Research Articles
Trends in Childhood Influenza Vaccination Coverage—U.S., 2004–2012
Tammy A. Santibanez, PhDa Peng-Jun Lu, MD, PhDa Alissa O’Halloran, MSPHa Ankita Meghani, MSPHb Mark Grabowsky, MDb James A. Singleton, PhDa
ABSTRACT Objective. We compared estimates of childhood influenza vaccination coverage by health status, age, and racial/ethnic group across eight consecutive influenza seasons (2004 through 2012) based on two survey systems to assess trends in childhood influenza vaccination coverage in the U.S. Methods. We used National Health Interview Survey (NHIS) and National Immunization Survey-Flu (NIS-Flu) data to estimate receipt of at least one dose of influenza vaccination among children aged 6 months to 17 years based on parental report. We computed estimates using Kaplan-Meier survival analysis methods. Results. Based on the NHIS, overall influenza vaccination coverage with at least one dose of influenza vaccine among children increased from 16.2% during the 2004–2005 influenza season to 47.1% during the 2011–2012 influenza season. Children with health conditions that put them at high risk for complications from influenza had higher influenza vaccination coverage than children without these health conditions for all the seasons studied. In seven of the eight seasons studied, there were no significant differences in influenza vaccination coverage between non-Hispanic black and non-Hispanic white children. Influenza vaccination coverage estimates for children were slightly higher based on NIS-Flu data compared with NHIS data for the 2010–2011 and 2011–2012 influenza seasons (4.1 and 4.4 percentage points higher, respectively); both NIS-Flu and NHIS estimates had similar patterns of decreasing vaccination coverage with increasing age. Conclusions. Although influenza vaccination coverage among children continued to increase, by the 2011–2012 influenza season, only slightly less than half of U.S. children were vaccinated against influenza. Much improvement is needed to ensure all children aged $6 months are vaccinated annually against influenza.
Centers for Disease Control and Prevention, National Center for Immunization and Respiratory Diseases, Atlanta, GA
a
National Vaccine Program Office, Washington, DC
b
Address correspondence to: Tammy A. Santibanez, PhD, Centers for Disease Control and Prevention, National Center for Immunization and Respiratory Diseases, 1600 Clifton Rd. NE, MS A-19, Atlanta, GA 30333; tel. 404-639-8304; e-mail .
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418 Research Articles
Recommendations to vaccinate children against influenza began in 1960, when people with certain health conditions that put them at increased risk of severe illness from influenza were recommended to receive annual influenza vaccination, implicitly including children with high-risk conditions.1 The recommendations for influenza vaccination of children remained unchanged until 2002, when providers were encouraged to vaccinate all children aged 6–23 months, regardless of medical conditions,2 and in 2004, when all children aged 6–23 months were explicitly recommended for vaccination.3 In 2006, the influenza recommendations were expanded to include annual vaccination for all children aged 6–59 months.4 Recommendations were further expanded in 2008 to include annual vaccination of all children aged 6 months to 18 years.5 Since the 2010–2011 influenza season, annual influenza vaccination has been recommended for all people aged 6 months and older.6 Children aged 6 months to 8 years should receive two doses of influenza vaccine, spaced four weeks apart, during their first season of vaccination and then one dose per season in subsequent seasons.7 During inter-pandemic seasons through 2011–2012, trivalent influenza vaccine was available, providing protection against two influenza A subtypes and one type B strain. During the 2009–2010 influenza season, two influenza vaccines were recommended: the trivalent seasonal influenza vaccination and the pandemic influenza A(H1N1)pdm09 (pH1N1) monovalent vaccination.8 The National Health Interview Survey (NHIS) and the National Immunization Survey-Flu (NIS-Flu) have been the primary surveys used to measure influenza vaccination coverage among children. NHIS, an inperson household survey, began collecting parental report of influenza vaccination in 2005.9 NHIS has been considered the most representative source for estimates of influenza vaccination coverage among children aged 6 months to 17 years and has served as the Healthy People data source for influenza vaccination estimates.10 NHIS, however, has not routinely allowed for state-level estimates and is not timely enough to enable the reporting of influenza estimates before the beginning of the next influenza season. NIS-Flu is an ongoing telephone survey of households with children aged 6 months to 17 years. National and state-level estimates of influenza vaccination coverage for children based on parental-reported vaccination status from NIS-Flu have been reported by fall of the subsequent influenza vaccination season.11,12 The aims of this study were to (1) examine estimates of childhood influenza vaccination coverage over time by age, race/ethnicity, and high-risk status; and (2)
compare estimates from NHIS and NIS-Flu, the two main survey systems currently used to measure influenza vaccination coverage among children in the U.S. METHODS Data and inclusion criteria We analyzed data from NHIS and NIS-Flu for this study. NHIS includes the civilian, non-institutionalized U.S. population with in-person interviews conducted throughout the year using a multistage area probability design. The survey is conducted for one adult per household, and, if children reside in the household, one child is randomly selected about which the adult respondent is interviewed. This study includes NHIS data from 2004 through 2012. The response rates for NHIS for 2004 through 2012 were, respectively, 79.4%, 77.5%, 78.8%, 76.5%, 72.3%, 73.4%, 70.7%, 74.6%, and 69.7%. During 2005–2009, influenza vaccination status was assessed by asking the respondent the following questions: “During the past 12 months, has [child] had a flu shot?;” “During what month and year did [child] receive [his/her] most recent flu shot?;” “During the past 12 months, has [child] had a flu vaccine sprayed in [his/her] nose by a doctor or other health professional?,” and “During what month and year did [child] receive [his/her] most recent flu nasal spray?” During part of 2009 and 2010, the questions were the same as noted except the word “seasonal” was inserted before the word “flu” in each question to distinguish it from the pH1N1 vaccine. Beginning in August 2010, the questions were changed to: “During the past 12 months, has [child] had a flu vaccination?;” “During what month and year did [child] receive [his/her] most recent flu vaccine?;” and “Was this a shot, or was it a vaccine sprayed in the nose?”13 NIS-Flu is a national, list-assisted, random-digit-dial, landline and cellular telephone survey of households with children that is conducted each influenza season. It includes three components: the NIS-Child for children aged 19–35 months at the time of interview, the NIS-Teen for children aged 13–17 years, and a short post-NIS influenza module for children aged 6–18 months and 3–12 years identified during the screening of households for the NIS-Child and NIS-Teen.14 The National 2009 H1N1 Flu Survey (NHFS) was also included in the analysis. In 2009, the NHFS was developed to rapidly estimate influenza vaccination coverage for both the 2009 H1N1 vaccine and the seasonal influenza vaccine for adults and children based upon parental report and was the precursor for the subsequent NIS-Flu. The main difference was that the post-NIS module in the NHFS included adults as well as
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Trends in Childhood Influenza Vaccination Coverage 419
children.15–17 The response rates for the three seasons ranged from 34% to 74% for the landline sample and 20% to 36% for the cell phone sample.17–19 For the 2009–2010 influenza season, influenza vaccination status was assessed on the NHFS by asking the parent the following questions: “Since August 2009, has [child] had a seasonal flu vaccination? There are two types of seasonal flu vaccinations. One is a shot and the other is a spray in the nose;” and “During what month did [child] receive [his/her] most recent flu vaccine?” For the 2010–2011 and 2011–2012 influenza seasons, the questions on NIS-Flu were: “Since July 1 [2011/2012] has [child] had a flu vaccination? There are two types of flu vaccinations. One is a shot and the other is a spray, mist, or drop in the nose;” and “During what month did [child] receive [his/her] first dose of the flu vaccine since July 1?” Analysis of influenza vaccination data We obtained influenza vaccination coverage estimates using the same method for both surveys. We used the Kaplan-Meier survival analysis procedure to calculate the percentage of children vaccinated with at least one dose of influenza vaccine, where vaccination month was used to define the event variable and interview date was used to define the censoring variable. Influenza vaccinations received from August to May, inclusive, were included. When the child was reported to have been vaccinated but was missing the month of vaccination, the month was imputed from donor pools matched for week (month for NHIS) of interview, age group, state (region for NHIS) of residence, and race/ ethnicity. The percentages imputed for NIS-Flu were 4.7%, 7.5%, and 2.3% for the 2009–2010, 2010–2011, and 2011–2012 seasons, respectively, and for NHIS ranged from 3.6% to 10.8% for the 2004–2005 through 2011–2012 seasons. For both NHIS and NIS-Flu, we report coverage limited to interviews conducted from September through June, with one exception. For NHIS data from the 2004–2005 season, we used interviews from January through June 2005 because influenza vaccination questions for children were not available prior to January 2005. We assessed influenza vaccination coverage overall and by child age group, high-risk status, and race/ ethnicity. The presence of high-risk conditions was determined only from NHIS; NIS-Flu does not include questions to determine high-risk health conditions. Based on ACIP recommendations and the questions available in NHIS, high-risk status was defined based on parental report of one or more of the following: ever being told by a physician that the child had cystic
fibrosis, sickle cell anemia, diabetes, congenital heart disease, other heart conditions, cerebral palsy, muscular dystrophy, and seizures; or reporting an asthma episode or attack in the past 12 months (i.e., current asthma). For both surveys, data were weighted to represent the population of children in the U.S., for households without telephones, and for nonresponse bias.20 We conducted all analyses using SAS® and SUDAAN®,21,22 and we reported estimates with 95% confidence intervals (CIs). Tests for linear trend were performed using a weighted linear regression on the season-specific estimates, using season number as the independent variable and weights as the inverse of the estimated variance of the estimated vaccination coverage. We did not conduct the trend test for NIS-Flu data because only three seasons of data were available. We conducted pair-wise comparisons of estimates using t-tests assuming large degrees of freedom and, thus, used the value of 1.96 for the critical value. All tests were two-tailed with the significance level set at 0.05. RESULTS Trends in influenza vaccination coverage overall, NHIS Based on NHIS, influenza vaccination coverage with at least one dose among children aged 6 months–17 years increased overall from the 2004–2005 influenza season to the 2011–2012 season (trend test p0.001). The average annual increase was 4.9 percentage points based upon the slope of the trend test. The estimates and annual changes from the previous season are shown in the Table. Trends in influenza vaccination coverage by high-risk status, NHIS Based on NHIS, coverage with at least one dose of influenza vaccine among children with health conditions that put them at increased risk for influenzarelated complications increased from 2004–2005 to 2011–2012 (trend test p0.001). Coverage for children without these health conditions also increased (trend test p0.001) (Table) Children with health conditions had higher influenza vaccination coverage than children without these health conditions for all the seasons studied (all p0.05) (Figure 1). The differences in coverage between high-risk and non-high-risk children ranged from a 6.9 percentage point difference in the 2011– 2012 season to an 18 percentage point difference in the 2008–2009 season.
