Attitudes and Practices towards HPV Vaccination and Its Social Processes in Europe: An Equity-Focused Scoping Review

: The sociological understanding of the human papillomavirus (HPV) vaccination offers the possibility to understand society better as the processes that shape health beliefs and inﬂuence HPV vaccine decisions relate to gender, power, and identity. This research aimed to locate, select, and critically assess scientiﬁc evidence regarding the attitudes and practices towards HPV vaccination and its social processes with a focus on health equity. A scoping review following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses extension for scoping reviews (PRISMA-ScR) and the recommendations made by the Joanna Briggs Institute was undertaken. Medline and Scopus were searched from their start date until December 2021. The review followed the Population/Concept/Context (PCC) inclusion criteria: Population = General population, adults and adolescents, Concept = Empirical data on determinants of HPV vaccination, Context = Studies on attitudes and practices towards HPV vaccination and its social processes with a focus on gender, class, and ethnic/racial inequalities. Of the 235 selected articles, 28 were from European countries and were the focus of this review, with special attention to socio-economic determinants in HPV vaccine hesitancy in Europe, a region increasingly affected by vaccination public distrust and criticism. Barriers and facilitators of HPV vaccine uptake and determinants of immunization were identiﬁed. Given the emphasis on health equity, these data are relevant to strengthening vaccination programs to promote vaccination for all people.


Introduction
The sociological understanding of the human papillomavirus (HPV) vaccination, which varies between and within countries [1], offers the possibility to better understand society as vaccination processes, and in particular, vaccination against HPV-a widespread and sexually transmitted viral infection responsible for approximately 70% of cervical cancer cases in the world [2]-are constructed within social, cultural, and institutional contexts that produce normative notions on rights and responsibilities of health citizenship. The distinctive fact about the HPV vaccine's target being sexually transmitted links it to longstanding controversies around sex, gender, and young women's bodies and sexual behaviors [3,4]. Cervical cancer can serve as an example of the systematic disadvantages that women experience due to social and sexual inequalities and enables us to understand how gender intersects other social hierarchies such as class and ethnicity/race to (re)produce social inequalities in health [5,6]. Although both men and women are at risk of developing HPV-related cancers, social campaigns regarding vaccination against HPV are aimed mainly at the prevention of cervical cancer for women [7]. The promotion of HPV vaccination is surrounded by feminization and moralization processes, influencing the understanding of HPV vaccination and the accessibility of vaccination as preventive health

Search Strategy
A systematic literature search was performed using Medline (via PubMed), and Scopus electronic databases, with combinations of the search terms, tailored to the syntax and functionality of each database. Searches were conducted on 14 December 2021 with no date range limitation. The following search query was used: "HPV vaccination" OR "Papillomavirus Vaccines"[Mesh] OR HPV OR "human papillomavirus" AND (("Vaccination Hesitancy"[Mesh]) OR "Vaccination Refusal" [Mesh] OR "Attitude to Health" [Mesh] OR "Patient Acceptance of Health Care" [Mesh] OR "Health Knowledge, Attitudes, Practice"[Mesh]) AND ("Health Equity" [Mesh] OR "Social Justice" [Mesh] OR "Intersectional Framework"[Mesh] OR Intersectional* OR "health disparities" OR "Gender Equity" [Mesh] OR "Ethnicity" [Mesh] OR "Racial Groups"[Mesh])). Only English-written documents were considered eligible for inclusion.

Inclusion and Exclusion Criteria
The Population (or participants)/Concept/Context (PCC) method recommended by JBI to identify the main concepts in the primary review questions was used for the search strategy and the definition of inclusion criteria [25]: P (Population = General population, adults and adolescents), C (Concept = Empirical data on determinants of HPV vaccination), C (Context = Studies that report on attitudes and practices towards HPV vaccination and its social processes with a focus on gender, class, and ethnic/racial inequalities). All publications based on empirical studies (regardless of research design) were included. The exception was intervention studies, which were excluded, because of their distinguished features compared to observational studies. Book chapters, book reviews, vignette studies, study protocols, commentaries, guidelines, and editorials were also excluded.
Each relevant record was reviewed independently by the two authors, who screened titles and abstracts, and, when needed, full texts. A final decision was obtained for each record and uncertainties were resolved by discussion between the two authors.

