SUPPLEMENT ARTICLE Progress toward Implementation of a Second-Dose Measles Immunization Requirement for All Schoolchildren in the United States Maureen S. Kolasa, Sonia Klemperer-Johnson, and Mark J. Papania National Immunization Program, Centers for Disease Control and Prevention, Atlanta, Georgia In 1998, the Advisory Committee on Immunization Practices and the American Academy of Pediatrics recommended that states ensure that all children in grades kindergarten through 12 receive 2 doses of measlesmumps-rubella (MMR) vaccine by 2001. In 2000, the National Immunization Program surveyed states, the District of Columbia, and United States territories, commonwealths, and protectorates to assess progress toward this goal. Almost all respondents (53 [98%] of 54) reported a second-dose requirement for entry to elementary school, middle school, or both. By fall of 2001, most (82%) school-aged children in the United States were in grades requiring a second dose of measles vaccine. For 29 responding programs, the requirement did not yet affect all grades. By 2009, 52 of 54 responding programs will require a second dose for all grades. Although not all states have achieved coverage of all schoolchildren with 2 doses of MMR vaccine, most states are well on their way toward this goal. Requiring immunizations at school entry has been a cornerstone of the US immunization program since the 1970s [1]. By the early 1980s, state requirements for a single dose of measles vaccine before school entry were instrumental in reducing the number of reported measles cases to record low levels [1]. However, outbreaks of measles continued to occur, mainly among unvaccinated preschool-aged children and vaccinated adolescents [2]. Primary vaccine failure (the lack of an effective immune response) contributed to the high proportion of cases among vaccinated children [3–5]. In 1989, to increase levels of immunity to measles in schoolchildren, the Advisory Committee on Immunization Practice (ACIP), the American Academy of Pediatrics (AAP), and the American Academy of Family Physicians (AAFP) recommended that schoolchildren receive a second dose of measles vaccine [6–8]. However, the ACIP, AAP, and AAFP did not agree on the timing of the second dose. The ACIP and AAFP rec- Reprints or correspondence: Dr. Maureen S. Kolasa, Centers for Disease Control and Prevention, 1600 Clifton Road, Mailstop E-61, Atlanta, GA 30333 (mxk2@ cdc.gov). The Journal of Infectious Diseases 2004; 189(Suppl 1):S98–103 This article is in the public domain, and no copyright is claimed. 0022-1899/2004/18909S1-0016 S98 • JID 2004:189 (Suppl 1) • Kolasa et al. ommended that children be vaccinated before entering elementary school, whereas the AAP recommended that adolescents receive a second dose before entering middle school [6]. State immunization programs began adopting second-dose school entry requirements, following either the recommendations from ACIP/AAFP or those of AAP. A few states adopted both recommendations and required 2 measles vaccinations of children entering both elementary and middle school [9]. Subsequent measles outbreaks demonstrated the effectiveness of a second dose at inducing an immune response in people who remained seronegative after a first dose and in preventing measles [10]. During a 1994 measles outbreak in Colorado, measles was contracted by 7 (44%) of 16 unvaccinated children and 10 (3%) of 320 children with only a single dose of measles vaccine, whereas none of the 289 children who had received 2 doses of measles vaccine developed disease [11]. In another outbreak among school-aged children in Utah, a single dose of measles was 97% efficacious, and 2 doses were 100% efficacious in preventing disease [12]. Because outbreaks continued to occur among schoolaged children not covered by a second dose, additional efforts were made to immunize all school-aged children with a second dose of measles vaccine [12]. In 1998, the ACIP, AAP, and AAFP synchronized their recommendations for a second dose before elementary school entry. In addition, the ACIP and AAP recommended that states require that all school-aged children receive a second dose of measles vaccine by 2001 [13, 14]. We conducted a survey to assess states’ progress toward the goal of coverage of all school-aged children with 2 doses of measles vaccine by 2001. Survey objectives were to describe when states implemented a second-dose requirement, how states assess second-dose coverage, and by what year all schoolaged children will be covered by the second-dose requirement. We also reviewed other data from the Health Employment Data Information Set (HEDIS) and the National Health Interview Survey (NHIS) for information regarding receipt of 2 doses of measles vaccine among school-aged children. METHODS A survey was sent via e-mail to the immunization program managers of every state, the District of Columbia, and the 8 territories, commonwealths, and protectorates of the United States. We collected data on the following: whether and when laws were enacted that require that children receive 2 doses of measles vaccine; type of measles vaccine required for the second dose; what grades are required to receive 2 doses in 2001; by what year all grades will be covered by the laws; whether the state or territory has any plans for accelerating coverage by grade; how second-dose measles vaccination coverage is assessed; and results from any such assessments. US census data were used to determine the size of grades for all states, the District of Columbia, Puerto Rico, and the Northern Mariana Islands [15]. Estimates of populations by single-year age were available for 1989–1999 for all states and the District of Columbia. Estimates of population by 5-year age groups were available for 1990–2001 for Puerto Rico and the Northern Mariana Islands. We assumed that each age would correspond to a single grade (e.g., 5-year-olds were considered to be kindergartners, 6-year-olds were considered to be first graders). We determined the grade