PEDIATRICS Vol. 120 No. 2 August 2007, pp. e401-e409 (doi:10.1542/peds.2007-0359)
ARTICLE |
Pediatricians' Adherence to Pneumococcal Conjugate Vaccine Shortage Recommendations in 2 National Shortages
a Center for Epidemiology and Biostatistics
c Division of Infectious Diseases, Cincinnati Children's Hospital Medical Center, University of Cincinnati, Cincinnati, Ohio
b National Center for Immunization and Respiratory Diseases
e Division of HIV/AIDS Prevention, National Center for HIV, STD, and TB Prevention, Centers for Disease Control and Prevention, Atlanta, Georgia
d National Vaccine Program Office, Washington, DC
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ABSTRACT |
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 TOP ABSTRACT METHODSRESULTSDISCUSSIONREFERENCES |
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OBJECTIVES. The goals were (1) to compare pediatricians' heptavalent pneumococcal conjugate vaccine shortage experience and adherence to shortage recommendations during 2 heptavalent pneumococcal conjugate vaccine shortages, (2) to assess factors associated with nonadherence to second shortage recommendations, and (3) to assess opinions about national immunization policy during vaccine shortages.
METHODS. We mailed surveys to all pediatrician immunization providers in the greater Cincinnati, Ohio, metropolitan area. We assessed heptavalent pneumococcal conjugate vaccine supply and immunization practices during the shortages and provider attitudes regarding immunization shortage policy.
RESULTS. The response rate was 61% (171 of 282 providers). Most pediatricians experienced heptavalent pneumococcal conjugate vaccine shortages (first shortage: 86%; second shortage: 84%). The rate of adherence to recommendations to defer the fourth heptavalent pneumococcal conjugate vaccine dose for healthy children was significantly higher during the second shortage, compared with the first shortage (first shortage: 62%; second shortage: 89%). Adherence to recommendations to administer the fourth dose to high-risk children remained unchanged (first shortage: 43%; second shortage: 45%). Controlling for other factors, pediatricians who reported a severe second shortage had greater odds of not fully vaccinating high-risk children, compared with those who reported no shortage. Contrary to recommendations, many pediatricians did not maintain tracking systems during the heptavalent pneumococcal conjugate vaccine shortages (first shortage: 37%; second shortage: 46%). Most pediatricians (91%) thought that national vaccine shortage recommendations were needed to protect them from liability.
CONCLUSIONS. The rate of adherence to recommendations to defer heptavalent pneumococcal conjugate vaccine doses for healthy children increased significantly from the first shortage to the second shortage. The nonadherent practice of deferring the fourth dose for high-risk children was associated with more severe shortages and, potentially, an inability to vaccinate.
Key Words: immunization • vaccine shortage • heptavalent pneumococcal conjugate vaccine
Abbreviations: PCV7—heptavalent pneumococcal conjugate vaccine • CDC—Centers for Disease Control and Prevention • ACIP—Advisory Committee on Immunization Practices • AAP—American Academy of Pediatrics • OR—odds ratio • CI—confidence interval
Recent shortages of many routinely recommended vaccines have highlighted severe problems in vaccine supply in the United States.1,2 These shortages have posed substantial challenges to clinicians who may be unable to provide vaccinations and to public health officials who are sought for guidance in modifying recommended schedules. Vaccines that are produced by only 1 company are especially susceptible to national shortages when production problems arise.2 Heptavalent pneumococcal conjugate vaccine (PCV7) (marketed as Prevnar by Wyeth Vaccines, Collegeville, PA) is a prominent example.
