Who's Calling the Shots Pediatricians' Adherence to the 2001–2003 Pneumococcal Conjugate Vaccine–Shortage Recommendations
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《小儿科》
National Immunization Program
Epidemiology Program Office, Centers for Disease Control and Prevention, Atlanta, Georgia
ABSTRACT
Background. A national shortage of heptavalent pneumococcal conjugate vaccine (PCV7) occurred from September 2001 through May 2003. In December 2001 and January 2002, the Advisory Committee on Immunization Practices and the American Academy of Pediatrics (AAP) issued PCV7-shortage recommendations, emphasizing that all health care providers decrease the number of doses for healthy children so that more children could receive some PCV7.
Objectives. We assessed (1) how the PCV7 shortage affected pediatricians, (2) whether children in the public and private sectors were vaccinated differently during the shortage, (3) pediatricians' knowledge of and adherence to the Advisory Committee on Immunization Practices/AAP recommendations, (4) and what factors were associated with nonadherence to the recommendations.
Methods. We conducted a cross-sectional mail survey of 2500 US physician-members of the AAP from November 2002 through March 2003; physicians providing childhood immunizations were eligible. We asked about PCV7-shortage experience, assessed recommendation adherence through clinical scenarios, and modeled potential factors associated with reported nonadherence to the recommendation to defer the fourth PCV7 dose.
Results. Of 2478 surveys sent to valid addresses, 1412 (57%) completed surveys were received; 946 (67%) of these were from eligible pediatricians. Overall, 79% experienced a PCV7 shortage, 94% reported being aware of the recommendations, and 42% reported barriers to recommendation adherence. Ninety-four percent reported vaccinating 6-month-old infants with private or public insurance in the same manner. As recommended, 91% reported fully vaccinating high-risk patients. Contrary to recommendations, 49% reported sometimes or always administering the fourth PCV7 dose to healthy children 12 to 15 months old; their reasons included recurrent otitis media, childcare attendance, and parental desire. Controlling for other characteristics, pediatricians who had no PCV7 shortage in their practices were significantly more likely to report administering the fourth dose than pediatricians who had a shortage (odds ratio [OR]: 3.67; 95% confidence interval [CI]: 2.40–5.63). Other factors associated with nonadherence were being in solo private practice (OR: 2.18; 95% CI: 1.26–3.77) or being male (OR: 1.51; 95% CI: 1.08–2.12). Among pediatricians deferring PCV7, 36% reported having no system to track children for whom PCV7 was deferred.
Conclusions. Many pediatricians, both with and without a PCV7 shortage, administered more PCV7 doses than recommended. Pediatricians without a shortage were less likely to limit use, which suggests that they might have focused on the perceived value of administering the full schedule to their patients in preference to broader public health goals. Providing more information to physicians on the effectiveness of a fewer-dose schedule and the risk of disease when vaccine is deferred and educating parents might increase adherence to recommendations and achieve more equitable coverage during vaccine shortages.
Key Words: adherence pneumococcal conjugate vaccine
Abbreviations: CDC, Centers for Disease Control and Prevention ACIP, Advisory Committee on Immunization Practices AAP, American Academy of Pediatrics PCV7, heptavalent pneumococcal conjugate vaccine OR, odds ratio CI, confidence interval Td, tetanus and diphtheria toxoids vaccine
2000 through 2003, an unprecedented number of vaccine shortages occurred in the United States, affecting 5 vaccines in the recommended childhood and adolescent immunization schedule. 1–5 To help clinicians manage these shortages and to achieve the benefits of vaccination for as many children as possible, the Centers for Disease Control and Prevention (CDC), the Advisory Committee on Immunization Practices (ACIP), the American Academy of Pediatrics (AAP), and the American Academy of Family Physicians developed and promoted unified vaccine-specific shortage recommendations 1–4,6–8 that differed from their routine childhood and adolescent immunization schedule.5
A shortage of the heptavalent pneumococcal conjugate vaccine (PCV7; marketed as Prevnar by Wyeth Vaccines, Collegeville, PA) began in September 2001,3 1 year after the AAP9 and ACIP10 published recommendations for universal PCV7 use in young children. In September 2001, the CDC issued brief recommendations for use of PCV7 during the shortage.3 In December 2001, when it was determined that the shortage would last longer and be more widespread than initially predicted, the ACIP released updated, detailed recommendations for PCV7 use in the setting of the prolonged shortage6; the AAP adopted these recommendations.7 The ACIP/AAP PCV7-shortage recommendations were based on preliminary data suggesting that a fewer-dose PCV7 schedule prevents invasive pneumococcal disease in healthy children, at least in the short term.6 The recommendations stated that health care providers should (1) prioritize children at high risk for invasive pneumococcal disease and vaccinate them according to the routine childhood and adolescent preshortage schedule, which recommends a 4-dose infant series, (2) defer the fourth dose for all healthy children not included in ACIP-specified high-risk categories, irrespective of individual practice shortage level, (3) make additional deferral decisions based on the practice's PCV7-shortage level, and (4) maintain a tracking system to recall children whose PCV7 vaccination was deferred.6,10 During the shortage, recommendations for the third PCV7 infant dose varied by shortage level. In the setting of no or moderate shortage, the third infant dose was recommended; in a severe shortage, the third dose should have been deferred.6 This national PCV7 shortage lasted 21 months; the CDC issued catch-up recommendations in May 2003.11
The ACIP/AAP PCV7-shortage recommendations had sound public health goals: to conserve vaccine to permit broad vaccination of children and to provide guidance to clinicians during the shortage. However, there was concern about implementation for several reasons. First, recommendations were complex at a time when clinicians were facing simultaneous vaccine shortages. Second, there was potential for different PCV7 availability and vaccination practices for patients using publicly and privately purchased PCV7, even within the same practice. Third, the recommendation to defer the fourth PCV7 dose for all healthy children, even in practices with an adequate supply, potentially created a conflict between the perceived interests of children within a practice and the public health interests of children in the community at large.
We undertook this study to determine (1) how the 2001–2003 PCV7 shortage affected US pediatricians, (2) if pediatricians vaccinated children in the public and private sectors differently, (3) if pediatricians had knowledge of and adhered to the ACIP/AAP PCV7-shortage recommendations, (4) and what factors were associated with nonadherence to the recommendations.
METHODS
Study Design and Population
We conducted a cross-sectional mail survey among 2500 US AAP physician members, excluding residents in training. The AAP provided a mailing list of members randomly sampled from 39621 members residing in the 50 states and the District of Columbia. In 2003, 79% of pediatricians certified by the American Board of Pediatrics were AAP members (American Academy of Pediatrics, American Board of Pediatrics board-certified pediatricians market share report, unpublished data, 2004). Sampled physicians received up to 4 mailings from November 2002 through March 2003; surveys from physicians who provided outpatient primary pediatric care and immunizations including PCV7 were eligible for analyses. The protocol was submitted to the CDC Institutional Review Board, which exempted it from review.