populations in Puerto Rico and the Northern Mariana Islands by dividing each 5-year age group into single-year age groups and calculated a 5-year moving average to smooth the data. School enrollment numbers are submitted by the Federated States of Micronesia to the Centers for Disease Control and Prevention (CDC). We used Microsoft Access and Excel for data entry and analysis. For states that assess second-dose measles vaccination coverage, we used the census estimates to calculate populationbased coverage levels. To estimate population-based coverage levels for future years, we projected current data to future years. To estimate the impact of second-dose measles vaccine requirement for schoolchildren, we plotted the numbers of con- firmed measles cases among persons 5–19 years of age reported by states to the CDC. We excluded imported cases occurring in persons who are not residents of the United States. RESULTS The survey response rate was 92% (54/59). All 50 states, the District of Columbia, Puerto Rico, the Northern Mariana Islands, and the Federated States of Micronesia returned the survey. The 5 nonresponders were all island territories. For the remainder of this paper, all responders will be referred to as “states.” By fall 2001, almost all (53 [98%] of 54) states require a second dose of measles vaccine at school entry, either at elementary school entry, middle school entry, or both. Idaho is the only state that has no requirement and no future plans to require a second dose of measles vaccine for school entry. The majority of states (36 [67%] of 54) have both elementary and middle school entry requirements. A number of these states introduced middle school entry requirements in the early 1990s and implemented a kindergarten requirement only after the 1998 recommendations. About one-quarter of states (14 [26%] of 54) rely solely on elementary school entry requirements. Three states (6%) have only middle school entry requirements, and all of these states plan to implement second-dose entry requirements for kindergarten in the near future. Most states implemented school entry requirements gradually, requiring 1 or 2 grades be vaccinated per year, but 16 states (30%) required all or many grades be vaccinated in a single year. Although measles vaccine is usually given in combination with mumps and rubella vaccines (MMR) for the first dose, states vary in what vaccines are required for the second dose. A majority of states (32 [59%] of 54) simply require that children receive a measles-containing vaccine. About one-third of states (19 [35%] of 54) require that children receive the MMR vaccine, and 2 states require the measles and rubella vaccine. States also vary in their approach to new entrants into the school system. When a child moves to a different state, the child may not be in compliance with the new state’s immunization requirements. Most states (39 [72%] of 54) require that new entrants into the school system be vaccinated with 2 doses of measles vaccine. A majority of these (22 [56%] of 39) require a second dose of measles vaccine for entrants into all grades, whereas 17 states (44%) require a second dose of measles vaccine only of new entrants into grades already covered by their second-dose requirement. All states that require a second dose of measles vaccine assess vaccination coverage through ⭓1 of the following methods: self-report by all schools; self-report by all elementary, all middle, or all high schools, but not all 3 types of schools; validation Second-Dose Measles Immunization Requirement • JID 2004:189 (Suppl 1) • S99 Table 1. State methods for assessing immunization coverage in school students. No. (%) of states by reporting method Validation method Validation audits, all schools Validation audits, sample of schools No validation audits Total All schools self-report 1 (2) 18 (33) Some schools self-report 0 17 (32) No schools self-report Total 6 (11) 7 (13) 3 (6) 38 (70) 7 (13) 1 (2) 1 (2) 9 (17) 26 (48) 18 (33) 10 (19) 54 (100) audits on a sample of schools; or validation audits on all schools (table 1). Most states (38 [70%] of 54) conduct validation audits on a sample of schools, whereas 7 states (13%) conduct validation audits in all schools and 9 (17%) do not conduct validation audits. Some states assess only whether children are compliant with all immunization requirements and do not assess for specific vaccines, such as the measles vaccine. Measles vaccine coverage is assessed among elementary school students in 38 states and among middle school students in 25 states. The median immunization coverage level for the second dose of measles vaccine was 97% (range, 57%–99%) for students entering elementary schools and 98% (range, 62%– 99%) for students entering middle schools. According to the survey results, by the fall of 2001, most (82%) school-aged children in the United States were in grades for which a second dose of measles vaccine was required. As the percent of children covered by a second-dose requirement has increased, the reported numbers of measles cases among school-aged children has decreased, from almost 10,000 per year in 1989–1990 to !50 per year for 1997–2001 (figure 1). Twenty-five states met the goal of covering all cohorts in grades kindergarten through 12th grade with a 2-dose measles vaccine requirement by 2001 (figures 2 and 3). Either by using projected data provided by states or by projecting current data to future years, we estimate that 52 of 54 states will have required a second dose for all grades by 2009 (figure 2). One of the remaining 2 states does not require a second dose for any grades, and the other state requires a second dose for middle school entry only. On the basis of data obtained by this survey, we calculated the impact of the recommendation for a second dose of measles vaccine on susceptibility to measles among children aged 5–17 years in 2001. To do this calculation, we made the following assumptions: the seroconversion rate after the first dose of measles vaccine is 