Pharmacists’ Perceived Barriers to Human Papillomavirus (HPV) Vaccination: A Systematic Literature Review
2.1. Search Strategy
2.2. Study Selection & Data Extraction
3.1. Literature Search and Study Characteristics
3.2. Barrier Levels
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Appendix A. PubMed Search Strategy
- Centers for Disease Control and Prevention. Cancers Associated with Human Papillomavirus, United States—2013–2017; USCS Data Brief; Centers for Disease Control and Prevention: Atlanta, GA, USA, 2020. Available online: https://www.cdc.gov/cancer/uscs/about/data-briefs/no18-hpv-assoc-cancers-UnitedStates-2013-2017.htm (accessed on 9 April 2021).
- Centers for Disease Control and Prevention. Human Papillomavirus (HPV): HPV Vaccination is Safe and Effective; Centers for Disease Control and Prevention: Atlanta, GA, USA, 2021. Available online: https://www.cdc.gov/hpv/parents/vaccinesafety.html (accessed on 18 August 2021).
- Office of Disease Prevention and Health Promotion. Immunization and Infectious Diseases: IID-11.4 Increase the Percentage of Female Adolescents Aged 13 through 15 Years Who Receive 2 or 3 Doses of Human Papillomavirus (HPV) Vaccine as Recommended; Office of Disease Prevention and Health Promotion: Washington, DC, USA, 2020. Available online: https://www.healthypeople.gov/2020/data-search/Search-the-Data#objid=4657 (accessed on 25 April 2021).
- Office of Disease Prevention and Health Promotion. Immunization and Infectious Diseases: IID-11.5 Increase the Percentage of Male Adolescents Aged 13 through 15 Years Who Receive 2 or 3 Doses of Human Papillomavirus (HPV) Vaccine as Recommended; Office of Disease Prevention and Health Promotion: Washington, DC, USA, 2020. Available online: https://www.healthypeople.gov/2020/data-search/Search-the-Data#objid=10676 (accessed on 25 April 2021).
- Walker, T.Y.; Elam-Evans, L.D.; Yankey, D.; Markowitz, L.E.; Williams, C.L.; Mbaeyi, S.A.; Fredua, B.; Stokley, S. National, Regional, State, and Selected Local Area Vaccination Coverage Among Adolescents Aged 13-17 Years-United States, 2017. Morb. Mortal. Wkly. Rep. 2018, 67, 909–917. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Centers for Disease Control and Prevention. Human Papillomavirus (HPV): HPV Vaccine Schedule and Dosing; Centers for Disease Control and Prevention: Atlanta, GA, USA, 2019. Available online: https://www.cdc.gov/hpv/hcp/schedules-recommendations.html (accessed on 18 August 2021).
- President’s Cancer Panel. HPV Vaccination for Cancer Prevention: Progress, Opportunities, and a Renewed Call to Action. A Report to the President of the United States from the Chair of the President’s Cancer Panel; President’s Cancer Panel: Bethesda, MD, USA, 2018. Available online: https://prescancerpanel.cancer.gov/report/hpvupdate/pdf/PresCancerPanel_HPVUpdate_Nov2018.pdf (accessed on 9 April 2021).
- National Vaccine Advisory Committee. Overcoming Barriers to Low HPV Vaccine Uptake in the United States: Recommendations from the National Vaccine Advisory Committee: Approved by the National Vaccine Advisory Committee on 9 June 2015. Public Health Rep. 2016, 131, 17–25. [Google Scholar] [CrossRef][Green Version]
- National Association of Chain Drug Stores (NACDS). Face-to-Face with Community Pharmacies. Available online: https://www.nacds.org/pdfs/about/rximpact-leavebehind.pdf (accessed on 26 July 2021).
- Shen, A.K.; Peterson, A. The pharmacist and pharmacy have evolved to become more than the corner drugstore: A win for vaccinations and public health. Hum. Vaccines Immunother. 2020, 16, 1178–1180. [Google Scholar] [CrossRef] [PubMed]
- U.S. Department of Health and Human Services. HHS Expands Access to Childhood Vaccines during COVID-19 Pandemic. 2020. Available online: https://www.hhs.gov/about/news/2020/08/19/hhs-expands-access-childhood-vaccines-during-covid-19-pandemic.html (accessed on 19 April 2021).
- National Alliance of State Pharmacy Associations. Pharmacist Immunization Authority. 2020. Available online: https://naspa.us/resource/pharmacist-authority-to-immunize/ (accessed on 19 April 2021).
