GYNAECOLOGY
HPV Awareness in Higher-Risk Young Women: The Need for a Targeted HPV Catch-Up Vaccination Program Stephanie Ahken, MD,1 Nathalie Fleming, MD, FRCSC,1,2,3,4 Tania Dumont, MD, FRCSC,1,2,3 Amanda Black, MD, MPH, FRCSC1,2,3 Department of Obstetrics and Gynecology and Newborn Care, The Ottawa Hospital, University of Ottawa, Ottawa ON
1
Ottawa Hospital Research Institute, Ottawa ON
2
Division of Gynecology, Children’s Hospital of Eastern Ontario, University of Ottawa, Ottawa ON
3
Children’s Hospital of Eastern Ontario Research Institute, Ottawa ON
4
Abstract
Résumé
Objective: To determine levels of HPV awareness and knowledge in higher-risk young women and their attitudes toward HPV vaccination and catch-up programs.
Objectif : Déterminer le niveau de sensibilisation au VPH et l’état des connaissances à ce sujet chez des jeunes femmes exposées à des risques accrus, ainsi que les attitudes de ces dernières envers la vaccination anti-VPH et les programmes de rattrapage.
Methods: An anonymous, cross-sectional, Internet-based, selfreported questionnaire was completed by women ages 13 to 25 attending two outreach clinics. Primary outcomes were HPV infection/vaccine awareness, vaccination rates, and catch-up program acceptability. Chi-square, Fisher exact test, and logistic regression analyses were performed. Results: Of 105 respondents (mean age 19.32), 66.7% received social assistance and 54.3% relied on walk-in clinics. Overall HPV awareness was 81.0% and vaccine awareness was 76.2%. HPV awareness was significantly higher in women < 20 years old (P = 0.032) and with past sexually transmitted infection (STI) history (P = 0.039) but didn’t differ by education level. Vaccine awareness differed significantly with STI history (P = 0.031) but not by age or education level. Awareness of HPV’s association with genital warts and cervical cancer was low (30.0%, 41.9%) and didn’t differ by education level or sexually transmitted infection history. Thirty percent had been vaccinated (of those, 42% had received 3 doses), mainly in school-based programs (71%). Odds of vaccination were significantly higher in those with a family doctor (OR 8.08). Reasons for not being vaccinated included: “Did not know about it”(28.5%) and “Don’t know” (28.5%). Catch-up program acceptability was high (92.8%, 95.2% if free) and did not differ significantly by age or education level. Conclusion: Higher-risk young women may have high levels of HPV infection/vaccine awareness but lack knowledge of HPV consequences. Those who missed or did not complete HPV vaccination opportunities would support free catch-up vaccination programs in accessible, youth-friendly centres. Key Words: Human papillomavirus, HPV vaccines, awareness, adolescent, youth, high risk, vaccination uptake, community outreach centres Competing Interests: None declared. Received on May 21, 2014 Accepted on August 22, 2014
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Méthodes : Un questionnaire Web d’autoévaluation anonyme et transversal a été rempli par des femmes (âges : 13-25 ans) fréquentant deux cliniques destinées à des groupes mal desservis. La sensibilisation à l’infection au VPH / à la vaccination anti-VPH, les taux de vaccination et l’acceptabilité des programmes de rattrapage constituaient les critères d’évaluation principaux. Le test de chi carré, le test exact de Fisher et des analyses de régression logistique ont été menés. Résultats : Parmi les 105 répondantes (âge moyen : 19,32), 66,7 % recevaient de l’aide sociale et 54,3% avaient recours aux services de cliniques sans rendez-vous. Le taux global de sensibilisation au VPH était de 81,0 % et le taux de sensibilisation à la vaccination était de 76,2 %. La sensibilisation au VPH était considérablement accrue chez les femmes de moins de 20 ans (P = 0,032) et chez celles qui présentaient des antécédents d’infection transmissible sexuellement (ITS) (P = 0,039); toutefois, elle n’était pas affectée par le niveau de scolarité. La sensibilisation à la vaccination variait considérablement en fonction des antécédents d’ITS (P = 0,031), mais non pas en fonction de l’âge ou du niveau de scolarité. La sensibilisation à l’association entre le VPH et les verrues génitales et le cancer du col utérin était faible (30,0 %, 41,9 %) et ne variait ni en fonction du niveau de scolarité ni en fonction des antécédents d’ITS. Trente pour cent des répondantes avaient été vaccinées (chez celles-ci, 42 % avaient reçu trois doses), principalement dans le cadre de programmes scolaires (71 %). La probabilité d’une vaccination était considérablement accrue chez les répondantes qui pouvaient compter sur les services d’un médecin de famille (RC, 8,08). Parmi les raisons expliquant le fait de ne pas avoir été vaccinée, on trouvait les suivantes : « Je n’étais pas au courant » (28,5 %) et « Je ne sais pas » (28,5 %). L’acceptabilité des programmes de rattrapage était élevée (92,8 %, 95,2 % si l’accès était gratuit) et ne variait pas de façon considérable en fonction de l’âge ou du niveau de scolarité.
