Published online October 2, 2006
PEDIATRICS Vol. 118 No. 4 October 2006, pp. 1394-1402 (doi:10.1542/peds.2006-0314)
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ARTICLE

The Impact of Conjugate Pneumococcal Vaccination on Routine Childhood Vaccination and Primary Care Use in 2 Counties

Peter G. Szilagyi, MD, MPHa, Marie R. Griffin, MD, MPHb,c, Laura P. Shone, DrPH, MSWa, Richard Bartha, Yuwei Zhu, MD, MSd, Stanley Schaffer, MD, MSa, Sandra Ambrose, MBAa, Jason Roy, PhDa, Katherine A. Poehling, MD, MPHb,e, Kathryn M. Edwards, MDe, Frances J. Walker, MSPHf, Benjamin Schwartz, MDf for the New Vaccine Surveillance Network

a Department of Pediatrics, Strong Children's Research Center, University of Rochester School of Medicine and Dentistry, Rochester, New York
b Departments of Preventive Medicine
c Medicine
d Biostatistics
e Pediatrics, Vanderbilt University Medical Center, Nashville, Tennessee
f National Immunization Program, Centers for Disease Control and Prevention, Atlanta, Georgia


    ABSTRACT
 TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
BACKGROUND. Pneumococcal conjugate vaccine immunization recommendations were rapidly implemented by primary care providers. Before the recommendations, concern was expressed that adding pneumococcal conjugate vaccine might result in delays in other vaccinations or preventive services.

OBJECTIVES. The study objectives were to measure whether incorporation of pneumococcal conjugate vaccine by primary care providers delayed other vaccinations or added primary health care visits.

DESIGN AND METHODS. In 2 counties surrounding Rochester and Nashville, we reviewed a representative sample of primary care charts for children born before and after licensure of pneumococcal conjugate vaccine. Receipt of vaccinations and health care visits were compared for the 2 age-matched cohorts.

RESULTS. We reviewed 1459 records from Rochester and 1857 records from Nashville. The pre–pneumococcal conjugate vaccine and post–pneumococcal conjugate vaccine cohorts had similar demographic characteristics. The median age for receipt of any vaccination was not older for the postvaccine cohort than for the prevaccine cohort in either community. The percentage of children up-to-date for vaccinations by 18 months for postvaccine versus prevaccine cohorts was similar in Rochester (72% in each cohort) and in Nashville (58% postvaccine and 65% prevaccine). The number of well-child care visits or other health care visits during the first 18 months of life was not statistically different between the 2 cohorts.

CONCLUSIONS. Implementation of pneumococcal conjugate vaccine was not associated with delays in other childhood vaccinations or more primary care visits.


Key Words: conjugate pneumococcal vaccination • PCV7 • vaccination practices

Abbreviations: PCV7—pneumococcal conjugate vaccine • WCC—well-child care

The pace of new national recommendations for childhood vaccinations has accelerated over the past 2 decades, with revised recommendations for established vaccines, such as polio,1 influenza,2,3 and measles-mumps-rubella,4 and for newly licensed vaccines, such as hepatitis B,5,6 varicella,7 rotavirus, 8,9 pneumococcal conjugate vaccine (PCV7),10 meningococcal conjugate,11 and acellular pertussis vaccine.12 New childhood vaccinations will continue to appear in the future, with new recommendations for hepatitis A13 and influenza vaccines14 and likely licensure of a new rotavirus vaccine,15 human papillomavirus vaccine,16 and several other vaccines for children and adolescents.1720

Most childhood vaccinations are administered in primary care offices,21,22 which also provide comprehensive preventive, acute, and chronic care to children.23 Alongside new vaccination recommendations, primary care providers are continually faced with revised guidelines for delivery of preventive services,2426 an increasing burden of chronic disease,27,28 and a high demand for acute services.29

Most studies focus on the impact of new vaccinations on either vaccination coverage or on the reduction in disease after vaccination implementation,3037 yet new vaccination policies have the potential to influence other aspects of primary care in both positive and negative ways. For example, the introduction of combination vaccines can potentially reduce missed opportunities for routine childhood vaccinations through fewer injections (a positive step). New vaccines may also alter clinical practice patterns, as evidenced by potential changes in evaluation for bacteremia in light of pneumococcal conjugate vaccination.38 However, the introduction of a new, multidose vaccine might also delay the administration of other routine childhood vaccinations because of the concern by some physicians and families for the number of injections or antigens provided per visit.3941 New vaccines might also result in additional health care visits,42 thereby adding to the burden of care. Few studies have assessed the impact of new vaccinations on these aspects of primary care.

