PEDIATRICS Vol. 122 No. 1 July 2008, pp. e33-e38 (doi:10.1542/peds.2007-2464)
ARTICLE |
Implementation of Rotavirus Immunization in Philadelphia, Pennsylvania: High Levels of Vaccine Ineligibility and Off-Label Use
a Section of Infectious Diseases, St Christopher's Hospital for Children, Philadelphia, Pennsylvania
b Department of Pediatrics, Drexel University College of Medicine, Philadelphia, Pennsylvania
c Division of Disease Control, Philadelphia Department of Public Health, Philadelphia, Pennsylvania
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ABSTRACT |
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 TOP ABSTRACT PATIENTS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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OBJECTIVE. Our goal was to predict, using delayed diphtheria-tetanus-acellular pertussis vaccination as an indicator, whether the current narrowly defined age limits for pentavalent rotavirus vaccine exclude a substantial proportion of children from complete immunization against rotavirus and to assess adherence of providers to recommended age limits by examining the first 6 months of use of pentavalent rotavirus vaccine in Philadelphia, Pennsylvania.
PATIENTS AND METHODS. Data from a computerized children's immunization registry in Philadelphia were analyzed. Demographics and age at immunization with first 3 diphtheria-tetanus-acellular pertussis doses were examined from 2001 to 2005. Similar characteristics were evaluated for children who received pentavalent rotavirus vaccine doses during the first 6 months of its availability (August 2006 through January 2007).
RESULTS. During the 5-year period, 24 403 of 103 967 recipients of first diphtheria-tetanus-acellular pertussis vaccine were >12 weeks of age; only 56 411 of 79 564 first diphtheria-tetanus-acellular pertussis recipients 
12 weeks of age received the first 3 doses at ages that they could have completed the pentavalent rotavirus vaccine series if vaccines were given at the same visit. Children using public providers were more likely to have delayed immunization. During the first 6 months of pentavalent rotavirus vaccine implementation, 5566 pentavalent rotavirus vaccine doses were recorded in the Kids Immunization Database/Tracking System: 3912 first doses, 1419 second doses, and 235 third doses. Of 3912 first-dose pentavalent rotavirus vaccine recipients, 770 were >12 weeks of age. Hospital-based providers were less likely to administer pentavalent rotavirus vaccine off-label.
CONCLUSIONS. With the current level of vaccine implementation and current pentavalent rotavirus vaccine recommendations for series initiation, a substantial proportion of children are expected to be excluded from receiving any pentavalent rotavirus vaccine or completing the series. In the first 6 months of availability, pentavalent rotavirus vaccine frequently was used off-label for age, underscoring the importance of education of immunization providers. Current outreach programs for finding 10-month-old toddlers delinquent for immunizations will not improve the possibility of protection against rotavirus.
Key Words: immunization • timeliness • rotavirus • off-label
Abbreviations: PRV—pentavalent rotavirus vaccine • KIDS—Kids Immunization Database/Tracking System • DTaP—diphtheria-tetanus-acellular pertussis
Until recently, rotavirus infection has been an inescapable part of childhood that results in high morbidity, mortality, and costs.1,2 The first licensed rotavirus vaccine (RotaShield [Wyeth Laboratories, Marietta, PA]) was withdrawn from the market after just 1 year of general use because of its association with intussusception.3–5 The risk for intussusception was found to increase 3 to 14 days after the first dose of RotaShield, and a smaller increase was detected during the same period after the second dose.5 As summarized by Rothman et al,6 the attributable risk for intussusception after RotaShield seemed to increase with age at first dose. In February 2006, the US Food and Drug Administration licensed a new bovine-based pentavalent rotavirus vaccine (PRV) (RotaTeq (Merck & Co Inc, Whitehouse Station, NJ). Because of the history of the previous vaccine, prelicensure safety studies of PRV involved >77 000 children in several countries and were conducted following narrowly defined age limits for initiation and completion of the 3-dose vaccine series.7 Licensure by the Food and Drug Administration, recommendations for the use of PRV by the Centers for Disease Control and Prevention Advisory Committee on Immunization Practices,2 and a policy statement by the American Academy of Pediatrics8 all mirror the strictly defined age limits of prelicensure safety trials: age <12 weeks 0 days for series initiation and 32 weeks 0 days for series completion.
We hypothesized that a proportion of children in Philadelphia, Pennsylvania, have delayed immunizations during infancy and will be affected by the current age limits for PRV series initiation and completion. We sought to predict what proportion of children in Philadelphia could be ineligible for the PRV series on the basis of their age at presentation for standard immunizations in infancy and to examine whether and to what extent PRV was used outside the recommended age limits (off-label) during the first 6 months of its implementation in Philadelphia.
