Elimination of Measles and of Disparities in Measles Childhood Vaccine Coverage among Racial and Ethnic Minority Populations in the United States

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1 SUPPLEMENT ARTICLE Elimination of Measles and of Disparities in Measles Childhood Vaccine Coverage among Racial and Ethnic Minority Populations in the United States Sonja S. Hutchins, 1 Ruth Jiles, 2 and Roger Bernier 1 1 National Immunization Program and 2 National Immunization Program, now the National Center for Chronic Disease and Health Promotion, Centers for Disease Control and Prevention, Atlanta, Georgia The gap in measles vaccine coverage between white and nonwhite children was as large as 18% in During the measles epidemic of , attack rates among nonwhite children!5 years of age were 4- to 7-fold higher than rates among white children. Because of the epidemic and of the known disparity in vaccine coverage and risk of disease, a dual strategy to eliminate measles in the United States was implemented: universal interventions likely to reach the majority of children and targeted interventions more likely to reach nonwhite children. In 1992, the gap in coverage between white and nonwhite children was reduced to 6% (from 15% in 1985); the risk of disease among nonwhite children was narrowed to 4-fold the risk of white children. During the 1990s, further implementation of the dual strategy resulted in narrowing the gap in vaccine coverage to 2% and elimination of endemic disease in all racial and ethnic populations. This dual strategy deserves close scrutiny by health professionals and policy makers in devising programs to meet the Healthy People 2010 objectives for the elimination of other health disparities. There has been a longstanding disparity between the levels of vaccine coverage among white children compared with that among children in racial and ethnic minority populations in the United States [1] (Centers for Disease Control and Prevention [CDC], unpublished data). The creation of the federal immunization grant program in 1963 to provide assistance to states in purchasing and delivering vaccines was justified, in part, as an effort to bring about greater equity in the receipt of the new oral polio vaccine, which had just been licensed in the United States in 1961 [2]. Since it was first created 40 years ago, the federal program has sought to address the disparity in vaccine coverage between white and nonwhite children. Throughout the 1970s and through the mid-1980s when coverage data were first routinely collected, the gap in vaccine coverage for 3 doses of diphtheria tetanus toxoids Reprints or correspondence: Dr. Sonja S. Hutchins, National Immunization Program, Mailstop E-61, Centers for Disease Control and Prevention, 1600 Clifton Road, Atlanta, GA (ssh1@cdc.gov). The Journal of Infectious Diseases 2004; 189:S This article is in the public domain, and no copyright is claimed /2004/18906S1-00XX pertussis or polio vaccines ranged from 12% to 26% and averaged 20% during this multiyear period (CDC, unpublished data). Throughout the same period, the gap in measles or measles-mumps-rubella vaccine coverage ranged from 10% to 18% and averaged 14% [1] (CDC, unpublished data). Routine measurement of vaccine coverage at the national level was temporarily halted in 1985, just before the large measles epidemic of [3], and was not reinstituted until the end of the epidemic in Therefore, the gap of 15% in 1985 [1] (CDC, unpublished data) is taken to be the best baseline estimate of the difference in vaccine coverage between white and nonwhite populations before the changes in vaccination activities started during the epidemic. During the epidemic, which produced 155,000 cases, the incidence of measles in nonwhite children was 4- to 7-fold higher than the incidence in white children [4]. This epidemic created widespread and unprecedented concern that the nation s immunization system was deficient, and a national initiative to improve the immunization delivery system was launched [5, 6]. Simultaneously, the initiative declared specific diseasereduction goals to be reached before 2000 for a variety Racial and Ethnic Disparities in Measles JID 2004:189 (Suppl 1) S000

2 Table 1. Summary of interventions and their impact on childhood vaccination and elimination of indigenous measles from the United States, Intervention Universal Second dose of measles vaccine Presidential priority Increased funding for health departments Immunization action plans Annual state survey of vaccine coverage Extra funds for state immunization programs New Standards for Pediatric Immunization Practices Quality improvement activities (AFIX) in clinics Assessments of vaccine coverage (HEDIS) in MCOs State-based immunization registries of children State-based coalitions of organizations Partnerships with national health organizations Research National public information campaigns Enforcement of laws/regulations for childcare centers Targeted Vaccines for Children program Extra funding for urban-area health departments a Annual assessment of vaccine coverage Local immunization action plans Linkage of WIC and immunization activities Discounted vaccine prices for Medicaid programs Higher reimbursement rates for Medicaid providers Quality improvement (AFIX) in public clinics More user-friendly hours for public clinics Partnerships with minority health organizations Special information campaigns Impact Reduced vaccine failures Increased attention and funding for childhood vaccinations Strengthened immunization activities Guided state immunization programs Measured state coverage of 19- to 35-month-old