Parental Knowledge, Attitudes, and Behaviours towards Human Papillomavirus Vaccination for Their Children: A Systematic Review from 2001 to 2011

Objectives. A systematic review of parental surveys about HPV and/or child HPV vaccination to understand parental knowledge, attitudes, and behaviour before and after FDA approval of the quadrivalent HPV vaccine and the bivalent HPV vaccine. Search Strategy. Searches were conducted using electronic databases limited to published studies between 2001 and 2011. Findings. The percentage of parents who heard about HPV rose over time (from 60% in 2005 to 93% in 2009), as did their appreciation for the HPV infection and cervical cancer link (from 70% in 2003 to 91% in 2011). During the FDA approval, there was a stronger vaccine awareness but it has waned. The same pattern is seen with parents whose children received the HPV vaccine (peak at 84% in 2010 and now 36% in 2011) or the intention to vaccinate (peak at 80% in 2008 and now 41% in 2011). Conclusions. Parents had safety concerns and wanted more information their physician from to recommend and to confidently HPV vaccinate their children.


Background
Human papillomavirus (HPV) is the most common sexually transmitted infection in the world and is an established causative agent for cervical, anal, and penile cancers, as well as genital warts in both men and women [1,2]. It is estimated that 75% of Canadians will experience an HPV infection at least once in their lifetime, with the highest rates of infection occurring in individuals under the age of 25 [3]. In June 2006, the US Food and Drug Administration (FDA) approved the quadrivalent vaccine for use in the prevention of HPV strains 6, 11, 16, and 18, which are associated with 70% of cervical cancer and 90% of genital warts cases [4,5]. In October 2009, the bivalent HPV vaccine was approved by the FDA for the prevention of HPV strains 16 and 18 which are associated with 70% of cervical cancer cases [4,6]. Unlike the quadrivalent vaccine, the bivalent HPV vaccine does not protect against strains of HPV that cause genital warts [6]. Both vaccines are administered in three doses over a period of six months.
As a result of the approval of the HPV vaccines, recent health policy discussions have introduced the idea of adjusting the age of initial PAP smears from 18 years old (or with sexual debut) to 21 or 22 years old (or with sexual debut) [7]. Additionally, a move away from PAP smears toward HPV viral testing for women over 30 with a concurrent decrease in the frequency of PAP smear testing from annually to every 3 to 5 years has been proposed [7]. These health policy shifts are rooted in the success of the HPV vaccines to guard against cervical cancer. This success is, necessarily, dependent on successful vaccine uptake.
Currently, policy is modelled on an 80% uptake by young women, which means when combined with vaccination, reducing the frequency of testing and increasing the age of initial PAP smear would be part of an efficient plan to reduce cervical cancer. However, actual uptake of the vaccines is relatively low and not consistent in all areas that the vaccine is offered. For example, in the province of Quebec where there is a passive consent strategy to school immunizations (i.e., parental consent must be explicitly withdrawn in a note to the school), there is an 80% vaccine uptake for grade-8 girls [8,9]. However, in the province of Ontario, where the school-based immunization program has an active consent strategy (i.e., parental consent is explicitly given in a note to the school), the vaccine uptake rate for grade 8-girls is 50% [8,9]. By comparison, the acceptance of the hepatitis B vaccine was accepted without difficulty yet both aim at preventing disease that is sexually acquired. The acceptance of the hepatitis B vaccine for grade-7 students in Ontario was 79.8% (range 65.2% to 95.2%) and in Quebec the acceptance for grade-8 students was between 85 and 95% [8,9]. The hepatitis vaccine is offered to both boys and girls and is marketed to prevent liver disease and liver cancer, which is relatively rare in the developed world compared to cervical cancer. Suggested reasons for a low vaccine uptake rate range from low knowledge levels regarding HPV and the HPV vaccine, to cost, to a perceived low efficacy of the vaccine. Recent literature has examined these possible factors as they relate to adolescent attitudes towards HPV vaccination [7]. However, given that the vaccines are targeted towards males and females in the 9-to 26-age group, with emphasis placed on ages 11 and 12 in order to promote inoculation prior to sexual debut [10], a key factor in the implementation of HPV vaccines is the extent to which parents accept HPV vaccination for their children. In order to fully understand the issues surrounding HPV vaccine uptake, parental attitudes towards the vaccine must be examined.