Data Extraction and Synthesis
For all the included articles, the following data were extracted: (1) author(s) and year of publication, (2) country and setting, (3) population (sample size, gender, age, nationality/ethnicity, and diversity), (4) rationale and aim, (5) design and methods, (6) HPV outcome(s), (7) overall results, (8) overall limitations, (9) and overall recommendations. Information regarding the journal's title, publication quartile, and domain of work (i.e., the domain with the highest quartile in the year of the study publication according to the Scimago Journal & Country Rank) was also collected.
Methodological quality or risk of bias of the included articles was not appraised because it was not relevant nor necessary to the scoping review objectives [25].
Results were synthesized using a thematic approach on the relevant themes related to the barriers and facilitators of HPV vaccine uptake, and its social processes, with a focus on gender, class, and ethnic/racial inequalities.

Results
A total of 533 articles were identified, 291 in PubMed and 241 in Scopus. After duplicate removal (n = 75), 458 articles remained for screening. Of these, 224 were excluded because they were not empirical studies (i.e., literature reviews, study protocols, or commentaries/letters) or were intervention studies or did not focus on HPV vaccination attitudes or practices, or the study population was only health professionals. As a result, 234 publications could be included, with publication dates ranging from 2007 to 2021. Most of the studies (n = 175; 75%) were conducted in the United States of America (USA), and only 28 articles (12%) were conducted in European countries and were selected to be included in this review for mapping the state of the art and to reveal the specific trends in the field in Europe. A flow diagram providing the number of articles included and excluded at each stage is provided in Figure 1.
Most of the studies (n = 175; 75%) were conducted in the United States of America (USA), and only 28 articles (12%) were conducted in European countries and were selected to be included in this review for mapping the state of the art and to reveal the specific trends in the field in Europe. A flow diagram providing the number of articles included and excluded at each stage is provided in Figure 1.

Who Is Being Studied and How?
The first publications (n = 2) were issued in 2008 (Table 1). The number of articles published each year ranged from zero articles in 2010, 2011, and 2013 to four articles in 2009, 2015, 2017, and 2018. All publications were in journals with an impact factor, and the majority ranked in the first quartile (21/28). Four articles were published in journals in the second quartile, and three articles in the third quartile. All articles were published in the medical and health sciences subject area, and one was also classified in social sciences (the journal of Medical Anthropology Quarterly).

Who Is Being Studied and How?
The first publications (n = 2) were issued in 2008 (Table 1). The number of articles published each year ranged from zero articles in 2010, 2011, and 2013 to four articles in 2009, 2015, 2017, and 2018. All publications were in journals with an impact factor, and the majority ranked in the first quartile (21/28). Four articles were published in journals in the second quartile, and three articles in the third quartile. All articles were published in the medical and health sciences subject area, and one was also classified in social sciences (the journal of Medical Anthropology Quarterly).
Three studies were conducted in the Netherlands [40][41][42], in 2014, 2015, and 2017, aiming to assess inequalities in vaccine uptake; one included a qualitative study with an intersectionality framework to capture the perceptions of migrant women from Somalia concerning cervical cancer prevention [42]. Three studies were conducted in Sweden [43][44][45], in 2014, 2017, and 2019, with different study designs and populations. The first study used individual interviews with parents who refused their daughters from receiving the HPV vaccination. The second study investigated HPV vaccination status in female adolescents and related sociodemographic factors, individual beliefs and knowledge about HPV prevention, and sexual experiences. The last study aimed to investigate inequities in HPV vaccine uptake 10 years after its introduction in the country, where three different delivery modes of the vaccine have existed since 2007.
Moreover, three studies were conducted in Denmark [46][47][48], one in 2015 and two in 2018, all using data from the Danish childhood immunization program.
Finally, five countries had one publication each, with different populations and approaches. The study conducted in Greece in 2020 focused on the vulnerable population of Roma women [49], while the study conducted in Poland in 2021 focused on Polish men [50]. Research conducted in Norway [51] and Spain [52] was centered on adolescent girls and parents, and the Italian study investigated factors related to HPV vaccination refusal in young adult women without starting or completing HPV vaccination [53].
The majority of the articles had as the main outcome HPV vaccination uptake and its determinants (n = 19), while others focused only on HPV vaccination intentions (n = 9). Twenty-two articles used a quantitative approach, mostly with a descriptive design, while six articles used a qualitative approach with individual interviews and focus groups. Table 1 presents more details on the characteristics of the studies.

Barriers and Facilitators of Vaccination Uptake
All the included articles referred to barriers or facilitators of vaccine uptake. Access, acceptance, and activation were the most frequent themes, and awareness and affordability were less frequent. Barriers and facilitators to HPV vaccine uptake subthemes were identified and are summarized in Table 2.