children Provided financial incentives for above-average performance Improved vaccination services at the point of delivery Raised immunization coverage Stimulated improvements in coverage through measurement Tracked and measured vaccination status Strengthened and extended existing immunization programs Promoted and maintained immunizations as a priority Tested interventions/found reasons for low vaccine coverage Improved knowledge of the benefits of vaccination Achieved high vaccine coverage in childcare centers Entitled uninsured or underinsured children to free vaccine Improved vaccine coverage of children in 28 urban areas Measured vaccine coverage in the same 28 urban areas Guided immunization programs in the 28 urban areas Screened 40% of all US births for immunization b Enabled Medicaid programs to vaccinate Increased the number of Medicaid providers Raised immunization coverage for low-income children Enabled access to vaccination services of low-income children Promoted and maintained immunizations as a priority Improved knowledge of Spanish-speaking populations NOTE. AFIX, Assessment, Feedback, Incentives, and exchange of information; HEDIS, Health Plan Employer Data and Information Set; MCO, managed care organization; WIC, Special Supplemental Nutrition Program for Women, Infants, and Children. a With at least 50% minority populations. b Screens US births enrolled in WIC and refers eligible children for vaccination. of vaccine-preventable diseases, including a renewal of the commitment first enunciated in 1966 and repeated in 1978, to eliminate indigenous transmission of measles in the United States [6, 7]. As part of this initiative, and because of the longstanding disparity in vaccine coverage among children of different racial and ethnic backgrounds, a dual immunization strategy was developed with interventions likely to reach the majority of children (e.g., new National Standards for Pediatric Immunization Practices distributed to all providers and others) and additional interventions more likely to reach subgroups of the population with higher proportions of children from racial and ethnic minority groups (e.g., the Vaccines for Children Program, entitling free vaccine for uninsured or underinsured children) [1]. At the same time, outbreak control and enhanced surveillance activities were initiated to respond more effectively to disease occurrence [8]. Here we examine the impact of the dual strategy in eliminating measles and the longstanding gap in measles vaccine coverage between children of different racial and ethnic minority groups in the United States. METHODS Description of the dual strategy. The dual strategy was a multicomponent set of interventions consisting of universal and targeted activities to improve vaccine coverage for measles and other vaccine-preventable diseases (table 1). Some of these interventions were applied as temporary measures during the measles epidemic in , and others were developed S000 JID 2004:189 (Suppl 1) Hutchins et al.

3 later in an ongoing manner as part of the Infant Immunization Initiative from and subsequently as part of the 1993 Childhood Immunization Initiative (table 1) [6, 9 21]. Estimates of measles vaccine coverage. To assess the impact of the dual strategy on measles vaccine coverage, the annual number of doses distributed and results of 4 types of surveys were used: the United States Immunization Survey (USIS), the National Health Interview Survey (NHIS), the National Immunization Survey (NIS), and retrospective school entrant surveys. Each of these surveys used different methods to assess coverage among preschool children of various ages. Although a comparison of estimates from these data would not be entirely valid because the surveys had different methods, it is possible to use these data to evaluate trends in vaccine coverage and to estimate vaccine coverage between subgroups within a survey [3]. The USIS began in 1959 and was conducted by the Bureau of the Census as an area-probability household survey [3]. The survey was changed in 1971 to become a telephone survey through The survey collected information on coverage with measles vaccine from 1964 through 1985 and on race from 1970 through The survey also collected information about age, poverty status, and whether the child lived in a central city area of a standard metropolitan statistical area. All data were reported by parents, and vaccination histories were reported from memory or from vaccination records kept in the home. The NHIS, including the Child Health Supplement, began in 1991 and was conducted by the CDC s National Center for Health Statistics [3, 22]. The NHIS is a household survey that targets US noninstitutionalized civilians to collect information about health status, use of medical care, and related topics. As a component of the Child Health Supplement, vaccination history was collected. In 1992 and 1993, vaccination history was obtained from parental recall or vaccination records for children!6 years of age. In 1994, the age group included any child in the home who was months of age, and the National Immunization Provider Record Check Survey (NIPRCS) was added to the survey. The NIPRCS requested immunization histories of surveyed children from health care providers. In 1997, the age range was changed to include children months of age. The NIS began in 1994 and continues today to monitor immunization levels of preschool-aged children [3, 23]. The NIS is a national random digit dialing telephone survey that collects vaccination information on children months of age. Immunization providers of participating children are