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49.5 6.7
24.4 3.5
12.5 1.7
9.4 1.8
Agef 6–23 months
2–4 years
5–12 years
13–17 years
46.8 6.1 –2.7 31.3 3.4 16.9d 18.6 1.9 16.1d 11.5 1.9 12.1
54.9 8.3 18.1 42.1 3.8 110.8d 24.4 2.0 15.8d 16.0 2.2 14.5d
62.7 6.7 17.8 44.6 4.2 12.5 28.4 2.3 14.0d 19.2 2.5 13.2
43.7 6.5 15.5 30.2 1.8 14.4d 60.6 8.1 –2.1 49.1 5.5 14.5 36.4 3.4 18.0d 22.5 3.1 13.3
52.9 7.3 19.2 34.9 2.1 14.7d 67.1 7.8 16.5 58.5 4.4 19.4d 42.2 2.3 15.8d 31.7 2.8 19.2d
54.1 5.7 11.2 43.5 2.0 18.6d 72.0 6.0 14.9 57.7 3.8 –0.8 45.9 2.7 13.7d 34.2 3.0 12.5
55.1 7.1 11.0 46.2 1.7 12.7d
68.0 6.5 –4.0 60.4 4.3 12.7 46.8 2.4 10.9 34.8 3.3 10.6
53.4 6.0 –1.7 46.5 1.9 10.3
47.1 1.8 10.2
14.4 1.3
38.2 4.7 16.3 25.8 1.5 16.7d
46.9 1.7 12.6d
Not high risk
31.9 4.6 10.2 19.1 1.3 14.7d
44.3 1.9 17.8d
31.7 4.8
36.5 2.1 15.4d
High-risk statuse High risk
31.1 1.7 13.9d
Overall 27.2 1.4 16.6d
16.2 1.3
Characteristics 20.6 1.3 14.4d
2004–2005 2005–2006 2006–2007 2007–2008 2008–2009 2009–2010 2010–2011 2011–2012 (n55,159) (n57,941) (n56,849) (n56,541) (n55,203) (n59,325) (n58,460) (n58,691) Percent Percent Percent Percent Percent Percent Percent Percent 95% CI 95% CI 95% CI 95% CI 95% CI 95% CI 95% CI 95% CIa Changeb Change Change Change Change Change Change
NHIS
NIS-Flu
4.0 0.5
5.2 0.5
5.3 1.0
3.5 1.1
5.0 0.5
3.9 1.0
4.9 0.6
31.9 2.7
41.3 1.9
56.2 3.9
74.6 2.5 16.4d 63.3 2.3 12.7 54.2 1.4 –0.5 33.7 1.6 –0.8
NA
NA
51.5 1.0 0.5
continued on p. 421
68.2 2.4 18.5d 60.6 2.3 14.4 54.7 1.5 113.4d 34.5 1.4 12.6
NA
NA
59.7 3.7
NA
51.0 0.9 17.3d NA
43.7 0.9
2009–2010 2010–2011 2011–2012 Trend testc (n5149,872) (n5116,799) (n596,254) Percent Percent Slope Percent 95% CI 95% CI 95% CI (95% CI) Change Change
Table. Influenza vaccination coverage (at least one dose) among children aged 6 months–17 years, by influenza season, data source, high-risk status, age, and racial/ethnic group: NHIS and NIS-Flu, U.S., 2004–2005 through 2011–2012 influenza seasons
Public Health Reports / September–October 2014 / Volume 129 39.8 4.3 17.6d 33.2 2.9 14.7d 37.7 5.5 13.0 48.9 8.7 18.1
45.3 3.1 15.5 d 42.5 2.5 19.3d 42.7 4.2 15.0 55.5 7.8 16.6
50.5 3.5 15.2d 44.7 2.2 12.2 46.6 4.9 13.9 51.6 5.3 –3.9
50.2 3.3 –0.3 44.1 2.6 –0.6 47.6 3.8 11.0 56.7 5.6 15.1
5.1 0.9
4.8 0.6
4.7 0.6
5.0 0.6
53.6 3.1
37.0 2.6
43.2 0.9
46.9 2.6
55.1 2.6 18.2 d 48.5 1.0 15.3d 50.8 2.9 113.8d 57.1 2.9 13.5
59.5 2.5 14.4 d 47.6 1.0 –0.9 53.7 2.9 12.9 53.6 2.8 –3.5
2009–2010 2010–2011 2011–2012 Trend testc (n5149,872) (n5116,799) (n596,254) Percent Percent Slope Percent 95% CI 95% CI 95% CI (95% CI) Change Change
NIS-Flu
Change in percentage points compared with the previous influenza season
Statistically significant at p0.05. Pair-wise comparisons between adjacent influenza seasons were conducted using t-tests.
NA 5 not available
CI 5 confidence interval
NIS-Flu 5 National Immunization Survey-Flu
NHIS 5 National Health Interview Survey
f
Age on November 1
e
High-risk status was defined based on parental report of one or more of the following: ever being told by a physician that the child had cystic fibrosis, sickle cell anemia, diabetes, congenital heart disease, other heart conditions, cerebral palsy, muscular dystrophy, or seizures; or reporting an asthma episode or attack in the past 12 months. This definition was based on Advisory Committee on Immunization Practices recommendations and the questions available in NHIS.
d
c
Tests for linear trend were performed using a weighted linear regression on the season-specific estimates, using season number as the independent variable and weights as the inverse of the estimated variance of the estimated vaccination coverage. The estimated slope coefficients were interpreted as the average change across seasons assuming a linear increase. Slopes and their 95% CIs are presented; all of the tests for linear trend were significant at p0.001.
b
a Estimates obtained using Kaplan-Meier survival analysis methods and reported with CI half-widths. Estimates for the 2009–2010 season include only the seasonal influenza vaccine and exclude the 2009 H1N1 vaccine.
Non-Hispanic other 20.5 4.8
Non-Hispanic black 15.6 3.1
Non-Hispanic white 15.0 1.7
32.2 3.3 13.3 28.5 2.3 12.9 34.7 4.4 16.8d 40.8 6.9 16.9
Race/ethnicity Hispanic 28.9 2.8 17.3d 25.6 2.1 16.6d 27.9 4.3 16.4d 33.9 6.1 14.0
18.6 2.8
Characteristics 21.6 2.9 13.0 19.0 1.8 14.0 d 21.5 3.3 15.9d 29.9 5.1 19.4d
2004–2005 2005–2006 2006–2007 2007–2008 2008–2009 2009–2010 2010–2011 2011–2012 (n55,159) (n57,941) (n56,849) (n56,541) (n55,203) (n59,325) (n58,460) (n58,691) Percent Percent Percent Percent Percent Percent Percent Percent 95% CI 95% CI 95% CI 95% CI 95% CI 95% CI 95% CI 95% CIa Changeb Change Change Change Change Change Change
NHIS
Table (continued). Influenza vaccination coverage (at least one dose) among children aged 6 months–17 years, by influenza season, data source, high-risk status, age, and racial/ethnic group: NHIS and NIS-Flu, U.S., 2004–2005 through 2011–2012 influenza seasons
422 Research Articles
Figure 1. Influenza vaccination coveragea (at least one dose) among children aged 6 months–17 years, by influenza season and high-risk status:b NHIS, U.S., 2004–2005 through 2011–2012 influenza seasons
a Estimates obtained using Kaplan-Meier survival analysis methods and reported with confidence interval half-widths. Estimates for the 2009–2010 season include only the seasonal influenza vaccine and exclude the 2009 H1N1 vaccine.
Based on ACIP recommendations and the questions available in NHIS, high-risk status was defined based on parental report of one or more of the following: ever being told by a physician that the child had cystic fibrosis, sickle cell anemia, diabetes, congenital heart disease, other heart conditions, cerebral palsy, muscular dystrophy, or seizures; or reporting an asthma episode or attack in the past 12 months.
b
Statistically significant at p0.05 based on comparison of high-risk with non-high-risk estimate
c
NHIS 5 National Health Interview Survey ACIP 5 Advisory Committee on Immunization Practices
Trends in influenza vaccination coverage by age group, NHIS Within each age group studied using NHIS data, influenza vaccination coverage increased from the 2004–2005 influenza season to the 2011–2012 season (trend test p0.001 each) (Table). The differences between adjoining seasons are shown in the Table. Children aged 6–23 months had higher influenza coverage compared with the older age groups during the influenza seasons studied, except for the 2009–2010 and 2011–2012 seasons, in which coverage was not significantly different from coverage in children aged 2–4 years (all p0.05 except for the 2009–2010 and 2011–2012 seasons). Children aged 2–4 years had higher coverage than older children for all influenza seasons; likewise, children aged 5–12 years had higher coverage than children aged 13–17 years for all influenza seasons studied (Table, Figure 2).
