Cervical cancer (CC) is the tenth most common cancer among French women 1 . In 2011, an estimated 2,800 new cases were diagnosed, leading to 1,000 deaths 1 . The fight against CC involves two strategies: Papanicolaou smear testing (Pap test), and vaccination against the sexually transmitted Human Papillomavirus (HPV) responsible for nearly all cases of CC 2 . In France, Pap test screening is recommended every 3 years for women aged 25–65 3 and its use since the 1970s has markedly decreased CC incidence (2.9% decrease per year between 1980 and 2005) and mortality (4.0% decrease per year). Nevertheless, adherence with Pap test screening recommendations is still insufficient: in the period 2006–2008, it was estimated that only 56.6% of 25–65 year old women had had the smear within the previous three years 3 . There are also major geographical and socio-economic disparities in take-up rate 4 .

More recently, a new primary prevention tool has become available with the development of two vaccines [5;6] targeting the high-risk HPV 16 and 18 genotypes responsible for 70% of CC 2 . These vaccines were licensed in France in 2007 and their use is funded. French health authorities recommended HPV vaccination for girls reaching 14 years with catch-up vaccination for girls aged 15–23 within their first year of sexual activity 5 . Since parental consent is required for vaccination of adolescent girls, parents, and especially mothers, are key decision-makers and potentially a major source of information for their daughters 6 .

Attitudes towards this new vaccine seem to be positive, with most studies on parental attitudes reporting acceptance rates above 60% 7 8 9 10 11 . Nevertheless, awareness about CC and HPV among women is limited 12 . Factors associated with the decision to vaccinate are complex and varied. Previous studies highlighted concerns about safety, but evidence on the influence of parental knowledge 10 13 14 15 , the preventive health practices of the mother 8 13 16 and socio-cultural context 8 10 11 17 18 is conflicting. In a recent meta-analysis of studies dealing with parental attitudes towards HPV vaccination, Trim et al. showed that being concerned about the potential risk of cancer and believing their daughters might contract HPV and related diseases were drivers for HPV vaccination 19 . However, parents would prefer to vaccinate older children and those who were sexually active. Previous attitudes towards other vaccines predicted acceptance of HPV vaccination, and a physician’s recommendation was also a major factor. In addition, because HPV is sexually transmitted, parental acceptance of the vaccine raises issues, including the perceived risk of promoting risky sexual behaviour 19 20 , which are broader and quite distinct from those raised by other vaccines 21 .

Most previously published studies on CC and HPV awareness have been from North America: with the exception of the United Kingdom, little such research has been carried out in Europe 19 . Several factors specific to France make it a particularly interesting case study of attitudes towards and uptake of HPV vaccination. First, the target age for immunization (14 years and above) is relatively old compared with that in other countries. Secondly, the controversy in the 1990s over the supposed link between the vaccination of adolescents against hepatitis B and the development of multiple sclerosis was sufficient to bring a halt to the immunization campaign. This particular scare about vaccination did not occur in other countries but may have had long-term effects on the perceived safety of mass vaccination in France. Such a finding would have wide implications. Finally, the fact that national regulators recommend HPV vaccination and the 65% reimbursement of costs could provide a favourable setting.

The first objective of this study, which combined quantitative and qualitative techniques, was to assess knowledge about CC, the Pap test and HPV vaccination in 18–65 year-old French women one year after the introduction of the vaccine. The second objective was to assess mothers’ acceptance of HPV vaccination for their 14–18 year old daughters and determinants of that acceptability. The age range 14–18 was chosen to encompass girls above the age at which vaccination is recommended in France and below the age at which they can themselves legally assent to the procedure. This study was part of the REMPAR (Recherche et Evaluation des Moyens de Prévention Anti-HPV en Rhône-Alpes) programme aimed at evaluating means of preventing HPV-mediated disease.

This cross-sectional study, conducted in the Rhône-Alpes region of France in June and July 2008, used both quantitative (self-administered questionnaire) and qualitative methods (semi-structured interviews).

One year after the licensing of the HPV vaccine in France, knowledge about the role of the Pap test in CC prevention is quite good. However, when asked an open-ended question about the cause of CC, the link between HPV and CC was not widely made. Even so, among mothers of 14–18 year old girls, the majority accepted the value of HPV vaccination -- although 37% were still undecided.

