Physician Perspectives Regarding Annual InfluenzaVaccination Among Children With Asthma

Kevin J. Dombkowski, DrPH, MS; Sonia W. Leung, MD; Sarah J. Clark, MPH

Objective.—National guidelines have historically varied forinfluenza vaccination of children with asthma, depending onasthma severity. This study aims to explore perspectives of pri-mary care physicians regarding influenza vaccination practicesfor children with persistent versus intermittent asthma.

Methods.—A cross-sectional survey was mailed to general pedi-atricians (n ¼ 300) and family physicians (n ¼ 300) in primarycare offices in Michigan in 2006. The main outcome measures in-cluded physicians’ influenza vaccination recommendations andreasons for nonadministration of influenza vaccine to childrenwith asthma for the 2005–2006 influenza season.

Results.—Ninety-six percent of respondents (N ¼ 320) reportedroutinely recommending influenza vaccination for children withpersistent asthma; fewer (82%) reported routinely recommendinginfluenza vaccination for those with intermittent asthma. The ad-justed odds of recommending influenza vaccination for intermit-tent asthma patients was significantly higher among pediatriciansversus family physicians (adjusted odds ratio 3.49, 95% confi-dence interval, 1.68–7.22), controlling for other practice charac-

teristics. Regardless of specialty, physicians with more than 25asthma patients were more likely than those with fewer asthmapatients to routinely recommend influenza vaccination. Physi-cians who do not routinely recommend influenza vaccination tochildren with intermittent asthma were more likely to cite over-looking discussion of influenza vaccine during the visit (50% vs13%, respectively; P < .0001) as a reason for lack of vaccination.

Conclusions.—Influenza vaccination practices of primary carephysicians reflect the inconsistencies historically found in na-tional recommendations. Further research is warranted to deter-mine whether the recent clarification of recommendations of theNational Asthma Education and Prevention Program (NAEPP)to remove distinctions by asthma severity is associated witha reduction in missed opportunities to vaccinate.

KEY WORDS: asthma; guidelines; influenza vaccination;survey

Ambulatory Pediatrics 2008;8:294–9

Children with high-risk conditions, includingasthma, are at increased risk for influenza-relatedmorbidity and mortality.1–5 The National Asthma

Education and Prevention Program (NAEPP), coordinatedby the National Heart, Lung, Blood Institute, publishedguidelines over a decade ago for the diagnosis and manage-ment of asthma, including specific recommendations re-garding influenza vaccination.6 The Advisory Committeeon Immunization Practices (ACIP) also publishes annualinfluenza vaccination recommendations for persons withasthma and other chronic diseases.7 The ACIP recommen-dations are harmonized with those of the American Acad-emy of Pediatrics and the American Academy of FamilyPhysicians to ensure consistency between each of these or-ganizations. Despite these long-standing recommenda-tions, most children with asthma do not receive influenzavaccination.8–14 Missed opportunities—visits when a vac-cine-eligible child is seen by a health care provider, yet novaccine is administered—have been identified as one con-tributor to low influenza vaccination rates among childrenwith asthma.10–13

From the Child Health Evaluation and Research Unit, Division of

General Pediatrics, University of Michigan, Ann Arbor, Mich.

Address correspondence to Kevin J. Dombkowski, DrPH, MS, Univer-

sity of Michigan, Division of General Pediatrics, 300 N Ingalls, Ann

Arbor, Michigan 48109-0456 (e-mail: kjd@med.umich.edu).

Received for publication July 19, 2007; accepted June 23, 2008.

AMBULATORY PEDIATRICSCopyright � 2008 by Academic Pediatric Association 29

Although the underlying reasons for missed opportuni-ties for influenza vaccination among children with asthmaare not well understood, there is evidence indicating thatphysicians may experience difficulties in identifyinghigh-risk children.15 One aspect of this difficulty may bethe result of inconsistencies in national influenza recom-mendations; the ACIP recommends annual influenzavaccination for all persons with asthma,7 whereas NAEPPguidelines have historically focused on individuals withpersistent asthma.6 Thus, NAEPP guidelines have implic-itly required that a patient have persistent asthma to beconsidered eligible for annual influenza vaccination.Unfortunately, physician assessment of asthma severityhas been characterized in prior studies as being both infre-quent16 and inaccurate17–20 and may result in varying influ-enza vaccination practices from patient to patient.Moreover, influenza vaccination practices may differ sub-stantially between pediatricians and family physicians,given prior reports of distinctions in asthma managementpractices.15–21

The degree to which primary care providers make influ-enza vaccination recommendations for children withasthma is not well understood. The objective of this studywas to explore primary care physicians’ perspectives re-garding influenza vaccination practices for children withasthma, contrasting their recommendation approaches forchildren with persistent asthma versus those with intermit-tent asthma.