HPV Awareness in Higher-Risk Young Women: The Need for a Targeted HPV Catch-Up Vaccination Program
Conclusion : Les jeunes femmes exposées à des risques accrus pourraient disposer d’une sensibilisation élevée à l’infection au VPH / à la vaccination anti-VPH, tout en présentant un manque de connaissances quant aux conséquences du VPH. Celles qui n’ont pu se prévaloir d’occasions de se faire vacciner contre le VPH (ou qui n’ont pu terminer un cycle de vaccination anti-VPH) seraient en faveur de l’offre de programmes gratuits de rattrapage de la vaccination au sein de centres accessibles et axés sur la jeunesse. J Obstet Gynaecol Can 2015;37(2):122–128
INTRODUCTION
H
uman papillomavirus is the most common sexually transmitted infection in the world and is known to be a causal factor for both genital warts and cervical cancer.1 Risk factors for HPV infection are younger age (14 to 24 years),2 low educational achievement, low income,3 smoking, single marital status, and increasing numbers of lifetime and recent sexual partners.4,5 The main risk factors for high-grade cervical disease in young women are high parity, lack of cervical screening, and inadequate follow-up care after detection of cervical disease.6 Although highly effective quadrivalent and bivalent vaccines are available in Canada, vaccination rates are low.7,8 Low levels of awareness of HPV infection and its link to cervical cancer, limited access to information and health care providers, and financial restrictions are associated with lower vaccination rates.9,10 Currently in Ontario, a government-funded program provides free quadrivalent HPV vaccinations to all consenting Grade 8 females. This program was implemented in 2007. Across Canada, similar programs exist for routine HPV vaccination in school. Depending on the province or territory, it may be given to females in Grades 4 to 8.11 In 2012, a catch-up vaccination program was implemented for girls in Grades 9 to 12 in Ontario who did not receive or complete their HPV immunization series in Grade 8. In order to receive the vaccine, these young women must personally contact their local public health unit and book an appointment. The Ottawa Hospital has established two satellite outreach clinics for young women in Ottawa. Young women attending these clinics at St. Mary’s Young Parent Outreach Centre and Youville Centre have many risk factors for HPV infection and are thus a higher-risk population. They also come from more socioeconomically disadvantaged backgrounds and may lack access to certain health care services. Thus they could benefit significantly from a funded HPV vaccination program in an accessible setting. At this time, funded HPV vaccination programs only exist for girls in Grades 8 to 12 and rely on school attendance. They also rely on personal knowledge of available
public health resources and motivation to seek catch-up vaccination through public health units. These may be significant barriers to vaccinating higher-risk populations such as those attending St-Mary’s Young Parent Outreach Centre and Youville Centre. The objectives of this study were to determine and assess the levels of knowledge and awareness of HPV infection and vaccination in higher-risk young women attending outreach clinics, their attitudes towards HPV vaccination, factors influencing HPV vaccination rates, and the need for and acceptability of an HPV vaccination program in an outreach setting. METHODS
An anonymous, cross-sectional survey was conducted between May 2012 and February 2013. Young women (13 to 25 years old) attending outreach clinics at St. Mary’s Young Parent Outreach Centre and Youville Centre in Ottawa were asked to complete an anonymous, cross-sectional, Internet-based, self-reported questionnaire (eAppendix). The questionnaire was completed on-site at the outreach clinics on either an iPad or a computer supplied by the investigators. Subjects provided informed consent. The survey was administered in French or English according to the respondent’s preference. The primary outcomes were rates of awareness of HPV infection and the HPV vaccine, rates of vaccination, and acceptability of an HPV vaccination catch-up program. Percentages of awareness of HPV infection, awareness of the HPV vaccine, vaccination rates, and catch-up vaccination program acceptability were calculated by age, education level, and past sexually transmitted infection (STI) history. Chi-square test and Fisher exact test were performed to detect within group differences. Logistic regression analyses were performed to determine the likelihood of HPV vaccination adjusted for age, smoking, and drug use. Data analysis was performed using SAS software version 9.2 (SAS Institute Inc., Cary, NC). The study was approved by The Ottawa Hospital Research Ethics Board and The Children’s Hospital of Eastern Ontario Research Ethics Board. RESULTS
A total of 105 subjects were recruited. Mean age (± SD) was 19.32 ± 2.20 years (range 13 to 25). The demographic characteristics of the respondents are summarized in Table 1. Additional characteristics identified as potential risk factors for HPV infection and/or low vaccination FEBRUARY JOGC FÉVRIER 2015 l 123
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Table 1. Demographic characteristics of respondents (n = 105) Characteristics
Proportion of respondents, %
Age, years < 20
55.2
≥ 20
42.9
Relationship status Dating but living alone or with family
37.1
Common-law or living with partner
30.5
Married
1.0
Not in a relationship
28.6
Living situation With parents
33.3
With partner
22.9
Alone
27.6
With roommates
2.9
In a shelter
1.0
At St. Mary’s Home
4.8
Current/highest level of education Less than Grade 8
1.9
Grade 8 to 12
85.7
Higher than Grade 12
11.4
*Not all columns add to 100% because of missing data for some questions or respondents could check all that apply
Table 2. HPV risk factors in respondents (n = 105) Specific risk factors
Proportion of respondents, %
Not in school
42.8
Smoker
45.7
Drug use
4.8
Number of lifetime sexual partners 1 to 5
54.2
6 to 10
19.1
> 10
19.1
Uses contraception
60.0
Previous pregnancy
85.7
≥ 2 previous pregnancies
48.6
Prior history of STI
33.3
Receiving social assistance
66.7
No family doctor
20.0
Rely on walk-in clinics for health concerns
54.3
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rates are summarized in Table 2. More than one third (37.1%) stated that they did not have health insurance and 66.7% were on social assistance. Over 19% of respondents had had more than 10 lifetime sexual partners, 33.3% had previously had an STI, 45.7% were smokers, 85.7% had previously been pregnant, and 42.9% were no longer in school. Although 74.3% stated that they had a family physician, 54.3% of respondents relied on walk-in clinics for health concerns. Awareness of HPV Infection and the HPV Vaccine
Awareness of HPV infection was determined by the question “Have you ever heard of HPV (human papillomavirus)?” Overall awareness of HPV infection was 81.0% and was significantly affected by age (P = 0.032) and by STI history (P = 0.039) but not by education level (Table 3). Women less than 20 years old and those with a history of STI infection were more likely to be aware of HPV infection. Awareness of genital warts (89.5%) and cervical cancer (93.3%) was high. Awareness of HPV vaccination was determined by the question “Have you ever heard of the HPV vaccine?” Overall, 76.2% of respondents were aware of the HPV vaccine. HPV vaccine awareness was significantly higher in those with a previous history of an STI (P = 0.031) but did not differ by age or education level (Table 3). Of those who were aware of HPV infection, the most common sources of information were school (67.0%), a doctor or nurse (58.9%), and family or friends (41.1%) (Table 4). Of those who were aware of the HPV vaccine, common sources of information included school (66.3%) and health care providers (56.3%). Awareness of HPV’s Association With Genital Warts and Cervical Cancer
Awareness of HPV’s association with genital warts and cervical cancer was determined by agreement with the statements “Genital warts are caused by HPV” and “Cervical cancer is caused by HPV.” Only 29.5% of respondents were aware that HPV was associated with genital warts, while 41.9% were aware that HPV is associated with cervical cancer. Awareness of the association between HPV and genital warts was not significantly affected by age, education level, or STI history (Table 5). Awareness of the association between HPV and cervical cancer was significantly higher in those > 20 years of age (P = 0.036) but did not differ by education level or STI history (Table 5). Although 80% agreed that it was important to have Pap smears, only 64.8% knew that these were used to screen for cervical cancer.
