key: cord-0952592-y8cpr84s
authors: Cohrs, Janessa R.; Mirtallo, Jay M.; Seifert, Jennifer L.; Jones, Sarah M.; Erdmann, Ashley M.; Li, Junan
title: Perceptions and barriers to the annual influenza vaccine as compared with the COVID-19 vaccine in an urban underserved population.
date: 2021-10-21
journal: J Am Pharm Assoc (2003)
DOI: 10.1016/j.japh.2021.10.019
sha: 73e7f62da86981e48bb42ada331e0cca8ad383cb
doc_id: 952592
cord_uid: y8cpr84s

Background For a vaccine to be successful, communities must perceive it as important, safe, effective, and necessary. However, there are many barriers and hesitancies to vaccination. Underserved patient populations may face additional challenges related to access and cost. Since community pharmacists improve vaccine access and increase vaccination rates, it is beneficial for pharmacists to understand perceptions and barriers to vaccinations in their community to increase vaccine confidence. Objective(s): This study aims to assess and compare barriers and perceptions of the annual influenza to the COVID-19 vaccine for underserved patients of a charitable pharmacy. Methods Patients who qualified to receive medications from an outpatient charitable pharmacy took an electronic survey when receiving medications. The survey incorporated questions developed by the World Health Organization’s Strategic Advisory Group of Experts on Vaccine Hesitancy on a 5-point Likert scale. Questions about the influenza and COVID-19 vaccines mirrored one another. Demographic data such as age, race, sex, and education level were also collected. Results Of the 189 patients surveyed at the charitable pharmacy, 71.7% were ages 55 and older and 58.9% were female. Of note, 78% and 77% of participants agreed or strongly agreed that the influenza and COVID-19 vaccines, respectively, were important for the health of others in their community. Side effects and the cost of the COVID-19 vaccine were noted to be significantly more of a concern with the COVID-19 vaccine when compared to the influenza vaccine (P<0.001). Conclusion(s): Ensuring equitable vaccine access, promoting the COVID-19 vaccine as free, and eliciting and addressing individual persons’ concerns related to vaccine safety and side effects are all important ways pharmacists as well as other healthcare providers and community stakeholders can help promote vaccine confidence within the populations they serve.

 The success of vaccines depends on individual and community-level acceptance and uptake; however, there are many complex and multifactorial reasons why individuals do not receive vaccines.  The COVID-19 vaccine poses a unique set of challenges and potential barriers to widespread acceptance.  Community pharmacies have demonstrated an increase in vaccination rates by increasing vaccine access.

What this study adds:

 An underserved patient population at a charitable pharmacy largely accepted both the influenza and COVID-19 vaccines as important, safe, and effective at preventing influenza and COVID-19, respectively.  The level of acceptance was similar for both the annual influenza vaccine and the COVID-19 vaccine.  Side effects and the cost of the COVID-19 vaccine were noted to be significantly more of a concern with the COVID-19 vaccine when compared to the influenza vaccine.

Vaccine hesitancy in an urban underserved population: The annual influenza vaccine compared with the COVID-19 vaccine 4

For any vaccine to be successful, it must not only pass rigorous safety and efficacy standards throughout laboratory tests and clinical trials, but the widespread community must also perceive it as important, safe, effective, and necessary. Vaccine acceptance happens at an individual level, yet the impact of receiving a vaccine moves beyond just the individual to also affecting the health of the greater community. Experts from Johns Hopkins School of Public Health, the World Health Organization (WHO), and many other organizations have stressed the importance of vaccine acceptance, especially in the face of the coronavirus (COVID-19) pandemic and the SARS-CoV-2 vaccines. 1 With the understanding that acceptance and uptake of vaccination is crucial to preventing the spread of a disease, there are many complex and multifactorial barriers and hesitancies to vaccination to address. Some of these barriers and hesitancies include concerns about vaccine safety, side effects, efficacy, and necessity, as well as societal and peer influences, lack of education and understanding, fear of needles, and mistrust of the healthcare system. Often, barriers and hesitancies are amplified in underserved and minority populations. Due to a lack of access, education, language barriers, and/or health literacy, underserved populations have a higher chance of receiving inadequate care, misunderstanding explanations of treatments, and becoming lost to follow-up within the healthcare system. One recent study focusing on vaccine hesitancy and uptake in underserved African American older adults notes that social isolation, living alone, loneliness, and poor mental health may be associated with lower vaccination rates. 2 The cost of vaccines is one example of an additional challenge that underserved patient populations may face.

