Research
Prevalence and predictors of human papillomavirus vaccination in adolescent girls Swetha Rao Palli, Sandhya Mehta, and Rajender R. Aparasu
Received November 2, 2010, and in revised form March 10, 2011. Accepted for publication March 14, 2011.
Abstract Objectives: To determine the prevalence and predictors of human papillomavirus (HPV) vaccination in adolescent girls who were recommended to receive the vaccine by their health care providers. Design: Cross-sectional study. Setting: United States in 2007–08. Participants: Parents or guardians most knowledgeable about health and health care of adolescent girls aged 12 to 17 years participating in the 2007 National Survey of Children’s Health (NSCH). Intervention: NCSH was a population-based telephone survey using a complex probability sampling design. Main outcome measures: Prevalence of HPV vaccination in adolescent girls who were recommended to receive the HPV vaccine and predisposing, enabling, and need factors associated with HPV vaccination. Results: Of 12.38 million adolescent girls aged 12 to 17 years, 3.69 million (29.76%) were recommended to receive the HPV vaccine by their health care provider. The majority who received the HPV vaccine recommendation were 13 to 17 years of age (83%), were white (71%), and had one or more preventive visits (94%). Among those for whom the HPV vaccine was recommended, 48.75% (95% CI 45.37–52.13) received the vaccine. Multivariate logistic regression analysis of those who were recommended revealed that enabling and predisposing factors were significantly associated with the HPV vaccination. Children living at 101% to 200% of the Federal Poverty Level (odds ratio 0.54 [95% CI 0.30–0.98]) and children in households with two or more adults (0.51 [0.33–0.80]) were negatively associated with HPV vaccination, whereas children with any preventive medical care visit(s) (2.28 [1.36–3.84]) in the previous year were positively associated with HPV vaccination. Conclusion: Nearly one-half of adolescent girls received the HPV vaccine among those who were recommended by their health care provider. The study finding emphasizes the importance of predisposing and enabling factors for HPV vaccination. Policy and education efforts can focus on these factors to improve HPV vaccination rates. Keywords: Human papillomavirus vaccine, health care services, adolescents, surveys. J Am Pharm Assoc. 2012;52:52–58. doi: 10.1331/JAPhA.2012.10195
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Swetha Rao Palli, BSPharm (Hons), MS, is a research analyst, HealthCore Inc., Wilmington, DE. Sandhya Mehta, BSPharm, MS, is a PhD candidate; and Rajender R. Aparasu, MPharm, PhD, is Professor and Division Head, College of Pharmacy, University of Houston, Texas Medical Center, Houston. Correspondence: Rajender R Aparasu, MPharm, PhD, College of Pharmacy, University of Houston, Texas Medical Center, 1441 Moursund St., Houston, TX 77030. Fax: 713795-8383. E-mail:
[email protected] Disclosure: The authors declare no conflicts of interest or financial interests in any product or service mentioned in this article, including grants, employment, gifts, stock holdings, or honoraria. Acknowledgment: To Mrs. Golda Hallett for editing assistance. Previous presentation: International Society for Pharmacoeconomics and Outcomes Research Annual International Meeting, May 15–19, 2010, Atlanta, GA.