HPV Awareness in Higher-Risk Young Women: The Need for a Targeted HPV Catch-Up Vaccination Program
Table 3. Awareness of HPV infection and HPV vaccine Variable
Aware of HPV infection, %
Age < 20 years
87.9
Age ≥ 20 years
71.1
Education level < Grade 10
92.9
Education level ≥ Grade 10
78.9
History of STI
91.4
No history of STI
74.2
P 0.032 0.30 0.039
Aware of HPV vaccination, %
P
82.5
0.11
68.9 85.7
0.51
75.3 88.6
0.031
69.2
Table 4. Sources of knowledge of HPV infection and HPV vaccine Source
HPV infection* (n = 85) n (%)
HPV vaccine* (n = 80) n (%)
School
57 (67.0)
53 (66.3)
Doctor or nurse
50 (58.9)
45 (56.3)
Family or friends
35 (41.1)
30 (37.5)
Commercial advertising
32 (37.6)
28 (35.0)
Internet
17 (20.0)
17 (21.2)
*Subjects were asked to indicate all that apply
Table 5. Awareness of HPV’s association with genital warts and cervical cancer Variable
Agree that genital warts are caused by HPV, %
Age < 20 years
22.4
Age ≥ 20 years
40.0
Education level < Grade 10
35.7
Education level ≥ Grade 10
27.8
History of STI
42.9
No history of STI
24.2
P 0.05 0.54 0.05
Agree that cervical cancer is caused by HPV, % 32.8
P 0.036
53.3 21.4
0.10
44.4 45.7
0.64
40.9
Table 6. Likelihood of HPV vaccination Number of women vaccinated (n = 31) n (%)
Adjusted odds ratio* (95% CI)
Has a family doctor
26 (53.1)
8.077 (1.4 to 47.1)
Has health insurance
17 (54.8)
1.6 (0.4 to 5.7)
Education ≥ Grade 10
24 (42.9)
0.6 (0.1 to 3.4)
History of pregnancy
22 (40.0)
1.7 (0.3 to 10.6)
History of STI
12 (52.2)
3.4 (0.9 to 13.0)
Characteristics
*Adjusted for age, smoking, and drug use
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Table 7. Reasons for not receiving HPV vaccine* Percentage n = 35 Did not know about it
28.5
Do not know
28.5
Too expensive/no insurance to pay for it
20.0
Too old to get it in school
17.1
Not available in school
11.4
Did not know how to get it
11.4
*Subjects were asked to indicate all that apply
Vaccination Rates
Vaccination rates were 29.5%. Amongst those vaccinated, only 41.9% had completed the three-dose course, although 29.0% were not sure whether they had completed the vaccination course or not. Of the 31 respondents who received the vaccine, 70.9% had received it in school and 16.1% had received it from their family physician. Vaccination rates did not differ significantly by age, education level, or STI history. The odds of vaccination were significantly higher for those who reported having a family doctor (aOR = 8.077; 95% CI 1.4 to 47.1) (Table 6). The main reasons for not being vaccinated are summarized in Table 7. Acceptability of an HPV Vaccination Program
Eighty-five percent (84.8%) of respondents agreed that they should reduce their chances of developing genital warts. Ninety-three percent (92.8%) of respondents were willing to receive the HPV vaccine if it was available at the outreach centres, and this acceptability increased to 95.2% if it could be provided free of charge. Willingness to receive the vaccine was not significantly affected by age, education level, STI history, or health insurance status. Acceptability of HPV vaccination did not change significantly after reading a structured paragraph containing information on HPV (P = 0.104). When asked how they would like to receive information on sexual health (e.g., STIs, vaccines, contraception, HPV), 63.8% stated they would like it on a one-to-one basis, 33.3% would like group talks given by a doctor or nurse, and 27.6% would like group talks given at the outreach centres. DISCUSSION
Although the average age of first intercourse in Canada is 16.5 years, the highest rates of STIs occur in the 15to 24-year-old age group.12 The human papillomavirus is associated with genital warts, cervical dysplasia, and cervical cancer, and hence can cause significant costs for the individual and society. In the United States, youth 126 l FEBRUARY JOGC FÉVRIER 2015
aged 15 to 24 years account for nearly 50% of new HPV infections, which corresponds to an incidence of over seven million new cases each year.10 The estimated total annual cost of HPV infection in young women (aged 15 to 24) is US$2.8 billion.13 There has been limited research on the burden of HPV infection in higher-risk youth populations such as those with a high number of sexual partners and increased pregnancy rates. The HPV vaccine has the potential to significantly decrease the burden of disease in women, perhaps even more so in young women who are socioeconomically disadvantaged. However, in order to target higher-risk youth effectively, we must determine the factors and limitations affecting HPV vaccination in these populations. This allows us to develop appropriate public health strategies and programs to increase HPV vaccination rates in higher-risk populations, thereby decreasing the burden of HPV in this population and decreasing HPVrelated costs to our health care system. The young women in our outreach centres have many demographic characteristics that put them at higher risk for HPV acquisition. Unfortunately, these same characteristics may be associated with difficulty accessing health care services, including HPV vaccination programs. Although the higher-risk young women in our study had high levels of awareness of HPV infection and the HPV vaccine, they lacked knowledge of the consequences of HPV infection. Giede et al. have shown that although many young women rank their knowledge of HPV as very good, few are able to correctly answer questions regarding methods of preventing HPV.14 Schools and social media have attempted to increase public awareness of HPV but further efforts are likely needed to educate the public on HPV’s causal relationship with cervical cancer and genital warts and consequently to increase knowledge of the role of HPV vaccination in the prevention of HPV-related diseases. Interestingly, awareness of HPV infection in our study was higher in those less than 20 years old, but participants over the age of 20 were more aware of HPV’s causal relation with cervical cancer. The introduction of school-based HPV vaccination programs may explain the increased awareness of HPV infection in those less than 20 years old. Although those more than 20 years old were less aware of HPV infection overall, they were more aware of HPV’s consequences. In addition, knowledge of HPV infection and vaccination was higher in participants with a prior history of STI. Although the association between STI history and awareness of HPV has not been addressed in prior studies, our findings are not surprising given that these young women, in the context of their STI diagnosis,
HPV Awareness in Higher-Risk Young Women: The Need for a Targeted HPV Catch-Up Vaccination Program