Specifically in the current COVID-19 pandemic, there are additional challenges that can further contribute to individual and community-level barriers and hesitancies. Some of these barriers include rapid vaccine development, limited supplies of high demand vaccines, decreased healthcare access due to diminished capacity and social distancing regulations, and changes to public transportation and access to public spaces. The COVID-19 pandemic has also highlighted new challenges that arise from the rapid dissemination of information and misinformation through media platforms. For the vulnerable, underserved people in a community, these pandemic-specific challenges may be amplified as well since many of these challenges already exist for patients who have difficulty accessing and utilizing the healthcare system One demonstrated means to improving vaccine acceptance is by increasing the number of accessible vaccine providers. Community pharmacists play a key role in improving vaccine access and vaccination rates, particularly in areas where healthcare was previously lacking that often are home to many underserved patient populations. 3, 4, 5 State and national-level health services have also acknowledged this as the U.S. Department of Health and Human Services recognized pharmacists' value as immunization providers by authorizing pharmacists to administer all childhood vaccines without a prescription during the COVID-19 pandemic. 6 As accessible authorized providers of immunizations who are also able to establish relationships with patients, pharmacists need to understand individuals' perceptions and barriers to vaccination as the first step to increasing vaccine rates and ensuring widespread uptake. This is especially true for pharmacists who work in underserved patient populations and have built the rapport needed to care for these patients.

Community pharmacies are an easily accessible point of the healthcare system creating enhanced opportunities for daily patient contact, administering vaccines, and establishing relationships with patients who may otherwise have difficulty navigating the healthcare system. Pharmacists are uniquely placed within communities to be approachable, knowledgeable, familiar faces at pharmacies that serve as no or low-cost points of access to the healthcare system with extended hours and unique understanding of their communities' needs. It is critical that pharmacists in community-based settings, especially in underserved areas, understand their patients' perceptions, potential hesitancies, and perceived barriers to vaccination. Especially in the COVID-19 pandemic, this understanding will help pharmacists as well as other healthcare providers know how to better address the perceptions and barriers their underserved patients may face to vaccination and medication access in general.

For the sake of improving individual health and public health during the COVID-19 pandemic, the purpose of this study is to compare an urban underserved patient populations' perceptions and barriers of the influenza vaccine to the perceptions and barriers of the COVID-19 vaccine. The objectives of this study are to: define the urban underserved patient population surveyed in this project, assess patients' perceptions and barriers of the influenza vaccine, assess patients' perceptions and barriers of the COVID-19 vaccine, and compare these urban underserved patients' perceptions and barriers to the influenza vaccine versus the COVID-19 vaccine. Ultimately, understanding patients better will elucidate ways to address the hesitancies and barriers this study identifies, and improve vaccination rates within this patient population.

For over a decade, The Charitable Pharmacy of Central Ohio's (CPCO) mission has been to provide affordable and appropriate pharmacy services and coordinate access to healthcare for people who are vulnerable in the community. CPCO strives to alleviate challenges related to cost and access by providing medication-related services at no cost for low-income, uninsured, and underinsured residents of Franklin County, Ohio.

The Charitable Pharmacy of Central Ohio (CPCO) provides prescription medications and pharmacy services to individuals living in Franklin County, Ohio who are uninsured or underinsured. CPCO served 1530 unduplicated patients in 2020 with 54.5% of patients being female and 45.5% male. Approximately 8% of CPCO's population is Hispanic/Latino. The breakdown of race is 48% Black or African American, 36% White, and 16% other or unknown. Twenty-nine-percent of CPCO's patients are 65 and older, 33.2% ages 55 to 64, and 37.3% 54 or younger. To qualify for CPCO's services, individuals must have an income at or below 200% of the federal poverty level. CPCO's services include prescription medications, medication counseling, medication therapy management, and blood pressure and blood glucose screenings (prior to moving services to fully curbside due to the COVID-19 pandemic). CPCO receives medications through multiple sources of inventory including donated repository medications, manufacturer bulk replenishment programs, and a formulary of purchased medications. Uniquely, CPCO also has a full-time social worker on site who coordinates the patient services team and connects patients to resources such as food, housing, transportation, and healthcare provider access.

