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Research Paper

Human papillomavirus vaccine administration behaviors and influences among Arizona pharmacists and pharmacy interns

ORCID Icon, , , &
Pages 3090-3095 | Received 22 Dec 2020, Accepted 14 Mar 2021, Published online: 22 Apr 2021

ABSTRACT

This study assessed 27 Arizona community pharmacists’ and pharmacy interns’ human papillomavirus (HPV) vaccine administration behaviors and influences. We recruited community pharmacists and pharmacy interns from a statewide pharmacy conference to complete a 40-item cross-sectional survey. Informed by the Theory of Planned Behavior, the survey assessed pharmacists’ HPV vaccine-related behaviors, intentions, attitudes, subjective norms, and perceived behavioral control to vaccinate against HPV. We analyzed all data using descriptive statistics and correlations. Overall, most pharmacists held positive attitudes about the HPV vaccine. However, the majority rarely administered the HPV vaccine. Intentions to vaccinate and subjective norms positively correlated with vaccine administration behavior. Pharmacists’ positive attitudes about the vaccine, subjective norm to vaccinate, and behavioral control or self-efficacy to recommend the vaccine impacted their intentions to vaccinate against HPV. Most surveyed pharmacists believed that the most substantial HPV vaccine administration barriers include parental consent and parental stigma against the vaccine. The most common pharmacy-related barrier was the lack of a tracking and reminder system to encourage patients to return for additional HPV vaccine doses. This work highlights the need to increase public awareness that pharmacists can administer vaccines to adolescents. Study authors recommend offering communication training to increase pharmacists’ perceived behavioral control to recommend the HPV vaccine.

Introduction

In the United States, human papillomavirus (HPV) causes more than 31,000 cancer cases each year.Citation1 Persistent infection with cancerous HPV strains, most commonly Types 16 and 18, is responsible for the majority of cervical, vulvar, vaginal, penile, and oropharyngeal cancers.Citation1 Further, two non-cancerous strains, Types 6 and 11, cause the majority of genital warts. A 9-valent HPV vaccine series (GARDASIL 9) protects against Types 6, 11, 16, and 18 and five additional cancerous strains and has shown promise to significantly reduce HPV-related cancer incidence and genital warts.Citation2 To maximize the HPV vaccine’s effectiveness, individuals must complete the vaccine series, and the number of doses required to complete the series varies based on age and immunocompetence.Citation3,Citation4 To eliminate new HPV infections, HealthyPeople.gov created an objective (IID-08) to increase HPV vaccine completion to 80% among all youth ages 13–15 years old by 2030.Citation5 The U.S. is far below this goal. In 2018, slightly more than half (51%) of age-eligible youth had completed the vaccine series, and 68% had received one or more doses of the HPV vaccine series.Citation6 In Arizona, among adolescents between ages 13–18, 48% of females had completed the HPV vaccine, and 43% of males completed it.Citation7 Provider recommendation is the most significant predictor of HPV vaccine uptake.Citation8 To increase HPV vaccine uptake, it is critical to ensure that healthcare providers consistently provide a strong recommendation to vaccinate against HPV to age-eligible populations.

Traditionally, families have relied on primary care providers (PCPs), particularly pediatric and family medicine practitioners, to administer the HPV vaccine series. PCPs’ reported barriers to HPV vaccine administration include competing priorities during the clinical visit, difficulty in having adolescent patients attend wellness (compared to acute) visits, and lack of a reminder system to prompt families to return for the additional HPV vaccine doses.Citation9,Citation10 To overcome these multiple barriers and increase HPV vaccine series initiation and completion, the National Vaccine Advisory Committee and also the President’s National Cancer Panel have recommended pharmacies serve as additional sites to offer the vaccine.Citation11,Citation12 Receiving HPV vaccine doses administered by pharmacists may prove to be a more convenient method of ensuring vaccine completion due to pharmacies’ extended hours of availability, lack of required appointments, and geographic proximity to patients’ homes.Citation13,Citation14

