Objective. To estimate the additional number of visits to primary care practices that would be required to deliver universal influenza vaccination to 6- to 23-month-old children.
Methods. Children who were covered by commercial and Medicaid managed care plans (70% of children in the region; >8000 children in each of 3 consecutive influenza seasons) in the 6-county region surrounding and including Rochester, New York, were studied. An analysis was conducted of insurance claims for visits (well-child care [WCC]; all other visits) to primary care practices during 3 consecutive influenza vaccination seasons (1998–2001). We determined the proportion of children who made 1 or 2 visits during the potential influenza vaccination period, simulating several possible lengths of time available for influenza vaccination (2, 3, 4, or 5 months). We measured the proportion of children who were vaccinated during each influenza vaccination period. The added visit burden was defined as the number of additional visits that would be required to vaccinate all children, simulating 2 scenarios: 1) administering influenza vaccination only during WCC visits and 2) considering all visits as opportunities for influenza vaccination.
Results. Results were similar for each influenza season. Considering a 3-month influenza vaccination window and assuming that no opportunities were missed, if only WCC visits were used for influenza vaccination, then 74% of 6- to 23-month-olds would require at least 1 additional visit for vaccination—39% would require 1 additional visit and 35% would require 2 additional visits. If all visits to the practice were used for influenza vaccination during the 3-month window, then 46% would require at least 1 additional visit—34% would require 1 additional visit and 12% would require 2 additional visits. Longer vaccination periods would require fewer additional visits; eg, if a 4-month period were available, then 54% of children would require 1 or 2 additional visits if only WCC visits were used and 29% would require 1 or 2 additional visits if all visits were used for influenza vaccinations. Younger children (eg, 6- to 11-month-olds) would require fewer additional visits than older children (12- to 23-month-olds) because younger children already have more visits to primary care practices.
Conclusions. Implementation of universal influenza vaccination will result in a substantial increased burden to primary care practices in terms of additional visits for influenza vaccination. Practice-level strategies to minimize the additional burden include 1) using all visits (not just WCC visits) as opportunities for vaccination, 2) providing influenza vaccination for the maximum possible time period by starting to vaccinate as early as possible and continuing to vaccinate as late as possible, and 3) implementing short and efficient vaccination-only visits to accommodate the many additional visits to the practice.
Influenza virus causes yearly1 epidemics and is associated with an estimated 36 000 deaths per year in the United States, mostly in the elderly.2 Although children are far less likely than the elderly to experience serious consequences from influenza infection, up to 1% of children younger than 6 months and 0.01% to 0.5% of children 6 months to 5 years of age are hospitalized annually as a result of influenza infection1,3–6 During an influenza season, 20% to 30% of children may develop clinical manifestations of influenza,7–10 resulting in missed school or child care; added outpatient medical visits11–13; antibiotic use for otitis media,14 pneumonia, or other infections associated with influenza; exacerbations of chronic underlying diseases such as asthma15,16; added medical costs17,18; and transmission of infections to high-risk adults.19,20
Pediatric influenza vaccination has been recommended for children who are older than 6 months and at increased risk for complications because of chronic pulmonary, cardiovascular, or other diseases.21 Although this recommendation includes children with asthma and covers approximately 10% of US children, only a fraction of eligible high-risk children are vaccinated.22,23 As a result of the mounting evidence of the burden of influenza,1,24,25 in April 2002, the Advisory Committee on Immunization Practices (ACIP) expanded on the recommendations for childhood influenza vaccination: “Because young, otherwise healthy children are at increased risk for influenza-related hospitalization, influenza vaccination of healthy children aged 6 to 23 months is encouraged when feasible. Vaccination of children aged ≥6 months who have certain medical conditions continues to be strongly recommended.”1 Vaccines for Children (VFC) coverage was added for this population and their household contacts starting in the 2003–2004 influenza season.26 The American Academy of Pediatrics (AAP) endorsed the ACIP encouragement of vaccination for children 6 to 23 months of age.27
This new ACIP encouragement represents a change in pediatric influenza vaccination policy by including the 6- to 23-month-old group as a high-risk group. This would result in a major shift in pediatric practice, from targeted vaccination of high-risk children (by disease) to universal vaccination of this entire age group. Influenza would be the first universal childhood vaccine administered annually and during a seasonal time frame rather than year-round. This current encouragement may soon become a formal recommendation. Because most young children would be vaccinated at their primary care practices, it is critical to consider the feasibility and additional burden of universally administering influenza vaccination in those settings.