Volume 8, Number 54 September-October 2008

AMBULATORY PEDIATRICS Perspectives on Flu Vaccination Among Children With Asthma 295

METHODS

We conducted a mailed survey of office-based generalpediatricians and family physicians in Michigan focusingon issues related to influenza vaccination among childrenwith asthma during the 2005–2006 influenza season. Thestudy was approved by the Institutional Review Board atthe University of Michigan.

A random sample of 300 pediatricians and 300 familyphysicians practicing in Michigan was obtained from theAmerican Medical Association (AMA) Physician Master-file. The AMA Physician Masterfile is the most comprehen-sive physician listing in the United States and includes bothAMA members and nonmembers. The sampling frameincluded all physicians self-described as pediatricians orfamily physicians in office-based direct patient care. Ex-cluded were physicians with multiple or specialty boardlistings, physicians aged 70 years or older, resident physi-cians, and physicians practicing at federal medical facilities(eg, Veterans Affairs, military).

A 1-page, 14-item survey instrument was developed thatconsidered physicians’ attitudes and experiences related toinfluenza vaccination for children with asthma during the2005–2006 influenza season. Survey questions were de-rived from one author’s (S.J.C.) previous studies of physi-cian immunization practices.22–24 Specific survey itemsincluded whether physicians routinely, sometimes, or rarelyrecommended influenza vaccine to children with persistentasthma and to children with intermittent asthma; reasons fornonadministration of influenza vaccine to children withasthma; the number of pediatric asthma patients in the re-spondent’s panel of patients; and the perceived influenzavaccination rate in their practice for children with asthma.Respondents were asked to indicate how frequently (never,rarely, sometimes, often) one or more of the following werereasons children with asthma left their practice without in-fluenza vaccine being administered: immunization deferredbecause of child’s current illness; child/parent refused vac-cine; child not identified as eligible for flu vaccine; child’sasthma not severe enough to warrant vaccination; flu vac-cine not available at time of visit; child had received/wouldreceive vaccine at specialists’ office, health department, orother site; physician overlooked discussion/recommenda-tion of flu vaccine at the time of the visit. The survey instru-ment was pilot tested with a convenience sample of 10primary care providers to establish construct validity andto ensure that interpretation of survey items was consistentacross pilot testers. Based on pilot test feedback, item word-ing and response choices were revised and then retested.Because the authors wished to field the survey shortly afterthe end of the influenza vaccination season, no further test-ing was conducted.

The survey was fielded in February 2006; 1 survey mail-ing was conducted to minimize recall bias. Survey packetscontained a cover letter explaining the purpose of the study,the survey form, and a small cash incentive.

The primary outcome measure was the proportion ofrespondents who indicated they routinely recommendedannual influenza vaccination for children with persistent

asthma and for those with intermittent asthma. A secondaryoutcome measure was the frequency of reasons reportedfor which children left a visit without receiving influenzavaccine.

Independent variables included physician practice char-acteristics: specialty (pediatrician, family physician), num-ber of physicians in the respondent’s practice, ownership/affiliation status, and the proportion of Medicaid patientsseen. In addition, practices were characterized in termsof whether they stocked publicly purchased (eg, from theVaccines for Children program) or privately purchasedinfluenza vaccine.

Statistical Analysis

Univariate frequencies were generated for each surveyitem. Chi-square tests were performed to assess the associ-ation between practice characteristics and influenza vacci-nation recommendations for children with persistent andintermittent asthma. In addition, we assessed the degreeto which missed opportunities may differ among thesegroups by characterizing the reasons children with asthmamay have left respondents’ practices without influenza vac-cine being administered. Odds ratios (ORs) were estimatedto assess the association between practice characteristicsand influenza vaccination recommendations for childrenwith persistent or intermittent asthma; characteristicsachieving an attained significance level of P < .2 were fur-ther assessed using multivariate logistic regression models.All statistical analyses were conducted using SAS version9.1 (SAS Institute Inc, Cary, NC).

