705

24. Pathman DE, Konrad TR, Freed GF, et al. The awareness-to-adherence model of the steps to clinical guideline compliance.Med Care.1996;34: 873– 889

25. Bauchner H, Philipp B. Reducing inappropriate oral antibiotic use: a prescription for change.Pediatrics. 1998;102:142–145

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DOI: 10.1542/peds.103.2.395

1999;103;395

Pediatrics

Howard Bauchner, Stephen I. Pelton and Jerome O. Klein

Parents, Physicians, and Antibiotic Use

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DOI: 10.1542/peds.103.2.395

1999;103;395

Pediatrics

Howard Bauchner, Stephen I. Pelton and Jerome O. Klein

Parents, Physicians, and Antibiotic Use

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by the American Academy of Pediatrics. All rights reserved. Print ISSN: 1073-0397.

Figure

TABLE 1.Characteristics of Physicians Participating in Anti-biotic Survey (n � 610)
TABLE 2.PercentageofPhysiciansExperiencingParentRequest for Unnecessary Antibiotics and How Often They Com-plied With Request

References

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