Survey Instrument
The survey included questions about the physicians and their practice characteristics; the physicians' PCV7-shortage experience, including perceived PCV7-shortage levels in their public and private vaccine supplies on a "typical" day during the fall of 2002; their knowledge of the PCV7-shortage recommendations; and the existence of a system to track children whose vaccination was deferred (a copy of the survey is available from the corresponding author [K.R.B.] by request). A shortage of PCV7 was defined as any shortfall of the 4-dose infant series.6 The degree of shortage was classified by using terminology in the ACIP/AAP shortage recommendations on the basis of the level of shortfall of the 4-dose infant series: none (0% shortfall), moderate (1–24%), severe (25–50%), more severe (51–99%),6 and no vaccine in stock (100%). During survey development, we solicited input from several practicing, Atlanta-based, pediatric health care providers.
To evaluate PCV7 vaccination practices and adherence to the ACIP/AAP shortage recommendations, we asked physicians to describe their vaccination practices at well-child visits in response to several hypothetical clinical scenarios. To evaluate adherence to the recommendation to defer the fourth dose for healthy children, physicians were asked to report how commonly they administered PCV7 at the 12- to 15-month well-child visit during the shortage in fall 2002 for a healthy child who had received all 3 infant doses. Physicians who reported "sometimes" or "always" administering this dose were considered to be nonadherent; those who "rarely" or "never" administered this dose were defined as adherent. Six other scenarios were also presented (Table 1, scenarios A–F), to which pediatricians could indicate that they would administer PCV7, not administer PCV7, or substitute pneumococcal polysaccharide vaccine. Adherence was assessed in conjunction with each pediatrician's reported PCV7-shortage level.6 Responses from scenarios A and B (Table 1) also were used to determine if PCV7 vaccination practices during the shortage differed for children insured through the public and private sectors. Adherence to the recommendation to maintain a tracking system for patient recall among pediatricians who reported deferring some PCV7 vaccinations was also evaluated; physicians who indicated that they maintained a tracking system, including a manual system (eg, keeping written patient lists), were defined as adherent. Physicians who reported maintaining no recall system, tracked patients only by writing notes in an unflagged chart, or asked parents to call the practice rather than have the practice track the patients, were considered to have no system and were defined as nonadherent.
Nonresponder Short Survey
To evaluate whether survey responders and nonresponders experienced the shortage differently, we conducted a short survey of office managers on a random sample of 125 nonresponding physicians from June 2003 through August 2003 using both telephone and fax. This nonresponder survey included questions designed to assess the proportion of nonresponders who were eligible for the study and the proportion who reported having any level of PCV7 shortage in their practice during fall 2002.
Statistical Analysis
The data were analyzed using SAS 8.0 (SAS Institute, Cary, NC). For each characteristic, missing and "don't know" responses were excluded from the analyses. We analyzed whether the presence of a PCV7 shortage in the practices' dominant vaccine supply (public versus private) and 7 physician demographic and practice characteristics were associated with physician-reported nonadherence to the ACIP/AAP shortage recommendations to defer the fourth PCV7 dose among healthy children. These 7 characteristics were selected on the basis of the literature and authors' clinical experience. Logistic regression was used to assess each of the variables in a univariate analysis and all 8 variables in a multivariate model; 2-tailed P values of <.05 were considered significant.
RESULTS
Of 2500 surveys mailed, 22 were returned by the postal service because of incorrect addresses. Of the remaining 2478 surveys, 1412 (57%) were completed; 946 (67%) of these respondents met the eligibility criteria and were included in the analyses. Because of missing and "don't know" responses, denominators used were less than the overall sample size. Of 928 eligible surveys with available information, 878 (95%) were completed by the surveyed physician; 5% were from an office representative, most commonly a nurse. Of the 125 nonresponders identified for the short follow-up survey, 3 subsequently were identified to have completed the study survey. Among 122 remaining nonresponders, 62 (51%) of their office managers (or other representatives) completed the follow-up survey. Five (4%) declined participation, 10 (8%) indicated that the physician was no longer working at the practice, and 45 (37%) could not be contacted. Among nonresponder surveys, 71% (44 of 62) of physicians met eligibility criteria for the study. Assuming the proportion of physicians who no longer worked at the practice was the same among the nonresponding physicians (8%) and the 2500 physicians on the initial survey mailing list, then the overall adjusted study survey response rate was calculated as 61% (1412 of 2300).
All eligible respondents indicated that they were pediatricians or pediatricians and internists; 50 of 932 (5%) reported having a pediatric subspecialty (Table 2). Compared with all US pediatricians in 2001,12 a similar proportion of female pediatricians and black and Asian pediatricians were represented in this study. Among 931 pediatricians, 744 (80%) cared for children with public and private insurance, 132 (14%) cared for only private patients, and 55 (6%) cared for only public patients. Of 877 pediatricians, 711 (81%) were in practices that administered vaccines through the federal Vaccines for Children (VFC) program.13
PCV7-Shortage Experience and Vaccination Practices in the Public and Private Sectors
Among the 788 study pediatricians who administered privately purchased PCV7, 621 (79%) reported some level of PCV7 shortage in their private supply; the percentage was the same (562 of 707 [79%]) for pediatricians who administered publicly purchased PCV7 during the fall of 2002. The distribution of reported shortage levels was similar among the pediatricians' private and public PCV7 supplies (Fig 1). Of 43 nonresponders, 35 (81%) reported a PCV7 shortage during the fall of 2002. From August 2001 through the time of survey completion, 690 of 869 (79%) study pediatricians reported being out of stock of PCV7 at some time; 63% had no PCV7 supply for 1 months.
Of 799 pediatricians who indicated that they provided immunizations during well-child visits for 6-month-olds in both the public and private sectors (Table 1, scenarios A and B), 751 (94%) reported vaccinating these infants with PCV7 in the same manner during the shortage. Pediatricians used the PCV7 as follows: vaccinated infants in both the public and private sector: 70%; didn't vaccinate either group: 24%; vaccinated private sector infants only: 4%; or vaccinated public sector infants only: 2%.
Reported Knowledge and Beliefs About ACIP/AAP PCV7-Shortage Recommendations
Among 905 pediatricians, 850 (94%) reported having some awareness of the ACIP/AAP PCV7-shortage recommendations; 92% of these pediatricians reported knowing the content of the recommendations "somewhat" or "very well." Among pediatricians with awareness of the recommendations, most reported learning about the recommendations from the AAP (85%) and CDC (53%). Of 818 pediatricians with awareness, 707 (86%) believed that the recommendations were "somewhat" or "very" applicable to their practice. Few (14%) pediatricians with awareness reported following state or local health department or other recommendations that they perceived as different from those of the ACIP/AAP. Among 735 pediatricians with awareness, 307 (42%) reported that barriers to use of the PCV7-shortage recommendations existed (Fig 2).
Reported Adherence to ACIP/AAP Recommendations
Among 779 pediatricians who reported some awareness of the ACIP/AAP PCV7-shortage recommendations, 660 (85%) reported following the recommendations "always" or "most of the time." On the basis of survey responses to scenarios from pediatricians, both with and without reported awareness of the recommendations, adherence levels varied for the components of the recommendations.