contacted for vaccination histories, after parental consent has been granted. In addition to coverage estimates for white and black children, the NIS provides estimates for Hispanic, American Indian/Alaska Native, and Asian/Pacific Islander children. The NIS is the most current and widespread estimate of vaccine coverage because data are collected to provide quarterly national estimates in addition to annual estimates at the national, state, and 28 urban-area levels. The previous surveys provide only national and regional estimates. In response to the measles resurgence, retrospective surveys of school entrants were performed to provide an easy, inexpensive, and valid estimate of vaccine coverage for children by their second birthday [3, 24]. The goal was to assess retrospectively children s vaccination history as of their second birthday. During the school years, retrospective surveys of school entrants were conducted as described elsewhere [3, 24]. State and local immunization program grantees performed a multistage cluster survey of school vaccination records of kindergarten or first-grade children enrolled in school. Children in surveys conducted during were 2 years of age during Estimates of measles incidence. To assess the impact of the dual strategy on measles incidence, the number of reported measles cases was examined. Each week, states report confirmed cases of measles to the National Notifiable Disease Surveillance System (NNDSS) at the CDC [25]. A confirmed case of measles was laboratory-confirmed or met the Council of State and Territorial Epidemiologists standard clinical case definition (generalized maculopapular rash, fever, and cough, conjunctivitis, or coryza) and was epidemiologically linked to a laboratoryconfirmed case or another case meeting the clinical case definition [25]. In 1996, the confirmed case definition was modified to exclude clinical cases that were only epidemiologically linked to a clinical case and to include laboratory-confirmed cases that did not meet the clinical case definition [26]. Information for measles cases is reported by state health departments to the NNDSS through the National Electronic Telecommunications System for Surveillance. Case information includes date of rash onset, source of transmission, race and ethnicity (since 1991), age, sex, and vaccination status. Race and ethnicity information is usually self-reported or assigned by case investigators. The Census Bureau definitions were used (e.g., non-hispanic white, non-hispanic black, Hispanic, American Indian/Alaska Native, and Asian/Pacific Islander), and references to black and white populations in this article were equivalent to the Census Bureau definitions for non-hispanic black and non-hispanic white. Each state and territory has regulations and or laws governing the reporting of measles by health care providers, hospitals, laboratories, schools, day care facilities, and other institutions. During the measles resurgence, national surveillance of measles by race and ethnicity was available only for the last year (1991). Before that time, reports of measles incidence by race and ethnicity were provided by large urban areas during epidemics. Only two-thirds of states reported measles cases by race and ethnicity to the NNDSS in Annual measles incidence by race and ethnicity was computed for 1991 by dividing the total number of confirmed race- and ethnicity- Racial and Ethnic Disparities in Measles JID 2004:189 (Suppl 1) S000

4 specific cases of measles reported to the NNDSS in 1991 by the estimated annual racial and ethnic populations of the United States in Incidence is reported per 100,000 population. We do not account for underreporting. Differences of underreporting by racial and ethnic minority populations are not clear. After the epidemic, from 1992 through 2001, the annual incidence of measles by race and ethnicity was also examined. During this period, race and ethnicity were reported to the NNDSS for 80% of patients with measles. Annual incidence was computed by dividing the total number of race- and ethnicity-specific confirmed cases of measles reported to the NNDSS each year by the estimated annual racial and ethnic population of the United States for the respective year. Measles incidence was reported per 100,000 population. RESULTS Implementation of the dual strategy. All of the universal and targeted interventions described in table 1 were implemented, albeit at different times and with different degrees of resources and intensity during the measles epidemic and the subsequent decade. Measles vaccine coverage. During the peak of the measles epidemic in 1990, 19 million doses of measles vaccine were distributed [7]. This was nearly a 4-fold increase over the annual average of 5 million doses during , before the epidemic. The number of doses distributed annually has stabilized at 14 million doses during , because the second dose of measles vaccine has been recommended for all children enrolled in schools and colleges and for health care workers. In addition, since 1980, vaccine coverage with at least a single dose of measles vaccine has been 195% at school entry [7]. Before the measles epidemic, measles vaccine coverage among children 1 4 years of age during in the USIS was 61% 64% (figure 1). This vaccine coverage was similar for children at the second birthday [3]. To assess vaccine coverage just before and during the first year of the epidemic, retrospective surveys of school entrants at their second birthday were used. In 1988 and 1989, measles vaccination coverage at the second birthday was an average of 70% 72% in the population of school