may have had more counselling with regard to HPV and the HPV vaccine. In our study, HPV vaccination acceptability was high, especially if it was given in accessible and youth-friendly centres. Acceptability was not affected by age, education level, STI history, or health insurance status. Lenehan et al. similarly found that women were strongly supportive of HPV vaccination and that this interest was unrelated to HPV knowledge, level of education, or number of previous sexual partners.15 In general, previous studies have repeatedly demonstrated that youth populations have low levels of awareness of HPV infection and vaccination but high acceptance of the HPV vaccine.16–18 Vaccination status may be dependent on schooling, awareness, access to health care, and health care provider counselling. Previous studies have found that one of the most important factors predicting HPV vaccination uptake in young women is recommendation by a physician.15–19 Young women in our study who had a family doctor were more likely to be vaccinated against HPV than those who did not have a family doctor. Rosenthal et al. also concluded that the strength of the recommendation by a physician played a significant role in the young women’s decision to be vaccinated.19 These authors demonstrated a four-fold greater likelihood of HPV vaccination in women who received a strong recommendation compared with those who received a less strong recommendation.19 Physician access is definitely a key factor affecting HPV vaccination uptake in higher-risk young women. Unfortunately, vaccination rates in our higher-risk young women were low. A variety of reasons were cited for the lack of immunization. It is interesting that vaccination rates are low, even in the presence of school-based government-funded HPV vaccination programs. There are many possible reasons for the low HPV vaccination rates in our cohort. Some of the respondents may have missed the publicly funded vaccination program when it was implemented for Grade 8 students in 2007 because they had already completed Grade 8. In addition, parental consent is required for school-based vaccination, and only 37% of young women in our study lived with their parents. Furthermore, these young women may have missed the vaccination opportunities in school because of high-risk behaviours that may be associated with truancy. Although school-based programs may succeed in vaccinating some low-risk youth against HPV, other strategies are needed to target the higher-risk youth who may lack access and vaccination opportunities because of social circumstances and socioeconomic disadvantages. Implementing a free catch-up vaccination program in a youth-friendly
setting such as our outreach clinics at St. Mary’s Young Parent Outreach Centre and Youville Centre may help to target and increase vaccination rates in these higher-risk populations. This study has demonstrated that while HPV vaccination rates are low, higher-risk young women are very supportive of free catch-up vaccination programs in accessible, youth-friendly outreach centres. Our study is one of the few to address issues and barriers that contribute to low HPV vaccination rates in higher-risk youth populations and is the only study to date to have targeted higher-risk young women in Ontario, specifically those in outreach centres. Limitations of the study include selection bias (inclusion of young women already attending medical clinics in outreach centres), recall bias (HPV vaccination history and number of doses received), and the small sample size. Future research that assesses the effect and success of vaccination programs targeting higher-risk youth will allow public health policy makers to determine the most effective strategy for vaccinating higher-risk populations and decreasing the burden of HPV. CONCLUSION
Higher-risk young women may have high levels of HPV infection and HPV vaccination awareness but lack knowledge of HPV consequences. Those who missed or did not complete HPV vaccination opportunities would support free catch-up vaccination programs in accessible, youth-friendly centres. The findings of this study support the development of targeted public health strategies and interventions regarding HPV vaccination. The implementation of an outreach catch-up vaccination program for higher-risk populations allows for access in a friendly and non-judgemental setting, and could significantly increase HPV vaccination rates in this population. This may ultimately contribute to improving long-term health outcomes, and in the future help to decrease the burden of genital warts and cervical dysplasia/cancer on our health care system. ACKNOWLEDGEMENTS
The authors wish to acknowledge the contributions of Tinghua Zhang who performed the statistical analysis for this paper. REFERENCES 1. Franco EL, Duarte-Franco E, Ferenczy, A. Cervical cancer: epidemiology, prevention and the role of human papillomavirus infection. CMAJ 2001;164(7):1017–25.
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2. Hariri S, Unger ER, Sternberg M, Dunne EF, Swan D, Patel S, Markowitz LE. Prevalence of genital human papillomavirus among females in the United States, the National Health and Nutrition Examination Survey, 2003–2006. J Infect Dis 2011;204(4):566–73. 3. Kahn JA, Lan D, Kahn RS. Sociodemographic factors associated with high-risk human papillomavirus infection. Obstet Gynecol 2007;110(3):713. 4. Dunne EF, Sternberg M, Markowitz LE, McQuillan G, Swan D, Patel S, et al. Human papillomavirus (HPV) 6, 11, 16, and 18 prevalence among females in the United States—National Health And Nutrition Examination Survey, 2003–2006: opportunity to measure HPV vaccine impact? J Infect Dis 2011;204(4):562–5. 5. Roteli-Martins CM, de Carvalho NS, Naud P, Teixeira J, Borba P, Derchain S, et al. Prevalence of human papillomavirus infection and associated risk factors in young women in Brazil, Canada, and the United States: a multicenter cross-sectional study. Int J Gynecol Pathol 2011;30(2):173–84. 6. Almonte M, Ferreccio C, Gonzales M, Delgado JM, Buckley CH, Luciani S, et al. Risk factors for high-risk human papillomavirus infection and cofactors for high-grade cervical disease in Peru. Int J Gynecol Cancer 2011;21:1654–63. 7. Smith LM, Brassard P, Kwong JC, Deeks SL, Ellis AK, Lévesque LE. Factors associated with initiation and completion of the quadrivalent human papillomavirus vaccine series in an Ontario cohort of grade 8 girls. BMC Public Health 2011;11:645.
11. National Advisory Committee on Immunization (NACI). Update on Human Papillomavirus (HPV) Vaccines. Canada Communicable Disease Report. 2012. 38. 12. Rotermann M. Sex, condoms and STDs among young people. Statistics Canada. Health Reports. 2005;16(3):39–45. 13. Chesson HW, Blandford JM, Gift TL, Tao G, Irwin KL. The estimated direct medical cost of sexually transmitted diseases among American youth, 2000. Perspect Sex Reprod Health 2004;36(1):11–9. 14. Giede C, McFadden LL, Komonoski P, Agrawal A, Stauffer A, Pierson R. The acceptability of HPV vaccination among women attending the University of Saskatchewan Student Health Services. J Obstet Gynaecol Can 2010;32(7):679–86. 15. Lenehan JG, Leonard KC, Nandra S, Isaacs CR, Mathew A, Fisher W. Women’s knowledge, attitudes, and intentions concerning human papillomavirus vaccination: findings of a waiting room survey of obstetrics-gynaecology outpatients. J Obstet Gynaecol Can 2008;30(6):489–99. 16. Price RA, Tiro JA, Saraiya M, Meissner H, Breen N. Use of human papillomavirus vaccines among young adult women in the United States: an analysis of the 2008 National Health Interview Survey. Cancer 2011;117(24):5560–8.
8. Shearer BD. HPV vaccination: understanding the impact on HPV disease. National Collaborating Centre for Infectious Diseases. Purple Paper no.34, 2011 Dec.
17. Sundstrom K, Tran TN, Lundholm C, Young C, Sparen P, Dahlstrom LA. Acceptability of HPV vaccination among young adults aged 18–30 years: a population based survey in Sweden. Vaccine 2010;28(47):7492–500.
9. Agius PA, Pitts MK, Smith AM. Mitchell A. Human papillomavirus and cervical cancer: Gardasil® vaccination status and knowledge amongst a nationally representative sample of Australian secondary school students. Vaccine 2010;28(27):4416–22.
18. Williams K, Forster A, Marlow L, Walker J. Attitudes towards human papillomavirus vaccination: a qualitative study of vaccinated and unvaccinated girls aged 17–18 years. J Fam Plann Reprod Health Care 2011;37:22–5.
10. Satterwhite CL, Terrone E, Meites E, Dunne E, Mahajan R, Ocfemia M, et al. Sexually transmitted infections among U.S. women and men: prevalence and incidence estimates, 2008. Sex Transm Dis 2013;40(3):187–93.
19. Rosenthal SL, Weiss TW, Zimet GD, Ma L, Good MB, Vichnin, MD. Predictors of HPV vaccine uptake among women aged 19–26: Importance of a physician’s recommendation. Vaccine 2011;29(5):890–5.
