HPV immunisation: A review of parent and stakeholder attitudes on school-based programmes

According to the Centers for Disease Control and Prevention (CDC) (2015) 8 billion dollars are spent annually in the United States on the management of complications for human papillomavirus (HPV) infections; exceeding the health-care and economic burden of any other sexually transmitted infection (STI) and leading to the importance of early HPV vaccination for both males and females. The CDC and the Advisory Committee on Immunization Practices (ACIP) recommend routine HPV vaccination for 9–26-year-olds to reduce HPV-associated cancers, preferably between the ages of 11 and 12 years (American College of Obstetricians and Gynaecologists [ACOG], 2017). Despite the clinical significance of routine vaccination, vaccination rates in adolescents in the United States are suboptimal.

HPV vaccination can help reduce the health-care burden by decreasing the incidence of cervical cancer, anogenital cancers, oropharyngeal cancers and genital warts. ACOG (2017) reports that only 41.9% of females and 28.1% of males in the recommended age groups received all of the recommended doses; proving the clinical significance of implementing an HPV vaccine school-based programme for males and females to prevent HPV-related cancers (CDC, 2015; ACOG, 2017).

Health-care providers, school staff members, public health officials and the media have a crucial role in educating stakeholders (i.e. school health staff members, adolescents and parents) about the importance of adhering to the vaccine schedule to reduce the HPV-related health-care burden (ACOG, 2017). Education should target middle school stakeholders due to the preferred target age range for initiating the HPV vaccine. By targeting students through their parents or health-care providers at this age, it will potentially better prepare them for participation in vaccine health-care decisions.

The significance of the clinical data obtained in review of the literature supports the development and implementation of HPV vaccine guidelines to promote prevention and early detection of HPV-related cancers and other conditions attributed to HPV. This integrative review explores school-based HPV vaccination programmes' strengths and areas for improvements.

‘Health-care providers, school staff members, public health officials, and the media have a crucial role in educating stakeholders about the importance of adhering to the vaccine schedule to reduce the HPV-related health-care burden.’

Background

Prevalence

HPV is the leading STI in the United States, associated with various cancers and genital warts, and affecting 79 million individuals (CDC, 2015). According to the CDC, 80% of women and 90% of men will become infected with at least one strain of HPV in their lifetime (Head et al, 2018). Approximately 14 million new cases occur each year with 7 million affecting 15–24-year-olds (CDC, 2015). HPV infections are generally asymptomatic initially, but repeated infections can lead to various cancers (Lu et al, 2015). In the United States, HPV is the most common STI with more than 120 genotypes of the virus (ACOG, 2017; CDC, 2015). The virus has the ability to affect the epithelium of the skin leading to warts or abnormal changes in the epithelium of the mucosa, which can lead to an increased predisposition to cervical cancer (CDC, 2015). HPV is associated with genital warts, and cervical, oropharyngeal and anogenital cancer (ACOG, 2017).

HPV is associated with approximately 44 000 cases of cancer per year in the United States; affecting nearly 25 000 women and 19 000 men (CDCa, 2019). An estimated 91% of cervical, 75% of vaginal, 69% of vulval, 63% penile, 91% of anal and 70% of oropharyngeal cancers are thought to be caused by HPV (CDCa, 2019). Worldwide, high risk strains 16 and 18 are associated with 70% of cervical cancers and 90% of genital warts are caused by low risk types 6 and 11 (ACOG, 2017). Cervical cancer is the 14th leading cause of death in women, affecting over 13 000 women and causing over 4 000 cancer-related deaths (Saslow et al, 2012; CDC, 2019). Whereas, oropharyngeal cancer is more common in men affecting 15 540 individuals. Cancers of the oropharynx traditionally associated with tobacco and alcohol use have recently been linked with HPV (CDCa, 2019).

Healthy People 2020 reviewed the statistics derived from the United States' National Immunization Survey (NIS) that targeted adolescents, and then created two objectives targeting males and females and HPV vaccine uptake. According to the data received from NIS, the number of females aged 13 to 15 years who received the recommended three doses and males who receive two or three doses of the HPV vaccine from 2008 to 2016 have steadily increased relating to the increase in education on the vaccine and its benefits. In 2008, the baseline for females was 16.6% and gradually increased to 45.1% in 2016 (US Department of Health and Human Services, 2020). In 2014, the objective for male adolescents was added to Healthy People 2020 as recommended in the revision to the 2012 ACIP. Male adolescents increased from 6.9% in 2012 to 36.4% in 2016. Both genders have a target goal of completed HPV vaccine series of 80% by 2020, which correlates with the CDC prediction of a decrease in 53 000 cancer cases (U.S. Department of Health and Human Services, 2020). The 2017 NIS-Teen survey has demonstrated an increase in vaccine coverage in both genders. Nearly 50% of adolescents were up to date on the HPV vaccine series by 2017 and 66% initiated the vaccine series without completion. Even though statistics are indicating an increase in HPV vaccine among adolescents, approximately 50% are still unvaccinated or have not completed the vaccine series (US Department of Health and Human Services, 2020). Despite the clinical significance of routine vaccination, vaccination rates in adolescents in the United States are alarmingly low.