RESULTS

Excluding 16 surveys returned as undeliverable, theoverall response rate was 67% (389 returned of 584). Ofthose, 49 responses were ineligible due to respondentsnot providing outpatient primary care to children, and 20responses were returned after data coding had beencompleted, yielding 320 surveys (55% pediatricians, 45%family physicians) that were eligible for analysis. Table 1summarizes the characteristics of the respondents’ prac-tices. Both specialties were similar with respect to practicesize and affiliation, although pediatricians were 2.5 timesmore likely than family physicians to have more than 25pediatric patients with asthma (P < .0001). Family physi-cians were less likely to see Medicaid patients (P <.0008) and less likely to stock influenza vaccine, both forprivate (P ¼ .01) and public (P < .0001) stock. Physicianspecialty was not associated with the number of physiciansor the ownership of respondents’ practices.

Ninety-six percent of respondents reported that theyroutinely recommended influenza vaccine to childrenwith persistent asthma during the 2005–2006 influenzavaccination season, and pediatricians were more likelythan family physicians to routinely recommend (OR14.4; P ¼ .01). Although fewer respondents (82%) re-ported that they routinely recommended influenza vac-cine to children with intermittent asthma, pediatricianswere more likely than family physicians to recommend

296 Dombkowski et al AMBULATORY PEDIATRICS

Table 1. Characteristics of Survey Respondents*

All Respondents (N ¼ 320) Pediatricians (n ¼ 175) Family Physicians (n ¼ 145) P Value

No. of asthma patients <.0001

#25 37 14 65

>25 63 86 35

No. of physicians in practice .51

1–2 33 30 36

3–5 37 38 37

>5 30 32 27

Ownership/affiliation .08

Private 66 70 61

Hospital/practice network 29 26 32

Other 5 4 7

Proportion pediatric patients in Medicaid .0008

<5% 27 19 37

5%–10% 15 14 17

11%–25% 21 23 19

26%–50% 21 28 13

>50% 16 16 15

Influenza vaccine inventory (2005–2006)

Private stock

Yes 91 95 87 .01

No 9 5 13

Public stock

Yes 68 79 56 <.0001

No 32 21 44

*Data are given as percentages except where noted.

influenza vaccine to children with intermittent asthma(OR 4.23; P < .0001). Regardless of specialty, physicianswho provide care for more than 25 pediatric asthma pa-tients were more likely than those with fewer asthma pa-tients to routinely recommend influenza vaccine to boththe persistent (OR 20.6; P ¼ .004) and intermittentgroups (OR 2.41; P ¼ .003). Additionally, those whostocked privately purchased influenza vaccine weremore likely than those who did not to routinely recom-mend influenza vaccine to children with persistentasthma (OR 6.1; P ¼ .006), although these groups didnot differ significantly regarding their recommendationsfor children with intermittent asthma (OR 1.95; P ¼.14). Physicians who stock publicly purchased influenzavaccine were equally likely as those who did not to rou-tinely recommend influenza vaccine to children with per-sistent asthma (OR 1.1; P ¼ .91) but were more likely torecommend for those with intermittent asthma (OR 2.1;P ¼ .01). There was no difference in recommendationof influenza vaccination to children with asthma basedon the number of physicians in the practice, practice af-filiation, or percentage of patients enrolled in Medicaid.

The multiple associations between influenza vaccina-tion recommendations and physician practice characteris-tics were further explored using multivariate logisticregression models (Table 2). Since recommendations forchildren with persistent asthma were nearly unanimous,we focused our multivariate models on recommendationsfor intermittent asthma patients. Multivariate models in-cluded practice characteristics with unadjusted ORs thatachieved an attained significance level of P < .2. Theadjusted odds of recommending influenza vaccinationfor intermittent asthma patients were significantly higher

among pediatricians versus family physicians (P ¼.0008), controlling for the number of asthma patientsand whether practices stock either private or public influ-enza vaccine.

