Abstract

As of June 2022, more than 590 million doses of COVID-19 vaccines have been administered in the United States, and 67.4% of the eligible population were fully vaccinated by that time. Pharmacists have administered more than 50% of COVID-19 vaccine doses. By March 2021, 95% of pharmacists who responded to an APhA survey reported that they were administering COVID-19 vaccines or had plans to begin vaccinating patients at some point in the future. As of June 8, 2022, community pharmacies alone had reported administering over 250 million doses both in stores and through other programs across the United States, including 8 million doses administered at long-term care facilities. Pharmacists on faculty at universities, on staff at hospitals, and in various other practice settings have taken up the charge as well. Across these settings, pharmacists have spearheaded the organization and coordination of massive vaccination clinics in their communities. Many pharmacists have even taken extra shifts or come out of retirement to administer vaccines. They have scrambled to train novice immunizers—including student pharmacists and certified pharmacy technicians—quickly and under the constraints of a global pandemic. Immunization trainers have moved courses online or to socially distanced outdoor settings to meet the immediate need for more immunizers. As a result of federal emergency legislation, student pharmacists and certified pharmacy technicians have gained the authority to administer COVID-19 vaccines, and they have risen to the occasion. Pharmacists, too, have exercised an expanded authority to vaccinate during this time due to federal authorization that overcame state-level barriers. Many in the profession hope these changes will last beyond the pandemic. Despite the best efforts from pharmacy team members, some 33% of eligible Americans remain unvaccinated against COVID-19. These unvaccinated people walk into pharmacies every day and provide pharmacists with a unique opportunity to learn about and address their concerns regarding vaccination. Pharmacists are well-equipped and prepared to build vaccine confidence in their communities. According to an APhA survey, 98% of pharmacist respondents were prepared to address vaccine hesitancy among their patients. Many of those who remain unvaccinated—the vaccine-contemplative—are still considering the choice, either for themselves or for their children. It takes time and patience, but pharmacists can uncover patients’ concerns, address them, and better equip their patients to separate fact from fiction when they research vaccines on their own. Vaccine refusal, while prevalent in response to COVID-19 vaccines, is in fact as old as vaccines themselves. When pharmacists became immunizers in the late 1990s, the health care professions already had centuries of experience with vaccine hesitancy behind them. Vaccine resistance movements date back to the time of English doctor Edward Jenner who worked to combat smallpox and faced resistance campaigns. “Two hundred years ago, people objected to the smallpox vaccine. Some because it was against God's will; others because they distrusted it. There have always been objections to vaccines,” said John Grabenstein, BSPharm, PhD, a vaccinologist and president of Vaccine Dynamics. Like people's current concerns around COVID-19 vaccines, people's reservations about the smallpox vaccine ran the gamut from religious to political to antiscience. Some people, including clergy, held that the cowpox-based smallpox vaccine, with its animal ingredients, was unchristian. Those with political reservations said it was a violation of their civil liberties that the government require that they get a vaccine. Others distrusted medicine in general or the ideas of Edward Jenner, the developer of the vaccine, in particular. Many of these 200-year-old concerns will sound familiar to pharmacists today. “But some of the unique circumstances of this pandemic and the nature of the emergency helped fuel COVID-19 vaccine hesitancy. For example, it's true the vaccines were developed quickly, but no important steps were skipped [in the process],” Grabenstein said. Over the course of the vaccine rollout, and even prior to the emergency use authorization of a COVID-19 vaccine, pharmacists heard a litany of reasons why some have chosen to abstain from receiving the vaccine for themselves or their children. The most pervasive concerns tend to fall into one of two categories: misinformation about the science or political beliefs. Many parents’ reservations about having their children vaccinated can also be chalked up to misinformation, a lack of information, or political views. “When it comes to misinformation about science—the vaccine contains a microchip or it will make me grow a tail, etc.