Abstract
OBJECTIVES. Our objective was to determine the following among US pediatricians: (1) perceptions regarding burden of rotavirus disease and need for a vaccine; (2) intentions for recommending a newly licensed rotavirus vaccine; (3) perceived barriers to implementation; and (4) factors associated with plans for vaccine adoption.
PATIENTS AND METHODS. A network of 431 pediatricians was recruited from a random sample of American Academy of Pediatrics’ members. The network was designed to be representative of the American Academy of Pediatrics with respect to region of the country, practice type, and practice setting. During January and February 2006, physicians were surveyed by Internet or mail. The survey contained a paragraph summarizing results of the new rotavirus vaccine trial. Respondents were asked about intentions to use the vaccine and anticipated barriers.
RESULTS. The survey response rate was 71%. Of the respondents, 52% strongly agreed and 37% somewhat agreed with the need for a rotavirus vaccine. If recommended for routine use, 50% would strongly recommend and 34% would recommend but not strongly; 52% would begin to use within 6 months and 27% from 6 months to 1 year. The top 3 “definite” barriers to implementation included concerns about uniform coverage of vaccine by insurers, lack of adequate reimbursement, and parental reluctance because of withdrawal of previous rotavirus vaccine. In multivariate analysis, factors associated with very likely adoption of the vaccine included perception of a high burden of rotavirus disease and a high level of confidence in prelicensure studies of vaccine safety. The presence of physician concerns about safety of the new vaccine and the perception of parental concerns about vaccine safety in general were negatively associated with adoption.
CONCLUSIONS. The majority of pediatricians reported willingness to implement the new rotavirus vaccine, most within 6 months. Major barriers to optimal implementation included provider concerns about reimbursement issues and parental acceptance of the vaccine.
Rotavirus is the leading cause of hospitalization and death from acute gastroenteritis among young children worldwide, especially in undeveloped countries.1–3 Although childhood rotavirus deaths are uncommon in developed countries, rotavirus causes ∼2.7 million episodes of diarrhea, resulting in ∼500000 office visits, 55000 to 70000 hospitalizations, and ∼20 to 60 deaths annually in the United States.4 The total costs associated with rotavirus infection in the United States have been estimated to be greater than $1 billion per year, approximately two thirds of which are nonmedical costs related to lost parental work.5
In 1998, a tetravalent rhesus-human reassortant rotavirus vaccine (RotaShield; Wyeth Laboratories) was licensed and recommended for routine immunization of infants in the United States.6,7 Shortly after recommendation, however, an association between RotaShield vaccination and intussusception was recognized8–11 at an estimated rate of 1 incident per 10000 vaccine recipients,10 and the vaccine was subsequently withdrawn from the market in October 1999.12 Shortly thereafter the manufacturer stopped production of the vaccine worldwide.13
Recently, the results of large clinical trials of 2 new rotavirus vaccines, both live oral vaccines intended for use in infants, were reported.14,15 Although the vaccines differ with respect to the strains and formulations used, both demonstrate high efficacy, particularly against severe disease and in preventing hospitalizations, and have not been associated with intussusception or other severe adverse events. In February 2006, the Food and Drug Administration (FDA) announced the approval of one of these vaccines, a pentavalent human-bovine reassortment rotavirus vaccine (RotaTeq; Merck, Whitehouse Station, NJ) for use in infants in the United States.16 Shortly thereafter, the Advisory Committee on Immunization Practices (ACIP) recommended routine use of the vaccine for infants in the United States at 2, 4, and 6 months of age. Dose 1 was recommended to be given by 12 weeks of age and all 3 vaccinations by 32 weeks of age, with at least a 4- to 10-week interval between doses.17
Concerns regarding introduction of any new vaccine include provider concerns regarding safety, reimbursement, vaccine supply, the growing number of pediatric vaccines, and the need to increase public awareness of the need for the vaccine. Because of the association of intussusception associated with RotaShield vaccine, RotaTeq may face more than the usual level of concern regarding unanticipated adverse effects. For the optimal implementation of this vaccine, the concerns of pediatricians must be understood and addressed. We conducted a national survey of pediatricians to determine the following: (a) perceptions regarding burden of rotavirus disease and the need for a vaccine; (b) previous experience with RotaShield; (c) intentions for recommending a new rotavirus vaccine; (d) perceived barriers to implementation of the new rotavirus vaccine; and (e) factors associated with plans for vaccine adoption.
