Abstract
Introduction:
Understanding patient factors associated with not being vaccinated is essential for successful implementation of influenza vaccination programs.
Methods:
We enrolled adults hospitalized with severe acute respiratory illness at 10 United States (US) hospitals during the 2019–2020 influenza season. We interviewed patients to collect data about influenza vaccination, sociodemographic characteristics, and vaccine perceptions.
Results:
Among 679 participants, 264 (38.9%) reported not receiving influenza vaccination. Among those not vaccinated, 135 (51.1%) reported choosing not to receive a vaccine because of perceived ineffectiveness (36.7%) or risk (14.4%) of influenza vaccination. Sociodemographic factors associated with not being vaccinated included no medical insurance (aOR=6.42; 95% CI: 2.52–16.38) and being non-White or Hispanic (aOR=1.54, 95% CI: 1.02–2.32).
Conclusions:
Optimizing uptake of influenza vaccination in the US may be improved by educational programs regarding vaccine safety and effectiveness and enhancing vaccine access, particularly among non-White and Hispanic Americans and those without medical insurance.
Keywords: vaccination, vaccine hesitancy, vaccine acceptance, influenza, medical insurance
Introduction
During the 2019–2020 influenza season, approximately 34–47 million people in the United States (US) suffered symptomatic influenza infection, 350,000–500,000 were hospitalized, and 18,000–29,000 died.1–3 Influenza vaccination is recommended each year for everyone in the US at least six months old without a contraindication to vaccination.4 Vaccine effectiveness against medically attended disease varies from year to year with estimates ranging from 19% to 60% over the past decade.5 Despite variable effectiveness, influenza vaccination is a cost-effective intervention to reduce morbidity and mortality, and increasing vaccine coverage would likely improve population health.4,6–9 However, the proportion of Americans who receive a seasonal influenza vaccine has remained less than 50%.7,8
Vaccine hesitancy is defined by the World Health Organization Strategic Advisory Group of Experts as the “delay in acceptance or refusal of vaccination despite availability.”10 Prior studies among outpatients found that factors that drive vaccine hesitancy include concerns about vaccine safety and efficacy, a perceived risk of influenza infection from the vaccine itself, and distrust of the healthcare system.9,11,12 Further, many patients do not perceive themselves of being at risk for influenza infection or severe illness from influenza.9
In this study, we build on prior work from the outpatient setting to evaluate patient characteristics and perceptions associated with failure to receive an influenza vaccine among severely ill US patients hospitalized for acute respiratory illness. Understanding factors associated with not being vaccinated in this population is important because these patients are the most likely to suffer severe complications and die from influenza. Furthermore, they tend to have higher burden of medical comorbidities than outpatients, potentially leading to higher perceived risk of severe influenza as motivation for obtaining influenza vaccination.
Methods
Setting
This study was a secondary analysis of an observational case-control vaccine effectiveness study13 conducted by the Influenza and Other Viruses in the Acutely Ill (IVY) Network, which is a collaborative clinical research network among academic medical centers in the US and the Centers for Disease Control and Prevention (CDC).13,14 Patients were enrolled at 10 hospitals in the IVY Network between October 10, 2019 and February 28, 2020. Enrolling hospitals were academic referral hospitals located in urban areas (Table S1). The study was funded by CDC and approved by the single institutional review board at Vanderbilt University Medical Center. Written informed consent was obtained from each patient or a legally authorized representative.
Population
The study population included adults hospitalized with severe acute respiratory infection, defined as hospitalization for an acute illness (symptoms ≤7 days) with ≥1 sign or symptom of infection and ≥1 sign or symptom of respiratory illness (full eligibility criteria are listed in Table S2). All enrolled patients underwent influenza testing both by clinical tests at the enrolling hospital and in a central research laboratory by reverse transcriptase polymerase chain reaction.13 Patients who tested positive for influenza by either a clinical or central test were classified as having influenza infection while those who tested negative by all influenza testing were classified as not having influenza infection. Details of the enrollment methodology are presented in Table S3.
