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A study protocol comprising educational interventions to improve HPV vaccination coverage among adolescents.A
NolwennLe Stang
PhD, RN
1,2✉Emailnolwenn.le.stang@univ-poitiers.frStéphanieMignot
MD, PhD, RN
1,2GautierDefossez
MD, PhD, RN
1,2PierreIngrand
MD, PhD, RN
1,2IsabelleIngrand
PhD, RN
1,2NolwennLeStang3
Poitou-CharentesGeneral3
1Poitou-Charentes General Cancer RegistryPoitiers University Hospital, Poitiers University, CIC-INSERM, axe SCALE-EPIPoitiersFrance
2University Center for Primary Care and Public HealthUnisantéLausanneSwitzerland
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Cancer RegistryPoitiers University Hospital, Poitiers University6 rue de la Milétrie86000PoitiersNolwenn Le Stanga, PhD, RN, Stéphanie Mignotb, MD, PhD, RN, Gautier Defosseza,, MD, PhD, RN, Pierre Ingranda, MD, PhD, RN, Isabelle Ingranda, PhD, RN
Authors’ Affiliations: Poitou-Charentes General Cancer Registry, Poitiers University Hospital, Poitiers University, CIC-INSERM, axe SCALE-EPI, Poitiers, France (Drs Le Stang, Defossez, Ingrand P and Ingrand I); Department of General Practice, Poitiers University, Clinical Research Center CIC1402, INSERM, Poitiers, France (Dr Mignot); Present address : Unisanté, University Center for Primary Care and Public Health, Lausanne, Switzerland (Dr Defossez).
Corresponding author : Nolwenn Le Stang, Poitou-Charentes General Cancer Registry, Poitiers University Hospital, Poitiers University,6 rue de la Milétrie, 86000 Poitiers, https://orcid.org/0000-0001-9522-6552 (nolwenn.le.stang@univ-poitiers.fr)
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Author Contribution
NLS – writing- review, editing; SM - writing – review, GD : writing – review, PI : conceptualization, project administration, II : writing – original draft, conceptualization, funding acquisition, supervision
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Abstract
Background
Human papillomavirus (HPV) is the main cause of sexually transmitted infections, especially cervical cancer, worldwide. Several of HPV-induced cancers affect boys also and (25% of cases). In France, HPV vaccination is recommended for boys and girls aged 11 to 14, with possible catch-up vaccination up to age 19. However, vaccination rates remain low, particularly among boys. Greater knowledge of both potential HPV-induced risks and vaccination benefits in population will help increase vaccination coverage.
Methods
This article presents a research protocol aimed at improving HPV vaccination coverage among adolescents aged 15 to 19 attending Rural Family Homes in three French departments, through an educational intervention combined with the distribution of comic book. Comparative analysis of three intervention groups, followed for 6 to 8 months, one of which included the distribution of a comic book, will be carried out using a mixed approach combining quantitative and qualitative methods.
Discussion
Multidisciplinary researchers and field workers have proposed an intervention programme. It was carry out by health professionals from Maternal and Infant Protection services, knowing this public very well moreover. For its part, comic book was designed on collaboration with adolescents. School interventions and educational media such as comic book help to raise knowledge of the importance of vaccination among adolescents and their parents, and should be more widely used.
Trial registration
This research programme received a favourable opinion from the French regulatory authorities on 13 June 2023 (national number 2023A0069639). Clinical trial number not applicable.
Key words
Human papilloma virus
vaccination
adolescent
educational intervention
comic book
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Introduction
Human papillomavirus is the main cause of sexually transmitted infections worldwide. In France, human papillomaviruses (HPV) are responsible for 6,300 cancers every year. While HPV infection is essential to the development of cervical cancers (99.7%), it is also responsible for the vast majority of anal canal cancers (90% HPV-induced), oropharyngeal cancers (35–63%) and penile cancers (60%). Although cervical cancer is the most common, the total number of other HPV-induced cancers is higher, and several of them affect boys, accounting for a quarter of all HPV-induced cancers: 1,750 new cases in men and 4,580 in women in France per year. HPV-induced cancers more frequent in men, particularly those of oropharynx, is constantly increasing, unlike those of cervix. Anal cancers are likewise rising sharply in both sexes [1–2].
