Abstract
We examined factors associated with high-grade squamous intraepithelial lesions (HSIL) and cervical cancer among human papillomavirus (HPV)-infected women in a prevalent case–control study conducted within a population-based cohort of 10 077 women in Costa Rica. We compared 146 women with HPV-positive HSIL or cancer (HSIL/CA) against 843 HPV-positive women without evidence of HSIL/CA. Subjects completed a risk factor questionnaire. We evaluated the associations between exposures and HSIL/CA among women positive for any HPV and restricted to those positive for high-risk HPV types. Risk of HSIL/CA increased with increasing number of live births (Ptrend= 0.04). Women who smoked 6+ cigarettes/day had a RR for HSIL/CA of 2.7 (95% CI = 1.1–6.7) compared to non-smokers. Current use of barrier contraceptives was associated with a reduction in risk of HSIL/CA (RR = 0.39; 95% CI = 0.16–0.96). Sexual behaviour and a self-reported history of sexually transmitted diseases (STDs) other than HPV were not associated with HSIL/CA. Oral contraceptive use was associated with HSIL/CA among women with <3 pregnancies. Effects were similar in analysis restricted to women positive for high-risk HPV types. Among women positive for high-risk HPV types, 44% of HSIL/CA could be attributed to multiparity (≥3 pregnancies) and/or smoking. Among HPV-positive women, multiparity and smoking are risk factors for HSIL/CA. Oral contraceptive use may be associated with HSIL/CA in subgroups of women. © 2001 Cancer Research Campaign http://www.bjcancer.com
Keywords: cervix, human papillomavirus, cancer, smoking, parity
Full Text
The Full Text of this article is available as a PDF (84.4 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Arbeit J. M., Howley P. M., Hanahan D. Chronic estrogen-induced cervical and vaginal squamous carcinogenesis in human papillomavirus type 16 transgenic mice. Proc Natl Acad Sci U S A. 1996 Apr 2;93(7):2930–2935. doi: 10.1073/pnas.93.7.2930. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bartholomew J. S., Glenville S., Sarkar S., Burt D. J., Stanley M. A., Ruiz-Cabello F., Chengang J., Garrido F., Stern P. L. Integration of high-risk human papillomavirus DNA is linked to the down-regulation of class I human leukocyte antigens by steroid hormones in cervical tumor cells. Cancer Res. 1997 Mar 1;57(5):937–942. [PubMed] [Google Scholar]
- Becker T. M., Wheeler C. M., McGough N. S., Stidley C. A., Parmenter C. A., Dorin M. H., Jordan S. W. Contraceptive and reproductive risks for cervical dysplasia in southwestern Hispanic and non-Hispanic white women. Int J Epidemiol. 1994 Oct;23(5):913–922. doi: 10.1093/ije/23.5.913. [DOI] [PubMed] [Google Scholar]
- Benichou J., Gail M. H. Variance calculations and confidence intervals for estimates of the attributable risk based on logistic models. Biometrics. 1990 Dec;46(4):991–1003. [PubMed] [Google Scholar]
- Bosch F. X., Manos M. M., Muñoz N., Sherman M., Jansen A. M., Peto J., Schiffman M. H., Moreno V., Kurman R., Shah K. V. Prevalence of human papillomavirus in cervical cancer: a worldwide perspective. International biological study on cervical cancer (IBSCC) Study Group. J Natl Cancer Inst. 1995 Jun 7;87(11):796–802. doi: 10.1093/jnci/87.11.796. [DOI] [PubMed] [Google Scholar]