The most commonly reported reasons why childrenwith asthma did not receive an influenza vaccination dur-ing a visit to their practice were unavailability of vaccineat time of visit (49%), child had received vaccine else-where (46%), and child or parent refusal of vaccine(44%). However, these reasons varied based on self-re-ported vaccination recommendation; the Figure contrastsresponses from physicians who rarely or sometimes rec-ommend influenza vaccination, with those who routinelyrecommend vaccination for children with intermittentasthma. Physicians who rarely or sometimes recommendinfluenza vaccine were more likely to cite several reasonsfor not administering influenza vaccine at the time ofvisit: that a child’s asthma was not severe enough to war-rant vaccination (P < .0001), the discussion of influenzavaccine at the time of visit was overlooked (P < .0001),and the child not identified as eligible for flu vaccine(P ¼ .0006). Similarly, physicians who provide care for25 or fewer pediatric asthma patients (compared withthose with more than 25) were more likely to report asreasons for lack of vaccination that a child’s asthmawas not severe enough to warrant vaccination (25% vs14%, respectively; P ¼ .01) and that discussion of influ-enza vaccine was overlooked at the time of visit (29%vs 15%, respectively; P ¼ .0028). Physicians in practiceswith 1 to 2 physicians were more likely to indicate thata child’s asthma was not severe enough to warrant vacci-nation versus those in larger practices (26% vs 14%, re-spectively; P ¼ .01).

AMBULATORY PEDIATRICS Perspectives on Flu Vaccination Among Children With Asthma 297

Table 2. Influenza Vaccination Recommendations by Physician Practice Characteristics

Recommend for Children With Intermittent Asthma (N ¼ 319)

OR* AOR† 95% CI‡

Physician specialty

Pediatricians 4.23§ 362 1.72–7.60

Family physicians Reference Reference

Number of asthma patients

>25 2.41jj 1.28 0.63–2.57

#25 Reference Reference

Number of physicians in practice

1–2 0.68

3–5 1.31

>5 Reference

Ownership/affiliation

Hospital/practice network 1.66{ 1.73 0.82–3.65

Other 0.60 0.57 0.16–2.08

Private Reference

Proportion pediatric patients in Medicaid

<10% 1.09 1.95 0.70–5.45

11%–50% 1.74{ 1.47 0.57–3.75

>50% Reference

Influenza vaccine inventory (2005–2006)

Private stock

Yes 1.95{ 0.88 0.32–2.42

No Reference Reference

Public stock

Yes 2.10** 1.88 0.88–4.01

No Reference Reference

*OR indicates odds ratio.

†AOR indicates adjusted odds ratio.

‡CI indicates confidence interval.

§P < .0001.

jjP < .01.

{P < .2.

**P < .05.

DISCUSSION

Findings from this study suggest that influenza vaccina-tion practices of primary care physicians reflect the incon-sistencies historically found in national recommendations.Although almost all pediatricians and family physiciansreport that they routinely recommend annual influenzavaccination for children with persistent asthma, their rec-ommendations are less consistent for children with inter-mittent asthma. Annual influenza vaccination has longbeen recommended for children with asthma, yet influenzavaccination rates in this population have been reported inprevious studies ranging from 7% to 29%.8–14 Missed op-portunities to administer influenza vaccination have beenidentified as one contributor to low influenza vaccinationrates,10–13 underscoring the considerable potential that ex-ists to improve vaccination rates among this vulnerablegroup of children. Children with asthma have high ratesof physician visits compared with healthy children, partic-ularly during fall and winter months when asthma symp-toms often worsen.25–27 Physician visits during thesemonths represent opportunities to administer influenzavaccine to children with asthma, yet there is clear evidencethat these opportunities are often missed.13 In this study,providers who did not routinely recommend influenza vac-cination for children with intermittent asthma recognizedthat missed opportunities were occurring. These physicians

frequently reported that children were unvaccinated due tofailure to identify eligible children, asthma not being se-vere enough to warrant vaccination, and the discussion ofinfluenza vaccination being overlooked. In contrast, thosewho routinely recommended vaccination for both thepersistent and intermittent asthma groups more commonlycited problems with influenza vaccine supply or that chil-dren received vaccine elsewhere.