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PATIENTS AND METHODS |
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TOPABSTRACTPATIENTS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Immunization Tracking in Philadelphia
The Philadelphia Department of Public Health, through its Division of Disease Control, maintains an immunization information system, the Kids Immunization Database/Tracking System (KIDS). The system captures data on immunizations given to all city residents who are <6 years old, consolidates information on immunizations received by multiple providers into a central registry, and facilitates community outreach initiatives in an effort to increase immunization up-to-date rates. All analyses were restricted to children who received at least 1 reported immunization in Philadelphia and excluded the records of children who moved outside of Philadelphia, were lost to follow-up by their provider, or died during the study period.
Estimation of Rotavirus Vaccine Ineligibility
The immunization records of children who were born and living in Philadelphia from January 2001 to December 2005 (before availability of the PRV) were analyzed. Immunization with the first, second, and third doses of the DTaP (pediatric formulation of diphtheria and tetanus toxoids and acellular pertussis antigens) vaccine or DTaP-containing vaccines was used as an indicator for opportunity to administer the PRV. Age and demographic features at immunization with DTaP were examined considering the age limits of PRV: for the first dose, age 12 weeks 0 days; for the second dose, age 28 weeks 0 days (allowing for the possibility for the completion of the PRV series if the minimal dose interval of 4 weeks is observed); and for the third dose, age 32 weeks 0 days.
Rotavirus Vaccine Off-Label Use
PRV was available to providers in Philadelphia through the Vaccines for Children program in early August 2006. The immunization records of children from the first 6 months of the implementation of PRV (August 1, 2006, to January 31, 2007) in Philadelphia were analyzed. We examined the age at immunization with the first, second, and third dose of PRV, demographic features of the recipients, and receipt of DTaP vaccine during the same visit.
Categorization of Immunization Providers
To examine trends of late-infancy immunization and of PRV off-label use according to the type of primary care provider, we classified the immunization providers in 3 main categories: public, private, and hospital. All federally qualified health centers and a number of smaller public clinics in the city were classified as public; all practices of pediatricians and family physicians were classified as private; and the hospital-owned clinics in which care was provided by resident physicians-in-training (under faculty supervision) or by faculty were classified as hospitals. Doses of DTaP that were administered in outbreak settings (following the Division of Disease Control practice of administering all age-appropriate immunizations to children managed during an outbreak) were excluded from the provider analysis.
Statistical Analysis
We used the 
2 test to assess associations between categorical variables. Exact binomial 95% confidence intervals were generated to compare proportions of ineligibility or off-label use across strata.9 All analyses were conducted in SAS 9.1.3 (SAS Institute, Cary, NC).
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RESULTS |
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TOPABSTRACTPATIENTS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Rotavirus Vaccine Ineligibility
During the 5-year study period, 103 967 recipients of the first dose of DTaP were identified; 24 403 (23%) would have been ineligible for the first dose of PRV because of their age at immunization. Of the remaining 79 564 (77%) first DTaP recipients
12 weeks of age, 1575 (2%) did not have a second DTaP dose recorded in the registry, and 4654 (6%) received their second DTaP dose at >28 weeks of age. If the second dose of PRV had been administered at the same visit as the delayed (>28-week) DTaP, these children would have been ineligible for completion of the PRV series with a third PRV dose, assuming that the minimal dose interval (4 weeks) would have been observed. Similarly, of the 73 335 recipients of the second DTaP dose who would have been eligible for completion of the PRV series, 1816 (2%) did not have a third dose of DTaP recorded in the registry, and 15 108 (21%) received their third DTaP dose at >32 weeks of age and, thus, would have been ineligible for the third dose of PRV and completion of the series. The percentage of children who would have been ineligible for PRV series initiation or completion on the basis of the pattern of DTaP administration decreased between 2001 and 2005 (Table 1).
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A total of 292 467 DTaP doses were administered during the 5-year study period: 139 579 by private providers, 85 841 by hospital-based providers, and 36 901 by public providers. For 29 123 doses, the provider was unknown. In addition, 1023 doses were administered in outbreak settings and were excluded from the provider analysis. Children who received immunizations from public providers were more likely to have late receipt (considering the PRV age limits) of any DTaP dose than the DTaP recipients in private and hospital-based settings (P < .001; Fig 1). The proportion of DTaP recipients who received a DTaP dose at an age older than the PRV age limits decreased every year for each provider category.