—I can manage those because I can show facts. I can show data,” said L.J. Tan, MS, PhD, chief policy and partnerships officer at Immunize.org (formerly Immunization Action Coalition). Pharmacists and other immunization stakeholders have a responsibility to provide accurate and appropriate information to help their patients make informed decisions. There is no shortage of data to prove to a patient which adverse effects and consequences do and do not come with the COVID-19 vaccines. Nearly 600 million doses administered in the United States help make up the more than 12 billion doses that have been administered worldwide. “This is probably the most-studied vaccine ever in terms of the number of doses given over a certain period of time,” Tan said. “So, we know what the vaccine's going to do regarding not only effectiveness but also safety.” Myths and misinformation about COVID-19 vaccines, such as claims about microchips and interference with one's DNA, abound. For pharmacists, the most common concerns that can be addressed with scientific data include ▪The FDA approval process was rushed or steps were skipped.▪The vaccine may cause unknown, serious adverse effects.▪The vaccine isn't safe for women who are pregnant, breastfeeding, or wish to become pregnant.▪COVID-19 is not serious enough to warrant a vaccine. Political concerns, Tan says, can be harder to counter. “I hear, ‘I'm not anti-vaccine. I believe the vaccine is safe, but you don't have the right to tell me what I can do with my body,’” Tan said. Similar concerns fueled antivaccine sentiment regarding the introduction of the smallpox vaccine as well, which gave rise to antivaccination organizations, rallies, and widely circulated journal articles. “That's an argument that requires a more nuanced conversation that, unfortunately, pharmacists don't always have time [to have].” These conversations, Tan adds, ought to include discussion of herd immunity and vaccines as a contribution to your community and to those who are in more vulnerable health. While the government has not in fact mandated COVID-19 vaccines, for some people the White House's and other federal agencies’ strong endorsement of it is concerning enough. “It's led to a distrust of the vaccine's origins,” Grabenstein said. These concerns can be particularly difficult to address in minority or marginalized populations in which distrust or fear of the government may have already been prevalent. “A lot of things have happened to Hawaiians in the past that have led to distrust of the government,” says Chaz Barit, PharmD, a clinical pharmacist at the VA Pacific Islands Health Care System in Honolulu. “And the government is the biggest promoter of the COVID-19 vaccine. A lot of people would rather hear it from anyone else but the government.” Undocumented immigrants may also fear the government's association with COVID-19 vaccines. Kevin Musto, PharmD, who owns Atlantic Apothecary in Smyrna, DE, ensures that immigrants know that they don't need to show identification or even provide their real name to become vaccinated. “I tell them that [when it's time for their second dose] they just need to provide the same name and birthdate … that they gave for their first,” Musto said. In instances when vaccine-contemplative patients are focused on the federal push to get the vaccine, Tan says, don't change the message; just change the messenger. Pharmacists should shift the focus to the local level and to entities patients are more likely to trust. “You might say, ‘The federal government is not mandating this vaccine, but the reason they are providing it for free and the reason that I, your pharmacist, recommend it is because it's going to protect you from the potentially disastrous consequences of COVID-19,” Tan said. “Remind them that it is not a government mandate, but that it is your recommendation as their pharmacist.” In these conversations, pharmacists may also add that not only they, but the vast majority of pharmacists, have been vaccinated against COVID-19. By May 2021, 92% of pharmacists who responded to an APhA survey were fully vaccinated (88%) or planned to be. One in ten Americans say that receiving a COVID-19 vaccine conflicts with their religious beliefs. Most are white evangelical Christians, according to a survey from the Public Religion Research Institute and the Interfaith Youth Core. While 60% of Americans and the majority of most major religious groups say there is no religious reason to refuse a COVID-19 vaccine, just 41% of white evangelicals would agree. The issue, however, is not restricted to white evangelicals. A 2021 Pew Research survey found that 33% of Black Protestants, compared to 36% of white evangelicals, were unwilling to get vaccinated. Catholics, too, may share some of the reservations that evangelicals have. The Pew study found that just over one in five (22%) of Catholics were unwilling to receive a COVID-19 vaccine. Christians’ reasons for abstaining from the COVID-19 vaccine vary. “There's a belief that your body is a temple, and [that] you have to keep it pure,” Grabenstein said. “There's the belief that God will protect you from COVID-19, and some people think that the vaccine contains aborted fetal cells, which it does not.” Richard K. Zimmerman's 2021 paper, “Helping patients with ethical concerns about COVID-19 vaccines in light of fetal cell lines used in some COVID-19 vaccines,” in the journal Vaccine details a set of responses clinicians can offer patients who have held off on the vaccine due to concerns about