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. Author manuscript; available in PMC: 2010 Oct 1.
Published in final edited form as: J Clin Virol. 2009 Aug 8;46(2):107–111. doi: 10.1016/j.jcv.2009.07.006

Epidemiology and risk factors for human papillomavirus infection in a diverse sample of low-income young women

Tasneem Shikary 1, David I Bernstein 1,2, Yan Jin 1, Gregory D Zimet 3, Susan L Rosenthal 4, Jessica A Kahn 1,5,*
PMCID: PMC2767195  NIHMSID: NIHMS132496  PMID: 19665924

Abstract

Background

Two HPV vaccines prevent infection with HPV-16 and HPV-18, high-risk (cancer-associated) HPV types which together cause approximately 70% of cervical cancers; one vaccine also prevents HPV-6 and HPV-11, which together cause approximately 90% of anogenital warts. Defining type-specific HPV epidemiology in sexually experienced women will help estimate the potential clinical benefits of vaccinating this population.

Objectives

To examine HPV epidemiology in a diverse sample of sexually experienced women, and to determine factors associated with high-risk HPV and vaccine-type HPV (HPV-6, -11, -16, -18).

Study Design

Cross-sectional study of 13-26 year-old women (N=409) who completed a questionnaire and provided a cervicovaginal swab. Swabs were genotyped for HPV using PCR amplification. Logistic regression models were used to determine whether participant characteristics, knowledge, and behaviors were associated with high-risk and vaccine-type HPV.

Results

Most women (68.4%) were positive for ≥ 1 HPV type, 59.5% were positive for ≥ 1 high-risk type, 33.1% were positive for ≥ 1 vaccine-type HPV, and 3.5% were positive for both HPV-16 and -18: none was positive for all four vaccine types. In adjusted logistic regression models, Black race (OR 2.03, 95% CI 1.21-3.41) and lifetime number of male sexual partners (OR 4.79, 95% CI 2.04-11.23 for ≥ 10 vs. ≤ 1 partner) were independently associated with high-risk HPV infection.

Conclusions

HPV prevalence was very high in this sample of sexually active young women, but < 5% were positive for both HPV-16 and HPV-18, suggesting that vaccination could be beneficial for many individual women who are sexually experienced.

Keywords: human papillomavirus, vaccination, cervical cancer, sexually transmitted infection, epidemiology

Background

Human papillomavirus (HPV) is a common sexually transmitted infection (STI) that may cause cervical cancer and other malignancies.1, 2 Two HPV vaccines have recently been licensed and are recommended by national immunization programs in at least 15 countries.3 Both vaccines prevent HPV-16 and HPV-18, high-risk (cancer-associated) types that together cause approximately 70% of cervical cancer, and one of the vaccines also prevents HPV-6 and HPV-11, which cause approximately 90% of anogenital warts.4, 5 Thus, vaccination has the potential to substantially reduce the global burden of cervical cancer and other HPV-associated diseases.6, 7

Prophylactic HPV vaccines are most effective if given prior to HPV exposure;8-10 therefore, there is consensus among national immunization programs that HPV vaccines should be targeted to girls who are < 15 years of age.3 However, many countries also recommend “catch-up” vaccination of older women. In the U.S., national guidelines state that HPV vaccination should be targeted to 11-12 year-old girls, but that previously unvaccinated 13-26 year-old women should also receive the vaccine, regardless of sexual experience.11 Because many sexually active women have already been exposed to HPV, the impact of widespread vaccination in this population is not well-defined. Therefore, understanding type-specific HPV epidemiology in sexually experienced women is important to help estimate the potential clinical benefit and cost-effectiveness of vaccinating this population. It is particularly important to understand the epidemiology of HPV in minority and low-income young women, who may be at higher risk for HPV infection or cervical cancer.12-14

Objectives

The aims of this study were to determine the prevalence of high-risk and vaccine-type HPV infection in a diverse sample of low-income women, and to examine whether participant sociodemographic characteristics, HPV knowledge, and behaviors are associated with high-risk and vaccine-type HPV infection.