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HPV Awareness in Higher-Risk Young Women: The Need for a Targeted HPV Catch-Up Vaccination Program Stephanie Ahken, MD,1 Nathalie Fleming, MD, FRCSC,1,2,3,4 Tania Dumont, MD, FRCSC,1,2,3 Amanda Black, MD, MPH, FRCSC1,2,3 Department of Obstetrics and Gynecology and Newborn Care, The Ottawa Hospital, University of Ottawa, Ottawa ON
1
Ottawa Hospital Research Institute, Ottawa ON
2
Division of Gynecology, Children’s Hospital of Eastern Ontario, University of Ottawa, Ottawa ON
3
Children’s Hospital of Eastern Ontario Research Institute, Ottawa ON
4
Abstract
Résumé
Objective: To determine levels of HPV awareness and knowledge in higher-risk young women and their attitudes toward HPV vaccination and catch-up programs.
Objectif : Déterminer le niveau de sensibilisation au VPH et l’état des connaissances à ce sujet chez des jeunes femmes exposées à des risques accrus, ainsi que les attitudes de ces dernières envers la vaccination anti-VPH et les programmes de rattrapage.
Methods: An anonymous, cross-sectional, Internet-based, selfreported questionnaire was completed by women ages 13 to 25 attending two outreach clinics. Primary outcomes were HPV infection/vaccine awareness, vaccination rates, and catch-up program acceptability. Chi-square, Fisher exact test, and logistic regression analyses were performed. Results: Of 105 respondents (mean age 19.32), 66.7% received social assistance and 54.3% relied on walk-in clinics. Overall HPV awareness was 81.0% and vaccine awareness was 76.2%. HPV awareness was significantly higher in women < 20 years old (P = 0.032) and with past sexually transmitted infection (STI) history (P = 0.039) but didn’t differ by education level. Vaccine awareness differed significantly with STI history (P = 0.031) but not by age or education level. Awareness of HPV’s association with genital warts and cervical cancer was low (30.0%, 41.9%) and didn’t differ by education level or sexually transmitted infection history. Thirty percent had been vaccinated (of those, 42% had received 3 doses), mainly in school-based programs (71%). Odds of vaccination were significantly higher in those with a family doctor (OR 8.08). Reasons for not being vaccinated included: “Did not know about it”(28.5%) and “Don’t know” (28.5%). Catch-up program acceptability was high (92.8%, 95.2% if free) and did not differ significantly by age or education level. Conclusion: Higher-risk young women may have high levels of HPV infection/vaccine awareness but lack knowledge of HPV consequences. Those who missed or did not complete HPV vaccination opportunities would support free catch-up vaccination programs in accessible, youth-friendly centres. Key Words: Human papillomavirus, HPV vaccines, awareness, adolescent, youth, high risk, vaccination uptake, community outreach centres Competing Interests: None declared. Received on May 21, 2014 Accepted on August 22, 2014
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Méthodes : Un questionnaire Web d’autoévaluation anonyme et transversal a été rempli par des femmes (âges : 13-25 ans) fréquentant deux cliniques destinées à des groupes mal desservis. La sensibilisation à l’infection au VPH / à la vaccination anti-VPH, les taux de vaccination et l’acceptabilité des programmes de rattrapage constituaient les critères d’évaluation principaux. Le test de chi carré, le test exact de Fisher et des analyses de régression logistique ont été menés. Résultats : Parmi les 105 répondantes (âge moyen : 19,32), 66,7 % recevaient de l’aide sociale et 54,3% avaient recours aux services de cliniques sans rendez-vous. Le taux global de sensibilisation au VPH était de 81,0 % et le taux de sensibilisation à la vaccination était de 76,2 %. La sensibilisation au VPH était considérablement accrue chez les femmes de moins de 20 ans (P = 0,032) et chez celles qui présentaient des antécédents d’infection transmissible sexuellement (ITS) (P = 0,039); toutefois, elle n’était pas affectée par le niveau de scolarité. La sensibilisation à la vaccination variait considérablement en fonction des antécédents d’ITS (P = 0,031), mais non pas en fonction de l’âge ou du niveau de scolarité. La sensibilisation à l’association entre le VPH et les verrues génitales et le cancer du col utérin était faible (30,0 %, 41,9 %) et ne variait ni en fonction du niveau de scolarité ni en fonction des antécédents d’ITS. Trente pour cent des répondantes avaient été vaccinées (chez celles-ci, 42 % avaient reçu trois doses), principalement dans le cadre de programmes scolaires (71 %). La probabilité d’une vaccination était considérablement accrue chez les répondantes qui pouvaient compter sur les services d’un médecin de famille (RC, 8,08). Parmi les raisons expliquant le fait de ne pas avoir été vaccinée, on trouvait les suivantes : « Je n’étais pas au courant » (28,5 %) et « Je ne sais pas » (28,5 %). L’acceptabilité des programmes de rattrapage était élevée (92,8 %, 95,2 % si l’accès était gratuit) et ne variait pas de façon considérable en fonction de l’âge ou du niveau de scolarité.
