A prospective study of absolute risk and determinants of human papillomavirus incidence among young women in Costa Rica

Megan Clarke, Mark Schiffman, Sholom Wacholder, Ana Cecilia Rodriguez, Allan Hildesheim, Wim Quint, Costa Rican Vaccine Trial Group, Mario Alfaro, Manuel Barrantes, M Concepcion Bratti, Fernando Cárdenas, Bernal Cortés, Albert Espinoza, Yenory Estrada, Paula Gonzalez, Diego Guillén, Rolando Herrero, Silvia E Jimenez, Jorge Morales, Lidia Ana Morera, Elmer Pérez, Carolina Porras, Ana Cecilia Rodriguez, Maricela Villegas, Enrique Freer, Jose Bonilla, Sandra Silva, Ivannia Atmella, Margarita Ramírez, Nora Macklin, Allan Hildesheim, Douglas R Lowy, Mark Schiffman, John T Schiller, Mark Sherman, Diane Solomon, Sholom Wacholder, Ligia Pinto, Alfonso Garcia-Pineres, Claire Eklund, Martha Hutchinson, Wim Quint, Leen-Jan van Doorn, Catherine Bougelet, Megan Clarke, Mark Schiffman, Sholom Wacholder, Ana Cecilia Rodriguez, Allan Hildesheim, Wim Quint, Costa Rican Vaccine Trial Group, Mario Alfaro, Manuel Barrantes, M Concepcion Bratti, Fernando Cárdenas, Bernal Cortés, Albert Espinoza, Yenory Estrada, Paula Gonzalez, Diego Guillén, Rolando Herrero, Silvia E Jimenez, Jorge Morales, Lidia Ana Morera, Elmer Pérez, Carolina Porras, Ana Cecilia Rodriguez, Maricela Villegas, Enrique Freer, Jose Bonilla, Sandra Silva, Ivannia Atmella, Margarita Ramírez, Nora Macklin, Allan Hildesheim, Douglas R Lowy, Mark Schiffman, John T Schiller, Mark Sherman, Diane Solomon, Sholom Wacholder, Ligia Pinto, Alfonso Garcia-Pineres, Claire Eklund, Martha Hutchinson, Wim Quint, Leen-Jan van Doorn, Catherine Bougelet

Abstract

Background: High risk human papillomaviruses (HR-HPV) are known to be extremely common, sexually transmitted infections, but more information is needed regarding the absolute risks of type-specific HR-HPV infections in the years following sexual debut.

Methods: We conducted a survival analysis of 3,737 women aged 18-25 from the control group of the Costa Rican Vaccine trial to determine the absolute risks of HR-HPV infections at 12 months, 24 months, and end of follow-up (average of 50.7 months). To corroborate determinants of infection, we used Cox proportional hazards methods to assess associations between demographics and sexual risk behaviors and incident HR-HPV.

Results: Cumulative incidence for HR-HPV infections was 51.3% at the end of the study period. The most common incident types were HPV52 (15.4%), HPV51 (13.6%), and HPV16 (12.4%). Type-specific cumulative incidence corresponded closely with type-specific prevalences, except that HPV16 was more prevalent than predicted by incidence, suggesting greater persistence. The strongest predictors of incident HR-HPV infections as a group in a multivariate analysis were the expected correlates of sexual behavior of the woman and her partner, such as being single (HR 1.6, 95% CI 1.4-1.8) or divorced/widowed (HR: 2.1, 95% CI: 1.7-2.7), having multiple HPV infections at enrollment (HR: 1.5, 95% CI: 1.3-1.7), and current smoking (HR: 1.2, 95% CI: 1.0-1.3). In women who reported being having only one lifetime sexual partner (being in a monogamous relationship), the strongest predictors of HR-HPV included not living with sex partner (HR: 2.1, 95% CI 1.7-2.5) and age of sex partner (HR: 1.4, 95% CI: 1.0-1.8).

Conclusion: We confirm the extremely high incidence of HR-HPV in young women, emphasizing the importance of vaccinating young girls before sexual debut.

Trial registration: ClinicalTrials.gov NCT00128661.