Study Design

Young women 13-26 years of age (N=409) who had had sexual contact were recruited between October 2006 and May 2007 from three primary care clinics: a hospital-based Teen Health Center (N=268), obstetrics and gynecology clinic in a community health center affiliated with the city’s Health Department (N=126), and sexually transmitted disease clinic also affiliated with the Health Department (N=15).15 Of 418 women who were approached by the research coordinators, 409 (98%) provided informed consent. All participants completed a self-administered questionnaire that assessed demographic factors, HPV knowledge, gynecologic history, and behaviors.15

Cervicovaginal swabs were collected from each participant using the same methods at each recruitment site. If the participant had to undergo a speculum examination, then specimens were collected during the exam by the clinician (70% of swabs); otherwise specimens were collected as a blind cervicovaginal swab by either clinicians (25%) or participants (4%). Results were combined based on a previous study of the same clinical population which found reasonable concordance between clinician- and self-testing for HPV DNA using the same method.16 Samples were genotyped using the Roche Linear Array test, a PCR amplification technique that uses an L1 consensus primer system and a reverse-line blot detection strip to identify 37 different HPV genotypes (Roche Molecular Systems, Alameda, CA).17 High- and low-level beta-globin controls were positive in 100% of the samples, indicating sufficient DNA and PCR amplification. This assay utilizes one capture probe that cross-reacts with HPV-33, -35, -52, and -58. A sample is considered positive for HPV-52 when it reacts with the HPV-52-cross-reactive probe but not with the remaining three type-specific individual probes.18 Therefore, reported values for HPV-52 include detection of HPV-52 DNA only and detection of HPV-52 with a cross-reacting type.

The main outcome variables were infection with ≥ 1 high-risk HPV type and infection with ≥ 1 vaccine-type HPV (HPV-6, HPV-11, HPV-16, or HPV-18). Participant data from each site were combined for univariate and multivariable analyses because participants from each recruitment site did not differ in terms of the two outcome variables. We used unadjusted logistic regression modeling to determine whether the following factors were associated with each of the two outcome variables (infection with ≥ 1 high-risk HPV type and infection with ≥ 1 vaccine-type HPV): 1) participant sociodemographic characteristics, 2) HPV knowledge, 3) gynecologic history (history of STI, abnormal Pap test, colposcopy, family history of cervical cancer, number of times pregnant), and 4) behaviors. Behaviors included age of sexual initiation, number of male sexual partners (lifetime, previous three months), condom use with main sexual partner (previous three months, at last sexual intercourse), and smoking in the previous 30 days. Those variables associated with the outcomes at p < .10 in univariable analyses were entered into two separate multivariable logistic regression models to identify factors associated independently with high-risk and vaccine-type HPV infection. In the multivariable models, a p value < .05 was considered statistically significant.

Results

The mean age of participants was 17.6 years, 62% reported that they were Black, 29% that they were White, and 9% that they were another race or multiracial.15 Six percent were Appalachian and 6% Latino. Participants were predominantly low-income: just under half (48%) had Medicaid insurance, 38% had no insurance or were unsure, and 14% had private insurance. Forty-nine percent reported a history of an STI, 35% an abnormal Pap test, and 43% a previous pregnancy. Age of first sexual intercourse was ≤ 14 years for 40% of participants and ≤ 18 years for 92% of participants. Eighteen percent reported ≤ 1 lifetime male sexual partners, 15% reported 2 partners, 14% reported 3 partners, 14% reported 4 partners, 25.3% reported 5-9 partners, and 14% reported ≥ 10 partners.

Most women (68.4%) were positive for ≥ 1 HPV type, 59.5% were positive for ≥ 1 high-risk type, and 33.1% were positive for ≥ 1 vaccine-type HPV (Table 1). The most common HPV types detected (prevalence ≥ 8%) were high risk types HPV-52, HPV-16, HPV-18, HPV-59, CP610, HPV-66, HPV-51, HPV-58, and low risk type HPV-6. The percentage of participants positive for the HPV types in the quadrivalent HPV vaccine were as follows: HPV-6 (9.4%), HPV-11 (2.5%), HPV-16 (17.3%), HPV-18 (11.6%). Although no participant was positive for all four vaccine types, 3.5% were positive for both HPV-16 and HPV-18.

Table 1.

Type-specific human papillomavirus infection among participants recruited fromaTeen Health Center and Health Department sites