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G
enital human papillomavirus (HPV) infection is the most common sexually transmitted infection worldwide.1 Persistent exposure to high-risk types of HPV increases the risk for developing cervical cancer.2,3 HPV infections also have been linked to other anogenital cancers, cervical neoplasia, and genital warts.1,4–7 Approximately 20 million people in the United States are infected with HPV currently, and an estimated 6.2 million between the ages of 14 and 44 years acquire it each year.1 In light of this morbidity and mortality threat, the first HPV vaccination (Gardasil—Merck & Co.) was licensed for use by the Food and Drug Administration in June 2006. This prophylactic vaccine prevents persistent HPV infection and HPV-associated (types 6, 11, 16, and 18) genital disease among uninfected women.4–8 Studies suggest that universal vaccination can prevent roughly 70% of cervical cancer cases and 90% of anogenital warts.1,8–12 Consequently, the Advisory Committee on Immunization Practic-
At a Glance Synopsis: Data from 2007 National Survey of Children’s Health (NSCH) were analyzed to determine prevalence and predictors of human papillomavirus (HPV) vaccination among adolescent girls (aged 12–17 years). Of 12.38 million adolescent girls, 3.69 million (29.76%) were recommended to receive the HPV vaccine by their health care provider. Those receiving the vaccine tended to be white (71%) teenagers (13–17 years of age; 83%) with one or more preventive visits (94%). Of adolescent girls for whom HPV vaccine was recommended, 48.75% received the vaccine. Children living at 101% to 200% of the Federal Poverty Level (FPL) and children in households with two or more adults were negatively associated with HPV vaccination, whereas children with any preventive medical care visit(s) in the previous year were positively associated with HPV vaccination. Analysis: Near-poor children (101–199% FPL) were less likely to receive the HPV vaccine compared with poor children (<100% FPL), which highlights the need for continued efforts to overcome financial barriers, including access to providers and vaccination for low-income families. Adolescent girls in households with two or more adults were less likely to receive the HPV vaccine than girls with a single parent/caregiver, which may be attributable to a protective nature in a single parent or greater awareness of the child’s risk by a single parent. The success of vaccination programs will likely depend on education and awareness regarding the underlying risk and behavior of adolescents. The odds of accepting HPV vaccination following a physician recommendation increased 2.23-fold if adolescents made one or more health care contacts in the previous year for preventive medical care. Better coverage and reimbursements for preventive visits for adolescents can help improve vaccination rates.
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es recommended this quadrivalent vaccine for routine immunization in girls 11 to 12 years of age, while administration to girls as young as 9 years was at the provider’s discretion. Catch-up vaccination was recommended for female patients aged 13 to 26 years if they had not been vaccinated.1–4 The probability of testing HPV positive is approximately 45% within 2 to 3 years of sexual initiation.13,14 Moreover, the risk of exposure to the oncogenic HPV types is highest during this period, implying that adolescents are the most vulnerable population for HPV acquisition.14–16 Research indicates that 3.7% of female students in the United States make their sexual debut before 13 years of age. The percentage of sexually active females rapidly increases to 24%, 40%, and 70% by the ages of 15, 16, and 18 years, respectively.17,18 The risk of adolescent girls acquiring HPV infection is a major public health concern. Consequently, HPV vaccination of adolescent girls is needed, preferably before their sexual debut, in order to prevent long-term health care and economic consequences.1,4,9,19–21 Postlicensing studies involving adolescent girls estimate that initiation rates of HPV vaccine were quite low, varying from nearly 6% to 37%22,23; however, limited national level data exist regarding HPV vaccination. Most of the studies focused on acceptance rates by physicians and parents before or after the HPV vaccine was approved.4,24–31 These studies also addressed the association between HPV vaccine acceptance and sociodemographic factors, general attitudes, knowledge, and other behavioral factors.24,31–33 In all these studies, physician endorsement emerged as a very critical factor for HPV vaccine acceptance. Rosenthal et al.31 estimated that physician recommendation increases the likelihood of accepting the HPV vaccine by 92%. A need exists to examine, at a national level, provider recommendations for HPV vaccination and the factors associated with vaccination following the recommendation.
Objective Using data from the 2007 National Survey of Children’s Health (NSCH), the current study aims to (1) estimate the prevalence of HPV vaccine recommendation by their health care provider and HPV vaccination rates of adolescent girls aged 12 to 17 years and (2) determine predictors of HPV vaccination in adolescent girls who were recommended to receive the HPV vaccine.
