Risk of seropositivity to multiple oncogenic human papillomavirus types among human immunodeficiency virus-positive and-negative Ugandan women

Journal of General Virology

Volumn 92, Issue 12, 2011, Pages 2776-2783

  Namujju, P B ^a,b,c   Waterboer, T ^d   Banura, C ^e   Muwonge, R ^f   Mbidde, E K ^b   Byaruhanga, R ^g   Muwanga, M ^h   Surcel, H M ^a   Pawlita, M ^d   Lehtinen, M ^c  

^a NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

^b UGANDA VIRUS RESEARCH INSTITUTE   (Uganda)

^c TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^d GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^e MAKERERE UNIVERSITY COLLEGE OF HEALTH SCIENCES   (Uganda)

^f INTERNATIONAL AGENCY FOR RESEARCH ON CANCER   (France)

^g St Francis Hospital Uganda   (Uganda)

^h Entebbe Hospital   (Uganda)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; CONFIDENCE INTERVAL; FEMALE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MULTIVARIATE LOGISTIC REGRESSION ANALYSIS; PRENATAL PERIOD; PRIORITY JOURNAL; UTERINE CERVIX CANCER; WART VIRUS;

ADOLESCENT; ADULT; ANTIBODIES, VIRAL; CONFIDENCE INTERVALS; DEVELOPING COUNTRIES; FEMALE; GENOTYPE; HIV SERONEGATIVITY; HIV SEROPOSITIVITY; HUMANS; LOGISTIC MODELS; MULTIVARIATE ANALYSIS; ODDS RATIO; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; PREGNANCY; QUESTIONNAIRES; RISK FACTORS; SEROEPIDEMIOLOGIC STUDIES; UGANDA; YOUNG ADULT;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN PAPILLOMAVIRUS; HUMAN PAPILLOMAVIRUS TYPES;

EID: 81255188957     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.035923-0     Document Type: Article

References (42)

