American Journal of Epidemiology Advance Access originally published online on January 27, 2006
American Journal of Epidemiology 2006 163(6):571-578; doi:10.1093/aje/kwj086
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Original Contribution |
Racial and Ethnic Disparities in Influenza Vaccination Coverage among Adults during the 2004–2005 Season
1 National Center for Chronic Disease Prevention and Health Promotion, Centers for Disease Control and Prevention, Atlanta, GA
2 National Immunization Program, Centers for Disease Control and Prevention, Atlanta, GA
Correspondence to Dr. Michael W. Link, Centers for Disease Control and Prevention, 4770 Buford Highway NE, K-66, Atlanta, GA 30341 (e-mail: MLink{at}cdc.gov).
Received for publication September 23, 2005. Accepted for publication December 28, 2005.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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During the 2004–2005 influenza season, the supply of vaccine to the United States was significantly reduced. In response, the Centers for Disease Control and Prevention and the Advisory Committee on Immunization Practices issued interim recommendations for prioritizing vaccination. Given trends in racial/ethnic disparities in vaccination for influenza, the authors assessed the impact of the shortage on those historically less likely to be vaccinated. Using data from the Behavioral Risk Factor Surveillance System, they considered vaccination coverage among those non-Hispanic Whites, non-Hispanic Blacks, and Hispanics who had priority for being vaccinated during the 2004–2005 influenza season. The vaccine shortage had a significant negative effect on coverage among adults aged 65 years or older across the three racial/ethnic groups. Yet, the magnitude of the disparities in coverage did not change significantly from previous seasons. This finding may imply similar patterns of vaccine-seeking behavior during shortage and nonshortage years. No racial/ethnic differences were seen among adults aged 18–64 years, which likely reflects the higher percentage of health-care workers in this age group. Yearly monitoring of influenza vaccine coverage is important to assess the long-term impact of shortages on overall coverage and gaps in coverage between racial/ethnic groups.
Behavioral Risk Factor Surveillance System; continental population groups; ethnic groups; immunization; influenza, human; public health
Abbreviations: ACIP, Advisory Committee on Immunization Practices; BRFSS, Behavioral Risk Factor Surveillance System; CI, confidence interval
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Influenza contributes to approximately 36,000 deaths per year in the United States (1
). Seasonal vaccination can substantially reduce the risk of mortality and morbidity associated with this disease, particularly among the elderly and those with chronic conditions who are most at risk for secondary infections (2–4). Research shows significant racial/ethnic disparities in coverage for influenza vaccine among adults, even among high-risk groups, with non-Hispanic Blacks and Hispanics being less likely than non-Hispanic Whites to be vaccinated (5–13). Differences in coverage by race/ethnicity have been observed even among those most likely to be vaccinated (e.g., persons of higher educational attainment and those who visit health-care providers frequently) (6). Gaps in coverage are long-standing and likely result from a combination of factors, including differences in sociodemographic characteristics, in the attitudes of patients and providers toward vaccination, in awareness of recommendations, and in systems used in clinics serving different patient populations (14–16).
On October 5, 2004, a major manufacturer of inactivated influenza vaccine announced that, because of production problems, none of the vaccine it was expected to produce would be available for distribution in the United States during the 2004–2005 influenza season. The result was that the US supply of influenza vaccine was cut nearly in half. The situation prompted the Centers for Disease Control and Prevention and the Advisory Committee on Immunization Practices (ACIP) to issue interim recommendations that certain groups be given priority for inactivated influenza vaccine: those at high risk of influenza-related complications, including all persons aged 65 years or older; and certain contacts of high-risk persons, including health-care workers and household contacts of children less than age 6 months. Persons not in the priority groups were asked to forego or defer vaccination for the 2004–2005 influenza season (17). Given the substantial racial/ethnic disparities in vaccination seen in previous seasons, we assessed the impact of the shortage of vaccine on those who have been historically less likely to be vaccinated.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Using data from the Behavioral Risk Factor Surveillance System (BRFSS) collected by the 50 US states and the District of Columbia, we assessed vaccination coverage across racial/ethnic groups among adults prioritized to be vaccinated during the 2004–2005 influenza season. BRFSS is a cross-sectional telephone survey conducted by the state health departments, with assistance from the Centers for Disease Control and Prevention, that uses random digit dialing to select a representative sample from each state's noninstitutionalized civilian population aged 18 years or older (18
). For this assessment, we limited our focus to racial/ethnic disparities in vaccination coverage among adults in ACIP-defined priority groups only. First, to provide a historical context, we looked at trends in coverage from the 2000–2001 through 2004–2005 influenza seasons. Before November 1, 2004, reports of inactivated influenza vaccination among adults were assessed in the BRFSS with a single question: "Have you had a flu shot in the past 12 months?" Thus, no information was collected on the specific month of vaccination. Because responses to this question often show seasonal effects (with more positive responses during the winter months and fewer during the summer), we examined responses for only those interviewed in the first quarter (January–March) of each year from 2001 through 2005—the time frame just after the period when most people receive their yearly vaccinations. Looking at information from only these 3 months also minimized the likelihood that a respondent would reference the previous influenza season in responding to the question. Trend analyses were limited to those aged 65 years or older because this was the only ACIP-defined priority group that could be identified with the information collected by BRFSS in each of the 5 years.