N (%) positive1 P value2

Teen Health Center (N=267) Health Department (N=138) All (N=405)
≥ 1 HPV type 190 (71.2) 87 (63.0) 277 (68.4) .10
≥ 1 high-risk HPV type 165 (61.8) 76 (55.1) 241 (59.5) .19
≥ 1 vaccine-type HPV 88 (33.0) 46 (33.3) 134 (33.1) .94
HPV-6 22 (8.2) 15 (10.9) 37 (9.4) .75
HPV-11 8 (3.0) 2 (1.5) 10 (2.5) .90
HPV-16 45 (16.9) 25 (18.1) 70 (17.3) .75
HPV-18 32 (12.0) 15 (10.9) 47 (11.6) .74
HPV-26 2 (0.8) 0 2 (.5) .31
HPV-31 13 (4.9) 9 (6.5) 22 (5.4) .49
HPV-33 2 (0.8) 1 (0.7) 3 (0.7) .98
HPV-35 11 (4.1) 6 (4.4) 17 (4.2) .91
HPV-39 15 (5.6) 7 (5.1) 22 (5.4) .82
HPV-40 11 (4.1) 1 (0.7) 12 (3.0) .06
HPV-42 21 (7.9) 5 (3.6) 26 (6.4) .10
HPV-45 14 (5.2) 3 (2.2) 17 (4.2) .14
HPV-51 23 (8.6) 10 (7.3) 33 (8.2) .63
HPV-52
 HPV-52 plus cross reacting type 30 (11.2) 14 (10.1) 44 (10.9) .74
 HPV-52 only 24 (9.0) 9 (6.5) 33 (8.1) .39
 HPV-52 total 54 (20.2) 23 (16.7) 77 (19.0) .39
HPV-53 18 (6.7) 12 (8.7) 30 (7.4) .48
HPV-54 9 (3.4) 13 (9.4) 22 (5.4) .01
HPV-55 9 (3.4) 3 (2.2) 12 (3.0) .50
HPV-56 6 (2.3) 7 (5.1) 13 (3.2) .13
HPV-58 20 (7.5) 13 (9.4) 33 (8.2) .50
HPV-59 33 (12.4) 8 (5.8) 41 (10.1) .04
HPV-61 17 (6.4) 6 (4.4) 23 (5.7) .41
HPV-62 17 (6.4) 11 (8.0) 28 (6.9) .55
HPV-64 2 (0.8) 0 (0) 2 (.5) .31
HPV-66 24 (9.0) 10 (7.3) 34 (8.4) .55
HPV-67 11 (4.1) 1 (0.7) 12 (3.0) .06
HPV-68 19 (7.1) 6 (4.4) 25 (6.2) .27
HPV-69 0 0 0 --
HPV-70 7 (2.6) 2 (1.5) 9 (2.2) .45
HPV-71 0 0 0 --
HPV-72 2 (0.8) 3 (2.2) 5 (1.2) .22
HPV-73 14 (5.2) 5 (3.6) 19 (4.7) .46
HPV-81 13 (4.9) 1 (0.7) 14 (3.5) .03
HPV-82 17 (6.4) 3 (2.2) 20 (4.9) .06
HPV-83 10 (3.8) 4 (2.9) 14 (3.5) .66
HPV-84 22 (8.2) 7 (5.1) 29 (7.2) .24
HPV-IS39 0 0 0 --
HPV-CP610 29 (10.9) 12 (8.7) 41 (10.1) .49
1

A total of 409 subjects enrolled in the study from all sites. HPV DNA results were missing for a total of 4/409 subjects: 1/268 from the Teen Health Center and 3/141 from the Health Department sites. Results are shown for the 405 subjects (99% of the 409 who enrolled) for whom HPV DNA results were available.

In adjusted logistic regression models, Black race and lifetime number of partners were independently associated (p < .05) with high-risk HPV infection (Table 2). Participants who self-identified as Black had twice the odds of high-risk HPV infection compared to those who identified as White. Participants with 10 or more lifetime partners had almost five times the odds of high-risk HPV infection. Only one category of lifetime number of sexual partners (4 vs. ≤ 1) was independently associated with vaccine-type HPV infection.

Table 2.

Variables associated with high-risk HPV (≥ 1 high-risk HPV type) and vaccine-type HPV (HPV-6, -11, -16, and/or -18) in participants recruited from a Teen Health Center and Health Department sites: results of unadjusted and adjusted logistic regression models

Unadjusted odds ratios (95% confidence intervals)1 Adjusted odds ratios (95% confidence intervals)2