entrants surveyed in states; no data were available by race and ethnicity (figure 1). By 1991, vaccine coverage of children aged months, measured by NHIS, was 82% (figure 1). By 1992, vaccine coverage was 84% for white children and 78% for nonwhite children (figure 2). From that point forward, measles vaccine coverage of preschool children increased from 83% (among children years of age in the NHIS) in 1992 to 92% (among children months of age in the NIS) in 2000 (figure 1). The immunization gap in vaccine coverage between white Figure 1. Measles vaccine coverage, United States, USIS, United States Immunization Survey (children aged 1 4 years and 24 months [ ]); RS, Retrospective Survey (vaccination at 24 months of age for children in kindergarten or first grade); NHIS, National Health Interview Survey (children aged months); and NIS, National Immunization Survey (children aged months). and nonwhite children (mostly black children) of up to 18% during the 1970s and 1980s virtually disappeared by the later 1990s (figure 2). Before the epidemic, in 1985, the immunization gap was an estimated 15%; vaccine coverage for nonwhite children was 49%, compared with coverage for white children of 64% [1] (CDC, unpublished data). After the epidemic in 1992, vaccine coverage was 78% for nonwhite children and 84% for white children, a gap of 6%. As vaccine coverage continued to increase for all racial and ethnic groups during the 1990s, the immunization gap narrowed to 1% 2% by 1996 (figure 3) [23]. By 1997, 89% of black children months of age, 88% of Hispanic children, 92% of American Indian/ Alaska Native children, and 90% of white and Asian/Pacific Islander children had received 1 dose of a measles-containing vaccine (figure 3). Since 1997, measles vaccine coverage has been sustained at 90% for both white and racial and ethnic minority children, and in 2001, coverage was 89% for black, 92% for Hispanic, 92% for white, 94% for American Indian/ Alaska Native, and 90% for Asian/Pacific Islander children. The confidence limits of the point estimates were narrow, from 1% to 4% [23]. Measles incidence. During the measles epidemic, the number of confirmed reported measles cases was 18,193 in 1989, 27,786 in 1990, and 9643 in The largest outbreaks primarily affected unvaccinated black and Hispanic children in large cities (e.g., Chicago, Dallas, Houston, Los Angeles, Milwaukee, and New York), constituting up to 82% of cases in an outbreak [4]. Nationally, although black and Hispanic populations represented 17% of the total US population during the epidemic, they accounted for 46% of reported measles cases and 66% of all cases in preschool children aged!5 years [5]. During the final year of the measles epidemic, in 1991, mea- S000 JID 2004:189 (Suppl 1) Hutchins et al.

5 Figure 2. Measles vaccine coverage among preschool-aged children in the United States by selected race/ethnicity and year, USIS, United States Immunization Survey (children aged 1 4 years); NHIS, National Health Interview Survey (children aged months); NIS, National Immunization Survey (children aged months). sles incidence in American Indian/Alaska Native populations (16.3 cases/100,000 population), the Hispanic population (8.7 cases/100,000 population), and the black population (3.6 cases/ 100,000 population) was 3- to 16-fold higher than the incidence in the white population (1.4 cases/100,000 population) or in the Asian/Pacific Islander population (1.3 cases/100,000 population) (figure 4). During , the overall incidence of measles markedly declined, from 2237 total reported cases (0.88 cases/100,000 population) in 1992 to 86 cases (0.03 cases/100,000 population) in 2000; since then, 100 cases or fewer were reported (116 cases [0.04 cases/100,000 population] in 2001 and 42 cases [0.02 cases/100,000 population] in 2002). The incidence of measles among racial and ethnic minority populations reached record Figure 3. Measles vaccine coverage among preschool-aged children in the United States by selected race/ethnicity and year, National Immunization Survey (NIS), NA, American Indian/Alaska Native; API, Asian/Pacific Islander. low levels by 1992 (between 0.2 and 2.8 cases/100,000 population) (figure 4). Moreover, compared with the measles incidence among whites (0.09 cases/100,000 population), disparities in measles incidence for all racial and ethnic minority populations ( /100,000 population) essentially disappeared by Measles incidence reached a record low level of 312 cases in Record low levels of measles cases have been sustained to the present [27]. An expert panel, convened in 2000, concluded that measles is no longer endemic in the United States [28]. DISCUSSION The elimination of endemic measles in the United States and the closing of a longstanding gap in measles vaccine coverage for racial and ethnic minority populations are landmark public health achievements [29, 30]. We conclude that universal and targeted interventions (a dual strategy) have been responsible for eliminating disparities in measles vaccine coverage and measles incidence between racial and ethnic minority populations in the United States. Although the disease elimination goal has received the most attention, the achievement of equity or near equity in measles vaccine coverage is an achievement in health service delivery of notable importance [31]. The fact that endemic measles has been eliminated from the United States is well established on the basis of surveillance of disease, vaccine coverage, and serological data reviewed by an expert committee [28]. Also, the absence of endemic disease has been continuously sustained for at least 6 years. Race and ethnicity were underreported in 1991 for a substantial proportion (one-third) of measles case patients, and measles incidence by race and ethnicity may be biased for that year; however, subsequent secular trends in race- and ethnic-specific Racial and Ethnic Disparities in Measles JID 2004:189 (Suppl 1) S000