Our study raises several concerns regarding the imple-mentation of national influenza vaccination guidelines forchildren with high-risk conditions such as asthma. Similarto earlier reports, we found that influenza vaccination prac-tices vary by asthma severity level.15 This finding is ofparticular significance because NAEPP guidelines havehistorically indicated that persons with persistent asthmashould receive annual influenza vaccination;6 for the pastdecade, these guidelines have contrasted with the broaderACIP recommendation that includes all persons withasthma.7 Data from our study demonstrate that a consider-able number of pediatricians and family physicians imple-ment influenza vaccine recommendations differently forchildren with intermittent versus persistent asthma, evenamong those physicians who have more pediatric patientswith asthma. These findings are consistent with previous re-ports of frequently missed opportunities to administer influ-enza vaccine to children with asthma.10–13 Our results also

298 Dombkowski et al AMBULATORY PEDIATRICS

9%13%

27%

39% 41%

48%51%52% 50% 50%

34%

57%

40%44%

0%

10%

20%

30%

40%

50%

60%

70%

80%

90%

100%

Asthmanot severe

enough

Vaccinationrecommendation

overlooked

Not identifiedas eligible for

flu vaccine

Deferreddue to current

illness

Child / parent refused

vaccine

Patient alreadyvaccinated

Vaccine notavailable

% o

f R

esp

on

den

ts

Vaccine AlwaysRecommended for Intermittent Asthma n = 59Vaccine Rarely or SometimesRecommended for Intermittent Asthma n = 260

Figure. Reported reasons for influenza vaccine not being administered to patients with asthma. N ¼ 319 respondents; 95% confidence intervals are

shown.

are consistent with an earlier study that found family physi-cians use influenza vaccination reminder systems less fre-quently than pediatricians and tend to experience greaterdifficulty in identifying children with high-risk conditionsfor influenza vaccination.15

Importantly, the NAEPP recently released revised asthmamanagement guidelines28 that include recommendations forinfluenza vaccination for all persons with asthma, removingthe former distinction by severity level, and in effect, harmo-nizing the NAEPP and ACIP recommendations. Our findingssuggest the potential benefits of this revision; prior studieshave demonstrated generally high levels of awareness ofNAEPP guidelines.21,29,30 The new NAEPP recommenda-tions are now consistent with the existing ACIP recommen-dations. This change may prove to be helpful in mitigatingprovider uncertainty and potentially improving vaccinationrates among children considered to be at increased risk forinfluenza complications.

Finally, in most practice settings, children will seea number of different providers. This may limit an individ-ual physician’s familiarity with a child’s asthma history,reducing the likelihood that the child will be identified asvaccine eligible. Even if vaccine eligibility is accuratelyassessed, children with high-risk conditions who are seenby multiple providers may experience missed opportunitiesbecause there is considerable uncertainty among physi-cians as to who should be responsible for administeringannual influenza vaccine.15

There are limitations to this study. These data are self-reported; we cannot determine the extent to which actualpractice may differ from self-report. There is also the pos-sibility of response bias, although its direction cannot bedetermined. However, the response rate compares favor-ably with that of other published studies of physician prac-tice patterns.31 The survey was conducted in a single state,which may limit its generalizability. Physicians’ knowl-edge regarding NAEPP and ACIP influenza vaccinationguidelines was not ascertained. In addition, we were unable

to determine the degree to which observed specialty differ-ences may be attributable to variations in asthma severityor vaccine acceptance between patients seen by familyphysicians and those seen by pediatricians.

Our findings underscore the implementation difficultiesthat are inherent to a risk-based influenza vaccinationrecommendation strategy for children with asthma. One al-ternative to a risk-based recommendation approach is theadoption of universal influenza vaccination for all childrenaged through 18 years as was recently announced by theACIP.32 However, even under this newly expanded recom-mendation, children with asthma and other high-risk condi-tions would still be considered priority groups in the eventof influenza vaccine shortages. Consequently, appropriateidentification of children with asthma and other high-riskconditions will remain important. Further research is war-ranted to determine whether recent clarification of NAEPPrecommendations to remove distinctions by asthma sever-ity could serve to alleviate provider uncertainty and helpachieve a higher degree of vaccination among children con-sidered to be at increased risk for influenza complications.

ACKNOWLEDGMENT

This study was supported by the Michigan Department of Community

Health.

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