A number of potential obstacles exist to universal vaccination of young children. These include vaccine-specific barriers such as the perception among some providers and parents that influenza is a benign disease and concerns about side effects and effectiveness of the vaccine.28,29 Other obstacles include the already crowded pediatric immunization schedule,30 the additional intramuscular vaccination needed for the current influenza vaccine,31 and the need for annual vaccination for many young children and 2 vaccinations in the first year that young children receive the vaccine. System-level barriers include difficulty in identifying and recalling eligible children for vaccination within the short vaccination period32–34 and financing issues. No published studies have addressed the practical barrier of the sheer number of children who would need additional visits during the vaccination period. The objective of this study was to estimate, on a population level, the additional number of health care visits to primary care practices that would be required to deliver influenza vaccination to all 6- to 23-month-old children.
Study Population and Sources of Data
The setting was a 6-county region in upstate New York (total population of just over 1 million in 200035), covering the urban county that includes the city of Rochester and 5 rural surrounding counties. An insurance claims database was analyzed that contains claims data from 5 managed care plans in the region: 1 independent practice association-model health maintenance organization, 2 physician hospital organizations, 1 Medicaid managed care plan, and the State Child Health Insurance Plan, which covers children of the working poor who do not qualify for Medicaid. These plans together insure approximately 70% of children in the region, including 40% of Medicaid enrollees.
Eligibility criteria for the study population were as follows: 1) children 6 to 23 months enrolled in 1 of these managed care plans in 1 of 3 influenza seasons: 1998–1999, 1999–2000, or 2000–2001; 2) residence within the 6 target counties; and 3) continuous enrollment in any plan or combination of plans during 1 of the influenza seasons (September 1 of one year through January 30 of the following year). The 6 counties had a 6- to 23-month-old population of approximately 17 500 in 2000,36 and the insurance database included 13 000 to 13 400 6- to 23-month-olds in each target year, with 8300 to 8700 meeting the criteria for inclusion in this study.
The primary care pediatricians and family physicians in this region were grouped by practices. Office visits to these practices, presence of chronic conditions that would have previously indicated the need for influenza vaccination1 (eg, asthma), and receipt of influenza vaccinations were identified using Physicians’ Current Procedural Terminology, Fourth Edition codes37 and International Classification of Diseases, Ninth Revision (ICD-9) codes.38
Ages (defined as the child’s age on the first of each month of each scenario) were categorized as 6 to 11 months, 12 to 23 months, and total (6–23 months). Residence was classified by zip code as follows: the city of Rochester was classified as urban, the rest of Monroe County was classified as suburban, and zip codes within the adjacent rural counties were classified as rural. Insurance type (all plans were managed care plans) was designated as commercial (including the State Child Health Insurance Plan39) or Medicaid. Practice type was delineated as pediatric private practice, family physician practice, neighborhood health center, hospital clinic, or other type. The 6 counties were combined in the analyses because results were similar across counties. Visits were classified as well-child care (WCC) visits, all other, and total visits to the practice. Analyses were performed separately for each influenza vaccination season.
Because the availability of influenza vaccine has varied depending on supply of vaccine1,40 and the onset and duration of the influenza season, we calculated different scenarios for possible “windows of opportunity” for universal influenza vaccination, ranging from lengthy to very short periods. These periods included 5 months (September 1–January 31), 4 months (October 1–January 31), 3 months (October 1–December 31), 2 months (November 1–December 31), and a second 2-month scenario (October 1–November 30, considered the optimal time to vaccinate because it precedes the influenza season). The presence of a high-risk condition that would have made the child eligible for influenza vaccination before universal vaccination (asthma, sickle cell anemia, chronic heart disease, chronic pulmonary disease, or immunologic disease) was determined from ICD-9 codes during the 12-month period of the target influenza season. Two separate services (eg, 2 visits for asthma) were required within the 12-month period to classify the child as having that diagnosis.
For each child, the following measures were calculated:
Completed visits: number of WCC and other visits made to the primary care practice during the influenza vaccination period
Vaccination: number of influenza vaccinations (0, 1, or 2) received during a particular influenza vaccination season
Number of vaccinations needed: number of vaccinations (1 or 2) needed according to current ACIP guidelines—1 if vaccinated the previous year, and 2 if not vaccinated the previous year (contraindications were not obtainable from the database)
Additional visit: number of additional visits (0, 1, or 2) needed during separate months (2 visits in the same month were not allowable because of vaccination timing requirements) within the influenza vaccination period for each scenario
Because missed opportunities for vaccination are less common during WCC visits than during other visits,29,30,41 we determined 2 additional scenarios: 1) assuming that all WCC visits (but only WCC visits) were used for influenza vaccination under a universal influenza vaccination policy and 2) assuming that all visits to the practice were used for influenza vaccination. This second scenario reduced the number of additional visits needed by assuming a perfectly efficient practice with no missed opportunities. Using the database, we were unable to calculate the percentage of all visits that would include vaccine contraindications; therefore, we used these 2 scenarios without considering contraindications.