6 Figure 4. Measles incidence in the United States by selected race/ethnicity and year, NA, American Indian/Alaska Native; API, Asian/ Pacific Islander. measles incidence are likely to be valid, because race and ethnicity have been reported for 180% of patients with measles. Although our ability to accurately assess changes in vaccine coverage over time is limited because of different survey methods, the finding of equivalence or near equivalence across racial and ethnic populations from 1996 to 2001 appears valid because estimates were derived from a single survey [23]. This survey used the same methods in all populations. What is less certain is the historical size of the gap, because the gap in previous years was determined by surveys different from that used in the late 1990s. Despite these methodological differences, all methods used before the late 1990s have always found a gap ranging from as little as 6% to as large as 18%. Although it is not possible to estimate precisely the magnitude of the gap that has been closed, it seems unlikely that the gap prior to the 1990s was!10%. Our best estimate based on the USIS data is that the gap was 15% before the major measles epidemic. Assuming that a 15% gap has been reduced and that minority children are now being vaccinated at essentially the same level as in the delivery systems serving the majority population, this translates into an estimated 400,000 minority children 2 years of age being protected earlier or on schedule in the United States each year. These children obtain a total of 1 million (3 4 years per child) extra years of protection against measles as a result of the earlier immunization. Protection against measles through vaccination is known to be cost-beneficial [32, 33]. Because the dual strategy used to achieve these goals contained a number of interventions, it is not possible to isolate which single intervention or combination of interventions was most responsible for the success. What seems plausible is that the gap in coverage would not have been closed without interventions that sought specifically to have greater impact, or to catch up, racial and ethnic minority populations. The contrary may also be correct that a strategy targeted only at catching up minority populations without emphasis on raising overall vaccine coverage for all children would not have succeeded. Put another way, equity was achieved not at the low overall immunization levels that predominated for everyone in a suboptimally performing delivery system prior to the epidemic but at the higher levels of an excellently performing delivery system characteristic of the 1990s. Although it is not possible to single out any interventions for their role in the success achieved, the overall program implemented a conceptual model that was effective and was based on core components of the PRECEDE model [34]. This model assumed that predisposing, enabling, and reinforcing activities had to be implemented to achieve desired goals, and several of the interventions noted in table 1 fell into these categories. For example, predisposing factors included the measles resurgence that led to childhood immunization becoming a priority of the president and the availability of national funding to improve childhood immunization and to control the measles epidemic [13]. An enabling factor was an effective strategy for eliminating measles that was based on scientific evidence and introduced a second dose coupled with the Vaccines for Children program. A reinforcing factor was setting national vaccine coverage and disease targets at 2-year intervals and closely monitoring these goals through annual assessments of vaccine coverage at national, state, and local levels through surveys and immunization registries. Although this program was successful in eliminating measles and disparities in vaccine coverage and disease, the program has to be vigilant, because each year nearly 4 million children are born in the United States, requiring 7 9 vaccines and vaccine doses by school entry. As more vaccines are added to the childhood vaccination schedule, closing of the immunization gap becomes more of a challenge. In addition, disparities exist in influenza and pneumococcal vaccine coverage S000 JID 2004:189 (Suppl 1) Hutchins et al.

7 among adults. Thus, the nation has to continue to improve on current immunization activities. This is the first systematic evaluation of a prevention program and its impact over several decades on the elimination of racial and ethnic disparities in health. Intensive, decade-long efforts to eliminate measles and improve childhood vaccination provide hope that we may be able to achieve similar successes in other areas by the year In fact, Healthy People 2010, the nation s health agenda, already calls for a dual strategy [35]. The first goal is to optimize the health of all by increasing the quality and years of healthy life. The second goal is not to leave anyone behind, by eliminating health disparities. A prevention program that has achieved health equity for racial and ethnic minority populations, such as the childhood immunization program, provides more specific and tested ideas for eliminating health disparities for other conditions and health care services. 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