Three vaccines are available to decrease the risk of HPV-related cancers, including the quadrivalent (HPV4), bivalent (HPV2), and nonavalent (HPV9) vaccines. All prevent high risk strains HPV types 16 and 18. However, despite recommendations, immunisation remains suboptimal compared to the Healthy People 2020 objectives. In 2015, only 49.8% of adolescent males and 62.8% of females had initiated the HPV vaccine series (CDC, 2015). Understanding the gap in HPV vaccine recommendations and administration during this age group is crucial to overcome the significant economic costs related to treatment and prevention of HPV-related cancers and associated complications, as well as, addressing preventable cancer-related deaths.

Human papillomavirus vaccine

In the 1980s, epidemiologic studies demonstrated cellular changes in cervical cells containing HPV DNA. These findings were consistent with an association between HPV and cervical cancer predisposition (CDC, 2015). The study published its findings in the 1990s and created an opportunity for future research into the association between high-risk HPV strains 16 and 18 and cervical cancer and anogenital cancer. High-risk HPV types (including 16 and 18) have been linked to 99% of cervical cancers (CDC, 2015). As a result, the first HPV vaccine was licensed in 2006 and three in total were approved in the United States (CDC, 2015). Quadrivalent HPV vaccine or HPV4, such as Gardasil, was approved by the US Food and Drug Administration in 2006 for both males and females aged 9 to 26 years of age. HPV4 vaccine contains 4 HPV genotypes, types 16 and 18 which are high-risk HPV types 6 and 11 which are low risk (CDC, 2015). Bivalent HPV vaccine or HPV2, such as Cervarix, was approved in 2009 for females aged 10 to 25 years of age. Cervarix contains HPV genotypes 16 and 18 (CDC, 2015). Both vaccines are highly effective against the prevention of HPV-related cervical intraepithelial neoplasia (CIN) 2 and/or 3 and adenocarcinoma in situ (AIS) (CDC, 2015). Clinical efficacy of the HPV4 vaccine was determined in two double-blind and placebo studies of females 16 through 26 years of age. The HPV4 vaccine has been found to prevent 97% of high-risk HPV 16 and 18-related CIN 2/3 and AIS and 99% against HPV 6, 11, 16, and 18 which are associated with genital warts (CDC, 2015). In men aged 16 to 26 years, the HPV4 vaccine prevents 88% of genital warts and 75% prevention of anal intraepithelial neoplasia 2 and/or 3 (CDC, 2015). Clinical efficacy of HPV2 vaccine was determined in two randomised and double-blind controlled trials in females 15 to 25 years of age. The HPV2 vaccine's efficacy against HPV 16 or 18-related CIN 2/3 or AIS was found to be 93% (CDC, 2015).

Epidemiologists have associated HPV with precursor lesions for cervical cancer and cervical cell abnormalities since the 1980s, leading to the first HPV vaccine in 2006 (CDC, 2015). HPV is transmitted via sexual contact and affects over 14 million men and women (CDC, 2015). With more than 120 different identifiable strains, most sexually active individuals will become infected with HPV and eliminate the virus without any symptoms and complications (CDC, 2015). However, repeated HPV infection with high risk strains leads to a predisposition of cervical cancer development by altering cervical epithelium cells (CDC, 2015). In addition to cervical cancer development, anogenital and oropharyngeal account for an increasing prevalence of cancer cases, and CIN 2, CIN 3 and AIS have been linked to persistent HPV infections (CDC, 2015).

Since the development of vaccines, many diseases that were once deadly and a great burden to the health-care system have dramatically decreased in incidence or have been eradicated. However, in recent years we have seen a re-emergence of many vaccine-preventable diseases worldwide, which have been associated with low vaccine coverage (Esposito et al, 2014). This further demonstrates the importance of routine recommendations, and the importance of implementing early screening and vaccine education.

Literature review

Literature search Between September 2019 and June 2020, a literature search was performed using electronic databases and academic journals. The search terms used included:

• Human papillomavirus
• HPV vaccine
• Adolescent vaccines
• School-based vaccine programmes
• School-based HPV vaccine programmes
• School health education
• Vaccine hesitancy
• Vaccine recommendations
• HPV provider vaccine recommendations.