METHODS
Study Setting
During January 4 to February 28, 2006, a mail and Internet survey was conducted regarding rotavirus infection and vaccination in a nationwide sample of pediatricians. This study was reviewed and approved for exempt status by the Colorado Multiple Institutional Review Board, and informed consent was not required.
Population: Development of the Pediatric Sentinel Provider Network
The investigation was conducted as part of the Vaccine Policy Collaborative Initiative, a program for rapid turnaround physician surveys developed collaboratively with the Centers for Disease Control and Prevention (CDC). For this program, a network of primary care pediatricians was developed. A random sample of 2500 members of the American Academy of Pediatrics (AAP) was sent up to 4 recruitment letters on letterhead from the AAP. Physicians were asked whether they would be willing to respond to 2 to 4 immunization-related surveys per year. Respondents who spent <50% of their time delivering primary care were excluded. No incentives to participate were provided. The sentinel pediatrician network was designed to be representative of the AAP membership overall. Using data from the AAP periodic membership survey,18 we determined the distribution of AAP members with respect to 3 characteristics: region of the country (Northwest, South, Midwest, and West); practice location (urban inner city, urban non–inner city/suburban, and rural); and practice setting (private, managed care, and community/hospital-based). Thirty-six unique combinations of practice characteristics were possible, each with an expected frequency based on the AAP membership survey. Applying these frequencies to target a sample size of 400, we then determined the desired number of respondents for each of these 36 “cells.” For cells with an excess number of respondents (>110% of the expected frequency), eligible physicians were randomly selected for study participation. For cells with an inadequate number of respondents (<90% expected), an additional recruitment letter was sent. In this manner, a sentinel network of 431 pediatricians was developed, with 29 (81%) of 36 cells containing the expected number of physicians. In the 7 underrepresented cells, there were 1 to 3 fewer physicians than expected. In a previous investigation conducted in this network, the attitudes of sentinel pediatricians regarding influenza vaccine shortages were compared with the attitudes of pediatricians randomly selected from the American Medical Association (AMA) master file. In that study, the attitudes of sentinel pediatricians regarding influenza vaccine were found to be generally comparable to the attitudes of pediatricians randomly sampled from the AMA.19
Survey Design
A survey regarding rotavirus infection and vaccination was developed collaboratively with the CDC. The survey was pilot tested in an advisory panel consisting of 6 practicing pediatricians from different regions of the country. The survey assessed knowledge, beliefs, and attitudes regarding rotavirus and rotavirus vaccine. It was theoretically based on the Health Belief Model20 and included questions in domains we hypothesized would affect vaccine adoption, including perceived severity, susceptibility, perceived benefit of vaccination, and perceived barriers to vaccination.21 In addition, the survey contained an informational paragraph about the trial of the new rotavirus vaccine (RotaTeq), which was licensed by the FDA on February 3, 2006.16 After reading this paragraph, physicians were asked about intention to use the described vaccine if recommended for permissive or routine use by the ACIP.
Survey Administration
When recruited for the sentinel network, physicians were asked whether they preferred to be surveyed by Internet or mail. All 280 physicians who preferred responding by Internet or did not have a preference were surveyed via the Internet; the remaining 151 physicians were surveyed by mail.
Internet
The Internet survey was administered through a Web-based survey company (Websurveyor Corp, Herndon, VA). After sending a presurvey e-mail introducing the survey topic, the Internet group was sent an email containing a link to the Web-based survey. Nonrespondents were sent up to 8 additional e-mail reminders over a 6-week period.
Physicians in the mail group were first sent a presurvey letter introducing the survey topic. A self-administered survey was then sent to all physicians in this group, with a reminder postcard sent 5 days later. Nonrespondents were sent up to 2 additional surveys at ∼2-week intervals, and responses were allowed for 8 weeks after the first survey was mailed.