Data Collection
Prospective data collection included review of the medical record and an interview with the patient or a surrogate if the patient was not able to answer questions about his/her medical history. Sociodemographic data collected included self-reported race and ethnicity, medical insurance status, and chronic medical conditions. Vaccination status was classified based on self-report of receiving a 2019–2020 influenza vaccine before hospital admission for the acute illness.
For patients who reported receiving an influenza vaccine, we asked them the primary reason why they received it, using the following answer options: 1) I believe the influenza vaccine is important for my health; 2) My doctor suggested I get the influenza vaccine; 3) I saw an advertisement for the influenza vaccine; 4) I believe getting the influenza vaccine is important to keep others healthy; 5) free text for any answer.
For patients who reported not receiving an influenza vaccine, we asked them the primary reason why they did not receive it, using the following answer options: 1) I don’t believe the influenza vaccine is important for my health; 2) I received the influenza vaccine in the past and still got the flu; 3) I think the influenza vaccine is dangerous for me; 4) I didn’t know that I should get the influenza vaccine; 5) The influenza vaccine costs too much money; 6) I was unable to get to a location that gives influenza vaccines; 7) I meant to get the influenza vaccine but never got around to it; and 8) free text for any answer. Free text answers were reviewed by two investigators (KLL, SPC) for categorization into one of the prespecified categories or an “other” category. When the first two investigators had discordant classification, a third investigator (WHS) reviewed the free text answer and final classification was determined by majority (Table S4). Answers #1 and #2 were consider to indicate perceived lack of vaccine effectiveness and answer #3 was considered perceived lack of vaccine safety.
Statistical Analysis
Patient characteristics were described for the study population stratified by vaccination status. The self-reported reasons for being vaccinated or unvaccinated were described for the study population overall and after stratification by race/ethnicity, medical insurance status, and influenza infection status. A multivariable logistic regression model was used to evaluate associations between patient characteristics and unvaccinated status. The dependent variable was self-report of not receiving the 2019–2020 influenza vaccine. Independent variables included: age; sex; race/ethnicity (dichotomized as White non-Hispanic vs non-White or Hispanic); medical insurance status (dichotomized as no insurance vs any insurance); enrolling hospital; chronic cardiovascular disease; chronic neurologic disease; chronic pulmonary disease; chronic gastrointestinal disease; chronic endocrine disease; chronic renal disease; chronic hematologic disease; chronic psychiatric disease; malignancy; and immunosuppression. Independent variables were selected a priori based on literature review.7,9,10 Associations with a p value <0.05 were considered significant. The analysis was conducted with STATA/IC 12.1 (College Station, Texas).
Results
Population
We enrolled 719 patients; of these, 40 (5.6%) were excluded because neither the patient nor available surrogates were able to report whether the patient received an influenza vaccine, resulting in an analytical population of 679 patients. Median (interquartile range) age was 58 (43 to 69) years and 298 (43.9%) were admitted to an ICU (Table 1). Receipt of influenza vaccine was reported by 415 (61.1%) patients. A primary care clinic was the most common location for vaccination (Table S5). Influenza virus was detected in 320 (47.1%) patients. Receipt of the influenza vaccine was reported by 168/320 (52.5%) patients with influenza virus detected and 247/359 (68.8%) patients without influenza virus detected.
Table 1.
Baseline characteristics of the study population stratified by self-report receipt of a 2019–2020 seasonal influenza vaccine.