Several online databases were used to identify evidence-based resources including (PubMed Central, Academic Search Premier, ScienceDirect, Elsevier, CDC, ACOG, The National Center for Biotechnology Information, the National Institutes of Health), as well as reference list searches from previous reputable sources. Approximately 6 750 articles were found and further reduced to a total of 17 articles after a review of the article titles, abstracts, keywords, time frame of less than 10 years, and clinical relevance to the aim and goal of the integrative review. Articles were eliminated based on relevance to integrative review, not peer-reviewed, not being a full-text, non-English and older than 5 years. A few articles within a 10-year time frame were included based on significance and support for the purpose of the integrative review. Seven articles were used for the introduction and to support the background and prevalence of the argument. Ten articles were further analysed and used to support the literature review (Thompson et al [2017], Vorsters and Van Damme [2018], Shapiro et al [2017], Hirth et al [2019], Head et al [2018], Dempsey and Schaffer [2010], Esposito et al [2014], Lu et al [2015], Reiter et al [2011] and Williams et al [2019]). Table 1 shows the barriers of implementation of HPV education and vaccination and themes found in the 17 articles included in this review.

Data evaluation

Evidence from research literature The World Health Organization recognises vaccine hesitancy as a global health concern even in the presence of vaccine recommendations. One of the most common reasons for vaccine hesitancy and adherence is related to parental attitudes and involvement in vaccine decision-making. Factors influencing decision-making include (Thompson et al, 2017):

• Vaccine safety
• Vaccine knowledge deficit
• Association of vaccines and increasing sexual activity of the child
• Insurance coverage
• Social and other parental influence.

Thompson et al (2017) reviewed parental attitudes and reasoning toward HPV vaccination in order to understand the barriers to improve vaccine rates. The level of vaccine hesitancy and reasoning for choosing not to vaccinate varied by gender. Vaccine attitudes have changed over time and is evident in the NIS-Teen survey from 2012 to 2015 referenced in this study. The primary reason for choosing not to vaccinate against HPV for males was the lack of primary care provider recommendation and vaccine knowledge deficit, whereas concern for safety and side effects was evident for females (Thompson et al, 2017). Understanding the information presented in this study can help practitioners with addressing parental concerns and improving vaccine coverage.

In the United States, a recent increase in male oropharyngeal and anal cancers has been found. Men in particular have lower incidences of HPV vaccine coverage. Previous research showed a vaccine acceptance rate of 1.4% in 2010 and 8.3% in 2011 in adolescent males (Lu et al, 2015). Lu et al (2015) were the first in the health-care community to address these disparities in coverage in adolescent males. Unvaccinated males pose a great burden to HPV infection transmission and potentially increase the occurrence of repeated infection and exposure. In turn, their female sexual partners are at increased risk of further exposure and cervical cancer with each exposure. The ACIP recommends the HPV vaccine to be considered as a routine vaccination for adolescent males and females related to the increased risks (Lu et al, 2015).

The 2013 NIS-Teen data was used to assess vaccine adherence and a multivariable logistic regression analysis and predictive marginal model was used to identify independent and dependent variables and barriers to vaccine adherence in male adolescents. There was a 34.6% vaccine coverage of adolescent men who received at least one dose and 13.9% received at least three doses of HPV vaccine (Lu et al, 2015). Non-Hispanic white males had lower incidences of coverage as compared to Hispanic and black ethnicities. Other factors that increased likelihood of higher vaccine coverage in adolescent males included (Lu et al, 2015):

• Having mothers who are unmarried (widowed, separated, or divorced)
• Having seem more than one physician in the past year
• Having one to two vaccine providers and facilities
• Having an 11–12-year-old well child visit
• Residing in urban and suburban areas.

In contrast, factors that reduced the rates of HPV vaccine coverage included (Lu et al, 2015):

• Mothers with a college education
• Higher household income
• Residing in Midwest or Southern United States,
• Receiving vaccines from a clinic.

The 2016 NIS-Teen statistics were compared to the previous 2013 NIS-Teen statistics to obtain vaccine data and assess progression of coverage. Between 2008 and 2016, the parents of 158 896 females and 173 515 males were interviewed (Hirth et al, 2019). Of the 332 411 participants, 143 721 parents provided regional data and 90 866 reported that they did not intend to get their child vaccinated (Hirth et al, 2019). Of the 90 866 parents who declined to vaccinate, 55% had male children (Hirth et al, 2019). The NIS-Teen results showed that 56% of adolescent males and 65% of females had initiated the HPV series and 38% of males and 50% of females had completed the series (Head et al, 2018). Both male and female adolescents fell below the Healthy People 2020 target goal of 80% indicating suboptimal vaccine rates; however, vaccine adherence rates had improved as compared to the previous 2013 NIS-Teen data. The number of parents who did not intend to vaccinate fell from 72% in 2008 to 58% in 2016 (Hirth et al, 2019). Approximately 22.4% of parents felt that the vaccine was not necessary, which was the most frequent reason for vaccine hesitancy, 16.2% reported a lack of provider recommendation, and 15.6% reported a lack of vaccine knowledge as the main reasons for declining the HPV vaccine (Hirth et al, 2019).