High-Risk HPV Vaccine-Type HPV High-Risk HPV Vaccine-Type HPV
Race
 Black vs. white 2.54 (1.57-3.90) 1.90 (1.15-3.13) 2.03 (1.21-3.41) 1.19 (0.68-2.14)
 Other vs. white 1.26 (0.60-2.65) 0.99 (0.42-2.34) 1.45 (0.62-3.73) 0.77 (0.30-1.99)
Ethnicity
 Appalachian 1.24 (0.531-2.87) 0.80 (0.32-1.96)
 Hispanic 0.73 (0.33-1.65) 0.80 (0.33-1.97)
Insurance status
 Uninsured vs. insured 1.17 (0.72-1.91) 0.88 (0.53-1.47)
 Medicaid vs. private 1.31 (0.72-2.38) 1.37 (0.72-2.62)
 No insurance vs. private 1.63 (0.88-3.02) 1.17 (0.60-2.28)
Marital status: unmarried vs. married 0.57 (0.264-1.24) 0.96 (0.42-2.19)
Age 0.96 (0.90-1.03) 1.03 (0.96-1.101)
History of STI 2.15 (1.43-3.24) 1.78 (1.17-2.72) 1.29 (0.78-2.13) 1.71 (1.02-2.88)
Pap screening: abnormal vs. normal Pap 1.22 (0.78-1.91) 1.31 (0.83-2.10)
Colposcopy 1.42 (0.78-2.57) 1.18 (0.64-2.15)
Family history of abnormal Pap 0.95 (0.56-1.61) 0.58 (0.32-1.05)
Family history of cervical cancer 0.77 (0.44-1.38) 0.97 (0.52-1.82)
Pregnancy history: number of pregnancies
 1 vs. 0 0.84 (0.52-1.37) 0.89 (0.54-1.47) 0.96 (0.56-1.64) 1.01 (0.59-1.73)
 ≥ 2 vs. 0 0.51 (0.30-0.87) 0.53 (0.29-0.98) 0.57 (0.31-1.05) 0.61 (0.32-1.19)
Knowledge about HPV 2.23 (0.875-5.68) 0.88 (0.34-2.31)
Age of first sexual intercourse 0.90 (0.81-1.0) 1.1 (0.941-1.17)
Lifetime number of partners
 2 vs. ≤ 1 1.89 (0.92-3.83) 1.44 (0.67-3.12) 1.81 (0.86-3.80) 1.31 (0.59-2.92)
 3 vs. ≤ 1 3.29 (1.56-6.95) 1.04 (0.46-2.34) 3.58 (1.61-7.96) 0.99(0.42-2.32)
 4 vs. ≤ 1 3.81 (1.78-8.17 2.89 (1.35-6.20) 3.62 (1.61-8.12) 2.53 (1.13 -5.68)
 5-9 vs. ≤ 1 3.18 (1.672-6.05) 1.40 (0.70-2.78) 2.95 (1.44-6.03) 1.17 (0.54-2.52)
 ≥10 vs. ≤ 1 4.71 (2.16-10.28) 1.36 (0.62-3.00) 4.79 (2.04-11.23) 1.22 (0.51-2.92)
Male sexual partners: past 3 months
 1 vs. 0 1.075 (0.59-2.0) 1.1 (0.57-2.12)
 2 vs. 0 1.61 (0.72-3.58) 1.99 (0.88-4.46)
 ≥3 vs. 0 1.31 (0.52-3.31) 1.2 (0.46-3.16)
New male partners: past 3 months
 ≥ 1 vs. 0 1.237 (0.81-1.88) 0.994 (0.64-1.54)
Ever had anal sex with male partner 1.44 (0.89-2.32) 1.42 (0.88-2.29)
Anal sex with male partner: past 3 months 1.47 (0.81-2.67) 1.32 (0.74-2.37)
Condom use with main sexual partner
 Never vs. always 1.33 (0.75-2.35) 0.83 (0.45-1.53)
 Occasionally vs. always 1.38 (0.74-2.59) 0.94 (0.49-1.82)
 Mostly vs. always 1.94 (0.97-3.88) 1.42 (0.72-2.81)
Condom use with main partner last sex 0.75 (0.48-1.16) 1.19 (0.75-1.87)
Condom use with partner other than main
sexual partner
 Never vs. always 0.71 (0.23-2.21) 0.89 (0.27-2.92)
 Occasionally vs. always 1.53 (0.43-5.43) 2.23 (0.70-7.07)
 Mostly vs. always 1.25 (0.46-3.39) 1.95 (0.76-5.02)
Smoked≥1 cigarettes in past 30 days 0.84 (0.55-1.28) 0.61 (0.38-.96) 0.67 (0.39-1.15)
1

Variables associated withhigh-risk HPV or vaccine-type HPV at p < .05 are shown in bold.

2

Only those variables entered into multivariable models and associated with HPV high risk type or HPV vaccine type at p < .05 are shown in these columns.