Point estimates were calculated of the number of visits made to the practice and the number of additional visits needed during any given influenza vaccination period, assuming different scenarios. Bivariate analyses compared results for the various independent variables.
Data for >8000 children were analyzed for each influenza season (Table 1). The largest proportion of children resided in urban areas, had commercial insurance, and attended private pediatric practices. Twenty-one percent of children who had asthma or high-risk conditions and were eligible for targeted influenza vaccination received the vaccination; almost no children received influenza vaccination unless they had a high-risk condition.
Table 2 shows the percentage of children who made 1 visit or 2 or more visits to their practice during the 2000–2001 influenza season, during each of the 5 possible time-period scenarios when influenza vaccination might have been available. Results for the 2 previous influenza vaccination years were virtually identical in this and all other tables (<2 percentage points different for all strata). Depending on the scenario, 41% to 60% of children had at least 1 WCC visit during the time period eligible for influenza vaccination. When all visits made to the primary care practice are considered, the percentage with 1 or more visits during the time period increased substantially.
Table 3 displays the percentage of children 6 to 23 months of age who would need no more visits, 1 additional visit, or 2 additional office visits during the first year of universal influenza vaccination, for each of the 5 possible time-period scenarios, based on the 2000–2001 influenza season. The number of additional visits required varied substantially depending on the possible time period for vaccination and whether only WCC visits or all visits would be used as vaccination opportunities. If only WCC visits were used for influenza vaccination, then 36% (5-month period), 54% (4-month window), 74% (3-month window), and 89% of children (2-month window) would require at least 1 additional visit for influenza vaccination. If all visits were used as opportunities for vaccination, then the percentage of children who would require at least 1 additional visit for influenza vaccination was lower by approximately 20 percentage points for each scenario compared with the situation in which only WCC visits were used for vaccination.
Because infants have more visits to primary care practices, the number of additional visits required for universal influenza vaccination varies by age, even within the narrow 6- to 23-month age group. Hence, younger children would require fewer additional visits (Table 4). For example, considering only WCC visits for influenza vaccination during a 3-month period, 66% of 6- to 11-month-olds but 78% of 12- to 23-month-olds would require 1 or 2 additional visits.
The percentage of children who would need 1 or 2 additional visits varied somewhat according to patient and provider characteristics, particularly when 2 additional visits were required for receipt of influenza vaccination. Figure 1 illustrates these differences for the scenario in which a 3-month influenza vaccination period exists and influenza vaccination occurs only during WCC visits (top) or during all visits (bottom). As shown, a higher percentage of urban children (compared with suburban or rural children) and children covered by Medicaid (compared with commercial insurance plans) would require 2 additional visits to the practice for influenza vaccination. Similarly, fewer children receiving care at private pediatric practices would require 2 additional visits compared with children who receive care at family physician practices, hospital clinics, or neighborhood health centers. More than 70% of all children would require 1 or 2 additional visits if the vaccination season lasted for 3 months and if only WCC visits were used for vaccination, whereas approximately 40% to 50% would require 1 or 2 additional visits if all visits were used for vaccination.
The discussion of universal influenza vaccination for young children has been dominated by the disease burden from influenza, efficacy and safety of the vaccine, vaccine supply, and provider concerns about feasibility. Surprisingly little has been researched about feasibility issues. We found that the additional burden on primary care practices in terms of added visits for influenza vaccination was substantial and varied depending on the length of the vaccination period and the degree to which providers take advantage of existing visits to the practice.
Length of the Vaccination Period
The added visit burden varied mostly with the length of the time period for influenza vaccination. If the vaccination period were 5 months, then only one fifth to one third of children would require 1 or 2 additional visits; however, if the vaccination period were only 2 months (eg, with short supply or an early epidemic season), then two thirds to nearly 90% of children would require 1 or 2 additional visits. Each month of shortening of the vaccination time period results in a 15 to 20 percentage point increase in the proportion of children who would require 1 or 2 additional visits for vaccination. Recommendations that encourage continued vaccination during the influenza season (ie, continuing to vaccinate into January) should be emphasized1 to reduce the number of extra visits required.