- Bosch F. X., Muñoz N., de Sanjosé S., Izarzugaza I., Gili M., Viladiu P., Tormo M. J., Moreo P., Ascunce N., Gonzalez L. C. Risk factors for cervical cancer in Colombia and Spain. Int J Cancer. 1992 Nov 11;52(5):750–758. doi: 10.1002/ijc.2910520514. [DOI] [PubMed] [Google Scholar]
- Chaouki N., Bosch F. X., Muñoz N., Meijer C. J., El Gueddari B., El Ghazi A., Deacon J., Castellsagué X., Walboomers J. M. The viral origin of cervical cancer in Rabat, Morocco. Int J Cancer. 1998 Feb 9;75(4):546–554. doi: 10.1002/(sici)1097-0215(19980209)75:4<546::aid-ijc9>3.0.co;2-t. [DOI] [PubMed] [Google Scholar]
- Chichareon S., Herrero R., Muñoz N., Bosch F. X., Jacobs M. V., Deacon J., Santamaria M., Chongsuvivatwong V., Meijer C. J., Walboomers J. M. Risk factors for cervical cancer in Thailand: a case-control study. J Natl Cancer Inst. 1998 Jan 7;90(1):50–57. doi: 10.1093/jnci/90.1.50. [DOI] [PubMed] [Google Scholar]
- Cox J. T., Lorincz A. T., Schiffman M. H., Sherman M. E., Cullen A., Kurman R. J. Human papillomavirus testing by hybrid capture appears to be useful in triaging women with a cytologic diagnosis of atypical squamous cells of undetermined significance. Am J Obstet Gynecol. 1995 Mar;172(3):946–954. doi: 10.1016/0002-9378(95)90026-8. [DOI] [PubMed] [Google Scholar]
- Fife K. H., Katz B. P., Brizendine E. J., Brown D. R. Cervical human papillomavirus deoxyribonucleic acid persists throughout pregnancy and decreases in the postpartum period. Am J Obstet Gynecol. 1999 May;180(5):1110–1114. doi: 10.1016/s0002-9378(99)70602-2. [DOI] [PubMed] [Google Scholar]
- Fife K. H., Rogers R. E., Zwickl B. W. Symptomatic and asymptomatic cervical infections with human papillomavirus during pregnancy. J Infect Dis. 1987 Dec;156(6):904–911. doi: 10.1093/infdis/156.6.904. [DOI] [PubMed] [Google Scholar]
- Geng Y., Savage S. M., Razani-Boroujerdi S., Sopori M. L. Effects of nicotine on the immune response. II. Chronic nicotine treatment induces T cell anergy. J Immunol. 1996 Apr 1;156(7):2384–2390. [PubMed] [Google Scholar]
- Harris R. W., Brinton L. A., Cowdell R. H., Skegg D. C., Smith P. G., Vessey M. P., Doll R. Characteristics of women with dysplasia or carcinoma in situ of the cervix uteri. Br J Cancer. 1980 Sep;42(3):359–369. doi: 10.1038/bjc.1980.246. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Herrero R., Brinton L. A., Reeves W. C., Brenes M. M., de Britton R. C., Tenorio F., Gaitan E. Injectable contraceptives and risk of invasive cervical cancer: evidence of an association. Int J Cancer. 1990 Jul 15;46(1):5–7. doi: 10.1002/ijc.2910460103. [DOI] [PubMed] [Google Scholar]
- Herrero R., Hildesheim A., Bratti C., Sherman M. E., Hutchinson M., Morales J., Balmaceda I., Greenberg M. D., Alfaro M., Burk R. D. Population-based study of human papillomavirus infection and cervical neoplasia in rural Costa Rica. J Natl Cancer Inst. 2000 Mar 15;92(6):464–474. doi: 10.1093/jnci/92.6.464. [DOI] [PubMed] [Google Scholar]
- Herrero R., Schiffman M. H., Bratti C., Hildesheim A., Balmaceda I., Sherman M. E., Greenberg M., Cárdenas F., Gómez V., Helgesen K. Design and methods of a population-based natural history study of cervical neoplasia in a rural province of Costa Rica: the Guanacaste Project. Rev Panam Salud Publica. 1997 May;1(5):362–375. doi: 10.1590/s1020-49891997000500005. [DOI] [PubMed] [Google Scholar]