Objectives
The purpose of this systematic paper is to compare the findings of previous studies that have examined parental knowledge, attitudes, and behaviours towards the HPV vaccine. Particular emphasis will be placed on changes within parental knowledge, attitudes, and behaviour following the availability of the HPV vaccines. Beyond identifying trends in uptake, the paper will also focus on factors that affect parental intentions to vaccinate their children against HPV. Based on previous studies regarding vaccination, these factors may include parental knowledge regarding cervical cancer and STIs (i.e., genital warts); perceived risk and severity of cervical cancer and genital warts; attitudes towards vaccines in general; issues concerning increase in sexual activity or promiscuity; availability of health insurance to cover vaccine costs. Additionally, a preliminary analysis of parental attitudes towards STI-prevention interventions versus anticancer interventions will be conducted to determine the policy implications of the two vaccines; one of which is part of an anticancer strategy as well as STI (genital warts) prevention and one of which only targets cervical cancer prevention.

Search Strategy.
Prior to conducting the literature search, a librarian was consulted for assistance in building a comprehensive search strategy. Relevant research studies were located through an extensive search of the electronic databases PubMed, Ovid MEDLINE, Embase, and Cumulative Index of Nursing and Allied Health Literature (CINAHL). Searches were limited to only those studies which were published between 2001 and 2011 in an effort to obtain the most recent articles regarding parental knowledge, attitudes, and behaviour before and after FDA approval of the quadrivalent HPV vaccine and the bivalent HPV vaccine.
A preliminary hand search of the literature was completed in order to identify appropriate keywords and medical subject heading (MESH) terms. The terms that were selected to be used in this paper were "HPV", "parent" and "vaccine," with "parent-child relations," "papillomavirus vaccine," "parent or child parent relation," and "wart virus vaccine" often being utilized as synonyms. Search terms were combined using the operators "AND" and "OR" to ensure that all relevant articles were located.

Study Selection.
A total of 325 articles were identified: 304 from the initial search strategy and an additional 21 articles were gathered from the hand search of the literature. Following the removal of duplicates (n = 71), 254 articles were screened for inclusion in the paper ( Figure 1). Inclusion criteria included (a) the study was about parents and their attitudes towards HPV and/or HPV vaccination; (b) the report had cross-sectional data about the parent's knowledge, attitudes, or beliefs about HPV that were not previously influenced by the research team with an intervention. Exclusion criteria included (a) sample population was not comprised of parents; (b) knowledge, attitudes, and/or behaviours of parents not discussed in results; (c) methodology of study did not include survey; (d) article was not based on original research (i.e., the study was a literature review); (e) the full article was not available in English. The results of the study selection process are shown in Figure 1.

Data Collection and Abstraction.
The data abstraction form was created and was pilot tested on five articles. Once the remaining modifications were made to the abstraction form, three coders extracted the data based on the coding information provided on the form. The data was then entered into SPSS for analysis, with information being transformed into percentages where possible. Initially, five outcomes that correspond to parental knowledge, attitudes, or behaviours were recorded. These five outcomes were that the parents had heard of HPV, heard of the HPV vaccine, knowledge of association between HPV and cervical cancer, an intention to vaccinate their child, and vaccinated their child(ren) with one or more doses of the vaccine. Following this initial analysis, an analysis of factors affecting parental attitudes toward the vaccines was conducted.