the use of fetal cells in their development or formulation. Zimmerman argues that taking the vaccine does not equate to complicity in the unrelated abortions of decades ago that led to the fetal cell lines used in the development of some, but not all, COVID-19 vaccines. Not taking the vaccine, however, equates to complicity in the further spread of the virus and the deaths associated with it. He also notes that mRNA vaccines, which are far more widely used in the United States, were not developed in fetal cell lines as the Johnson & Johnson/Janssen vaccine was. Zimmerman also says that to take the vaccine is an altruistic act; religious texts and religious leaders support vaccination. For example, Pope Francis has publicly stated that it is an “act of love” to receive a COVID-19 vaccine. Indeed, evangelical resistance to the COVID-19 vaccine is not coming down from the top, either. Before the COVID-19 vaccine became available, a national survey of evangelical leaders conducted by the National Association of Evangelicals found that 95% of evangelical leaders surveyed planned to get the vaccine when it became available, and 89% said they would encourage others to get it as well. Survey respondents stated that scientific evidence supporting the vaccine was sufficient and that getting vaccinated was part of a Christian obligation to care for others. Walter Kim, president of the National Association of Evangelicals, said, “While some have concerns about the newness of the vaccine, possible side effects or efficacy, a careful look at the science behind the vaccines is convincing, and the Christian ethic to love is compelling.” For its part, the Southern Baptist Convention, the governing body of the country's largest evangelical denomination, requires its foreign missionaries to get vaccinated. Last year, the organization's then-president Rev. J.D. Greear posted a photo of himself on Facebook as he received the vaccine. Still, the subset of Christians who continue to hold out against vaccination may be particularly difficult to persuade, research shows. In a study published in Proceedings of the National Academy of Science prior to the release of the COVID-19 vaccine, messaging that appealed to community interest, reciprocity, and the potential embarrassment of getting sick after refusing a vaccine was effective in persuading white evangelicals to accept vaccination once available. However, those same messages and others no longer persuaded white evangelicals who were still unvaccinated in May 2021. The FDA's extension of vaccination authorization to increasingly younger children—most recently to children from ages 6 months through 5 years—has given rise to another subset of vaccine contemplatives: parents who may have readily taken the vaccine themselves but who are not yet ready for their children to get it. Parents who hesitate to vaccinate or treat their child with any new drug or technology are not novel. Laws that mandated that children up to age 14 receive the smallpox vaccine caused great public outcry against vaccines in 1867. Both the Anti Vaccination League and the Anti-Compulsory Vaccination League arose in response to these laws. Perhaps the most famous parent who held back from embracing an early prevention option was Benjamin Franklin. In 1736, 60 years before a smallpox vaccine was available, some avoided death by smallpox through inoculation. This approach used a string which had been pulled through a smallpox pustule and then dried out. The string was then pulled through an incision made in the person to be inoculated, which infected them with an attenuated virus. The inoculated person would typically become only mildly ill, during which time they were contagious and after which time they were immune. About 2% of inoculated people died from smallpox, compared to the 15% who died after contracting it naturally. In his autobiography, Franklin wrote, “In 1736, I lost one of my sons, a fine boy of 4 years old, by the smallpox taken in the common way. I long regretted bitterly and still regret that I had not given it to him by inoculation. This I mention for the sake of the parents who omit that operation, on the supposition that they should never forgive themselves if a child died under it; my example showing that the regret may be the same either way, and that, therefore, the safer should be chosen.” Parents today who fear unknown consequences of COVID-19 vaccines for children are not so different from Franklin. And whether they choose to vaccinate or not vaccinate their child, all parents share one thing in common. “The parent is always trying to do what's right for their child. And we need to make sure that we don't belittle that,” Tan said. Parents tend to cite one of the following two reasons for holding out on having their children vaccinated. 