1. af Geijersstam, V., Kibur, M., Wang, Z., Koskela, P., Pukkala, E., Schiller, J., Lehtinen, M. & Dillner, J. (1998). Stability over time of serum antibody levels to human papillomavirus type 16. J Infect Dis 177, 1710-1714.
2. Ault, K. A. & Future II Study Group (2007). Effect of prophylactic human papillomavirus L1 virus-like-particle vaccine on risk of cervical intraepithelial neoplasia grade 2, grade 3, and adenocarcinoma in situ: a combined analysis of four randomised clinical trials. Lancet 369, 1861-1868.
3. Banura, C., Franceschi, S., van Doorn, L. J., Arslan, A., Kleter, B., Wabwire-Mangen, F., Mbidde, E. K., Quint, W. & Weiderpass, E. (2008). Prevalence, incidence and clearance of human papillomavirus infection among young primiparous pregnant women in Kampala, Uganda. Int J Cancer 123, 2180-2187.
4. Banura, C., Franceschi, S., Doorn, L. J., Arslan, A., Wabwire-Mangen, F., Mbidde, E. K., Quint, W. & Weiderpass, E. (2008). Infection with human papillomavirus and HIV among young women in Kampala, Uganda. J Infect Dis 197, 555-562.
5. Banura, C., Sandin, S., van Doorn, L. J., Quint, W., Kleter, B., Wabwire-Mangen, F., Mbidde, E. K. & Weiderpass, E. (2010). Typespecific incidence, clearance and predictors of cervical human papillomavirus infections (HPV) among young women: a prospective study in Uganda. Infect Agent Cancer 5: 7.
6. Blossom, D. B., Beigi, R. H., Farrell, J. J., Mackay, W., Qadadri, B., Brown, D. R., Rwambuya, S., Walker, C. J., Kambugu, F. S. (2007). Human papillomavirus genotypes associated with cervical cytologic abnormalities and HIV infection in Ugandan women. J Med Virol 79, 758-765.
7. Brown, D. R., Kjaer, S. K., Sigurdsson, K., Iversen, O. E., Hernandez-Avila, M., Wheeler, C. M., Perez, G., Koutsky, L. A., Tay, E. H. (2009). The impact of quadrivalent human papillomavirus (HPV; types 6, 11, 16, and 18) L1 virus-like particle vaccine on infection and disease due to oncogenic nonvaccine HPV types in generally HPVnaive women aged 16-26 years. J Infect Dis 199, 926-935.
8. Carter, J. J., Koutsky, L. A., Hughes, J. P., Lee, S. K., Kuypers, J., Kiviat, N. & Galloway, D. A. (2000). Comparison of human papillomavirus types 16, 18, and 6 capsid antibody responses following incident infection. J Infect Dis 181, 1911-1919.
9. Clifford, G. M., Goncalves, M. A., Franceschi, S. & HPV and HIV Study Group (2006). Human papillomavirus types among women infected with HIV: a meta-analysis. AIDS 20, 2337-2344.
10. Clifford, G. M., Shin, H. R., Oh, J. K., Waterboer, T., Ju, Y. H., Vaccarella, S., Quint, W., Pawlita, M. & Franceschi, S. (2007). Serologic response to oncogenic human papillomavirus types in male and female university students in Busan, South Korea. Cancer Epidemiol Biomarkers Prev 16, 1874-1879.
11. Clifton, D. (2009). Combating cross-generational sex in Uganda. Washington DC: Population Reference Bureau. www.prb.org/Articles/2009/crossgenerationalsex.aspx (accessed January 2010).
12. De Vuyst, H., Lillo, F., Broutet, N. & Smith, J. S. (2008). HIV, human papillomavirus, and cervical neoplasia and cancer in the era of highly active antiretroviral therapy. Eur J Cancer Prev 17, 545-554.
13. Dillner, J., Kallings, I., Brihmer, C., Sikström, B., Koskela, P., Lehtinen, M., Schiller, J. T., Sapp, M. & Mardh, P. A. (1996). Seropositivities to human papillomavirus types 16, 18, or 33 capsids and to Chlamydia trachomatis are markers of sexual behavior. J Infect Dis 173, 1394-1398.
14. Dondog, B., Clifford, G.M., Vaccarella, S., Waterboer, T., Unurjargal, D., Avirmed, D., Enkhtuya, S., Kommoss, F., Wentzensen, N. (2008). Human papillomavirus infection in Ulaanbaatar, Mongolia: a population-based study. Cancer Epidemiol Biomarkers Prev 17, 1731-1738.