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Rotavirus Vaccine Off-Label Use
During the first 6 months of the implementation of PRV in Philadelphia, 110 immunization-provider sites ordered PRV through the Vaccines for Children program; 17 443 PRV doses were distributed, and 5566 PRV administrations were recorded in the registry. Of 5566 doses, 3912 were administered as first doses, 1419 as second doses, and 235 as third doses. For 3912 first doses, 770 (19.7%) were given to children >12 weeks of age (off-label). Of the 1419 second PRV doses, 14 (9.7%) were given to children >32 weeks of age (off-label), and of the 235 third PRV doses, 9 (3.8%) were given to children >32 weeks of age (off-label). All off-label third-dose PRV recipients had received their second dose before 32 weeks of age (on-label). The age distribution of the first-dose PRV off-label recipients is shown in Fig 2. The median age of the children who received first-dose PRV off-label was 18 weeks (range: 85 days to 46 weeks). Of 336 children who received first-dose PRV between 121 and 150 days of age (Fig 2), 256 (76%) received their second dose of DTaP at the same visit, and of 103 first-dose PRV recipients >180 days old, 70 (68%) received their third dose of DTaP concurrently.
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Of 3912 first-dose PRV recipients, 2047 (52.3%) received PRV by hospital-based providers, 1319 (33.7%) by private providers, and 532 (13.6%) by public providers; in 14 cases (0.4%), the provider was unknown. Hospital-based providers were less likely than other types of providers to administer PRV off-label (P < .01; Fig 3).
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DISCUSSION |
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TOPABSTRACTPATIENTS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Although the proportion of children who receive the required number of immunizations by 19 to 35 months of age has increased in the United States over the last 5 years,10 a dwindling proportion of children receive all immunizations at the actual recommended ages (ie, on time).11–15 Underimmunization in the first years of life has led to outbreaks of highly transmissible imported diseases such as measles,16 exposure of vulnerable populations to diseases such as pertussis as a result of lack of herd immunity,17 and increased mortality and morbidity rates resulting from diseases such as invasive Haemophilus influenzae infection.18 Consequently, timeliness of immunizations is recognized as a factor with growing importance in the improvement of vaccine implementation.
In view of the novel narrowly defined age limits for the PRV, timeliness of immunizations is a pressing priority. The preclusion of infants >12 weeks of age from initiation of a vaccine series is unprecedented and represents a new challenge for pediatricians. It is possible in the future that experience of field use of PRV in large birth cohorts would provide us with adequate safety data to allow revision of the current narrowly defined age limits. However, in light of the existing recommendations,2,8 our study showed a predicted exclusion rate of 23% for initiation of the PRV series on the basis of the timing of the first DTaP dose. Although in a larger study based on the National Immunization Survey the percentage of delayed first-dose DTaP recipients (administration by 3 months [ie, 13 weeks of age]) was lower (10%),15 our finding is consistent with other studies in urban settings with large minority populations that have shown delay of first immunizations in 18% to 30% of children.19,20
We found that public health care facilities had the highest proportion of children who initiate DTaP vaccination too late to be eligible for simultaneous PRV administration. Other studies have identified similar receipt of care in public primary care facilities as a risk factor for late initiation of immunization or for delay in age-appropriate immunization.19,21,22 Factors identified as associated more with public primary care providers are high levels of missed appointments, missed opportunities, and failure to immunize as a result of invalid contraindications.21 The fact that in Philadelphia (the fifth largest metropolitan area in the United States) >80% of children are eligible for Medicaid or are self-insured, 30% live below the poverty level,23 and our finding that infants receive 42% of their primary health care in public and hospital-based clinics illustrate that risk factors already associated with the absence of age-appropriate immunization were present in our population as well. The type of insurance coverage, Medicaid enrollment, and the lack of standard primary care provider are also well-documented risk factors for underimmunization.12,19,20,24 In a recent study of a Philadelphia primary care network, it was reported that children with Medicaid or no insurance were more likely to have delay of immunizations at 24 months of age; the most reliable predictor of delayed immunizations at 24 months was delay at 3 months of age.20
Although only 17% of rotavirus-associated hospitalizations occur before 6 months of age,2,25 Fischer et al26 have reported that black and Hispanic children have been hospitalized for rotavirus at a younger age than white children, with a substantial proportion of hospitalizations occurring by 6 months of age and a higher case fatality rate among those in the minority group. Furthermore, patients covered by Medicare and Medicaid were hospitalized for rotavirus at a younger age and had significantly longer hospital stays than those with commercial insurance.26,27 With 98% efficacy of PRV against rotavirus-associated severe disease and hospitalization,7 timely immunization against rotavirus is necessary for eliminating socioeconomic disparities in health care.