We also examined univariable associations between all predictor variables and three individual high-risk HPV types - HPV-16, HPV-18, and HPV-52 - to further characterize demographic and behavioral risk factors for these HPV types. The only factor associated significantly with HPV-16 was Black race (OR 2.72, 95% CI 1.33-5.58). No factors were associated with HPV-18. Factors associated with HPV-52 (HPV-52 only, without cross-reacting types) were: number of sexual partners (OR 5.17, 95% CI 1.03-26.02 for 3 vs. ≤ 1 partners), having ever had anal sex (OR 3.01, 95% CI 1.43-6.34) and having had anal sex within the past three months (OR 3.83, 95% CI 1.71-8.56).

Discussion

In this study, we examined the epidemiology of HPV and risk factors associated with high-risk and vaccine-type HPV infection in a racially and ethnically diverse, predominantly low-income population of sexually experienced young women eligible for “catch-up” HPV vaccination. The cross-sectional prevalence of HPV in this sample was high at 68%: this likely underestimates the cumulative lifetime prevalence of HPV as most infections do not persist. Previous studies of predominantly low-income adolescents have demonstrated similarly high prevalence rates.19, 20 In contrast, the prevalence of HPV in study samples that are more representative of the U.S. population is considerably lower,21 supporting the growing evidence that poverty is a strong predictor of HPV infection.14 The high rates of HPV infection in our study sample, combined with evidence that HPV is often acquired soon after sexual initiation,22 suggest that vaccinating young women prior to sexual initiation must be a priority to maximize both the individual and population-level health benefits of vaccination.

Although almost 70% of participants were positive for HPV, fewer than 20% were positive for HPV-16 or HPV-18, < 5% were positive for both HPV-16 and HPV-18, and none was infected with all four vaccine types. HPV vaccines do not have clinical benefit in women who are infected with vaccine-type HPV at the time of vaccination; however, women who are uninfected with some of those types should derive partial benefit from vaccination.23 Thus, even in this sample of women, who had a very high overall HPV prevalence rate, the majority would be expected to benefit at least partially from vaccination. The findings do not address the question of whether vaccination of sexually active women will be cost-effective or have population-level benefit, but they provide evidence that individual women are likely to benefit.

In addition to HPV-16 and HPV-18, one of the most commonly identified HPV types was HPV-52. Global epidemiologic studies suggest that HPV-52 prevalence varies across regions but is particularly common in Africa and Asia.24-26 Although HPV-52 has substantially lower potential to cause cervical neoplasia in comparison to HPV-16 and HPV-18,27, 28 these high prevalence rates are concerning as HPV-52 is not targeted by the two licensed vaccines. To our knowledge, previous studies have not examined risk factors for HPV-52. In this study, risk factors were similar for HPV-52 as for other high-risk types, with the exception of anal sex, which was associated only with HPV-52. Additional information is needed regarding the epidemiology of HPV-52, its role in carcinogenesis, and what clinical significance it will have in the vaccination era.

Identification of factors associated with high-risk and vaccine-type HPV infection may help to inform decisions about vaccine delivery and the design of interventions to prevent infection. Our finding that Black race and number of sexual partners were associated with high-risk HPV is consistent with previous studies.14, 19, 29, 30 However, a previous analysis suggests that higher rates of HPV infection in Black compared to White women are explained in large measure by racial differences in marital status and income. In that study, Black women were more likely than White women to be unmarried and poor, and those socioeconomic factors explained racial differences in HPV infection.14 Racial differences may also be driven by unmeasured disparities in social and economic assets related to income, such as wealth, community resources, and access to health services and education. The findings suggest that minority and low-income women must have enhanced access not only to HPV vaccines, but also to education and other preventive health services to prevent cervical cancer, including Pap screening. Culturally sensitive educational interventions about HPV vaccines are especially important for minority women, as mistrust of medical professionals and the government may underlie concerns about new vaccines among Black women.31-34

In this study sample, measures of recent sexual activity were not independently associated with high-risk HPV infection, whereas lifetime number of sexual partners was associated with infection. Our findings are similar to that of a study of sexually active urban adolescents.19 Number of lifetime partners may be a more reliable and stable measure of exposure to HPV and other STI in adolescent and young adult women because number of recent partners may not be a reliable marker of sexual history; for example, among those with few recent partners, there may be substantial variation in lifetime number of partners. In contrast to the findings related to high-risk HPV infection, no variables were independently associated with vaccine-type HPV infection, supporting current recommendations for universal vaccination.