Trends in influenza vaccination coverage by race/ethnicity, NHIS Within all four racial/ethnic groups studied using NHIS data, influenza vaccination coverage increased from the 2004–2005 influenza season to the 2011–2012 season (trend test p0.001 each). The change in vaccination coverage from one season to the next within each group is indicated in the Table. As shown in Figure 3, in seven of the eight seasons studied, there were no statistically significant differences in influenza vaccination coverage between nonHispanic black and non-Hispanic white children; in the 2007–2008 season, non-Hispanic black children had higher coverage than non-Hispanic white children. Hispanic children had higher influenza vaccination coverage than non-Hispanic white children in the 2004– 2005, 2008–2009, 2010–2011, and 2011–2012 seasons. Influenza vaccination coverage among n on-Hispanic
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Trends in Childhood Influenza Vaccination Coverage 423
black and Hispanic children did not differ significantly during any season. Non-Hispanic children of other or multiple races had higher influenza vaccination coverage than non-Hispanic white children during all influenza seasons studied. Non-Hispanic children of other or multiple races also had higher coverage than non-Hispanic black and/or Hispanic children in most influenza seasons. NHIS vs. NIS-Flu NHIS and NIS-Flu estimates were compared overall, within age groups, and within each racial/ethnic group. Of the 27 comparisons (Figure 4), 10 had significant differences between estimates from the two surveys. Of these 10 differences, nine showed that the estimates from NIS-Flu were higher than those from NHIS (percentage point differences ranged from 3.5 to 9.3). The remaining difference was in the 2009–2010 influenza
season among non-Hispanic black children, with a higher estimate from NHIS compared with NIS-Flu. The remaining 17 comparisons were not statistically different. Similar to NHIS, NIS-Flu estimates by age group each season indicated decreasing vaccination rates with increasing age group (Figure 2). Based on NISFlu data, non-Hispanic white children had higher coverage than non-Hispanic black children during the 2009–2010 influenza season, but there was no difference in the 2010–2011 season, and then non-Hispanic black children had higher coverage than non-Hispanic white children in the 2011–2012 season (Figure 3). Hispanic children had higher influenza vaccination coverage than non-Hispanic white children during the 2009–2010, 2010–2011, and 2011–2012 influenza seasons based on NIS-Flu data. Based on NIS-Flu estimates, Hispanic children had higher influenza vaccination
Figure 2. Influenza vaccination coveragea (at least one dose) among children aged 6 months–17 years, by influenza season and age group:b,c NHIS and NIS-Flu, U.S., 2004–2005 through 2011–2012 influenza seasons
a Estimates obtained using Kaplan-Meier survival analysis methods and reported with confidence interval half-widths. Estimates for the 2009–2010 season include only the seasonal influenza vaccine and exclude the 2009 H1N1 vaccine. b
Age as of November 1 for each influenza season
All comparisons between the age groups within each season were statistically significant at p0.05, except for in 2009–2010 where with both NHIS and the NIS-Flu data, the 6- to 23-month age group did not differ from the 2- to 4-year age group, and in 2011–2012 with NHIS data, where the 6- to 23-month age group and the 2- to 4-year age group did not differ. c
NHIS 5 National Health Interview Survey NIS-Flu 5 National Immunization Survey-Flu
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Figure 3. Influenza vaccination coveragea (at least one dose) among children aged 6 months–17 years, by influenza season, racial/ethnic group, NHIS, and NIS-Flu: U.S., 2004–2005 through 2011–2012 influenza seasons
100 90
Percentage vaccinated
80 70 60 50 40 30 20 10 0 2004–05 2005–06 2006–07 2007–08 2008–09 2009–10 2010–11 2011–12
2009–10 2010–11 2011–12
Influenza season a Estimates obtained using Kaplan-Meier survival analysis methods and reported with confidence interval half-widths. Estimates for the 2009–2010 season include only the seasonal influenza vaccine and exclude the 2009 H1N1 vaccine. b
Statistically significant (p0.05) differences between groups are denoted as well as the direction of the difference.
NHIS 5 National Health Interview Survey NIS-Flu 5 National Immunization Survey-Flu H 5 Hispanic W 5 non-Hispanic white only O 5 non-Hispanic other or multiple race B 5 non-Hispanic black only
coverage than non-Hispanic black children in the 2009–2010, 2010–2011, and 2011–2012 seasons. Similar to NHIS, non-Hispanic children of other or multiple races had higher influenza vaccination coverage than non-Hispanic white children in all influenza seasons studied based on NIS-Flu (Figure 3). DISCUSSION Data from both NHIS and NIS-Flu demonstrate increasing influenza coverage among all children, including increases among those with and without high-risk conditions and among all age and racial/ethnic groups. This encouraging finding suggests that efforts to promote influenza vaccination among children are having a growing impact. However, estimated influenza
vaccination coverage for the 2011–2012 season was well below the Healthy People 2020 target of 70% for children aged 6 months to 17 years overall.10 It is encouraging to note, though, that more than 70% of children aged 6–23 months received at least one dose of influenza vaccine for the first time during the 2010–2011 season. Children with high-risk conditions have higher vaccination coverage than those without high-risk conditions, probably in part because providers might be more accustomed to vaccinating people with high-risk conditions due to the longer-standing recommendations and also because these children are more likely to seek health care during the period of influenza vaccination. The fact that younger children have higher coverage than older children might be related to recommendations for influenza vaccination
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Trends in Childhood Influenza Vaccination Coverage 425
initially targeting younger age groups, then expanding to older children; their higher risk of influenza-related complications relative to older children; more time for changes in provider practices; and more frequent visits to providers.23 Influenza coverage was generally similar among non-Hispanic white and non-Hispanic black children based on NHIS and NIS-Flu. In most influenza seasons, there was no difference in vaccination coverage; in one season (2009–2010, NIS-Flu), non-Hispanic white children had higher vaccination coverage, and in two seasons (2007–2008 NHIS and 2011–2012 NISFlu), non-Hispanic black children had higher vaccination coverage. Hispanic and other/multiple-race
children had coverage as high as or higher than that of non-Hispanic white children. Increased access to vaccination through the Vaccines for Children (VFC) program might contribute to higher vaccination of these children.24 Beginning with the 2003–2004 flu season, ACIP voted to include annual influenza vaccination for children 6–23 months of age in the VFC program (it was not covered during the 2002–2003 season).25 Subsequently, as more child age groups were added to the influenza recommendation, the age groups were also added to the VFC resolution for influenza. The VFC program has been an important contributor to successfully achieving high coverage levels of routinely recommended vaccines for children
Figure 4. Comparison of survey estimatesa of influenza vaccination coverage (at least one dose) among children aged 6 months–17 years, by influenza season, age group, and race/ethnicity: NHIS and NIS-Flu, U.S., 2009–2010 through 2011–2012 influenza seasons
b b
a Estimates obtained using Kaplan-Meier survival analysis methods and reported with confidence interval half-widths. Estimates for the 2009–2010 season include only the seasonal influenza vaccine and exclude the 2009 H1N1 vaccine. b
Statistically significant (p0.05) differences between groups are denoted.
NHIS 5 National Health Interview Survey NIS-Flu 5 National Immunization Survey-Flu m 5 months y 5 years
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by providing publicly purchased vaccines to providers for use in children who are (1) Medicaid-eligible, (2) uninsured, (3) American Indian or Alaska Native, or (4) covered by health insurance that does not cover the cost of vaccine, when the child is served at a Federally Qualified Health Center or Rural Health Center.26 While no racial/ethnic disparities exist for influenza vaccination coverage among children, these disparities persist among adults.27 Based on data from NHIS and NIS-Flu, overall trends in influenza vaccination coverage among children aged 6 months–17 years were similar. There were some differences by data source in estimated coverage from one influenza season to the next and in patterns of differences by race/ethnicity. Differences between NHIS and NIS-Flu estimates suggest that NIS-Flu estimates are likely slightly biased upward compared with NHIS estimates, because although two-thirds of the estimates were not statistically significant, of the onethird that were, the point differences ranged from 3.5 to 9.3 higher for NIS-Flu. Differences between NHIS and NIS-Flu that may contribute to systematic differences in estimates include survey mode (face-to-face vs. telephone survey), response rate (61% vs. 30%–74% landline/20%–36% cell phone), weighting methodology, or survey question wording. Random survey variation also contributes to differences. Both NIS-Flu and NHIS estimates are subject to error from misclassification of children’s vaccination status reported by parents.28 Because NHIS has a more complete sample frame (including households with no type of telephone service) and higher response rates, the estimates may be more representative. On the other hand, national estimates from NIS-Flu are more precise than from NHIS due to a larger sample size. The timeliness of NIS-Flu and the allowance of the production of routine state-level estimates make NIS-Flu useful for public health action, keeping in mind that the estimates have a slight upward bias. While NHIS and NIS-Flu are the primary sources for monitoring influenza vaccination coverage among children, there are some other data sources that can provide additional information not available with NHIS and NIS-Flu. These sources include the Behavioral Risk Factor Surveillance System optional child influenza module;29,30 the National Flu Survey (NFS), previously named the Rapid Flu Survey; and Immunization Information Systems (IISs). The NFS included questions on knowledge and attitudes toward influenza disease and vaccination, as well as reasons for vaccination and non-vaccination.31–33 IISs have been used to monitor provider report of influenza vaccination coverage among children and are particularly useful
for local area estimates and for obtaining two-dose influenza coverage; however, not all states have equally functional IISs.34 Limitations The findings in this article are subject to at least three limitations. First, influenza vaccination estimates were based on parental report rather than medical records and may be subject to recall bias. Studies have shown that parental report overestimates influenza vaccination coverage compared with medical records.35–37 Second, during the 2009–2010 season, respondents may have misclassified receipt of the seasonal vs. the H1N1 influenza vaccine. Third, receipt of two doses of influenza vaccine was not evaluated in this study; as such, results may differ when two-dose coverage is evaluated.38 CONCLUSION Influenza vaccination coverage among children continues to increase. However, based on data through the 2011–2012 influenza season, only slightly less than half of children in the U.S. were vaccinated against influenza. Although vaccination levels have increased substantially since 2004, much improvement is needed to ensure that all children aged $6 months are vaccinated annually against influenza. Strategies that have been shown to improve influenza vaccination coverage include reminder/recall systems and standing orders. The Community Guide to Preventive Services provides information on effective strategies to increase the use of recommended vaccinations, including influenza vaccination.39 The findings and conclusions in this article are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention (CDC). Institutional Review Board approval was obtained for the National Health Interview Survey and National Immunization Survey-Flu by the National Center for Health Statistics, CDC.