In February 2000, the Food and Drug Administration licensed a 7-valent conjugate pneumococcal vaccine (PCV7) for use in children <2 years and in children 2 to 5 years who have high-risk medical conditions.10 The suggested vaccination schedule is 1 dose at 2, 4, 6, and 12 to 15 months of age. Physician acceptance and uptake was rapid,43 with subsequent supply shortages attributable in part to high demand for the vaccine.4446 Within a few years, studies showed marked declines in invasive pneumococcal disease in children47 and even declines in the disease burden among nonvaccinated adults through herd immunity.48 However, despite concerns that introduction of this vaccine might shift vaccine priorities with health care providers potentially delaying the administration of other vaccines in favor of timely delivery of PCV7, we are aware of only 2 studies that assessed the impact of PCV7 on these other aspects of primary care, and both studies involved physician self-reported behavior. One fifth of physicians responding to a physician survey in Rochester and Nashville reported delaying other vaccinations or scheduling additional visits in response to the new PCV7 vaccination.49 A physician self-report survey in Massachusetts found that many physicians reported either shifting routine vaccinations to visits other than the one involving PCV7 or adding additional visits for certain infants.50 Studies that go beyond self-report and examine medical charts to determine vaccination delivery in response to PCV7 have not been reported.

The objective of this study was to measure the impact of PCV7 on vaccine delivery and administration of other routine vaccines. Specifically, we assessed whether incorporation of PCV7 resulted in: (1) a delay in administration of other vaccinations or (2) additional visits to primary care offices to complete the childhood vaccination series. We hypothesized that some physicians might prioritize PCV7 over existing vaccinations, choosing to delay and schedule additional visits to administer either hepatitis B or varicella vaccination rather than increase the number of required injections to as many as 4 per visit.


    METHODS
 TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
The study methods were approved by the institutional review boards of the University of Rochester, Vanderbilt University, and the Centers for Disease Control and Prevention.

Setting
The setting involved 2 communities: Monroe County, New York, an upstate county with a total population of 750000, including the city of Rochester; and Davidson County, Tennessee, an urban setting with a population of 595000, including the city of Nashville. This study was part of the New Vaccine Surveillance Network,51 which was established in 1999 by the Centers for Disease Control and Prevention to perform active surveillance for common respiratory viral infections in young children52 and to conduct other studies of the impact of new vaccine recommendations on disease outcome.5356

Study Design
The study used a pre/postcohort design to evaluate vaccination delivery by community-wide medical chart review at primary care offices among 2 age-matched birth cohorts of children. The pre-PCV7 cohort was composed of children who were born before PCV7 licensure with birth dates between September 1, 1999, and November 30, 1999. The post-PCV7 cohort was composed of children who were born after PCV7 licensure with birth dates between September 1, 2000, and November 30, 2000. A physician survey in the 2 communities showed that the majority of physicians began offering PCV7 around August 2000 in Monroe County and around September or October 2000 in Davidson County.49 Very few of the children in the pre-PCV7 cohort received any PCV7 before their first birthday, and most of the children in the post-PCV7 cohort were eligible to receive PCV7 by 2 months of age. Some shortages of PCV7 were noted in both counties after licensure57 but not until the post-PCV7 cohort was >6 to 9 months of age.

Countywide Assessment of Vaccination Practices
Study Population and the Development of Practice Denominators
We identified all of the primary care practices in the 2 counties and sent a letter to each practice requesting collaboration with the medical chart reviews.58 We then obtained a potential denominator of eligible children for the pre-PCV7 and post-PCV7 cohorts from patient listings at each practice (see below). In Monroe County, 85 pediatric or family physician practices were eligible, and 70 participated (comprising >90% of the countywide birth cohort). In Davidson County, 32 pediatric or family physician practices were eligible, and 22 participated (comprising ~62% of the countywide birth cohort). Practice denominators were obtained from billing files in >90% of the practices; medical chart reviews generated practice denominators for the remainder.

Study Sample: Selection of Cohorts
The 2 cohorts (pre-PCV7 and post-PCV7) were selected from the practice denominators based on the child's date of birth and completion of a minimum of 1 visit to the index practice by 18 months of age. Previous power calculations determined that a decrease of 7% in hepatitis B coverage (from a baseline of 85% to 78%) required 600 subjects per cohort per county, and an increase of 10% in vaccination visits (from a baseline of 5.0 to 5.5 visits per year) required 750 subjects per cohort per county. We therefore selected >700 subjects per cohort per county by randomly sampling the number of subjects per practice proportionate to the practice size and desired sample size.

