Human papillomavirus (HPV) is a necessary cause of cervical dysplasia and cancer. Genital warts are one of the most prevalent sexually transmitted diseases in Europe. HPV vaccine coverage is thus an important public health concern and understanding the reasons for accepting or rejecting vaccination is essential for increasing compliance.1

The reasons for decreased vaccination coverage seemed to be different according to region and circumstances.2 There were factors such as the negative impact of mass media, misinformation from anti-vaccination movements, as well as the initial “aggressive” campaigns carried out by commercial companies.3–5 In Spain, these campaigns started a polemical debate even before the vaccination program was launched, possibly creating uncertainty regarding the indications for HPV vaccination among some healthcare professionals. Vaccination coverage in the first campaign, in a cohort of girls born in 1994 vaccinated with three doses, was 75.2% of the total target population. However, in the following campaign (1995 cohort), it decreased to 62.5%. And although it increased again slightly to 67.6% in the 1996 cohort, the overall rate did not improve in the region.6 Economic studies carried out before and after the vaccination program stated that vaccination coverage of 70%, or higher, was necessary to predict cost-effectiveness of an intervention.2–5 Nevertheless, these rates were relatively low compared to others obtained in England, Scotland or Wales (84.0%), where funding and implementation conditions were similar.7

Prior to the vaccination program, literature suggested that ethnicity, socio-demographic and psychosocial factors could play a decisive role in vaccination.8 Research after the vaccination programs were launched6,8–14 confirmed that age, perceived access to vaccination, cultural norms, religion, knowledge about the severity of the disease and risk perception, directly influenced the acceptance of the vaccine.1,15 These factors, together with the usual acceptance difficulties that any vaccine may have, are a challenge to achieve better vaccination coverage rates.

This study was designed to determine the drivers associated with HPV vaccination in the region of Valencia (Spain), and to ascertain whether there was a major determining factor in order to carry out more effective interventions to improve vaccination rates.

A questionnaire was distributed among 1,278 girls and their mothers, and we obtained 833 adequate answers (64.5%; 95%CI: 61.9-67.1). We chose a sample of 37 schools but only 31 participated (83.8%; 95%CI: 69.9-97.7), either because they were not given authorization by the parent school governing body (n=4) or due to school program issues (n=2).

From the descriptive analysis of the girls’ socio-demographic and family profile (Table 1), we found that 86.1% (95%CI: 83.7-84.8) of the girls were born in Spain, 79% (95%CI: 76.2-81.8) lived with both parents and 85.5% (95%CI: 83.2-88.0) had siblings. Regarding religion, 76.5% mothers and 66.4% daughters were believers, while 46.5% and 30%, respectively, were practicing individuals.

Regarding the multivariate analysis (Table 2), from 833 cases, 73 (8.7%; 95%CI: 6.8-10.6) were excluded due to uncertain vaccination status. A total of 566 cases (74.5%; 95%CI: 71.4-77.6) were positive vaccinations and 194 (25.5%; 95%CI: 22.4-28.6) were negative vaccinations.

Sixty-five variables were selected from a total of 155 to be included in the logistic regression model (40 variables from the girls’ questionnaire and 25 from the mothers’). The final logistic regression model included 84.5% of the cases, with 0.4 Cox & Snell and, 0.6 Nagelkerke coefficients. The success rate in the model prediction in vaccinated cases was 92.1% and 74.6% in non-vaccinated cases (global 87.9%).

After controlling for the covariates included, the multivariate model showed that the main factors associated with the HPV vaccination were the origin of the families (adjusted odds ratio [aOR]: 0.49; p=0.04), the civil status of the parents (aOR: 0.33; p=0.01), knowledge/beliefs about the vaccine when the source of information was the nurse (aOR: 1.83; p=0.048), the information source about the vaccine (aOR: 2.32; p=0.002), preventive healthcare centre visits (aOR: 2.1; p=0.02) and nurse advice (aOR: 6.6; p <0.001).

This was one of the most comprehensive randomized study carried out in Spain. It had a large sample size and a data collection period of eighteen consecutive months. It focused on the drivers associated with HPV vaccination in order to carry out more effective interventions to improve vaccination rates.