This observational, cross-sectional study consisted of designing and implementing a survey tool to gauge patients' perceptions and barriers to both the influenza and COVID-19 vaccines.

The survey tool was derived from the question matrix developed by World Health Organization's Strategic Advisory Group of Experts (WHO SAGE) on Vaccine Hesitancy 7 . The survey contained statements on a 5-point Likert scale about perceptions of the influenza vaccine and COVID-19 vaccine as well as barriers to receiving each of the vaccines. The questions about each vaccine mirrored one-another for consistency and analysis. Responses to survey questions with a mean greater than 3 suggests most participants agree or strongly agree with the statement and mean values less than 3 for negative statements suggest the majority of participants disagree or strongly disagree with the statements. Perception-related questions included importance of the vaccine to the health of the individual and others, vaccine efficacy, side effects, trust of healthcare providers' recommendations, and willingness to receive each vaccine (once available). Barrier-related items assessed included travel, wait time, hours of operation, and vaccine cost. Demographic questions on the survey included age, gender, race/ethnicity, United States residency status, insurance status, and education level. Income level was not included as all CPCO patients must have an income at or below 200% of the federal poverty level. A full copy of the survey is available as a supplement to this manuscript. The survey tool was face-validated for readability and comprehension via additional proofreading and testing by five individuals who were non-healthcare professionals. A native Spanish-speaking employee of CPCO and a bilingual member of the research team translated the survey into Spanish to help capture a sample that was more representative of the population CPCO serves.

This study was approved by The Ohio State University Institutional Review Board as Exempt category 2b. From January 2021 to March 2021, all new and existing patients of CPCO that speak English or Spanish and were 18 years old or older were eligible to participate in the survey and receive a $5 gift card as an optional incentive for completing the survey. Funding for the gift card came from within CPCO's general operating budget. Willing participants consented to participate in the survey. This study excluded individuals who came to CPCO on behalf of qualified CPCO patients and were not qualified CPCO patients themselves, were less than 18 years old, and/or did not speak English or Spanish. The first survey question asked each participant if they had previously completed the survey to help ensure participants did not take the survey more than once. Student research assistant volunteers from The Ohio State University College of Pharmacy (listed in the IRB) assisted in the recruitment, data collection, and incentive distribution. These students were trained on data collection policies through a virtual orientation as well as an on-site orientation on their first day of data collection.

When patients arrived at the pharmacy to pick up medication refills (curbside pickup only at the time of the study), the student research assistants asked the patients if they would like to participate in an optional survey and gave an "invitation" on a half sheet of paper containing a brief explanation of the survey, its purpose, and offer for the incentive gift card for completing the survey. This paper also contained a short link and a QR code to access the survey via an electronic device. If patients did not have an electronic device, they had the option of taking the survey on one of CPCO's iPads while they waited for their medications to be delivered to their vehicle. A student assisting with data collection could also help them access the survey on their personal electronic device.

To allow for the broadest and most generalizable study population, patients who received their prescriptions from CPCO through the mail received the same invitation paper (with the explanation of the survey, its purpose, the incentive gift card for completing the survey, and link/QR code to access the survey via an electronic device) in the mail with their prescription medications.

Upon completion of the survey, participants were redirected to a separate, optional survey where they entered their name and address to receive the optional incentive provided by CPCO. Participants could receive the $5 gift card either in-person at the pharmacy or through the mail. To keep survey responses anonymous, the information collected in the incentive survey remained separate from the study survey and could not be traced to any participants' responses.

The Charitable Pharmacy of Central Ohio serves approximately 1500 unduplicated patients each year. Based on a 7% margin of error (ME) and a 50% response rate, we aimed to invite 348 patients to participate in the survey to obtain a target sample of 176 complete responses.