According to a meta-analysis, high-income countries that have introduced HPV vaccination have demonstrated its population-level efficacy in preventing HPV infections and precancerous lesions [3]. Increasing vaccination coverage is therefore essential to reduce morbidity and mortality associated with HPV infections.
French National Authority for Health (HAS) recommends extending HPV vaccination to boys in French vaccination schedule, comprising:
- aged between 11 and 14, using a 2-dose schedule (M0, M6),
- catch-up vaccination for unvaccinated adolescents and young adults aged 15 to 19, using a 3-dose schedule (M0, M2, M6).
However, parental consent for vaccinations, including HPV, is compulsory for minors in France, as in other countries. National coverage is low compared with other vaccinations, and below the optimal threshold. In France, by the end of 2021, only 45.8% of 15-year-old girls and only 6% of boys of the same age had received at least one dose of vaccine [4–5].
Between 2014 and 2020, a number of literature reviews were identified to evaluate the effectiveness of interventions in improving vaccination uptake among adolescents. These studies showed that when adolescents and their parents received information and education about vaccination, more adolescents were vaccinated. Health education thereby improved HPV vaccination. Strategies that have been shown to be effective in improving HPV vaccination rates include: community awareness and information campaigns on HPV, training of healthcare providers, integration of HPV vaccination in a school setting, coordinated efforts through multi-sector partnerships, vaccination reminder and vaccine recall systems [6–11].
It is important to focus on adolescents aged 15 to 19, a minority of whom, particularly boys, will have been previously vaccinated. Interaction and discussion within families, as well as levels of argumentation, understanding and debate, may be more developed. In addition, these adolescents, who are closer to the beginning of their emotional and sexual lives [12], may be more concerned about vaccination benefits than the 11–14 year-old population.
A study carried out in France has highlighted the crucial role played by parents in the decision to vaccinate their adolescents [13]. Among parents informed about vaccine, those who belonged to occupational groups with lower education levels and whose child's school was located in more deprived areas were much less likely to report favourable attitudes and more likely undecided attitudes towards the safety, usefulness and accessibility of the HPV vaccine {14]. Involving adolescents in the decision making process could improve vaccine acceptance, even though parental consent is required for vaccination.
For example, RFHs [15], a network of 430 establishments in France, independent of French Ministry of National Education, aims to provide training and education for young people and adults, as well as their social and professional integration. These establishments seem to us to provide a favourable environment both in terms of reducing social inequalities and in terms of project feasibility and ‘success’.
The aim of this research is to test an intervention by healthcare professionals supplemented by the distribution of a comic book (CB) on HPV infections among adolescents aged 15 to 19 attending a Rural Family Home (RFH) and to determine whether this intervention method improves HPV vaccination coverage of adolescents. Secondary outcomes include the intention to be vaccinated against HPV, as well as obstacles and levers to this vaccination. Qualitative and quantitative evaluation of the effectiveness of the intervention will be supplemented by an evaluation of process indicators, in view of transferring the action to a wider population.
Methods
Population
All adolescents aged 15 to 19 enrolled in classes of Seconde (Year 11 in UK), Première (Year 12 in UK) and CAP (Certificate of professional aptitude in France, youth training National Vocational Qualification in UK) in one of participating RFHs are included in the study. Adolescents who have already been vaccinated against HPV infections are not excluded from the study or the intervention.
Design
Adopted methodology is based on several successive stages, knowledge synthesis, controlled experimentation, evaluation of the action, feedback, and finally process evaluation. This research is carried out in three phases (Fig. 1), with as comprehensive evaluation as possible, using qualitative (observation sessions and focus groups) and quantitative (questionnaires) methods with the target population: adolescents, their parents, Maternal and Infant Protection (MIP) doctors and midwives, and RFH managers and health referents.
Fig. 1
General outline of the Programme to improve the HPV vaccination rate. Diagram of the various stages and timetable for applying the designed protocol.