1) There is little data on the vaccine and potential adverse effects in children compared to data on adults; and 2) the perception that children don't get very sick or die from COVID-19. Data on numbers of children who have become sick or died from COVID-19 are readily available for pharmacists to share with patients. While outcomes are indeed better for children than for adults, the risks of COVID-19 infection are far greater and more serious than any risks associated with the vaccine. Pharmacists can communicate these risks to parents. Likewise, while it is true that less data is available on younger vaccine recipients, large numbers of children have received the vaccine, and data is published about them. How pharmacists approach parents who are not ready to have their children vaccinated will depend on each parent's specific concern, but in every case “pharmacists can point out to parents that 100% of children's hospitals and 100% of health departments recommend the vaccine,” Grabenstein said. Pharmacists can also put parents’ actions into perspective. “Passive risk is much easier to accept than active risk. That is, if something bad happens because I didn't do something, I'm much more willing to accept that than if something bad happens because I did do something,” Tan said. “But the choice not to vaccinate a child is actually an active choice to leave that child vulnerable, potentially, to death.” For parents who may be unconcerned about their own child's vulnerability to COVID-19, pharmacists can remind them that vaccinated children are less likely to carry the virus and infect others with it, which helps protect vulnerable people in the family and community. For some parents, the option to receive vaccines from the familiar face of their local, community pharmacist may be enough to set their minds at ease. Pharmacists can leverage this role to help increase vaccination rates among children within their community. Mayank Amin, owner of Skippack Pharmacy in Skippack, PA, has gotten his fair share of pediatric vaccine experience since the COVID-19 vaccines became available. More than 25,000 children have received the vaccine through his pharmacy, either in store or at one of the many large public events he coordinated. Amin's public events resembled street parties, where music, food, and drink flowed and Amin circulated the crowd in a Superman costume. Receiving a vaccine was a special event inside his pharmacy, too. Amin created a dedicated vaccination room complete with aromatherapy, a television, colorful lights, and materials for patients of all ages to make thank-you cards during their post-injection 15-minute wait. Thousands of cards are plastered to the walls of the immunization room. “We weren't a pharmacy that had any specialization in pediatric vaccines, but some pediatricians—instead of ordering their own supply of vaccines—sent all their patients to us. Kids would come in the pharmacy shaking or trying to run away, but by the time they left, we heard many of them say to their parents, ‘Can we come back here for all our shots?’” George Zikry, PharmD, also made special accommodations for children at Hendricks Pharmacy in Claremont, CA. “We didn't know how hesitant or scared [adolescent patients] were going to be—and we never wanted anyone to feel rushed—so we scheduled longer appointments for them,” he said. Patients’ reasons for refusing or holding off on the COVID-19 vaccine for themselves or their children are not always immediately clear. But pharmacists are well positioned to ask. When you ask patients why they or their children have not received the vaccine, “Listen not to respond. Listen to understand,” Tan said. “Once you understand whether the patient's concerns [stem from] politics or misinformation, then you can acknowledge it and then start [the conversation] with the part that you agree on.” The point of agreement may be that you also have children; that you voted for the same candidate that they did; or that you, too, were surprised how quickly a vaccine became available. This validation may be enough to begin to move the needle with some patients. People who have not yet received the vaccine may be accustomed to, and even expect, pushback from health care providers in response to their stance. When they are met with patience, empathy, and understanding instead of resistance, it may change their attitude. “They want to be heard, and as soon as you listen and share your own story, people are a lot more comfortable,” said Renee Robinson, PharmD, an associate professor of pharmacy at the University of Alaska Anchorage/Idaho State University (UAA/ISU) Doctor of Pharmacy Program. Only after listening, understanding, and acknowledging, Tan said, should you address the patient's specific concern. These conversations can take time. “But once you address all their concerns … they are much more apt to get the vaccine,” Robinson said. Numerous online resources offer guidance for pharmacists and other clinicians on how to respond to common questions, fears, and misconceptions about COVID-19 vaccines. The APhA Vaccine Confident Playbook (apha.us/VCPlaybook) offers guidance for pharmacist-patient conversations about COVID-19 vaccines, with the goal of bolstering vaccine confidence, and increasing vaccine uptake. And the Immunize.org website includes handouts with tips for building vaccine confidence from various organizations available. Regardless of a patient's reasons for refusing a COVID-19 vaccine, keeping the focus on the