Medical Chart Assessments
Medical chart reviews were performed by trained chart abstractors. Demographic information, vaccination dates, and dates and types of health care visits were recorded on a standardized chart abstraction form. Well-child care (WCC) visits were distinguished from other types of visits by noting standardized WCC forms or other standardized procedures (such as height and head circumference measurements) in medical charts. Progress notes, summary pages, and written communications were all reviewed to locate, verify, and crosscheck the dates and types of vaccinations received. Interrater reliability checks showed agreement for >98% of the subjects for key vaccination dates.

Measures
Demographic measures included residence (city, suburbs, or surrounding area), race/ethnicity (black non-Hispanic, white non-Hispanic, or Hispanic), and health insurance at the most recent visit (private, Medicaid, State Children's Health Insurance Program, other, or none). The key vaccination measure was the median age in days of receipt of each routine childhood vaccination (median days were used, because the age of receipt of vaccination was often not normally distributed). Visit-related measures included: (1) mean number of visits that involved vaccinations, (2) mean number of vaccinations per visit, (3) mean number of WCC or other visits, and (4) missed opportunities for vaccinations. For these visit-related measures, 2 time periods were analyzed: 0 to 6 months and 13 to 18 months (the 7- to 12-month period had an insufficient number of vaccinations either recommended or given for analyses, because fewer vaccines are recommended during this time frame). The first time period (0–6 months) represents a "clean" comparison, because virtually no subjects from the pre-PCV7 cohort received PCV7 during the first 6 months of life, and most subjects in the post-PCV7 cohort received ≥1 dose of PCV7 during the first 6 months of life. Missed opportunities were defined as any visit during which a child was eligible for but did not receive a specific vaccine (unless a contraindication was noted in the chart).59,60

Analyses
Stratified analyses using Stata version 7 software (Stata Corp, College Station, TX) were performed by county, because it was possible that vaccination practices varied geographically. Bivariate analyses compared vaccination status and visit-related measures for pre-PCV7 and post-PCV7 cohorts within each county. {chi}2 and t tests were used to compare demographic characteristics and numeric measures, respectively, and the median test61 was used to compare the median age (in days) for receipt of vaccinations between the 2 cohorts.


    RESULTS
 TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Most demographic characteristics were generally similar for the pre-PCV7 and post-PCV7 cohorts (Table 1). The proportion of children covered by Medicaid increased between the 2 cohorts, and the proportion covered by private insurance declined slightly, reflecting national trends.62 A slightly greater proportion of the post-PCV7 cohort in Rochester was eligible for the Vaccines for Children program because of a higher proportion of that cohort being enrolled in Medicaid. The Nashville area was predominantly urban. More than 70% of children attended office-based pediatric practices, and ~15% attended hospital-based clinics in both counties.


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TABLE 1 Demographic Characteristics of the Sample Within Each County

 
Although we had hypothesized that introduction of PCV7 might result in delay in receipt of other vaccinations, a delay was not found for any routine vaccination (Table 2). For several vaccinations, the median age in days at receipt of vaccination was actually younger in the post-PCV7 cohort. For other vaccinations, the median ages did not differ statistically, and in some cases median ages were statistically younger in the post-PCV7 group but not clinically different. The overall coverage rates at 18 months did not differ between the pre- and post-PCV7 groups in either community. Many children in the pre-PCV7 cohort received PCV7 after 10 months of age, suggesting rapid uptake after licensure of PCV7. Overall, these data indicate that primary care providers did not delay other vaccinations while they incorporated PCV7 into their vaccination schedules.


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TABLE 2 Median Age in Days at Which Each Vaccination (or Combination of Vaccinations) Was Received for Pre-PCV7 and Post-PCV7 Cohorts

 
Table 3 shows the mean number of visits that involved vaccinations and the mean number of vaccinations per visit for the pre-PCV7 and post-PCV7 cohorts by county. Two time periods are analyzed: 0 to 6 months and 13 to 18 months. In Nashville (but not in Rochester), there were slightly more WCC and other types of health care visits that involved vaccinations among children 0 to 6 months of age in the post-PCV7 cohort than in the pre-PCV7 cohort; however, the opposite trend was noted for children 13 to 18 months of age. In both counties, the more striking finding is that health care providers generally increased the number of vaccinations per visit for infants 0 to 6 months of age, thereby accommodating the additional PCV7 vaccination within routine visits.