In addition, to closely monitor the 2004–2005 shortage as it unfolded, on November 1, 2004, new questions were temporarily added to the BRFSS to supplement the single question on receipt of inactivated influenza vaccine in the preceding 12 months. The intent was to obtain more precise information on vaccine use for all persons aged 6 months or older, including month and year of vaccination, whether the respondent was in one of the ACIP's priority groups for that season (persons aged 
65 years or 6–23 months; health-care workers with patient contact; high-risk persons aged 2–64 years, including pregnant women; and adult household contacts of infants aged <6 months), and the main reason for not being vaccinated. Adults were considered high risk if they had diabetes, asthma or other lung disease, heart disease, a weakened immune system, kidney disease, sickle cell anemia, or other anemia.
Several milestones during the 2004–2005 season needed to be considered in structuring the analysis. By early December 2004, it was clear that many of those persons recommended to receive vaccination had not been vaccinated (19). Later in December 2004, ACIP expanded its recommendations to include all adults aged 50 years or older. To capture the changing dynamics of the 2004–2005 season, we examined vaccination coverage at two points in time: through November 30, 2004, and through January 31, 2005. Thus, the first inspection was just before the ACIP revised its recommendations in December, and the last was toward the end of the season after the vast majority of vaccinations had occurred and vaccine was still available (20).
We also conducted two logistic regression analyses, one for adults aged 18–64 years and the other for those aged 65 years or older. We thought that the mechanisms driving disparities by race/ethnicity might differ significantly between these two age groups. For instance, although all of those aged 65 years or older were included in the ACIP priority groups, among adults aged 18–64 years, only those who met certain criteria (such as being a health-care worker with patient contact or having a chronic condition) were included. Conversely, younger adults were more likely than older adults to be health-care workers. They were also less likely to have some form of health-care coverage.
Data for logistic regression analyses were collected through the BRFSS and included race, Hispanic ethnicity, sex, age, education, chronic-condition status, employment as a health-care worker, and having health-care coverage, such as health insurance, a prepaid plan such as a health maintenance organization, or a government plan such as Medicare or Medicaid. To account for the potential impact of vaccine supply, the regression analyses also included state-level supply variables that reflected the ratio of the number of vaccine doses distributed to a state to the estimated number of vaccine-priority adults (as defined by ACIP) in the state. For the calculations, we used vaccine orders placed directly with the vaccine manufacturer and doses ordered through the Centers for Disease Control and Prevention. The first variable accounted for supply when the shortage was announced (October 5, 2004), and the second reflected state supplies as of February 2, 2005. The former was used to analyze vaccination rates for early in the season (i.e., through November 30, 2004), while the second was used to analyze coverage through January 31, 2005. The supply variables provided only rough estimates of the amount of vaccine available for vaccine-priority adults; we used ordering data and did not have exact figures for the number of doses distributed, when those doses were distributed, or if and how they were used. Available data on the distribution of inactivated influenza vaccine included the number of doses shipped by zip code, but information on secondary distribution of vaccine beyond the zip code for the initial shipping address was not available.