Analytic Methods
Items regarding physician knowledge and attitudes about rotavirus and the vaccine, their intention to use the vaccine, and potential barriers to using the vaccine were asked using 4-point Likert scales. Responses on the negative side of the scale (eg, “somewhat disagree” and “strongly disagree”) were grouped for all survey questions, because there were relatively few negative responses. Items regarding physician reasons for delaying using the vaccine were dichotomous with physicians being asked to agree or disagree with each response. For bivariate and multivariate analyses, the primary outcome was treated as a dichotomous variable (would strongly recommend rotavirus vaccine versus all other responses). Independent variables pertaining to categorical data in the model were also treated as dichotomous (“strongly agree” or “definitely a barrier” vs all other responses) for analysis on the basis of the distribution of the responses. There were large percentages of “somewhat agree” or “somewhat of a barrier” responses, and in our predictive model we wanted to clearly identify more strongly held perception of burden and barriers. Bivariate analyses were performed to determine the association between the outcome variable and physician characteristics, knowledge, beliefs, and barriers that we hypothesized would affect vaccine adoption. Factors significant at P < .25 in bivariate analyses were tested in multivariate models by using a backward elimination procedure in which the least significant predictor in the model was eliminated sequentially. At each step, estimates were checked to make sure other variables were not largely affected by dropping the least significant variable. This resulted in the retention of only those factors that were significant at P < .05 in the final model. All statistical analyses were performed by using SAS software (SAS 9.1, SAS Institute, Cary, NC).
RESULTS
Of the 431 sentinel physicians, 151 (35%) received the survey by mail and 280 (65%) by e-mail. A total of 305 completed the survey, yielding an overall response rate of 71% (74% for mail and 69% for e-mail respondents). Respondents were similar to nonrespondents with regard to physician age or gender, practice setting, practice location, or region of the country (Table 1). Table 1 also shows additional characteristics of the respondents in terms of insurance status and race/ethnicity of their patient population and whether they participated in the Vaccines for Children (VFC) program.
Comparison of Survey Respondents and Nonrespondents and Additional Characteristics of Respondents’ Practices
Burden of Rotavirus Disease and the Need for a Vaccine
Most physicians were aware of the burden of rotavirus infection in the United States and the greater burden of this disease in developing countries (Table 2). Fifty-one percent of physicians strongly agreed that the burden of rotavirus disease was sufficient in the United States to justify the need for a rotavirus vaccine, and 83% agreed that the burden of rotavirus disease in developing countries was sufficient to justify the need for a rotavirus vaccine globally. Only 10% somewhat or strongly disagreed with the need for a vaccine in the United States. This subgroup of providers was less likely to have administered RotaShield routinely before its withdrawal than were other providers (32% vs 54%; P = .02). Those who disagreed with the need for a vaccine were also significantly more likely than other physicians to perceive a variety of factors as definite barriers to adoption of rotavirus vaccine including the “up-front” costs of purchasing vaccine, their concerns about the safety of rotavirus vaccine, parental concerns about vaccine safety in general, parents not thinking rotavirus vaccine is necessary, concerns about overloading the vaccine schedule, and their own belief that rotavirus was not a severe disease that required vaccination (P < .01 for all comparisons; data not shown).
Perceived Burden of Rotavirus (N = 305)
Previous Experience with RotaShield
All physicians surveyed were aware of the problems associated with RotaShield and its subsequent withdrawal from the market. Before its withdrawal, 52% reported they routinely administered the vaccine, 9% administered the vaccine but not routinely, and 39% did not administer the vaccine. Twelve percent of respondents were aware of patients in their practice or in other practices in their community who developed intussusception possibly associated with RotaShield administration. Half of respondents said they would routinely discuss the association of the previously licensed rotavirus vaccine and intussusception when introducing the new rotavirus vaccine to parents, whereas 34% would only discuss it if the parents brought it up, 6% would not discuss it, and 11% were unsure. Those who reported they would routinely discuss the previous vaccine were more often male than were those who would not routinely discuss it (62% vs 47%; P = .01). In addition, this subgroup were less likely to have confidence in prelicensure studies in determining vaccine safety and were more likely to perceive parental reluctance regarding vaccination because of withdrawal of the previous rotavirus vaccine and their own concerns about the safety of rotavirus vaccine as definite barriers to adoption of rotavirus vaccine (P < .01 for all comparisons; data not shown).