This study has several limitations. Because participants were predominantly minority and low-income, and because only sexually experienced women were included, the results are not generalizable to all young women eligible for catch-up HPV vaccination. Sexual and gynecologic history was self-reported, possibly limiting validity. We did not include income measures, limiting our ability to explore associations between poverty, race, and HPV infection. The HPV assay used in this study included several high-risk types that are not included in the HPV tests that are commercially available and commonly used in clinical practice; therefore, HPV prevalence in this study may be higher than if a routine clinical test were used. Despite these limitations, this study provides novel data about the prevalence and risk factors associated with type-specific HPV infection in a diverse sample of sexually experienced women, shortly after the quadrivalent HPV vaccine was licensed in the U.S. Our findings provide support for universal vaccination of sexually experienced 13-26 year-old young women in the U.S.

Acknowledgements

The authors would like to acknowledge Dr. Richard Ward and staff in the Laboratory for Specialized Clinical Studies, Division of Infectious Diseases, Cincinnati Children’s Hospital Medical Center, for performing HPV DNA testing.

Conflict of Interest

Funding: Charlotte R. Schmidlapp Women’s Scholar Award, Fifth Third Bank, Cincinnati, OH (J. Kahn, Principal Investigator) R01 AI073713 (J. Kahn, Principal Investigator), and Medical School Training Grant T35 DK 060444 (J. Heubi, Principal Investigator).

Abbreviations

HPV

human papillomavirus

OR

odds ratio

CI

confidence interval

STI

sexually transmitted infection

PCR

polymerase chain reaction

Footnotes

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Competing Interests:

Ms. Shikary: none declared

Dr. Bernstein: none declared

Dr. Jin: none declared

Dr. Zimet is a co-Principal Investigator on an investigator initiated grant funded by Merck and serves as a research consultant/collaborator on a Merck-sponsored research project

Dr. Rosenthal is a co-Principal Investigator on an investigator initiated grant funded by Merck and serves as a research consultant/collaborator on a Merck-sponsored research project and on a Merck advisory board.

Dr. Kahn is a co-Principal Investigator on an NIH-funded HPV vaccine clinical trial in HIV-infected adolescents, for which Merck, Inc., is providing HPV vaccine and immunogenicity testing.

Ethical Approval: The study was approved by the Institutional Review Boards of Cincinnati Children’s Hospital Medical Center and the Cincinnati Health Department