All estimates presented here were adjusted to account for differential probabilities in being selected, the age and sex distribution of the adult population, and the size of the adult population in each state. SPSS version 13 software with the Complex Samples module was used in the analyses to account for the complex sampling design and to calculate the 95 percent confidence intervals (21).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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For the trend analyses, the number of completed interviews conducted with those aged 65 years or older in each of the quarters examined ranged from 9,024 for the 2001–2002 season to 15,758 for the 2003–2004 season. The median state-level Council of American Survey Research Organizations response rates across this period ranged from 52.7 percent in 2004–2005 to 58.3 percent in 2001–2002 (22
). The 4 months of data collected to assess vaccination coverage during the 2004–2005 influenza season included 45,920 completed interviews with adults in priority groups, with a median state-level response rate of 54.4 percent.
Trends in receipt of influenza vaccination, 2000–2001 to 2004–2005
For all three racial/ethnic groups (White non-Hispanic, Black non-Hispanic, Hispanic), the estimated percentage of adults aged 65 years or older who received influenza vaccine in the previous 12 months was lower for 2004–2005 than for any of the earlier time frames assessed (table 1). For non-Hispanic Whites, the percentage for 2004–2005 (66.0 percent) was significantly lower than that for any of the previous periods. For non-Hispanic Blacks and Hispanics, the estimates for 2004–2005 (43.1 percent and 52.5 percent, respectively) were lower than those in 2000–2001, but the differences across the years were not statistically significant.
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In terms of disparities by race/ethnicity, for all five periods, the rates for non-Hispanic Whites were higher than those for Blacks among adults aged 65 years or older (table 1). For example, for 2004–2005, the gap between this group and non-Hispanic Blacks was 22.9 percentage points, similar to the gap observed in the 2000–2001 season (23.4 percentage points). Differences between non-Hispanic Whites and Hispanics were not as wide, and they were statistically significant in only 3 of the 5 years (2000–2001, 2003–2004, 2004–2005), with the difference of 13.5 percentage points in 2004–2005 being the largest gap observed.
The absolute percentage decrease from the 2003–2004 to 2004–2005 seasons for each group was quite similar and was not statistically different, however. The decline in the percentage vaccinated was 10.5 percent for Whites (2003–2004 = 76.5 percent, 2004–2005 = 66.0 percent), 12.9 percent for Blacks (2003–2004 = 56.0 percent, 2004–2005 = 43.1 percent), and 14.1 percent for Hispanics (2003–2004 = 66.6 percent, 2004–2005 = 52.5 percent).
Vaccination coverage by month for 2004–2005
During the 2004–2005 influenza season, as noted, the supply of vaccine was significantly lower than originally anticipated. Gaps in coverage by race/ethnicity began early in the season, particularly among those aged 65 years or older (table 2). Disparities by race/ethnicity among vaccine-priority adults differed somewhat by age. For persons aged 65 years or older, coverage at the end of October 2004 was 28.0 percent for Whites, 15.7 percent for Blacks, and 17.9 percent for Hispanics; at the end of January 2005, there were still large differences, with estimates for that point of 63.6 percent, 44.4 percent, and 45.1 percent, respectively.
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In contrast, among vaccine-priority adults aged 18–64 years, significant differences in coverage were seen between non-Hispanic Whites and Blacks at the end of October, November, and December; however, at the end of January, the two groups did not differ statistically (29.2 percent for Whites, 22.0 percent for Blacks). For Hispanics aged 18–64 years, coverage rates did not differ significantly from those for Whites at any of the time points. At the end of January 2005, coverage for Hispanics (22.6 percent) and Blacks (22.0 percent) did not differ significantly.
Factors related to 2004–2005 coverage among vaccine-priority adults
Using logistic regression analyses, we found that, among vaccine-priority adults aged 65 years or older, race/ethnicity significantly affected coverage both at midseason (November 30, 2004) and near season's end (January 31, 2005) (table 3). As of midseason, the odds that Blacks had been vaccinated were 63 percent lower than those for Whites, while the odds for Hispanics and Whites did not differ statistically. Having insurance, being older (aged 75 years), having a chronic condition, and having at least a high school education were also positively related to coverage at this point. Supply of vaccine also had a significant effect: coverage was significantly higher in states where the supply was better.
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When Whites were used as a referent group, the odds of vaccination were 52 percent lower for Blacks and 42 percent lower for Hispanics by the end of January 2005 (table 3). Again, age, education, and having a chronic condition were positively related to coverage, but having health insurance was not. The supply of vaccine had an impact; for example, in states where the estimated ratio of doses to vaccine-priority adults was 75:100 or greater, the odds of coverage were almost twice as great as in states where this ratio was below 50:100.