- Hildesheim A., Schiffman M. H., Gravitt P. E., Glass A. G., Greer C. E., Zhang T., Scott D. R., Rush B. B., Lawler P., Sherman M. E. Persistence of type-specific human papillomavirus infection among cytologically normal women. J Infect Dis. 1994 Feb;169(2):235–240. doi: 10.1093/infdis/169.2.235. [DOI] [PubMed] [Google Scholar]
- Ho G. Y., Kadish A. S., Burk R. D., Basu J., Palan P. R., Mikhail M., Romney S. L. HPV 16 and cigarette smoking as risk factors for high-grade cervical intra-epithelial neoplasia. Int J Cancer. 1998 Oct 29;78(3):281–285. doi: 10.1002/(SICI)1097-0215(19981029)78:3<281::AID-IJC3>3.0.CO;2-R. [DOI] [PubMed] [Google Scholar]
- Johnson J. D., Houchens D. P., Kluwe W. M., Craig D. K., Fisher G. L. Effects of mainstream and environmental tobacco smoke on the immune system in animals and humans: a review. Crit Rev Toxicol. 1990;20(5):369–395. doi: 10.3109/10408449009089870. [DOI] [PubMed] [Google Scholar]
- Kjaer S. K., van den Brule A. J., Bock J. E., Poll P. A., Engholm G., Sherman M. E., Walboomers J. M., Meijer C. J. Human papillomavirus--the most significant risk determinant of cervical intraepithelial neoplasia. Int J Cancer. 1996 Mar 1;65(5):601–606. doi: 10.1002/(SICI)1097-0215(19960301)65:5<601::AID-IJC8>3.0.CO;2-6. [DOI] [PubMed] [Google Scholar]
- Krüger-Kjaer S., van den Brule A. J., Svare E. I., Engholm G., Sherman M. E., Poll P. A., Walboomers J. M., Bock J. E., Meijer C. J. Different risk factor patterns for high-grade and low-grade intraepithelial lesions on the cervix among HPV-positive and HPV-negative young women. Int J Cancer. 1998 May 29;76(5):613–619. doi: 10.1002/(sici)1097-0215(19980529)76:5<613::aid-ijc1>3.0.co;2-t. [DOI] [PubMed] [Google Scholar]
- Mitrani-Rosenbaum S., Tsvieli R., Tur-Kaspa R. Oestrogen stimulates differential transcription of human papillomavirus type 16 in SiHa cervical carcinoma cells. J Gen Virol. 1989 Aug;70(Pt 8):2227–2232. doi: 10.1099/0022-1317-70-8-2227. [DOI] [PubMed] [Google Scholar]
- Mittal R., Tsutsumi K., Pater A., Pater M. M. Human papillomavirus type 16 expression in cervical keratinocytes: role of progesterone and glucocorticoid hormones. Obstet Gynecol. 1993 Jan;81(1):5–12. [PubMed] [Google Scholar]
- Moreno V., Muñoz N., Bosch F. X., de Sanjosé S., Gonzalez L. C., Tafur L., Gili M., Izarzugaza I., Navarro C., Vergara A. Risk factors for progression of cervical intraepithelial neoplasm grade III to invasive cervical cancer. Cancer Epidemiol Biomarkers Prev. 1995 Jul-Aug;4(5):459–467. [PubMed] [Google Scholar]
- Muñoz N., Bosch F. X., de Sanjosé S., Vergara A., del Moral A., Muñoz M. T., Tafur L., Gili M., Izarzugaza I., Viladiu P. Risk factors for cervical intraepithelial neoplasia grade III/carcinoma in situ in Spain and Colombia. Cancer Epidemiol Biomarkers Prev. 1993 Sep-Oct;2(5):423–431. [PubMed] [Google Scholar]
- Ngelangel C., Muñoz N., Bosch F. X., Limson G. M., Festin M. R., Deacon J., Jacobs M. V., Santamaria M., Meijer C. J., Walboomers J. M. Causes of cervical cancer in the Philippines: a case-control study. J Natl Cancer Inst. 1998 Jan 7;90(1):43–49. doi: 10.1093/jnci/90.1.43. [DOI] [PubMed] [Google Scholar]