95%, and of those who do not seroconvert after the first dose, seroconversion after the second dose is 95% [11, 13, 16, 17]; coverage in the United States for 1 dose of measles vaccine at school age is 96% [18], and on the basis of the data herein, 82% of school-aged children are covered by a second-dose measles requirement. Using these assumptions, we estimate that without a second-dose recommendation, 4.5 million school-aged children would have been susceptible to measles in 2001. With the second-dose recommendation and current coverage levels, only ∼650,000 school-aged children were susceptible to measles in 2001. Figure 1. Comparison of school-aged children (ages 5–19 years) covered by a 2-dose measles vaccine requirement and measles cases in schoolaged children, 1989–2001. S100 • JID 2004:189 (Suppl 1) • Kolasa et al. Figure 2. Number of states with 2-dose measles vaccine requirement for all children in kindergarten through grade 12 (K-12), 1992–2009 DISCUSSION In accordance with the 1998 policy recommendations, by 2001 almost all states had implemented second-dose measles vaccine requirements for school entry. Although only 25 states achieved the 2001 goal of complete coverage of all schoolchildren with a requirement for 2 doses of a measles vaccine, most states are well on their way toward this goal, and measles cases in schoolaged children are at an all-time low [19]. Various grades are covered by states’ second-dose measles vaccination laws, with some states requiring the second dose at entry to elementary school, others at entry to middle school, and still others at both elementary and middle school entry. This variation likely results from different second-dose recommendations given by ACIP, AAP, and AAFP in 1989. Synchronization of second- Figure 3. dose measles vaccination recommendations in 1998 has helped to decrease this variation among states. Methods used to assess immunization coverage levels and approaches to new entrants into the school system differ greatly between states; thus, comparing coverage data among states is problematic. In addition, not all states assess receipt of 2 doses of measles vaccine among new entrants (i.e., transferring students) into a school system. This creates the opportunity for failure to identify underimmunized children. For example, a child in elementary school with only 1 dose of measles vaccine moving from a state with a middle school entry requirement to a state with an elementary school entry requirement might not be identified as needing a second dose. It is important to distinguish vaccine coverage from a vaccine Number of grades covered by school requirements for second-dose measles vaccination in 2001 Second-Dose Measles Immunization Requirement • JID 2004:189 (Suppl 1) • S101 requirement. State assessments indicate that a median of 97%– 98% of children subject to a 2-dose requirement have received 2 doses. On the other hand, many children may be vaccinated without being subject to a requirement. According to data collected in 1997 by HEDIS on children enrolled in managed care organizations, the mean plan coverage of 13-year-olds for 2 doses of MMR was 61% [20]. In 1997, data from the NHIS indicated that 89% of 13- to 15-year-olds had received a second dose of measles vaccine [21]. In comparison, the results of our survey showed that !50% of middle school–aged children in the United States had actually been required to receive a second dose of measles vaccine by 1997. This suggests that actual 2dose measles vaccine coverage may be substantially higher than coverage solely calculated with a state requirement for 2 doses, especially among adolescents. The high coverage results for 2 doses of measles vaccine as reported by HEDIS and NHIS are further verified by data 6 states submitted to the CDC on assessments of second-dose measles vaccination coverage among grades not covered by the school entry requirements. These states reported a median coverage level for 2 doses of measles vaccine of 60% among children not required to receive the second dose and a median coverage level of 197% among children covered by a seconddose requirement. Many physicians and parents appear to have followed the recommendations of ACIP, AAP, and AAFP and vaccinated children with 2 doses of measles vaccine, even if this was not yet required by the state. The fact that second-dose coverage among children not required to receive the second dose is lower than coverage among children who are required to have the second dose suggests that school entry requirements are at least partially responsible for increasing the level of second-dose coverage. Study limitations include our reliance on self-reports from states regarding their second-dose laws: we did not review state legislation ourselves. We also relied on state reports of seconddose coverage, which are limited because states use various methods to assess second-dose coverage, and 17% of states (9/ 54) do not conduct validation audits on their assessment results. Because most surveyed states submitted data only for grades covered by second-dose immunization requirements, we could not ascertain coverage levels in grades not covered by the requirements. We did not use school enrollment figures, which would have given us a better indication of the actual numbers of children affected by these laws. In summary, although not all states have yet achieved coverage of all schoolchildren with 2 doses of measles vaccine, most states are well on their way toward this goal. Almost all states have implemented second-dose measles vaccine laws for school entry, and by 2009, all but 2 states will require schoolchildren in every grade to have 2 doses of measles vaccine. Because of the variation among states in requiring the S102 • JID 2004:189 (Suppl 1) • Kolasa et al. second dose at elementary school and middle school entry, we recommend that all new entrants into the school system be assessed for 2 doses of measles vaccine. 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