Intentions for Recommending the New Rotavirus Vaccine
The percentage of respondents who intended to recommend the vaccine was much higher if the ACIP made a recommendation for routine vaccination than if it made a recommendation for permissive vaccination (Fig 1). Permissive vaccine use was defined in the survey as a vaccine available for use by individual clinicians “at their discretion.” On the basis of a recommendation for routine use, 50% would strongly recommend and 34% would recommend but not strongly. If recommended for routine use, 52% reported they would begin to use the vaccine within 6 months, 27% from 6 months to 1 year, 7% from 1 to 2 years, 1% > 2 years, 0.3% would never recommend, and 13% were unsure. For physicians who would wait >6 months before using the vaccine (n = 143), the most common reasons included waiting for insurers to cover vaccine and waiting to see whether adverse effects were present (Fig 2).
Intentions for recommending new rotavirus vaccine if recommended by ACIP/AAP for routine versus permissive use (n = 305).
Reasons for waiting to use rotavirus vaccine among those who would wait >6 months to use vaccine (n = 143).
Perceived Barriers to Implementation of New Rotavirus Vaccine Recommendations
As shown in Table 3, the most commonly perceived barriers to implementation were physician concerns about uneven coverage of the vaccine by insurers (definitely or somewhat of a barrier for 81%), lack of adequate reimbursement for the vaccine (definitely or somewhat of a barrier for 75%), and parents’ reluctance to have their child vaccinated because of withdrawal of the previous rotavirus vaccine (definitely or somewhat of a barrier for 68%).
Perceived Barriers to Giving Rotavirus Vaccine (N = 305)
Factors Associated With Vaccine Adoption
The final multivariate model predicting physicians’ intentions to strongly recommend rotavirus vaccine included only 4 variables, all significant at P < .05 and no confounding between variables was observed. (Table 4) Significant factors positively associated with our major outcome in both bivariate and multivariate analyses included the perception that rotavirus is a common and potentially severe infection in the United States and having a great deal of confidence in prelicensure studies in determining vaccine safety. Factors that were negatively associated included physician concerns about safety of the rotavirus vaccine and parent concerns about vaccine safety in general.
Bivariate and Multivariate Analyses of Factors Significantly Associated With Being Very Likely to Recommend Rotavirus Vaccine Versus All Others (N = 299)
DISCUSSION
The recent licensure of a new efficacious rotavirus vaccine and a recommendation for routine vaccination of US infants by ACIP has renewed hopes that morbidity and mortality from rotavirus can be dramatically reduced both in this country and in developing countries. The findings of this nationally representative survey demonstrate that pediatricians recognize the burden of rotavirus disease and the value of a rotavirus vaccine for children in this country. In addition, despite universal awareness of the safety issues with the previous rotavirus vaccine, the majority of pediatricians report that they will either strongly recommend or recommend this new vaccine on the basis of its safety and efficacy profile, and about half would use it within the first 6 months after recommendations are issued. In addition, our data indicate that ACIP’s recent decision to recommend the vaccine for routine rather than permissive use will result in higher percentages of pediatricians making a strong rather than a more neutral recommendation for vaccination to parents. Reported barriers to the new vaccine were similar to those reported for other new vaccines, with reimbursement issues being predominant. As expected, concerns about parental reluctance because of previous withdrawal of RotaShield and physician concerns about safety of the vaccine were also in the top 5 most commonly cited barriers to implementation.
Only 2 previous publications have assessed pediatricians’ willingness to adopt a new rotavirus vaccine after RotaShield’s withdrawal from the market. Both presented information about a hypothetical vaccine, because they predated the clinical trials of the 2 new vaccines. The first included survey data from pediatricians in 2 states in 2001 and demonstrated a high level of willingness to use a new rotavirus vaccine if it were safer than RotaShield and were recommended by the AAP and ACIP.22 The second study,23 reporting survey results of pediatricians and family medicine physicians about a hypothetical rotavirus vaccine, also suggested a majority of pediatricians would adopt a new vaccine if certain safety and efficacy criteria were met, the vaccine was covered by most insurance plans, and it was recommended for routine use by the AAP and ACIP. Results from this study must be interpreted with caution, however, because the response rate to the survey was <5% of those contacted.