Pediatricians adhered better to recommendations to continue administering PCV7 doses according to the preshortage schedule than to recommendations to defer doses during the shortage.6 In the hypothetical scenarios to evaluate adherence to the recommendation to continue vaccinating children with high-risk medical conditions (Table 1, scenarios C and D), 91% of pediatricians reported administering the fourth PCV7 dose to 15-month-old children with sickle cell anemia with public (729 of 797) or private insurance (791 of 874). Likewise, of 528 pediatricians with no, moderate, or severe shortage, 518 (98%) reported continuing to provide the second PCV7 dose to a healthy 4-month-old infant (Table 1, scenario E), as recommended. In the healthy 6-month-old infant scenarios (Table 1, scenarios A and B), among pediatricians with no shortage or a moderate shortage, 84% to 87% reported administering the third PCV7 dose as recommended (Table 3). By contrast, only 43% to 46% of pediatricians with a severe or worse shortage reported deferring the third dose, as was recommended in this situation. In the scenario to evaluate use of PCV7 in an unvaccinated, healthy 2-year-old (Table 1, scenario F), 350 of 877 (40%) pediatricians reported administering PCV7, contrary to recommendations.
Reported adherence to the recommendation to defer the fourth PCV7 dose also was limited. Of 906 pediatricians, 441 (49%) reported nonadherence in a hypothetical scenario for a healthy child 12 to 15 months old who had received the 3 infants doses; 168 (19%) reported "sometimes" and 273 (30%) reported "always" administering the fourth dose. Of the 465 adherent pediatricians, 164 (18% of the total) reported "rarely" and 301 (33% of the total) reported "never" administering this dose. A greater proportion of pediatricians with no PCV7 shortage in the practice's dominant PCV7 supply (72%) were nonadherent than pediatricians with a shortage (42%). Of 290 pediatricians who reported "sometimes" or "rarely" administering the fourth dose, the following factors were commonly noted to influence their decision to administer the fourth dose: a child's attendance in childcare (75%); a history of recurrent otitis media (60%); and parental desire for vaccine (49%). The child's race (18%) and insurance status (17%) were less commonly reported as influential factors.
To evaluate potential factors associated with reported nonadherence to the recommendation to defer the fourth dose, univariate and multivariate analyses of physician and practice characteristics were performed (Table 4). In the multivariate analysis, 3 factors for nonadherence were statistically significant (P < .05): no PCV7 shortage in the practices' dominant PCV7 supply (public versus private), compared with any level of shortage (odds ratio [OR]: 3.67; 95% confidence interval [CI]: 2.40–5.63); solo private practice compared with nonsolo private practice (OR: 2.18; 95% CI: 1.26–3.77); and being male (OR: 1.51; 95% CI: 1.08–2.12). Results were similar in an analysis that excluded pediatricians who reported having no PCV7 available (data not shown).
Tracking-System Adherence
Among 897 pediatricians providing information about whether they deferred PCV7 doses, 855 (95%) reported deferring PCV7 vaccination for their patients during the shortage. Among 834 pediatricians who reported deferring PCV7, 298 (36%) reported not maintaining any system to track and recall these patients and were nonadherent; 417 (50%) reported using a manual system (Fig 3).
DISCUSSION
Our study demonstrates that the 2001–2003 PCV7 shortage had a substantial impact on US primary care pediatricians and their patients. Nearly 80% of physicians reported experiencing a shortage in their public and private PCV7 vaccine supplies during the shortage. More than 60% reported being out of stock of PCV7 for 1 months, and virtually all changed their PCV7 vaccination practices as a result. To the best of our knowledge, our study is the first to assess what factors influence US clinicians' immunization decision-making during a vaccine shortage. It provides insight to help formulate recommendations and improve physician adherence to recommendations during future vaccine shortages.
We found that the PCV7 shortage had a similar impact on children in the public and private sectors, with 94% of pediatricians in our study reporting using PCV7 in the same manner for children in both sectors. In addition, few of pediatricians (17%) cited a child's insurance status as a factor influencing their PCV7 immunization decision-making. During the shortage, the CDC worked closely with the manufacturer to promote equitable distribution of PCV7 among the public and private vaccine supplies. This effort seems to have been effective and should be implemented during future vaccine shortages.
Two prior studies assessed how the PCV7 shortage affected health care providers.14,15 Early in the shortage, during the fall of 2001, Freed et al14 interviewed staff responsible for ordering vaccine at private practices in 12 states that do not purchase all childhood vaccines from the public sector. Similar to our study findings, 70% and 80% of practices reported disruptions in the PCV7 public and private vaccine supplies, respectively. During the winter of 2002, Stokely et al15 surveyed health care providers enrolled in the publicly purchased Vaccines for Children program. In contrast to our study and that of Freed et al, less than half of health care providers reported a problem ordering or receiving PCV7 during the shortage.15 Similar to our study, both earlier studies suggested that the PCV7 shortage had an equitable impact on the public and private PCV7 supplies.14,15
Most pediatricians in our study reported knowing about and at least partially adhering to the PCV7-shortage recommendations; however, adherence varied by the specific recommendation. Adherence to recommendations that supported preshortage schedules and permitted delivery of more vaccine doses to individual patients was higher than adherence to recommendations to decrease the number of doses provided. During the shortage, >90% of pediatricians reported vaccinating high-risk patients with sickle cell anemia with the complete 4-dose schedule, as recommended. Although we only assessed adherence for children with sickle cell anemia, these findings likely could be extrapolated to children with other ACIP-specified high-risk medical conditions. By contrast, approximately half of the pediatricians reported that they sometimes or always administered the fourth PCV7 dose to healthy 15-month-old children during the shortage, contrary to recommendations. As with pediatricians in our study, more than half of US emergency-department physicians reported using extra tetanus and diphtheria toxoids vaccine (Td), beyond that recommended, during a national Td shortage.16
Significant demographic and practice characteristics associated with extra PCV7 vaccination during the shortage included being male or a solo practitioner. These factors also were associated with reported nonadherence in other physician studies of recommendation adherence.17–19 Although these results identify categories of physicians who might benefit from targeted education to improve adherence, they do not provide insight into why many pediatricians did not follow recommendations to defer PCV7 during the shortage.
"First, Do No Harm"
A significant factor associated with providing the fourth PCV7 dose to healthy children during the 2001–2003 shortage was not having a PCV7 shortage in an individual practice. In addition, more than half of the pediatricians who reported sometimes or rarely administering the fourth PCV7 dose during the shortage noted that childcare attendance or history of recurrent otitis media, factors associated with increased physician recommendation of PCV7 for older children before the shortage,20 influenced their decision-making. Taken together, these findings suggest that many pediatricians who decided to administer the fourth dose did so because they had vaccine available and believed that they were serving the best interests of their patients. Pediatricians who faced a shortage in their own practice might have prioritized available PCV7 and followed recommendations to provide the broadest benefit to children within their patient population.
