HPV vaccine introduction is different to infant vaccination programs as it is targeted at a new user group (9–14-year-old) for which no existing platforms exist. Furthermore, sensitivities around sexual activity have been shown to raise concerns by parents of adolescent girls targeted for the vaccine [23]. The WHO recommends that HPV delivery strategies are targeted to country specific health system and sociocultural contexts [2]. Understanding the factors that influence HPV vaccine uptake such as cultural acceptance and delivery feasibility is crucial for decision-makers. This study provides perspectives on knowledge, attitudes and perceptions of the HPV vaccine from a pilot program among school aged girls within a rural community in Northern Nigeria where research is lacking.
HPV vaccination knowledge and attitudes
Knowledge about HPV and cervical cancer is fair in adolescent girls in Yauri GSSC. However, as expected, girls in at higher secondary school level had higher knowledge scores compared to those in the lower secondary level classes. A study in India showed that older college students were more aware about HPV and cervical cancer than their younger and male counterparts [24]. This points to the importance of education in awareness about cervical cancer and its prevention by the HPV vaccine.
Community sensitization
Effective community sensitization prior to vaccine introduction is vital to community acceptability [25,26,27]. Advocacy plays a major role in shifting stakeholders’ views towards the HPV vaccine [28, 29]. In Yauri, advocacy efforts improved community acceptance of the vaccine. Initial reports of vaccine introduction triggered negative messages in the community; members of the community feared the vaccine was for birth control and withheld support. However, following sensitization and awareness with teachers and health workers, more individuals were receptive to the vaccine. As in other studies, convincing parents on the severity of cervical cancer and the preventative benefits of the vaccine is necessary to obtain their support and consent for vaccination [27].
Partnership with key influencers and stakeholders
A key component of HPV vaccine delivery is multi-stakeholder collaboration. Several studies show that coordination and collaboration between ministries of health, development partners, the education sector, community-based and professional groups is a key driver of vaccine uptake [8, 9, 30]. Our study largely supports these findings, coordination between teachers, health care workers, and community leaders was crucial to the success of the pilot program in Yauri. Students and community members attributed successful messaging to health workers embedded in the community who deconstructed key health information and clarified questions on the vaccines, and teachers who effectively followed up with students and parents.
Our findings also highlight the importance of selecting appropriate mechanisms and actors for dissemination of key messages. In our study setting, teachers played a key role in obtaining parental consent for the pilot program. A study by Masika et al., suggests that empowering teachers as vaccine champions may be a feasible way to increase awareness and disseminate key messages on the HPV vaccine and cervical cancer [31].
In Yauri, parent groups and community leaders were also identified as key influencers of HPV vaccination. The study had to be defended to the Parents Teachers Association of GSSC Yauri who served as gatekeepers to the school. Additionally, the most important gatekeeper for the entire project was the Emir of Yauri, an eminent traditional and religious leader who provided community approval for the pilot project. As the most respected leader in the community, in the absence of his approval and support, the pilot project would have likely failed. These findings highlight the importance of ensuring that all relevant stakeholders are mapped, consulted, and carried along from inception to conclusion including HPV vaccination strategy design, implementation and evaluation.
Barriers to implementation
Costs
Without Universal Health Coverage, vaccine availability remains a major barrier to access [14, 17]. None of the study participants could afford the discounted vaccine costs which was considered unaffordable by all the parents of the study participants. The prohibitive cost of the vaccine has been shown to negatively impact attitude toward the vaccine and therefore constitutes a main barrier to vaccine uptake in LMICs [32,33,34,35]. In Nigeria, the price of a complete dose of the HPV vaccine ranges from US$30 - US$50 and studies suggest that even at the lowest obtainable public sector price of approximately US$36, study participants consider the vaccines unaffordable [32, 33]. Currently, HPV vaccines are not included as part of the free vaccines offered under the National Immunization Programme (NIP) in Nigeria and are paid for out-of-pocket by the recipient [20, 34, 36]. Considering up to 45% of Nigerians live on less than US$ 2 a day, costs will remain a main barrier to vaccine uptake, specifically in poorer communities. As such, governments must prioritize funding mechanisms to ensure access to vaccines particularly in low resource communities.
Additionally, the HPV vaccine is relatively expensive to procure, and operational costs of vaccine delivery can be substantial. Many countries have found that the cost of implementing an HPV vaccination program is significant [2, 36]. While the vaccine was provided for free, operational costs including engagement of healthcare workers for administration and safe transportation logistics (for health workers and cold chain) significantly increased the vaccination program costs and was one reason for limiting the study to 100 participants.
Health workforce
With less than 20 health care workers per 100,000 population, Nigeria faces a shortage in availability of qualified health personnel for vaccine delivery; nurses and CHEWs are already overstretched at their health facilities or not available at all in many communities [37, 38]. Health care worker supervision, allowances and transportation costs have frequently been reported as been drivers of high vaccine delivery costs [6]. Such costs need to be considered particularly in rural communities where vaccination campaigns may require health workers from outside the target community, increasing vaccine delivery costs.
Infrastructure
The logistics of vaccine delivery from state and LGA cold stores to the school posed a considerable challenge. The established vaccine supply chain in Nigeria currently ends at Primary Health Centers (PHCs), therefore reaching rural, hard to reach areas is hindered by lack of infrastructure which further increases costs on an already underfunded system [39, 40]. For this study, vaccines were stored in a nearby town with cold storage facilities and provisions were made for power using generators further increasing program costs. With ambient temperatures greater than 37 °C, maintaining cold chain was critical. The team had to mitigate for lack of constant electricity supply in Yauri by relying on low technology, portable cold chain containers. Studies in low resource settings show there is a large risk of exposing vaccines to temperatures above the limit of 2o to 8 °C and programs must account for effective cold chain in their planning [41]. Overall, the study points to the careful planning required for vaccine delivery in rural hard-to-reach communities to ensure effective supply chain to the target user.
COVID-19
The biggest unforeseen challenge was the COVID-19 pandemic and subsequent school closures which impacted the study. Consequently, the cohort could not be reached in school as intended after the first dose, highlighting the importance of risk assessment and a limitation of the school-based vaccine delivery approach. While this approach is effective and convenient at reaching a large number of the target audience at a central location, it needs to be complemented with a method designed to reach those who are out of school [2, 42, 43]. Leveraging the strong buy-in from the Emir and program support by the community, the project team returned in November 2020 to vaccinate girls that had not completed their dosage within the recommended 6 months schedule. On the follow up vaccination, the 5 girls aged 15 and above were not present and lost to follow up. In Nigeria, 10.5 million children aged 5–14 are not in school [13]. The numbers are even more grim in the Northern states like Kebbi state where almost 50% of girls are not enrolled in primary school [12]. A national school-based HPV vaccination strategy must include an approach that targets out of school children as well as strategies to maximize follow up such as verification of two points of contact for every schoolgirl to minimize drop-out rates and maximize vaccine coverage.
Study limitations
The study adopted the purposive sampling technique (a non-probability sampling technique) to select GSSC Yauri. Therefore, the findings of this study may not be generalizable to other study settings. Our methods of obtaining parental consent may have introduced selection bias into the study; obtaining parental consent over the phone may have introduced systematic bias by excluding students whose parents did not have phone access. Additionally, we were not able to collect data from students whose parents refused consent. It can be argued that those with parental refusal differ in their knowledge and attitudes towards the vaccine compared to our study participants. Notwithstanding, we believe the results of this study are aligned with findings in similar studies conducted in low resource settings. Therefore, these findings can be useful to other researchers and decision makers working on HPV vaccination delivery.