REFERENCES 1. Burney LE. Influenza immunization: statement. Public Health Rep 1960;75:944. 2. Prevention and control of influenza: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep 2002;51(RR-3):1-36. 3. Harper SA, Fukuda K, Uyeki TM, Cox NJ, Bridges CB. Prevention and control of influenza: recommendations of the Advisory Committee on Immunization Practices (ACIP) [published erratum appears in MMWR Morb Mortal Wkly Rep 2004;53(32):743]. MMWR Recomm Rep 2004;53(RR-6):1-40. 4. Smith NM, Bresee JS, Shay DK, Uyeki TM, Cox NJ, Strikas RA. Prevention and control of influenza: recommendations of the Advisory Committee on Immunization Practices (ACIP) [published erratum appears in MMWR Morb Mortal Wkly Rep 2006;55(29):800]. MMWR Recomm Rep 2006;55(RR-10):1-42.
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Trends in Childhood Influenza Vaccination Coverage 427
5. Prevention and control of seasonal influenza with vaccines: recommendations of the Advisory Committee on Immunization Practices (ACIP), 2008. MMWR Recomm Rep 2008;57(RR-7):1-60. 6. Fiore AE, Uyeke TM, Broder K, Finelli L, Fuler GL, Singleton JA, et al. Prevention and control of influenza with vaccines: recommendations of the Advisory Committee on Immunization Practices (ACIP), 2010 [published erratum appears in MMWR Morb Mortal Wkly Rep 2010;59(31):993]. MMWR Recomm Rep 2010;59(RR-8):1-62. 7. Grohskopf LA, Shay DK, Thimabukuro TT, Sokolow LZ, Keitel WA, Bresee JS, et al. Prevention and control of seasonal influenza with vaccines: recommendations of the Advisory Committee on Immunization Practices (ACIP)—United States, 2013–2014 [published erratum appears in MMWR Morb Mortal Wkly Rep 2013;62(45):906]. MMWR Recomm Rep 2013;62(RR-7):1-43. 8. Use of influenza A (H1N1) 2009 monovalent vaccine: recommendations of the Advisory Committee on Immunization Practices (ACIP), 2009. MMWR Recomm Rep 2009;58(RR-10):1-8. 9. Centers for Disease Control and Prevention (US). National Health Interview Survey: questionnaires, datasets, and related documentation: 1997 to the present [cited 2013 Apr 12]. Available from: URL: http://www.cdc.gov/nchs/nhis/quest_data_related_1997_forward .htm 10. Department of Health and Human Services (US). Healthy people 2020: topics & objectives—immunization and infectious diseases [cited 2013 Jul 26]. Available from: URL: http://www.healthypeople .gov/2020/topicsobjectives2020/objectiveslist.aspx?topicid=23 11. Centers for Disease Control and Prevention (US). Seasonal influenza (flu): 2012–13 state and regional vaccination trend report [cited 2014 May 8]. Available from: URL: http://www.cdc.gov/flu /fluvaxview/reports/reporti1213/trends/index.htm 12. Centers for Disease Control and Prevention (US). Seasonal influenza (flu): flu vaccination coverage, United States, 2012–13 influenza season [cited 2014 May 18]. Available from: URL: http://www.cdc .gov/flu/fluvaxview/coverage-1213estimates.htm 13. Centers for Disease Control and Prevention (US). National Health Interview Survey, survey questionnaires [cited 2013 Nov 7]. Available from: URL: ftp://ftp.cdc.gov/pub/Health_Statistics/NCHS /Survey_Questionnaires/NHIS 14. Lu P-J, Santibanez TA, Williams WW, Zhang J, Ding H, Bryan L, et al. Surveillance of influenza vaccination coverage—United States, 2007–08 through 2011–12 influenza seasons. MMWR Surveill Summ 2013;62(SS-4):1-29. 15. Santibanez TA, Singleton JA, Santibanez SS, Wortley P, Bell BP. Socio-demographic differences in opinions about 2009 pandemic influenza A (H1N1) and seasonal influenza vaccination and disease among adults during the 2009–2010 influenza season. Influenza Other Respir Dis 2012;7:383-92. 16. Interim results: influenza A (H1N1) 2009 monovalent vaccination coverage—United States, October–December 2009. MMWR Morb Mortal Wkly Rep 2010;59(early release):1-5. 17. Centers for Disease Control and Prevention (US). Season influenza (flu): final state-level monthly cumulative influenza vaccination coverage estimates for the 2009–10 season—United States, August 2009 through May 2010 [cited 2013 Nov 7]. Available from: URL: http://www.cdc.gov/flu/professionals/vaccination/reporti0910 /reportI0910 18. Centers for Disease Control and Prevention (US). Seasonal influenza (flu): flu vaccination coverage, United States, 2011–12 influenza season [cited 2013 Nov 7]. Available from: URL: http://www.cdc .gov/flu/professionals/vaccination/coverage_1112estimates.htm 19. Centers for Disease Control and Prevention (US). Final state-level influenza vaccination coverage estimates for the 2010–11 season— United States, National Immunization Survey and Behavioral Risk Factor Surveillance System, August 2010 through May 2011 [cited 2013 Nov 7]. Available from: URL: http://www.cdc.gov/flu/professionals /vaccination/coverage_1011estimates.htm
20. Smith PJ, Battaglia MP, Huggins VJ, Hoaglin DC, Roden A, Khare M, et al. Overview of the sampling design and statistical methods used in the National Immunization Survey. Am J Prev Med 2001;20 (4 Suppl):17-24. 21. SAS Institute, Inc. SAS®: Version 9.3 for Windows. Cary (NC): SAS Institute, Inc.; 2011. 22. Research Triangle Institute, Inc. SUDAAN®: Release 11.0. Research Triangle Park (NC): Research Triangle Institute, Inc.; 2012. 23. Poehling KA, Edwards KM, Griffin MR, Szilagyi PG, Staat MA, Iwane MK, et al. The burden of influenza in young children, 2004–2009. Pediatrics 2013;131:207-16. 24. Walker AT, Smith PJ, Kolasa M. Reduction of racial/ethnic disparities in vaccination coverage, 1995–2011. MMWR Surveill Summ 2014;63:7-12. 25. Childhood influenza-vaccination coverage—United States, 2002–03 influenza season. MMWR Morb Mortal Wkly Rep 2004;53(37):863-6. 26. Centers for Disease Control and Prevention (US). Vaccines for Children Program (VFC): about VFC [cited 2013 Apr 11]. Available from: URL: http://www.cdc.gov/vaccines/programs/vfc/about /index.html 27. Centers for Disease Control and Prevention (US). Recent influenza vaccination trends across influenza seasons [cited 2013 Apr 11]. Available from: URL: http://www.cdc.gov/flu/fluvaxview/trends-summary .htm 28. Brown C, Clayton-Boswell H, Chaves SS, Prill MM, Iwane MK, Szilagyi PG, et al. Validity of parental report of influenza vaccination in young children seeking medical care. Vaccine 2011;29:9488-92. 29. Centers for Disease Control and Prevention (US). Behavioral Risk Factor Surveillance System: questionnaires [cited 2013 Apr 12]. Available from: URL: http://www.cdc.gov/brfss/questionnaires .htm#about 30. Estimated influenza vaccination coverage among adults and children—United States, September 1, 2004–January 31, 2005. MMWR Morb Mortal Wkly Rep 2005;54(12):304-7. 31. Centers for Disease Control and Prevention (US). Results from the November 2010 National Flu Survey—United States, 2010–11 influenza season [cited 2013 Nov 7]. Available from: URL: http:// www.cdc.gov/flu/pdf/fluvaxview/nationalflusurvey_nov2010results .pdf 32. Centers for Disease Control and Prevention (US). Results from the March 2011 National Flu Survey—United States, 2010–11 influenza season [cited 2013 Nov 7]. Available from: URL: http://www.cdc .gov/flu/pdf/fluvaxview/fluvacsurvey.pdf 33. Centers for Disease Control and Prevention (US). National mid-season flu vaccination coverage, National Flu Survey, United States, 2011–12 influenza season [cited 2013 Nov 7]. Available from: URL: http:// www.cdc.gov/flu/professionals/vaccination/national-flu-survey .htm 34. Brief report: influenza vaccination coverage among children aged 6–23 months—six immunization information system sentinel sites, United States, 2005–06 influenza season. MMWR Morb Mortal Wkly Rep 2006;55(49):1329-30. 35. Nowalk MP, Zimmerman RK, Lin CJ, Ko FS, Raymund M, Hoberman A, et al. Parental perspectives on influenza immunization of children aged 6 to 23 months. Am J Prev Med 2005;29:210-4. 36. Shinall MC Jr, Plosa EJ, Poehling KA. Validity of parental report of influenza vaccination in children aged 6 to 59 months of age. Pediatrics 2007;120:e783-7. 37. Lu P, Dorell C, Yankey D, Santibanez TA, Singleton JA. A comparison of parent and provider reported influenza vaccination status of adolescents. Vaccine 2012;30:3278-85. 38. Yoo BK, Berry A, Kasajima M, Szilagyi PG. Association between Medicaid reimbursement and child influenza vaccination rates. Pediatrics 2010;126:e998-1010. 39. Guide to Community Preventive Services. Increasing appropriate vaccination [cited 2013 Jul 30]. Available from: URL: http://www .thecommunityguide.org/vaccines/index.html
Public Health Reports / September–October 2014 / Volume 129
Trends in Childhood Influenza Vaccination Coverage—U.S., 2004–2012
Tammy A. Santibanez, PhDa Peng-Jun Lu, MD, PhDa Alissa O’Halloran, MSPHa Ankita Meghani, MSPHb Mark Grabowsky, MDb James A. Singleton, PhDa
ABSTRACT Objective. We compared estimates of childhood influenza vaccination coverage by health status, age, and racial/ethnic group across eight consecutive influenza seasons (2004 through 2012) based on two survey systems to assess trends in childhood influenza vaccination coverage in the U.S. Methods. We used National Health Interview Survey (NHIS) and National Immunization Survey-Flu (NIS-Flu) data to estimate receipt of at least one dose of influenza vaccination among children aged 6 months to 17 years based on parental report. We computed estimates using Kaplan-Meier survival analysis methods. Results. Based on the NHIS, overall influenza vaccination coverage with at least one dose of influenza vaccine among children increased from 16.2% during the 2004–2005 influenza season to 47.1% during the 2011–2012 influenza season. Children with health conditions that put them at high risk for complications from influenza had higher influenza vaccination coverage than children without these health conditions for all the seasons studied. In seven of the eight seasons studied, there were no significant differences in influenza vaccination coverage between non-Hispanic black and non-Hispanic white children. Influenza vaccination coverage estimates for children were slightly higher based on NIS-Flu data compared with NHIS data for the 2010–2011 and 2011–2012 influenza seasons (4.1 and 4.4 percentage points higher, respectively); both NIS-Flu and NHIS estimates had similar patterns of decreasing vaccination coverage with increasing age. Conclusions. Although influenza vaccination coverage among children continued to increase, by the 2011–2012 influenza season, only slightly less than half of U.S. children were vaccinated against influenza. Much improvement is needed to ensure all children aged $6 months are vaccinated annually against influenza.
Centers for Disease Control and Prevention, National Center for Immunization and Respiratory Diseases, Atlanta, GA
a
National Vaccine Program Office, Washington, DC
b
Address correspondence to: Tammy A. Santibanez, PhD, Centers for Disease Control and Prevention, National Center for Immunization and Respiratory Diseases, 1600 Clifton Rd. NE, MS A-19, Atlanta, GA 30333; tel. 404-639-8304; e-mail .
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418 Research Articles
Recommendations to vaccinate children against influenza began in 1960, when people with certain health conditions that put them at increased risk of severe illness from influenza were recommended to receive annual influenza vaccination, implicitly including children with high-risk conditions.1 The recommendations for influenza vaccination of children remained unchanged until 2002, when providers were encouraged to vaccinate all children aged 6–23 months, regardless of medical conditions,2 and in 2004, when all children aged 6–23 months were explicitly recommended for vaccination.3 In 2006, the influenza recommendations were expanded to include annual vaccination for all children aged 6–59 months.4 Recommendations were further expanded in 2008 to include annual vaccination of all children aged 6 months to 18 years.5 Since the 2010–2011 influenza season, annual influenza vaccination has been recommended for all people aged 6 months and older.6 Children aged 6 months to 8 years should receive two doses of influenza vaccine, spaced four weeks apart, during their first season of vaccination and then one dose per season in subsequent seasons.7 During inter-pandemic seasons through 2011–2012, trivalent influenza vaccine was available, providing protection against two influenza A subtypes and one type B strain. During the 2009–2010 influenza season, two influenza vaccines were recommended: the trivalent seasonal influenza vaccination and the pandemic influenza A(H1N1)pdm09 (pH1N1) monovalent vaccination.8 The National Health Interview Survey (NHIS) and the National Immunization Survey-Flu (NIS-Flu) have been the primary surveys used to measure influenza vaccination coverage among children. NHIS, an inperson household survey, began collecting parental report of influenza vaccination in 2005.9 NHIS has been considered the most representative source for estimates of influenza vaccination coverage among children aged 6 months to 17 years and has served as the Healthy People data source for influenza vaccination estimates.10 NHIS, however, has not routinely allowed for state-level estimates and is not timely enough to enable the reporting of influenza estimates before the beginning of the next influenza season. NIS-Flu is an ongoing telephone survey of households with children aged 6 months to 17 years. National and state-level estimates of influenza vaccination coverage for children based on parental-reported vaccination status from NIS-Flu have been reported by fall of the subsequent influenza vaccination season.11,12 The aims of this study were to (1) examine estimates of childhood influenza vaccination coverage over time by age, race/ethnicity, and high-risk status; and (2)
compare estimates from NHIS and NIS-Flu, the two main survey systems currently used to measure influenza vaccination coverage among children in the U.S. METHODS Data and inclusion criteria We analyzed data from NHIS and NIS-Flu for this study. NHIS includes the civilian, non-institutionalized U.S. population with in-person interviews conducted throughout the year using a multistage area probability design. The survey is conducted for one adult per household, and, if children reside in the household, one child is randomly selected about which the adult respondent is interviewed. This study includes NHIS data from 2004 through 2012. The response rates for NHIS for 2004 through 2012 were, respectively, 79.4%, 77.5%, 78.8%, 76.5%, 72.3%, 73.4%, 70.7%, 74.6%, and 69.7%. During 2005–2009, influenza vaccination status was assessed by asking the respondent the following questions: “During the past 12 months, has [child] had a flu shot?;” “During what month and year did [child] receive [his/her] most recent flu shot?;” “During the past 12 months, has [child] had a flu vaccine sprayed in [his/her] nose by a doctor or other health professional?,” and “During what month and year did [child] receive [his/her] most recent flu nasal spray?” During part of 2009 and 2010, the questions were the same as noted except the word “seasonal” was inserted before the word “flu” in each question to distinguish it from the pH1N1 vaccine. Beginning in August 2010, the questions were changed to: “During the past 12 months, has [child] had a flu vaccination?;” “During what month and year did [child] receive [his/her] most recent flu vaccine?;” and “Was this a shot, or was it a vaccine sprayed in the nose?”13 NIS-Flu is a national, list-assisted, random-digit-dial, landline and cellular telephone survey of households with children that is conducted each influenza season. It includes three components: the NIS-Child for children aged 19–35 months at the time of interview, the NIS-Teen for children aged 13–17 years, and a short post-NIS influenza module for children aged 6–18 months and 3–12 years identified during the screening of households for the NIS-Child and NIS-Teen.14 The National 2009 H1N1 Flu Survey (NHFS) was also included in the analysis. In 2009, the NHFS was developed to rapidly estimate influenza vaccination coverage for both the 2009 H1N1 vaccine and the seasonal influenza vaccine for adults and children based upon parental report and was the precursor for the subsequent NIS-Flu. The main difference was that the post-NIS module in the NHFS included adults as well as
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Trends in Childhood Influenza Vaccination Coverage 419
children.15–17 The response rates for the three seasons ranged from 34% to 74% for the landline sample and 20% to 36% for the cell phone sample.17–19 For the 2009–2010 influenza season, influenza vaccination status was assessed on the NHFS by asking the parent the following questions: “Since August 2009, has [child] had a seasonal flu vaccination? There are two types of seasonal flu vaccinations. One is a shot and the other is a spray in the nose;” and “During what month did [child] receive [his/her] most recent flu vaccine?” For the 2010–2011 and 2011–2012 influenza seasons, the questions on NIS-Flu were: “Since July 1 [2011/2012] has [child] had a flu vaccination? There are two types of flu vaccinations. One is a shot and the other is a spray, mist, or drop in the nose;” and “During what month did [child] receive [his/her] first dose of the flu vaccine since July 1?” Analysis of influenza vaccination data We obtained influenza vaccination coverage estimates using the same method for both surveys. We used the Kaplan-Meier survival analysis procedure to calculate the percentage of children vaccinated with at least one dose of influenza vaccine, where vaccination month was used to define the event variable and interview date was used to define the censoring variable. Influenza vaccinations received from August to May, inclusive, were included. When the child was reported to have been vaccinated but was missing the month of vaccination, the month was imputed from donor pools matched for week (month for NHIS) of interview, age group, state (region for NHIS) of residence, and race/ ethnicity. The percentages imputed for NIS-Flu were 4.7%, 7.5%, and 2.3% for the 2009–2010, 2010–2011, and 2011–2012 seasons, respectively, and for NHIS ranged from 3.6% to 10.8% for the 2004–2005 through 2011–2012 seasons. For both NHIS and NIS-Flu, we report coverage limited to interviews conducted from September through June, with one exception. For NHIS data from the 2004–2005 season, we used interviews from January through June 2005 because influenza vaccination questions for children were not available prior to January 2005. We assessed influenza vaccination coverage overall and by child age group, high-risk status, and race/ ethnicity. The presence of high-risk conditions was determined only from NHIS; NIS-Flu does not include questions to determine high-risk health conditions. Based on ACIP recommendations and the questions available in NHIS, high-risk status was defined based on parental report of one or more of the following: ever being told by a physician that the child had cystic
fibrosis, sickle cell anemia, diabetes, congenital heart disease, other heart conditions, cerebral palsy, muscular dystrophy, and seizures; or reporting an asthma episode or attack in the past 12 months (i.e., current asthma). For both surveys, data were weighted to represent the population of children in the U.S., for households without telephones, and for nonresponse bias.20 We conducted all analyses using SAS® and SUDAAN®,21,22 and we reported estimates with 95% confidence intervals (CIs). Tests for linear trend were performed using a weighted linear regression on the season-specific estimates, using season number as the independent variable and weights as the inverse of the estimated variance of the estimated vaccination coverage. We did not conduct the trend test for NIS-Flu data because only three seasons of data were available. We conducted pair-wise comparisons of estimates using t-tests assuming large degrees of freedom and, thus, used the value of 1.96 for the critical value. All tests were two-tailed with the significance level set at 0.05. RESULTS Trends in influenza vaccination coverage overall, NHIS Based on NHIS, influenza vaccination coverage with at least one dose among children aged 6 months–17 years increased overall from the 2004–2005 influenza season to the 2011–2012 season (trend test p0.001). The average annual increase was 4.9 percentage points based upon the slope of the trend test. The estimates and annual changes from the previous season are shown in the Table. Trends in influenza vaccination coverage by high-risk status, NHIS Based on NHIS, coverage with at least one dose of influenza vaccine among children with health conditions that put them at increased risk for influenzarelated complications increased from 2004–2005 to 2011–2012 (trend test p0.001). Coverage for children without these health conditions also increased (trend test p0.001) (Table) Children with health conditions had higher influenza vaccination coverage than children without these health conditions for all the seasons studied (all p0.05) (Figure 1). The differences in coverage between high-risk and non-high-risk children ranged from a 6.9 percentage point difference in the 2011– 2012 season to an 18 percentage point difference in the 2008–2009 season.
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Public Health Reports / September–October 2014 / Volume 129
49.5 6.7
24.4 3.5
12.5 1.7
9.4 1.8
Agef 6–23 months
2–4 years
5–12 years
13–17 years
46.8 6.1 –2.7 31.3 3.4 16.9d 18.6 1.9 16.1d 11.5 1.9 12.1
54.9 8.3 18.1 42.1 3.8 110.8d 24.4 2.0 15.8d 16.0 2.2 14.5d
62.7 6.7 17.8 44.6 4.2 12.5 28.4 2.3 14.0d 19.2 2.5 13.2
43.7 6.5 15.5 30.2 1.8 14.4d 60.6 8.1 –2.1 49.1 5.5 14.5 36.4 3.4 18.0d 22.5 3.1 13.3
52.9 7.3 19.2 34.9 2.1 14.7d 67.1 7.8 16.5 58.5 4.4 19.4d 42.2 2.3 15.8d 31.7 2.8 19.2d
54.1 5.7 11.2 43.5 2.0 18.6d 72.0 6.0 14.9 57.7 3.8 –0.8 45.9 2.7 13.7d 34.2 3.0 12.5
55.1 7.1 11.0 46.2 1.7 12.7d
68.0 6.5 –4.0 60.4 4.3 12.7 46.8 2.4 10.9 34.8 3.3 10.6
53.4 6.0 –1.7 46.5 1.9 10.3
47.1 1.8 10.2
14.4 1.3
38.2 4.7 16.3 25.8 1.5 16.7d
46.9 1.7 12.6d
Not high risk
31.9 4.6 10.2 19.1 1.3 14.7d
44.3 1.9 17.8d
31.7 4.8
36.5 2.1 15.4d
High-risk statuse High risk
31.1 1.7 13.9d
Overall 27.2 1.4 16.6d
16.2 1.3
Characteristics 20.6 1.3 14.4d
2004–2005 2005–2006 2006–2007 2007–2008 2008–2009 2009–2010 2010–2011 2011–2012 (n55,159) (n57,941) (n56,849) (n56,541) (n55,203) (n59,325) (n58,460) (n58,691) Percent Percent Percent Percent Percent Percent Percent Percent 95% CI 95% CI 95% CI 95% CI 95% CI 95% CI 95% CI 95% CIa Changeb Change Change Change Change Change Change
NHIS
NIS-Flu
4.0 0.5
5.2 0.5
5.3 1.0
3.5 1.1
5.0 0.5
3.9 1.0
4.9 0.6
31.9 2.7
41.3 1.9
56.2 3.9
74.6 2.5 16.4d 63.3 2.3 12.7 54.2 1.4 –0.5 33.7 1.6 –0.8
NA
NA
51.5 1.0 0.5
continued on p. 421
68.2 2.4 18.5d 60.6 2.3 14.4 54.7 1.5 113.4d 34.5 1.4 12.6
NA
NA
59.7 3.7
NA
51.0 0.9 17.3d NA
43.7 0.9
2009–2010 2010–2011 2011–2012 Trend testc (n5149,872) (n5116,799) (n596,254) Percent Percent Slope Percent 95% CI 95% CI 95% CI (95% CI) Change Change
Table. Influenza vaccination coverage (at least one dose) among children aged 6 months–17 years, by influenza season, data source, high-risk status, age, and racial/ethnic group: NHIS and NIS-Flu, U.S., 2004–2005 through 2011–2012 influenza seasons
Public Health Reports / September–October 2014 / Volume 129 39.8 4.3 17.6d 33.2 2.9 14.7d 37.7 5.5 13.0 48.9 8.7 18.1
45.3 3.1 15.5 d 42.5 2.5 19.3d 42.7 4.2 15.0 55.5 7.8 16.6
50.5 3.5 15.2d 44.7 2.2 12.2 46.6 4.9 13.9 51.6 5.3 –3.9
50.2 3.3 –0.3 44.1 2.6 –0.6 47.6 3.8 11.0 56.7 5.6 15.1
5.1 0.9
4.8 0.6
4.7 0.6
5.0 0.6
53.6 3.1
37.0 2.6
43.2 0.9
46.9 2.6
55.1 2.6 18.2 d 48.5 1.0 15.3d 50.8 2.9 113.8d 57.1 2.9 13.5
59.5 2.5 14.4 d 47.6 1.0 –0.9 53.7 2.9 12.9 53.6 2.8 –3.5
2009–2010 2010–2011 2011–2012 Trend testc (n5149,872) (n5116,799) (n596,254) Percent Percent Slope Percent 95% CI 95% CI 95% CI (95% CI) Change Change
NIS-Flu
Change in percentage points compared with the previous influenza season
Statistically significant at p0.05. Pair-wise comparisons between adjacent influenza seasons were conducted using t-tests.
NA 5 not available
CI 5 confidence interval
NIS-Flu 5 National Immunization Survey-Flu
NHIS 5 National Health Interview Survey
f
Age on November 1
e
High-risk status was defined based on parental report of one or more of the following: ever being told by a physician that the child had cystic fibrosis, sickle cell anemia, diabetes, congenital heart disease, other heart conditions, cerebral palsy, muscular dystrophy, or seizures; or reporting an asthma episode or attack in the past 12 months. This definition was based on Advisory Committee on Immunization Practices recommendations and the questions available in NHIS.
d
c
Tests for linear trend were performed using a weighted linear regression on the season-specific estimates, using season number as the independent variable and weights as the inverse of the estimated variance of the estimated vaccination coverage. The estimated slope coefficients were interpreted as the average change across seasons assuming a linear increase. Slopes and their 95% CIs are presented; all of the tests for linear trend were significant at p0.001.
b
a Estimates obtained using Kaplan-Meier survival analysis methods and reported with CI half-widths. Estimates for the 2009–2010 season include only the seasonal influenza vaccine and exclude the 2009 H1N1 vaccine.
Non-Hispanic other 20.5 4.8
Non-Hispanic black 15.6 3.1
Non-Hispanic white 15.0 1.7
32.2 3.3 13.3 28.5 2.3 12.9 34.7 4.4 16.8d 40.8 6.9 16.9
Race/ethnicity Hispanic 28.9 2.8 17.3d 25.6 2.1 16.6d 27.9 4.3 16.4d 33.9 6.1 14.0
18.6 2.8
Characteristics 21.6 2.9 13.0 19.0 1.8 14.0 d 21.5 3.3 15.9d 29.9 5.1 19.4d
2004–2005 2005–2006 2006–2007 2007–2008 2008–2009 2009–2010 2010–2011 2011–2012 (n55,159) (n57,941) (n56,849) (n56,541) (n55,203) (n59,325) (n58,460) (n58,691) Percent Percent Percent Percent Percent Percent Percent Percent 95% CI 95% CI 95% CI 95% CI 95% CI 95% CI 95% CI 95% CIa Changeb Change Change Change Change Change Change
NHIS
Table (continued). Influenza vaccination coverage (at least one dose) among children aged 6 months–17 years, by influenza season, data source, high-risk status, age, and racial/ethnic group: NHIS and NIS-Flu, U.S., 2004–2005 through 2011–2012 influenza seasons
422 Research Articles
Figure 1. Influenza vaccination coveragea (at least one dose) among children aged 6 months–17 years, by influenza season and high-risk status:b NHIS, U.S., 2004–2005 through 2011–2012 influenza seasons
a Estimates obtained using Kaplan-Meier survival analysis methods and reported with confidence interval half-widths. Estimates for the 2009–2010 season include only the seasonal influenza vaccine and exclude the 2009 H1N1 vaccine.
Based on ACIP recommendations and the questions available in NHIS, high-risk status was defined based on parental report of one or more of the following: ever being told by a physician that the child had cystic fibrosis, sickle cell anemia, diabetes, congenital heart disease, other heart conditions, cerebral palsy, muscular dystrophy, or seizures; or reporting an asthma episode or attack in the past 12 months.
b
Statistically significant at p0.05 based on comparison of high-risk with non-high-risk estimate
c
NHIS 5 National Health Interview Survey ACIP 5 Advisory Committee on Immunization Practices
Trends in influenza vaccination coverage by age group, NHIS Within each age group studied using NHIS data, influenza vaccination coverage increased from the 2004–2005 influenza season to the 2011–2012 season (trend test p0.001 each) (Table). The differences between adjoining seasons are shown in the Table. Children aged 6–23 months had higher influenza coverage compared with the older age groups during the influenza seasons studied, except for the 2009–2010 and 2011–2012 seasons, in which coverage was not significantly different from coverage in children aged 2–4 years (all p0.05 except for the 2009–2010 and 2011–2012 seasons). Children aged 2–4 years had higher coverage than older children for all influenza seasons; likewise, children aged 5–12 years had higher coverage than children aged 13–17 years for all influenza seasons studied (Table, Figure 2).
Trends in influenza vaccination coverage by race/ethnicity, NHIS Within all four racial/ethnic groups studied using NHIS data, influenza vaccination coverage increased from the 2004–2005 influenza season to the 2011–2012 season (trend test p0.001 each). The change in vaccination coverage from one season to the next within each group is indicated in the Table. As shown in Figure 3, in seven of the eight seasons studied, there were no statistically significant differences in influenza vaccination coverage between nonHispanic black and non-Hispanic white children; in the 2007–2008 season, non-Hispanic black children had higher coverage than non-Hispanic white children. Hispanic children had higher influenza vaccination coverage than non-Hispanic white children in the 2004– 2005, 2008–2009, 2010–2011, and 2011–2012 seasons. Influenza vaccination coverage among n on-Hispanic
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black and Hispanic children did not differ significantly during any season. Non-Hispanic children of other or multiple races had higher influenza vaccination coverage than non-Hispanic white children during all influenza seasons studied. Non-Hispanic children of other or multiple races also had higher coverage than non-Hispanic black and/or Hispanic children in most influenza seasons. NHIS vs. NIS-Flu NHIS and NIS-Flu estimates were compared overall, within age groups, and within each racial/ethnic group. Of the 27 comparisons (Figure 4), 10 had significant differences between estimates from the two surveys. Of these 10 differences, nine showed that the estimates from NIS-Flu were higher than those from NHIS (percentage point differences ranged from 3.5 to 9.3). The remaining difference was in the 2009–2010 influenza
season among non-Hispanic black children, with a higher estimate from NHIS compared with NIS-Flu. The remaining 17 comparisons were not statistically different. Similar to NHIS, NIS-Flu estimates by age group each season indicated decreasing vaccination rates with increasing age group (Figure 2). Based on NISFlu data, non-Hispanic white children had higher coverage than non-Hispanic black children during the 2009–2010 influenza season, but there was no difference in the 2010–2011 season, and then non-Hispanic black children had higher coverage than non-Hispanic white children in the 2011–2012 season (Figure 3). Hispanic children had higher influenza vaccination coverage than non-Hispanic white children during the 2009–2010, 2010–2011, and 2011–2012 influenza seasons based on NIS-Flu data. Based on NIS-Flu estimates, Hispanic children had higher influenza vaccination
Figure 2. Influenza vaccination coveragea (at least one dose) among children aged 6 months–17 years, by influenza season and age group:b,c NHIS and NIS-Flu, U.S., 2004–2005 through 2011–2012 influenza seasons
a Estimates obtained using Kaplan-Meier survival analysis methods and reported with confidence interval half-widths. Estimates for the 2009–2010 season include only the seasonal influenza vaccine and exclude the 2009 H1N1 vaccine. b
Age as of November 1 for each influenza season
All comparisons between the age groups within each season were statistically significant at p0.05, except for in 2009–2010 where with both NHIS and the NIS-Flu data, the 6- to 23-month age group did not differ from the 2- to 4-year age group, and in 2011–2012 with NHIS data, where the 6- to 23-month age group and the 2- to 4-year age group did not differ. c
NHIS 5 National Health Interview Survey NIS-Flu 5 National Immunization Survey-Flu
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Figure 3. Influenza vaccination coveragea (at least one dose) among children aged 6 months–17 years, by influenza season, racial/ethnic group, NHIS, and NIS-Flu: U.S., 2004–2005 through 2011–2012 influenza seasons
100 90
Percentage vaccinated
80 70 60 50 40 30 20 10 0 2004–05 2005–06 2006–07 2007–08 2008–09 2009–10 2010–11 2011–12
2009–10 2010–11 2011–12
Influenza season a Estimates obtained using Kaplan-Meier survival analysis methods and reported with confidence interval half-widths. Estimates for the 2009–2010 season include only the seasonal influenza vaccine and exclude the 2009 H1N1 vaccine. b
Statistically significant (p0.05) differences between groups are denoted as well as the direction of the difference.
NHIS 5 National Health Interview Survey NIS-Flu 5 National Immunization Survey-Flu H 5 Hispanic W 5 non-Hispanic white only O 5 non-Hispanic other or multiple race B 5 non-Hispanic black only
coverage than non-Hispanic black children in the 2009–2010, 2010–2011, and 2011–2012 seasons. Similar to NHIS, non-Hispanic children of other or multiple races had higher influenza vaccination coverage than non-Hispanic white children in all influenza seasons studied based on NIS-Flu (Figure 3). DISCUSSION Data from both NHIS and NIS-Flu demonstrate increasing influenza coverage among all children, including increases among those with and without high-risk conditions and among all age and racial/ethnic groups. This encouraging finding suggests that efforts to promote influenza vaccination among children are having a growing impact. However, estimated influenza
vaccination coverage for the 2011–2012 season was well below the Healthy People 2020 target of 70% for children aged 6 months to 17 years overall.10 It is encouraging to note, though, that more than 70% of children aged 6–23 months received at least one dose of influenza vaccine for the first time during the 2010–2011 season. Children with high-risk conditions have higher vaccination coverage than those without high-risk conditions, probably in part because providers might be more accustomed to vaccinating people with high-risk conditions due to the longer-standing recommendations and also because these children are more likely to seek health care during the period of influenza vaccination. The fact that younger children have higher coverage than older children might be related to recommendations for influenza vaccination
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initially targeting younger age groups, then expanding to older children; their higher risk of influenza-related complications relative to older children; more time for changes in provider practices; and more frequent visits to providers.23 Influenza coverage was generally similar among non-Hispanic white and non-Hispanic black children based on NHIS and NIS-Flu. In most influenza seasons, there was no difference in vaccination coverage; in one season (2009–2010, NIS-Flu), non-Hispanic white children had higher vaccination coverage, and in two seasons (2007–2008 NHIS and 2011–2012 NISFlu), non-Hispanic black children had higher vaccination coverage. Hispanic and other/multiple-race
children had coverage as high as or higher than that of non-Hispanic white children. Increased access to vaccination through the Vaccines for Children (VFC) program might contribute to higher vaccination of these children.24 Beginning with the 2003–2004 flu season, ACIP voted to include annual influenza vaccination for children 6–23 months of age in the VFC program (it was not covered during the 2002–2003 season).25 Subsequently, as more child age groups were added to the influenza recommendation, the age groups were also added to the VFC resolution for influenza. The VFC program has been an important contributor to successfully achieving high coverage levels of routinely recommended vaccines for children
Figure 4. Comparison of survey estimatesa of influenza vaccination coverage (at least one dose) among children aged 6 months–17 years, by influenza season, age group, and race/ethnicity: NHIS and NIS-Flu, U.S., 2009–2010 through 2011–2012 influenza seasons
b b
a Estimates obtained using Kaplan-Meier survival analysis methods and reported with confidence interval half-widths. Estimates for the 2009–2010 season include only the seasonal influenza vaccine and exclude the 2009 H1N1 vaccine. b
Statistically significant (p0.05) differences between groups are denoted.
NHIS 5 National Health Interview Survey NIS-Flu 5 National Immunization Survey-Flu m 5 months y 5 years
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by providing publicly purchased vaccines to providers for use in children who are (1) Medicaid-eligible, (2) uninsured, (3) American Indian or Alaska Native, or (4) covered by health insurance that does not cover the cost of vaccine, when the child is served at a Federally Qualified Health Center or Rural Health Center.26 While no racial/ethnic disparities exist for influenza vaccination coverage among children, these disparities persist among adults.27 Based on data from NHIS and NIS-Flu, overall trends in influenza vaccination coverage among children aged 6 months–17 years were similar. There were some differences by data source in estimated coverage from one influenza season to the next and in patterns of differences by race/ethnicity. Differences between NHIS and NIS-Flu estimates suggest that NIS-Flu estimates are likely slightly biased upward compared with NHIS estimates, because although two-thirds of the estimates were not statistically significant, of the onethird that were, the point differences ranged from 3.5 to 9.3 higher for NIS-Flu. Differences between NHIS and NIS-Flu that may contribute to systematic differences in estimates include survey mode (face-to-face vs. telephone survey), response rate (61% vs. 30%–74% landline/20%–36% cell phone), weighting methodology, or survey question wording. Random survey variation also contributes to differences. Both NIS-Flu and NHIS estimates are subject to error from misclassification of children’s vaccination status reported by parents.28 Because NHIS has a more complete sample frame (including households with no type of telephone service) and higher response rates, the estimates may be more representative. On the other hand, national estimates from NIS-Flu are more precise than from NHIS due to a larger sample size. The timeliness of NIS-Flu and the allowance of the production of routine state-level estimates make NIS-Flu useful for public health action, keeping in mind that the estimates have a slight upward bias. While NHIS and NIS-Flu are the primary sources for monitoring influenza vaccination coverage among children, there are some other data sources that can provide additional information not available with NHIS and NIS-Flu. These sources include the Behavioral Risk Factor Surveillance System optional child influenza module;29,30 the National Flu Survey (NFS), previously named the Rapid Flu Survey; and Immunization Information Systems (IISs). The NFS included questions on knowledge and attitudes toward influenza disease and vaccination, as well as reasons for vaccination and non-vaccination.31–33 IISs have been used to monitor provider report of influenza vaccination coverage among children and are particularly useful
for local area estimates and for obtaining two-dose influenza coverage; however, not all states have equally functional IISs.34 Limitations The findings in this article are subject to at least three limitations. First, influenza vaccination estimates were based on parental report rather than medical records and may be subject to recall bias. Studies have shown that parental report overestimates influenza vaccination coverage compared with medical records.35–37 Second, during the 2009–2010 season, respondents may have misclassified receipt of the seasonal vs. the H1N1 influenza vaccine. Third, receipt of two doses of influenza vaccine was not evaluated in this study; as such, results may differ when two-dose coverage is evaluated.38 CONCLUSION Influenza vaccination coverage among children continues to increase. However, based on data through the 2011–2012 influenza season, only slightly less than half of children in the U.S. were vaccinated against influenza. Although vaccination levels have increased substantially since 2004, much improvement is needed to ensure that all children aged $6 months are vaccinated annually against influenza. Strategies that have been shown to improve influenza vaccination coverage include reminder/recall systems and standing orders. The Community Guide to Preventive Services provides information on effective strategies to increase the use of recommended vaccinations, including influenza vaccination.39 The findings and conclusions in this article are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention (CDC). Institutional Review Board approval was obtained for the National Health Interview Survey and National Immunization Survey-Flu by the National Center for Health Statistics, CDC.