The substantial off-label use of PRV during the first 6 months of its availability and implementation in Philadelphia is remarkable. We speculate that the availability date of the vaccine for use (August 2006) a few months before the publication of guidelines by the recommending bodies,2,8 in conjunction with the uniquely narrow age limits of the PRV, may partially explain this phenomenon. The recommended age limits for PRV are novel in at least 2 aspects. First, few vaccines have an upper age limit for their initiation, and in the case of PRV, the upper limit (12 weeks) for initiation falls even earlier than the "on-time" benchmark for regular infancy immunizations such as DTaP (3 months [ie, 13 weeks]). Second, PRV is the only vaccine with age limits for recommended use counted in weeks. If this had been the primary source of confusion, however, one would expect that most of the off-label use would have occurred between the 12th and 13th week of age. Most off-label use of the first PRV dose occurred at the age of >4 months (Fig 2), usually concurrently with a DTaP dose (generally not the first DTaP dose), which suggests a lack of knowledge about the guidelines for use of PRV by the providers. It is possible that unavailability of PRV in some practices during the early days of its implementation in Philadelphia was responsible for a proportion of the off-label use, and this fraction of the off-label use could presumably disappear with unimpeded availability of PRV in the future. Because all Philadelphia hospital clinics are part of academic centers, it is likely that education and awareness of restrictions early in the implementation of PRV explain the lesser amount of off-label use found for the hospital-based providers. In contrast to our finding that most DTaP doses were administered in private settings, the majority of PRV doses were given by hospital-based providers, which underscores the important role that academic centers can play in the implementation of new vaccines in the community.
In our population there was no case of intussusception associated with the PRV. On the basis of a study that used the Healthcare Cost and Utilization Project's state inpatient database, the background rate for intussusception is very low for infants <9 weeks of age but increase rapidly thereafter, peaking at 26 to 29 weeks of age.28 In the case of RotaShield, it was believed that "catch-up" vaccination of older infants could have been a major contributor to its association with intussusception.29 Accordingly, the use especially of the first PRV dose off-label could lead to confusion because of the increased chance of temporal association with intussusception and a potentially unwarranted conclusion of PRV causation.
There are several limitations to this study. The study was based on the KIDS registry, which is subject to the universal registry restrictions of completeness and accuracy. The registry is thought to represent >95% of Philadelphia's children <6 years of age,30 but the inputting of data relies on the immunization providers' reporting, and the most effective and accurate method (ie, the direct entry of electronic data at the immunization episode) is performed by only a fraction of providers.31 Accordingly, in our PRV exclusion estimates, we did not include children who had missing records for the second and third doses of DTaP, because the possibility exists that some of these children received doses that were not recorded in the registry. Our study involved children from only 1 metropolitan area in the United States. Despite the fact that urban populations share characteristics associated with implementation of immunizations, the results may not represent all inner-city populations.
The high levels of PRV ineligibility have several associated public health implications. A substantial number of children can be excluded from adequate protection against rotavirus, and others (of high and low risk for complications from rotavirus infection) could be precluded from the benefit of herd effect. To increase protection against rotavirus, providers should aim to improve the timeliness of immunizations in early infancy. The existing outreach initiatives are triggered at 10 months of age. Their effectiveness in increasing immunization rates has been demonstrated in an intervention-control study. Children in the outreach group were 2.5 times as likely to have received an immunization as children in the control group.32 To have any impact on PRV immunization, however, the target age for assessment and outreach must be <3 months of age, and intervention must be rapid. Some data from the Philadelphia population suggest that initiatives for addressing delayed immunization should start at the birth hospital, because maternal factors such as absent or insufficient prenatal care are strong predictors of time to first immunization33 and outreach initiatives have been proven to be ineffective for children of mothers who received inadequate prenatal care.32
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CONCLUSIONS |
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TOPABSTRACTPATIENTS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Continuous performance-improvement initiatives through community outreach and enhanced education of immunization providers can assist in eliminating or decreasing the incidence of vaccine-preventable diseases, with direct impact on the health of children and the population.
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ACKNOWLEDGMENTS |
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We thank Brian Jorgage, MS, for assistance with data extraction from the KIDS registry.
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FOOTNOTES |
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Accepted Jan 4, 2008.
Address correspondence to Irini Daskalaki, MD, St Christopher's Hospital for Children, Department of Pediatrics, Erie Avenue at Front Street, Philadelphia, PA 19134. E-mail: irini.daskalaki{at}drexelmed.edu
Financial Disclosure: Dr Watson serves on advisory boards at Merck & Co and GlaxoSmithKline; the other authors have indicated they have no financial relationships relevant to this article to disclose.
| What's Known on This Subject Timeliness of immunization has been recognized as an important factor in the prevention of infectious diseases. The new rotavirus vaccine has been licensed for use within narrow age limits because of the association of a previous rotavirus vaccine with intussusception.
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| What This Study Adds Time at vaccination with DTaP was used as an indicator to predict the rate of infants excluded from rotavirus immunization. Our study examined the first 6 months of implementation of the new rotavirus vaccine in a large metropolitan area.
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