Methods Data source The study analyzed data from the 2007 NSCH. NSCH is a population-based, cross-sectional survey that uses a complex probability sampling design to produce national and state-specific prevalence estimates of selected child health indicators.34 NSCH is a component of the State and Local Area Integrated Telephone Survey, which is conducted by the Centers for Disease Control and Prevention National Center for Health Statistics and sponsored by the Maternal and Child Health Bureau of the Health Resources and Services Administration. NSCH involves random digit dialing to recruit households with children younger than 18 years of age from each of the 50 www. japh a. or g
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states and the District of Columbia. One child was randomly selected from each of these eligible households, and the parent/ caretaker most knowledgeable about the sampled child’s health and health care was interviewed. These interviews were conducted in English or Spanish. Data were collected pertaining to eight specific domains (demographics, physical and mental health status, health insurance, health care use and access, medical home, family functioning, parents’ health, and neighborhood characteristics). Estimates obtained were based on a total of 91,642 interviews conducted between April 2007 and July 2008. Because nearly 80% of the interviews were completed in 2007, the survey is referred to as the 2007 NSCH. The weighted overall response rate of the 2007 NSCH was 46.7%. A detailed description of the survey design and procedure was published previously.35 Study sample and analytical framework This study was exempt by the University of Houston Institutional Review Board. The study sample included adolescent girls 12 to 17 years of age. The analysis focused on HPV vaccine recommendation by providers and eventual vaccination. HPV vaccine recommendation was operationalized based on the response to the following close-ended question: “Did a doctor or health care provider recommend that selected child [S.C.] receive HPV shots?” HPV vaccine receipt was defined as receiving at least one injection of the three-shot vaccine series22–24,33 if a positive response was received to the question, “Has [S.C.] ever received any HPV shots?,” and if the respondent reported one or more injection in response to the question, “Please tell me how many HPV shots [S.C.] received?” The Andersen Behavioral Model was used to identify the predictors of HPV vaccination in adolescent girls following a physician recommendation. This model has been used extensively to understand the factors associated with health service and medication use.36–39 Within its conceptual framework, an individual’s health service utilization is expressed as a function of predisposing, enabling, and need factors. Predisposing factors are influential characteristics of an individual that exist prior to illness and include demographics, social structure (e.g., occupation), and health beliefs (e.g., personal attitudes). Enabling factors represent community and personal resources. Income, health insurance, and availability of services signify the enabling factors that facilitate an individual’s use of health services. Need factors are determined by a subjective acknowledgment of a need, such as a patient’s symptoms or an objective professional recognition of a need for services because of diagnosis and disease severity. In this study, factors were selected based on availability in the NSCH dataset and previous literature. Variable categories were either retained from the original survey or collapsed to aid interpretation. Predisposing factors included age (preteens [12 years] versus teens [13–17 years]), race (white versus nonwhite), ethnicity (Hispanic versus non-Hispanic), number of children (one, two, three or more) and adults (one versus two or more) in the household, maternal age (<40, 40–49, ³50 years), highest level of education in the household (more than high school versus high school or less than high school), and maternal health (excellent to good versus fair or poor). Enabling 54 • JAPhA • 5 2 : 1 • J a n / F e b 2012