There have been 2 national shortages of PCV7 since it was recommended for routine administration to infants and young children in 2000.3,4 The first shortage occurred from September 2001 through May 2003, 
1 year after PCV7 was recommended for routine use.5,6 The second shortage occurred from February 2004 through September 2004, only 8 months after the earlier shortage ended.7,8
Modified PCV7 vaccination recommendations were published during each shortage, to conserve vaccine nationally and to maintain effective disease prevention. Recommendations during the first shortage were made by the Centers for Disease Control and Prevention (CDC), with guidance from the Advisory Committee on Immunization Practices (ACIP)5,9; the American Academy of Pediatrics (AAP) adopted the ACIP recommendations.10 During the second shortage, the CDC (with the ACIP), the AAP, and the American Academy of Family Physicians issued harmonized recommendations.7,11,12 During both shortages, PCV7 vaccination continued to be recommended with a 4-dose schedule for children in groups defined by the ACIP as having a high risk for invasive pneumococcal disease (eg, those with sickle cell anemia). Both shortage recommendations also stated that the fourth PCV7 dose should be deferred for healthy children (ie, those without an ACIP-specified, high-risk, medical condition) and a tracking system should be maintained for catch-up vaccination of those for whom PCV7 was deferred. Recommendations regarding the third PCV7 dose for healthy children differed between the first and second shortages. During the first shortage, providers were asked to classify the level of shortage in their practices and to defer the third and fourth doses if the practice had a "severe" shortage. During most of the second shortage (from March 2004 through July 2004), providers were advised to defer the third and fourth doses for all healthy children, regardless of practice-specific vaccine availability. At the beginning and end of the second shortage, recommendations were to defer only the fourth dose.5,7,11,12
In developing recommendations for the second PCV7 shortage, experiences from the first shortage and lessons learned were considered13; however, whether adherence to recommendations differed between shortages has not been well described. The objectives of this study were (1) to compare self-reported PCV7 shortage experience and adherence to CDC/AAP PCV7 shortage recommendations among pediatricians in the greater Cincinnati metropolitan area during the first (2001–2003) and second (2004) vaccine shortages, (2) to assess factors associated with nonadherence to PCV7 shortage recommendations for healthy and high-risk children during the second shortage, and (3) to assess opinions about national immunization policy during vaccine shortages.
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METHODS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
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Study Design and Population
We conducted a cross-sectional, mailed survey of all pediatricians in the 7 counties in southwestern Ohio and northern Kentucky that constitute the greater Cincinnati metropolitan area. Our mailing list was compiled from the Unified Physician Information Repository (an online listing of all physicians practicing in Cincinnati) and from an internal list of pediatricians from patient services at Cincinnati Children's Hospital Medical Center. The survey was mailed to 285 pediatricians in September 2004. A second mailing of the survey was sent 1 month later to pediatricians who had not responded. That mailing was followed in January 2005 by a telephone reminder to office managers in practices that had not responded and by a faxed version of the survey and cover letter to practices that had not responded. The protocol for this study was approved by the institutional review board at Cincinnati Children's Hospital Medical Center; the CDC relied on the Cincinnati Children's Hospital Medical Center institutional review board for review.
Survey Instrument
Our 30-item, closed-ended survey instrument was modeled after a questionnaire used by the CDC in a previous national survey to assess responses to the first PCV7 shortage (2001–2003) (a copy of the study survey is available from the corresponding author by request).13 The study survey instrument included questions about physician demographic characteristics, practice type, Medicaid penetration, and source of vaccine supply for the practice (public, private, or both). Pediatricians were asked to describe the vaccine supply they used for patients in their practice as only public (including Vaccines for Children), both public and private, only private, or not known. We asked pediatricians to report on the following for the first and second shortages: level and severity of PCV7 shortage in the practice; whether they had administered the third and/or fourth PCV7 doses to healthy and high-risk children; factors that influenced vaccination practices during the shortage; and tracking system and practices for recalling children when PCV7 had been deferred. In addition, we asked pediatricians about their perceptions of the effectiveness of fewer-dose PCV7 schedules and their general opinions of CDC and AAP vaccine shortage recommendations.
Definitions of Shortage and Nonadherence to Recommendations
For each PCV7 shortage, the overall practice shortage status was assessed as a 3-level variable (none, moderate, or severe). Pediatricians who reported not being aware of any shortage in their practice were considered to have no shortage. Among those with a shortage, pediatricians who classified their shortage as moderate (<25% shortfall in available doses, on the basis of the 4-dose infant schedule) were considered to have experienced a moderate shortage, whereas those who reported their shortage as severe (25%–50% shortfall) or more than severe (>50% shortfall) were considered to have experienced a severe shortage. The degree of shortage was adapted from definitions used in ACIP recommendation during the first shortage.9
Nonadherence to the recommendations for the fourth PCV7 dose was defined separately for healthy children without ACIP-specified, high-risk, medical conditions and high-risk children, on the basis of physicians' responses to the survey. For healthy children, nonadherence was defined as administration of the fourth dose to 
10% of healthy children <2 years of age. For high-risk children, nonadherence was defined as administration of the fourth dose to 
90% of children <5 years of age.