In addition, reasons for declining the vaccine vary by gender, across regions and ethnicities. Hirth et al (2019) found that non-Hispanic black and Hispanic families were more hesitant and more likely to decline the HPV vaccine due to concern for increasing sexual behaviour after vaccination as compared to white parents. Hispanic parents were more likely to report a lack of provider recommendation, a lack of vaccine knowledge, and no school requirement as reasons for declining vaccination compared to white parents. This is concerning due to the disproportionately higher prevalence of HPV-related cervical and oral cancers among the Hispanic population (Hirth et al, 2019). The white parents were more likely to decline immunisation due to the notion that the vaccine was not needed or a requirement compared to Hispanic parents. Non-Hispanic black parents were more likely to report a lack of provider recommendation, lack of vaccine knowledge, or parental decisions for declining vaccination. However, non-Hispanic black parents were less likely to report vaccine safety concern, appropriate age, cost, or child vaccine fears as reasons for declining as compared to white parents. Groups other than Hispanic, black or white were more likely to report lack of provider recommendation and lack of vaccine knowledge as the main reasons for choosing to not vaccinate and a lower incidence of vaccine safety concerns. Alarmingly, the most frequent reasoning for declining vaccination among all groups assessed was a lack of provider recommendations (Hirth et al, 2019).

There are also regional differences among parents in the United States who decline HPV vaccine. Parents in the Midwest, South, and West are least likely to report lack of provider recommendation. Parents in the South were least likely to report that the vaccine was not age appropriate as a reason for declining. Western parents were least likely to report vaccine safety concerns and male gender as a reason for declining. Midwestern parents are more likely to report lack of vaccine knowledge as compared to the Northeast. The parents of the Midwest, South, and West were more concerned with time and cost associated with vaccination and more likely to report that the vaccine was not required for school as compared to the Northeastern parents (Hirth et al, 2019).

Williams et al (2019) discussed the factors associated with vaccination rates among adolescents in metropolitan statistical areas (MSA) versus rural areas. MSA and principle cities are considered urban areas and MSA non-principal cities as suburban areas and non-MSA as rural locations (Williams et al, 2019). The study compared all respective regions and adolescent adherence to vaccine coverage and analysed sociodemographic and socioeconomic variances to vaccine adherence. The 2016 and 2017 National Immunization Surveys-Teen (NIS-Teen) survey was analysed among 13-to-17-year olds in the United States. A telephone interview with age-appropriate households was initially conducted. Parents and guardians were asked specific questions regarding vaccine history and adherence, sociodemographic factors of the adolescent and household, and obtained consent to contact the primary care provider. A questionnaire was sent via mail to the adolescents' primary care provider in regard to detailed vaccine history (Williams et al, 2019).

Adolescents in suburban and rural areas had a lower incidence of having received the first dose of the HPV vaccine compared to urban areas. Multiple barriers for HPV vaccine administration were common across all MSA areas. Common barriers that affect vaccine rates are (Williams et al, 2019):

• Living in the Southern United States
• Some maternal college education
• Increasing maternal age
• A lack of well child visit for 11–12-year-olds
• No HPV recommendation from health-care providers.

Additional factors may be related to the increased occurrence of HPV-related health-care burden, such as a lack of primary care providers, and preventative screening and care. A reduction in vaccine coverage in these areas is thought to be associated with financial burdens, lack of access to health care, and reduction in provider recommendations for screening and vaccination (Williams et al, 2019). This is concerning based on the high incidence of cancer-related occurrences with each increase in HPV infection, and the lower vaccine coverage in the rural areas, which generally experience a greater burden with HPV-related cancers (Williams et al, 2019).

The study analysed a total of 41 424 adolescents between 11 to 12-year olds who received tetanus, diphtheria and acellular pertussis (Tdap), quadrivalent meningococcal conjugate (MenACWY), and the first dose of the series of the HPV vaccine as part of routine administration (Williams et al, 2019). A bivariate analysis and multiple logistic regression was performed to evaluate the sociodemographic and its effect on HPV vaccine administration or refusal, as well as, missed opportunities where a provider failed to initiate the HPV vaccine series during the administration of Tdap and/or MenACWY when the initiation of the vaccine would have been appropriate (Williams et al, 2019). According to the CDC, the 2016 NIS-Teen revealed 7.5% to 15.6% lower rates of HPV vaccine coverage in MSA non-principal cities and rural areas as compared to principal cities (Williams et al, 2019). The disparity was not as significant for Tdap or MenACWY. Similarly, in 2017 HPV vaccine coverage in adolescents of greater than one dose of the series was 7.0 % to 10.8% lower in rural areas and MSA non-principal cities as compared to MSA principal cities (Williams et al, 2019).

Findings from the 2017 NIS-Teen study concluded that 88.7% of adolescents received at least one dose of the Tdap, 85.1% MenACWY, but only 65.5% received more than one dose of the HPV vaccine, and 48.6% completed the two-dose series (Williams et al, 2019). Overall, there was a 37% rate of missed opportunities for initiation of HPV vaccine among adolescents. Within this sample, those residing in suburban areas were more likely to miss opportunities (82.2%), compared to those in mostly urban areas (79.3%) and those in mostly rural locations (78.9%). If the HPV vaccine was initiated during primary care visits when other vaccines were given (e.g. Tdap and/or MenACWY) all areas would have increased to over a 90% HPV vaccine uptake rate (Williams et al, 2019).