As with our study, others have suggested that physicians adhere less well to guidelines that recommend suspending an established behavior than they do to guidelines that recommend adding a new behavior.21 This phenomenon is likely due in part to a difference in goals, perceptions, and expectations between the clinical practitioners who use the recommendations and the public health experts who develop them. A study of Canadian family physicians' acceptance and beliefs about the 1980 recommendation from the Canadian Task Force on Periodic Health Examination (predecessor to the Canadian Task Force on Preventive Health Care) to discontinue the routine annual physical examination found that most physicians continued to support this practice; all believed that "it was easier to live with not following guidelines than with having missed a diagnosis."22
This same principle to "first, do no harm" to an individual patient may explain why many US pediatricians with available vaccine continued to vaccinate children contrary to recommendations during the 2001–2003 PCV7 shortage. After PCV7 licensure, physicians rapidly adopted the 4-dose PCV7 series into their vaccination practices.20 In 2001, when the PCV7 shortage began, given limited prelicensure evidence that the 3-dose PCV7 series was effective against invasive pneumococcal disease, physicians might have believed that the 4-dose series was substantially better than the fewer-dose series. Recent preliminary CDC postlicensure data support the short-term effectiveness of deferring the fourth PCV7 dose among healthy children.23 The 4-dose PCV7 series was found to be 97% effective (95% CI: 76–100%) against invasive pneumococcal disease caused by serotypes represented in the vaccine; the 3-dose series was 87% effective (95% CI: 71–94%) among children who received it before 1 year of age.23 Because the 4-dose infant schedule might provide long-term benefits to vaccinated individuals and the population, in the absence of a shortage, it continues to be recommended.5,10,11
Patient-Tracking System
Although nearly all pediatricians reported deferring PCV7 vaccinations during the shortage, more than one third (36%) reported that they did not maintain any system to track and recall their patients when vaccination was deferred; half reported using a manual system that might be cumbersome, especially if a shortage persists. During the 5 childhood vaccine shortages from 2001 to 2003, all interim recommendations specified that providers should maintain a patient call-back system to help facilitate timely catch-up vaccination after resolution of the shortages.1,2,4,6 Our study and the survey of emergency-department physicians during the Td shortage16 suggest that the intent of this goal was not optimally achieved. Although immunization reminder-recall systems are effective24 and recommended as a standard preventive care measure,25 only 16% of US pediatricians responding to a national survey reported using them routinely26; lack of time or funding and inability to identify children at a specific age were cited as the most common barriers.26 In our study, among pediatricians reporting barriers to PCV7-shortage recommendation adherence, most (82%) noted difficulty about recalling patients whose vaccination was deferred and staff time constraints (55%) as barriers to adherence. Promoting strategies to increase use of practice-based immunization reminder-recall systems, which might include identifying and training a staff person in the practice and expanding use of immunization registries,26 might strengthen practices' ability to implement patient-recall systems during times of vaccine shortage.
Limitations
Our study had several limitations. The adjusted response rate of 61% was comparable to the mean response rates (52–61%) for published mail surveys of physicians.27,28 Nevertheless, responders might have differed from nonresponders. Information obtained from a sample of nonresponders suggested that a similar proportion as responders experienced a PCV7 shortage and met eligibility criteria. As with all surveys, our study only assessed reported behavior, which might be different from actual behavior. Finally, our study only evaluated pediatricians, and thus our findings might not be generalizable to family physicians, nonphysician practitioners, or nurses who also provide immunizations to children. Several studies have noted a difference in immunization beliefs and practices between pediatricians and family physicians.20,29,30
A Second PCV7 Shortage
Multiple recent vaccine shortages and systematic factors affecting the vaccine industry suggested that future vaccine shortages would occur,31,32 and in February 2004, a second shortage of PCV7 did occur.33 Drawing on lessons learned from the 2001–2003 shortage, the CDC, in collaboration with the AAP, American Academy of Family Physicians, and ACIP, implemented measures designed to improve physician adherence to 2004 PCV7-shortage recommendations. Recommendations were simpler than those issued during the 2001–2003 shortage: the fourth dose (and later the third and fourth doses) was suspended for all healthy children irrespective of practice shortage levels, and health care providers were not asked to quantify the level of shortage.23,33 The complete 4-dose vaccination series continued to be recommended for children at high risk for invasive pneumococcal disease.10,23,33 The 2004 recommendations included preliminary data showing that the fewer-dose PCV7 schedule among healthy children was effective in the short term.23,33 In addition, because our survey identified parental pressure for PCV7 to be a common barrier to adherence among pediatricians, the CDC and AAP posted information on the Internet for parents about the shortage.34 As with the first PCV7 shortage, the CDC worked closely with the manufacturer and state health departments to promote an equitable distribution between the public and private sectors. During the second shortage, the manufacturer also voluntarily implemented an allocation system to facilitate an equitable distribution among private purchasers.35 The second shortage ended in September 2004.36 Studies are underway to evaluate whether physicians had better adherence to the 2004 PCV7-shortage recommendations, compared with the 2001–2003 shortage recommendations. Studies are needed to assess the success of catch-up vaccination and whether physicians resume routine PCV7 vaccination practices after prolonged vaccine shortages. In addition, studies will be needed to determine if lessons learned from the PCV7-shortage experiences are applicable to other vaccine shortages and to identify strategies that improve physician adherence to national vaccine-shortage recommendations, including use of patient-tracking and -recall systems.
ACKNOWLEDGMENTS
We thank the numerous individuals who contributed to this study including: Martha Cook, MS, Karen O'Connor, and Sanford Sharp (American Academy of Pediatrics staff); Renee Renfus, MD, Mary Beth Noonan, MD, Terrance A. Yoder, MD, Laura Yedvobnick PA, Jo Ann West, PNP, Sandy Boyles, PNP, Elliot Feit, MD, J. Vincent Vigil, MD, Monica Marlowe, MD, Jennifer D. Smart, MD, Jan Fitzgerald-Soapes, MD, Richard Shelton, MD, David Levine, MD, and Jalal Zuberi, MD (Atlanta-based health care providers); and Stephanie Renna, Shannon Stokely, MPH, Jeanne M. Santoli, MD, MPH, Stephanie Payne, Cynthia G. Whitney, MD, MPH, Sonja S. Hutchins, MD, MPH, and Kristine M. Bisgard, DVM, MPH (Centers for Disease Control and Prevention colleagues).
FOOTNOTES
Accepted Oct 19, 2004.
Preliminary data were presented at the National Immunization Conference; March 17–20, 2003; Chicago, IL; and at the American Academy of Pediatrics National Conference and Exhibition; November 1–5, 2003; New Orleans, LA.
No conflict of interest declared.
Mr MacNeil's current address is: Graduate School of Arts and Sciences, Harvard University, Boston, Massachusetts.