It is important to note that in August 2020, due to the COVID-19 pandemic, the U.S. Department of Health and Human Services amended the Public Readiness and Emergency Preparedness (PREP) Act.Citation15 The amendment allows state-licensed immunizing pharmacists and pharmacy interns to administer FDA-approved vaccines to individuals between ages 3–18.Citation15 Before that time, states varied in terms of pharmacists’ abilities to offer pediatric and adolescent vaccines, including the HPV vaccine, based on patients’ ages.Citation16 A few months before the PREP Act amendment, the American Pharmacy Association reported that in two states, New York and New Hampshire, pharmacists were not allowed to administer the HPV vaccine. In Missouri and Georgia, states required pharmacists to receive a provider prescription to administer the vaccine, regardless of the patients’ ages.Citation16 In Arizona, according to Arizona Revised Statute 32–1974, an immunizing pharmacist and trained pharmacy interns under the supervision of a pharmacist could initiate and complete all vaccine doses (including the HPV vaccine) for children ages 13 and older and all booster doses for children ages six years old and older.Citation17 For children between ages 6–12, pharmacists needed a provider prescription to administer the first dose of any vaccine except for the flu vaccine.Citation17 Few research studies have assessed pharmacists’ behaviors related to administering the HPV vaccine, and, to our knowledge, none were theoretically-driven.Citation18–20 Our current research study, guided by the Theory of Planned Behavior (TPB),Citation21 assessed Arizona pharmacists’ and pharmacy interns’ HPV vaccine administration behaviors and influences after the federal government ratified the PREP Act amendment.

Previously, health researchers have utilized the TPB to guide research studies related to healthcare providers’ HPV vaccine communication and administration behaviors.Citation22,Citation23 TPB theoretical constructs include behavior, intention, attitudes, subjective norms (the belief that people who are important to an individual wish for them to enact or avoid certain actions), and perceived behavioral control (the self-efficacy to enact a behavior).Citation21 Further past research has used the TPB to guide survey research to assess pharmacy students’ intentions and attitudes related to administering vaccinations.Citation24 Therefore, driven by the TBP, our research study assessed community pharmacists’ and pharmacy interns’ behaviors, intentions, subjective norms, and perceived behavioral control and response efficacy to recommend/administer the HPV vaccine to age-eligible individuals.

Methods

Participant recruitment

We utilized a cross-sectional survey to assess HPV vaccine administration behaviors and influences among Arizona pharmacists and pharmacy interns. In October 2020, we recruited a convenience sample of community pharmacists and pharmacy interns at an annual statewide pharmacy convention. Due to COVID-19, the conference was held as a virtual conference via a mobile app. We created a virtual booth at the conference and advertised the study at the booth, in chat boxes during breakout sessions about immunizations, and on the discussion board located on the main page of the conference app.

We administered the survey online through the Qualtrics platform. The first page of the survey assessed whether potential participants met inclusion criteria (e.g., worked as either a pharmacy intern or pharmacist in an independent community or chain pharmacy). The next page provided study information and asked if participants consented to participate in the study. The survey software presented items which assessed TPB constructs in a randomized order. On average, participants took less than 10 minutes to complete the survey. The research team asked participants to provide their name and e-mail address on a non-linked survey page to e-mail them a 10 USD Amazon e-gift card as remuneration for their participation.

Survey instrument

Two study authors, including one study author with experience developing a theoretically-driven survey that assessed healthcare providers’ intentions to vaccinate against HPV,Citation22 collaborated to create a theory-informed survey. Two pharmacists, one who worked for a chain community pharmacy and the other who worked in a community clinic (and both regularly administered vaccinations in their practices), pretested the survey instrument. Based on their feedback, we refined the survey. The final instrument consisted of 40 items, 7 of which assessed survey respondents’ sociodemographic information, 23 of which assessed TPB psychosocial constructs, and 10 of which assessed various barriers and facilitators to vaccinating against HPV. The Arizona State University Institutional Review Board approved all study protocols and instruments.

We selected vaccine administration-related behaviors as the dependent variable. The survey assessed four different vaccine administration behaviors. The first question asked participants, “Have you ever vaccinated a patient against HPV?” (B1). Response options included the dichotomy of Yes/No. Questions 2–3 asked participants the same vaccine behavior question twice, once for age-eligible female and once for their age-eligible male patients. These questions asked, “In the past three months, how often have you recommended the HPV vaccine to age-eligible female (B2)/male (B3) patients (or their caregivers if they are minors)?” The last question asked participants “How often have you administered the HPV vaccine in the past three months?” (B4) Response options for Questions 2–4 included: Never (0% of the time), Not very often (1–33% of the time), Often (34–66% of the time), Very often (67–100% of the time).