| Characteristic | Not Vaccinated N=264 | Vaccinated N=415 | P-value |
|---|---|---|---|
| Age, median (IQR) [years] | 50 (35, 62) | 62 (51, 72) | <0.001 |
| Age categories, n (column %) | |||
| 18 – 49 years | 129 (48.9) | 97 (23.4) | |
| 50 – 64 years | 86 (32.6) | 131 (31.6) | |
| ≥ 65 years | 49 (18.6) | 187 (45.1) | |
| Sex – Female, n (%) | 132 (50.0) | 217 (52.3) | 0.561 |
| Race/ethnicity, n (column %) | 0.014 | ||
| White Non-Hispanic | 141 (53.4) | 269 (64.8) | |
| Black Non-Hispanic | 75 (28.4) | 96 (23.1) | |
| Hispanic | 35 (13.3) | 41 (9.9) | |
| Other Race Non-Hispanic | 13 (4.9) | 9 (2.2) | |
| Race/Ethnicity binary, n (column %) | 0.003 | ||
| White non-Hispanic | 141 (53.4) | 269 (64.8) | |
| Non-White or Hispanic | 123 (46.6) | 146 (35.2) | |
| Insurance Status, n (column %) | <0.001 | ||
| Medicare | 60 (22.7) | 214 (51.6) | |
| Medicaid | 70 (26.5) | 58 (14.0) | |
| Private | 86 (32.6) | 120 (28.9) | |
| No medical insurance | 35 (13.3) | 6 (1.5) | |
| Other | 13 (4.9) | 17 (4.1) | |
| Source of vaccine history information during interview, n (%) | 0.559 | ||
| Patient | 213 (80.7) | 345 (83.1) | |
| Surrogate | 42 (15.9) | 54 (13.0) | |
| Mix of patient and surrogate | 9 (3.4) | 16 (3.9) | |
| Chronic medical conditions, n (column %) | |||
| Cardiovascular disease | 130 (49.2) | 295 (71.1) | <0.001 |
| Neurologic disease | 25 (9.5) | 69 (16.6) | 0.009 |
| Pulmonary disease | 94 (35.6) | 194 (46.8) | 0.004 |
| Gastrointestinal disease | 18 (6.8) | 39 (9.4) | 0.237 |
| Endocrine disease | 78 (29.6) | 196 (47.2) | <0.001 |
| Renal disease | 23 (8.7) | 104 (25.1) | <0.001 |
| Hematologic disease | 49 (18.6) | 80 (19.3) | 0.817 |
| Active malignancy | 25 (9.5) | 76 (18.3) | 0.002 |
| Immunosuppressive condition | 84 (31.8) | 193 (46.5) | <0.001 |
| Psychiatric disease | 58 (22.0) | 119 (28.7) | 0.052 |
| Current pregnancy, n (column %) | 6 (2.3) | 3 (0.7) | 0.085 |
| Currently smoking, n (column %) | 85 (32.2) | 75 (18.1) | <0.001 |
| Type of Admission, n (column %) | 0.619 | ||
| Non-ICU admission | 145 (54.9) | 236 (56.9) | |
| ICU admission | 119 (45.1) | 179 (43.1) | |
| Pre-illness home, n (column %) | 0.037 | ||
| Home in community | 233 (88.3) | 361 (87.0) | |
| Nursing home | 4 (1.5) | 16 (3.9) | |
| Assisted living home | 4 (1.5) | 15 (3.6) | |
| Subacute or other chronic care facility | 2 (0.8) | 7 (1.7) | |
| School housing | 0 | 1 (0.2) | |
| Homeless | 16 (3.1) | 10 (2.4) | |
| Other | 5 (1.9) | 5 (1.2) |
Patient characteristics associated with not receiving influenza vaccine
In multivariable analysis, several patient factors were associated with unvaccinated status, including younger age, being non-White or Hispanic, not having medical insurance, and not having chronic medical conditions (Table 2). Regarding race/ethnicity, 123/269 (45.7%) patients who were non-White or Hispanic were unvaccinated compared with 141/410 (34.4%) who were White non-Hispanic (aOR=1.54; 95% CI: 1.02 to 2.32). Regarding medical insurance, 35/41 (85.4%) patients without medical insurance were unvaccinated, and 229/638 (35.9%) patients with any type of medical insurance were unvaccinated (aOR=6.42; 95% CI:2.52 to 16.38).
Table 2.