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Centers for Disease Control and Prevention. Limited supply of pneumococcal conjugate vaccine. MMWR Morb Mortal Wkly Rep. 2003;52 :1234
Centers for Disease Control and Prevention. Pneumococcal conjugate vaccine shortage resolved. MMWR Morb Mortal Wkly Rep. 2004;53 :851 –852(Karen R. Broder, MD, FAAP)
Epidemiology Program Office, Centers for Disease Control and Prevention, Atlanta, Georgia
ABSTRACT
Background. A national shortage of heptavalent pneumococcal conjugate vaccine (PCV7) occurred from September 2001 through May 2003. In December 2001 and January 2002, the Advisory Committee on Immunization Practices and the American Academy of Pediatrics (AAP) issued PCV7-shortage recommendations, emphasizing that all health care providers decrease the number of doses for healthy children so that more children could receive some PCV7.
Objectives. We assessed (1) how the PCV7 shortage affected pediatricians, (2) whether children in the public and private sectors were vaccinated differently during the shortage, (3) pediatricians' knowledge of and adherence to the Advisory Committee on Immunization Practices/AAP recommendations, (4) and what factors were associated with nonadherence to the recommendations.
Methods. We conducted a cross-sectional mail survey of 2500 US physician-members of the AAP from November 2002 through March 2003; physicians providing childhood immunizations were eligible. We asked about PCV7-shortage experience, assessed recommendation adherence through clinical scenarios, and modeled potential factors associated with reported nonadherence to the recommendation to defer the fourth PCV7 dose.
Results. Of 2478 surveys sent to valid addresses, 1412 (57%) completed surveys were received; 946 (67%) of these were from eligible pediatricians. Overall, 79% experienced a PCV7 shortage, 94% reported being aware of the recommendations, and 42% reported barriers to recommendation adherence. Ninety-four percent reported vaccinating 6-month-old infants with private or public insurance in the same manner. As recommended, 91% reported fully vaccinating high-risk patients. Contrary to recommendations, 49% reported sometimes or always administering the fourth PCV7 dose to healthy children 12 to 15 months old; their reasons included recurrent otitis media, childcare attendance, and parental desire. Controlling for other characteristics, pediatricians who had no PCV7 shortage in their practices were significantly more likely to report administering the fourth dose than pediatricians who had a shortage (odds ratio [OR]: 3.67; 95% confidence interval [CI]: 2.40–5.63). Other factors associated with nonadherence were being in solo private practice (OR: 2.18; 95% CI: 1.26–3.77) or being male (OR: 1.51; 95% CI: 1.08–2.12). Among pediatricians deferring PCV7, 36% reported having no system to track children for whom PCV7 was deferred.
Conclusions. Many pediatricians, both with and without a PCV7 shortage, administered more PCV7 doses than recommended. Pediatricians without a shortage were less likely to limit use, which suggests that they might have focused on the perceived value of administering the full schedule to their patients in preference to broader public health goals. Providing more information to physicians on the effectiveness of a fewer-dose schedule and the risk of disease when vaccine is deferred and educating parents might increase adherence to recommendations and achieve more equitable coverage during vaccine shortages.
Key Words: adherence pneumococcal conjugate vaccine
Abbreviations: CDC, Centers for Disease Control and Prevention ACIP, Advisory Committee on Immunization Practices AAP, American Academy of Pediatrics PCV7, heptavalent pneumococcal conjugate vaccine OR, odds ratio CI, confidence interval Td, tetanus and diphtheria toxoids vaccine
2000 through 2003, an unprecedented number of vaccine shortages occurred in the United States, affecting 5 vaccines in the recommended childhood and adolescent immunization schedule. 1–5 To help clinicians manage these shortages and to achieve the benefits of vaccination for as many children as possible, the Centers for Disease Control and Prevention (CDC), the Advisory Committee on Immunization Practices (ACIP), the American Academy of Pediatrics (AAP), and the American Academy of Family Physicians developed and promoted unified vaccine-specific shortage recommendations 1–4,6–8 that differed from their routine childhood and adolescent immunization schedule.5
A shortage of the heptavalent pneumococcal conjugate vaccine (PCV7; marketed as Prevnar by Wyeth Vaccines, Collegeville, PA) began in September 2001,3 1 year after the AAP9 and ACIP10 published recommendations for universal PCV7 use in young children. In September 2001, the CDC issued brief recommendations for use of PCV7 during the shortage.3 In December 2001, when it was determined that the shortage would last longer and be more widespread than initially predicted, the ACIP released updated, detailed recommendations for PCV7 use in the setting of the prolonged shortage6; the AAP adopted these recommendations.7 The ACIP/AAP PCV7-shortage recommendations were based on preliminary data suggesting that a fewer-dose PCV7 schedule prevents invasive pneumococcal disease in healthy children, at least in the short term.6 The recommendations stated that health care providers should (1) prioritize children at high risk for invasive pneumococcal disease and vaccinate them according to the routine childhood and adolescent preshortage schedule, which recommends a 4-dose infant series, (2) defer the fourth dose for all healthy children not included in ACIP-specified high-risk categories, irrespective of individual practice shortage level, (3) make additional deferral decisions based on the practice's PCV7-shortage level, and (4) maintain a tracking system to recall children whose PCV7 vaccination was deferred.6,10 During the shortage, recommendations for the third PCV7 infant dose varied by shortage level. In the setting of no or moderate shortage, the third infant dose was recommended; in a severe shortage, the third dose should have been deferred.6 This national PCV7 shortage lasted 21 months; the CDC issued catch-up recommendations in May 2003.11
The ACIP/AAP PCV7-shortage recommendations had sound public health goals: to conserve vaccine to permit broad vaccination of children and to provide guidance to clinicians during the shortage. However, there was concern about implementation for several reasons. First, recommendations were complex at a time when clinicians were facing simultaneous vaccine shortages. Second, there was potential for different PCV7 availability and vaccination practices for patients using publicly and privately purchased PCV7, even within the same practice. Third, the recommendation to defer the fourth PCV7 dose for all healthy children, even in practices with an adequate supply, potentially created a conflict between the perceived interests of children within a practice and the public health interests of children in the community at large.
We undertook this study to determine (1) how the 2001–2003 PCV7 shortage affected US pediatricians, (2) if pediatricians vaccinated children in the public and private sectors differently, (3) if pediatricians had knowledge of and adhered to the ACIP/AAP PCV7-shortage recommendations, (4) and what factors were associated with nonadherence to the recommendations.
METHODS
Study Design and Population
We conducted a cross-sectional mail survey among 2500 US AAP physician members, excluding residents in training. The AAP provided a mailing list of members randomly sampled from 39621 members residing in the 50 states and the District of Columbia. In 2003, 79% of pediatricians certified by the American Board of Pediatrics were AAP members (American Academy of Pediatrics, American Board of Pediatrics board-certified pediatricians market share report, unpublished data, 2004). Sampled physicians received up to 4 mailings from November 2002 through March 2003; surveys from physicians who provided outpatient primary pediatric care and immunizations including PCV7 were eligible for analyses. The protocol was submitted to the CDC Institutional Review Board, which exempted it from review.
