Skip to main content
PMC home page
British Journal of Cancer logoLink to British Journal of Cancer
. 1997;76(5):651–657. doi: 10.1038/bjc.1997.440

Present evidence on the value of HPV testing for cervical cancer screening: a model-based exploration of the (cost-)effectiveness.

M van Ballegooijen 1, M E van den Akker-van Marle 1, P G Warmerdam 1, C J Meijer 1, J M Walboomers 1, J D Habbema 1
PMCID: PMC2228006  PMID: 9303366

Abstract

Human papillomavirus (HPV) is the main risk factor for invasive cervical cancer. High risk ratios are found in cross-sectional data on HPV prevalence. The question raised is whether this present evidence is sufficient for making firm recommendations on HPV screening. A validated cervical cancer screening model was extended by adding HPV infection as a possible precursor of cervical intraepithelial neoplasia (CIN). Two widely different model quantifications were constructed so that both were compatible with the observed HPV risk ratios. One model assumed a much longer duration of HPV infection before progressing to CIN and a higher sensitivity of the HPV test than the other. In one version of the model, the calculated mortality reduction from HPV screening was higher and the (cost-)effectiveness was much better than for Pap smear screening. In the other version, outcomes were the opposite, although the cost-effectiveness of the combined HPV + cytology test was close to that of Pap smear screening. Although small follow-up studies and studies with limited strength of design suggest that HPV testing may well improve cervical cancer screening, only large longitudinal screening studies on the association between HPV infection and the development of neoplasias can give outcomes that would enable a firm conclusion to be made on the (cost-)effectiveness of HPV screening. Prospective studies should address women aged 30-60 years.

Full text

PDF
657

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bauer H. M., Hildesheim A., Schiffman M. H., Glass A. G., Rush B. B., Scott D. R., Cadell D. M., Kurman R. J., Manos M. M. Determinants of genital human papillomavirus infection in low-risk women in Portland, Oregon. Sex Transm Dis. 1993 Sep-Oct;20(5):274–278. doi: 10.1097/00007435-199309000-00007. [DOI] [PubMed] [Google Scholar]
  2. Bergeron C., Barrasso R., Beaudenon S., Flamant P., Croissant O., Orth G. Human papillomaviruses associated with cervical intraepithelial neoplasia. Great diversity and distinct distribution in low- and high-grade lesions. Am J Surg Pathol. 1992 Jul;16(7):641–649. doi: 10.1097/00000478-199207000-00002. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Cuzick J., Szarewski A., Terry G., Ho L., Hanby A., Maddox P., Anderson M., Kocjan G., Steele S. T., Guillebaud J. Human papillomavirus testing in primary cervical screening. Lancet. 1995 Jun 17;345(8964):1533–1536. doi: 10.1016/s0140-6736(95)91086-7. [DOI] [PubMed] [Google Scholar]
  5. Cuzick J., Terry G., Ho L., Hollingworth T., Anderson M. Type-specific human papillomavirus DNA in abnormal smears as a predictor of high-grade cervical intraepithelial neoplasia. Br J Cancer. 1994 Jan;69(1):167–171. doi: 10.1038/bjc.1994.28. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Eluf-Neto J., Booth M., Muñoz N., Bosch F. X., Meijer C. J., Walboomers J. M. Human papillomavirus and invasive cervical cancer in Brazil. Br J Cancer. 1994 Jan;69(1):114–119. doi: 10.1038/bjc.1994.18. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gaarenstroom K.N., Melkert P., Walboomers J.M.M., