Rosanna W. Setse1, Helen Ding2, Gary L. Euler3, James A. Singleton3. Missed Opportunities for Influenza Vaccination among Adults with Chronic Conditions, United States, 2009-2010 Influenza Season Rosanna W. Setse1, Helen Ding2, Gary L. Euler3, James A. Singleton3. 1Science Applications International Corporation (SAIC), 2Chenega Government Consulting LLC , 3Assessment Branch, Immunization Services Division NCIRD, CDC. National Center for Immunization & Respiratory Diseases Immunization Services Division

Influenza vaccination Each year, in the United States, serious illness, hospitalization and deaths result from influenza epidemics. Persons with chronic medical conditions are at increased risk for complications, hospitalizations and death from influenza . Annual vaccination can effectively reduce influenza-related morbidity and mortality among vulnerable person. Influenza vaccination recommended for persons with chronic conditions for several years. Healthy People 2020 objective:– 90% influenza vaccination coverage for adults with chronic/high-risk conditions. Each year, in the United States, epidemics of influenza typically occur resulting in serous illness, hospitalizations and deaths. Persons with chronic medical conditions are particularly at an increased risk for complications, hospitalizations and death from influenza . Fortunately, we have the influenza vaccine which effectively reduces influenza-related morbidity and mortality among vulnerable persons when vaccinated. Currently, the ACIP recommends influenza vaccination for all persons 6months and older. For persons with chronic medical conditions, influenza vaccination has been recommended by the ACIP for many years and one of the healthy people 2020 national influenza vaccination coverage objectives is to achieve coverage levels of 90% for adults with high risk conditions.

Influenza vaccination coverage among adults with chronic medical conditions Influenza vaccination coverage level among adults with chronic medical conditions is suboptimal. Seasonal influenza vaccination coverage for adults 18–49 yrs with high-risk conditions in the 2009-10 season was 38.2 %1. In the 2007-08 & 2008–09 seasons, influenza vaccination coverage levels among adults with high–risk conditions 18–49 years were 30.4% and 33%, respectively (NHIS data). During the 2006-2007 season, among adults aged 18-64 years with asthma, influenza vaccination coverage was 39.9% (95% CI=38.3, 41.5%)2. Despite the long-standing recommendations influenza vaccination coverage level among adults with chronic medical conditions has been suboptimal. For the 2009-10 influenza season, seasonal influenza vaccination coverage among adults 18-49years with high risk conditions was only 38%. In the 2007–08 and 2008–09 influenza seasons, estimated vaccination coverage levels (based on NHIS data) among adults with high–risk conditions aged 18–49 years were 30.4% and 33%, respectively The story is no different when we look at earlier seasons. For the 2006-2007 season, among adults aged 18-64 years with asthma, influenza vaccination coverage was only 40%.

Factors affecting influenza vaccination coverage among adults Programmatic - Existing recommendations - Vaccine availability - Reimbursement of providers Patient factors - Perceived susceptibility - Beliefs about vaccine effectiveness - Concerns about vaccine safety -- Health insurance coverage - Health visits during influenza season Provider - Provider personal beliefs/practices - Use of recall /reminder systems - Missed opportunities Several factors contribute to the low influenza vaccination coverage among adults with high risk conditions. These include programmatic/policy related factors such as Existing recommendations, Vaccine availability And timely reimbursement of providers Patient related factors also affect influenza vaccination coverage among adults. These include: Beliefs about susceptibility - Beliefs about vaccine effectiveness - Concerns about vaccine safety, - Procrastination - Health insurance coverage - Health visits during influenza season Finally, provider related factors such as: - Provider personal beliefs Lack of recall/reminder systems - Missed opportunities, which is really the focus of this presentation, All affect infleunza vaccination coverage among adults

Missed Opportunities Definition: Failure to administer recommended vaccines to un-vaccinated patients who present for medical care. Previous studies among children and adults indicate opportunities for influenza vaccination are often missed3. Few studies have evaluated missed opportunities for influenza vaccination among adults with chronic conditions. 1999 NHIS data:- Only 46% of high-risk patients with a physician encounter in 1998 received influenza vaccine (). Missed opportunities more common for blacks and younger patients3. In the vaccination world, Missed vaccination opportunities is often defined as failure to administer recommended vaccines to un-vaccinated patients who present for medical care. A number of studies have examined missed opportunities for vaccination among children and among adults. These indicate that opportunities for influenza vaccination are often missed. However, few have evaluated missed opportunities for influenza vaccination among adults with high risk conditions who are at and increased risk for influenza complications (e.g., during hospitalizations for other causes). 1999 Nhis data indicate that, among high risk patients with a physician encounter in 1998, only 46% received influenza vaccination and missed opportunities were more common for blacks and younger patients.

Objectives To examine missed opportunities for seasonal influenza vaccination among adults with high-risk conditions in the 2009-10 influenza season. To examine reasons for non-vaccination and attitudes / opinions of non-recipients of influenza vaccine. To identify correlates of missed influenza vaccination opportunities among adults with high-risk conditions during the 2009-10 influenza season in the United States.

Methods The National H1N1 Flu Survey (NHFS) List-assisted random digit-dial telephone (landline and cell phones) survey conducted in all 50 states and the District of Columbia October 2009- June 2010. Households were screened into the survey based on the presence of a household member aged ≥18 years. The Council of American Survey and Research Organizations (CASRO) response levels for landline and cellular telephones - 35% and 27%; cooperation levels - 45% and 57%, respectively. Provided state-specific estimates of seasonal influenza and influenza A (H1N1) 2009 monovalent vaccination coverage in the 2009-10 season. The survey collected information on demographics, influenza vaccination, opinions and attitudes and intent.

Methods Eligibility criteria: - Variables of interest: – Adults 18 - 64 years with ≥1 chronic conditions* interviewed April through June 2010 Variables of interest: – Vaccination variables: Receipt of seasonal flu vaccination since August 2009, vaccination month, shot or spray and receipt of HCP recommendation for vaccination. Demographics: - Age, race/ethnicity, gender, state of residence, educational level and medical insurance . Opinions and attitudes related to seasonal and pandemic influenza, vaccination intention and recent respiratory illness Adults 18 - 64 yrs with at least one chronic condition who were enrolled in NHFS and and interviewed April through June 2010 were eligible for this study. For our analysis, we were interested in vaccination variables including: Receipt of seasonal flu vaccination since August 2009, vaccination month, number of doses and type of vaccine ie shot or spray. Socio-demographic variables of interest included: Age, race/ethnicity, gender, state of residence, educational level and medical insurance coverage. The other variables of interest were Opinions and attitudes related to seasonal and pandemic influenza, vaccination intention and recent respiratory illness. *Asthma, lung condition other than asthma, heart condition, diabetes, kidney or liver condition, weakened immune system caused by a chronic illness or medicines taken for a chronic illness

Statistical Analysis Examined demographics of study population: age (18-49 years & 50-64 years) gender (categorized as males, females) race/ethnicity (non-Hispanic black, non-Hispanic white, Hispanic & other) educational level (<12years, 12 years, some college or college graduate) medical insurance status (Yes/No) ≥1 health care visit since August 2009 (Yes/No) Recommendation of influenza vaccination by HCP Compared selected demographics characteristics by seasonal influenza vaccination receipt using chi-square tests. Determined probability of un-vaccination among persons with no health care visit ≥1 health-care visit with HCP recommendation for vaccination ≥1 health care visit and no HCP recommendation for vaccination First, we examined the baseline demographics of the study population and compared selected demographics by seasonal infleunza vaccination using chi-squared tests. Next we determined the probability of unvaccination among persons with: no health care visit ≥1 health-care visit with HCP recommendation for vaccination ≥1 health care visit and no HCP recommendation for vaccination

Statistical Analysis Among participants ≥1 health care visit: Determined the prevalence of missed vaccination opportunities (i.e. ≥1 healthcare visit since August 2009, but no HCP recommendation for influenza vaccination and no influenza vaccination) Determined correlates of missed vaccination opportunities using univariate and multivariable logistic regression models. Final model included variables significant at p< 0.05 in univariate analysis. Compared opinions/attitudes’ and reasons for non-vaccination among recipients and non-recipients of HCP recommendation for influenza vaccination. Analyses conducted using SAS version 9.1 and SUDAAN. Data weighted to reflect the demographic distribution of the US non-institutionalized civilian population.

Study Population Missed opportunity for Influenza vaccination Adults 18-64 years, High- risk conditions N=4341 ≥1 Health visit* (83.5%) HCP† recommendation for vaccination (48.9%) Vaccinated Un-vaccinated No HCP† recommendation for vaccination (51.1%) No Health visit* (16.5%) This flow chart shows how the study population was divided. We had approx 4300 eligible adults with hrc in our study. Over 80% had at least 1 health visit since August 2009. Of those with > 1 visit, approximately half received a hcp recommendation for vaccination and half did not. Persons who had >1 visit, no hcp recommendation and remained unvaccinated were classified as missed opportunities. Missed opportunity for Influenza vaccination since August 2009 † Health care personnel

Results: Influenza vaccination among adults 18-64 years, with high risk medical conditions, NHFS, April -June 2010 Overall, influenza vaccination coverage in our population of adults with Hrc was 55%. 27% had a missed opportunity for vaccination. 10% remained unvaccinated in-spite of receive a hcp recommendation And 8.2% were unvaccinated and had no visit