Survey Instrument
The survey included questions about the physicians and their practice characteristics; the physicians' PCV7-shortage experience, including perceived PCV7-shortage levels in their public and private vaccine supplies on a "typical" day during the fall of 2002; their knowledge of the PCV7-shortage recommendations; and the existence of a system to track children whose vaccination was deferred (a copy of the survey is available from the corresponding author [K.R.B.] by request). A shortage of PCV7 was defined as any shortfall of the 4-dose infant series.6 The degree of shortage was classified by using terminology in the ACIP/AAP shortage recommendations on the basis of the level of shortfall of the 4-dose infant series: none (0% shortfall), moderate (1–24%), severe (25–50%), more severe (51–99%),6 and no vaccine in stock (100%). During survey development, we solicited input from several practicing, Atlanta-based, pediatric health care providers.
To evaluate PCV7 vaccination practices and adherence to the ACIP/AAP shortage recommendations, we asked physicians to describe their vaccination practices at well-child visits in response to several hypothetical clinical scenarios. To evaluate adherence to the recommendation to defer the fourth dose for healthy children, physicians were asked to report how commonly they administered PCV7 at the 12- to 15-month well-child visit during the shortage in fall 2002 for a healthy child who had received all 3 infant doses. Physicians who reported "sometimes" or "always" administering this dose were considered to be nonadherent; those who "rarely" or "never" administered this dose were defined as adherent. Six other scenarios were also presented (Table 1, scenarios A–F), to which pediatricians could indicate that they would administer PCV7, not administer PCV7, or substitute pneumococcal polysaccharide vaccine. Adherence was assessed in conjunction with each pediatrician's reported PCV7-shortage level.6 Responses from scenarios A and B (Table 1) also were used to determine if PCV7 vaccination practices during the shortage differed for children insured through the public and private sectors. Adherence to the recommendation to maintain a tracking system for patient recall among pediatricians who reported deferring some PCV7 vaccinations was also evaluated; physicians who indicated that they maintained a tracking system, including a manual system (eg, keeping written patient lists), were defined as adherent. Physicians who reported maintaining no recall system, tracked patients only by writing notes in an unflagged chart, or asked parents to call the practice rather than have the practice track the patients, were considered to have no system and were defined as nonadherent.
Nonresponder Short Survey
To evaluate whether survey responders and nonresponders experienced the shortage differently, we conducted a short survey of office managers on a random sample of 125 nonresponding physicians from June 2003 through August 2003 using both telephone and fax. This nonresponder survey included questions designed to assess the proportion of nonresponders who were eligible for the study and the proportion who reported having any level of PCV7 shortage in their practice during fall 2002.
Statistical Analysis
The data were analyzed using SAS 8.0 (SAS Institute, Cary, NC). For each characteristic, missing and "don't know" responses were excluded from the analyses. We analyzed whether the presence of a PCV7 shortage in the practices' dominant vaccine supply (public versus private) and 7 physician demographic and practice characteristics were associated with physician-reported nonadherence to the ACIP/AAP shortage recommendations to defer the fourth PCV7 dose among healthy children. These 7 characteristics were selected on the basis of the literature and authors' clinical experience. Logistic regression was used to assess each of the variables in a univariate analysis and all 8 variables in a multivariate model; 2-tailed P values of <.05 were considered significant.
RESULTS
Of 2500 surveys mailed, 22 were returned by the postal service because of incorrect addresses. Of the remaining 2478 surveys, 1412 (57%) were completed; 946 (67%) of these respondents met the eligibility criteria and were included in the analyses. Because of missing and "don't know" responses, denominators used were less than the overall sample size. Of 928 eligible surveys with available information, 878 (95%) were completed by the surveyed physician; 5% were from an office representative, most commonly a nurse. Of the 125 nonresponders identified for the short follow-up survey, 3 subsequently were identified to have completed the study survey. Among 122 remaining nonresponders, 62 (51%) of their office managers (or other representatives) completed the follow-up survey. Five (4%) declined participation, 10 (8%) indicated that the physician was no longer working at the practice, and 45 (37%) could not be contacted. Among nonresponder surveys, 71% (44 of 62) of physicians met eligibility criteria for the study. Assuming the proportion of physicians who no longer worked at the practice was the same among the nonresponding physicians (8%) and the 2500 physicians on the initial survey mailing list, then the overall adjusted study survey response rate was calculated as 61% (1412 of 2300).
All eligible respondents indicated that they were pediatricians or pediatricians and internists; 50 of 932 (5%) reported having a pediatric subspecialty (Table 2). Compared with all US pediatricians in 2001,12 a similar proportion of female pediatricians and black and Asian pediatricians were represented in this study. Among 931 pediatricians, 744 (80%) cared for children with public and private insurance, 132 (14%) cared for only private patients, and 55 (6%) cared for only public patients. Of 877 pediatricians, 711 (81%) were in practices that administered vaccines through the federal Vaccines for Children (VFC) program.13
PCV7-Shortage Experience and Vaccination Practices in the Public and Private Sectors
Among the 788 study pediatricians who administered privately purchased PCV7, 621 (79%) reported some level of PCV7 shortage in their private supply; the percentage was the same (562 of 707 [79%]) for pediatricians who administered publicly purchased PCV7 during the fall of 2002. The distribution of reported shortage levels was similar among the pediatricians' private and public PCV7 supplies (Fig 1). Of 43 nonresponders, 35 (81%) reported a PCV7 shortage during the fall of 2002. From August 2001 through the time of survey completion, 690 of 869 (79%) study pediatricians reported being out of stock of PCV7 at some time; 63% had no PCV7 supply for 1 months.
Of 799 pediatricians who indicated that they provided immunizations during well-child visits for 6-month-olds in both the public and private sectors (Table 1, scenarios A and B), 751 (94%) reported vaccinating these infants with PCV7 in the same manner during the shortage. Pediatricians used the PCV7 as follows: vaccinated infants in both the public and private sector: 70%; didn't vaccinate either group: 24%; vaccinated private sector infants only: 4%; or vaccinated public sector infants only: 2%.
Reported Knowledge and Beliefs About ACIP/AAP PCV7-Shortage Recommendations
Among 905 pediatricians, 850 (94%) reported having some awareness of the ACIP/AAP PCV7-shortage recommendations; 92% of these pediatricians reported knowing the content of the recommendations "somewhat" or "very well." Among pediatricians with awareness of the recommendations, most reported learning about the recommendations from the AAP (85%) and CDC (53%). Of 818 pediatricians with awareness, 707 (86%) believed that the recommendations were "somewhat" or "very" applicable to their practice. Few (14%) pediatricians with awareness reported following state or local health department or other recommendations that they perceived as different from those of the ACIP/AAP. Among 735 pediatricians with awareness, 307 (42%) reported that barriers to use of the PCV7-shortage recommendations existed (Fig 2).
