The objective of this study was to determine human papillomavirus (HPV) prevalence and identify factors associated with infection in sexually experienced and inexperienced females initiating HPV vaccination.
Methods
Participants were 13- to 21-year-old females receiving their first HPV vaccine dose, recruited from an adolescent primary care clinic between June 2008 and June 2010. These data are from the baseline visit of a longitudinal study that was approved by the hospital’s institutional review board. Each participant completed a questionnaire assessing sociodemographic factors and behaviors. History of sexual contact was assessed using the following item: “Have you ever had sexual contact with a male or female (by sexual contact we mean genital, skin-to-skin contact only)?” Sexual experience was defined as a response of yes to the following item: “Have you ever had sex with a male or female (by sex we mean vaginal or anal sex)?” Cervicovaginal swabs were self- or clinician-collected and tested for HPV DNA.1,2 Logistic regression models were estimated to determine variables associated with HPV infection in sexually experienced and inexperienced females. The outcome measure was infection with 1 or more HPV types.
Results
Of the 259 eligible females, 190 (73.4%) were sexually experienced. Sexually experienced females were older than sexually inexperienced females (mean [SD] age, 17.6 [2.2] years vs 14.8 [1.3] years; P<.001); there were no significant differences by race or health insurance coverage. Seventy-eight percent of females were African American, 16.6% reported having no health insurance, and 75.2% had public insurance. Among sexually experienced females, the mean (SD) number of lifetime male sexual partners was 5.7 (7.3), 40.7% reported a history of Chlamydia, and 24.3% reported a history of gonorrhea. Thirteen percent of sexually inexperienced females reported a history of sexual contact, and none reported a history of Chlamydia or gonorrhea.
All swabs tested for HPV DNA were adequate for analyses, defined as positive for β-globin. The prevalence of HPV in sexually experienced and inexperienced females is shown in the Table. Among sexually experienced females, 70.0% (133 of 190) were HPV positive (≥1 type): 17.4% (33 of 190) for HPV-16 and 6.3% (12 of 190) for HPV-18. The only variable independently associated with HPV in a multivariable model was history of multiple sexual partners (2-5 partners vs 1: odds ratio, 6.2; 95% CI, 2.1-18.1 and ≥6 partners vs 1: odds ratio, 10.3; 95% CI, 2.6-41.5).
Table.
Overall and Type-Specific HPV Infection at the Time of HPV Vaccine Initiation in 13- to 21-Year-Old Females, by Sexual Experience
| No. (%) |
||||
|---|---|---|---|---|
| Total (N = 259) |
Sexually Experienced (n = 190) |
Sexually Inexperienced (n = 69) |
P Value | |
| No. of HPV types detected, mean (SD) [range] | 1.7 (2.3) [0-12] | 2.3 (2.4) [0-12] | 0.2 (0.7) [0-3] | |
| Overall HPVa | 141 (54.4) | 133 (70.0) | 8 (11.6) | <.001b |
| Bivalent vaccine typesc | 42 (16.2) | 40 (21.1) | 2 (2.9) | <.001d |