Characteristics of Study Samples.
The literature search resulted in 53 studies that met inclusion criteria and were included in this systematic paper . All included studies have been listed by publication date, research question, and focus in were administered to parents in 2007 or earlier in 60.4% of the studies. The majority of the studies were conducted in North America (USA: 56.6%; Canada: 3.8%), however, the European Union (24.5%), Asia (9.4%), and New Zealand or Australia (5.7%) were also represented. Figure 2 highlights the geographic representation of the sample. Forty-one percent of studies were conducted in a school or medical setting, while 45.3% used some form of population-based sampling (e.g., census or government data, random digit dialling, or an existing longitudinal study), and 13.2% used other sampling procedures. These "other" sampling procedures included pretest data from an educational HPV intervention or mixed methods. Figure 3 demonstrates the methodology of the studies in the sample. The total number of parents included in this study was 54,194 with a median study sample size of 506, and a mean study sample size of 1,022 (SD = 2,099). Six studies only reported "parents" and did not differentiate between mothers and fathers. Twenty-three studies (43%) reported mothers' responses only. Of those studies that reported both mothers' and fathers' attitudes, the majority of respondents were mothers with the average sample size of mothers at 82.3% (minimum: 47.7% and maximum: 95.1%).

Framework for Analyses.
Studies posed a wide variety of research questions; in order to simplify analyses, each study's central question and results were grouped according to whether they were concerned with parental knowledge of HPV, parental behaviours toward the HPV vaccines, parental intent to vaccinate their children against HPV (attitudes), or a combination of the three factors (Table 1).
Of the 53 studies included, 73.6% (39/53) attempted to gauge parental knowledge of HPV and the HPV vaccine.  Other (e.g., school, clinic, etc.) This ranged from whether parents were aware of HPV to whether parents could correctly identify HPV as the causative agent of cervical cancer. Thirty-eight percent (20/53) of studies focused on parental behaviour (i.e., whether parents had already inoculated their child or children against HPV with either of the two vaccines available). Finally, 92.5% (49/53) of studies focused on parental attitudes toward the vaccine (whether parents intend to vaccinate their children against HPV). Many studies also focused on factors affecting parental attitudes and behaviour regarding the HPV vaccine. These factors included perceived vaccine efficacy; vaccine safety; perceived threat of HPV. They will be discussed more thoroughly in the section regarding factors and barriers.    Obstetrics and Gynecology International    Obstetrics and Gynecology International

Knowledge Trends.
Three primary knowledge questions were examined: whether parents had heard of HPV, whether they had heard of the HPV vaccine, and whether they could correctly identify the relationship between HPV and cervical cancer. Of the 53 studies, 19 studies (36%) asked parents whether they had heard of HPV prior to being included in the study (Figure 4). Parental awareness of HPV increased in 2008 and 2009. Of the 53 studies, 15 studies (28%) asked parents whether they had heard of the HPV vaccines prior to being included in the study ( Figure 5).
Parental awareness of the HPV vaccine spiked in 2007 with a mean percentage of 59% compared to 14% in 2006. Awareness continued to climb to 65% in 2008 and dropped off slightly to 47% by 2010. These years are of particular interest since they mark the introduction and availability of the quadrivalent HPV vaccine and the bivalent HPV vaccine. Of the 53 studies, 5 studies (9%) asked parents if they could identify the relationship between cervical cancer and HPV ( Figure 6).
It is important to note that only 5 studies asked parents to make the connection between HPV and cervical cancer. In the study in which data were collected most recently (2011), an average of 74% of parents could correctly identify the relationship between HPV and cervical cancer. With only 5 studies examining parental knowledge of the relationship between HPV and cervical cancer, it is difficult to make any connections between knowledge and the introduction and availability of the HPV vaccine.

Behaviour Trends.
Of the 53 studies, 17 studies (32%) asked parents whether their child or children had already been vaccinated against HPV (Figure 7).
Following the availability of the quadrivalent HPV vaccine in 2007, studies began asking whether parents had already vaccinated their children against HPV. The highest percentages of parents who had vaccinated their children against HPV occurred in 2009 and 2010. This is following the introduction and availability of the bivalent HPV vaccine in 2009.

