Background: Persistent suboptimal vaccination coverage rates

Suboptimal vaccine uptake is a worldwide public health issue, in low-, middle- and high-income countries, leading to the occurrence of epidemics (measles), delayed pandemic response (COVID-19) and a high burden of avoidable diseases (e.g., cervical cancers, meningitis, pneumonia)1,2. Vaccine hesitancy has long been cited as an important causal factor, particularly in high-income countries, and was listed in 2019 by the World Health Organization (WHO) as one of the top ten global health threats3. However, the reasons for suboptimal uptake are multifactorial, complex and programmatic, and logistic; even political mechanisms are involved4. A large body of literature shows an association between the low uptake of vaccines and individual socioeconomic deprivation and/or territorial isolation, leading to substantial health inequities and raising the issue of vaccine access5,6.

By 2016, the French population had acquired an international reputation of being particularly vaccine hesitant, with 41% having negative opinions about vaccine safety7, contributing to low coverage rates against vaccine-preventable diseases such as measles8 (80% among children at age two) and influenza9 (50% among individuals aged ≥65 years). However, hesitancy is not observed for all vaccines at the same level, but is directed especially to some ‘controversial’ vaccines. The most emblematic example is that of human papillomavirus (HPV) vaccination, which has been recommended in France since 2007, but is not among the 11 infant vaccines made mandatory for school entry in 2018 (diphtheria, tetanus, poliovirus infection, pertussis, H. influenzae type b infection, hepatitis B, measles, mumps and rubella, pneumococcal disease, and meningococcal group C disease). Indeed, complete vaccine coverage among 16-year-old girls in France was systematically <25.0% between 2011 and 2018, a rate lower than that reported in most other high-income and European countries10. In 2023, the coverage rate reached 44.7%11, which remains far from the goal of 90% defined by the 2030 WHO’s strategy12, despite various strategies implemented during the last decade by French public health authorities (Table 1). These strategies aimed to overcome low coverage rates of vaccines in general (including HPV) and the HPV vaccine specifically, considering existing social and/or territorial inequalities, with the aim of reducing them. But their lack of success in significantly increasing the French rates of HPV vaccination is due, at least in part, to the implementation of programs that lack appropriate evidence of effectiveness.

Table 1 Main strategies to overcome low coverage rates of HPV vaccines implemented in France over the past 10 years

In this paper, we first examine the data behind the policy strategies applied in France during the last decade (Table 1) to highlight their low level of evidence and to justify the need for well-conducted interventional population health research, using the example of the PrevHPV project. Second, we emphasize that such research should help public health authorities decide not only what policy to implement but also how to implement it to maximize its public health impact.

The need to promote interventional research on vaccine uptake

The abovementioned implemented policy strategies have been identified and motivated on the basis of various data, such as experiences in other countries or results from local ‘policy experiments’.

First, the scientific literature has identified a list of various barriers and/or reasons why people in high-income countries such as France do not receive vaccination10,13. Among these reasons, we note the following here: (i) the profusion of vaccine information disseminated ranging from alternative health information or beliefs to genuinely fake information, which is amplified by the increased use of the internet and social media, and the fact that a person is more likely to believe this information if his or her knowledge and awareness of vaccine benefits are low; (ii) the weak commitment of doctors to promote vaccination and their difficulties in convincing some patients to receive vaccination; and (iii) the complex access to vaccination for organizational and/or financial reasons. Most strategies that have been implemented in France over the last decade are expected to address these identified barriers. However, their effectiveness in increasing vaccination coverage and reducing inequities has never been evaluated in well-conducted studies before their national implementation.

Second, information about vaccination strategies and policies implemented in other countries and their level of vaccine coverage may be valuable; thus, benchmarking is often used to determine a plan of action in terms of the national public health policy. For example, some European countries have long integrated HPV vaccination within school settings (e.g., Scandinavia, the United Kingdom, Spain, and Belgium Flanders)10, and these countries have high HPV vaccine coverage rates. This element contributed to the political decision to implement national HPV vaccination campaigns in French middle schools for seventh graders from the 2023–2024 school year onward. However, such observational data do not necessarily indicate a causal relationship between strategy and vaccine coverage, and ‘what works abroad’ may not work in another context due to cultural features.