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factors were represented by geographical region (northeast, midwest, south, and west), metropolitan statistical area (MSA) status (MSA versus non-MSA), primary language spoken in the household (English versus non-English), medical home availability (yes or no), employment status in the household (employed versus unemployed), Federal Poverty Level (FPL) of the household (≤100%, 101–200%, >200%), type of insurance, and whether the adolescent girls had adequate insurance (yes or no) and preventive medical care visits. The variable "medical home" is a measure of quality of care and has been defined by the American Academy of Pediatrics as primary care that is accessible, continuous, comprehensive, family centered, coordinated, compassionate, and culturally effective.40 The insurance variable was stratified as continuous public or private insurance, gained insurance, lost insurance, and full-year uninsured.38,41 Children who were insured at the time of the survey but had a gap in the insurance coverage in the previous 12 months were classified as gained insurance. On the contrary, lost insurance represents children who were uninsured at the time of the survey but had coverage at some point in the preceding 12 months. Preventive medical care visits were defined as whether at least one visit was made to a health care provider (in the previous 12 months) for the purpose of preventive medical care and categorized as a twolevel discrete variable. Perceived health status of the child was identified as the need factor that would determine HPV vaccine acceptability. It was dichotomized to compare excellent/very good/good with fair/poor health. Descriptive weighted analysis and chi-square statistics were used to examine HPV vaccination among those who were recommended by their health care provider. As a result of survey design complexities, sampling weights were assigned to the sampling unit to obtain national estimates for noninstitutionalized U.S. children. These sampling weights were adjusted for the complex survey design, households with multiple children, and potential nonresponse biases. These biases account for multiple telephone lines and noncoverage of nontelephone households. Multivariate logistic regression was used to identify the predic-
Table 1. Prevalence of age-based HPV vaccination and vaccine recommendations by health care providers for adolescent girls aged 12 to 17 years in the United States Characteristic n HPV vaccine recommendationb Age 12 years Age 13–17 years Subsequent HPV vaccination Age 12 years Age 13–17 years
Estimate No (%)a 12.38 million 3,685.27 (29.76) 626.96 (5.06) 3,058.31 (24.7) 2,092.85 (16.9) 342.02 (2.76) 1,750.83 (14.14)
c2 P
<0.0001c
<0.0001c
Abbreviation used: HPV, human papillomavirus. a Estimates in thousands. b Recommendations were made by a physician or a health care provider to adolescent girls c P values significant at 0.05. Source: Reference 34.
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Table 2. Characteristics of adolescent girls aged 12 to 17 years receiving HPV vaccine recommendation in the United States Characteristic n Age (years) 12 13–17 Race White Nonwhite Ethnicity Non-Hispanic Hispanic No. of children in household ≤2 ≥3 No. of adults in household 1 ≥2 Highest level of education in the household ≤High school ≥High school Language English Other Maternal age (years) <40 40–49 ≥50 Maternal health Excellent, very good, good Fair, poor Region Northwest Midwest South West MSA status Non-MSA MSA Insurance Public insurance Private insurance Gained insurance Lost insurance Full-year uninsured Adequate insurance Yes No Family income (% of FPL) ≤100
Estimatea No. (%) 3,685.27 626.96 (17.01) 3,058.31 (82.99) 2,608.96 (70.79) 1,076.31 (29.21) 3,173.28 (86.11) 511.99 (13.89) 2,477.32 (67.22) 1,207.95 (32.78) 507.99 (13.78) 3,177.29 (86.22) 985.59 (26.74) 2,699.69 (73.26) 3,473.37 (94.25) 211.9 (5.75) 1,110.69 (30.14) 1,955.71 (53.07) 618.87 (16.79) 3,159.01 (85.72) 526.26 (14.28) 902.19 (24.48) 793.53 (21.53) 1,285.65 (34.89) 703.91 (19.1) 868.76 (23.57) 2,816.51 (76.43) 673.91 (18.29) 2,684.94 (72.86) 179.52 (4.87) 71.02 (1.93) 75.88 (2.06) 219.88 (5.97) 3,465.40 (94.03) 389.23 (10.56)
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101–200 >200 Medical home Yes No Preventive medical care visits 0 ≥1 Perceived health of the child Excellent, very good, good Fair, poor HPV vaccine Yes No
544.9 (14.79) 2,751.13 (74.65) 1,446.36 (39.25) 2,238.91 (60.75) 207.24 (5.62) 3,478.03 (94.38) 3,604.87 (97.82) 80.4 (2.18) 1,745.50 (47.36) 1,939.77 (52.64)
Abbreviation used: FPL, Federal Poverty Level; HPV, human papillomavirus; MSA, metropolitan statistical area. a Estimates in thousands. Source: Reference 34.
tors of HPV vaccination for adolescent girls who were recommended for vaccination. All data analyses were performed using SAS version 9.2 (SAS Institute, Cary, NC). SURVEYFREQ and SURVEYLOGISTIC procedures used the sampling weights and study design variables provided in the NSCH dataset to produce population-based national estimates. The alpha level was set at 0.05 to identify significant associations.