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TABLE 3 Mean number of WCC and Other Visits That Involved Vaccinations and Mean Number of Vaccinations Administered During These Visits for the Pre-PCV7 Cohort and the Post-PCV7 Cohort

 
In each county, the mean number of WCC or other visits in the pre-PCV7 and post-PCV7 cohorts was not different for the 3 age groups (0–6 months, 7–12 months, and 13–18 months; see Table 4). These results, together with findings from Table 3, suggest that health care providers did not schedule more visits to accommodate PCV7 vaccinations. Rather, they administered PCV7 vaccinations during existing WCC or other visits.


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TABLE 4 Mean Number of WCC or Other Visits During 3 Age Periods

 
Finally, we examined the number of missed opportunities for vaccinations during existing visits and found no substantive differences between the pre-PCV7 and post-PCV7 cohorts (results available from authors). For example, we had hypothesized that providers may delay varicella vaccination and administer PCV7 instead. In Rochester, the mean number of missed opportunities for varicella was 0.31 for the pre-PCV7 cohort and 0.29 for the post-PCV7 cohort (P = .01); in Nashville it was 0.27 for the pre-PCV7 cohort and 0.27 for the post-PCV7 cohort (P = .2). Thus, there is no evidence that missed opportunities for varicella vaccination increased after incorporation of PCV7; if anything, the opposite trend was observed.


    DISCUSSION
 TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Despite concerns that the addition of a new multidose vaccination to the childhood immunization schedule might delay other vaccinations or cause additional visits to the primary care office, this study found that the incorporation of PCV7 into the infant vaccination schedule was not associated with either a delay in other vaccinations or in substantially more visits to primary care practices. Instead, health care providers seemed to simply add PCV7 to the immunization schedule (ie, add another injection) and to use existing WCC and some other visits to vaccinate infants. Similar results were noted in the 2 disparate communities, strengthening the findings.

These findings support 2 previous and related studies that evaluated vaccination delivery after the recommended switch from oral polio vaccine to injectable polio vaccine. At that time there was concern that the additional injection could delay coverage. In 2 types of settings, health maintenance organizations63 and public health clinics,64 the switch to injectable polio vaccine did not seem to result in delayed coverage for either polio or other vaccinations. The current study is different in that it examines the addition of a fourth injection rather than a switch from oral to injectable vaccination, yet similar findings were noted. Although there is some evidence that health care providers may be more reluctant to add multiple injections than are parents,65 our study found that the rapid uptake of PCV7 was implemented through additional injections, perhaps because both health care providers and parents had a high degree of acceptance of this new vaccine.

Provider Self-Report Versus Chart Review to Assess Vaccination Practices
Multiple studies have investigated health care provider self-report regarding immunization delivery.6673 Two previous studies used self-reported questionnaires to assess whether physicians delayed other vaccinations in response to incorporation of PVC7. One of these 2 studies was a survey in the same 2 communities as in the current study,49 and it noted that 20% of physicians reported delaying other vaccinations or scheduling additional visits. The second study in Massachusetts50 found that 30% of physicians reported moving other vaccines to visits in addition to the PCV7-related visit. In both studies, the vaccines most likely to be delayed were hepatitis B, varicella, or polio vaccines. Interestingly, our current chart-review study did not find delays in other vaccinations after PCV7, nor did we find additional health care visits post-PCV7 compared with pre-PCV7.

We can only speculate why our current findings differ from these previous studies. First, the methodologies were quite different. The current study involved medical chart reviews across the entire communities, whereas the previous studies involved physician self-reported behavior. Previous studies have noted that physician self-reported behavior in fields other than vaccinations is not always confirmed by observed behavior.7476 A number of reports have also noted that physicians overestimate the up-to-date coverage of their practices.7779 It is possible that, in this case, physicians' self-reports overestimated the extent to which they altered their vaccination practices in response to PCV7. Thus, self-reporting of vaccination behavior may be inaccurate in this situation. A second possibility is that our study reflects community-wide assessments, whereas the physician self-report studies used physicians as the unit of analysis and did not weight for practice sizes; thus, responses from physicians from smaller practices counted as much as responses from physicians from larger practices, although they may vary by physician characteristics.80 A third possibility is that physicians who might otherwise have changed their practices did not do so because of the introduction of new combination vaccines. In fact, 2 other changes occurred in these communities between the pre-PCV7 and post-PCV7 cohorts: introduction of the ComVax combination vaccine and incorporation of thimerosal-free newborn hepatitis B vaccination in Nashville. These changes resulted in earlier receipt of Haemophilus influenzae vaccine in Rochester and incomplete recording of hepatitis B vaccine in Nashville but would not have affected the PCV7-related impact on receipt of many other vaccinations. In addition, these changes may have made introduction of PCV7 easier, reducing the number of injections needed. A fourth possibility is that the nonresponders in any of the studies somehow affected the findings,81 if their vaccination behaviors differed markedly from that of responders.