HPV Awareness in Higher-Risk Young Women: The Need for a Targeted HPV Catch-Up Vaccination Program
Conclusion : Les jeunes femmes exposées à des risques accrus pourraient disposer d’une sensibilisation élevée à l’infection au VPH / à la vaccination anti-VPH, tout en présentant un manque de connaissances quant aux conséquences du VPH. Celles qui n’ont pu se prévaloir d’occasions de se faire vacciner contre le VPH (ou qui n’ont pu terminer un cycle de vaccination anti-VPH) seraient en faveur de l’offre de programmes gratuits de rattrapage de la vaccination au sein de centres accessibles et axés sur la jeunesse. J Obstet Gynaecol Can 2015;37(2):122–128
INTRODUCTION
H
uman papillomavirus is the most common sexually transmitted infection in the world and is known to be a causal factor for both genital warts and cervical cancer.1 Risk factors for HPV infection are younger age (14 to 24 years),2 low educational achievement, low income,3 smoking, single marital status, and increasing numbers of lifetime and recent sexual partners.4,5 The main risk factors for high-grade cervical disease in young women are high parity, lack of cervical screening, and inadequate follow-up care after detection of cervical disease.6 Although highly effective quadrivalent and bivalent vaccines are available in Canada, vaccination rates are low.7,8 Low levels of awareness of HPV infection and its link to cervical cancer, limited access to information and health care providers, and financial restrictions are associated with lower vaccination rates.9,10 Currently in Ontario, a government-funded program provides free quadrivalent HPV vaccinations to all consenting Grade 8 females. This program was implemented in 2007. Across Canada, similar programs exist for routine HPV vaccination in school. Depending on the province or territory, it may be given to females in Grades 4 to 8.11 In 2012, a catch-up vaccination program was implemented for girls in Grades 9 to 12 in Ontario who did not receive or complete their HPV immunization series in Grade 8. In order to receive the vaccine, these young women must personally contact their local public health unit and book an appointment. The Ottawa Hospital has established two satellite outreach clinics for young women in Ottawa. Young women attending these clinics at St. Mary’s Young Parent Outreach Centre and Youville Centre have many risk factors for HPV infection and are thus a higher-risk population. They also come from more socioeconomically disadvantaged backgrounds and may lack access to certain health care services. Thus they could benefit significantly from a funded HPV vaccination program in an accessible setting. At this time, funded HPV vaccination programs only exist for girls in Grades 8 to 12 and rely on school attendance. They also rely on personal knowledge of available
public health resources and motivation to seek catch-up vaccination through public health units. These may be significant barriers to vaccinating higher-risk populations such as those attending St-Mary’s Young Parent Outreach Centre and Youville Centre. The objectives of this study were to determine and assess the levels of knowledge and awareness of HPV infection and vaccination in higher-risk young women attending outreach clinics, their attitudes towards HPV vaccination, factors influencing HPV vaccination rates, and the need for and acceptability of an HPV vaccination program in an outreach setting. METHODS
An anonymous, cross-sectional survey was conducted between May 2012 and February 2013. Young women (13 to 25 years old) attending outreach clinics at St. Mary’s Young Parent Outreach Centre and Youville Centre in Ottawa were asked to complete an anonymous, cross-sectional, Internet-based, self-reported questionnaire (eAppendix). The questionnaire was completed on-site at the outreach clinics on either an iPad or a computer supplied by the investigators. Subjects provided informed consent. The survey was administered in French or English according to the respondent’s preference. The primary outcomes were rates of awareness of HPV infection and the HPV vaccine, rates of vaccination, and acceptability of an HPV vaccination catch-up program. Percentages of awareness of HPV infection, awareness of the HPV vaccine, vaccination rates, and catch-up vaccination program acceptability were calculated by age, education level, and past sexually transmitted infection (STI) history. Chi-square test and Fisher exact test were performed to detect within group differences. Logistic regression analyses were performed to determine the likelihood of HPV vaccination adjusted for age, smoking, and drug use. Data analysis was performed using SAS software version 9.2 (SAS Institute Inc., Cary, NC). The study was approved by The Ottawa Hospital Research Ethics Board and The Children’s Hospital of Eastern Ontario Research Ethics Board. RESULTS
A total of 105 subjects were recruited. Mean age (± SD) was 19.32 ± 2.20 years (range 13 to 25). The demographic characteristics of the respondents are summarized in Table 1. Additional characteristics identified as potential risk factors for HPV infection and/or low vaccination FEBRUARY JOGC FÉVRIER 2015 l 123
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Table 1. Demographic characteristics of respondents (n = 105) Characteristics
Proportion of respondents, %
Age, years < 20
55.2
≥ 20
42.9
Relationship status Dating but living alone or with family
37.1
Common-law or living with partner
30.5
Married
1.0
Not in a relationship
28.6
Living situation With parents
33.3
With partner
22.9
Alone
27.6
With roommates
2.9
In a shelter
1.0
At St. Mary’s Home
4.8
Current/highest level of education Less than Grade 8
1.9
Grade 8 to 12
85.7
Higher than Grade 12
11.4
*Not all columns add to 100% because of missing data for some questions or respondents could check all that apply
Table 2. HPV risk factors in respondents (n = 105) Specific risk factors
Proportion of respondents, %
Not in school
42.8
Smoker
45.7
Drug use
4.8
Number of lifetime sexual partners 1 to 5
54.2
6 to 10
19.1
> 10
19.1
Uses contraception
60.0
Previous pregnancy
85.7
≥ 2 previous pregnancies
48.6
Prior history of STI
33.3
Receiving social assistance
66.7
No family doctor
20.0
Rely on walk-in clinics for health concerns
54.3
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rates are summarized in Table 2. More than one third (37.1%) stated that they did not have health insurance and 66.7% were on social assistance. Over 19% of respondents had had more than 10 lifetime sexual partners, 33.3% had previously had an STI, 45.7% were smokers, 85.7% had previously been pregnant, and 42.9% were no longer in school. Although 74.3% stated that they had a family physician, 54.3% of respondents relied on walk-in clinics for health concerns. Awareness of HPV Infection and the HPV Vaccine
Awareness of HPV infection was determined by the question “Have you ever heard of HPV (human papillomavirus)?” Overall awareness of HPV infection was 81.0% and was significantly affected by age (P = 0.032) and by STI history (P = 0.039) but not by education level (Table 3). Women less than 20 years old and those with a history of STI infection were more likely to be aware of HPV infection. Awareness of genital warts (89.5%) and cervical cancer (93.3%) was high. Awareness of HPV vaccination was determined by the question “Have you ever heard of the HPV vaccine?” Overall, 76.2% of respondents were aware of the HPV vaccine. HPV vaccine awareness was significantly higher in those with a previous history of an STI (P = 0.031) but did not differ by age or education level (Table 3). Of those who were aware of HPV infection, the most common sources of information were school (67.0%), a doctor or nurse (58.9%), and family or friends (41.1%) (Table 4). Of those who were aware of the HPV vaccine, common sources of information included school (66.3%) and health care providers (56.3%). Awareness of HPV’s Association With Genital Warts and Cervical Cancer
Awareness of HPV’s association with genital warts and cervical cancer was determined by agreement with the statements “Genital warts are caused by HPV” and “Cervical cancer is caused by HPV.” Only 29.5% of respondents were aware that HPV was associated with genital warts, while 41.9% were aware that HPV is associated with cervical cancer. Awareness of the association between HPV and genital warts was not significantly affected by age, education level, or STI history (Table 5). Awareness of the association between HPV and cervical cancer was significantly higher in those > 20 years of age (P = 0.036) but did not differ by education level or STI history (Table 5). Although 80% agreed that it was important to have Pap smears, only 64.8% knew that these were used to screen for cervical cancer.