- Page, M.J.; McKenzie, J.E.; Bossuyt, P.M.; Boutron, I.; Hoffmann, T.C.; Mulrow, C.D.; Shamseer, L.; Tetzlaff, J.M.; Akl, E.A.; Brennan, S.E.; et al. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. BMJ 2021, 372. [Google Scholar] [CrossRef]
- Ouzzani, M.; Hammady, H.; Fedorowicz, Z.; Elmagarmid, A. Rayyan—A web and mobile app for systematic reviews. Syst. Rev. 2016, 5, 210. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Hastings, T.J.; Hohmann, L.A.; McFarland, S.J.; Teeter, B.S.; Westrick, S.C. Pharmacists’ attitudes and perceived barriers to Human Papillomavirus (HPV) vaccination services. Pharmacy 2017, 5, 45. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Ryan, G. Exploring opportunities to leverage pharmacists in rural areas to promote administration of Human Papillomavirus vaccine. Prev. Chronic Dis. 2020, 17. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Berce, P.C.; Bernstein, R.S.; MacKinnon, G.E.; Sorum, S.; Martin, E.; MacKinnon, K.J.; Rein, L.E.; Schellhase, K.G. Immunizations at Wisconsin Pharmacies: Results of a statewide vaccine registry analysis and pharmacist survey. Vaccine 2020, 38, 4448–4456. [Google Scholar] [CrossRef]
- Islam, J.Y.; Gruber, J.F.; Kepka, D.; Kunwar, M.; Smith, S.B.; Rothholz, M.C.; Brewer, N.T.; Smith, J.S. Pharmacist insights into adolescent Human Papillomavirus vaccination provision in the United States. Hum. Vaccines Immunother. 2019, 15, 1839–1850. [Google Scholar] [CrossRef] [PubMed]
- Skiles, M.P.; Cai, J.; English, A.; Ford, C.A. Retail pharmacies and adolescent vaccination—An exploration of current issues. J. Adolesc. Health 2011, 48, 630–632. [Google Scholar] [CrossRef]
- Tolentino, V.; Unni, E.; Montuoro, J.; Bezzant-Ogborn, D.; Kepka, D. Utah pharmacists’ knowledge, attitudes, and barriers regarding Human Papillomavirus vaccine recommendation. J. Am. Pharm. Assoc. 2018, 58, S16–S23. [Google Scholar] [CrossRef]
- Hurley, L.P.; Bridges, C.B.; Harpaz, R.; Allison, M.A.; O’Leary, S.T.; Crane, L.A.; Brtnikova, M.; Stokley, S.; Beaty, B.L.; Jimenez-Zambrano, A.; et al. US physicians’ perspective of adult vaccine delivery. Ann. Intern. Med. 2014, 160, 161–170. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Dillman, D.A. Mail and Internet Surveys: The Tailored Design Method; Wiley & Sons: New York, NY, USA, 1999. [Google Scholar]
- Holman, D.M.; Benard, V.; Roland, K.B.; Watson, M.; Liddon, N.; Stokley, S. Barriers to Human Papillomavirus vaccination among US adolescents: A systematic review of the literature. JAMA Pediatrics 2014, 168, 76–82. [Google Scholar] [CrossRef] [PubMed][Green Version]
- McCave, E.L. Influential factors in HPV vaccination uptake among providers in four states. J. Community Health 2010, 35, 645–652. [Google Scholar] [CrossRef]
- Barnack, J.L.; Reddy, D.M.; Swain, C. Predictors of Parents’ Willingness to Vaccinate for Human Papillomavirus and Physicians’ Intentions to Recommend the Vaccine. Women’s Health Issues 2010, 20, 28–34. [Google Scholar] [CrossRef]
- Centers for Disease Control and Prevention. Vaccine For Children (VFC) Program. 2016. Available online: https://www.cdc.gov/vaccines/programs/vfc/about/index.html (accessed on 18 August 2021).
- Malo, T.L.; Hassani, D.; Staras, S.A.; Shenkman, E.A.; Giuliano, A.R.; Vadaparampil, S.T. Do Florida Medicaid providers’ barriers to HPV vaccination vary based on VFC program participation? Matern. Child Health J. 2013, 17, 609–615. [Google Scholar] [CrossRef][Green Version]
- Walsh, B.; Doherty, E.; O’Neill, C. Since the start of the vaccines for children program, uptake has increased, and most disparities have decreased. Health Aff. 2016, 35, 356–364. [Google Scholar] [CrossRef][Green Version]
- Dullea, E.; Knock, K. Successes and Barriers to Pharmacists’ Participation in the Vaccines for Children (VFC) Program in the US. Immunize Colorado. 2020. Available online: https://teamvaccine.com/2020/08/04/successes-and-barriers-to-pharmacists-participation-in-the-vaccines-for-children-vfc-program-in-the-u-s/ (accessed on 20 April 2021).