15. Ho, G. Y., Studentsov, Y., Hall, C. B., Bierman, R., Beardsley, L., Lempa, M. & Burk, R. D. (2002). Risk factors for subsequent cervicovaginal human papillomavirus (HPV) infection and the protective role of antibodies to HPV-16 virus-like particles. J Infect Dis 186, 737-742.
16. Ho, G. Y., Studentsov, Y. Y., Bierman, R. & Burk, R. D. (2004). Natural history of human papillomavirus type 16 virus-like particle antibodies in young women. Cancer Epidemiol Biomarkers Prev 13, 110-116.
17. Kaasila, M., Koskela, P., Kirnbauer, R., Pukkala, E., Surcel, H.-M. & Lehtinen, M. (2009). Population dynamics of serologically identified coinfections with human papillomavirus types 11, 16, 18 and 31 in fertile-aged Finnish women. Int J Cancer 125, 2166-2172.
18. Katahoire, R. A., Jitta, J., Kivumbi, G., Murokora, D., Arube, W. J., Siu, G., Arinaitwe, L., Bingham, A., Mugisha, E. (2008). An assessment of the readiness for introduction of the HPV vaccine in Uganda. Afr J Reprod Health 12, 159-172.
19. Kibur, M., Koskela, P., Dillner, J., Leinikki, P., Saikku, P., Lehtinen, M. & Hakama, M. (2000). Seropositivity to multiple sexually transmitted infections is not common. Sex Transm Dis 27, 425-430.
20. Kizito, D., Woodburn, P. W., Kesande, B., Ameke, C., Nabulime, J., Muwanga, M., Grosskurth, H. & Elliott, A. M. (2008). Uptake of HIV and syphilis testing of pregnant women and their male partners in a programme for prevention of mother-to-child HIV transmission in Uganda. Trop Med Int Health 13, 680-682.
21. Kjellberg, L., Wang, Z., Wiklund, F., Edlund, K., Angström, T., Lenner, P., Sjöberg, I., Hallmans, G., Wallin, K. L. (1999). Sexual behaviour and papillomavirus exposure in cervical intraepithelial neoplasia: a population-based case-control study. J Gen Virol 80, 391-398.
22. Merikukka, M., Kaasila, M., Namujju, P. B., Palmroth, J., Kirnbauer, R., Paavonen, J., Surcel, H. M. & Lehtinen, M. (2011). Differences in incidence and co-occurrence of vaccine and non-vaccine human papillomavirus (HPV) types in Finnish population before HPV mass vaccination suggest competitive advantage for HPV33. Int J Cancer 128, 1114-1119.
23. Michael, K. M., Waterboer, T., Pfister, H., Gariglio, M., Majewski, S., Favre, M. & Pawlita, M. (2010). Seroreactivity of 38 human papillomavirus types in epidermodysplasia verruciformis patients, relatives, and controls. J Invest Dermatol 130, 841-848.
24. Molano, M., Van den Brule, A., Plummer, M., Weiderpass, E., Posso, H., Arslan, A., Meijer, C. J., Muñoz, N., Franceschi, S. & HPV Study Group (2003). Determinants of clearance of human papillomavirus infections in Colombian women with normal cytology: a population-based, 5-year follow-up study. Am J Epidemiol 158, 486-494.
25. Moscicki, A. B., Ellenberg, J. H., Farhat, S. & Xu, J. (2004). Persistence of human papillomavirus infection in HIV-infected and-uninfected adolescent girls: risk factors and differences, by phylogenetic type. J Infect Dis 190, 37-45.
26. Mpairwe, H., Muhangi, L., Namujju, P. B., Kisitu, A., Tumusiime, A., Muwanga, M., Whitworth, J. A., Onyango, S., Biryahwaho, B. & Elliott, A. M. (2005). HIV risk perception and prevalence in a program for prevention of mother-to-child HIV transmission: comparison of women who accept voluntary counseling and testing and those tested anonymously. J Acquir Immune Defic Syndr 39, 354-358.
27. Namujju, P. B., Surcel, H.-M., Kirnbauer, R., Kaasila, M., Banura, C., Byaruhanga, R., Muwanga, M., Mbidde, E. K., Koskela, P. & Lehtinen, M. (2010). Risk of being seropositive for multiple human papillomavirus types among Finnish and Ugandan women. Scand J Infect Dis 42, 522-526.