Results According to NSCH, 12.38 million (95% CI 11.94–12.83) adolescent girls aged 12 to 17 years were living in the United States in 2007–08. The prevalence of HPV vaccine recommendation and subsequent vaccination, as well as corresponding age-based distributions, are shown in Table 1. Approximately 3.68 million (95% CI 3.44–3.93; or 29.76% [28.04–31.48]) adolescent girls aged 12 to 17 years were recommended to receive the HPV vaccine by their health care provider. Girls who received HPV vaccine recommendations from their health care providers were predominantly 13 to 17 years of age (82.99%), white (70.79%), non-Hispanic (86.11%), and privately insured (72.86%) (Table 2). A majority of those who were recommended made at least one preventive care visit in the preceding 12 months (94.38%) and were 200% above the FPL (74.65%). Overall, 48.75% (95% CI 45.37–52.13) of adolescent girls initiated the HPV vaccine series in both age groups: 48.64% (42.10–60.62) among those 12 years of age and 47.10% (49.30– 56.50) of those aged 13 to 17 years. Multivariate logistic regression analysis revealed that predisposing (number of adults in the household and preventive medical care visits) and enabling (socioeconomic status) factors were significantly associated with HPV vaccination (Table 3) after controlling for other factors. Children in households with two or more adults (odds ratio 0.57 [95% CI, 0.36–0.90]) were negatively associated with receiving the HPV vaccination. Children living at 101% to 200% of the FPL (0.54 [0.30–0.99]) were less likely to receive the vaccine than those living at 100% or www. japh a. or g
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Table 3. Predictors of HPV vaccination among adolescent girls aged 12 to 17 years recommended for vaccination Characteristic Predisposing factors Age (years) 12 13 –17 Race White Nonwhite Ethnicity Non-Hispanic Hispanic Preventive medical care visits 0 ≥1 No. of children in household ≤2 ≥3 No. of adults in household 1 ≥2 Highest level of education in the household ≤High school ≥High school Maternal age (years) <40 40–49 ≥50 Maternal health Excellent, very good, good Fair, poor Enabling factors Region Northwest Midwest South West MSA status Non-MSA MSA Insurance Public insurance Private insurance Gained insurance Lost insurance Full-year uninsured Adequate insurance Yes No
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Adjusted odds ratio (95% CI)
Reference 1.02 (0.69–1.51)
P
0.92
Reference 1.14 (0.82–1.59)
0.45
Reference 1.00 (0.61–1.61)
0.98
Reference group 2.23 (1.27–3.92)
0.01a
Reference 1.20 (0.90–1.60)
0.22
Reference 0.57 (0.36–0.90)
0.02a
Reference 1.07 (0.74–1.55)
0.72
Reference 0.74 (0.53–1.02) 1.02 (0.69–1.49)
0.06 0.94
Reference 1.12 (0.78–1.62)
0.53
Reference 0.83 (0.62–1.12) 0.95 (0.70–1.31) 0.92 (0.59–1.44)
0.22 0.77 0.71
Reference 0.91 (0.73–1.15)
0.44
Reference 0.98 (0.63–1.53) 0.74 (0.35–1.55) 1.22 (0.47–3.18) 2.81 (0.85–9.24)
0.93 0.42 0.68 0.09
Reference 1.60 (0.82–3.13)
0.17
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Family income (% of FPL) ≤100 101–200 >200 Medical home Yes No Need factors Perceived health of child Excellent, very good, good Fair, poor
Reference 0.54 (0.30–0.99) 0.65 (0.35–1.21)
0.05a 0.18
Reference 1.01 (0.78–1.32)
0.93
Reference 0.57 (0.19–1.72)
0.3
Abbreviation used: FPL, Federal Poverty Level; HPV, human papillomavirus; MSA, metropolitan statistical area. a P values significant at 0.05. Source: Reference 34.
lower of FPL. The odds of HPV vaccination were 2.2 times (2.23 [1.27–3.92]) higher in adolescent girls with any previous preventive medical care visit compared with those who did not make any preventive medical care visits in the previous 12 months.