- Merck Helps. Gardasil 9. Available online: https://www.merckhelps.com/GARDASIL%209 (accessed on 18 August 2021).
- The Henry J. Kaiser Family Foundation. The HPV Vaccine: Access and Use in the U.S. 2018. Available online: https://files.kff.org/attachment/fact-sheet-the-hpv-vaccine-access-and-use-in-the-u-s (accessed on 18 August 2021).
- Javanbakht, M.; Stahlman, S.; Walker, S.; Gottlieb, S.; Markowitz, L.; Liddon, N.; Plant, A.; Guerry, S. Provider perceptions of barriers and facilitators of HPV vaccination in a high-risk community. Vaccine 2012, 30, 4511–4516. [Google Scholar] [CrossRef]
- Calo, W.A.; Gilkey, M.B.; Shah, P.; Marciniak, M.W.; Brewer, N.T. Parents’ willingness to get Human Papillomavirus vaccination for their adolescent children at a pharmacy. Prev. Med. 2017, 99, 251–256. [Google Scholar] [CrossRef] [PubMed]
- Shah, P.D.; Calo, W.A.; Marciniak, M.W.; Golin, C.E.; Sleath, B.L.; Brewer, N.T. Service quality and parents’ willingness to get adolescents HPV vaccine from pharmacists. Prev. Med. 2018, 109, 106–112. [Google Scholar] [CrossRef]
- American Academy of Paediatrics. AAP: HHS Action on Pharmacy Vaccination ‘Misguided’. 2020. Available online: https://www.aappublications.org/news/2020/08/19/immunization081920 (accessed on 26 April 2021).
- American Academy of Paediatrics. American Academy of Pediatrics Opposes HHS Action on Childhood Vaccines; Calls It ‘Incredibly Misguided’. 2020. Available online: https://services.aap.org/en/news-room/news-releases/aap/2020/american-academy-of-pediatrics-opposes-hhs-action-on-childhood-vaccines-calls-it-incredibly-misguided/ (accessed on 26 April 2021).
- Omecene, N.E.; Patterson, J.A.; Bucheit, J.D.; Andersot, A.N.; Rogers, D.; Goode, J.V.; Caldas, L.M. Implementation of pharmacist-administered pediatric vaccines in the United States: Major barriers and potential solutions for the outpatient setting. Pharm. Pract. 2019, 17. [Google Scholar] [CrossRef][Green Version]
- Centers for Disease Control and Prevention. Immunization Information Systems. 2019. Available online: https://www.cdc.gov/vaccines/programs/iis/about.html (accessed on 18 August 2021).
- Martin, D.W.; Lowery, N.E.; Brand, B.; Gold, R.; Horlick, G. Immunization information systems: A decade of progress in law and policy. J. Public Health Manag. Pract. 2015, 21, 296. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Rand, C.M.; Brill, H.; Albertin, C.; Humiston, S.G.; Schaffer, S.; Shone, L.P.; Blumkin, A.K.; Szilagyi, P.G. Effectiveness of centralized text message reminders on Human Papillomavirus immunization coverage for publicly insured adolescents. J. Adolesc. Health 2015, 56, S17–S20. [Google Scholar] [CrossRef] [PubMed]
- Fiks, A.G.; Grundmeier, R.W.; Mayne, S.; Song, L.; Feemster, K.; Karavite, D.; Hughes, C.C.; Massey, J.; Keren, R.; Bell, L.M.; et al. Effectiveness of decision support for families, clinicians, or both on HPV vaccine receipt. Pediatrics 2013, 131, 1114–1124. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Wang, J.; Ford, L.J.; Uroza, S.F.; Jaber, N.; Smith, C.T.; Randolph, R.; Lane, S.; Foster, S.L. Effect of pharmacist intervention on herpes zoster vaccination in community pharmacies. J. Am. Pharm. Assoc. 2013, 53, 46–53. [Google Scholar] [CrossRef][Green Version]
- Tyler, R.; Kile, S.; Strain, O.; Kennedy, C.A.; Foster, K.T. Impact of pharmacist intervention on completion of recombinant zoster vaccine series in a community pharmacy. J. Am. Pharm. Assoc. 2021, 61, S12–S16. [Google Scholar] [CrossRef]
|Author, Publication Year||Sample Size||Study Population Characteristics||Pharmacy Setting||Vaccines Examined|
|Berce et al., 2020 ||236||Pharmacists located in Wisconsin (USA). 79% worked in pharmacies that were primarily located in urban counties (79%), 7% were in rural counties and 14% were located in multiple counties and/or in both rural and urban areas||Health system community (29%), chain community (27%), independent (26%), ambulatory care clinic (11%), inpatient (7%)||HPV, Influenza, Zoster, Pneumococcal, Tdap/Td, DTap, Hepatitis A and B, Hepatitis A, Meningococcal, MMR, Varicella, Polio and others|
|Hastings et al., 2017 ||154||One participant represented each pharmacy which included pharmacy owners, managers, or staff pharmacists located in Alabama (USA)||Chain pharmacy (53%), and independently owned (47%)||HPV|
