In 2006, Health Canada approved the first vaccine to prevent Human Papillomavirus (HPV) infection (Gardasil, Merck Frosst Canada Ltd). Gardasil^® is a highly effective quadrivalent HPV vaccine targeting highrisk HPV subtypes 16 and 18 as well as low-risk HPV subtypes 6 and 11 [1-4]. The National Advisory Committee on Immunization (NACI) released a statement in 2007 with the recommendation to vaccinate girls between 9 and 13 years of age for the prevention of infection caused by the HPV subtypes 6, 11, 16, and 18 and their associated diseases like cervical cancer, vulvar and vaginal cancers, genital warts (Condyloma Acuminata, Cervical Adenocarcinoma In Situ (AIS), Cervical Intraepithelial Neoplasia (CIN) grades 1, 2 and 3, vulvar and Vaginal Intraepithelial Neoplasia (VIN) grades 2 and 3 [1]. In February 2010, Gardasil^® was authorized to expand its indications to include males 9 to 26 years of age for the prevention of infection caused by HPV subtypes 6, 11, 16, and 18. In April 2011, Gardasil^® was approved for use in women up to the age of 45 years.

Since then, HPV vaccination programs have become widespread in Canada. On May of 2008, Manitoba has announced the introduction of a HPV immunization program whereby every grade six girl will be vaccinated with Gardasil^®, provided consent from her parent or legal guardian is obtained [4].

HPV immunization programs; through combined primary prevention (immunization) and secondary prevention (screening); are expected to reduce the morbidity and mortality of cervical cancer, its precursors and other HPV-related cancers in women in Canada and to ease the burden of abnormal cytological results providing a high level of vaccine uptake is achieved. Uptake of the HPV vaccine across Canada varies between 50% and 80%, compared to 90% uptake for the Hepatitis B vaccine [5]. In Manitoba, uptake for the complete vaccination series is only 40% [1].

Health care providers are a significant resource to parents regarding the efficacy and safety of vaccines [6,7]. However, there is a paucity of Canadian research about physician attitudes and practice patterns since the approval of the HPV vaccine and the publication of recommendations about its use. Additionally, there is a distinct lack of information about the role of physicians in vaccine uptake when a school-based vaccination program is in place.

We sought to determine the pediatricians’, gynecologists’, and family practitioners’ knowledge, attitudes and practice patterns regarding the HPV vaccine in the context of the NACI recommendation for immunizing the girls aged 9 to 13 years of age and initiation of schoolbased HPV vaccination program in the province of Manitoba (2008).

The College of Physician and Surgeons of Manitoba’s online database was used to obtain mailing addresses for all paediatricians (n=133), obstetrician-gynaecologists (n=67) and family practitioners (n=1064) practicing in Manitoba. Potential participants were excluded at the outset if they were listed as residents/fellows (n=23), had no office mailing address listed (n=23), were retired (n=9), practiced outside of Manitoba (n=2) or were listed as a locum tenens (n=13). In addition, given the large number of family practitioners compared to the other two specialties, the decision was made to select every 3rd family practitioner (after above exclusions) from an alphabetical list to be included in the study (every 3rd of 1013 = 336). In total, 120 paediatricians, 63 obstetrician-gynaecologists and 336 family practitioners were sent a mailing asking for participation in our study by completing the enclosed survey. The surveys sent out the first quarter of 2010.

Ethics approval was obtained from the Research Ethics Board of the University of Manitoba Bannatyne Campus (H2010:059).

The survey consisted of a 43-item questionnaire that comprised six sections assessing: (1) physician demographics (four items); (2) knowledge about HPV (six items); (3) knowledge about the HPV vaccine (eight items); (4) attitudes about the HPV vaccine (nine items); (5) perceived role of the physician with regard to vaccination against HPV (nine items); and, (6) perceived barriers to uptake of the HPV vaccination (seven items). Study questions were adopted from a variety of previously published surveys on this topic [8-10]. Of note, one HPV vaccine knowledge question was excluded from the analysis on account of ambiguity identified by participants through written comments on the returned surveys. To analyze knowledge questions, composite scores were constructed for both HPV knowledge and HPV vaccine knowledge.