Reported Adherence to ACIP/AAP Recommendations
Among 779 pediatricians who reported some awareness of the ACIP/AAP PCV7-shortage recommendations, 660 (85%) reported following the recommendations "always" or "most of the time." On the basis of survey responses to scenarios from pediatricians, both with and without reported awareness of the recommendations, adherence levels varied for the components of the recommendations.
Pediatricians adhered better to recommendations to continue administering PCV7 doses according to the preshortage schedule than to recommendations to defer doses during the shortage.6 In the hypothetical scenarios to evaluate adherence to the recommendation to continue vaccinating children with high-risk medical conditions (Table 1, scenarios C and D), 91% of pediatricians reported administering the fourth PCV7 dose to 15-month-old children with sickle cell anemia with public (729 of 797) or private insurance (791 of 874). Likewise, of 528 pediatricians with no, moderate, or severe shortage, 518 (98%) reported continuing to provide the second PCV7 dose to a healthy 4-month-old infant (Table 1, scenario E), as recommended. In the healthy 6-month-old infant scenarios (Table 1, scenarios A and B), among pediatricians with no shortage or a moderate shortage, 84% to 87% reported administering the third PCV7 dose as recommended (Table 3). By contrast, only 43% to 46% of pediatricians with a severe or worse shortage reported deferring the third dose, as was recommended in this situation. In the scenario to evaluate use of PCV7 in an unvaccinated, healthy 2-year-old (Table 1, scenario F), 350 of 877 (40%) pediatricians reported administering PCV7, contrary to recommendations.
Reported adherence to the recommendation to defer the fourth PCV7 dose also was limited. Of 906 pediatricians, 441 (49%) reported nonadherence in a hypothetical scenario for a healthy child 12 to 15 months old who had received the 3 infants doses; 168 (19%) reported "sometimes" and 273 (30%) reported "always" administering the fourth dose. Of the 465 adherent pediatricians, 164 (18% of the total) reported "rarely" and 301 (33% of the total) reported "never" administering this dose. A greater proportion of pediatricians with no PCV7 shortage in the practice's dominant PCV7 supply (72%) were nonadherent than pediatricians with a shortage (42%). Of 290 pediatricians who reported "sometimes" or "rarely" administering the fourth dose, the following factors were commonly noted to influence their decision to administer the fourth dose: a child's attendance in childcare (75%); a history of recurrent otitis media (60%); and parental desire for vaccine (49%). The child's race (18%) and insurance status (17%) were less commonly reported as influential factors.
To evaluate potential factors associated with reported nonadherence to the recommendation to defer the fourth dose, univariate and multivariate analyses of physician and practice characteristics were performed (Table 4). In the multivariate analysis, 3 factors for nonadherence were statistically significant (P < .05): no PCV7 shortage in the practices' dominant PCV7 supply (public versus private), compared with any level of shortage (odds ratio [OR]: 3.67; 95% confidence interval [CI]: 2.40–5.63); solo private practice compared with nonsolo private practice (OR: 2.18; 95% CI: 1.26–3.77); and being male (OR: 1.51; 95% CI: 1.08–2.12). Results were similar in an analysis that excluded pediatricians who reported having no PCV7 available (data not shown).
Tracking-System Adherence
Among 897 pediatricians providing information about whether they deferred PCV7 doses, 855 (95%) reported deferring PCV7 vaccination for their patients during the shortage. Among 834 pediatricians who reported deferring PCV7, 298 (36%) reported not maintaining any system to track and recall these patients and were nonadherent; 417 (50%) reported using a manual system (Fig 3).
DISCUSSION
Our study demonstrates that the 2001–2003 PCV7 shortage had a substantial impact on US primary care pediatricians and their patients. Nearly 80% of physicians reported experiencing a shortage in their public and private PCV7 vaccine supplies during the shortage. More than 60% reported being out of stock of PCV7 for 1 months, and virtually all changed their PCV7 vaccination practices as a result. To the best of our knowledge, our study is the first to assess what factors influence US clinicians' immunization decision-making during a vaccine shortage. It provides insight to help formulate recommendations and improve physician adherence to recommendations during future vaccine shortages.
We found that the PCV7 shortage had a similar impact on children in the public and private sectors, with 94% of pediatricians in our study reporting using PCV7 in the same manner for children in both sectors. In addition, few of pediatricians (17%) cited a child's insurance status as a factor influencing their PCV7 immunization decision-making. During the shortage, the CDC worked closely with the manufacturer to promote equitable distribution of PCV7 among the public and private vaccine supplies. This effort seems to have been effective and should be implemented during future vaccine shortages.
Two prior studies assessed how the PCV7 shortage affected health care providers.14,15 Early in the shortage, during the fall of 2001, Freed et al14 interviewed staff responsible for ordering vaccine at private practices in 12 states that do not purchase all childhood vaccines from the public sector. Similar to our study findings, 70% and 80% of practices reported disruptions in the PCV7 public and private vaccine supplies, respectively. During the winter of 2002, Stokely et al15 surveyed health care providers enrolled in the publicly purchased Vaccines for Children program. In contrast to our study and that of Freed et al, less than half of health care providers reported a problem ordering or receiving PCV7 during the shortage.15 Similar to our study, both earlier studies suggested that the PCV7 shortage had an equitable impact on the public and private PCV7 supplies.14,15
Most pediatricians in our study reported knowing about and at least partially adhering to the PCV7-shortage recommendations; however, adherence varied by the specific recommendation. Adherence to recommendations that supported preshortage schedules and permitted delivery of more vaccine doses to individual patients was higher than adherence to recommendations to decrease the number of doses provided. During the shortage, >90% of pediatricians reported vaccinating high-risk patients with sickle cell anemia with the complete 4-dose schedule, as recommended. Although we only assessed adherence for children with sickle cell anemia, these findings likely could be extrapolated to children with other ACIP-specified high-risk medical conditions. By contrast, approximately half of the pediatricians reported that they sometimes or always administered the fourth PCV7 dose to healthy 15-month-old children during the shortage, contrary to recommendations. As with pediatricians in our study, more than half of US emergency-department physicians reported using extra tetanus and diphtheria toxoids vaccine (Td), beyond that recommended, during a national Td shortage.16
Significant demographic and practice characteristics associated with extra PCV7 vaccination during the shortage included being male or a solo practitioner. These factors also were associated with reported nonadherence in other physician studies of recommendation adherence.17–19 Although these results identify categories of physicians who might benefit from targeted education to improve adherence, they do not provide insight into why many pediatricians did not follow recommendations to defer PCV7 during the shortage.
"First, Do No Harm"
A significant factor associated with providing the fourth PCV7 dose to healthy children during the 2001–2003 shortage was not having a PCV7 shortage in an individual practice. In addition, more than half of the pediatricians who reported sometimes or rarely administering the fourth PCV7 dose during the shortage noted that childcare attendance or history of recurrent otitis media, factors associated with increased physician recommendation of PCV7 for older children before the shortage,20 influenced their decision-making. Taken together, these findings suggest that many pediatricians who decided to administer the fourth dose did so because they had vaccine available and believed that they were serving the best interests of their patients. Pediatricians who faced a shortage in their own practice might have prioritized available PCV7 and followed recommendations to provide the broadest benefit to children within their patient population.