Responding to multiple choice questions, 93.7% of women knew that the Pap test should be conducted yearly or every 2–3 years and 82.0% answered correctly that screening should continue throughout adult life. However, only 61% answered that the purpose of Pap testing is to prevent CC. It seems that women passively accept the Pap test without really knowing why: 80% of French women are reported to have Pap tests on the advice of their physician and not on their own initiative (cervical screening in France is opportunistic.) 24 . Our data suggest that the cause of CC is not widely known. Despite information campaigns on CC and its prevention related to the marketing of HPV vaccines, few respondents (17% of the wider population of women studied and 21% of mothers) spontaneously mentioned HPV. Nevertheless, this level of awareness is much higher than before introduction of the vaccine: in surveys reported in 2001 and 2004, fewer than 2% of women mentioned HPV as the cause of CC 25 26 .

In contrast, the HPV vaccine itself is now well known: 76% of our overall sample and 91% of mothers had heard of it. However, they did not know precisely who should be vaccinated or at which age. This may be explained by the fact that the predominant source of information on the vaccine is the media (mentioned by 54.7%). Few women had been individually informed by their physicians.

The majority of mothers with a 14–18 year old daughter were supportive of HPV vaccination. A substantial proportion (38% in our sample) is still undecided, but very few (< 1%) are clearly opposed. Even if French physicians have also been shown to be supportive of HPV vaccination 22 , the reality is that in France in 2010, only 38.7% of 14 year old girls had received at least one dose of the vaccine. The corresponding uptake among 16 year olds was 50.0%, and among 17 year olds 52.6%. HPV vaccine acceptance in our sample was lower than was suggested by data from 2007 when the proportion of parents intending to vaccinate their child was 67% 19 . The main issue remains the large population of undecided mothers, and we need a better understanding of factors influencing parental decisions. Protecting one’s daughter against a potentially lethal cancer is the main reason mothers give for vaccinating their daughters. Efficacy is not questioned, and the main concern with HPV immunization is the newness of the vaccine. A year after the vaccine’s introduction, mothers still feared the emergence of unexpected side effects. Vaccine safety is frequently the main concern about HPV immunization reported in the literature 10 17 26 27 . In our interviews, mothers who were still to make up their minds linked their reluctance to accept the new vaccine to the controversy in France about the suggested connection between Hepatitis B vaccination and multiple sclerosis 28 .

Physicians represent a key influence 29 , and their advice is crucial in avoiding misconceptions among undecided mothers 7 17 27 . Freed et al. showed that the principal information source that mothers trusted was their physician (76%) 30 and Little et al. found that mothers who received information from their health care provider were significantly more likely to intend to vaccinate their daughters than those who did not receive such information (OR=3.56 [1.52-8.45]) 31 . Along with others, our data suggest that provision by physicians of more complete information on vaccine safety could encourage acceptance 10 13 32 . As a specific example of this, we found that mothers who knew the target population for the HPV vaccine were more favourable towards it.

We also identified other determinants. Having already vaccinated their children against pneumococcus was associated with a positive attitude towards HPV vaccination. This may reflect a wider attitude towards vaccination. Mothers who believe vaccines in general are safe are more willing to vaccinate their daughters against HPV 10 33 34 35 . More surprisingly perhaps, our findings suggested that mothers who did not know how frequently Pap testing should take place were more favourable towards HPV vaccination than those with greater knowledge. A possible explanation is that women who are more aware of Pap testing regard it as an effective method to prevent CC and so see less need for vaccination. In justifying their position, some mothers unfavourable to the vaccine argued that an effective method to prevent CC already existed.

However, on multivariate analysis, Pap test adherence itself was not associated with less acceptance of the vaccine.

Socio-economic characteristics were not associated with HPV vaccine acceptance. Unfavourably disposed mothers did not mention cost as a barrier to vaccination in either the questionnaire or interviews. This may be due to the partial reimbursement (65%) by French public health insurance.