Although community-wide chart review may be more accurate than provider self-report in evaluating some aspects of vaccinations, this method is also quite resource intensive. Further study is needed to compare the relative benefits and weaknesses of each methodology to optimally assess primary care provider vaccination practices in the future. One promise involves the use of either immunization registries,82 if they are implemented community-wide, or linked electronic medical charts to assess health care visits in addition to vaccination dates. With the addition of new vaccinations in the coming years, efficient methods will be needed to measure both the positive and potential unintended consequences of new vaccines on primary health care.

Limitations
This study has several limitations. Regarding external validity, we only examined 2 communities, and it is possible that findings would differ in other settings. Although immunization rates may be higher in these 2 communities than in other urban areas,83 the 2 communities have similar rates of ambulatory visits to primary care pediatricians and family physicians compared with national rates (based on unpublished analyses of the National Ambulatory Medical Care Survey and the National Hospital Ambulatory Medical Care Survey, 2000). Also, immunization rates varied between the 2 counties, with Nashville having slightly lower rates, yet the same PCV7-related trends were noted, further supporting the study findings. A second limitation is that our scenario involved PCV7 vaccine, in which uptake was rapid. This may not be the case for all new vaccines, and in fact uptake of varicella vaccine was not as rapid. Our findings may be more generalizable to vaccines that have a high degree of acceptance.

Regarding threats to internal validity, a number of limitations exist. Vaccinations received outside of the practices might have been missed; however, these missed vaccinations should have occurred for both the pre-PCV7 and post-PCV7 cohorts and should not substantially affect the comparisons between cohorts. Practices that did not participate may differ from those that did participate in terms of their response to PCV7; however, most practices participated, and, in addition, the weight variables accounted for the nonparticipating practices in terms of practice characteristics. Most importantly, it is possible that external factors other than PCV7 might have led toward provision of other vaccinations more expeditiously and, without PCV7 the vaccination rates of the post-PCV7 cohort, might have been even better. There were no major changes in the routine childhood vaccination or WCC visit schedules other than PCV7 during the study time period. As mentioned, the switch in Nashville to newborn thimerosal-free hepatitis B vaccination and the incorporation of ComVax in both communities may have affected measures for hepatitis B and H influenzae type b.


    CONCLUSIONS
 TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
In these 2 communities, PCV7 was rapidly implemented by primary care providers after its licensure and incorporated into regular primary care visits without delays in other vaccinations or increased primary care visits. Providers seemed to administer PCV7 primarily within existing WCC visits, although other visits were also used for vaccination.

Implications
The major implication for clinicians is that despite concerns about multiple injections now required for childhood immunizations, primary care physicians are able to incorporate a major new multidose vaccination into their routine schedules without delaying vaccination coverage for other vaccines or increasing the visit burden to their practices.

The major implication for research is that findings from chart review-based studies may differ from findings from physician self-reports. In assessing future impact of vaccine recommendations on primary care, both types of study methods will likely be needed.

An implication for policy-makers is that rapid implementation of a new vaccine is possible without disruption of primary care, if the new vaccine is embraced by primary care providers. Because most childhood vaccinations are delivered in primary care settings, it is essential to provide adequate communication about the importance of new vaccines, as well as the need to maintain high coverage for the growing array of established childhood vaccinations.


    ACKNOWLEDGMENTS
 
We gratefully acknowledge the help of the Rochester practices that participated in this study, Diane Kent, RN, Carol A. Clay, RN, Ed Mitchel, MS, and the Nashville practices that participated in this study. We thank Marika K. Iwane, PhD, MPH, Stacey Martin, MSc, Caroline B. Bridges, MD, Ranee Seither, MPH, and Guillermo Herrera, MD, MBA (Centers for Disease Control and Prevention).


    FOOTNOTES
 
Accepted May 23, 2006.

Address correspondence to Peter G. Szilagyi, MD, MPH, Box 632, Strong Memorial Hospital, 601 Elmwood Ave, Rochester, NY 14642. E-mail: peter_szilagyi{at}urmc.rochester.edu

The findings and conclusions in this article are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention.

The authors have indicated they have no financial relationships relevant to this article to disclose.


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 CONCLUSIONS
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