| Quadrivalent vaccine typese | 61 (23.6) | 58 (30.5) | 3 (4.3) | <.001d |
| Nonavalent vaccine typesf | 90 (34.7) | 85 (44.7) | 5 (7.2) | <.001d |
| Multiple typesg | 103 (39.8) | 98 (51.6) | 5 (7.2) | <.001d |
| At least 1 high-risk typeh | 111 (42.9) | 105 (55.3) | 6 (8.7) | <.001d |
| High-risk types other than HPV-16 and HPV-18h | 98 (37.8) | 93 (48.9) | 5 (7.2) | <.001d |
| HPV-6 | 20 (7.7) | 19 (10.0) | 1 (1.4) | .02d |
| HPV-11 | 5 (1.9) | 4 (2.1) | 1 (1.4) | >.99d |
| HPV-16 | 35 (13.5) | 33 (17.4) | 2 (2.9) | .002d |
| HPV-18 | 12 (4.6) | 12 (6.3) | 0 | NA |
| HPV-26 | 4 (1.5) | 4 (2.1) | 0 | NA |
| HPV-31 | 7 (2.7) | 7 (3.7) | 0 | NA |
| HPV-33 | 1 (0.4) | 1 (0.5) | 0 | NA |
| HPV-35 | 16 (6.2) | 16 (8.4) | 0 | NA |
| HPV-39 | 16 (6.2) | 16 (8.4) | 0 | NA |
| HPV-40 | 10 (3.9) | 10 (5.3) | 0 | NA |
| HPV-42 | 18 (6.9) | 18 (9.5) | 0 | NA |
| HPV-45 | 11 (4.2) | 11 (5.8) | 0 | NA |
| HPV-51 | 15 (5.8) | 14 (7.4) | 1 (1.4) | .08d |
| HPV-52 | 22 (8.5) | 21 (11.1) | 1 (1.4) | .01d |
| HPV-53 | 17 (6.6) | 17 (8.9) | 0 | NA |
| HPV-54 | 11 (4.2) | 11 (5.8) | 0 | NA |
| HPV-55 | 9 (3.5) | 9 (4.7) | 0 | NA |
| HPV-56 | 13 (5.0) | 12 (6.3) | 1 (1.4) | .19d |
| HPV-58 | 24 (9.3) | 23 (12.1) | 1 (1.4) | .007d |
| HPV-59 | 21 (8.1) | 20 (10.5) | 1 (1.4) | .02d |
| HPV-61 | 7 (2.7) | 6 (3.2) | 1 (1.4) | .68d |
| HPV-62 | 20 (7.7) | 20 (10.5) | 0 | NA |
| HPV-64 | 1 (0.4) | 1 (0.5) | 0 | NA |
| HPV-66 | 21 (8.1) | 20 (10.5) | 1 (1.4) | .02d |
| HPV-67 | 6 (2.3) | 6 (3.2) | 0 | NA |
| HPV-68 | 16 (6.2) | 14 (7.4) | 2 (2.9) | .25d |
| HPV-69 | 0 | 0 | 0 | NA |
| HPV-70 | 3 (1.2) | 2 (1.1) | 1 (1.4) | >.99d |
| HPV-71 | 0 | 0 | 0 | NA |
| HPV-72 | 1 (0.4) | 1 (0.5) | 0 | NA |
| HPV-73 | 11 (4.2) | 11 (5.8) | 0 | NA |
| HPV-81 | 8 (3.1) | 7 (3.7) | 1 (1.4) | .69d |
| HPV-82 | 6 (2.3) | 6 (3.2) | 0 | NA |
| HPV-83 | 14 (5.4) | 14 (7.4) | 0 | NA |
| HPV-84 | 21 (8.1) | 20 (10.5) | 1 (1.4) | .02d |
| HPV-IS39 | 2 (0.8) | 2 (1.1) | 0 | NA |
| HPV-CP610 | 20 (7.7) | 20 (10.5) | 0 | NA |
Abbreviations: HPV, human papillomavirus; NA, not applicable because one or more categories had no subjects.
Overall HPV = positivity for 1 or more HPV types.
χ2 Test.
Bivalent vaccine types = positivity for HPV-16 and/or HPV-18.
Fisher exact test.
Quadrivalent vaccine types = positive for HPV-16, HPV-18, HPV-6, and/or HPV-11.
Nonavalent vaccine types = positive for HPV-16, HPV-18, HPV-6, HPV-11, HPV-31, HPV-33, HPV-45, HPV-52, and/or HPV-58.
Multiple types = positive for 2 or more HPV types.
High-risk HPV types = 16, 18, 31, 33, 35, 39, 45, 51, 52, 53, 56, 58, 59, and 68.
Among sexually inexperienced females, 11.6% (8 of 69) were HPV infected: 2.9% (2 of 69) for HPV-16, 0% for HPV-18, and 4.3% (3 of 69) for any vaccine-type HPV. Human papillomavirus types 16 and 68, each detected in 2.9% (2 of 69), were the most commonly detected types. Five participants (62.5%) had multiple types: 2 had 2 types and 3 had 3 types. No variables were significantly associated with HPV in sexually inexperienced females.