References

  • 1.Walboomers JM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV, et al. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Path. 1999;189:12–19. doi: 10.1002/(SICI)1096-9896(199909)189:1<12::AID-PATH431>3.0.CO;2-F. [DOI] [PubMed] [Google Scholar]
  • 2.Bosch FX, Lorincz A, Munoz N, Meijer CJ, Shah KV. The causal relation between human papillomavirus and cervical cancer. J Clin Pathol. 2002;55:244–65. doi: 10.1136/jcp.55.4.244. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Koulova A, Tsui J, Irwin K, Van Damme P, Biellik R, Aguado MT. Country recommendations on the inclusion of HPV vaccines in national immunization programmes among high-income countries, June 2006-January 2008. Vaccine. 2008;26:6529–41. doi: 10.1016/j.vaccine.2008.08.067. [DOI] [PubMed] [Google Scholar]
  • 4.Harper DM, Franco EL, Wheeler CM, Moscicki AB, Romanowski B, Roteli-Martins CM, et al. Sustained efficacy up to 4.5 years of a bivalent L1 virus-like particle vaccine against human papillomavirus types 16 and 18: follow-up from a randomised control trial. Lancet. 2006;367:1247–55. doi: 10.1016/S0140-6736(06)68439-0. [DOI] [PubMed] [Google Scholar]
  • 5.Villa LL, Costa RL, Petta CA, Andrade RP, Ault KA, Giuliano AR, et al. Prophylactic quadrivalent human papillomavirus (types 6, 11, 16, and 18) L1 virus-like particle vaccine in young women: a randomised double-blind placebo-controlled multicentre phase II efficacy trial. Lancet Oncol. 2005;6:271–8. doi: 10.1016/S1470-2045(05)70101-7. [DOI] [PubMed] [Google Scholar]
  • 6.Goldie SJ, Kohli M, Grima D, Weinstein MC, Wright TC, Bosch FX, et al. Projected clinical benefits and cost-effectiveness of a human papillomavirus 16/18 vaccine. J Natl Cancer Inst. 2004;96:604–15. doi: 10.1093/jnci/djh104. [DOI] [PubMed] [Google Scholar]
  • 7.Goldie SJ, O’Shea M, Campos NG, Diaz M, Sweet S, Kim SY. Health and economic outcomes of HPV 16,18 vaccination in 72 GAVI-eligible countries. Vaccine. 2008;26:4080–93. doi: 10.1016/j.vaccine.2008.04.053. [DOI] [PubMed] [Google Scholar]
  • 8.Garland SM, Hernandez-Avila M, Wheeler CM, Perez G, Harper DM, Leodolter S, et al. Quadrivalent vaccine against human papillomavirus to prevent anogenital diseases. N Engl J Med. 2007;356:1928–43. doi: 10.1056/NEJMoa061760. [DOI] [PubMed] [Google Scholar]
  • 9.Paavonen J, Jenkins D, Bosch FX, Naud P, Salmeron J, Wheeler CM, et al. Efficacy of a prophylactic adjuvanted bivalent L1 virus-like-particle vaccine against infection with human papillomavirus types 16 and 18 in young women: an interim analysis of a phase III double-blind, randomised controlled trial. Lancet. 2007;369:2161–70. doi: 10.1016/S0140-6736(07)60946-5. [DOI] [PubMed] [Google Scholar]
  • 10.Hildesheim A, Herrero R, Wacholder S, Rodriguez AC, Solomon D, Bratti MC, et al. Effect of human papillomavirus 16/18 L1 viruslike particle vaccine among young women with preexisting infection: a randomized trial. JAMA. 2007;298:743–53. doi: 10.1001/jama.298.7.743. [DOI] [PubMed] [Google Scholar]
  • 11.Centers for Disease Control and Prevention Quadrivalent Human Papillomavirus Vaccine: Recommendations of the Advisory Committee on Immunization Practices. Morbidity and Mortality Weekly Report. 2007;56:1–24. [PubMed] [Google Scholar]
  • 12.Krieger N, Quesenberry C, Jr., Peng T, Horn-Ross P, Stewart S, Brown S, et al. Social class, race/ethnicity, and incidence of breast, cervix, colon, lung, and prostate cancer among Asian, Black, Hispanic, and White residents of the San Francisco Bay Area, 1988-92 (United States) Cancer Causes Control. 1999;10:525–37. doi: 10.1023/a:1008950210967. [DOI] [PubMed] [Google Scholar]
  • 13.Freeman HP, Wingrove BK. Excess cervical cancer mortality: a marker for low access to health care in poor communities. National Cancer Institute, Center to Reduce Cancer Health Disparities; Rockville, MD: May, 2005. NIH Pub. No. 05-5282. [Google Scholar]
  • 14.Kahn JA, Lan D, Kahn RS. Sociodemographic Factors Associated With High-Risk Human Papillomavirus Infection. Obstet Gynecol. 2007;110:87–95. doi: 10.1097/01.AOG.0000266984.23445.9c. [DOI] [PubMed] [Google Scholar]
  • 15.Kahn JA, Rosenthal SL, Jin Y, Huang B, Namakydoust A, Zimet GD. Rates of human papillomavirus vaccination, attitudes about vaccination, and human papillomavirus prevalence in young women. Obstet Gynecol. 2008;111:1103–10. doi: 10.1097/AOG.0b013e31817051fa. [DOI] [PubMed] [Google Scholar]
  • 16.Kahn JA, Slap GB, Huang B, Rosenthal SL, Wanchick AM, Kollar LM, et al. Comparison of adolescent and young adult self-collected and clinician-collected samples for human papillomavirus. Obstet Gynecol. 2004;103:952–9. doi: 10.1097/01.AOG.0000124569.61462.8d. [DOI] [PubMed] [Google Scholar]