There has been substantial concern about whether the withdrawal of the previous rotavirus vaccine would heighten safety concerns on the part of providers and parents, thus affecting adoption of a new rotavirus vaccine. Indeed, our data demonstrate that ∼70% of pediatricians think that parental reluctance because of withdrawal of RotaShield will be somewhat or definitely a barrier to vaccination. Slightly less than half of pediatricians themselves express concerns about the vaccine’s safety as definitely or somewhat of a barrier to implementation. Concerns about safety on the part of physicians as well as their perception of vaccine safety concerns on the part of parents predicted lower rates of adoption, whereas a higher level of confidence in prelicensure studies assessing vaccine safety predicted higher rates of adoption. Interestingly, half of the respondents said they would routinely discuss the previous rotavirus vaccine with parents of infants for whom the vaccination is recommended. However, the time it would take to discuss rotavirus vaccine safety was an anticipated barrier to use for <15% of providers. How much of a time burden routinely discussing the previous rotavirus vaccine would be will depend on a number of factors that are currently unknown, most importantly the proportion of parents with infants <6 months of age that will be aware of the withdrawal of the first rotavirus vaccine and to what extent safety concerns will deter them from vaccinating their children. The Vaccine Information Sheet (VIS) that must routinely be given to parents before any vaccination is currently available for this vaccine.24 It briefly discusses the association of the previous vaccine with intussusception and the fact that no such association has been found with RotaTeq in trials with over 70000 children. Hopefully, inclusion of this information will be helpful in alleviating concerns of parents who were already aware of problems associated with RotaShield and in shortening providers’ time spent discussing safety issues. Inclusion of this information, however, may not be welcomed by the portion of pediatricians who feel that introduction of the new vaccine should not be linked to the previous one.
Other anticipated barriers to the implementation of rotavirus vaccination mirror those experienced for other new vaccines, with reimbursement concerns topping the list. Vaccine expenditures have increased dramatically in the past decade as a result of new vaccines with relatively higher prices.25 The financial issues that arose over introduction of the heptavalent pneumococcal conjugate vaccine (PCV7; Prevnar, Wyeth, Madison, NJ) may foreshadow what primary care physicians will encounter with implementation of rotavirus and other new vaccines. The addition of PCV7 almost doubled the overall cost of all recommended childhood vaccines through 6 years of age.26 Although uptake of PCV7 was high in the year after introduction, in a national survey of family medicine and pediatric physicians, approximately one-third reported that the cost of PCV7 influenced their purchase and administration of the vaccine and changed their practices regarding screening children for insurance coverage in general.25 Some providers were also more likely to refer children without insurance coverage for PCV7 to a public health clinic, whereas they were more likely to vaccinate children with coverage for the vaccine in their office, creating a 2-tiered system of delivery for this vaccine.25 Because providers receive vaccine from the VFC program for their publicly insured and uninsured patients and from a distributor or manufacturer for privately insured patients, imbalances in the timing of coverage in these 2 sectors can create problems for physicians who are committed to delivering uniform care to all of their patients. For PCV7, differences in the timing of availability of vaccine from the VFC program and in the timing of coverage by private-sector managed care and insurance plans created an ethical dilemma for physicians who had to decide whether to withhold vaccine from some patients while giving to others, to vaccinate all patients without certainty of reimbursement or to delay implementing the vaccine until there was more uniform coverage.27
Many of these same issues are likely to impact the implementation of rotavirus recommendations. RotaTeq is currently priced at $63.25 if purchased in the private sector and $52.00 if purchased by the VFC program, similar to the costs of PCV7.26 As our data demonstrate, pediatricians are concerned about the issues of uneven coverage of the vaccine by insurance companies, lack of adequate reimbursement to their practice for vaccination, and the enormous “up-front” costs of buying the vaccine without certainty of reimbursement in the first years after recommendation of this new vaccine. After recommendation of a new vaccine, there are delays in being able to bill for the vaccine from private health plans, and practices have to “carry” the costs of buying and administering the vaccine, sometimes for prolonged periods of time.28 In addition, previous studies have shown that for the practitioner to recover the full costs of buying and administering vaccine, they need to be paid by the health plans approximately 120% to 130% of what they initially paid to purchase vaccine.29 As an illustration, a recent study in Colorado found that the average nonvaccine cost per shot was $10.67, whereas the average reimbursement by insurers was $8.27.30 Interestingly, although the financial issues were raised as major barriers in the present study, they were not predictive of willingness to strongly recommend the vaccine in multivariate modeling. Despite the challenges of a 2-tiered system of delivery, participation in the VFC program was also not related to plans to adopt the vaccine. Waiting to see whether insurers would cover the vaccine was, however, the major reason given for delaying implementation for >6 months.