Using Existing Visits as Opportunities for Vaccination
The additional burden of visits varied greatly depending on whether only existing WCC visits were used for vaccination or all visits were used. This study highlights the critical role that missed opportunities will inevitably play in universal influenza vaccinations, just as missed opportunities play a major role in routine childhood41–44 and adult vaccination rates.45 Taking advantage of all visits instead of just WCC visits would reduce by approximately 20 percentage points the number of additional visits required. The most difficult change in practice would be to use every single visit to the practice as an opportunity for influenza vaccination, including acute visits and follow-up visits when parents and clinicians alike may be averse to giving vaccines. Influenza vaccine is safe and effective even if given during an acute illness such as an asthma exacerbation or a common infectious condition.1 Education of practitioners and parents is needed about the safety and efficacy of influenza vaccination during acute visits.46
Strategies to Improve Influenza Vaccination Rates
The additional influenza vaccination visits may pose challenges for some offices, especially during busy winter months. For example, a typical group practice, with a birth cohort of 500 newborns per year, that provided influenza vaccinations only during WCC visits during a 3-month window, would need to accommodate approximately 800 additional visits (200 6- to 11-month-olds and 600 12- to 23-month-olds) for universal influenza vaccination. A recent study found that although the time within offices that was currently spent on “influenza vaccine only” visits was relatively short, extrapolating these times to an entire age cohort would produce a substantial burden on primary care practices in terms of room availability and personnel time.47 Thus, practices may wish to add influenza-vaccine hours or clinics during which a large number of children are efficiently vaccinated without disrupting the normal flow of a busy practice. The number of children who are vaccinated during these special hours would depend on the number of assigned rooms and personnel. Case descriptions of practices that have used such vaccine-only hours suggest that they can be efficient.48 Of note, the availability of nasal influenza vaccine would not lengthen the time for vaccination (Sharon Humiston, personal communication, Rochester, NY, May 19, 2003).
The additional office visits needed to vaccinate children during influenza vaccination season will be partially offset by fewer acute visits that are averted by the influenza vaccination. Although the exact number of potential averted office visits is unknown and depends on the influenza season and effectiveness of the vaccine, extrapolation from Neuzil’s findings6 of the excess outpatient visits attributable to influenza results in the following: for the above-mentioned practice with a birth cohort of 500 children (ie, 750 children 6–23 months of age), universal influenza vaccination of 6- to 23-month-olds would result in 38 fewer outpatient visits for 6- to 11- month-olds and 55 fewer visits for 12- to 23-month-olds, or 93 total fewer outpatient visits (assuming 100% vaccine coverage and effectiveness). Thus, even with 100% coverage and effectiveness of the influenza vaccine, the visits saved by vaccinating children is far less than the number of additional visits required to vaccinate this cohort of children.
Given the large number of additional influenza vaccination visits that will be required for universal influenza vaccination and the relatively few outpatient visits averted, it will become critical to vaccinate children efficiently and to make use of all opportunities to provide influenza vaccination when children are already in the primary care office for any reason. A number of strategies have been found to reduce missed opportunities for vaccinations; these include standing orders for vaccinations,49,50 educational sheets provided to parents on registration,51 and provider prompts placed on medical charts or on encounter forms at the time of patient visits to remind providers to vaccinate children.41,47,48
In addition, practices will need to implement telephone or mailed reminder strategies52 to identify and recall children who are eligible for universal influenza vaccination because many eligible children will not otherwise visit the practice. This heightens the potential role of immunization registries53 or databases of managed care organizations, both of which have the capability to contact entire populations about influenza vaccination.
Achieving high influenza vaccination rates assumes that both parents and providers support the recommendations to vaccinate healthy children. Provider adherence to universal influenza vaccination depends on a variety of factors,54 and any 1 factor (eg, concerns about safety) could threaten high rates. A public awareness campaign should accompany the recommendations for universal influenza vaccination of young children.
A critical system-wide change that needs to occur for universal influenza vaccination to succeed is financial coverage.54 The recent experience with the conjugate pneumococcal vaccine, in which recommendations preceded full insurance and VFC coverage of the vaccine, placed some providers in a difficult position of having insurance coverage for only a portion of their population for a short time period.55,56 Because VFC coverage will exist for the 2003–2004 influenza vaccination season,25 widespread commercial insurance coverage for universal vaccination of this age group may be forthcoming.