Adherence to tracking guidelines was also assessed. Among pediatricians who reported deferring PCV7 during the shortage, those who maintained no system or only made an indication in the chart to track children when PCV7 was deferred were considered nonadherent. Pediatricians with other informative responses were defined as adherent.
Statistical Analyses
Statistical analyses were conducted by using SAS 9.1 (SAS Institute, Cary, NC). We conducted univariate analyses to compare the shortage experience and rates of adherence between the first and second shortages and agreement analyses to assess whether individual pediatricians' responses differed between the 2 shortages. McNemar's test for significance was used to assess agreement in pediatrician responses.14 For the second shortage, we conducted univariate and multivariate analyses using logistic regression to examine factors associated with nonadherence to the CDC/AAP shortage recommendations for healthy children and high-risk children. Shortage status (as defined above) and other covariates, including pediatrician gender, practice type (public/university versus private), Medicaid penetration (75% versus >75%), vaccine supply type, and pediatricians' opinion about the effectiveness of administering the fourth dose, were examined in the adherence analysis. Medicaid penetration, practice type, and vaccine supply type were highly correlated with each other (P < .0001); therefore, only Medicaid penetration was included in the multivariate model. Two-tailed P values of <.05 were considered significant.
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RESULTS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
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Pediatrician Characteristics
Overall, 174 (61%) of 285 surveys mailed were completed. Three responding pediatricians were not eligible to participate because they did not provide PCV7 in an outpatient setting, which resulted in 171 eligible surveys returned. Among respondents, 50% were female, most (72%) practiced in a
2-physician private setting, and most (75%) reported Medicaid penetration rates of <25%. Only 9 pediatricians (5%) answered that they had only public supplies of PCV7, whereas 42% reported having only private supplies (Table 1).
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Shortage Experience During First and Second Shortages
Few pediatricians reported experiencing no PCV7 shortage during the first shortage (14%) and the second shortage (16%) (Fig 1). Only 11 pediatricians (8%) reported having adequate PCV7 supplies during both shortages (data not shown). The shortage seemed to have similar effects on the public and private PCV7 supplies during each shortage. In the first shortage, 90% of pediatricians with private-only PCV7 supplies, 85% with both public and private supplies, and 67% with public-only supplies experienced some shortage. Proportions during the second shortage were similar (86%, 84%, and 67%, respectively). However, only 9 pediatricians reported having public-only supplies, and differences in shortage experience according to supply type were not significant.
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The proportions of pediatricians who reported severe shortage during the first and second shortages were 41% and 32%, respectively (P = .13). Individual physicians often experienced different levels of shortage during the 2 periods; 21 (24%) of 88 pediatricians who experienced no or moderate shortage during the first period reported severe shortage during the second period, and 29 (48%) of 60 pediatricians who experienced severe shortage during the first period reported no or moderate shortage during the second period.
Adherence to CDC/AAP Recommendations for Vaccinating Healthy and High-Risk Children During First and Second Shortages
Reported adherence to the recommendation to suspend the fourth PCV7 dose for healthy children was 89% for the second shortage, compared with 62% for the first shortage (P < .0001) (Fig 1). Reported adherence to the recommendations to administer the fourth PCV7 dose to high-risk children was lower and did not improve between the 2 shortages (first shortage: 45%; second shortage: 43%; P = .66). When pediatricians with a severe shortage were excluded, adherence rates were higher but remained similar across shortages (first shortage: 58%; second shortage: 46%; P = .12).
For healthy children, physicians who adhered to the recommendation to defer the fourth dose during the first shortage were likely to adhere during the second. Among the 74 physicians who were adherent for healthy children in the first shortage, 71 (96%) were also adherent in the second shortage (McNemar's test, P < .0001).
Of the 54 physicians who were adherent for high-risk children and administered the fourth PCV7 dose in the first shortage, only 37 (69%) were also adherent in the second shortage. Becoming nonadherent for high-risk children in the second shortage was not associated significantly with more-severe shortage for those physicians. However, becoming adherent for high-risk children was associated significantly with experiencing less-severe shortage during the second shortage.