We treated all other TPB constructs (intentions, attitudes, subjective norms, and perceived behavioral control) as independent variables. For all questions, response options included a 5-point Likert scale ranging from “totally disagree” to “totally agree”. We created an intention scale comprised of two statements. The first statement was, “Over the next three months, I intend to recommend the HPV vaccine to age-eligible individuals (or their caregivers if they are minors),” The second stated “Over the next three months, I intend to administer the HPV vaccine.” We measured attitude about recommending the vaccine with five statements. We included the following items: “The best way to prevent HPV infection is via vaccination”; “The HPV vaccine is a safe way to prevent HPV-related cancers”; “It is worthwhile for me to recommend the HPV vaccine”; “The HPV vaccine is an effective cancer prevention resource”; and “I believe recommending the HPV vaccine is acceptable.” We created a subjective norm scale based on four statements. These statements included the following: “The pharmacy I work for wants me to recommend the HPV vaccine to my patients”; “My pharmacy manager wants me to recommend the HPV vaccine”; “I believe that my patients want me to recommend the HPV vaccine”; and “I believe that my colleagues expect me to recommend the HPV vaccine.” Finally, we created a perceived behavioral control scale which included five statements. We asked participants to rate the following questions: “I am comfortable recommending the HPV vaccine to age-eligible children”; “I am confident about initiating a discussion about the HPV vaccine”; “I have the knowledge I need to recommend the HPV vaccine”; “I am confident that I can explain the HPV vaccine in a way that patients can understand”; and “I am confident that I can address patients’ questions and concerns when I talk to them about the HPV vaccine.” Additionally, we included the following three statements to assess pharmacists’ behavioral control to administer the vaccine: “It is easy for me to administer the HPV vaccine”; I have enough time to administer the HPV vaccine to patients”; and “My pharmacy usually has enough staff working to allow me to administer vaccines (such as the HPV vaccine).”

We asked participants to provide demographic information (age, gender, race) and professional information (e.g., designation as a pharmacist or pharmacy intern, years worked in retail pharmacy). We also asked participants to provide information about their pharmacy’s designation (e.g., independent, commercial/chain, or other), patient reminder capabilities (e.g., text message or phone call reminders to pick up prescriptions), and whether their pharmacy stocked the HPV vaccine. Last, we included two questions that assessed pharmacists’ perceived personal and organizational barriers to administering and strategies to increase HPV vaccination in their workplace.Citation25

Data analysis

We ran descriptive statistics to summarize participants’ characteristics. We used medians and interquartile ranges to describe TPB categorical data outcomes. We also used Spearman’s rho (ρ) to examine the correlations between vaccine administration behaviors and the TPB constructs. Statistical significance was set at α level < 0.05 with a 2-sided test. We conducted all analyses using IBM’s Statistical Package for the Social Sciences (SPSS) software, Version 26.0.

Results

A total of 304 individuals, including pharmacists (clinical, specialty, community, etc.), pharmacy technicians, researchers, and other individuals working in the healthcare industry, attended the conference. Of the attendees, 27 individuals completed the survey. The study sample was largely non-Hispanic White (n = 22, 81.5%), female (n = 19, 70.4%), and a mean age of 38.7 years old (ranging between ages 22–56). Among participants, 22 (81.5%) regularly administered vaccines as part of their job-related duties. The majority (19, 70.4%) reported that they knew their pharmacy stocked the HPV vaccine, and 16 (59.3%) have previously administered the vaccine. Most surveyed pharmacists reported they either never or infrequently administered the vaccine to age-eligible patients. However, four (14.8%) pharmacists often (34–66% of the time) vaccinated both male and female patients against HPV. See for additional information on pharmacy and pharmacy professionals’ characteristics and HPV vaccine-related behaviors.