Only participants saying, "yes, I consent to participate in this survey" were included in the data analysis. Since all questions were optional and voluntary, some of these participants did not respond to all questions, leading to missing data for various questions throughout the survey. All statistical tests were two-sided, and the significance level was preset at α= 0.05. All individuals involved with data analysis only had access to deidentified data from the Qualtrics survey. Demographic characteristics and patients' responses were first analyzed using descriptive statistics. Discrete data was presented as count (n) and frequency (%), and Likert scale data was summarized as mean and standard deviation (SD). Comparison of discrete data among different groups was analyzed using χ2 tests or Fisher's exact tests where appropriate; Likert scale data was compared among different groups using Student's t tests (2 groups) or one-way ANOVA (3 and more groups). Potential associations between responses to different questions were analyzed using χ2 tests or Fisher's exact tests (between two discrete variables), Student's J o u r n a l P r e -p r o o f t tests or one-way ANOVA (between a discrete variable and a Likert scale variable) and Pearson's correlation analyses (between two Likert scale variables). Although open-ended survey questions were included in the survey tool, responses were not included in this analysis. R3.4 software (The R project for statistical computing, http://www.r-project.org) was used in this study.

Demographics At the conclusion of data collection, 189 patients at the Charitable Pharmacy of Central Ohio (CPCO) consented to participate in this survey-based study. In general, participants were known to be a part of an underserved population as they met the qualifications to receive medications from CPCO. Patient-reported demographics are listed in Table 1 below. Of those who participated, 60.4% were ages 55 and older and 34.9% were female. Participants were White (33.3%) and Black or African American (21.6%) and 7.9% had an education of 11 th grade or less. Of note, the age and gender distribution are comparable to that of CPCO's general patient population. However, of the participants who disclosed their race, a larger portion of participants were White, as compared to CPCO's patient population. 

Vaccine hesitancy in an urban underserved population: The annual influenza vaccine compared with the COVID-19 vaccine 9

Influenza and COVID-19 vaccine perceptions When looking at the perception questions for both influenza and COVID-19 vaccines alone, as shown in Table 2 , most participants answered in a way that reflected a positive view on vaccines, with mean values above 3 for positive statements, suggesting the majority of participants agreed or strongly agreed with the statements. Of note, participants most strongly agreed with the statement, "Getting the COVID-19 vaccine is important for the health of others in my community." Seventy-seven percent of participants agreed or strongly agreed with this statement. For the mirrored statement regarding influenza vaccines, 78% of participants agreed or strongly agreed. Also, 77% of participants agreed or strongly agreed with the statement, "I plan to get the COVID-19 vaccine this year." Approximately 76% of participants agreed or strongly agreed with the same statement regarding influenza vaccines.

Similar to the perception questions for both influenza and COVID-19 vaccines alone, the majority of participants had a positive outlook on the barriers. With means less than 3 for each barrier listed, most participants disagree or strongly disagreed that any of the suggested options were perceived as a potential or actual barrier to receiving either the influenza or COVID-19 vaccine, as seen in Table 2 . It is worth noting, however, that some individuals within the surveyed population did identify the options to be an actual or potential barrier to receiving the influenza and/or COVID-19 vaccine. The cost of the COVID-19 vaccine was the largest perceived potential barrier, with 10 (7%) participants strongly agreeing and 36 (25%) participants agreeing that cost of the COVID-19 vaccine could make it difficult to receive the COVID-19 vaccine. All other barrier-related questions had no more than 26 participants total agreeing or strongly agreeing that any of the barriers listed could make it difficult for them get the influenza or COVID-19 vaccine.

We compared participants' answers for each set of mirrored questions and found that there was largely no statistically significant difference in the way questions were answered regarding influenza vaccines and COVID-19 vaccines, as seen as the p-values in Table 2 . Exceptions to this were concerns for serious side effects and the cost of the vaccines as a perceived barrier to these vaccines. More individuals expressed concerns for serious side effects with the COVID-19 vaccine than the influenza vaccine. Also, more individuals expressed concerns regarding cost of the vaccine being a barrier with the COVID-19 vaccine than the influenza vaccine. 

Based on the results of this study, the underserved population at CPCO has a positive perception toward both the influenza vaccine and COVID-19 vaccines as being effective and important for their health and the health of others in their community. Participants also had a mostly positive outlook on the vaccine information and recommendations they receive from members of their healthcare teams. Additionally, the majority of the survey population did not perceive issues related to vaccine cost, clinic/pharmacy hours, travel, or transportation to be major barriers to receiving either vaccine. The results of this survey also showed that although the survey population trusted the vaccine recommendations from their physicians the highest, pharmacists as well as nurses, nurse practitioner, and physician assistants are also trusted by this population. This information can be useful to show how pharmacists and other members of patients' healthcare teams can promote vaccination and fulfill roles as vaccine experts and educators.