REFERENCES 1. Burney LE. Influenza immunization: statement. Public Health Rep 1960;75:944. 2. Prevention and control of influenza: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep 2002;51(RR-3):1-36. 3. Harper SA, Fukuda K, Uyeki TM, Cox NJ, Bridges CB. Prevention and control of influenza: recommendations of the Advisory Committee on Immunization Practices (ACIP) [published erratum appears in MMWR Morb Mortal Wkly Rep 2004;53(32):743]. MMWR Recomm Rep 2004;53(RR-6):1-40. 4. Smith NM, Bresee JS, Shay DK, Uyeki TM, Cox NJ, Strikas RA. Prevention and control of influenza: recommendations of the Advisory Committee on Immunization Practices (ACIP) [published erratum appears in MMWR Morb Mortal Wkly Rep 2006;55(29):800]. MMWR Recomm Rep 2006;55(RR-10):1-42.
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5. Prevention and control of seasonal influenza with vaccines: recommendations of the Advisory Committee on Immunization Practices (ACIP), 2008. MMWR Recomm Rep 2008;57(RR-7):1-60. 6. Fiore AE, Uyeke TM, Broder K, Finelli L, Fuler GL, Singleton JA, et al. Prevention and control of influenza with vaccines: recommendations of the Advisory Committee on Immunization Practices (ACIP), 2010 [published erratum appears in MMWR Morb Mortal Wkly Rep 2010;59(31):993]. MMWR Recomm Rep 2010;59(RR-8):1-62. 7. Grohskopf LA, Shay DK, Thimabukuro TT, Sokolow LZ, Keitel WA, Bresee JS, et al. Prevention and control of seasonal influenza with vaccines: recommendations of the Advisory Committee on Immunization Practices (ACIP)—United States, 2013–2014 [published erratum appears in MMWR Morb Mortal Wkly Rep 2013;62(45):906]. MMWR Recomm Rep 2013;62(RR-7):1-43. 8. Use of influenza A (H1N1) 2009 monovalent vaccine: recommendations of the Advisory Committee on Immunization Practices (ACIP), 2009. MMWR Recomm Rep 2009;58(RR-10):1-8. 9. Centers for Disease Control and Prevention (US). National Health Interview Survey: questionnaires, datasets, and related documentation: 1997 to the present [cited 2013 Apr 12]. Available from: URL: http://www.cdc.gov/nchs/nhis/quest_data_related_1997_forward .htm 10. Department of Health and Human Services (US). Healthy people 2020: topics & objectives—immunization and infectious diseases [cited 2013 Jul 26]. Available from: URL: http://www.healthypeople .gov/2020/topicsobjectives2020/objectiveslist.aspx?topicid=23 11. Centers for Disease Control and Prevention (US). Seasonal influenza (flu): 2012–13 state and regional vaccination trend report [cited 2014 May 8]. Available from: URL: http://www.cdc.gov/flu /fluvaxview/reports/reporti1213/trends/index.htm 12. Centers for Disease Control and Prevention (US). Seasonal influenza (flu): flu vaccination coverage, United States, 2012–13 influenza season [cited 2014 May 18]. Available from: URL: http://www.cdc .gov/flu/fluvaxview/coverage-1213estimates.htm 13. Centers for Disease Control and Prevention (US). National Health Interview Survey, survey questionnaires [cited 2013 Nov 7]. Available from: URL: ftp://ftp.cdc.gov/pub/Health_Statistics/NCHS /Survey_Questionnaires/NHIS 14. Lu P-J, Santibanez TA, Williams WW, Zhang J, Ding H, Bryan L, et al. Surveillance of influenza vaccination coverage—United States, 2007–08 through 2011–12 influenza seasons. MMWR Surveill Summ 2013;62(SS-4):1-29. 15. Santibanez TA, Singleton JA, Santibanez SS, Wortley P, Bell BP. Socio-demographic differences in opinions about 2009 pandemic influenza A (H1N1) and seasonal influenza vaccination and disease among adults during the 2009–2010 influenza season. Influenza Other Respir Dis 2012;7:383-92. 16. Interim results: influenza A (H1N1) 2009 monovalent vaccination coverage—United States, October–December 2009. MMWR Morb Mortal Wkly Rep 2010;59(early release):1-5. 17. Centers for Disease Control and Prevention (US). Season influenza (flu): final state-level monthly cumulative influenza vaccination coverage estimates for the 2009–10 season—United States, August 2009 through May 2010 [cited 2013 Nov 7]. Available from: URL: http://www.cdc.gov/flu/professionals/vaccination/reporti0910 /reportI0910 18. Centers for Disease Control and Prevention (US). Seasonal influenza (flu): flu vaccination coverage, United States, 2011–12 influenza season [cited 2013 Nov 7]. Available from: URL: http://www.cdc .gov/flu/professionals/vaccination/coverage_1112estimates.htm 19. Centers for Disease Control and Prevention (US). Final state-level influenza vaccination coverage estimates for the 2010–11 season— United States, National Immunization Survey and Behavioral Risk Factor Surveillance System, August 2010 through May 2011 [cited 2013 Nov 7]. Available from: URL: http://www.cdc.gov/flu/professionals /vaccination/coverage_1011estimates.htm
20. Smith PJ, Battaglia MP, Huggins VJ, Hoaglin DC, Roden A, Khare M, et al. Overview of the sampling design and statistical methods used in the National Immunization Survey. Am J Prev Med 2001;20 (4 Suppl):17-24. 21. SAS Institute, Inc. SAS®: Version 9.3 for Windows. Cary (NC): SAS Institute, Inc.; 2011. 22. Research Triangle Institute, Inc. SUDAAN®: Release 11.0. Research Triangle Park (NC): Research Triangle Institute, Inc.; 2012. 23. Poehling KA, Edwards KM, Griffin MR, Szilagyi PG, Staat MA, Iwane MK, et al. The burden of influenza in young children, 2004–2009. Pediatrics 2013;131:207-16. 24. Walker AT, Smith PJ, Kolasa M. Reduction of racial/ethnic disparities in vaccination coverage, 1995–2011. MMWR Surveill Summ 2014;63:7-12. 25. Childhood influenza-vaccination coverage—United States, 2002–03 influenza season. MMWR Morb Mortal Wkly Rep 2004;53(37):863-6. 26. Centers for Disease Control and Prevention (US). Vaccines for Children Program (VFC): about VFC [cited 2013 Apr 11]. Available from: URL: http://www.cdc.gov/vaccines/programs/vfc/about /index.html 27. Centers for Disease Control and Prevention (US). Recent influenza vaccination trends across influenza seasons [cited 2013 Apr 11]. Available from: URL: http://www.cdc.gov/flu/fluvaxview/trends-summary .htm 28. Brown C, Clayton-Boswell H, Chaves SS, Prill MM, Iwane MK, Szilagyi PG, et al. Validity of parental report of influenza vaccination in young children seeking medical care. Vaccine 2011;29:9488-92. 29. Centers for Disease Control and Prevention (US). Behavioral Risk Factor Surveillance System: questionnaires [cited 2013 Apr 12]. Available from: URL: http://www.cdc.gov/brfss/questionnaires .htm#about 30. Estimated influenza vaccination coverage among adults and children—United States, September 1, 2004–January 31, 2005. MMWR Morb Mortal Wkly Rep 2005;54(12):304-7. 31. Centers for Disease Control and Prevention (US). Results from the November 2010 National Flu Survey—United States, 2010–11 influenza season [cited 2013 Nov 7]. Available from: URL: http:// www.cdc.gov/flu/pdf/fluvaxview/nationalflusurvey_nov2010results .pdf 32. Centers for Disease Control and Prevention (US). Results from the March 2011 National Flu Survey—United States, 2010–11 influenza season [cited 2013 Nov 7]. Available from: URL: http://www.cdc .gov/flu/pdf/fluvaxview/fluvacsurvey.pdf 33. Centers for Disease Control and Prevention (US). National mid-season flu vaccination coverage, National Flu Survey, United States, 2011–12 influenza season [cited 2013 Nov 7]. Available from: URL: http:// www.cdc.gov/flu/professionals/vaccination/national-flu-survey .htm 34. Brief report: influenza vaccination coverage among children aged 6–23 months—six immunization information system sentinel sites, United States, 2005–06 influenza season. MMWR Morb Mortal Wkly Rep 2006;55(49):1329-30. 35. Nowalk MP, Zimmerman RK, Lin CJ, Ko FS, Raymund M, Hoberman A, et al. Parental perspectives on influenza immunization of children aged 6 to 23 months. Am J Prev Med 2005;29:210-4. 36. Shinall MC Jr, Plosa EJ, Poehling KA. Validity of parental report of influenza vaccination in children aged 6 to 59 months of age. Pediatrics 2007;120:e783-7. 37. Lu P, Dorell C, Yankey D, Santibanez TA, Singleton JA. A comparison of parent and provider reported influenza vaccination status of adolescents. Vaccine 2012;30:3278-85. 38. Yoo BK, Berry A, Kasajima M, Szilagyi PG. Association between Medicaid reimbursement and child influenza vaccination rates. Pediatrics 2010;126:e998-1010. 39. Guide to Community Preventive Services. Increasing appropriate vaccination [cited 2013 Jul 30]. Available from: URL: http://www .thecommunityguide.org/vaccines/index.html
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