HPV Awareness in Higher-Risk Young Women: The Need for a Targeted HPV Catch-Up Vaccination Program
Table 3. Awareness of HPV infection and HPV vaccine Variable
Aware of HPV infection, %
Age < 20 years
87.9
Age ≥ 20 years
71.1
Education level < Grade 10
92.9
Education level ≥ Grade 10
78.9
History of STI
91.4
No history of STI
74.2
P 0.032 0.30 0.039
Aware of HPV vaccination, %
P
82.5
0.11
68.9 85.7
0.51
75.3 88.6
0.031
69.2
Table 4. Sources of knowledge of HPV infection and HPV vaccine Source
HPV infection* (n = 85) n (%)
HPV vaccine* (n = 80) n (%)
School
57 (67.0)
53 (66.3)
Doctor or nurse
50 (58.9)
45 (56.3)
Family or friends
35 (41.1)
30 (37.5)
Commercial advertising
32 (37.6)
28 (35.0)
Internet
17 (20.0)
17 (21.2)
*Subjects were asked to indicate all that apply
Table 5. Awareness of HPV’s association with genital warts and cervical cancer Variable
Agree that genital warts are caused by HPV, %
Age < 20 years
22.4
Age ≥ 20 years
40.0
Education level < Grade 10
35.7
Education level ≥ Grade 10
27.8
History of STI
42.9
No history of STI
24.2
P 0.05 0.54 0.05
Agree that cervical cancer is caused by HPV, % 32.8
P 0.036
53.3 21.4
0.10
44.4 45.7
0.64
40.9
Table 6. Likelihood of HPV vaccination Number of women vaccinated (n = 31) n (%)
Adjusted odds ratio* (95% CI)
Has a family doctor
26 (53.1)
8.077 (1.4 to 47.1)
Has health insurance
17 (54.8)
1.6 (0.4 to 5.7)
Education ≥ Grade 10
24 (42.9)
0.6 (0.1 to 3.4)
History of pregnancy
22 (40.0)
1.7 (0.3 to 10.6)
History of STI
12 (52.2)
3.4 (0.9 to 13.0)
Characteristics
*Adjusted for age, smoking, and drug use
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Table 7. Reasons for not receiving HPV vaccine* Percentage n = 35 Did not know about it
28.5
Do not know
28.5
Too expensive/no insurance to pay for it
20.0
Too old to get it in school
17.1
Not available in school
11.4
Did not know how to get it
11.4
*Subjects were asked to indicate all that apply
Vaccination Rates
Vaccination rates were 29.5%. Amongst those vaccinated, only 41.9% had completed the three-dose course, although 29.0% were not sure whether they had completed the vaccination course or not. Of the 31 respondents who received the vaccine, 70.9% had received it in school and 16.1% had received it from their family physician. Vaccination rates did not differ significantly by age, education level, or STI history. The odds of vaccination were significantly higher for those who reported having a family doctor (aOR = 8.077; 95% CI 1.4 to 47.1) (Table 6). The main reasons for not being vaccinated are summarized in Table 7. Acceptability of an HPV Vaccination Program
Eighty-five percent (84.8%) of respondents agreed that they should reduce their chances of developing genital warts. Ninety-three percent (92.8%) of respondents were willing to receive the HPV vaccine if it was available at the outreach centres, and this acceptability increased to 95.2% if it could be provided free of charge. Willingness to receive the vaccine was not significantly affected by age, education level, STI history, or health insurance status. Acceptability of HPV vaccination did not change significantly after reading a structured paragraph containing information on HPV (P = 0.104). When asked how they would like to receive information on sexual health (e.g., STIs, vaccines, contraception, HPV), 63.8% stated they would like it on a one-to-one basis, 33.3% would like group talks given by a doctor or nurse, and 27.6% would like group talks given at the outreach centres. DISCUSSION
Although the average age of first intercourse in Canada is 16.5 years, the highest rates of STIs occur in the 15to 24-year-old age group.12 The human papillomavirus is associated with genital warts, cervical dysplasia, and cervical cancer, and hence can cause significant costs for the individual and society. In the United States, youth 126 l FEBRUARY JOGC FÉVRIER 2015
aged 15 to 24 years account for nearly 50% of new HPV infections, which corresponds to an incidence of over seven million new cases each year.10 The estimated total annual cost of HPV infection in young women (aged 15 to 24) is US$2.8 billion.13 There has been limited research on the burden of HPV infection in higher-risk youth populations such as those with a high number of sexual partners and increased pregnancy rates. The HPV vaccine has the potential to significantly decrease the burden of disease in women, perhaps even more so in young women who are socioeconomically disadvantaged. However, in order to target higher-risk youth effectively, we must determine the factors and limitations affecting HPV vaccination in these populations. This allows us to develop appropriate public health strategies and programs to increase HPV vaccination rates in higher-risk populations, thereby decreasing the burden of HPV in this population and decreasing HPVrelated costs to our health care system. The young women in our outreach centres have many demographic characteristics that put them at higher risk for HPV acquisition. Unfortunately, these same characteristics may be associated with difficulty accessing health care services, including HPV vaccination programs. Although the higher-risk young women in our study had high levels of awareness of HPV infection and the HPV vaccine, they lacked knowledge of the consequences of HPV infection. Giede et al. have shown that although many young women rank their knowledge of HPV as very good, few are able to correctly answer questions regarding methods of preventing HPV.14 Schools and social media have attempted to increase public awareness of HPV but further efforts are likely needed to educate the public on HPV’s causal relationship with cervical cancer and genital warts and consequently to increase knowledge of the role of HPV vaccination in the prevention of HPV-related diseases. Interestingly, awareness of HPV infection in our study was higher in those less than 20 years old, but participants over the age of 20 were more aware of HPV’s causal relation with cervical cancer. The introduction of school-based HPV vaccination programs may explain the increased awareness of HPV infection in those less than 20 years old. Although those more than 20 years old were less aware of HPV infection overall, they were more aware of HPV’s consequences. In addition, knowledge of HPV infection and vaccination was higher in participants with a prior history of STI. Although the association between STI history and awareness of HPV has not been addressed in prior studies, our findings are not surprising given that these young women, in the context of their STI diagnosis,
HPV Awareness in Higher-Risk Young Women: The Need for a Targeted HPV Catch-Up Vaccination Program