Results: Influenza vaccination coverage by receipt of healthcare personnel (HCP) recommendation for vaccination, adults 18-64 years with ≥1 health visit, NHFS, April -June 2010 We found that persons who received hcp recommendation were significantly more likely to have been vaccinated than those who did not receive hcp recommendations

Contribution of no health visit and ≥1 health visit with or without HCP* recommendation to un-vaccination among adults 18-64 with high risk medical conditions, NHFS, April -June 2010 We examined factors that contributed to unvaccination among adults with chronic conditions across the different demographic characteristics. The factors we examined were no health visits, at least 1 health visit with HCP recommendation for vaccination and at least 1 health visit with no hcp recommendation for influenza vaccination. We found that in all demographic strata, the greatest contributory factor to un-vaccination was missed opportunities ie persons with at least 1 health visit but no hcp recommendation for influenza vaccination and no vaccination. * Health care personnel

* High-Risk conditions Bivariate associations between missed influenza vaccination opportunities and selected baseline characteristics, adults 18-64 years with high-risk conditions and ≥1 health visit, NHFS, April -June 2010 18-49 yrs vs. 50-64 yrs Males vs. Females N-H black vs. white Hispanic vs. white N-H other vs. white <12 years education vs. college grad 12 years education vs. college grad Some college vs. college grad Asthma vs. other HRC* No medical insurance vs. have insurance Bivariate analysis showed a significant association between mvo and all selected baseline demographics except non-H other versus white race/ethnicity. * High-Risk conditions

Multivariable analysis: Association between missed influenza vaccination opportunities and selected baseline characteristics, adults 18-64 yrs with high-risk conditions & ≥1 health visit, NHFS, April -June 2010 18-49 yrs vs. 50-64 yrs Males vs. Females N-H black vs. white Hispanic vs. white N-H other vs. white <12 years education vs. college grad 12 years education vs. college grad Some college vs. college grad Asthma vs. other HRC* No medical insurance vs. have insurance In multivariable analysis, adults 18-49 years were significantly more likely to have a mvo compared to adults 50-64 years and males were more likely to have a mvo compared to females. We found a marginally significant independent associations between race/ethnicity and missed opportunities with blacks and hispanics more likely to have a missed opportunity compared to whites. Persons who had <12 years of education were significantly more likely to have a mvo and finally those with no medical insurance were more likely to have a mvo compared to those with no health insurance.

Reasons for non-vaccination among adults (18-64 years) with high risk medical conditions and ≥1 health visit by receipt of health care personnel (HCP) recommendation for influenza vaccination, NHFS, April -June 2010 2010 This slide shows reasons for non-vaccination among those with at least 1 visit, by receipt of hcp recommendations. We found that persons who did not receive hcp recommendation were more likely to think vaccination was not needed and those who received a hcp recommendation but were unvaccinated were more likely to indicate vaccine unavailability was the reason for non vaccination

Attitudes of non-recipients of seasonal influenza vaccination by health care personnel (HCP) recommendation for vaccination, adults 18-64 years with high risk medical conditions, NHFS, April -June 2010 This slide also shows that those who received a hcp recommendation but did not get vaccinated were more worried about getting influenza than those who did not receive a hcp recommendatin for vaccination.

Summary No health visits, lack of recommendation for vaccination during visits and personal choice contributed to low seasonal influenza vaccination coverage among adults with high risk conditions in the 2009-10 season. Missed opportunities for vaccination - greatest measured contributory factor to un-vaccination among persons with HRCs. Younger adults (18-49 years), males, Hispanics, persons <12 years of education and those without medical insurance more likely to have missed vaccination opportunities. HCP recommendation for vaccination were associated with opinions and attitudes of persons with HRCs. A sizable sub-group of persons with HRC presenting for care may be unwilling to get vaccinated in the absence of outreach efforts. No health visits, lack of recommendation for vaccination during medical visits and attitudes of patients all contribute to low vaccination coverage among adults with HRCs Although the majority of persons with high-risk conditions accessed health care during the influenza season, missed opportunities for influenza vaccination were common and was the greatest contributory factor to un-vaccination among persons with HRCs Younger adults (18-49 years), males, Hispanics, persons <12 years of education and those without medical insurance more likely to have missed vaccination opportunities. Our findings underscore the importance of provider-based recommendations for vaccination and suggest recommendations from HCP play a role in positively shaping the opinions and attitudes of adults with high-risk conditions. Our results also show that there is a sizable subgroup of patients who see health care providers during the vaccination season, but may be unwilling to get vaccinated in the absence of outreach efforts aimed at overcoming their resistance.