Attitude Trends.
Of the 53 studies included, 30 studies (57%) asked parents whether they intend to vaccinate their child or children against HPV (Figure 8). The

Parents Agreed That Children Should Be Older and Sexually
Active to Receive the Vaccine. There were 10 studies (19%) that mentioned the child's age affecting the parents' decision to vaccinate. Parents were less likely to vaccinate their children if they believed their children were too young or not sexually active [34,40,44,48]. Some studies indicated that parents were more likely to vaccinate their children if they were sexually active [23] or older [32,34,[53][54][55]57].  [19] or had a general belief in the efficacy of vaccines [15,24,25,32,45,[48][49][50]62] were more likely to vaccinate (10 studies or 19%). Parents who had refused previous vaccines for their children [11,18,45,47,63] and had concerns about too many vaccinations [45,60] were less likely to vaccinate (6 studies or 11%).

Discussion
This paper reviews the parental knowledge, attitudes, and behaviours toward having their daughters and sons vaccinated against cervical cancer. The parents in these studies were largely from a high resource background. The percentage of parents that participated in these surveys who had heard about HPV clearly rose over time (from 60% in 2005 to 93% in 2009). Parents' appreciation for the link between HPV infection and cervical cancer did rise (70% in 2003 to 91% in 2011). During the era of FDA approval of the vaccines, there appeared to be stronger awareness of the vaccines and this has waned with time. This same pattern is seen with the percentage of parents whose children had received the HPV vaccine (high of 84% in 2010 and now 36% in 2011). Unfortunately, this pattern is also seen with the intention to have a child vaccinated against HPV (peak at 80% in 2008 and now 41% in 2011).
In terms of barriers against the vaccine, parents still have safety and side-effect questions and they want more information. Parents view the vaccine like the oral contraceptive pill; it is best to invest in it only when you become at risk (i.e., you are sexually active). Parents who have high cancer worries and receive strong messages about HPV risks are more likely to advocate for the HPV vaccine. Parents look to their physicians to recommend the vaccine.
The strengths of this study are that it involves information gathered from a large number of parents from several countries. It shows trends in knowledge, attitudes, and behaviours over a time period just preceding the FDA approval of the vaccine; during the approval phase when there were extensive educational campaigns both by the pharmaceutical companies, professional societies, and media, after the FDA approval. The limitations of this study was an inability to validate parental responses, for example, determining how many parents had their child vaccinated with at least one dose of the vaccine.
It will be interesting to see if there are changes in parental attitudes as the types of information about HPV and the HPV vaccine continue to flood the literature. The information about the role of oncogenic HPV in more than cervical cancer is certainly evolving. We are just beginning to grasp the prevention implications of the HPV vaccine in the prevention of anal, oropharengeal, and a proportion of vulvovaginal, and penile cancers. The recent approval of the vaccine in young men may have an impact on decreasing condyloma transmission and having an impact on the rise of anal dysplasia/cancer in the male having sex with male population. As the cervical screening strategy moves toward primary HPV testing, this will also enhance education of the population. Although cost did not emerge as a significant barrier, as the vaccine prices continue to fall, it will be fascinating to see the impact on parental attitudes and behaviour. As public health looks at successful populationbased prevention strategies, it will be interesting to look at parental attitudes toward passive consent versus active consent in school-based vaccination programs. Time will provide information on how durable the vaccine is and longterm sequelae; whether this will influence parental attitudes remains to be seen.
In terms of future implications for policy, when the goal is to preserve the health of the population, certainly the passive consent approach, whether it is for vaccination or cervical screening, seems to be showing profound benefits.
There is preliminary data that shows women who are vaccinated have less need for cervical precancer procedures like biopsies and treatment, however, how this will impact guidelines and availability of such services in the future remains to be seen.

Conclusion
Initial awareness of the virus and the ability of the virus to cause cancer have increased in the time period under study. However, awareness of the vaccine, intent to vaccinate, rates of vaccination rose during the initial introduction of the HPV vaccine but have fallen in subsequent years. Surveys have confirmed that parents want more knowledge and reassurance from their physicians that the HPV vaccine is safe for their children to receive. Policy programs, aimed at increasing HPV vaccination rates as part of an overall HPV strategy to reduce the incidents of cancers and infections caused by the virus, will need to heed the parents' concerns and information needs to be effective.