- The phase I: An initial questionnaire is collected before the intervention and a second between 15 days and one month afterwards.
- The phase II, six to eight months after intervention, uses a sequential explanatory mixed methods design, which begins with collection of quantitative data, followed by collection of qualitative data to explain and enrich the quantitative results [16]. Quantitative data are collected via a third questionnaire from adolescents who participated in first phase of the study and their parents, and analysed using quantitative approaches. Qualitative data are obtained through group discussions with adolescents and individual interviews with health advisors and RFH managers. This phase takes place before the end of school year.
- In the phase III, barriers and levers for all the players involved are identified, and the process evaluated. This will help to validate the general framework of an intervention aimed at improving uptake of the HPV vaccine among adolescents, so that it could be generalised to other regions or proposed to other adolescent populations.
Sampling
Adolescents are divided into three groups receiving one of three intervention modes:
- Group I: a presentation on health education and training in emotional and sexual life, as currently provided in schools by a health referent.
- Group II: an intervention by a health referent, followed by a standardised intervention carried out by a MIP health professional.
- Group III: an intervention by a health referent, followed by a standardised intervention carried out by a MIP health professional, and handing over of the CB.
A group in which only the CB would be distributed was not chosen, as it was shown that adolescents felt that although written information was useful, it should be more user-friendly and supplemented by discussions in small groups [17].
All classes in the same RFH were assigned to the same group. The RFHs were stratified according to department, main vocational orientation, distribution of adolescents by sex, and class size, in order to obtain a homogeneous distribution of clusters between three groups by randomisation within the strata.
Data collection
Before the intervention (T0) and then between 15 days and one month after intervention (T1), all adolescents (groups I, II and III) are asked to complete a questionnaire assessing their respective knowledge of HPV infections and vaccination. In addition, six to eight months after intervention, the same questionnaire (T2) is given in intervention and control classes.
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Their parents are asked to complete a questionnaire to assess intervention impact on adolescent, his or her family and their opinion of the intervention. (Supplementary data) This questionnaire is based on validated models in this field: the Health Belief (HBM) which consists of 6 cognitive constructs perceived susceptibility, perceived severity, perceived benefits, perceived barriers and cues to action, incentives to action, attitude, subjective norms and the Theory of Planned Behaviour (TPB) which assumes that individuals act rationally, according to their attitudes, subjective norms, and perceived behavioral control [18–20].Focus groups with adolescents set up after final questionnaire has been collected will enable to gain better understanding of correlations identified by quantitative approach, to identify precisely levers that lead adolescents to get vaccinated. Focus-group method encourages interactive discussions between participants [21], and seemed appropriate to help overcome adolescents’ apprehensions, especially as groups are already established, and used to discussing a variety of subjects.
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Focus groups (duration 60 minutes) are conducted by a moderator with help of an observer, using semi-structured interview guides drawn up on the basis of quantitative study results and data from literature. They cover topics such as vaccination knowledge, information and communication methods, gather expectations and needs of information. Groups of adolescents are mixed. Discussions are audio recorded with participants’ agreement. Total number of discussion groups will be determined by saturation principle. Individual interviews are conducted with MIP professionals, health referents and RFH managers to assess how the programme was implemented and understood within establishments. Finally, around twenty interviews will be conducted with all the key partners in the project in order to evaluate the research implementation process.Results
The comic book
Documentary medium was designed to be an attractive, easy-to-read CB. A young author and illustrator with experience in popularising and promoting science was asked to take part in the project. Three preliminary manga-like illustrations were produced. They were used to check understanding level between illustrator, involved researchers and clinicians. A number of adolescents were able to see drawings and express their comfort with the medium and its content. They were then presented to a small group of adolescents to check that they corresponded with their language level, knowledge and acceptance.
The tool (Fig. 2) was then designed on basis of three focus groups with the CB author, adolescents and a clinician. Involvement of adolescents in CB development greatly contributed to its quality. It has been shown that to create an educational tool, it is first necessary to understand ideas and questions of target audience. When it comes to creating a CB, it's not up to health professionals, educators or adults to make choices; only adolescents’ demands should be taken into account. Focus groups constituted a panel of around ten adolescents, boys and girls from Nouvelle-Aquitaine region, aged 15 to 19, having previously received sound information on HPV infections and vaccination.