Access and Affordability
Demographic and socioeconomic status were common barriers to HPV vaccine uptake in different European countries [35,41,48,49]. Specific barriers were also reported for people with refugee/migrant or ethnic minority backgrounds [48,49,52]. For example, Spencer et al. combined the use of the index of multiple deprivations and census ethnicity data to explore the links between HPV vaccination and cervical screening uptake with deprivation and ethnic composition of the area of residence in a deprived region in England. Results revealed that girls from the most deprived areas were less likely to complete the three vaccine doses. The authors concluded that there is a group of women from disadvantaged backgrounds and with a higher concentration of ethnic minorities who miss both cervical screening and HPV vaccination [35].
Several socioeconomic predictors of HPV vaccination were found in a cohort study based on the national HPV childhood vaccination program in Denmark. Ethnicity was found to be a strong determinant of initiation and completion of HPV vaccination. A social gradient regarding education, income and employment status was also observed, where decreases in vaccine coverage were associated with girls whose mothers were more disadvantaged [48]. A cross-sectional study in the Netherlands also found that vaccination uptake was higher in low urbanized settings and among girls without a religious background [41].   In Southeast Europe, a cross-sectional study in Greece with various groups of vulnerable women found that nationality was related to knowledge and attitudes on cervical cancer etiology and the HPV vaccine, with native women demonstrating higher knowledge than migrant and Roma women. The findings also indicated that Roma women faced higher levels of marginalization and social exclusion compared to legalized migrant women [49]. Additional factors associated with limited knowledge on risk factors for cervical cancer and erroneous attitudes and perceptions on cervical cancer prevention (Pap smear and HPV vaccine) included older age, low educational level, housing conditions, and lack of insurance coverage [49]. The lower uptake of the HPV vaccine among refugee girls is a challenge to immunization programs in raising ethnically diverse societies [47].
Socioeconomic factors and education were among the identified facilitators of vaccine uptake [43], in addition to factors such as country of origin and time of residence as predictors of uptake in migrant populations [47]. Routine school-based vaccination and free-of-charge vaccination were also identified as providing equitable delivery, yet needing to be complemented with information campaigns designed to optimize the uptake of the HPV vaccine by reducing disparities in some socio-economic disadvantaged sub-groups with lower vaccine uptake [45,51]. A nationwide cohort study in Sweden, for example, compared three delivery modes of the vaccine and concluded that free-of-charge schoolbased HPV vaccination was the most effective and equitable delivery mode, including high-risk groups for cervical cancer [45].
A qualitative Swedish study among parents who did not consent to their daughters receiving the HPV vaccination showed that parents went through a complex decision process, in an equation of the perceived risks and benefits of the vaccine, leading to the choice to vaccinate, or not to. Reasons for HPV vaccination refusal relate to the belief that it was better for the daughter's health and well-being. Given the private and intimate nature of the HPV vaccination (perceived as a behavioral vaccine), some parents chose not to vaccinate based on the fact that the common good of herd immunity was of minor interest compared with the best interests of their daughter. Another key reason for declining HPV vaccination was the perceived absence of sufficient knowledge about HPV and the vaccine. Parents rated the information received from the school health system unsatisfactory and preferred to postpone vaccination. Levels of trust in vaccinations, healthcare providers, and governments also were found to affect the complex HPV vaccine decision process [43].
There were less data on vaccine affordability. A study among vulnerable women in Greece pointed out the need to increase access by way of enlarging insurance coverage and reviewing screening recommendations. Improved healthcare delivery systems, towards more direct patient care, reduced delayed care, and appropriate preventive health services, were highlighted to reduce non-financial barriers to vaccination [49].
Enabling factors identified, such as insurance coverage for HPV vaccination, echo the ability of the person to navigate the healthcare system and in obtaining social benefits. Interventions to increase uptake in catch-up age groups must safeguard that vaccine costs are included [26].