|Islam et al., 2019 ||40||Pharmacists from 8 states (Alabama, Indiana, California, Maine, Kentucky, Tennessee, Texas, and Washington) in the USA that previously or currently were administering HPV, Meningococcal, Tdap or TD vaccines to adolescents||Chain (78%), independent (13%), grocery (5%), big box retailer (5%)||HPV|
|Ryan et al., 2020 ||11||Pharmacists in 7 rural counties in Iowa (USA)||Independently owned (100%)||HPV|
|Skiles et al., 2011 ||24||Pharmacy association directors or designees from all 50 states in the USA were targeted (92% were pharmacists)||Information not reported||HPV, Tdap, Influenza|
|Tolentino et al., 2018 ||240||Community pharmacists in Utah (USA)||Community/outpatient (80%), ambulatory care clinic (10%), community outpatient and inpatient (8%), other (3%)||HPV|
|Author, Publication Year||Study Design||Data Collection Tool||Data Reporting|
|Berce et al., 2020 ||Cross-sectional survey design using an anonymous electronic survey||Modified version of a previous national physician survey  on barriers to adult vaccination which asks respondents to classify multiple potential barriers to immunization on a 4-point response scale.||Barriers were grouped by pharmacies that provide and do not provide immunization.|
|Hastings et al., 2017 ||Cross-sectional survey design using a modified version of Dillman’s Tailored Design Method of survey administration ||A 65-item survey that took approximately 15 min to complete. Measures were categorized into 5 sections: 1. key informant and pharmacy site demographic characteristics; 2. general vaccination services and strategies used to increase HPV vaccine uptake; 3. pharmacists’ perceptions of HPV and the vaccine; 4. perceived system barriers to the provision of HPV vaccinations; and 5. perceived parental reasons for HPV vaccine hesitancy. Most of the questions were 5-point Likert-type rating scales. Questions measuring HPV and the vaccine perceptions were adapted from an existing instrument. Questions assessing system barriers were informed by previous research.||Descriptive statistics were used to describe participants characteristics, vaccine practices, barriers and attitudes.|
|Islam et al., 2019 ||Cross-sectional study design using semi-structed interview to complete a survey||Survey items included 52 close-ended questions and 24 open-ended questions to examine pharmacists insights into administering vaccines. Interviews lasted 30–60 min.||Semi-qualitative responses were analyzed using thematic analysis, to create response categories and then coded using descriptive frequency statistics.|
|Ryan et al., 2020 ||Cross-sectional study design using interview.||Interview guide using questions and concepts adapted from a previous project that included the following topics: the role of rural, independent pharmacists in HPV vaccine promotion and uptake; willingness to educate parents, refer patient, and administer the HPV vaccine; priority of HPV vaccine promotion, and vaccination barriers and facilitators in the pharmacy and the community||Interview responses were analyzed using thematic analysis.|
|Skiles et al., 2011 ||Cross-sectional study design using telephone interviews to complete a survey||Survey questions asked about immunization practices, vaccine beliefs, minor consent issues, and minor consent laws. Responses to the attitude and/or belief questions were measured on a 5-point Likert scale.||Attitude and belief responses were collapsed to a dichotomous response for analysis. Differences in attitudes across vaccines were tested using score test on the basis of the generalized estimating equation for the generalized linear model.|
|Tolentino et al., 2018 ||Cross-sectional study design using an anonymous electronic survey||A 73-item survey adapted from an HPV vaccination survey previously conducted with Utah primary care providers that asked about HPV vaccination knowledge, attitudes about the HPV vaccine, behavior for recommending the vaccines (HPV, influenza, meningococcal disease, Tdap), and barriers for adolescents’ vaccination. Survey questions were multiple choice, true/false, and Likert scale.||Descriptive statistics were used to analyze the demographics of pharmacists, as well|
as their knowledge and attitudes regarding the HPV vaccine, vaccine recommendation levels and strategies, and self-identified barriers to vaccine recommendations. Content analyses were used to identify the themes.