Figures

Figure 1
Figure 1
A plot of the percent prevalence versus percent cumulative incidence by HR-HPV type.

References

    1. 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;197:279–282. doi: 10.1086/524875.
    1. Burchell AN, Winer RL, de Sanjose S, Franco EL. Chapter 6: epidemiology and transmission dynamics of genital HPV infection. Vaccine. 2006;24(Suppl 3:S3):52–61.
    1. Ho GY, Bierman R, Beardsley L, Chang CJ, Burk RD. Natural history of cervicovaginal papillomavirus infection in young women. N Engl J Med. 1998;338:423–428. doi: 10.1056/NEJM199802123380703.
    1. Kemp TJ, Hildesheim A, Safaeian M, Dauner JG, Pan Y, Porras C, Schiller JT, Lowy DR, Herrero R, Pinto LA. HPV16/18 L1 VLP vaccine induces cross-neutralizing antibodies that may mediate cross-protection. Vaccine. 2011;29:2011–2014. doi: 10.1016/j.vaccine.2011.01.001.
    1. 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;174:679–689. doi: 10.1093/infdis/174.4.679.
    1. Winer RL, Hughes JP, Feng Q, O'Reilly S, Kiviat NB, Holmes KK, Koutsky LA. Condom use and the risk of genital human papillomavirus infection in young women. N Engl J Med. 2006;354:2645–2654. doi: 10.1056/NEJMoa053284.
    1. Wawer MJ, Tobian AA, Kigozi G, Kong X, Gravitt PE, Serwadda D, Nalugoda F, Makumbi F, Ssempiija V, Sewankambo N. et al.Effect of circumcision of HIV-negative men on transmission of human papillomavirus to HIV-negative women: a randomised trial in rakai, uganda. Lancet. 2011;377:209–218. doi: 10.1016/S0140-6736(10)61967-8.
    1. Herrero R, Hildesheim A, Rodriguez AC, Wacholder S, Bratti C, Solomon D, Gonzalez P, Porras C, Jimenez S, Guillen D. et al.Rationale and design of a community-based double-blind randomized clinical trial of an HPV 16 and 18 vaccine in guanacaste, costa rica. Vaccine. 2008;26:4795–4808. doi: 10.1016/j.vaccine.2008.07.002.
    1. Giuliano AR, Harris R, Sedjo RL, Baldwin S, Roe D, Papenfuss MR, Abrahamsen M, Inserra P, Olvera S, Hatch K. Incidence, prevalence, and clearance of type-specific human papillomavirus infections: the young Women's health study. J Infect Dis. 2002;186:462–469. doi: 10.1086/341782.
    1. Nielsen A, Iftner T, Munk C, Kjaer SK. Acquisition of high-risk human papillomavirus infection in a population-based cohort of danish women. Sex Transm Dis. 2009;36:609–615. doi: 10.1097/OLQ.0b013e3181a96d0e.
    1. Muñoz N, Méndez F, Posso H, Molano M, Van Den Brule AJC, Ronderos M, Meijer C, Muñoz Á. Incidence, duration, and determinants of cervical human papillomavirus infection in a cohort of colombian women with normal cytological results. J Infect Dis. 2004;190:2077–2087. doi: 10.1086/425907.
    1. Franco EL, Villa LL, Sobrinho JP, Prado JM, Rousseau MC, Désy M, Rohan TE. Epidemiology of acquisition and clearance of cervical human papillomavirus infection in women from a high-risk area for cervical cancer. J Infect Dis. 1999;180:1415–1423. doi: 10.1086/315086.
    1. Moscicki AB, Hills N, Shiboski S, Powell K, Jay N, Hanson E, Miller S, Clayton L, Farhat S, Broering J. et al.Risks for incident human papillomavirus infection and low-grade squamous intraepithelial lesion development in young females. JAMA. 2001;285:2995–3002. doi: 10.1001/jama.285.23.2995.
    1. de Sanjose S, Bosch FX, Munoz N, Shah K. Social differences in sexual behaviour and cervical cancer. IARC Sci Publ. 1997. pp. 309–317.