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Awareness and Acceptance Lack of information/knowledge or perceived need were frequently cited barriers to vaccination [27,29,32,37,39,42,43,49,50]. One cross-sectional study among young adult women in Italy showed that participants with more concerns about the safety and efficacy of HPV vaccination were less likely to be vaccinated. Results seem to indicate the need for delivering accurate and clear information about vaccine efficacy and safety to boost HPV vaccination coverage [53]. An exploratory study in Poland on the knowledge about HPV infection and HPV-related cancers also found that the danger is poorly understood among men. The authors suggest that healthcare professionals need to broaden their knowledge about the specific health needs of underserved populations such as LGBTQ+ communities to prevent health disparities [50].  [29,32,36,40,42,49] Mollers et al. found that vaccinated girls in the Netherlands were less likely to have a religious background, and amongst those who professed religion, vaccinated girls were more often Catholic while unvaccinated girls were more often Protestant Christian. Moreover, no differences were found in terms of sexual risk behavior and knowledge of HPV infection and transmission, while differences were found in contraceptive use, the number of lifetime sexual partners, and opinions on the use of condoms after HPV vaccination and the protection of vaccination against all HPV types [41].
A six-month follow-up study conducted in 2006 shortly after the HPV vaccine was licensed in England found that young women with a history of an abnormal Pap test were less likely to have received the vaccine. This fact was confirmed by others [51]. On the contrary, identified predicted factors for HPV vaccination included the belief that one's parents, partners, and clinicians recommended HPV vaccination [26].
A survey in Spain also pointed out that advice from the nurse and physician was the key factor in HPV vaccination [52]. This result adds to the understanding that social norms predict HPV vaccine intent and uptake [47].
Among the facilitators, the intention was a strong predictor of uptake, together with past childhood vaccination uptake. Furthermore, HPV vaccination intention and uptake are based on similar determinants in the different ethnic groups, meaning that interventions based on similar behavior change methods (e.g., psychological inoculation or peer modeling) could be designed with added actions to reach different ethnic populations [40].

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Activation towards vaccination uptake Nurses and doctors lead the health processes of healthcare users, and the uptake of their recommendations [43,52]. Catch-up campaigns may improve immunization coverage with doctors' and trusted individuals' endorsements and promote vaccination as normative [47].
In the case of vulnerable populations, interventions to increase the prevention of cervical cancer, routine examination with the Pap test, and HPV vaccination need the healthcare delivery systems to be adapted accounting for cultural, social, and religious diversity [49]. Ethnic disparities in HPV vaccination may be understood in light of the levels of concern about the vaccine [29]. Interventions to increase immunization should be culturally tailored and community-based [29,33,40,42,49].

Attitudes and Beliefs about the HPV Vaccine
There are diverse health beliefs and objections to vaccination. Mollers et al. found that vaccinated and unvaccinated girls in the Netherlands were comparable in most sexual risk behaviors and had similar scores on knowledge of HPV infection and HPV transmission, but they differed for characteristics such as contraceptive use, the number of lifetime sexual partners, and their opinions on the use of condoms after HPV vaccination and the protection of vaccination against all HPV types. Sexually active vaccinated girls were more aware of the risk of HPV infection when engaging in unprotected sex [41].
Some studies mentioned the role of religious and cultural prohibitions on sex before marriage as a barrier to vaccination, related to low levels of awareness in some minority groups [35]. For some families, the HPV vaccination was not considered compatible with their life values. Building self-confidence in girls to delay sexual debut was chosen among other alternative methods of prevention [43].
Besides moral concerns, some studies indicate that there is a group of parents who consider that the vaccine is not necessary and/or serves the interest of the government or pharmaceutical companies. In this case, HPV vaccine decline is linked to the belief that vaccines are unnatural. Other reasons include the belief that vaccinations are used for population control [43]. A qualitative study in Romania points out that mothers' main reasons for not vaccinating their daughters are the belief that the vaccine represents an "experiment that uses their daughters as guinea pigs", the belief that the vaccine embodies a conspiracy theory to reduce the population, and mistrust in the health system [37].