Adherence to Tracking System Recommendation During First and Second Shortages
Most pediatricians reported deferring doses during the shortages (first shortage: 95%; second shortage: 99%). Among the pediatricians who deferred doses, 37% and 46% in the first and second shortages, respectively, were considered nonadherent because they reported not maintaining any tracking system or only making an indication in the chart (P = .11) (Fig 2). During both shortages, a manual system (ie, keeping a list) was the most commonly used method to track patients (first shortage: 53%; second shortage: 45%; P = .18). Few (<10%) reported using a computerized tracking system (either an office-based system or the immunization registry) during either shortage. After the first shortage, 54% of 135 pediatricians with informative responses reported that they had called patients for catch-up PCV7 vaccination (data not shown). Physicians with computerized or manual tracking systems were each more likely to report recalling patients (58% and 93%, respectively) than were physicians with no adequate tracking system (7%; P < .0001). Physicians with manual systems were more likely than those with computerized systems to report recalling patients (P < .0001).
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Rationale for PCV7 Vaccination Decisions for Healthy and High-Risk Children During Second Shortage
Among the 100 pediatricians who reported administering the third or fourth dose to some healthy children, the most commonly reported reason for vaccination was having sufficient PCV7 available in the practice (64%) (data presented in this section are not shown). Forty-eight percent of respondents indicated that a child's history of recurrent otitis media and current day care attendance influenced their decision to administer these doses, and 10% of pediatricians reported that parental request factored into their vaccination practices for healthy children.
Among the 114 pediatricians who reported not administering the third and/or fourth dose to some high-risk children, the most frequently reported reason was that they lacked vaccine at the time of the patient visit (51%). Thirty-three percent of pediatricians reported that "conserving vaccine for other patients in the practice" contributed to the decision not to vaccinate. Only 3 pediatricians reported not vaccinating high-risk children because of their belief that the "dose is not important to protect some high-risk children from pneumococcal infection."
Factors Associated With Nonadherence to Fourth-Dose Vaccination Recommendations During Second Shortage
To investigate nonadherence to recommendations more thoroughly, we performed univariate and multivariate analyses to assess the effects of gender, shortage severity, Medicaid penetration, and physician opinion regarding the relative effectiveness of the fourth dose for disease prevention for both healthy and high-risk children (Table 2). In multivariate analyses, shortage severity was the only factor associated statistically with nonadherence to the high-risk recommendations. Pediatricians who reported experiencing moderate shortage had 4 times the odds of deferring the fourth dose for high-risk children, contrary to recommendations, compared with pediatricians who reported no shortage (odds ratio [OR]: 3.92; 95% confidence interval [CI]: 1.37–11.2; P = .011). The OR for nonadherence to the high-risk recommendation was higher among pediatricians who experienced severe shortage (OR: 5.15; 95% CI: 1.65–16.0; P = .005). The same dose-response relationship between shortage severity and nonadherence was observed for healthy children, in the opposite direction, but it did not reach statistical significance. Pediatricians who reported severe shortage more often deferred the fourth dose as recommended, compared with pediatricians who reported no shortage, but traditional statistical significance was not reached (OR: 0.22; 95% CI: 0.05–1.01; P = .051).
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To assess adherence to the recommendations for high-risk children among pediatricians who had some vaccine, we excluded 17 pediatricians who had no vaccine for an extended period and thus no ability to vaccinate and we repeated the analysis. The association between shortage level and nonadherence remained significant.
Belief in the relative effectiveness of the fourth dose also was linked with PCV7 fourth dose deferral practices, but the level of association did not reach statistical significance. The odds of deferring the fourth dose for high-risk children, contrary to recommendations, was increased for pediatricians who reported a belief that 4 doses, compared with 3 doses, provided "little or no more protection" or "somewhat more protection" (OR: 1.74; 95% CI: 0.88–3.44; P = .11). In contrast, the odds of administering the fourth dose to healthy children, contrary to recommendations, was decreased for pediatricians with this belief (OR: 0.37; 95% CI: 0.12–1.11; P = .08).