Data analysis was performed using SAS (Version 9.2, SAS Institute Inc., Cary N.C.). Descriptive statistics were performed when appropriate. Non-parametric data was analyzed using Chi-squared, Fisher’s Exact Test and the Cochran-Mantel-Haenszel statistical test. Parametric data was analyzed using Wilcoxon scores and the Kruskall- Wallis statistical test. Significance was set at p<0.05.

A total of 114 surveys were returned (22% response rate, Table 1). Of these, six surveys were excluded from the analysis because the respondents had selected “other” or “retired” for type of practice.

Table 1: Population characteristics by specialty.

Population characteristics by specialty

A higher proportion of obstetrician-gynaecologists and paediatricians were female as compared to family practitioners (Table 1). The distribution of years in practice did not vary by specialty (Table 1). Of note, number of years in practice was not found to be associated with any marker of knowledge, belief, perceived role, practice pattern, or perceived barrier to HPV vaccination.

Physician knowledge about HPV and the HPV vaccine

The overall mean score for knowledge about HPV was 4.1 out of 6 (median 4, range 0 to 6). The obstetrician-gynaecologists scored significantly higher (p=0.001) with a mean score of 4.9 (median 5, range 3 to 6), followed by paediatricians (mean 4.2, median 4, range 0 to 6) and family physicians (mean 3.6, median 3, range 1 to 6). HPV knowledge was poorest with regard to whether infections with HPV 6 and 11 were associated with cervical cancer (only 37%, n=40 of respondents answered correctly).

The overall mean score for knowledge about the HPV vaccine was 5.7 out of 7 (median 6, range 2 to 7). Here again, obstetriciangynaecologists scored significantly higher (p=0.03) with a mean score of 6.2 (median 5, range 3 to 7), followed by paediatricians (mean 5.8, median 4, range 0 to 7) and family practitioners (mean 5.3, median 3, range 1 to 6). HPV vaccine knowledge was poorest with regard to whether the vaccine had been approved for use in pregnancy (only 52%, n=56 of respondents answered correctly).

Effect of knowledge on practice patterns

Knowledge was significantly correlated with reported patterns of patient education about the HPV vaccine (Figure 1). Physicians who agreed or strongly agreed with educating eligible patients routinely about the HPV vaccine had higher scores for both HPV knowledge (p=0.0086) and HPV vaccine knowledge (p=0.0004). Conversely, those who responded that they provided education only upon parental request were more likely to have lower scores on HPV knowledge (p=0.0128) and HPV vaccine knowledge (p=0.0084). Knowledge was not significantly associated with any other markers of belief, reported practice pattern or perceived role.

Figure 1: Association between HPV vaccine knowledge and reported patterns of patient education.

Physician beliefs about the HPV vaccine

When considering the target population of the vaccine, the majority of respondents (95.4%) agreed or strongly agreed that the vaccine should be administered to girls before the beginning of sexual activity. Most respondents (66.7%) also agreed or strongly agreed that the HPV vaccine should be given to all sexually active females. A small minority (9.3%) agreed or strongly agreed that the vaccine should only be given to individuals with many sexual partners and a smaller minority (2.8%) supported the statement that vaccination against HPV promotes promiscuity.

In terms of the impact of the HPV vaccine, only a very small proportion of the respondents (3.7%) thought the vaccination would eliminate the need for annual Pap tests. A small minority (6.5%) also supported the idea that the HPV vaccine negatively impact women’s health by giving women a false sense of security.

Perceived role regarding vaccination against HPV

Seventy-three percent of respondents agreed or strongly agreed that much of the responsibility for successful delivery of the HPV vaccine belongs to health care providers. The vast majority of respondents (91.6%) agreed or strongly agreed that individual physicians still play an important role in the uptake of the HPV vaccine even in the context of a school-based vaccination program. Significant differences were detected between specialties with regard to HPV vaccination practices, as outlined in Tables 2 and 3. A few notable differences are worth highlighting. A significantly higher proportion of paediatricians (86.1%) responded that they would recommend the vaccine to all eligible patients compared to obstetrician-gynaecologists and family practitioners (65.2% and 67.4%, respectively, p=0.04). Additionally, paediatricians were more likely to recommend the vaccine and try to persuade those who are reluctant (79.4%) compared to obstetriciangynaecologists and family practitioners (56.5% and 42.9%, respectively, p=0.02).