- Nobbenhuis M. A., Walboomers J. M., Helmerhorst T. J., Rozendaal L., Remmink A. J., Risse E. K., van der Linden H. C., Voorhorst F. J., Kenemans P., Meijer C. J. Relation of human papillomavirus status to cervical lesions and consequences for cervical-cancer screening: a prospective study. Lancet. 1999 Jul 3;354(9172):20–25. doi: 10.1016/S0140-6736(98)12490-X. [DOI] [PubMed] [Google Scholar]
- Olsen A. O., Dillner J., Skrondal A., Magnus P. Combined effect of smoking and human papillomavirus type 16 infection in cervical carcinogenesis. Epidemiology. 1998 May;9(3):346–349. [PubMed] [Google Scholar]
- Pater M. M., Hughes G. A., Hyslop D. E., Nakshatri H., Pater A. Glucocorticoid-dependent oncogenic transformation by type 16 but not type 11 human papilloma virus DNA. Nature. 1988 Oct 27;335(6193):832–835. doi: 10.1038/335832a0. [DOI] [PubMed] [Google Scholar]
- Prokopczyk B., Cox J. E., Hoffmann D., Waggoner S. E. Identification of tobacco-specific carcinogen in the cervical mucus of smokers and nonsmokers. J Natl Cancer Inst. 1997 Jun 18;89(12):868–873. doi: 10.1093/jnci/89.12.868. [DOI] [PubMed] [Google Scholar]
- Rando R. F., Lindheim S., Hasty L., Sedlacek T. V., Woodland M., Eder C. Increased frequency of detection of human papillomavirus deoxyribonucleic acid in exfoliated cervical cells during pregnancy. Am J Obstet Gynecol. 1989 Jul;161(1):50–55. doi: 10.1016/0002-9378(89)90231-7. [DOI] [PubMed] [Google Scholar]
- Reeves W. C., Caussy D., Brinton L. A., Brenes M. M., Montalvan P., Gomez B., de Britton R. C., Morice E., Gaitan E., de Lao S. L. Case-control study of human papillomaviruses and cervical cancer in Latin America. Int J Cancer. 1987 Oct 15;40(4):450–454. doi: 10.1002/ijc.2910400403. [DOI] [PubMed] [Google Scholar]
- Roteli-Martins C. M., Panetta K., Alves V. A., Siqueira S. A., Syrjänen K. J., Derchain S. F. Cigarette smoking and high-risk HPV DNA as predisposing factors for high-grade cervical intraepithelial neoplasia (CIN) in young Brazilian women. Acta Obstet Gynecol Scand. 1998 Jul;77(6):678–682. doi: 10.1034/j.1600-0412.1998.770617.x. [DOI] [PubMed] [Google Scholar]
- Schiffman M. H., Bauer H. M., Hoover R. N., Glass A. G., Cadell D. M., Rush B. B., Scott D. R., Sherman M. E., Kurman R. J., Wacholder S. Epidemiologic evidence showing that human papillomavirus infection causes most cervical intraepithelial neoplasia. J Natl Cancer Inst. 1993 Jun 16;85(12):958–964. doi: 10.1093/jnci/85.12.958. [DOI] [PubMed] [Google Scholar]
- Schiffman M. H., Brinton L. A. The epidemiology of cervical carcinogenesis. Cancer. 1995 Nov 15;76(10 Suppl):1888–1901. doi: 10.1002/1097-0142(19951115)76:10+<1888::aid-cncr2820761305>3.0.co;2-h. [DOI] [PubMed] [Google Scholar]
- Schiffman M., Herrero R., Hildesheim A., Sherman M. E., Bratti M., Wacholder S., Alfaro M., Hutchinson M., Morales J., Greenberg M. D. HPV DNA testing in cervical cancer screening: results from women in a high-risk province of Costa Rica. JAMA. 2000 Jan 5;283(1):87–93. doi: 10.1001/jama.283.1.87. [DOI] [PubMed] [Google Scholar]
- Schneider A., Hotz M., Gissmann L. Increased prevalence of human papillomaviruses in the lower genital tract of pregnant women. Int J Cancer. 1987 Aug 15;40(2):198–201. doi: 10.1002/ijc.2910400212. [DOI] [PubMed] [Google Scholar]
- Smith E. M., Johnson S. R., Jiang D., Zaleski S., Lynch C. F., Brundage S., Anderson R. D., Turek L. P. The association between pregnancy and human papilloma virus prevalence. Cancer Detect Prev. 1991;15(5):397–402. [PubMed] [Google Scholar]