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These adolescents and their parents have been informed of the study’s objective and were not opposed to taking part. Clinicians involved in the project also took part in focus groups to provide answers to any scientific questions that might be asked, and because they know this public very well. Researchers spoke to the designer to explain expectations and needs expressed by adolescents during focus groups. Needs expressed by adolescents and the means of helping them to adhere to vaccination programme were taken into account. Focus groups were recorded and transcribed anonymously for use by comic book artist and project team.Content of comic book reflects themes that emerged during focus groups. Advice on how to broach the subject with parents was included in the script.
Fig. 2
Comic book cover. Front cover of the comic book showing the title and author's name.
MIP professionals’ interventions
MIP [22] services are an original feature of French health system, combining medico-psycho-social prevention activities with public health activities aimed at families, children and young people. Their activities are part of a global approach to health problems. Clinicians and midwives from MIP services seemed to be particularly qualified to carry out this preventive action, because they already carry out actions in RFHs and they know this public very well.
MIP professionals' intervention is designed on the basis of data in literature [17–18, 23–24], previously published guidelines or recommendations and their own experience as experts in the field. It is based on validated models: HBM and TPB. widely used in research on behaviours associated with disease prevention, including vaccinations [25].
In addition, internal or external factors are required to trigger this action.
Since knowledge is an important prerequisite for behavioural change, these HPV-focused interventions cover causes of different types of cancer induced, transmission and the most effective methods for preventing infection, as well as the most appropriate time or age for vaccination, known side-effects and beneficial effects observed in countries that vaccinate entire younger generation.
Interventions leave plenty of room for discussion led by midwives and clinicians involved, in view of optimally meeting target population needs. A gender-sensitive approach is used both to increase uptake rates among boys and to ‘normalise’ recommendations for a vaccine that is still strongly associated in public mind with female sexual behavior [26].
Indeed, a meta-analysis showed that gender was the strongest and most consistent predictor of having heard about HPV, that girls were more likely to have heard about vaccination and, interestingly, that many boys did not feel concerned. The challenge is consequently to develop an intervention equally relevant to both sexes, thereby promoting equal participation of men vaccination project.
Discussion
This paper describes the development of an original educational programme, involving a clinician or midwife’s intervention, using a new tool - a comic book [27] - to improve knowledge and involvement of adolescents of both sexes aged 15 to 19 in decision-making process concerning vaccination against HPV infections, and to improve their parents' reluctance to have them vaccinated through exchanges based on this intervention and comic book.
The development process was designed as interventional health research, a knowledge-generating process consisting first the design and testing of solutions, and then their application [28]. The study is therefore based on several successive stages: knowledge synthesis, controlled experimentation, action evaluation, feedback and finally, process evaluation. Developed methodology was designed with stakeholders’ involvement: adolescents for the comic book design, and healthcare professionals for the intervention content design.
School-based education programmes have been shown to be effective in producing significant positive changes in HPV knowledge, but generally concern adolescents aged 9 to 13 [11], or focus more on parents‘ or healthcare professionals’ perceptions [29–30]. The study protocols currently being evaluated concern adolescents aged 11 to 14 [31–33], but it is necessary to target adolescents aged 15 to 19, a minority of whom, particularly boys, will have been vaccinated previously, and for whom catch-up vaccination using a 3-dose schedule is recommended.
Solving problems associated with HPV vaccines acceptance requires the use of good communication strategies [34]. Multi-component interventions, with dialogue-based language tailored to specific audience seem to be the most effective. Adolescents need to understand value of vaccination through simple examples employing a graphic approach. Starting from observation that 47% of 15–19 year-old are comic readers, creation of this CB therefore stemmed from a desire to offer adolescents a tool that lives subsequent to the intervention, allowing them to communicate with peers and families. It has been shown that as part of a prevention activity, particularly in schools, comics can be an excellent way of starting discussions. In addition, this tool could meet the challenge of maintaining knowledge over time, getting adolescents and their parents to discuss vaccination and make decisions [35].