Third, some strategies have been implemented following the conclusive results of ‘policy experiments’. An experiment involving the administration of HPV vaccination in schools launched in Northeast France in 201914 likely contributed to the political decision to establish HPV vaccination campaigns in middle schools. However, experiments are launched to assess the feasibility of implementing a strategy in real-life settings, and data on vaccine coverage rates are collected before and after implementation to gain insight into the potential effects. Thus, their design prevents us from identifying a causal relationship between the intervention and the coverage rates observed.

Ideally, public health strategies should be formulated—at least in part—according to the results of well-conducted interventional population health studies that use designs that provide high levels of evidence and that are performed in the context where the strategies are meant to be implemented in the case of positive results. In addition, these studies should evaluate not only the effectiveness of strategies but also their implementation and scalability. This information is critical for policy decisions and for subsequently implementing strategies in real-life settings. However, such population health research has only recently been developed in France and remains scarce both in general and in the field of vaccination in particular15,16,17,18. For example, as part of the 2014-2019 cancer plan, the French health research authorities launched a research project in 2019 on the acceptability of HPV vaccination for adolescents, which was called the PrevHPV project19. Briefly, this project included the following three phases: (i) First, the ‘diagnostic’ phase aimed at exploring knowledge, beliefs, behaviors, practices, barriers, motivations and preferences concerning HPV vaccination among four population groups (adolescents, parents, school staff, and general practitioners). (ii) Second, the ‘coconstruction’ phase aimed to design a three-component intervention believed to improve HPV vaccine coverage while reducing social and territorial inequalities. The intervention included adolescents’ and parents’ education and motivation at school, general practitioners’ training, and access to free-of-charge vaccination at school. (iii) Third, the ‘experimental’ phase aimed at evaluating the effectiveness, efficiency and implementation of the intervention in France via a pragmatic cluster randomized controlled study design20.

The need to strengthen collaboration between researchers and public health authorities and actors

Preliminary conclusive results of the experimental phase of PrevHPV18,21, together with results from the policy experiment in northeastern France and data on school-based vaccination campaigns abroad, led to the announcement of national HPV vaccination campaigns in middle schools by the French president in February 2023. However, the short time between this announcement and the start of the national campaigns (six months) prevented national and regional public health authorities from identifying the ‘best way’ to implement this strategy. Indeed, such a strategy is complex22, as it involves different stakeholders (adolescents, parents, school staff, and health professionals from vaccination centers) who take part in different stages of the process leading to vaccine uptake (e.g., integration of vaccination days into school life, information, management of parental consent forms, vaccination center mobilization, vaccine administration and adolescent monitoring, collection of individual vaccine records and traceability). Coordinated efforts via multisectoral partnerships are needed, as the optimal way to implement the strategy is highly dependent on each local context.

Many lessons have been learned from the PrevHPV study concerning implementation issues (fidelity, dose, reach, acceptability and sustainability) and facilitators of and barriers to school-based vaccination. All this valuable information, as well as various materials and tools codeveloped with stakeholders to facilitate implementation in real-life contexts, could have been useful for organizing the national HPV vaccination campaigns. The development and optimization of a process that aims to implement a national public health intervention requires time to allow the sharing of experiences between different parties (public health professionals, researchers, school staff, and vaccination centers). From the point of view of the French government and national public health authorities, acting quickly is essential because they must address health issues (i.e., there are 6300 new cases of HPV-related-cancers and 100,000 new cases of genital condyloma per year in France); however, rushing to establish new strategies is probably not the best way to reach the goal of 90% defined by the WHO’s 2030 strategy12. Ultimately, the results of the national HPV vaccination campaigns at schools led to a vaccine coverage increase of only 17% among girls and 15% among boys between the start and the end of the first campaigns. These results are slightly disappointing and may be improved through the use of research experience and tools. However, this approach would require (i) researchers to take the time to better communicate with public health authorities on research results and, more generally, to promote knowledge transfer to society, and (ii) public health authorities to take the time to obtain appropriate research results, review them and use them to make decisions.

Conclusion

Identifying and developing new interventions to improve national vaccination coverage while reducing social and/or territorial inequalities are crucial and require the promotion and development of interventional population health research. The strategy to integrate effective interventions into public health policies should consider the results and experiences of such research. Challenges related to the implementation of vaccination programs should not be underestimated, and findings from implementation science may be of great interest21,22. Thus, partnerships between public health and human sciences researchers and public health authorities/actors must be strengthened to encourage them to share their respective experiences. In the short term, this collaboration may be considered a constraint that slows political decisions concerning a public health problem; however, in the long term, it is probably one of the best ways to reach vaccine coverage goals, regardless of people’s social background.