School-based programmes

School-based policies have been found to be the most effective tool to improve vaccination rates in the United States with school entry requirements being the most effective. These requirements vary state by state and are commonly associated with MenACWY and Tdap requirements (Head et al, 2018). The HPV vaccine series is commonly initiated with these two vaccines but are not part of state mandates as school requirements. Administering the HPV vaccine with these two vaccines may lessen resistance if all three are given together. Requiring HPV vaccines as part of these school mandates have been an ongoing debate. Some states have attempted to initiate the requirement but have received backlash from the general public, public health officials, and parents (Head et al, 2018). To date, the only states and districts that have required HPV vaccine for school entry are Virginia, Rhode Island, and Washington DC. Rhode Island is the only state that has demonstrated significant improvement in vaccine rates and equal gender school entry requirements (Head et al, 2018).

Statistical data supporting the association of reinfection of HPV and its direct link to cervical cancer has brought the discussion of HPV vaccination to the forefront of health care (Dempsey and Schaffer, 2010). Several research studies have focused on improving recommended vaccine coverage in the adolescent population. Past studies have concluded that adolescents are educated about vaccines through parents, physicians, peers and the media (Dempsey and Schaffer, 2010). Research has focused on methods to educate adolescents about recommended vaccines and become more active in the decision to become vaccinated. Targeting middle and high school students (11–18-year-olds) is an alternative option to educating adolescents. Educating health-care professionals and teachers in middle school and high school about HPV and HPV vaccine scheduling and safety is an important avenue to improve vaccine uptake. However, there is currently no national mandated HPV education in health education classes and the material that is chosen is primarily decided by state and local school districts allowing for a wide array of material discussed and inconsistency among all schools (Dempsey and Schaffer, 2010).

These same authors analysed the HPV health education in middle and high schools across 6 states in 155 schools. They noted that approximately two out of three health education teachers discussed adolescent vaccines and 71.6% included HPV-related health information in the curriculum. Approximately 84.3% of high schools and co-ed classrooms included HPV education in the curriculum, compared to 54.5% of middle schools and non-co-ed settings (Dempsey and Schaffer, 2010). In addition, HPV was more likely to be discussed in schools that included STI education (77.1%) compared to those that did not (0%), as well as 83.3% of schools that educated about general adolescent vaccines versus 50% in those with no discussion (Dempsey and Schaffer, 2010). Genital warts were the least discussed HPV-related education among middle school and high school classrooms. This finding is concerning because the HPV vaccine was licensed for males to prevent the spread of HPV infection between sexual partners and specifically for preventing genital warts in men (Dempsey and Schaffer, 2010). Including the discussion in health education courses about the association between genital warts and HPV infection may increase HPV vaccine demand among adolescent males and reduce the complications of HPV infection (Dempsey and Schaffer, 2010).

Improving HPV epidemiology and HPV vaccine knowledge among key stakeholders will improve their clinical knowledge and confidence in vaccine administration or referral. Reiter et al (2011) cited that implementing educational programmes can be beneficial to vaccine education and possibly adherence. HPV educational programmes have been implemented in other countries with success but are very limited in the United States. The Guilford County HPV Campaign partnered with school systems and the health department to develop a school-based HPV vaccination educational programme to inform school staff members and parents. Guilford County, North Carolina had a cervical cancer mortality rate as high as 6.1 deaths per 100 000 women per year, which is among the highest in the state (Reiter et al, 2011). An HPV educational campaign was carried out in Guildford County local middle schools that targeted individuals who would have the most contact with adolescents, which included local school administrators, faculty, nurses, health educators and parents (Reiter et al, 2011). Following the study, 90% of school staff members agreed that HPV educational programmes were beneficial in middle schools, and 85% were supportive of the implementation of vaccine clinics in schools (Reiter et al, 2011).

HPV vaccine programmes have become more apparent in 80 countries or territories since May 2018. They consist of school-based, community-based or primary care-based programmes (Vorsters and Van Damme, 2018). The recent increase in vaccine programmes have resulted from concerns related to a decrease in HPV vaccine coverage. In response, the HPV Prevention and Control Board assembled local and international experts to discuss HPV vaccine success, experiences, and lessons learned from vaccine programme implementation over four organised meetings. The aim of these meetings was to improve HPV vaccine uptake and prevention in countries who were naïve to vaccine programmes or had been unsuccessful. Four scenarios were evident following implementation of the immunisation programmes (Vorsters and Van Damme, 2018):

• Successfully launched programme with high vaccine uptake
• Successfully launched programme with decrease in vaccine uptake
• Suboptimal launched programme and low vaccine uptake
• Vaccine programme launched without implementation.