Discussion Immunizations are considered the mainstay of preventive care in the United States. However, the immense success achieved by the childhood vaccination programs have not been replicated in adolescents.42–44 The current national study examined the postlicensing HPV vaccine recommendation rates for adolescent girls aged 12 to 17 years and predictors of HPV vaccination following a physician recommendation using the data-rich NSCH. We found that the vaccine was recommended to nearly 30% of adolescent girls, with most recommendations (83%) directed toward teens aged 13 to 17 years within 1 to 2 years of vaccine licensure. Limited population level data exist regarding HPV vaccine recommendation rates. However, the study findings regarding recommendations for teens are consistent with previous studies that evaluated acceptance and intentions to recommend HPV vaccination.8,45–49 Among those to whom recommendations were made, 47% received the HPV vaccine. The vaccination rates among preteens (49%) and teens (47%) were similar, suggesting that variation in acceptance of HPV vaccination recommendations may not be based on age. This was further confirmed by the multivariate analysis. The high vaccination rates among preteens appear to suggest that parents and at-risk preteens are willing to accept HPV immunization. Previous literature reported that parents were more willing to accept HPV immunization of older adolescents compared with preadolescents.4,20,27,50,51 Overall, the findings indicate that physician recommendation plays a major role in HPV vaccination irrespective of the age of adolescents. The multivariate logistic regression analysis revealed that the predisposing and enabling factors are associated with HPV vaccination following physician recommendation. The number of adults in the household emerged as a significant predisposing Journal of the American Pharmacists Association
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factor for HPV vaccination. Adolescent girls belonging to a family with two or more adults in the household were less likely to receive the HPV vaccine than girls with a single parent/caregiver. High HPV vaccination among girls with single-parent households may be attributable to a protective nature in a single parent or greater awareness of the child’s risk by a single parent. Consequently, the success of vaccination programs will likely depend on education and awareness regarding the underlying risk and behavior of adolescents. Having one or more preventive medical care visits in the preceding 12 months was identified as a strong predisposing factor for HPV vaccination. The odds of accepting the vaccine following a physician recommendation increased 2.23-fold if the adolescent made one or more health care contacts in the previous year for preventive medical care. Such preventive visits are an indication of healthy behavior or greater involvement of parents in reducing the health risk of their children and subsequent willingness to accept the vaccination. Better coverage and reimbursements for preventive visits for adolescents can help improve vaccination rates. Among the enabling factors, near-poor children (101–199% FPL) were less likely to receive the HPV vaccine compared with poor children (≤100% FPL). Consistent with previously reported adolescent use of health services, it appears that children in the lower income category experienced greater barriers to vaccination compared with their counterparts in higher income families.52,53 This may be attributed to low-income families, who mainly consisted of the working poor, having issues accessing health care providers.53 These findings highlight the need for continued efforts to overcome financial barriers, including access to providers and vaccination for low-income families. Legislative and public health initiatives are needed to overcome these financial barriers to improve HPV vaccinate rates among this vulnerable population.8,22,45