Results of a multivariable logistic regression model evaluating the association of patient characteristics and unvaccinated status for the 2019–2020 seasonal influenza vaccine among 679 adults hospitalized in the US with severe acute respiratory illness.
| Characteristic | Adjusted odds ratio for being unvaccinated* | 95% CI | P-value |
|---|---|---|---|
| Age (per year) | 0.98 | 0.96 – 0.99 | <0.001 |
| Sex - Female | 0.93 | 0.65 – 1.33 | 0.684 |
| Race/Ethnicity (Non-White or Hispanic vs White Non-Hispanic) | 1.54 | 1.02 – 2.32 | 0.039 |
| Insurance Status (Uninsured vs any insurance) | 6.41 | 2.51–16.3 | <0.001 |
| Cardiovascular chronic disease | 0.88 | 0.58 – 1.33 | 0.552 |
| Neurologic chronic disease | 0.65 | 0.38 −1.11 | 0.114 |
| Pulmonary chronic disease | 0.60 | 0.41 – 0.87 | 0.004 |
| Gastrointestinal chronic disease | 0.69 | 0.36 – 1.34 | 0.277 |
| Endocrine chronic disease | 0.65 | 0.45 – 0.95 | <0.001 |
| Renal chronic disease | 0.41 | 0.24 – 0.71 | <0.001 |
| Hematologic chronic disease | 1.65 | 0.92 – 2.95 | 0.93 |
| Active malignancy | 0.66 | 0.35 – 1.25 | 0.21 |
| Immunosuppressive condition | 0.57 | 0.34 – 0.96 | <0.001 |
| Psychiatric chronic disease | 0.73 | 0.48 – 1.12 | 0.15 |
One multivariable logistic regression model was constructed to evaluate the association between patient characteristics and not receiving the 2019–2020 seasonal influenza vaccine. The dependent variable was self-report of not receiving the 2019–2020 influenza vaccine. The model included the 14 independent variables listed in this table. Age was included as a continuous variable. All other independent variables were dichotomous. Independent variables were selected a priori based on literature review.7,9,10
Perceptions of vaccine acceptance and hesitancy
Among the 415 patients who reported receiving an influenza vaccine, the most common primary reasons for obtaining the vaccine were: “I believe the influenza vaccine is important for my health” (62.9%); and “My doctor suggested I get the influenza vaccine” (28.9%). The pattern of answers was similar in subgroups defined by race/ethnicity, medical insurance status, and influenza infection status (Table 3).
Table 3.
Primary reason why the 2019–2020 seasonal influenza vaccine was received based on self-report from 415 adults hospitalized during the 2019–2020 influenza season with severe acute respiratory illness in the US who received the vaccine. Results are reported for all vaccinated patients in the study (n=415) and with the vaccinated population stratified by race/ethnicity, by medical insurance status, and by influenza infection status.
| Primary reason for receiving the vaccine | Full vaccinated population (n=415) | Vaccinated population stratified by race/ethnicity | Vaccinated population stratified by medical insurance status | Vaccinated population stratified by influenza infection status | |||
|---|---|---|---|---|---|---|---|
| White, Non-Hispanic (n=269) | Non-White or Hispanic (n=146) | Any medical insurance (n=409) | No medical insurance (n=6) | Influenza positive (n = 168) | Influenza negative (n = 247) | ||
| “I believe the influenza vaccine is important for my health”, n (column %) | 261 (62.9) | 177 (65.8) | 84 (57.5) | 259 (63.3) | 2 (33.3) | 107 (63.7) | 154 (62.4) |
| “My doctor suggested I get the influenza vaccine”, n (column %) | 120 (28.9) | 67 (24.9) | 53 (36.3) | 117 (28.6) | 3 (50.0) | 49 (29.2) | 71 (28.7) |
| “I believe getting the influenza vaccine is important to keep others healthy”, n (column %) | 12 (2.9) | 10 (3.7) | 2 (1.4) | 11 (2.7) | 1 (16.7) | 4 (2.4) | 8 (3.2) |
| “I saw an advertisement for the influenza vaccine”, n (column %) | 0 (0) | 0 (0) | 0 (0) | 0 (0) | 0 (0) | 0 (0) | 0 (0) |
| Other, n (column %) | 22 (5.3) | 15 (5.6) | 7 (4.8) | 22 (5.4) | 0 (0) | 8 (4.8) | 14 (5.7) |
Among the 264 patients who reported not receiving an influenza vaccine, 135 (51.1%) reported actively choosing not receiving a vaccine because of perceived ineffectiveness (36.7%) or danger (14.4%) from the vaccine (Table 4). Seventy-seven (29.2%) patients indicated they intended to get an influenza vaccine but did not get one prior to becoming sick. Eleven (4.2%) patients stated they did not know they were supposed to receive an influenza vaccine. Cost of the vaccine or lack of transportation to a location where vaccines were administered was the primary barrier to vaccination reported by 23 (8.7%) patients, which was more common in patients without medical insurance (22.9%) than those with medical insurance (6.6%) (p=0.001).