Race/ethnicity had no apparent impact on season-end vaccination rates for vaccine-priority adults aged 18–64 years (data not shown). Having insurance, being aged 50–64 (vs. 18–49) years, and being a health-care worker were all related to increased likelihood of vaccination; men had significantly lower odds than women did. Where the ratio of doses to vaccine-priority adults was 75:100 or greater, the odds of vaccination were more than twice as great as in states where this ratio was below 50:100.
Reasons for not being vaccinated
As noted earlier, respondents who indicated that they had not received a vaccination during the 2004–2005 season were asked why they had not been vaccinated. Among those interviewed in November 2004, the pattern of reasons was generally similar by race/ethnicity (data not shown). However, Blacks were less likely than Whites to have tried to get vaccinated but could not: 17.1 percent (95 percent confidence interval (CI): 12.7, 22.8 percent) versus 25.3 percent (95 percent CI: 23.6, 27.1 percent). Blacks were also more likely than Whites to have some concerns about the vaccine: 13.7 percent (95 percent CI: 9.6, 19.2 percent) versus 8.0 percent (95 percent CI: 6.9, 9.2 percent).
On the basis of February 2005 interviews, Blacks were less likely than Whites to think that they were saving vaccine for others by not being vaccinated—3.3 percent (95 percent CI: 1.9, 5.8 percent) vs. 9.5 percent (95 percent CI: 8.1, 11.1 percent)—and to say that they tried to get vaccinated but could not—11.3 percent (95 percent CI: 8.2, 15.4 percent) versus 18.2 percent (95 percent CI: 16.3, 20.3 percent) (data not shown). Similarly, the percentage of Hispanics who had tried but failed to get vaccinated—7.9 percent (95 percent CI: 4.3, 13.9 percent)—was significantly lower than that for Whites.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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While coverage for influenza vaccination increased across the 2000–2001 to 2003–2004 seasons among those aged 65 years or older in the three racial/ethnic groups we examined, the very large reduction in available vaccine during the 2004–2005 season led to a decline in rates to levels on par with or below those for the 2000–2001 season, another period during which the supply of vaccine was constrained (1
). Significant disparities by race/ethnicity were seen in all the years studied. In 2004–2005, we found coverage rates for both Blacks and Hispanics that were significantly below those for Whites. However, the absolute percentage decrease from the 2003–2004 to 2004–2005 seasons for each group was quite similar and not statistically different. Although the smaller sample sizes for Blacks and Hispanics may have limited our ability to detect statistically significant differences across these groups, the percentages from a programmatic standpoint are not dramatically different either. It appears, therefore, that the vaccine shortage led to a rather uniform absolute decline in vaccination rates across these three groups.
These patterns in disparities could reflect differences between these groups in several areas. For example, a study of Medicare beneficiaries found that Blacks were less likely than Whites and Hispanics to visit a physician solely to be vaccinated (23). Another study found that Blacks were less likely than Whites and Hispanics to receive their influenza vaccination in a nonmedical setting, such as a pharmacy or drug store or workplace (16). In the current study, we found that both Blacks and Hispanics were less likely than Whites to have tried but failed to be vaccinated. Perhaps these findings speak to differential levels of motivation, but more research is needed on vaccination behaviors before this possibility can be concluded. However, we might expect that, if Whites were more motivated or better informed about the shortage, we would have seen larger declines in the absolute percentages of Blacks and Hispanics who were vaccinated and an increase in the magnitude of the gaps between racial/ethnic groups during the shortage season. Likewise, if physicians or clinics that primarily serve Black and Hispanic patients had greater difficulty obtaining supplies of vaccine compared with those vaccinating primarily White patients, we would also expect to see an increase in the size of the gaps between groups. Yet, neither the absolute decline in rates from 2003–2004 to 2004–2005 for Blacks and Hispanics as compared with Whites nor the size of the gaps in vaccination across groups increased appreciably. Why?