Comment
The prevalence of HPV in this population was higher than that reported in a nationally representative sample of young women, likely because of differences in sexual behaviors in the 2 populations studied.3 As expected, sexually inexperienced females had lower rates of HPV than sexually experienced females; however, a subgroup of sexually inexperienced females was positive for both vaccine and nonvaccine types. Our finding that 11.6% of sexually inexperienced females were positive for at least 1 HPV type is consistent with findings of previous studies that enrolled females who were likely to have had sexual contact.4-6 We found that 4.3% of sexually inexperienced females were already infected with vaccine-type HPV, potentially through hand-genital or genital, skin-to-skin contact. This demonstrates that sexually inexperienced females are at risk for HPV infection and supports national recommendations to target HPV vaccination to 11- to 12-year-old girls. Clinicians and parents should not delay HPV vaccination because an adolescent is not sexually active.
Acknowledgments
Financial Disclosure: Dr Brown receives honoraria for lectures related to HPV and vaccination from Merck and Co Inc. These honoraria are donated to charities. Dr Brown’s laboratory is funded in part by a grant from Merck and Co Inc. Indiana University and Merck and Co Inc have a confidential agreement that pays the university based on certain landmarks of vaccine development. Dr Brown receives a portion of these payments as income. Dr Brown serves on the Women’s Health Advisory Board at Merck and Co Inc. Dr Shew is an investigator for Merck and Co Inc–related vaccine trials. Dr Fortenberry received a 1-time honorarium for delivery of educational material, not related to the content of this article, from Merck and Co Inc, makers of a quadrivalent HPV vaccine. Dr Kahn serves as co-chair of 2 clinical trials of the quadrivalent HPV vaccine in HIV-infected individuals. The trials are funded by the National Institutes of Health but Merck and Co Inc is providing vaccine and immunogenicity testing for both. She also chairs a grant review committee for the Society for Adolescent Health and Medicine; the grant mechanism is funded through Merck and Co Inc.
Footnotes
Author Contributions: Study concept and design: Widdice, Bernstein, Shew, Fortenberry, and Kahn. Acquisition of data: Brown, Patel, and Kahn. Analysis and interpretation of data: Widdice, Brown, Bernstein, Ding, Fortenberry, and Kahn. Drafting of the manuscript: Widdice, Bernstein, Patel, and Fortenberry. Critical revision of the manuscript for important intellectual content: Widdice, Brown, Bernstein, Ding, Patel, Shew, Fortenberry, and Kahn. Statistical analysis: Widdice and Ding. Obtained funding: Fortenberry and Kahn. Administrative, technical, and material support: Widdice, Patel, and Fortenberry. Study supervision: Widdice, Bernstein, and Kahn.
References
- 1.Kahn JA, Slap GB, Huang B, et al. Comparison of adolescent and young adult self-collected and clinician-collected samples for human papillomavirus. Obstet Gynecol. 2004;103(5, pt 1):952–959. doi: 10.1097/01.AOG.0000124569.61462.8d. [DOI] [PubMed] [Google Scholar]
- 2.Brown DR, Legge D, Qadadri B. Distribution of human papillomavirus types in cervicovaginal washings from women evaluated in a sexually transmitted diseases clinic. Sex Transm Dis. 2002;29(12):763–768. doi: 10.1097/00007435-200212000-00005. [DOI] [PubMed] [Google Scholar]
- 3.Forhan SE, Gottlieb SL, Sternberg MR, et al. Prevalence of sexually transmitted infections among female adolescents aged 14 to 19 in the United States. Pediatrics. 2009;124(6):1505–1512. doi: 10.1542/peds.2009-0674. [DOI] [PubMed] [Google Scholar]
- 4.Ley C, Bauer HM, Reingold A, et al. Determinants of genital human papillomavirus infection in young women. J Natl Cancer Inst. 1991;83(14):997–1003. doi: 10.1093/jnci/83.14.997. [DOI] [PubMed] [Google Scholar]
- 5.Oh JK, Ju YH, Franceschi S, Quint W, Shin HR. Acquisition of new infection and clearance of type-specific human papillomavirus infections in female students in Busan, South Korea: a follow-up study. BMC Infect Dis. 2008;8:13. doi: 10.1186/1471-2334-8-13. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Weaver B, Shew M, Qadadri B, et al. Natural history of multiple human papillomavirus infections in female adolescents with prolonged follow-up. J Adolesc Health. 2011;48(5):473–480. doi: 10.1016/j.jadohealth.2010.08.003. [DOI] [PubMed] [Google Scholar]