Adolescents were deeply involved in CB design, through exchanges with the author-illustrator, which contributed substantially to its quality. What is more, in producing educational CB, the author targeted his audience (although he did not rule out distributing the tool to other audiences), and his scientific and educational choices in producing the storyboard were careful to convey scientific information sparingly so as to avoid being indigestible. Storyboard was reviewed by specialists to check, before the work was too far advanced, that it was in line with the objective and to avoid certain errors. After any corrections to initial version, a new scientific evaluation by specialists, taking into account adolescents' feelings about the medium and its contents, resulted in final version. One of limitations of comic book development process is that discussions took place during the COVID-19 pandemic, which limited the number of adolescents involved in its design.
Information provided in schools by a healthcare professional of MIP, who is therefore a reliable and competent source of information, should prove more effective than an intervention by another professional, as is currently the case in these establishments. Health professionals' communication strategies are known to be associated with uptake of HPV vaccination by adolescents [36–37]. Proposed intervention could help develop an educational culture based on collaboration between healthcare professionals and the school environment. Indeed, it is at school that each individual can be educated to adopt health-promoting behaviours.
CB contents and intervention by MIP professionals covered not only cervical cancer in women [11], but also oropharyngeal cancer, the most common HPV-associated cancer in men, and all HPV-induced infections. This tool, the CB, which is to be applied subsequent to the intervention, is not only a reminder of the information given during the intervention, but also a tool for communicating with peers and parents. This medium is important because interventions that act on knowledge alone show variable effectiveness, which does not seem to last subsequent to the intervention [6].
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Parents, without whose consent adolescents cannot be vaccinated, were involved in evaluating the intervention. An English study showed that parents who would be willing to vaccinate their children had a higher level of knowledge about HPV than parents who would be unprepared or unsure [38]. In addition, mothers generally have a major role in health information for young people [19, 39].Studies have shown that when adolescents and parents have received information about vaccination, more adolescents intend to be vaccinated against HPV [24]. The vaccination programme presented, which can potentially be generalised, consists of a solid information campaign by a MIP professional who disseminates precise information about HPV infections and vaccination, and distributes of a comic book, a tool designed to facilitate communication between adolescents, parents and peers.
Conclusion
We proposed presentation by a MIP health professional, supported by an easy-to-read comic book suitable for adolescents. This tool was designed to help maintain knowledge of HPV infections and vaccination subsequent to the intervention. It was also designed to be a driving force in the decision to vaccinate, which, based on literature, does not seem to las, and as a means of sharing knowledge and facilitating exchanges within the peer group and the family.
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Acknowledgement
The authors would like to thank :Aurélien Fernandez, who wrote and illustrated the comic book.Sarah Dujoncquoy, who conducted the group interviews with the adolescents to create the comic book.The group of adolescents interviewed to create the comic book.Rémi Douat and the directors and health advisers of the RFH in Poitou and Gironde who took part in the research.MIP clinicians and midwives, and the clinicians who gave talks at the RFH.Professor Frédéric Chauvaud and the regional comic research network.Jeffrey Arsham for linguistic revision of the manuscript.
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Funding
This research was funded by the French National Cancer League.
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Data Availability
Data sharing not applicable to this article as no datasets were generated or analysed during the current study.
Declarations
Competing interests :
None of the authors has any financial or personal interest with persons and/or organisations likely to influence their professional judgement.
Ethics and Guidelines : This research programme was received an ethical approval from the French regulatory authorities, the Comité de Protection des Personnes Ouest VI on 13 June 2023 (national number 2023-A00696-39) and was in accordance with the Declaration of Helsinki guidelines. Clinical trial number: not applicable.
Consent to participate:
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Adolescents, parents and teachers received an information letter detailing the aims and progress of the study, as well as an informed consent form. A
The study began in the three class groups after verbal informed consent had been obtained from each adolescent, and their parents had not objected.Consent to publication :
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All authors consent to publication.Consent to Publish
Not Applicable
Electronic Supplementary Material
Below is the link to the electronic supplementary material
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