28. Namujju, P. B., Hedman, L., Hedman, K., Banura, C., Mbidde, E. K., Kizito, D., Byaruhanga, R. N., Muwanga, M., Kirnbauer, R. (2011). Low avidity of human papillomavirus (HPV) type 16 antibodies is associated with increased risk of low-risk but not highrisk HPV type prevalence. BMC Res Notes 4, 170.
29. Odida, M., de Sanjose ́, S., Quint, W., Bosch, X. F., Klaustermeier, J. & Weiderpass, E. (2008). Human papillomavirus type distribution in invasive cervical cancer in Uganda. BMC Infect Dis 8, 85.
30. Paavonen, J., Naud, P., Salmerón, J., Wheeler, C. M., Chow, S. N., Apter, D., Kitchener, H., Castellsague, X., Teixeira, J. C. (2009). Efficacy of human papillomavirus (HPV)-16/18 AS04-adjuvanted vaccine against cervical infection and precancer caused by oncogenic HPV types (PATRICIA): final analysis of a double-blind, randomised study in young women. Lancet 374, 301-314.
31. Palmroth, J., Namujju, P., Simen-Kapeu, A., Kataja, V., Surcel, H.-M., Tuppurainen, M., Yliskoski, M., Syrjänen, K. & Lehtinen, M. (2010). Natural seroconversion to high-risk human papillomaviruses (hrHPVs) is not protective against related HPV genotypes. Scand J Infect Dis 42, 379-384.
32. Parkin, D. M., Whelan, S. L., Ferlay, J., Teppo, L. & Thomas, D. (editors) (2002). Cancer Incidence in Five Continents, vol. VIII, edn 155. Lyon, France: IARC Scientific Publication.
33. Safaeian, M., Kiddugavu, M., Gravitt, P. E., Gange, S. J., Ssekasanvu, J., Murokora, D., Sklar, M., Serwadda, D., Wawer, M. J. (2008). Determinants of incidence and clearance of high-risk human papillomavirus infections in rural Rakai, Uganda. Cancer Epidemiol Biomarkers Prev 17, 1300-1307.
34. Serwadda, D., Wawer, M. J., Shah, K. V., Sewankambo, N. K., Daniel, R., Li, C., Lorincz, A., Meehan, M. P., Wabwire-Mangen, F. & Gray, R. H. (1999). Use of a hybrid capture assay of self-collected vaginal swabs in rural Uganda for detection of human papillomavirus. J Infect Dis 180, 1316-1319.
35. Slaymaker, E., Bwanika, J. B., Kasamba, I., Lutalo, T., Maher, D. & Todd, J. (2009). Trends in age at first sex in Uganda: evidence from Demographic and Health Survey data and longitudinal cohorts in Masaka and Rakai. Sex Transm Infect 85 (Suppl. 1), i12-i19.
36. Soto-De Leon, S., Camargo, M., Sanchez, R., Munoz, M., Perez-Prados, A., Purroy, A., Patarroyo, M. E. & Patarroyo, M. A. (2011). Distribution patterns of infection with multiple types of human papillomaviruses and their association with risk factors. PLoS ONE 6, e14705.
37. Syrjänen, S., Waterboer, T., Sarkola, M., Michael, K., Rintala, M., Syrjänen, K., Grenman, S. & Pawlita, M. (2009). Dynamics of human papillomavirus serology in women followed up for 36 months after pregnancy. J Gen Virol 90, 1515-1526.
38. Trottier, H., Mahmud, S., Costa, M. C., Sobrinho, J. P., Duarte-Franco, E., Rohan, T. E., Ferenczy, A., Villa, L. L. & Franco, E. L. (2006). Human papillomavirus infections with multiple types and risk of cervical neoplasia. Cancer Epidemiol Biomarkers Prev 15, 1274-1280.
39. Wabinga, H., Ramanakumar, A. V., Banura, C., Luwaga, A., Nambooze, S. & Parkin, D. M. (2003). Survival of cervix cancer patients in Kampala, Uganda: 1995-1997. Br J Cancer 89, 65-69.
40. Waterboer, T., Sehr, P., Michael, K. M., Franceschi, S., Nieland, J. D., Joos, T. O., Templin, M. F. & Pawlita, M. (2005). Multiplex human papillomavirus serology based on in situ-purified glutathione Stransferase fusion proteins. Clin Chem 51, 1845-1853.
41. Waterboer, T., Sehr, P. & Pawlita, M. (2006). Suppression of nonspecific binding in serological Luminex assays. J Immunol Methods 309, 200-204.
42. Woodman, C. B., Collins, S., Winter, H., Bailey, A., Ellis, J., Prior, P., Yates, M., Rollason, T. P. & Young, L. S. (2001). Natural history of cervical human papillomavirus infection in young women: a longitudinal cohort study. Lancet 357, 1831-1836.