The successfully launched programmes showing continuing success after implementation included Australia, the United Kingdom and Belgium (Vorsters and Van Damme, 2018). Successfully launched programmes with a decrease in vaccine adherence related to concerns of vaccine side effects were found in Japan, Ireland and Denmark (Vorsters and Van Damme, 2018). Programmes with minimal launch success and vaccine adherence that continued to demonstrate substandard results included the United States and France (Vorsters and Van Damme, 2018). Lastly, Romania was the only country, out of the 80 countries reviewed, that launched a nationwide vaccine programme, but never officially implemented it due to various multi-system-level barriers (Vorsters and Van Damme, 2018).

After reviewing the four scenarios, the experts of the HPV Prevention and Control Board developed a step-by-step approach to increase success in the unsuccessful countries. The first step is to inform health-care professionals involved in implementing the vaccine programmes about HPV, HPV-associated complications, HPV vaccination recommendations and prevention to improve adherence which could be delivered through training sessions for providers. The next step is to create an action plan that would include a budget to carry out the immunisation programmes, suggestions for improving communication about HPV and HPV immunisation through informative face-to-face or media sessions, a crisis control centre for safety concerns and questions to be directed to, social media use and management, and primary and secondary prevention programmes discussed concurrently (Vorsters and Van Damme, 2018). The last portion of the action plan discusses the importance of screening and prevention of HPV together because they both have the same goal of reducing HPV-related disease complications (Vorsters and Van Damme, 2018). The third step is to assess and reflect on the crisis and mitigation response of HPV from the beginning of the initiation of HPV immunisation programmes (Vorsters and Van Damme, 2018). This could be involving political leadership and public health officials from the beginning and overcoming anti-vaccine rhetoric on social media early to reduce confusion and hesitancy (Vorsters and Van Damme, 2018). The last step is to monitor and follow-up on immunisation programmes. If vaccine coverage is suboptimal in countries where vaccine services are readily available, it may be due to vaccine misinformation and hesitancy. It is recommended to follow up every 2 years with regular surveys to assess vaccine attitudes and make necessary alterations if needed to maintain support and vaccine adherence (Vorsters and Van Damme, 2018).

The oncogenic protection and immunogenicity of the HPV vaccine can assist in eradicating the complications and reducing the associative economic and health-care burden (Shapiro et al, 2017). Due to these protective methods, various countries have adopted and implemented an HPV immunisation programme to increase vaccine coverage. More specifically, Canada is a country that has demonstrated repeated success with the implementation of HPV immunisation programmes. The Canadian Immunization Committee set a target goal of 80% and 90% of school-aged girls to be vaccinated within 2 to 5 years of introduction of the immunisation programme (Shapiro et al, 2017). The Public Health Agency of Canada successfully implemented a publicly funded school-based HPV immunisation programme within all 13 of its jurisdictions (Shapiro et al, 2017). The vaccine is administered by a public health nurse who is responsible for record-keeping, administering the vaccine and following up with each student after the first dose to ensure the second dose is given 6 months after the initial dose. If the child is unable to obtain the second dose from the public health nurse, they are able to receive the dose from their primary care provider, pharmacist, or another public health nurse (Shapiro et al, 2017). By offering the publicly funded school-based programmes, there are fewer missed opportunities or catch-up and missed doses which optimising vaccine coverage. Due to the successful implementation of the school-based immunisation programmes, The Canadian Immunization Committee has recently stressed the need for a national vaccine registry, cervical cancer registry, and national HPV sentinel surveillance system (Shapiro et al, 2017). The registries and surveillance system will be used to monitor and evaluate the HPV immunisation programmes and the prevention of associative cancers and diseases. The development of a national registry can assist in accurately tracking HPV vaccine rates and eventually using it for international comparison to identify vaccine coverage differences and facilitate the sharing of reduction strategies to reduce the global HPV health concern (Shapiro et al, 2017). All 13 jurisdictions were shown to vaccinate girls and ranged from 46.7% to 93.9%, whereas only six vaccinated boys and ranged from 75% to 87.4% (Shapiro et al, 2017). The wide range was due to the inability to share vaccine data between Canadian jurisdictions. If values are correct then within the short duration of the study, the Public Health Agency of Canada met its target goal of vaccinating 80 to 90% of their adolescents in some areas (Shapiro et al, 2017).

Recommendations and limitations

Head et al (2018) offered suggestions to improve vaccine rates. The authors' recommendations included:

• Changing the vaccine policies to recommend fewer doses that, which may appeal to younger population
• Administering the vaccine routinely with MenACWY and Tdap
• Provider recommendations at or before the recommended ages to initiate early discussion
• Implementating an HPV vaccine benchmark for providers
• Early provider training in medical school through continuing medical education
• Setting reminders in the electronic medical health record of age-appropriate patients.