may have had more counselling with regard to HPV and the HPV vaccine. In our study, HPV vaccination acceptability was high, especially if it was given in accessible and youth-friendly centres. Acceptability was not affected by age, education level, STI history, or health insurance status. Lenehan et al. similarly found that women were strongly supportive of HPV vaccination and that this interest was unrelated to HPV knowledge, level of education, or number of previous sexual partners.15 In general, previous studies have repeatedly demonstrated that youth populations have low levels of awareness of HPV infection and vaccination but high acceptance of the HPV vaccine.16–18 Vaccination status may be dependent on schooling, awareness, access to health care, and health care provider counselling. Previous studies have found that one of the most important factors predicting HPV vaccination uptake in young women is recommendation by a physician.15–19 Young women in our study who had a family doctor were more likely to be vaccinated against HPV than those who did not have a family doctor. Rosenthal et al. also concluded that the strength of the recommendation by a physician played a significant role in the young women’s decision to be vaccinated.19 These authors demonstrated a four-fold greater likelihood of HPV vaccination in women who received a strong recommendation compared with those who received a less strong recommendation.19 Physician access is definitely a key factor affecting HPV vaccination uptake in higher-risk young women. Unfortunately, vaccination rates in our higher-risk young women were low. A variety of reasons were cited for the lack of immunization. It is interesting that vaccination rates are low, even in the presence of school-based government-funded HPV vaccination programs. There are many possible reasons for the low HPV vaccination rates in our cohort. Some of the respondents may have missed the publicly funded vaccination program when it was implemented for Grade 8 students in 2007 because they had already completed Grade 8. In addition, parental consent is required for school-based vaccination, and only 37% of young women in our study lived with their parents. Furthermore, these young women may have missed the vaccination opportunities in school because of high-risk behaviours that may be associated with truancy. Although school-based programs may succeed in vaccinating some low-risk youth against HPV, other strategies are needed to target the higher-risk youth who may lack access and vaccination opportunities because of social circumstances and socioeconomic disadvantages. Implementing a free catch-up vaccination program in a youth-friendly
setting such as our outreach clinics at St. Mary’s Young Parent Outreach Centre and Youville Centre may help to target and increase vaccination rates in these higher-risk populations. This study has demonstrated that while HPV vaccination rates are low, higher-risk young women are very supportive of free catch-up vaccination programs in accessible, youth-friendly outreach centres. Our study is one of the few to address issues and barriers that contribute to low HPV vaccination rates in higher-risk youth populations and is the only study to date to have targeted higher-risk young women in Ontario, specifically those in outreach centres. Limitations of the study include selection bias (inclusion of young women already attending medical clinics in outreach centres), recall bias (HPV vaccination history and number of doses received), and the small sample size. Future research that assesses the effect and success of vaccination programs targeting higher-risk youth will allow public health policy makers to determine the most effective strategy for vaccinating higher-risk populations and decreasing the burden of HPV. CONCLUSION
Higher-risk young women may have high levels of HPV infection and HPV vaccination awareness but lack knowledge of HPV consequences. Those who missed or did not complete HPV vaccination opportunities would support free catch-up vaccination programs in accessible, youth-friendly centres. The findings of this study support the development of targeted public health strategies and interventions regarding HPV vaccination. The implementation of an outreach catch-up vaccination program for higher-risk populations allows for access in a friendly and non-judgemental setting, and could significantly increase HPV vaccination rates in this population. This may ultimately contribute to improving long-term health outcomes, and in the future help to decrease the burden of genital warts and cervical dysplasia/cancer on our health care system. ACKNOWLEDGEMENTS
The authors wish to acknowledge the contributions of Tinghua Zhang who performed the statistical analysis for this paper. REFERENCES 1. Franco EL, Duarte-Franco E, Ferenczy, A. Cervical cancer: epidemiology, prevention and the role of human papillomavirus infection. CMAJ 2001;164(7):1017–25.
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2. Hariri S, Unger ER, Sternberg M, Dunne EF, Swan D, Patel S, Markowitz LE. Prevalence of genital human papillomavirus among females in the United States, the National Health and Nutrition Examination Survey, 2003–2006. J Infect Dis 2011;204(4):566–73. 3. Kahn JA, Lan D, Kahn RS. Sociodemographic factors associated with high-risk human papillomavirus infection. Obstet Gynecol 2007;110(3):713. 4. Dunne EF, Sternberg M, Markowitz LE, McQuillan G, Swan D, Patel S, et al. Human papillomavirus (HPV) 6, 11, 16, and 18 prevalence among females in the United States—National Health And Nutrition Examination Survey, 2003–2006: opportunity to measure HPV vaccine impact? J Infect Dis 2011;204(4):562–5. 5. Roteli-Martins CM, de Carvalho NS, Naud P, Teixeira J, Borba P, Derchain S, et al. Prevalence of human papillomavirus infection and associated risk factors in young women in Brazil, Canada, and the United States: a multicenter cross-sectional study. Int J Gynecol Pathol 2011;30(2):173–84. 6. Almonte M, Ferreccio C, Gonzales M, Delgado JM, Buckley CH, Luciani S, et al. Risk factors for high-risk human papillomavirus infection and cofactors for high-grade cervical disease in Peru. Int J Gynecol Cancer 2011;21:1654–63. 7. Smith LM, Brassard P, Kwong JC, Deeks SL, Ellis AK, Lévesque LE. Factors associated with initiation and completion of the quadrivalent human papillomavirus vaccine series in an Ontario cohort of grade 8 girls. BMC Public Health 2011;11:645.
11. National Advisory Committee on Immunization (NACI). Update on Human Papillomavirus (HPV) Vaccines. Canada Communicable Disease Report. 2012. 38. 12. Rotermann M. Sex, condoms and STDs among young people. Statistics Canada. Health Reports. 2005;16(3):39–45. 13. Chesson HW, Blandford JM, Gift TL, Tao G, Irwin KL. The estimated direct medical cost of sexually transmitted diseases among American youth, 2000. Perspect Sex Reprod Health 2004;36(1):11–9. 14. Giede C, McFadden LL, Komonoski P, Agrawal A, Stauffer A, Pierson R. The acceptability of HPV vaccination among women attending the University of Saskatchewan Student Health Services. J Obstet Gynaecol Can 2010;32(7):679–86. 15. Lenehan JG, Leonard KC, Nandra S, Isaacs CR, Mathew A, Fisher W. Women’s knowledge, attitudes, and intentions concerning human papillomavirus vaccination: findings of a waiting room survey of obstetrics-gynaecology outpatients. J Obstet Gynaecol Can 2008;30(6):489–99. 16. Price RA, Tiro JA, Saraiya M, Meissner H, Breen N. Use of human papillomavirus vaccines among young adult women in the United States: an analysis of the 2008 National Health Interview Survey. Cancer 2011;117(24):5560–8.
8. Shearer BD. HPV vaccination: understanding the impact on HPV disease. National Collaborating Centre for Infectious Diseases. Purple Paper no.34, 2011 Dec.
17. Sundstrom K, Tran TN, Lundholm C, Young C, Sparen P, Dahlstrom LA. Acceptability of HPV vaccination among young adults aged 18–30 years: a population based survey in Sweden. Vaccine 2010;28(47):7492–500.
9. Agius PA, Pitts MK, Smith AM. Mitchell A. Human papillomavirus and cervical cancer: Gardasil® vaccination status and knowledge amongst a nationally representative sample of Australian secondary school students. Vaccine 2010;28(27):4416–22.
18. Williams K, Forster A, Marlow L, Walker J. Attitudes towards human papillomavirus vaccination: a qualitative study of vaccinated and unvaccinated girls aged 17–18 years. J Fam Plann Reprod Health Care 2011;37:22–5.
10. Satterwhite CL, Terrone E, Meites E, Dunne E, Mahajan R, Ocfemia M, et al. Sexually transmitted infections among U.S. women and men: prevalence and incidence estimates, 2008. Sex Transm Dis 2013;40(3):187–93.
19. Rosenthal SL, Weiss TW, Zimet GD, Ma L, Good MB, Vichnin, MD. Predictors of HPV vaccine uptake among women aged 19–26: Importance of a physician’s recommendation. Vaccine 2011;29(5):890–5.
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