Table 4.
Primary reason why the 2019–2020 seasonal influenza vaccine was not received based on self-report from 264 adults hospitalized during the 2019–2020 influenza season with severe acute respiratory illness in the US who did not receive the vaccine. Results are reported for all unvaccinated patients in the study (n=264) and with the unvaccinated population stratified by race/ethnicity, by medical insurance status, and by influenza infection status.
| Primary reason for not receiving the vaccine | Full unvaccinated population (n=264) | Unvaccinated population stratified by race/ethnicity | Unvaccinated population stratified by medical insurance status | Unvaccinated population stratified by influenza infection status | |||
|---|---|---|---|---|---|---|---|
| White, Non-Hispanic (n=141) | Non-White or Hispanic (n=123) | Any medical insurance (n=229) | No medical insurance (n=35) | Influenza positive (n = 152) | Influenza negative (n = 112) | ||
| Perceived concerns about ineffectiveness | |||||||
| “I don’t believe the influenza vaccine is important for my health”, n (column %) | 72 (27.3) | 45 (31.9) | 27 (22.0) | 62 (27.1) | 10 (28.6) | 42 (27.6) | 30 (26.8) |
| “I received the influenza vaccine in the past and still got the flu”, n (column %) | 25 (9.5) | 9 (6.4) | 16 (13.0) | 24 (10.5) | 1 (2.9) | 15 (9.9) | 10 (8.9) |
| Perceived concerns about safety | |||||||
| “I think the influenza vaccine is dangerous for me”, n (column %) | 38 (14.4) | 20 (14.2) | 18 (14.6) | 36 (15.7) | 2 (5.7) | 18 (11.8) | 20 (17.9) |
| Knowledge deficit | |||||||
| “I didn’t know I should get the influenza vaccine”, n (column %) | 11 (4.2) | 6 (4.3) | 5 (4.1) | 9 (3.9) | 2 (5.7) | 9 (5.9) | 2 (1.8) |
| Financial or transportation barrier | |||||||
| “The influenza vaccine costs too much money”, n (column %) | 4 (1.5) | 4 (2.8) | 0 | 1 (0.4) | 3 (8.6) | 1 (0.7) | 3 (2.7) |
| “I was unable to get to a location that gives influenza vaccines”, n (column %) | 19 (7.2) | 10 (7.1) | 9 (7.3) | 14 (6.1) | 5 (14.3) | 13 (8.6) | 6 (5.4) |
| Lack of urgency | |||||||
| “I meant to get the influenza vaccine but never got around to it”, n (column %) | 77 (29.2) | 40 (28.4) | 37 (30.1) | 69 (30.1) | 8 (22.9) | 42 (27.6) | 35 (31.3) |
| Other, n (column %) | 18 (6.8) | 7 (5.0) | 11 (8.9) | 14 (6.1) | 4 (11.4) | 12 (7.9) | 6 (5.4) |
Discussion
In this study of influenza vaccine acceptance and hesitancy among hospitalized adults with an acute respiratory illness at 10 US hospitals during the 2019–2020 influenza season, we identified several findings that complement other studies conducted among less severely ill patients. First, approximately half of severely ill adults hospitalized with an acute influenza infection were unvaccinated. Second, perceptions that influenza vaccination is ineffective was a major contributor to low vaccine uptake in this population. Third, specific subgroups within the US population are more likely to be unvaccinated, including those without medical insurance and those with a non-White or Hispanic race/ethnicity.