  • 17.Gravitt PE, Peyton CL, Alessi TQ, Wheeler CM, Coutlee F, Hildesheim A, et al. Improved amplification of genital human papillomaviruses. Journal of Clinical Microbiology. 2000;38:357–61. doi: 10.1128/jcm.38.1.357-361.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Coutlee F, Rouleau D, Ghattas G, Hankins C, Vezina S, Cote P, et al. Confirmatory real-time PCR assay for human papillomavirus (HPV) type 52 infection in anogenital specimens screened for HPV infection with the linear array HPV genotyping test. J Clin Microbiol. 2007;45:3821–3. doi: 10.1128/JCM.01145-07. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Tarkowski TA, Koumans EH, Sawyer M, Pierce A, Black CM, Papp JR, et al. Epidemiology of human papillomavirus infection and abnormal cytologic test results in an urban adolescent population. J Infect Dis. 2004;189:46–50. doi: 10.1086/380466. [DOI] [PubMed] [Google Scholar]
  • 20.Brown DR, Shew ML, Qadadri B, Neptune N, Vargas M, Tu W, et al. A longitudinal study of genital human papillomavirus infection in a cohort of closely followed adolescent women. J Infect Dis. 2005;191:182–92. doi: 10.1086/426867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Dunne EF, Unger ER, Sternberg M, McQuillan G, Swan DC, Patel SS, et al. Prevalence of HPV infection among females in the United States. JAMA. 2007;297:813–19. doi: 10.1001/jama.297.8.813. [DOI] [PubMed] [Google Scholar]
  • 22.Winer RL, Feng Q, Hughes JP, O’Reilly S, Kiviat NB, Koutsky LA. Risk of female human papillomavirus acquisition associated with first male sex partner. J Infect Dis. 2008;197:279–82. doi: 10.1086/524875. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Wright TC, Jr., Huh WK, Monk BJ, Smith JS, Ault K, Herzog TJ. Age considerations when vaccinating against HPV. Gynecol Oncol. 2008;109:S40–7. doi: 10.1016/j.ygyno.2008.02.002. [DOI] [PubMed] [Google Scholar]
  • 24.Chen CA, Liu CY, Chou HH, Chou CY, Ho CM, Twu NF, et al. A Taiwan Cooperative Oncologic Group Study The distribution and differential risks of human papillomavirus genotypes in cervical preinvasive lesions. Int J Gynecol Cancer. 2006;16:1801–8. doi: 10.1111/j.1525-1438.2006.00655.x. [DOI] [PubMed] [Google Scholar]
  • 25.Castellsague Xea., editor. HPV and Cervical Cancer in the World 2007 Report. Vaccine. 2007;25(Suppl 3):C1–230. doi: 10.1016/S0264-410X(07)01183-8. [DOI] [PubMed] [Google Scholar]
  • 26.Vet JN, de Boer MA, van den Akker BE, Siregar B, Lisnawati, Budiningsih S, et al. Prevalence of human papillomavirus in Indonesia: a population-based study in three regions. Br J Cancer. 2008;99:214–8. doi: 10.1038/sj.bjc.6604417. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Ho CM, Chien TY, Huang SH, Lee BH, Chang SF. Integrated human papillomavirus types 52 and 58 are infrequently found in cervical cancer, and high viral loads predict risk of cervical cancer. Gynecol Oncol. 2006;102:54–60. doi: 10.1016/j.ygyno.2005.11.035. [DOI] [PubMed] [Google Scholar]
  • 28.Naucler P, Ryd W, Tornberg S, Strand A, Wadell G, Hansson BG, et al. HPV type-specific risks of high-grade CIN during 4 years of follow-up: a population-based prospective study. Br J Cancer. 2007;97:129–32. doi: 10.1038/sj.bjc.6603843. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Burk RD, Ho GY, Beardsley L, Lempa M, Peters M, Bierman R. Sexual behavior and partner characteristics are the predominant risk factors for genital human Papillomavirus infection in young women. J Infect Dis. 1996;174:679–89. doi: 10.1093/infdis/174.4.679. [DOI] [PubMed] [Google Scholar]
  • 30.Winer RL, Lee SK, Hughes JP, Adam DE, Kiviat NB, Koutsky LA. Genital human papillomavirus infection: incidence and risk factors in a cohort of female university students. Am J Epidemiol. 2003;157:218–26. doi: 10.1093/aje/kwf180. [DOI] [PubMed] [Google Scholar]
  • 31.Shui I, Kennedy A, Wooten K, Schwartz B, Gust D. Factors influencing African-American mothers’ concerns about immunization safety: a summary of focus group findings. J Natl Med Assoc. 2005;97:657–66. [PMC free article] [PubMed] [Google Scholar]
  • 32.Shui IM, Weintraub ES, Gust DA. Parents concerned about vaccine safety: Differences in race/ethnicity and attitudes. Am J Prev Med. 2006;31:244–51. doi: 10.1016/j.amepre.2006.04.006. [DOI] [PubMed] [Google Scholar]
  • 33.Newman PA, Duan N, Roberts KJ, Seiden D, Rudy ET, Swendeman D, et al. HIV vaccine trial participation among ethnic minority communities: barriers, motivators, and implications for recruitment. J Acquir Immune Defic Syndr. 2006;41:210–7. doi: 10.1097/01.qai.0000179454.93443.60. [DOI] [PubMed] [Google Scholar]
  • 34.Moutsiakis DL, Chin PN. Why blacks do not take part in HIV vaccine trials. J Natl Med Assoc. 2007;99:254–7. [PMC free article] [PubMed] [Google Scholar]

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