Table 2: Perceived role and practice patterns with regard to vaccination against HPV as a function of specialty.

Table 3: The effect of gender on beliefs and practice patterns regarding HPV vaccination.

Perceived barriers to the uptake of the HPV vaccine

The vast majority of respondents (88.9%) believed that the high cost to the individual family of vaccinating girls who missed or who were not eligible for the school-based program is an important barrier to vaccine uptake. Other perceived barriers to uptake of the HPV are illustrated in Figure 2.

Figure 2: Perceived Barriers to High Uptake of the HPV Vaccine.

The data presented in this study represents information collected from physicians approximately 1.5 years after a province-wide HPV vaccination program was instated. To the best of our knowledge these findings represent some of the first reports in the literature that consider the perceived role of physicians and practice patterns with regard to the HPV vaccine in the context of a school-based vaccination program. The Manitoba program is somewhat limited in its scope since there are currently no catch up options for girls who do not qualify for the school program (i.e. were born prior to 1997).

The advent of the school-based program fundamentally changed HPV vaccine delivery by removing the need for administration in the physician office. In spite of this paradigm shift, over ninety percent of physicians surveyed agreed that they still have an important role to play in the uptake of the vaccine. The program has likely caused a shift in the perceived physician role toward an educational one, since over half of physicians felt that their primary role was to counsel parents rather than to prescribe the vaccine. In contrast to this statement, our finding that only 67% of physician’s routinely educate about the HPV vaccine suggested discordance between perceived role and actual practice. Of further concern was the finding that only 70% of physicians routinely recommend the vaccine to all eligible patients, which raised concerns over the effectiveness of a “safety net” to capture and catch up those girls missed by the school-based program.

Given that the physician’s role with regard to the HPV vaccine in the context of a school-based vaccination program appears to be the role of educator, it is relevant that we found a strong association between knowledge scores and a physician’s reported propensity to educate about HPV. This appears to support Chow’s report of HPV vaccine knowledge improving likelihood of physicians initiating conversations about the HPV vaccine [11]. There is evidence from influenza immunization that educational interventions aimed at increasing physician vaccine knowledge do increase uptake, but this has yet to be demonstrated with regard to the HPV vaccine [12].

Paediatricians in our study were more likely to (1) recommend the vaccine to all of their eligible patients and were also more likely to (2) try to persuade those who are reluctant compared to obstetriciangynaecologists and family practitioners. These findings may be related to an increased comfort among paediatricians in counseling for immunization in general which may translate well to counseling about the HPV vaccine. A recent study found that the majority of obstetrician-gynaecologists’ surveyed believed that their training with regard to immunizations in general was less than adequate [13,14]. As such, educational campaigns directed at non-paediatricians aimed at improving general immunization counseling competence might increase the propensity to counsel about the vaccine.

Barriers identified are remarkably consistent with previous studies [8-10]. Despite the advent of a school-based vaccination program, the high cost of the vaccine was the most important barrier to high vaccine uptake identified by physicians. While individuals do not incur any personal costs if being vaccinated through the school-based program, physicians surveyed were identifying cost as being a barrier for uptake of the vaccine for those who did not qualify for the school-based vaccination program.

Limitations of our study include a low response rate (22%), which may be related to the use of a traditional mail-based survey rather than an email-based survey owing to the fact that physician email addresses are not centralized in our province. Responder bias is inherent to our survey-based study and as such, gaps in knowledge and propensity to routinely educated and recommend the vaccine might be more significant than our results depict.

Overall these findings are important in confirming that despite a school-based program, physicians still have an important role to play in HPV vaccine delivery, albeit one based more on counseling than delivery. We have identified specific gaps in physician knowledge and practice that could be targeted, but further research is required to determine whether efforts to close these gaps would translate into improved vaccine uptake.