It is important to note that the literature also shows limitations related to initiating HPV immunisation in school-based settings. The United States has implemented school-based vaccine programmes with other vaccines with success. However, there are some concerns and limitations that need to be addressed for future interventions in schools. Reimbursement for administration of the vaccine is a concern because schools may not have the ability to bill the insurance for payment for services. State laws and school requirements may have additional barriers, such as requirements for consent of administration of the vaccine for underage students without parents' presence. This may be more complicated in rural or low economic areas where parents do not have access to transportation, are unable to pay for additional transportation to school or have to miss work. Vaccine storage, administration, and documentation must be considered as well when deciding to implement school-based programmes due to availability and cost (Head et al, 2018). Additional limitations to HPV vaccine promotion that were discussed were that it is a multi-dose vaccine, it is not required for school entry by the majority of US states, it has a broad age range for administration and it is marketed to prevent STIs (Head et al, 2018).

Data analysis

Themes

According to HPV vaccination research and analysis of the 10 publications included in this review, there were common factors that influenced the implementation of HPV education and vaccination management in school-based settings (Table 3). HPV-associated complications are a public health concern. Assessment, screening, and preventative interventions for adolescents are essential to reduce associative risks and improve vaccine adherence. Overall, six themes were consistently noted through the literature. Themes addressed included vaccine knowledge deficit, parental hesitancy, patient hesitancy, lack of provider recommendation, vaccine safety and side effect concerns, and association with an increase in sexual behaviour related to vaccine administration.

Vaccine knowledge deficit

Low vaccine rates are related to a lack of vaccine knowledge from the parent and provider; therefore, education should be directed to parents and providers (Esposito et al, 2014). Improving vaccine knowledge is the first step in accepting the vaccine. The most common barrier to HPV immunisation was found to be related to vaccine knowledge deficit and a common theme in eight articles. More parents reported they were unfamiliar with the benefits and risk reduction with their child receiving the HPV vaccine. After a discussion, parents were more likely to accept the vaccine after they learned of the benefits associated and received a strong provider recommendation (Thompson et al, 2017). Parents of adolescent males were more apprehensive before they were educated about the vaccine and were more likely to request the HPV vaccine after they learned of the risk reduction for both their child and future partners. Thompson et al (2017) attributes this increased concern of male parents to the delay in HPV vaccine approval and recommendations by clinicians. As a result, an increase in educational marketing and campaigns have been developed to target those lacking vaccine education and who are apprehensive. Incorporating these educational campaigns in the school system and distribution of educational pamphlets about HPV and the HPV vaccine before the beginning of the school year or along with school entry requirements may be an opportunity to increase awareness and vaccine acceptance.

Lack of provider recommendation

Provider recommendations have frequently been shown to be the most important and influential factor in reducing vaccine hesitancy and increasing HPV vaccine adherence (Head et al, 2018). Lack of a provider recommendation was the second most common barrier and found mentioned in five articles. There has been significant data indicating gender disparities in provider recommendations with providers recommending the HPV vaccine less often for males than females (Thompson et al, 2017). In addition, many providers do not address HPV vaccine recommendations in a timely and appropriate manner and can potentially miss various opportunities to inform both patient and parents about the benefits of the vaccine and risk reduction. Providers have missed opportunities due to timing, inconsistency and urgency with recommendations during the same office visit, or delaying discussion (Head et al, 2018). Interventions are necessary to avoid these missed opportunities. School-based programmes can be the alternative option to address these missed opportunities and provide catch-up vaccines. Implementing routine vaccine reminders in the electronic medical record or text messages for adolescents can remind providers or school-based staff members to discuss the HPV vaccine with patients and parents (Head et al, 2018).

Researchers and the media previously focused on addressing HPV vaccine awareness but, after increasing studies were published indicating a need for strong provider recommendations, it has become apparent that this needs to be addressed to improve vaccine uptake (Hirth et al, 2019). Providers have been targeted due to a strong association between higher vaccine rates and lower parental hesitancy with strong provider recommendations. Provider recommendations have improved with the use of American Academy of Pediatrics and American Academy of Family Physicians recommendations (Hirth et al, 2019). In addition, face-to-face interactions with the patient and patient education can significantly improve vaccine rates by involving the child in their medical decision-making. Reasons for choosing not to vaccinate have changed over time, therefore ongoing surveys and research areneeded to reassess parental and patient attitudes toward immunisation in order to improve HPV vaccination rates.

Vaccine safety and side effect

Despite the widespread dissemination of research study results, there are still concerns about the vaccine safety and side effects. This second most common barrier surrounding HPV vaccination was noted in five publications. Concern that the vaccine is new and thus unsafe has been heightened by anti-vaccine messages in the media and negative connotation (Head et al, 2018; Thompson et al, 2017). Parents were commonly found to have a strong social network of parents with similar beliefs. Primary care providers and school-based personal need to address anti-vaccine messages and vaccine concerns during well child visits. An open and non-judgemental discussion about the vaccine safety and possible side effects should occur. If the parent and patient are still hesitant providing them with reputable resources discussing vaccine safety and then referring them to follow up either with their primary care provider or other school-based professional is warranted.