Table 1. Study participants’ personal demographic information, work-related characteristics, and vaccine-related behaviors (n = 27) variable

illustrates TPB construct medians and interquartile ranges, with higher scores meaning stronger agreement with survey items. Two items received scores lower than a 4.0 on a 5-point scale. For subjective norms, participants neither agreed nor disagreed (3.00; 3.00–4.00) to the statement about their patients wanting them to recommend the HPV vaccine. Second, pharmacy professionals neither agreed nor disagreed (3.00; 2.00–4.00) that their pharmacies had adequate staffing to enable them to administer the HPV vaccine.

Table 2. Medians and interquartile ranges (IQRs) of theory of planned behavior constructs scores among pharmacy professionals (n = 27)

presents the correlations between TPB constructs and whether or not the pharmacist had ever administered the HPV vaccine. There was a good correlation between intention to vaccinate and HPV vaccination behavior (ρ = 0.457, p < .05). Similarly, there was a good correlation between their subjective norm to vaccinate and HPV vaccination behavior (ρ = 0.394, p < .05). Subjective norms to vaccinate (ρ = 0.719, p < .01), positive attitudes about the HPV vaccine (ρ = 0.719, p < .01), and behavioral control to recommend the vaccine (ρ=0.683, p < .01) were highly correlated with pharmacists’ intentions to administer the HPV vaccine to their patients.

Table 3. Correlation matrix examining theory of planned behavior constructs and HPV vaccination behavior (n = 27)

presents pharmacists’ reported HPV vaccine challenges and strategies to increase HPV vaccination. Pharmacists most often reported parental consent to vaccinate their children and also parents’ stigma against the HPV vaccine as barriers for pharmacist-administered HPV vaccinations. The most commonly reported strategies to increase HPV vaccination included providing parents with education about the HPV vaccine (n = 25, 92.3%). Additionally, 20 (74.1%) pharmacists identified having a system to remind patients to return for additional HPV vaccine doses as a strategy to overcome the lack of HPV vaccine completion.

Table 4. Barriers and strategies to administering the HPV vaccine among pharmacists and pharmacy interns (n = 27)

Discussion

This research utilized the TPB to identify influences on HPV vaccination behavior among immunizing pharmacists and pharmacy interns. In our study, and similar to past research,Citation20 pharmacists and pharmacy interns reported positive attitudes about the HPV vaccine, believing it is a helpful, important, and acceptable cancer prevention resource. However, regardless of their attitudes, most surveyed participants reported they either never or rarely administered the HPV vaccine. Past research surveyed a nationwide sample of pharmacists and reported that only 39% administered the HPV vaccine.Citation26 Another recent statewide study found that the HPV vaccine was the least administered immunization in Wisconsin pharmacies.Citation27

Survey data showed that pharmacists’ intentions to vaccinate followed by their subjective norms to administer the vaccine were the most significant correlations of their HPV vaccine administration behaviors. Although pharmacists and pharmacy interns reported their intentions to administer the HPV vaccine, most did not regularly vaccinate patients against HPV. This brings into question the effectiveness of using behavioral intentions to predict behavior. A meta-analysis of 185 research studies using the TPB to predict behavior change reported behavioral intentions are weak to moderate predictors of behavior (R = .47).Citation28 However, intentions are stronger predictors of behavior compared to other TPB constructs.Citation28

Pharmacists reported lower perceived subjective norm scores than scores for other TPB constructs. The median scores by survey item () illustrated that pharmacists neither agreed nor disagreed that patients or caregivers expected them to recommend the HPV vaccine, signifying a lack of patient demand for the vaccine. Similarly, past survey research with community pharmacists in Alabama identified the lack of patient demand for the HPV vaccine as a perceived barrier to vaccine administration.Citation20 Caregivers may lack awareness that many pharmacists can administer vaccines to children and adolescents.Citation19 Future health promotion efforts should raise awareness of pharmacy professionals’ abilities to administer adolescent vaccines, including the HPV vaccine.

Perceived behavioral control to vaccinate did not correlate with any other TPB construct. Further, it was the only construct that did not correlate with HPV vaccine-related intentions. Past research reported that perceived behavioral control was less predictive than subjective norms and positive attitudes on HPV vaccine administration intentions and behaviors among pediatricians.Citation22 On the other hand, perceived behavioral control to recommend the vaccine did correlate with HPV vaccine-related intentions. Future research could explore the impact of communication training for pharmacists and pharmacy interns to increase these providers’ perceived behavioral control to recommend the HPV vaccine to their patients.