recommendations of local figures may persuade the vaccine-contemplative. Pharmacists around the country have had success in boosting community vaccination rates by leveraging the influence of trusted local messengers. It may be enough to refer to trusted local people or organizations in conversations with patients. To those who are skeptical of the sweeping government support of the vaccine, pharmacists can point to local hospitals, universities, or other organizations that recommend vaccination. “You can say, for example, ‘Not just that university, but also our state university recommends it,’” Grabenstein recommended. Formal partnerships with respected locals also go a long way. Ritesh Patel, PharmD, organized vaccine clinics at area churches in North Carolina and Virginia, but rather than spread the word about the clinics himself, he had pastors email their parishioners and knock on their doors. “You can hear it from political officials or health care workers, but people listen to their pastors,” Patel said. “When pastors emailed, went door-to-door, and opened up their churches [for the clinics], we gave two, three, four thousand shots a day.” Victoria Hennessey, PharmD, owner of Community Pharmacy in Springdale, AR, leveraged trusted Marshallese leaders to help her vaccinate residents of Springdale, home to the largest population of Marshall Islanders outside of the Republic of the Marshall Islands. She partnered with the Marshallese Consulate and one of only two Marshallese physicians in the United States to offer a vaccine clinic to help address a deep-seated distrust of the U.S. health care system after past medical abuses. Rossi Pharmacy in Brooklyn, NY, partnered with UJA-Federation of New York, a Jewish philanthropic organization, to bring the vaccine to Jewish community centers in their area, which is home to the largest Orthodox Jewish community outside of Israel. There, rabbis joined forces with the pharmacists to address people's concerns and get the message out about the importance of vaccination. The UJA-Federation of New York provided volunteers from the local Jewish community, whose presence went a long way to reassure those who might be hesitant. “We even saw some of the volunteers hold the patients’ hands while they got vaccinated,” said Ambar Keluskar, PharmD, supervising pharmacist at Rossi Pharmacy. Pharmacists also leverage revered community members as vaccine advocates. Shadreka McIntosh, PharmD, a pharmacist in a predominantly African American community in Fort Myers, FL, found that young African American men were especially resistant to the vaccine. However, “Once you vaccinate a leader among them, they tell their friends where to go to get the vaccine,” she said. After McIntosh immunized a local barber, she saw many other young African American men follow his lead. “A barber can be seen almost like a counselor among African American men. Once this barber got vaccinated, he told lots of other men that they should get vaccinated too, and sent them here.” Residents of rural America may also get particular benefit from messaging that emphasizes local leadership and trusted community members. The National Rural Health Association offers a vaccine confidence communication toolkit for hospitals, business/community partners, and the community on its website. Conversations with vaccine-contemplative patients can be time-consuming, and the reality of a busy pharmacy is that pharmacists don't always have that kind of time. Realistically, it may take multiple conversations over weeks or months to persuade the last holdouts to get a COVID-19 vaccine. In the meantime, pharmacists must recognize that between encounters, patients will continue to be exposed to vaccine information and misinformation online by viewing it themselves or hearing from a family member or friend. Even people who may not consider themselves vaccine skeptics are susceptible to misinformation. Dipan Ray, BSPharm, PhD, an assistant professor at Touro College of Pharmacy and immunizer at a Rite Aid Pharmacy in New Jersey, says that combating misinformation has been a unique challenge of the COVID-19 pandemic. “People are going on Google, social media (e.g., Facebook, Twitter) and getting all kinds of stories, and they don't realize that they are all myths,” Ray said. Myths and misinformation appear on digital screens in response to the most seemingly innocuous search terms, according to a 2020 paper in Human Vaccines & Immunotherapeutics. Among 87 videos that appeared on YouTube as the search results to the queries “vaccine safety” and “vaccines and children,” a staggering 65% of them expressed antivaccine sentiment. Just 5.6% of the 87 videos were produced by government entities, and only 36.8% offered scientific evidence for claims made in the videos. In response to the queries “COVID-19” and “coronavirus,” 27.5% of the videos contained false information and, at the time the study was conducted they had received over 60 million views. Additionally, research published in 2021 in the Journal of Osteopathic Medicine found that from February 2020 to February 2021, Google searches for “infertility,” “infertility AND vaccine,” and “infertility AND COVID vaccine” skyrocketed, increasing by more than 1,000%. Dispelling these myths, Ray said, takes time. “I don't want to lose any patients due to wrong information. I have to spend time with them and make sure that they are comfortable.” For pharmacists struggling with busy schedules, perhaps the best use of limited time with vaccine-contemplative patients is spent educating them on how to separate fact from fiction and how to identify quality credible sources on the internet. “When you search for ‘vaccine safety’ and ‘vaccine information,’ you are going to find antivaccine sites,” Tan said. “You have to know where the information is coming from.” Pharmacists may suggest that patients ask themselves the following questions about the information they find online. The APhA Vaccine Confident Playbook offers further guidance under the topic “Identifying credible information about COVID-19.” ▪What kind of organization created this website? Web addresses that end in .edu or .gov may be more reliable sources of information, though that is not necessarily a hard-and-fast rule. Addresses that end in .org typically belong to nonprofit organizations that may or may not have conflicts of interest regarding the information they provide. Sites that end in .com are commercial and not the best place to start a search for unbiased and factual information about science.▪Does the information come from or include citations of peer-reviewed medical or scientific journals? To find out if an online journal is peer-reviewed, readers can look at the authors’ or contributors’ guidelines and make sure they say the articles are “peer-reviewed.”▪Does the provider of the information have an obvious financial conflict of interest? Patients should avoid websites that sell books, courses, or supplements or that charge for information.▪Does the provider of the information have experience in vaccine science or policy? Readers can search to see if the writer has published a peer-reviewed study; held a position on an advisory committee for CDC, FDA, or the European Medicines Agency; or held a position as a professor at a reputable university in a relevant area.▪Does the provider of information make their case with anecdotes or data? Multiple anecdotes do not equal a clinical study. In peer-reviewed research, scientists include thousands of people, not a handful of anecdotes. When pharmacists explain to patients the difference between anecdotes and data, they should acknowledge that “Storytelling is very compelling. When a mother says that her child was healthy until the child received a vaccine, these stories are incredibly powerful and compelling, but [you shouldn't] make a decision based on an anecdote. You should be very aware that you are reading a narrative,” Tan said. This type of vetting requires more legwork than patients may expect. So, too, does the research that goes into proving the safety and efficacy of a new vaccine. It's important for patients to understand that neither they nor vaccine researchers can conduct thorough research on a smartphone while waiting at a red light or in line at the grocery store. Challenges to vaccine confidence during the COVID-19 pandemic could be a sign of decline in global vaccine confidence in general on the horizon. Evidence of this is already apparent in some states where parents have managed to prevent the school system from requiring COVID-19 vaccination for school entry. “The antivaccine forces have used this argument to say, ‘If you can't mandate a COVID-19 vaccine for school entry, then you can't mandate that my child get any vaccine for school entry,’” Tan said. Vaccine advocates are working in these states to prevent COVID-19 vaccine exemptions from undermining previously existing vaccine requirements related to school entry. Lessons learned during the COVID-19 pandemic can help restore vaccine confidence in the future. For starters, lack of access to vaccines can help justify already skeptical patients in their decision to abstain. Lack of access comes in many forms. It could be a geographic or a digital barrier. There was no existing infrastructure prior to the pandemic for the swift dissemination of vaccines to the entire population. “We didn't have an adult immunization infrastructure in place. We set that up during COVID-19—increased use of pharmacists as immunizers, mass immunization clinic sites, etc. Let's do more of that. Let's keep those in place for flu shots and pneumococcal vaccines,” Tan said. Given growing skepticism toward the government and the health care system as a whole, Tan suggests the principal source of vaccine messaging going forward should be individual health care providers—including physicians, nurses, and pharmacists—more than national and federal organizations. “We have to make sure that our providers remain the number one trusted source of medical information,” Tan said. “It's about trusting relationships between patients and providers, and we need to leverage those trusted providers to communicate that all of these other vaccines are vaccines we have been giving for decades.”

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