    1. Ferreccio C, Prado RB, Luzoro AV, Ampuero SL, Snijders PJ, Meijer CJ, Vaccarella SV, Jara AT, Puschel KI, Robles SC. et al.Population-based prevalence and age distribution of human papillomavirus among women in santiago, chile. Cancer Epidemiol Biomarkers Prev. 2004;13:2271–2276.
    1. Chan PK, Chang AR, Cheung JL, Chan DP, Xu LY, Tang NL, Cheng AF. Determinants of cervical human papillomavirus infection: differences between high- and low-oncogenic risk types. J Infect Dis. 2002;185:28–35. doi: 10.1086/338010.
    1. Sopori M. Effects of cigarette smoke on the immune system. Nat Rev Immunol. 2002;2:372–377. doi: 10.1038/nri803.
    1. Goodman MT, Shvetsov YB, McDuffie K, Wilkens LR, Zhu X, Thompson PJ, Ning L, Killeen J, Kamemoto L, Hernandez BY. Prevalence, acquisition, and clearance of cervical human papillomavirus infection among women with normal cytology: hawaii human papillomavirus cohort study. Cancer Research. 2008;68:8813–8824. doi: 10.1158/0008-5472.CAN-08-1380.
    1. Sellors JW, Karwalajtys TL, Kaczorowski J, Mahony JB, Lytwyn A, Chong S, Sparrow J, Lorincz A. Incidence, clearance and predictors of human papillomavirus infection in women. CMAJ. 2003;168:421–425.
    1. Lazcano-Ponce E, Herrero R, Munoz N, Cruz A, Shah KV, Alonso P, Hernandez P, Salmeron J, Hernandez M. Epidemiology of HPV infection among mexican women with normal cervical cytology. Int J Cancer. 2001;91:412–420. doi: 10.1002/1097-0215(20010201)91:3<412::AID-IJC1071>;2-M.
    1. Peyton CL, Gravitt PE, Hunt WC, Hundley RS, Zhao M, Apple RJ, Wheeler CM. Determinants of genital human papillomavirus detection in a US population. J Infect Dis. 2001;183:1554–1564. doi: 10.1086/320696.
    1. Marks M, Gravitt PE, Gupta SB, Liaw KL, Tadesse A, Kim E, Phongnarisorn C, Wootipoom V, Yuenyao P, Vipupinyo C. et al.Combined oral contraceptive use increases HPV persistence but not new HPV detection in a cohort of women from thailand. J Infect Dis. 2011;204:1505–1513. doi: 10.1093/infdis/jir560.
    1. Tobian AA, Gray RH. Male foreskin and oncogenic human papillomavirus infection in men and their female partners. Future Microbiol. 2011;6:739–745. doi: 10.2217/fmb.11.59.
    1. Castellsague X, Bosch FX, Munoz N, Meijer CJ, Shah KV, de Sanjose S, Eluf-Neto J, Ngelangel CA, Chichareon S, Smith JS. et al.Male circumcision, penile human papillomavirus infection, and cervical cancer in female partners. N Engl J Med. 2002;346:1105–1112. doi: 10.1056/NEJMoa011688.
    1. Albero G, Castellsague X, Giuliano AR, Bosch FX. Male circumcision and genital human papillomavirus: a systematic review and meta-analysis. Sex Transm Dis. 2012;39:104–113. doi: 10.1097/OLQ.0b013e3182387abd.
    1. Rylander E, Ruusuvaara L, Almstromer MW. et al.The absence of vaginal human papillomavirus 16 DNA in women who have not experienced sexual intercourse. Obstet Gynecol. 1994;83:735–737.
    1. Winer RL, Lee S, 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;157:218–226. doi: 10.1093/aje/kwf180.
    1. United Nations Department of Economic and Social Affairs Population Division. World contraceptive Use 2009. Geneva, Switzerland: World Health Organization HIV/AIDS Department; 2007. Available at . Accessed February 20, 2013.
    1. United Nations, Department of Economic and Social Affairs, Population Division. World Contraceptive Use 2009 (POP/DB/CP/Rev2009) New York, NY; 2009.

Source: PubMed

3
Subscribe