Limitations Influenza vaccination and HCP recommendations for vaccination were self-reported and were subject to recall bias. We did not have information on the nature of health visits (i.e. sick visit or check-up). Could not assess causality between HCP recommendation and opinions/attitudes of participants BRFSS estimates did not include households with only cellular telephone service. Response rates for NHFS were low and non-response bias can remain even after weighting adjustments. Our study has a number of limitations. First, influenza vaccination status and HCP recommendations for vaccination were self-reported (as opposed to determined from medical records or other direct measurements) and may have been subject to recall bias. Self-report of influenza vaccination among adults, has however been found to be a valid source of information on vaccination status We also did not have information on the nature of medical visits. It is possible some of these missed vaccination opportunities occurred during acute care visits when vaccination for influenza may not have been paramount BRFSS estimates did not include households with only cellular telephone service. Households with only cellular telephone service are more likely to have younger occupants, minorities and renters whose vaccination levels may be lower than among those living in other households. Response rates for BRFSS and NHFS were low and non-response bias can remain even after weighting adjustments to reflect the national population sub-group distribution and non-response.

Public Health significance Interventions aimed at improving coverage and reducing missed opportunities for vaccination particularly among risk groups identified are needed: Promote provider recommendations for influenza vaccination Educate adults with high-risk conditions about the importance of influenza vaccinations Addressing concerns about vaccine safety Encourage patients to seek out vaccination information from their providers More research needed to explain causes of racial and demographic disparities in missed opportunities. We demonstrated that missed opportunities are common among adults with hrcs and interventions targeted at improving influenza vaccination coverage, reducing missed opportunities for vaccination, and eliminating racial/ethnic and other socio-demographic disparities in vaccination coverage are needed: These include reminding HCP about importance of recommending influenza vaccination and educating adults with high-risk conditions about the importance of influenza vaccinations. Messages aimed at addressing concerns about vaccine safety and encouraging patients to seek out vaccination information from their providers and vaccination at alternate settings.

Helen Ding, Gary L. Euler, James A. Singleton Acknowledgments Co-authors: Helen Ding, Gary L. Euler, James A. Singleton NORC – Ken Copeland Margrethe Montgomery Nick Davis CDC NCIRD ISD – Amparo Gonzalez-Feliciano Carla Black Carolyn Furlow Cindy Weinbaum Liz Monsell Leah Bryan Peng-Jun Lu Stacie Greby Tammy Santibanez

Thank-you. Rosanna W. Setse rsetse@cdc.gov Disclaimer: The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the Centers for Disease Control & Prevention.

References Final estimates for 2009-10 Seasonal Influenza and Influenza A (H1N1) 2009 Monovalent Vaccination Coverage — United States, August 2009 through May, 2010. Available at http://www.cdc.gov/flu/professionals/vaccination/vaccinecoverage.htm Lu PJ, Euler GL, Callahan DB. Influenza vaccination among adults with asthma findings from the 2007 BRFSS survey. Am J Prev Med 2009;37(2):109-15. Maurer J, Harris KM, Lurie N. Reducing missed opportunities to vaccinate adults against influenza: what is realistic? Arch Intern Med 2009;169(17):1633-4. Egede LE, Zheng D. Racial/ethnic differences in influenza vaccination coverage in high-risk adults. Am J Public Health 2003;93(12):2074-8.

Influenza vaccination rates, adults (18-64 years) with high-risk medical conditions – United States, NHFS, March-June 2010 Un-wgt’d sample wgt'd % Vaccinated n wgt'd % p-value Age (years) 18-49 1961 57.1 889 37.4 <.0001 50-64 2380 42.9 1456 59.5 Gender Male 1577 42.2 807 43.3 0.03 Female 2764 57.8 1538 49.5 Race/Ethnicity Hispanic 263 12.2 117 32.6 <.001 Non-Hispanic white 3327 66.1 1868 50.9 Non-Hispanic black 475 15.2 206 38.4 Other 276 6.5 154 52.8 Education < 12 years 435 13.1 189 32.1 12 years 1007 24.5 507 46.5 Some College 1296 30.6 687 46.2 College Graduate 1487 31.9 915 55.4 High-risk medical condition Asthma 1788 41.7 961 44.4 0.12 Other conditions 2553 58.3 1384 48.7 Medical Insurance coverage Yes 3674 83.8 2121 51.8 No 557 16.2 179 24.2 Health care visit since Aug 09 None 630 16.8 279 32.8 At least one 3708 83.5 2064 49.7

Probability of un-vaccination given no health visit and ≥1 health visit with or without HCP* recommendation for influenza vaccination by socio-demographics, adults 18-64 years, with high risk medical conditions, NHFS, April -June 2010 * Health care personnel