The generally positive perception of the COVID-19 vaccine seen with the patients at CPCO is different than what other studies and the media have reported. One national survey by Szilagyi et al. demonstrated an overall decline in self-reported likelihood of getting a COVID-19 vaccine when comparing participants surveyed in April 2020 to December 2020. 8 The survey did not specifically evaluate contributing factors to participants' likelihood to receive a vaccine, but these authors believe educational campaigns may help increase the public's willingness to receive a COVID-19 vaccine. Meanwhile, Nguyen et al. found that intent to receive the COVID-19 vaccine had increased from September 2020 to December 2020 by approximately 10% across the United States. 9 However, they noted that adults with less education, less income, and without insurance still had lowest rates of COVID-19 vaccine intent. This may contrast the results of our survey which generally showed a positive view of the COVID-19 vaccine. Nguyen et al believe that addressing concerns of individual persons and communities is an important way to increase vaccine confidence and ultimately prevent COVID-19. 9 Educational campaigns and equitable vaccine access noted in these studies will certainly help increase vaccine confidence. 8, 9 However, our patients' differing, more-positive results are potentially also due, in part, to the existing efforts CPCO takes every day to build relationships with patients, listen to their concerns, and help address any barriers to accessing healthcare this population may face.

As one of the significant differences in survey answers for the influenza and COVID-19 vaccines, side effects is an aspect of vaccine hesitancy that pharmacists, public health initiatives, and other healthcare providers can help address for patients. Nguyen et al discovered that concerns for side effects and vaccine safety were the top reasons for not intending to get the COVID-19 vaccine. 9 Another survey-based study based in Finland evaluated perceived risk of COVID-19 infection, perceived safety of a COVID-19 vaccine, and intentions to accept a COVID-19 vaccine. 10 Overall, participants perceived COVID-19 as a more threatening disease than influenza or measles; but the views of vaccine safety was shown as the strongest predictor of participants intending to receive a COVID-19 vaccine, which is like Nguyen et al's findings. 9,10 These findings of side effect and safety are consistent with our participants' concerns related to side effects of the COVID-19 vaccine. Just like with any other disease state or medication, pharmacists and other healthcare providers need to take time to discuss each individuals' concerns related to vaccination, especially related to safety and side effects. Healthcare professionals should be forthcoming about vaccine safety information, potential side effects, how long these side effects should last, and how to manage side effects, as appropriate. Community pharmacists are uniquely positioned to listen to specific barriers and hesitancies, address and acknowledge patients' concerns, and inform patients using evidence as well as personal testimonies. Ultimately, building this rapport with patient will increase vaccine confidence, understanding, and uptake.

As with any survey-based research, this study has several limitations including: survey fatigue leading to skipped survey questions, potential social desirability bias influencing individuals' responses, and the possibility that individuals who were not qualified as CPCO patients but were at the pharmacy to pick up medications for another individual could have taken the anonymous survey. Historical bias, meaning conditions outside of the survey's control such as evolving conditions of the COVID-19 pandemic and vaccine availability, changes in political climate, and COVID-19 vaccine coverage on social media, could change participants' responses which could be a limitation to this study as well. However, a preliminary data set consisting of the mean and standard deviation for each question halfway through data collection were compared to the final data and there were no major, meaningful differences in survey responses. Lastly convenience sampling is a limitation of this survey-based study. Patients who did not come to the pharmacy during the data collection time period or individuals who received the survey invitation via mail but did not have internet access could not participate in the survey.

Although this study provides insight into one underserved patient populations' perceptions and barriers of the annual influenza vaccine and the COVID-19 vaccine, future studies could further evaluate subgroups of this populations' views and concerns related to these vaccines. Evaluating which sources and types of information this population finds most helpful when making choices about vaccines could also be beneficial to develop more targeted, effective promotional and educational tools to improve vaccine confidence.