Having monthly data for the 2004–2005 influenza season provided some interesting insights. We found that, on October 31, 2004, just 26 days after the manufacturer's announcement about its inability to produce vaccine, coverage among Blacks aged 65 years or older was only half that for Whites, with the rate for Hispanics slightly higher than that for Blacks. By January 31, 2005, coverage among Blacks and Hispanics increased substantially from the earlier date, but, even so, coverage for them was still far below that for Whites. Because similar data are not available for past years, we do not know whether the pattern of vaccination for each of these groups differs from the norm. However, if vaccine-seeking behaviors are similar during vaccine shortage and nonshortage years and the amount of available vaccine is reduced across all areas (not just those with higher concentrations of minorities) during a shortage year, then we might expect to see the pattern demonstrated during the 2004–2005 season. That is, a decrease in the percentage of persons who were vaccinated across all three groups but a gap in coverage levels that remains relatively consistent from previous seasons. A further mitigating factor may have been the high visibility of the vaccine shortage, which we could speculate sensitized clinicians and public health practitioners to these disparities, motivating them to make an extra effort to vaccinate minorities to the extent possible. This factor would have reduced the level of decline in vaccination levels that might have otherwise occurred among Blacks and Hispanics. However, data beyond those collected for this study are required to explore this hypothesis more fully.
Although we found disparities among older adults by race/ethnicity, this was not the case for adults aged 18–64 years. By the end of January 2005, coverage rates for those aged 18–64 years were statistically equivalent across the three groups. Among those aged 18–64 years, the probability of being vaccinated during the 2004–2005 season seemed to be less a function of race/ethnicity and more attributable to better vaccine supply, employment as a health-care worker, having insurance, and being relatively older within this group (i.e., aged 50–64 years). Research on racial/ethnic differences among vaccine-priority adults in this younger age range is sparser than is the literature for those aged 65 years or older. One study focusing on high-risk adults aged 18–64 years reported significant racial differences between Whites and Blacks with diabetes, chronic heart conditions, and chronic obstructive pulmonary disease but not those with cancer or asthma (7). However, the sample in the current study differed significantly from the group examined in that study; we were looking at those aged 18–64 years in all ACIP-defined priority groups and not simply those with high-risk conditions. Of those aged 18–64 years examined in our study, 63 percent had a chronic condition, 25 percent were health-care workers with direct patient contact, 6 percent both had a chronic condition and worked in the health-care field, and 6 percent had a child aged 6 months or younger in the household. In general, health-care workers, regardless of race/ethnicity, would have had better access to vaccine and have likely been encouraged by their employers to receive vaccination. Therefore, work setting is likely to have been an important influence in reducing disparities among these younger adults.
This study has several limitations. First, BRFSS is a land-line, telephone-based survey and thus excludes those segments of the population without telephones or using only cellular telephones. Second, data are self-reported and subject to potential recall and misclassification bias, particularly for questions that require recall over a longer period; therefore, for certain behaviors, prevalence might be underestimated or overestimated. Third, the sample sizes for both Blacks and Hispanics were relatively modest, which may have limited our ability to detect differences across the three racial/ethnic groups in some of these analyses. Fourth, certain priority groups were not considered in the survey, including institutionalized adults and adult caretakers of children aged less than 6 months outside of the home (i.e., child-care workers). Finally, although large compared with those in most other surveys, the samples did not contain enough cases to permit valid and reliable analysis of vaccination rates for racial/ethnic groups beyond the three examined here.
In sum, the sudden and substantial reduction in the amount of vaccine available in the United States for the 2004–2005 influenza season had a negative effect on coverage levels among vaccine-priority adults across the three racial/ethnic groups we examined. However, the absolute percentage decline in vaccination rates across these groups was similar, and the magnitude of the disparities in coverage across these groups among those aged 65 years or older did not change significantly from that of the previous seasons. Among those aged 18–64 years in ACIP-defined vaccine priority groups, there were no significant differences in coverage across the three racial/ethnic groups by the end of the 2004–2005 season, which may reflect the higher percentage of health-care workers within this age group who would have had easier access to vaccine than most other adults regardless of race/ethnicity. It will be important to continue to monitor vaccination coverage over subsequent influenza seasons to determine whether future coverage levels and racial/ethnic disparities are affected by the 2004–2005 vaccine shortage and resulting adjustments in national recommendations or whether this was a single-season abnormality.
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ACKNOWLEDGMENTS |
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The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention.
Conflict of interest: none declared.
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