As with our study, others have suggested that physicians adhere less well to guidelines that recommend suspending an established behavior than they do to guidelines that recommend adding a new behavior.21 This phenomenon is likely due in part to a difference in goals, perceptions, and expectations between the clinical practitioners who use the recommendations and the public health experts who develop them. A study of Canadian family physicians' acceptance and beliefs about the 1980 recommendation from the Canadian Task Force on Periodic Health Examination (predecessor to the Canadian Task Force on Preventive Health Care) to discontinue the routine annual physical examination found that most physicians continued to support this practice; all believed that "it was easier to live with not following guidelines than with having missed a diagnosis."22
This same principle to "first, do no harm" to an individual patient may explain why many US pediatricians with available vaccine continued to vaccinate children contrary to recommendations during the 2001–2003 PCV7 shortage. After PCV7 licensure, physicians rapidly adopted the 4-dose PCV7 series into their vaccination practices.20 In 2001, when the PCV7 shortage began, given limited prelicensure evidence that the 3-dose PCV7 series was effective against invasive pneumococcal disease, physicians might have believed that the 4-dose series was substantially better than the fewer-dose series. Recent preliminary CDC postlicensure data support the short-term effectiveness of deferring the fourth PCV7 dose among healthy children.23 The 4-dose PCV7 series was found to be 97% effective (95% CI: 76–100%) against invasive pneumococcal disease caused by serotypes represented in the vaccine; the 3-dose series was 87% effective (95% CI: 71–94%) among children who received it before 1 year of age.23 Because the 4-dose infant schedule might provide long-term benefits to vaccinated individuals and the population, in the absence of a shortage, it continues to be recommended.5,10,11
Patient-Tracking System
Although nearly all pediatricians reported deferring PCV7 vaccinations during the shortage, more than one third (36%) reported that they did not maintain any system to track and recall their patients when vaccination was deferred; half reported using a manual system that might be cumbersome, especially if a shortage persists. During the 5 childhood vaccine shortages from 2001 to 2003, all interim recommendations specified that providers should maintain a patient call-back system to help facilitate timely catch-up vaccination after resolution of the shortages.1,2,4,6 Our study and the survey of emergency-department physicians during the Td shortage16 suggest that the intent of this goal was not optimally achieved. Although immunization reminder-recall systems are effective24 and recommended as a standard preventive care measure,25 only 16% of US pediatricians responding to a national survey reported using them routinely26; lack of time or funding and inability to identify children at a specific age were cited as the most common barriers.26 In our study, among pediatricians reporting barriers to PCV7-shortage recommendation adherence, most (82%) noted difficulty about recalling patients whose vaccination was deferred and staff time constraints (55%) as barriers to adherence. Promoting strategies to increase use of practice-based immunization reminder-recall systems, which might include identifying and training a staff person in the practice and expanding use of immunization registries,26 might strengthen practices' ability to implement patient-recall systems during times of vaccine shortage.
Limitations
Our study had several limitations. The adjusted response rate of 61% was comparable to the mean response rates (52–61%) for published mail surveys of physicians.27,28 Nevertheless, responders might have differed from nonresponders. Information obtained from a sample of nonresponders suggested that a similar proportion as responders experienced a PCV7 shortage and met eligibility criteria. As with all surveys, our study only assessed reported behavior, which might be different from actual behavior. Finally, our study only evaluated pediatricians, and thus our findings might not be generalizable to family physicians, nonphysician practitioners, or nurses who also provide immunizations to children. Several studies have noted a difference in immunization beliefs and practices between pediatricians and family physicians.20,29,30
A Second PCV7 Shortage
Multiple recent vaccine shortages and systematic factors affecting the vaccine industry suggested that future vaccine shortages would occur,31,32 and in February 2004, a second shortage of PCV7 did occur.33 Drawing on lessons learned from the 2001–2003 shortage, the CDC, in collaboration with the AAP, American Academy of Family Physicians, and ACIP, implemented measures designed to improve physician adherence to 2004 PCV7-shortage recommendations. Recommendations were simpler than those issued during the 2001–2003 shortage: the fourth dose (and later the third and fourth doses) was suspended for all healthy children irrespective of practice shortage levels, and health care providers were not asked to quantify the level of shortage.23,33 The complete 4-dose vaccination series continued to be recommended for children at high risk for invasive pneumococcal disease.10,23,33 The 2004 recommendations included preliminary data showing that the fewer-dose PCV7 schedule among healthy children was effective in the short term.23,33 In addition, because our survey identified parental pressure for PCV7 to be a common barrier to adherence among pediatricians, the CDC and AAP posted information on the Internet for parents about the shortage.34 As with the first PCV7 shortage, the CDC worked closely with the manufacturer and state health departments to promote an equitable distribution between the public and private sectors. During the second shortage, the manufacturer also voluntarily implemented an allocation system to facilitate an equitable distribution among private purchasers.35 The second shortage ended in September 2004.36 Studies are underway to evaluate whether physicians had better adherence to the 2004 PCV7-shortage recommendations, compared with the 2001–2003 shortage recommendations. Studies are needed to assess the success of catch-up vaccination and whether physicians resume routine PCV7 vaccination practices after prolonged vaccine shortages. In addition, studies will be needed to determine if lessons learned from the PCV7-shortage experiences are applicable to other vaccine shortages and to identify strategies that improve physician adherence to national vaccine-shortage recommendations, including use of patient-tracking and -recall systems.
ACKNOWLEDGMENTS
We thank the numerous individuals who contributed to this study including: Martha Cook, MS, Karen O'Connor, and Sanford Sharp (American Academy of Pediatrics staff); Renee Renfus, MD, Mary Beth Noonan, MD, Terrance A. Yoder, MD, Laura Yedvobnick PA, Jo Ann West, PNP, Sandy Boyles, PNP, Elliot Feit, MD, J. Vincent Vigil, MD, Monica Marlowe, MD, Jennifer D. Smart, MD, Jan Fitzgerald-Soapes, MD, Richard Shelton, MD, David Levine, MD, and Jalal Zuberi, MD (Atlanta-based health care providers); and Stephanie Renna, Shannon Stokely, MPH, Jeanne M. Santoli, MD, MPH, Stephanie Payne, Cynthia G. Whitney, MD, MPH, Sonja S. Hutchins, MD, MPH, and Kristine M. Bisgard, DVM, MPH (Centers for Disease Control and Prevention colleagues).
FOOTNOTES
Accepted Oct 19, 2004.
Preliminary data were presented at the National Immunization Conference; March 17–20, 2003; Chicago, IL; and at the American Academy of Pediatrics National Conference and Exhibition; November 1–5, 2003; New Orleans, LA.
No conflict of interest declared.
Mr MacNeil's current address is: Graduate School of Arts and Sciences, Harvard University, Boston, Massachusetts.
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