Parental hesitancy

Parents are one of the most influential determinants of vaccine adherence in adolescents (Thompson et al, 2017). One of the most common reasons for vaccine hesitancy and adherence is related to parental attitudes and involvement in vaccine decision-making. Parental hesitancy toward the HPV vaccine was discussed in four articles. Parental attitudes and reasoning toward declining the HPV vaccine have changed over time and vary by gender. Increasing availability of vaccine and HPV education, early and routine screenings for HPV-associated cancers, and the American Academy of Pediatrics and American Academy of Family Physicians guidelines have overcome vaccine hesitancy among many parents. This is made evident by the reduction in the number of parents who refused vaccination. The number of parents who chose to decline HPV vaccination reduced from 72% to 58% from 2008 to 2016 (Hirth et al, 2019). Nearly 25% parents felt that the vaccine was unnecessary which was the most frequent reason for parental hesitancy (Hirth et al, 2019).

Association with an increase in sexual behaviour related to vaccine administration

A common parental concern is the fear that initiating the HPV vaccine at a young age will promote earlier sexual activity or give the child permission to engage in sexual activity. This concern was made evident in four articles. Parents commonly associate HPV with sexually transmitted infections, and therefore the HPV vaccine with preventing STIs and giving permission to engage in sexual activity (Head et al, 2018). Twenty publications have studied this association and found no risk following HPV vaccination (Head et al, 2018). Educating parents and students together about HPV, associative complications, HPV vaccine, sexual transmitted infections and how to prevent them can improve vaccine adherence. Education can take place face to face during well visits and the provider can offer educational handouts to discuss when they get home and follow-up with any questions or concerns.

Patient hesitancy

The least common barrier to receiving the HPV vaccine gleaned from the literature was patient hesitancy. The barrier was only reported in one article by Shapiro et al (2017), which discussed a publicly funded school-based HPV programme. Students in that programme reported vaccine hesitancy related to fear of needles or declining the vaccine for fear of being shamed at school for either not receiving the vaccine or reporting a fear of needles. The majority of data related to declining the HPV vaccine is related to parental opinions and knowledge deficits, or provider related. The authors concluded that the decision to vaccinate should involve the children and parents, and providers should encourage the child to become more involved in medical decision-making and made aware of the lifelong complications and diseases associated with HPV.

HPV vaccine coverage across all adolescents is suboptimal in the United States, with the lowest coverage rates among adolescent males, rural areas, and middle school-aged students. Educating parents and stakeholders of school-based vaccination programmes about the importance of HPV vaccination can play a crucial role in improving vaccine rates of these specific groups of adolescents. Success of school-based programmes has been evident in other countries and three in the United States. Rhode Island in particular has had success with the implementation of school-based programmes through mandated school requirements. Therefore, universal mandates for school-entry would be beneficial in the future establishment of other school-based programme in the United States to improve vaccination rates. Instituting a school-based HPV educational programme targeting 11–12-year-old males and females has shown success with increasing HPV vaccine uptake.

Conclusions

Incorporating school-based HPV vaccination programmes can be beneficial in improving overall vaccine education and adherence among the recommended age groups. Evaluating stakeholder attitudes, concerns, and knowledge about HPV; HPV sequelae; and HPV vaccination is an important first step in improving vaccine adherence. An integrative review was developed to explore the attitudes, concerns, and knowledge regarding HPV vaccination and explore benefits and barriers to HPV school-based vaccination programmes. The literature reviewed revealed five barriers to implementing school-based HPV vaccination programmes in the United States, these include vaccine knowledge deficit, parental hesitancy, patient hesitancy, lack of provider recommendation, vaccine safety and side effect concerns, and association with increasing sexual activity.

There has been a strong association between higher vaccine rates and lower parental hesitancy with strong provider recommendations. Therefore, improving provider communication with parents and patients about HPV; complications; and HPV vaccine risks, benefits and schedule will improve vaccine education and rates. Nurse practitioners in particular focus on health promotion, screenings and continuous patient education. Therefore, nurse practitioners have a pivotal role in getting involved in the community and serving as consultants or volunteers to the school-based clinics to raise the percentage of age-appropriate girls and boys getting the HPV vaccine series. It is imperative to improve the communication between nurse practitioners and school health systems will improve the efficiency and accuracy of vaccine data collection and ensure that there are no missed opportunities with HPV vaccination.

Overall, more research is necessary to ensure the best strategies to successfully implement school-based vaccination programmes in the United States. Moving forward, a multi-level approach through provider training, age-based recommendations and health promotion among stakeholders, improving public health and school policies, and increasing effective educational tools for the public are key in overcoming stigmas and barriers to improving vaccination education and uptake rates.