We observed that 74.5% of girls were vaccinated, with a vaccination rate slightly higher than that published by the Public Health Department that year (66.5%), probably because the profile of the analysed cases which did not answer the questionnaire or the profile of the excluded cases, responded to a slightly less vaccinated group than that included in the analysis. However, when comparing the resulting sample with the socio-demographic, cultural and family profile of the general population6 we can observe similar profiles. The sampling bias is thus compensated and it is considered representative.

The main drivers associated with vaccination were:

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  Country of origin of the mothers: the mothers’ country of origin as a determining factor for vaccination, has been associated, in the literature, with the difference between native groups versus immigrant groups, possibly due to cultural beliefs.16 The same occurs with cervical screening, since immigrant women do not undergo as many smear tests as native women.17 One may also associate these differences with the socioeconomic status of immigrant families and not just with their cultural beliefs.18 However, this is not the case here as there is free access to the HPV vaccine in Valencia. Therefore, we consider the difference to be due to the existence of a cultural barrier.

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  Marital status of the parents: the girls whose parents were separated were vaccinated less often than those living in a traditional family. This highlights the health protection a traditional family grants versus less conventional family models.19

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  Knowledge about how to avoid HPV infection: knowledge and beliefs about HPV vaccine can influence the vaccination decision directly. However, a reason they are a determining factor is due to the perception of safety and efficacy that these knowledge or beliefs give the individual when making a decision.20

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  Information source about HPV infection and vaccine: the source of information about the vaccine is also important. Information leaflets issued by local authorities were a positive factor for vaccination, although there are studies that show that television advertising was positively linked to vaccination in young girls, as well as internet information, which also had a strong influence in adolescent girls over eighteen years old.21

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  Knowledge about the vaccine from information leaflets: it was generally stated that most girls and mothers who had some information about HPV vaccine had seen it in leaflets issued by the local health authorities.14,19,20 It seems reasonable to affirm that the information campaign carried out among the target population was effective.

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  Girls’ perception of the vaccine: the girls’ health habits were the same as those of the general population, as seen in the Health Survey of the Valencian region of that year (2011).22 It needs to be emphasized that girls who were less prone to drinking alcohol, or never tried it, had a lower vaccination rate than the rest. Perhaps, girls with a cautious attitude towards alcohol had a lower risk perception about HPV infection. We can consider that a more conservative profile was linked to less risky actions, and mothers and daughters had an overall lower risk perception.

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  Use of healthcare system resources: preventive visit to their community nurse: as seen in different studies,23,24,26 girls who visited their community nurse several times in the last year had a higher vaccination rate than those who did not go to their healthcare centre.

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  Advice from a nurse or physician: this linear correlation seems based on the importance of the health professional's advice, where the nurse plays an essential role in the health system.24,25 Nurses, as well as doctors, lead the health processes of healthcare users, and their advice definitely influences vaccination.23,26 However, this influence is not always positive. Without a doubt, the main determining driver of the analysis was the healthcare professional's advice, mainly nursing staff, as they are the ones directly involved in the vaccination process. The nurses who endorsed the vaccine obtained significant results. The results were equally significant when they advised against vaccination. Many studies have shown the strong influence that this recommendation can have on parents and patients when deciding whether or not to have a vaccine.8,12,13,26 Therefore, adequate training and information of healthcare professionals directly involved in vaccination endorsement, particularly nurses, could improve HPV vaccine acceptance. For this reason, all the actions aimed at training healthcare professionals in detecting the cases which are less likely to be vaccinated and aimed at reminding patients about the link between HPV chronic infection and cervical cancer, as well as vaccine safety and efficacy, would help to decrease HPV infection and increase vaccine coverage.27,28

Of all the factors associated with vaccination, advice from the nurse together with their physician's advice was the main determining driver. Therefore, it is essential that healthcare professionals are adequately trained to inform patients about HPV infection and vaccination. Interventions aimed at increasing vaccine coverage should be focused on raising nurses’ and doctors’ HPV awareness in order to improve the health of adolescent girls.

Enrique Castro Sánchez.

The corresponding author on behalf of the other authors guarantee the accuracy, transparency and honesty of the data and information contained in the study, that no relevant information has been omitted and that all discrepancies between authors have been adequately resolved and described.

All authors were involved in writing the manuscript and approve of its final version.

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