Results of this study can help target strategies for increasing vaccine uptake in the patient population represented in this study, which largely consisted of older adults with multiple chronic medical conditions. The two most common reasons patients reported for receiving an influenza vaccine in this study were believing that influenza vaccines were important for their health and because a physician recommended they receive a vaccine. This suggests that targeting strategies that boost provider-patient discussions about influenza vaccination each fall could be an important strategy for increasing vaccine uptake in this population. Conversely, seeing an advertisement recommending vaccination, such as on television or on a billboard, was not cited by any of the vaccinated patients as the primary reason they obtained an influenza vaccine. Furthermore, only 4.2% of patients who were unvaccinated reported that they did not know that an influenza vaccine was recommended for them. These results suggest that increasing direct public advertising with the goal of increasing awareness for the recommendation to be vaccinated is likely to have low yield for increasing vaccination rates in this population.
Among unvaccinated patients in this study, about half actively chose to avoid vaccination due to a perception of the vaccine being ineffective or unsafe. The other half of patients who were unvaccinated reported that they were open to vaccination but had not been vaccinated prior to becoming ill, with the most common response in this group being, “I meant to get the influenza vaccine but never got around to it”. These results suggest a two-pronged approach may be necessary for optimizing vaccine uptake—one that increases education about vaccine safety and effectiveness, and one that reduces barriers to vaccination among those already open to vaccination.
Our findings included lower influenza vaccination rates among non-White and Hispanic populations in the US. Increasing vaccine confidence among these populations appears critical to elevating vaccination rates and reducing morbidity and mortality from influenza in the US.
While our manuscript was strengthened by a diverse, multicenter cohort of severely ill patients hospitalized with an acute respiratory illness, there are limitations to consider. Social desirability bias could have affected participant responses, such that participants answered questions about vaccine acceptance and hesitancy based on what the interviewer would find desirable. Although patients may have had several reasons for their vaccination preference, our assessment only asked about a single primary reason for vaccination decisions. We did not ask patients about their perceived risk of being infected with influenza or becoming severely ill if infected, which prior research has shown to be associated with vaccine hesitancy.9,12 Although we adjusted for age and a broad set of chronic medical conditions in the models evaluating for an association between race/ethnicity and vaccine status and medical insurance and vaccine status, residual confounding was possible. The study was conducted at large, academic hospitals, and results may not generalize to other hospital settings, which tend to have fewer critically ill patients.
Conclusion
During the 2019–2020 influenza season, we found that nearly 40% of hospitalized adults with severe acute respiratory illness had not received an influenza vaccine, including almost half of those diagnosed with influenza. Approximately 36% of unvaccinated patients expressed doubt about the effectiveness of influenza vaccines while 14% expressed concerns about vaccine safety. Furthermore, patients without medical insurance and those with non-White race or Hispanic ethnicity were substantially less likely to have been vaccinated. Optimizing vaccination programs in the US will require new strategies for improving vaccine distribution and accessibility to non-White and Hispanic people and those without medical insurance.
Supplementary Material
Highlights.
In a cohort of 679 severely ill adults hospitalized with an acute respiratory illness during the 2019–2020 influenza season, 38.9% had not received a seasonal influenza vaccine.
Among those not vaccinated, 51.1% reported intentionally avoiding vaccination due to perceived ineffectiveness (36.7%) or risk (14.4%) of vaccination.
Lack of medical insurance and being non-White or Hispanic were associated with not being vaccinated.
Funding:
This work was supported by the United States Centers for Disease Control and Prevention through contract 75D30119C05670 to Dr. Self.
Footnotes
A complete list of the IVY Network contributors is listed in the Supplementary Appendix.
Publisher's Disclaimer: 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 and Prevention.
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