Pediatricians' Perspectives About CDC/AAP Guidelines
When asked about their motivation to follow the 2-dose PCV7 schedule recommended for healthy children during most of the second shortage, 89% agreed or strongly agreed that they were motivated to ensure adequate PCV7 supplies within their own practice and 80% agreed that they followed the 2-dose schedule to ensure that there would be adequate PCV7 supplies in the country (Fig 3). Almost all respondents (91%) agreed or strongly agreed that national recommendations during a vaccine shortage are needed to protect physicians from potential liability if they defer doses (Fig 3). In addition, 89% agreed or strongly agreed that, during the course of a vaccine shortage, the CDC/AAP should adapt recommendations to reflect changes in vaccine supplies. Only 15% of the pediatricians thought that, during a shortage, the CDC/AAP should only present facts, rather than making recommendations, so that practices can individualize provision of vaccine on the basis of their own supplies.
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DISCUSSION |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
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Both the 2001 to 2003 and 2004 PCV7 shortages had substantial effects on PCV7 vaccination practices of pediatricians in the Cincinnati area. Although the impact of single shortages of different vaccines has been studied,13,15–18 this is the first study, to our knowledge, to compare physicians' reported shortage experience and recommendation adherence across 2 shortage periods for the same vaccine. We found significant improvements in adherence to recommendations to defer vaccine doses for healthy children without high-risk medical conditions but low and unchanged rates of adherence to recommendations for full vaccination of children at high risk for invasive pneumococcal disease. Our results suggest that the nonadherent practice of deferring the fourth dose for high-risk children was associated with more-severe vaccine shortage and, potentially, an inability to administer the vaccine.
In both shortages, national recommendations specified that providers should defer doses for healthy children, fully vaccinate high-risk children, maintain a tracking system, and recall children for whom PCV7 was deferred. Findings in this study of suboptimal adherence during the first shortage to the recommendations to defer doses for healthy patients and to track patients were consistent with findings by Broder et al,13 based on a national survey. Furthermore, our finding that, by the second shortage, adherence to this recommendation improved significantly was consistent with the high rate of adherence reported elsewhere for immunization providers' vaccination practices during the 2004 shortage.19 In addition, results of the Cincinnati study were consistent with findings in the study by Broder et al13 that having sufficient PCV7 available in the practice was associated with administering the fourth dose to healthy children, contrary to recommendations.
Although similar proportions of providers experienced a PCV7 shortage during the 2 shortages, reported adherence rates improved substantially during the second shortage. We speculate that several factors contributed to this change. Physicians might have more clearly perceived the need to conserve vaccine, the 2004 recommendations might have been easier to follow, scientific data supporting the effectiveness of 2- and 3-dose PCV7 schedules for healthy children were presented in the recommendations,7,11 and communication from the CDC and the medical societies to physicians and parents was improved.
Although vaccine effectiveness data support deferring the fourth PCV7 dose for healthy children to conserve vaccine for the broader population,11 no data support a fewer-dose schedule for children at high risk for invasive pneumococcal disease. In the present study, fewer than one half of Cincinnati pediatricians reported administering the fourth dose to high-risk children, in accordance with recommendations, and the degree of adherence showed no improvement between the first and second shortages. The association between shortage severity and nonadherence and the finding that not having PCV7 available at the time of the visit was the most commonly reported reason for not administering doses to high-risk children suggest that, in many cases, physicians were unable to comply with the recommendation. This finding is consistent with results from other studies of adherence during the first shortage13,16 and is consistent with the report that providers often were not aware of a national shortage until they were affected, at which point it was too late to prioritize for high-risk children.15 Broder et al13 reported high rates of adherence to the recommendation to vaccinate high-risk children fully during the first shortage, on the basis of reported vaccination practices for toddlers with sickle cell anemia during a "typical" day in autumn 2002. It is not known whether the difference in adherence rates between these studies is attributable to differences in the survey wording or reflects a regional difference in practices between Cincinnati and general US pediatricians.13
Administration of catch-up PCV7 doses after the shortage is important because no studies suggest long-term effectiveness of reduced dose schedules. In addition, a recent study of short-term effectiveness indicated that the fourth dose, which is the dose most often skipped during the shortage, adds significant protection over the primary series.20 Although nearly all pediatricians reported deferring PCV7 doses during each shortage, many reported not maintaining a tracking system. Moreover, despite experience with the first PCV7 shortage, the proportion of providers who maintained a tracking system during the second shortage did not increase. Although it is unlikely that many providers would have established new automated systems during the few-month interval between shortages, manual systems could have been implemented. Effective tracking systems would allow the first of those who had their doses withheld to be the first to receive their doses once the shortage ended. This would decrease the time between doses and would allow all children to be vaccinated in a timely manner.