|Author||Summary of Findings|
|Skiles et al. ||96% reported that financial challenge is a barrier to HPV vaccination access for adolescents (p < 0.001); 75% of participants reported that access to HPV vaccine is moderately to extremely difficult (p = 0.030); 67% reported that ACIP recommendations are moderately to extremely controversial in the community (p < 0.001)|
|Hastings et al. ||Participants reported the following as very/extremely likely to be a system-related barrier to HPV vaccination: lack of demand (56.5%), failure of cost coverage by insurance (54.8%), vaccine expiration before use (54.1%), difficulty ensuring patients are completing the necessary 3 doses (39.9%), and lack of adequate reimbursement (38.4%).|
Participants reported that they somewhat agree/strongly agree that the following are parent-related barriers to HPV vaccination: lack of education (86.6%) safety concerns (78.7%), reluctancy to talk about sexuality/sexually transmitted infections (76%), concerns that agreeing to vaccination means they support premarital sex (67.3%), concerns about efficacy of vaccine (64.6%), cost (53.3%), believe that their children are not at risk (67.3%), believe that their children are too young (65.3%), concern that children will practice riskier sexual behaviors (58.7%).
|Berce et al. ||Insurance and time/priority were reported as largest barrier. Compared with those that do not immunize, financial barrier was larger among those that do immunize (p = 0.022).|
Barriers reported among those that do immunize included patients having insurance coverage for vaccines (90%), patients refusal due to financial reasons (89%), patients refusing vaccine (89%), determining insurance reimbursement (87%), other responsibilities taking precedence (84%), patient refusal due to perceived safety issues (79%), lack of staff (78%), remembering to screen patients (76%), having enough demand to justify the cost of stocking vaccines (71%), upfront cost of buying vaccines and supplies (55%), adequate compensation for administration (72%), and adequate compensation for product (68%) and supplies (58%) purchase.
Barriers reported among those that do not immunize included other responsibilities taking precedence over vaccinating (94%), patient refusal (72%), patient refusal due to perceived safety issues (67%), determining insurance reimbursement (66%), lack of staff (61%), remembering to screen patients (60%), patient having insurance coverage (57%) and adequate compensation for administration (53%).
|Ryan et al. ||Barriers were grouped into personal and organizational barrier. Personal barriers included sensitivity on the subject of HPV infection, lack of information, safety concerns, misinformation about HPV vaccination coverage and access. Organization barriers include lack of time and staff, liability issues relating to adverse effect after vaccination, low number of adolescents coming to the pharmacy, and competition with local health care providers.|
|Tolentino et al. ||Barriers reported included lack of parental knowledge, parental concerns/opposition, lack of educational materials for parents, high copay, lack of demand from parents, lack of time and space, high priority for other vaccines compared with HPV, and lack of incentive for series completion.|
|Islam et al. ||Major barriers to providing HPV vaccines to adolescents included the following: parental consent (28%), tracking and recall of patients (17%), stigma about vaccination among parents (17%), education/vaccination promotion (17%), cost of vaccination (11%), potential adverse reactions (11%).|
|Author, Year||Barrier Levels|
|Skiles et al., 2011 |
|Hastings et al., 2017 |
|Tolentino et al., 2018 |
|Islam et al., 2019 |
|Berce et al., 2020 |
|Ryan et al., 2020 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Oyedeji, O.; Maples, J.M.; Gregory, S.; Chamberlin, S.M.; Gatwood, J.D.; Wilson, A.Q.; Zite, N.B.; Kilgore, L.C. Pharmacists’ Perceived Barriers to Human Papillomavirus (HPV) Vaccination: A Systematic Literature Review. Vaccines 2021, 9, 1360. https://doi.org/10.3390/vaccines9111360
Oyedeji O, Maples JM, Gregory S, Chamberlin SM, Gatwood JD, Wilson AQ, Zite NB, Kilgore LC. Pharmacists’ Perceived Barriers to Human Papillomavirus (HPV) Vaccination: A Systematic Literature Review. Vaccines. 2021; 9(11):1360. https://doi.org/10.3390/vaccines9111360Chicago/Turabian Style
Oyedeji, Oluwafemifola, Jill M. Maples, Samantha Gregory, Shauntá M. Chamberlin, Justin D. Gatwood, Alexandria Q. Wilson, Nikki B. Zite, and Larry C. Kilgore. 2021. "Pharmacists’ Perceived Barriers to Human Papillomavirus (HPV) Vaccination: A Systematic Literature Review" Vaccines 9, no. 11: 1360. https://doi.org/10.3390/vaccines9111360