Potential difficulty in obtaining adequate vaccine supplies was also a barrier reported by about half of pediatricians surveyed, also echoing what pediatricians faced with implementation of PCV7.31 RotaTeq, like 7 other childhood vaccines currently on the routine schedule, is produced by a single company,32 making it particularly vulnerable to production problems. In addition, supplies may be inadequate because of inaccurate estimates of projected uptake by providers or market forces that may not be aligned with maximizing implementation of the vaccine.33 After their experiences with shortages with PCV7, providers are concerned about having adequate and stable supplies of a new vaccine in both the private and public sectors before they begin implementation.
Because our survey was conducted before ACIP issued its recommendations, a potential implementation challenge that we did not specifically address is the confusion practitioners may face in complying with the fairly strict age criteria for vaccine use. The large clinical trial establishing safety of this vaccine used the 6- to 12-week window as the time for receipt of the first dose because these infants have a lower background rate of intussusception than older infants, permitting more rapid detection of any signal intussusception related to vaccine.34 Given the previous history of the first rotavirus vaccine, ACIP chose to have the age criteria in the recommendations strictly adhere to the conditions of the clinical trial. It is likely that many questions will arise about whether an infant who presents after 12 weeks can receive the vaccine if it is requested and what should occur if all doses of the vaccine are not administered by 32 weeks of age. Given the percentage of infants who are delayed in receiving immunizations,35,36 this latter situation may arise fairly frequently, and primary care physicians caring for children will need guidance about the best course of action.
This study has some important strengths and limitations. The surveyed physicians are representative of pediatricians in the AAP nationally with respect to demographic and practice characteristics and location throughout the United States. The response rate for the survey was also high. Despite the sample seeming representative, however, those who agreed to be surveyed may not express similar views as those who chose not to be surveyed or did not respond to this survey. In addition, respondents in this survey reported anticipated actions and these might differ from what they actually choose to do.
CONCLUSIONS
The benefits of new rotavirus vaccines, if widely implemented, will be substantial in the United States, and could be much more profound in developing countries.1,37–40 Our data suggest that the majority of pediatricians in this country will be willing to implement RotaTeq, most within 6 months of recommendations, despite their experience with the previous rotavirus vaccine and continued concerns about safety. Implementation in this country will be greatly facilitated if lessons learned from the implementation of other recent new vaccines such as PCV7 are heeded. Some of the problems faced by pediatricians in the initial stages of implementation, including substantial delays in being able to bill for vaccines to insurers who have not yet changed their billing procedures to accommodate a new vaccine and unsynchronized timing of coverage between the public and private sectors, might well be ameliorated by increased coordination between ACIP, vaccine manufacturers, and health plans before recommendation of a new vaccine. Answers to other problems such as inadequate reimbursement for vaccines and problems with vaccine supplies and distribution are complex and may require substantial structural changes in our vaccine financing system over time.32 Despite the recognized challenges that pediatricians will face in implementing the new rotavirus vaccine, the results of this survey indicate that they are eager to help realize the promise of this vaccine.
Acknowledgments
This investigation was funded by Centers for Disease Control and Prevention grant SIP 5 U48 DP000054-03. This funding was obtained and administered through the Rocky Mountain Prevention Research Center, University of Colorado at Denver and Health Sciences Center, Denver, Colorado.
We thank Lynn M. Olson, PhD, and Karen O’Connor of the AAP for assistance in establishing the pediatric sentinel physician network.
Footnotes
- Accepted September 14, 2006.
- Address correspondence to Allison Kempe, MD, MPH, 1056 E 19th Ave, B032, Denver, CO 80218. E-mail: kempe.allison{at}tchden.org
The authors have indicated they have no financial relationships relevant to this article to disclose.
Portions of this work were presented at the Advisory Council on Immunization Practices; February 21, 2006; Atlanta, GA.
Dr Kempe had full access to all of the data in this study and takes responsibility for the integrity of the data and the accuracy of the data analysis.
The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention, US Department of Health and Human Services.
REFERENCES
- Copyright © 2007 by the American Academy of Pediatrics
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