The added visit burden will entail a real cost to insurers (if the influenza vaccination is covered) or to primary care practices (if not covered). These additional costs should be offset by reduced hospitalizations and fewer outpatient and emergency department visits as a result of protection of this age cohort (and potential contacts) from influenza disease. These factors point out the need for both cost-effectiveness studies and surveillance studies to evaluate the changing burden of disease from influenza viral infection and subsequent universal influenza vaccination.
Strengths and Limitations
Study strengths include the analysis of a database for a large population so that data are applicable at the community level, the inclusion of several years of data to account for temporal variations, and the use of both conservative and more liberal assumptions (eg, short vs longer vaccination periods, use of only WCC visits or all visits for vaccinations).
Several study limitations exist. One limit to internal validity involves our need to include only children who were continuously enrolled in health insurance or Medicaid during the influenza vaccination season to be able to determine visits to the practice during that time period. It is possible that utilization patterns of children who were not continuously enrolled differed from those who were continuously enrolled. Second, we used the insurance database to identify children who received influenza vaccine during the previous year. Studies have found that insurance databases underestimate true vaccination rates.57,58 This may have reduced somewhat the estimate of the proportion of children who would need a second influenza vaccination during the target year. Such errors would not alter the findings much because only approximately 10% of children would have been eligible for influenza vaccination under the targeted recommendations in effect during the previous year. Third, we assessed 2 possible scenarios for vaccination (WCC visits or all visits); in reality, some children would be too ill during those visits to be vaccinated (or would have a febrile illness and would not be vaccinated), and our analyses therefore underestimate the actual number of additional visits that would be required.
Regarding external validity, this study represents 1 community only, and it is possible that visits to practices vary in other communities. Although national data were not available for comparison for precisely this 6- to 23-month age group, visit rates for acute respiratory diseases in young children in this database closely followed visit rates nationally—for example, for children between 1 and 4 years of age, visit rates were similar in this database versus national visit rates as determined by the National Ambulatory Medical Care Survey59 for otitis media (74 in 100 children in Rochester, 65 in 100 children across the United States) and any acute respiratory diagnosis from a list of ICD-9 diagnoses (168 in 100 and 167 in 100). This insured managed care population may also have more primary care visits than children who are covered by indemnity plans or who are uninsured.60–62 All of these factors would tend toward more frequent visits in this study population than some other populations, so even greater additional visits would be required in those populations to vaccinate children with influenza vaccine.
This study used 3 previous influenza seasons as the basis for estimating visits to primary care offices. The findings are dependent on the assumptions. One assumption is that the 3 previous years will reflect future years. It is possible that during future years, utilization patterns may change irrespective of universal influenza vaccination. An unusually severe respiratory illness season may cause more acute visits to offices than observed during these 3 study years, changing the proportion of children who already make a visit during the potential vaccination season. A second study assumption is that only 1 of 2 “patterns” of care would occur: using all WCC visits as opportunities for influenza vaccination or using all visits as opportunities. In fact, it is likely that something in between may really happen. Many offices are likely to increase the number of influenza vaccination-only visits but not provide influenza vaccinations during acute office visits. However, the above 2 patterns may establish the 2 boundaries for the additional visits that would be required. Third, this study focused on the burden of visits during the first year that universal influenza vaccination would take place. During subsequent years, those children who were vaccinated the previous year would require only 1 additional visit the subsequent year, so the visit burden would be lower for this subset of children.
The implementation of universal influenza vaccination will result in many additional visits to primary care practices. The additional burden will depend greatly on the length of the influenza vaccination period, whether providers vaccinate during both WCC and other visits, and the number of illness visits to the practice. The additional burden in visits will be less for younger children who make more visits but greater for poor children who make fewer visits. For universal influenza vaccination to achieve high coverage rates, changes will be needed both at the practice and the system level. At the practice level, these changes include 1) efficient use of existing visits (eliminating missed opportunities), 2) starting to vaccinate as early as possible and continuing to vaccinate as late in the season as possible, 3) using effective strategies to remind and recall the eligible population, and 4) implementing efficient means for vaccinating this many children during short, vaccination-only visits. At the system level, the following changes would be needed: 1) adequate coverage and reimbursement via insurers for these influenza vaccination visits, 2) use of immunization registries or managed care databases to help primary care providers identify and recall eligible children, 3) education of providers and families about the importance of influenza vaccination for healthy children, and 4) adequate supply of influenza vaccine as early as possible during the year.
This work was funded by the Centers for Disease Control and Prevention (Cooperative Agreement U38YCCU217969-01).
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