Discussion
This study described barriers and facilitators of HPV vaccine uptake and identified determinants of under-immunization, reviewing data on European countries, where HPV vaccination has been gradually introduced in the national immunization programs since 2007. Given the chosen focus on health equity, these data are relevant to strengthening vaccination programs to promote vaccination for all people.
Health policies and practical implementation processes of HPV vaccination vary across European countries, as shown in Table 3, with information on HPV national immunization programs of the 10 countries covered in this review (Denmark, Greece, Italy, Netherlands, Norway, Poland, Romania, Spain, Sweden, United Kingdom). In most countries, the HPV vaccine is administered in public health clinics, while countries such as Norway, Sweden, and the UK have established school vaccination programs, and Spain offers a combination of school and/or health centers depending on the region.
Four of the analyzed countries (Italy, the Netherlands, Norway, and Poland) recommended gender-neutral vaccination, i.e., vaccination in all girls/women and boys/men, and one (the United Kingdom) for men from specific subgroups (men who have sex with men). However, information concerning HPV vaccination coverage rates is missing in men, indicating the need for better surveillance [54,55].
Access to and acceptance of HPV vaccination are key factors influencing vaccine uptake, therefore requiring multilevel action. Access barriers were the country of origin related to the sociodemographic status, and cultural beliefs [52]. Local delivery of HPV vaccination and organizational factors are central to reducing cervical cancer inequities [35], such as the role of school nurses in increasing HPV vaccine uptake among vulnerable groups [56].
A recent study that reviewed HPV vaccination coverage in 31 European countries has concluded that structured vaccination programs targeting females early in adolescence and free-of-charge vaccine administration were more frequently observed in countries with high vaccination coverage rates. Facilitating access to HPV vaccination by increasing onsite vaccine availability, sending invitations and reminders to attend for vaccination, and relying on schools as the main setting to administer the vaccine could also be important factors to achieve higher vaccine uptake [54].
The findings of this review have shown that besides HPV vaccination policies and practical implementation, HPV vaccination is also influenced by sociocultural factors and individual characteristics.
Religion has been shown to influence the vaccination decision-making process with certain religious or ideological groups being linked to anti-vaccination movements and outbreaks of vaccine-preventable diseases [57]. Some parents perceived their daughters to be too young to be vaccinated and to be sexually active. A more flexible vaccination schedule with the option of offering vaccinations later and providing more adequate and comprehensive explanations about the virus and the vaccine could be strategies to improve vaccine uptake [43].
Interventions aimed at increasing HPV vaccine coverage should be focused on raising health professionals' HPV awareness to better inform patients about HPV infection and vaccination [52]. The dissemination of culturally adapted and unbiased information, together with the opportunity to talk about the vaccine with healthcare professionals, could contribute to trust in public government recommendations and increase vaccine coverage [43]. As the COVID-19 pandemic has revealed, the success of public health campaigns relies on trust in leaders, experts, and medical professionals, however social determinants like race, class, and gender influence vaccines attitudes and beliefs, on the one hand, and also the state, on the other, because interactions with the state are multifaceted, bureaucratic, and can be coercive. Further investigation on attitudes toward immunization among marginalized populations is needed to identify alternative practices from dominant narratives that could better inform inclusive public health outreach [58].

Strengths and Limitations of the Research
The results of this review should be interpreted in light of its limitations. First, only two different databases were consulted for locating papers with no additional search strategy, such as searching references of the included papers or references of literature reviews identified during the screening process. This may have limited the inclusion of more articles from the social sciences field, although Scopus is among the largest databases, with a wide global and regional coverage of scientific journals. A strong point, nevertheless, is that the search strategy was comprehensive and followed the recommendations made by the Joanna Briggs Institute (JBI) [25], such as the Population/Concept/Context method, to identify the main concepts and the definition of inclusion criteria.
The second limitation is that only the studies conducted in European countries were included in this review, with no inclusion of comparisons with other contexts for a broader mapping of the state of the art regarding the attitudes and practices towards HPV vaccination and its social processes. Given the great variability in terms of the social, cultural, and institutional vaccine contexts and national vaccination programs, efforts were made to add more knowledge about the European contexts, that were less investigated, to better identify tailored and evidence-informed strategies.
Finally, all articles, independently of the study design or quality, were included to jointly present findings, which may also be considered a limitation. However, this review aimed to summarize the scientific evidence regarding the barriers and facilitators with a focus on health equity; therefore, all identified articles were included to facilitate the overview of the key factors influencing vaccine uptake.

Recommendations for Research and Action
This review is not representative of the European region, considering that included studies came from only ten countries, largely focusing on Western Europe. Given that all EU/EEA countries have introduced HPV vaccination in their national programs, and many countries have recently changed or are changing to a gender-neutral HPV vaccination [59], there is a need for more data on HPV vaccination with disaggregated data for diversity, which is rarely collected by national data. Monitoring HPV vaccination uptake and policies at a European level, as well as sharing experiences between countries, could contribute to the success of HPV vaccination programs and address health inequities [54].
Certain subpopulations were not well reported and did not reflect on how different intersecting identities place people at multiple disadvantages, such as LGBT people, different migrant and ethnic minorities, and several other vulnerable and most at-risk-identified populations. This indicates a need for HPV vaccine uptake datasets in Europe that disaggregate by diversity to monitor HPV vaccination inequalities. Sub-analyses on vulnerable populations could be conducted with disaggregated data from general population studies.
Joining vaccination strategies with other recommended healthcare services for populations burdened by HPV infection and HPV-related diseases, such as LGBT people, could increase vaccination in these populations where HPV vaccine acceptability tends to be high [9].
Action plans to address specific perceptions and barriers towards HPV vaccination should be co-designed with the most at-risk-identified populations and inclusive catch-up initiatives could be considered drawing on new models of good practice in vaccine delivery employed during the COVID-19 pandemic [23].