National recommendations to providers from the CDC and professional medical societies regarding vaccination practices are commonly made during a vaccine shortage. We found nearly unanimous agreement among respondents that national recommendations were needed in a time of shortage. Respondents also thought that recommendations should be adapted during shortages, to reflect changes in the vaccine supply.
This study had several limitations. Results are self-reported and may not reflect true behavior. Although there may be a theoretical bias toward providing an answer indicating adherence with a recommendation, we found high rates of nonadherence for several recommendations. An ongoing study in Cincinnati to assess PCV7 vaccination practices during the shortages with medical chart review will assess potential differences between reported and actual behaviors. Another potential limitation is the 61% response rate. Although this rate is comparable to response rates for published mail surveys of physicians,21,22 nonrespondents might have differed from respondents. Although we did not obtain information from a sample of nonrespondents, the previous CDC survey by Broder et al13 found that similar proportions of respondents and nonrespondents experienced a PCV7 shortage and met eligibility criteria. Another limitation might be related to the timing of the survey; responses about the second shortage might be more accurate than responses about the first shortage. Despite this possibility, results of the present study are consistent with those of a previous national study conducted closer to the time of the first shortage. Finally, because our study involved only pediatricians in the greater Cincinnati area, findings may not be generalizable to other categories of physicians or to pediatricians throughout the United States. Studies have shown differences in immunization practices and beliefs between pediatricians and other physicians.23,24 The similarities in reports of shortage and recommendation adherence for healthy children and tracking systems between pediatricians in Cincinnati during the first shortage in this study and pediatricians nationally in the CDC study suggest that some findings from Cincinnati may be generalizable to US pediatricians.
On the basis of our findings and those of other investigators, we suggest several recommendations for policymakers in settings of a vaccine shortage. Authoritative national guidance is perceived as important, and physicians are willing to defer doses to help conserve vaccine for others in their practices and to support national priorities. Modifying recommendations to reflect changes in vaccine supply during a shortage, so that they are most applicable to the situation physicians are facing in their practices, is preferred. Practice-specific variations in vaccine supply during shortages are likely, however, and recommendations should provide guidance for physicians who may be unable to provide a recommended dose. Improving tracking systems so that children who have had doses deferred can be recalled and vaccinated is an issue that needs particular focus, given the poor adherence with this recommendation. Although vaccination registries may be used for this function, our results show that manual systems can be used effectively and do not require the development or application of new technology at the state or practice level. Finally, it is important not only to be able to respond better to shortages but also to decrease their occurrence and impact. One strategy currently being pursued is to maintain national stockpiles, particularly for vaccines with a single manufacturer.25 In addition, working with manufacturers to distribute available supplies more equitably if shortages occur may help minimize the impact on individual practices and improve physicians' ability to adhere to recommendations.
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ACKNOWLEDGMENTS |
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This work was funded by the CDC National Vaccine Surveillance Network project (grant U38/CCU522352001).
We thank the pediatricians in the greater Cincinnati area who gave their time to complete this survey. We also thank Stacey Martin and the members of the New Vaccine Surveillance Network team for advice and support.
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FOOTNOTES |
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Accepted Apr 3, 2007.
Address correspondence to Gerry Fairbrother, PhD, Center for Epidemiology and Biostatistics, Cincinnati Children's Hospital Medical Center, 3333 Burnet Ave, MLC 7014, Cincinnati, OH 45229-3039. E-mail: gerry.fairbrother{at}cchmc.org
The authors have indicated they have no financial relationships relevant to this article to disclose.
This work was presented in part at the annual meeting of the Pediatric Academic Societies; April 29, 2006; San Francisco, CA.
The findings and conclusions in this study are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention.
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TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
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PEDIATRICS (ISSN 1098-4275). ©2007 by the American Academy of Pediatrics
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