Pharmacists reported various barriers to administering the HPV vaccine. Patient-related barriers were often related to parents’ discomfort and stigma against this vaccine. In past research, other patient-related barriers have included patients’ lack of insurance, vaccine refusal, lack of perceived need for the vaccine, and patients’ preference for receiving the vaccine elsewhere.Citation26 Other studies have identified the lack of insurance coverage (by non-governmental insurance plans) for pharmacist-administered HPV vaccination as a significant barrier to pharmacist-administered HPV vaccination.Citation19,Citation20,Citation29 To increase underinsured populations’ access to pharmacy-administered HPV vaccination, state Medicaid programs and health departments should expand their state’s Vaccine for Children program to recognize pharmacy professionals as vaccine providers.Citation29 In Arizona, specifically, the state health department and Medicaid program should change the Vaccines for Children Operations GuideCitation30 and policies to allow pharmacists, independent of physician oversight, to apply for the program and administer vaccinations.Citation29 Further, commercial insurance companies (third party insurers) should expand their plans’ vaccination benefits to include vaccination as a pharmacy benefit.Citation31Additionally, they should produce easy-to-understand insurance benefits information to increase insurance holders’ awareness that pharmacists can also administer adolescent and adult immunizations.Citation31

Pharmacists also identified pharmacy-related barriers to providing the HPV vaccine. They identified the lack of a reminder system to prompt patients and caregivers to return to the pharmacy for additional vaccine doses as an organizational-level barrier. Past research cited the following additional barriers at the pharmacy-level: financial loss when vaccines expire, inadequate vaccine reimbursement for pharmacist-administered vaccinations, costs of purchasing vaccines, and lack of having a separate, physical location to administer vaccines.Citation26

Before the August 2020 amendment to the PREP Act,Citation15 Arizona state law required pharmacists to receive a prescription to initiate vaccine series among individuals between ages 9–14. This law may have discouraged pharmacy professionals from administering the HPV vaccine. The need for a provider prescription created one additional step for these licensed professionals to offer vaccines to adolescents. Future work should assess the impact that the new federal amendment had on vaccine administration for children and adolescents.

Readers should consider numerous study limitations when interpreting our findings. First, our study included a small, non-diverse sample. However, previous research studies with pharmacy professionals have shared similar demographics.Citation19 We could not obtain the information related to the number of community pharmacists registered for this conference. Therefore, we could not calculate a response rate for survey completion among conference attendees. We conducted this survey at a virtual conference. Given the highly-motivated nature of individuals who attend conferences, our results may reflect sample bias. Further, the first author advertised this study by posting a study announcement. Individuals who view vaccines more favorably may have been more likely to respond, resulting in sample bias. Next, we assessed the barrier of lack of time to vaccinate with only one survey item. Past research has reported how community pharmacies often lack support staff, have a large workload, and have minimal time for breaks, leading to a stressful work environment.Citation32 Such an environment may impact pharmacists’ and pharmacy interns’ abilities to counsel patients about the HPV vaccine and administer vaccine doses. Finally, given the cross-sectional nature of this study, we cannot infer why some pharmacists regularly administered the HPV vaccine. Future qualitative research should explore why some immunizing pharmacists more often vaccinate their patients against HPV compared to pharmacists who less often administer this vaccine.

Conclusion

Pharmacy professionals have the potential to contribute to the prevention of HPV-related cancers by serving as another, more convenient location for age-eligible populations to receive HPV vaccine doses. Pharmacists and pharmacy interns have positive attitudes about the vaccine. However, pharmacy professionals in Arizona seldomly or never administer this vaccine. Positive attitudes about the vaccine and subjective norms to vaccinate against this virus were most strongly correlated with pharmacy professionals’ intentions to vaccinate against HPV. Future efforts should focus on increasing public awareness that pharmacists administer vaccines to adolescents, potentially impacting patient demand for this cancer prevention vaccine.

Disclosure of potential conflicts of interest

No potential conflicts of interest were disclosed.

Additional information

Funding

This research was support by the Arizona State University’s Institute for Social Science Research. The funding source was not involved in study design, collection, analysis, and interpretation of the data; in the writing of the report; and in the decision to submit this article;Arizona State University, Institute for Social Science Research.

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