Our results do not support the concern raised previously that underprivileged populations or populations with low adherence to Pap test screening would be less accepting of HPV vaccination. With regard to educational level, the results tended to be the reverse, with a lower acceptance of HPV vaccination among better educated mothers, as has previously been found 10 11 17 27 . However, two factors found relevant in a recent review were little mentioned by mothers in our study 19 . Our respondents did not express the fear that vaccination would encourage more risky sexual activity, and they did not reflect a belief that the age for vaccination was too young 19 . With respect to lack of concern about potential sexual disinhibition, our findings are in line with those of the recent Canadian study by Ogilvie et al. 28 . And in relation to the age recommended in France for HPV vaccination, it is worth noting that this is in fact older than in many countries 36 . Since the median age at first intercourse in France is 17, many girls aged 14–18 will already have begun sexual activity, while others are close to doing so.

Possible limitations in our findings should be mentioned. Certain factors previously shown to be associated with HPV vaccine acceptance, such as the younger age of mothers, STD history, tobacco consumption and educational level, were significant in univariate analysis but not after multivariate adjustment. A lack of power due to the relatively small sample of mothers could explain these discrepancies. Another limitation is that since recruitment took place during a GP consultation our respondents may have been more attuned than the wider population to their medical needs. Women included had a history of good gynaecological follow-up and a high rate of Pap test screening: 82.9% of the women sampled (and 87.0% of mothers) had had their most recent Pap testing within the past three years. Data from the French public health insurance system estimate that Pap test coverage nationally is only 56.6% 3 . However in a more recent study, 79.7% of a sample of 1,688 20–65 year old women reported having had a Pap test in the past three years 37 , and our sample’s characteristics seem to be representative of women in the Rhône-Alpes region with a similar age distribution.

Our choice of question to assess the acceptability of HPV vaccination, and the multiple choice responses offered, could also be debated. Our intention was to cover the range of mothers’ attitudes and behaviour. Focus groups prior to the study showed a good understanding of this question and of the options for response. Moreover, all respondents were able to justify their opinion and give further detail in an open ended question; and those interviewed had additional opportunities to discuss why they were favourable towards vaccination, or otherwise.

Finally, we used a cross-sectional design. This did not allow us to determine whether the associated factors identified are the cause or the consequence of HPV vaccine acceptance: greater knowledge about the vaccine could be the result of information given during its administration or, alternatively, might have driven the decision to seek vaccination.

One year after French national health authorities recommended HPV vaccination, knowledge and awareness about HPV as the cause of CC is still poor a mothers of girls in the targeted age range are globally favourable towards the HPV vaccine but are seeking additional information. The results of this study suggest the type of information that could be disseminated to improve vaccine uptake. This relates principally to the record of vaccine safety. However, women do not fully understand the place of HPV vaccination alongside Pap testing in CC prevention because they are not fully aware of HPV as the cause. The need to complete this link in the information chain could also be addressed. Appropriate information on these topics may improve mothers’ acceptance of vaccination for their daughters. Physicians seem best placed to answer their questions.

Women know that the aim of Pap testing is to prevent CC; and they know that there is an HPV vaccine. But they do not know that HPV causes CC. The majority of mothers of 14–18 year old daughters were favourable towards HPV vaccination. Those who were unfavourable justified their opinion mainly by the fear of side effects. Factors associated with acceptability were knowledge about the HPV vaccine, acceptance of other vaccines and lack of knowledge about the recommended frequency of Pap testing. Compliance with recommendations for Pap test screening and socioeconomic factors did not significantly affect views on HPV vaccination. GPs seem to have a key role in providing further information about HPV vaccination (particularly in relation to the virus as the cause of CC) and in reassuring women of its safety.

CC: Cervical cancer; GP: General practitioner; HPV: Human Papillomavirus; OR: Odds ratio; STD: Sexually transmitted disease.

Authors declared no competing interests expect Yann Leocmach and Anne-Carole Jacquard who are employees of Sanofi Pasteur MSD, Lyon, France.

JH: performed the statistical analysis and interpretation of data, wrote the manuscript. DL-M: participated in the design of the study, helped to draft the manuscript and revised it critically for important intellectual content. JK: conducted and interpreted the interviews, wrote the qualitative part of the manuscript. GB: participated in the design of the study and coordinated the data collection. A-CJ: has given final approval of the version to be published. VR: participated in the design of the study. YL: helped in the interpretation of data and has given final approval of the version to be published. PV: participated in the design of the study. FC: participated in the design of the study and helped in the interpretation of data. CL: participated in the design of the study and its coordination and helped in the interpretation of data; revised the manuscript critically for important intellectual content. All authors read and approved the final manuscript.