Limitations The current work involved limitations resulting from the study design and data source. First, the cross-sectional nature of the data does not allow causal associations between variables. Second, data collected based on parent/caregiver reports may be subject to recall bias. Bias may exist from nonresponse and from noninclusion of households without landline telephones. Households that use cellular phones tend to be younger, belong to minority groups, be uninsured, and be mobile.33 The variables included in the analyses were based on availability in NSCH. Because the interviews were conducted in English and/or Spanish, potential errors in reporting may have occurred for respondents who were not fluent in these two languages. Finally, an issue common to all secondary databases is the possibility of coding errors.38
Conclusion In this national study of adolescent girls aged 12 to 17 years, nearly 30% received HPV vaccine recommendations; of these, nearly 50% received the HPV vaccination. Multivariate analysis revealed that predisposing (e.g., number of adults in household, Journal of the American Pharmacists Association
preventive care visits) and enabling (e.g., income level of household) factors were significant predictors of vaccine uptake in adolescent girls who received an HPV vaccine recommendation from their health care provider. These findings suggest that policy changes should be designed in tandem with proactive education efforts, in order to improve HPV vaccine recommendations and the accessibility and affordability of the vaccine. References 1. Markowitz LE, Dunne EF, Saraiya M, et al. Quadrivalent human papillomavirus vaccine: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep. 2007;56:1–24. 2. Jemal A, Siegel R, Ward E, et al. Cancer statistics, 2008. CA Cancer J Clin. 2008;58:71–96. 3. Trottier H, Franco EL. The epidemiology of genital human papillomavirus infection. Vaccine. 2006;24(suppl 1):S4–15. 4. Dempsey AF, Zimet GD, Davis RL, Koutsky L. Factors that are associated with parental acceptance of human papillomavirus vaccines: a randomized intervention study of written information about HPV. Pediatrics. 2006;117:1486–93. 5. Garland SM, Hernandez-Avila M, Wheeler CM, et al. Quadrivalent vaccine against human papillomavirus to prevent anogenital diseases. N Engl J Med. 2007;356:1928–43. 6. FUTURE II Study Group. Quadrivalent vaccine against human papillomavirus to prevent high-grade cervical lesions. N Engl J Med. 2007;356:1915–27. 7. Villa LL, Costa RL, Petta CA, et al. High sustained efficacy of a prophylactic quadrivalent human papillomavirus types 6/11/16/18 L1 virus-like particle vaccine through 5 years of follow-up. Br J Cancer. 2006;95:1459–66. 8. Daley MF, Liddon N, Crane LA, et al. A national survey of pediatrician knowledge and attitudes regarding human papillomavirus vaccination. Pediatrics. 2006;118:2280–9. 9. Christian WJ, Christian A, Hopenhayn C. Acceptance of the HPV vaccine for adolescent girls: analysis of state-added questions from the BRFSS. J Adolesc Health. 2009;44:437–45. 10. Dunne EF, Unger ER, Sternberg M, et al. Prevalence of HPV infection among females in the United States. JAMA. 2007;297:813–9. 11. Adams M, Jasani B, Fiander A. Human papilloma virus (HPV) prophylactic vaccination: challenges for public health and implications for screening. Vaccine. 2007;25:3007–13. 12. Kahn JA, Lan D, Kahn RS. Sociodemographic factors associated with high-risk human papillomavirus infection. Obstet Gynecol. 2007;110:87–95. 13. Woodman CB, Collins S, Winter H, et al. Natural history of cervical human papillomavirus infection in young women: a longitudinal cohort study. Lancet. 2001;357:1831–6. 14. Winer RL, Lee SK, Hughes JP, et al. Genital human papillomavirus infection: incidence and risk factors in a cohort of female university students. Am J Epidemiol. 2003;157:218–26. 15. Herrero R, Castle PE, Schiffman M, et al. Epidemiologic profile of type-specific human papillomavirus infection and cervical neoplasia in Guanacaste, Costa Rica. J Infect Dis. 2005;191:1796–807. 16. Stone KM, Karem KL, Sternberg MR, et al. Seroprevalence of human papillomavirus type 16 infection in the United States. J Infect Dis. 2002;186:1396–402. www. japh a. or g
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