For the sake of improving individual health and public health by preventing the spread of COVID-19, it is important to understand all patients' perceptions and barriers to the COVID-19 vaccine. This study found that this underserved patient population largely accepted both the influenza and COVID-19 vaccines as important, safe, and effective at preventing influenza and COVID-19, respectively. The level of acceptance was similar for both the annual influenza vaccine and the COVID-19 vaccine. This underserved population largely did not perceive barriers such as cost and transportation as issues to receiving either vaccine. Although the participants did not see cost as a concern overall, participants perceived cost as well as side effects as more concerning with the COVID-19 vaccine when compared to their mirrored responses to the influenza vaccine. Ensuring equitable vaccine access, promoting the COVID-19 vaccine as no cost to the patient, eliciting individual persons' concerns related to vaccine safety and side effects, and addressing these concerns in a personable manner are all important ways pharmacists as well as other healthcare providers and community stakeholders can help promote vaccine confidence within the populations they serve.

Note: all questions were asked using a 5- Distance to the pharmacy/clinic could make it difficult for me to get a COVID-19 vaccine. In the past, the hours that the clinic/pharmacy is open has made it difficult for me to get my flu vaccine.

The hours that the clinic/pharmacy is open could make it difficult for me to get a COVID-19 vaccine. In the past, wait time at the clinic/pharmacy has made it difficult for me to get my flu vaccine.

Wait time at the clinic/pharmacy could make it difficult for me to get a COVID-19 vaccine. In the past, the cost it takes to get to the clinic/pharmacy has made it difficult for me to get my flu vaccine.

The cost it takes to get to the clinic/pharmacy could make it difficult for me to get a COVID-19 vaccine. In the past, transportation issues have made it difficult for me to get my flu vaccine Transportation issues could make it difficult for me to get a COVID-19 vaccine. In the past, the cost of the vaccine has made it difficult for me to get my flu vaccine.

The cost of the vaccine could make it difficult for me to get a COVID-19 vaccine. If I had to travel for over an hour to get the flu vaccine, it is worth my time to get it.

If I had to travel for over an hour to get the COVID-19 vaccine, it is worth my time to get it. If I had to wait for over an hour at the clinic/pharmacy to get the flu vaccine, it is worth my time to get it.

If I had to wait for over an hour at the clinic/pharmacy to get the COVID-19 vaccine, it is worth my time to get it.

J o u r n a l P r e -p r o o f . 

Enhancing public trust and health with COVID-19 vaccination: Why "If we build it/they will come" may not apply to humans and vaccines and what can be done about it

Influenza vaccination among underserved African-American older adults

The impact of pharmacy-based immunization services on the likelihood of immunization in the United States

Impact of pharmacists on access to vaccine providers: A geospatial analysis

Pharmacy provision of influenza vaccinations in medically underserved communities

HHS expands access to childhood vaccines during COVID-19 pandemic. U.S. Department of Health and Human Services Website

Measuring vaccine hesitancy: The development of a survey tool

National trends in the US public's likelihood of getting a COVID-19 vaccine

COVID-19 Vaccination intent, perceptions, and reasons for not vaccinating among groups prioritized for early vaccination -United States

Side effects, long term side effects Is it free? When can I get it? Am I allergic to it? Will it affect my health conditions? Am I receiving a live virus? How effective is it? / Does it work?

Perceptions and barriers to the annual influenza vaccine as compared with the COVID-19

PharmD*; Clinical Pharmacist, Heart of Ohio Family Health

The American Society for Parenteral and Enteral Nutrition and Professor Emeritus

Director of Continuing Professional Development and PGY-1 Community-Based Residency Program Director

Jones, PharmD; Pharmacy Manager at Linden Community Pharmacy, The Charitable Pharmacy of Central Ohio

The Ohio State University College of Pharmacy Junan Li, PhD; The Ohio State University College of Pharmacy *former PGY-1 Community-based Pharmacy Practice Resident, The Ohio State University College of Pharmacy and The Charitable Pharmacy of Central Ohio **former Executive Director

Cohrs: conceptualization, methodology, validation, formal analysis, investigation, resources, data curation, writing -original draft, writing -review and editing, visualization, supervision

Mirtallo: conceptualization, methodology, formal analysis, writing -review and editing, supervision

Seifert: conceptualization, methodology, writing -review and editing, supervision

Jones: conceptualization, methodology, writing -review and editing

Erdmann: conceptualization, methodology, writing -review and editing Junan Li: methodology, formal analysis, resources, data curation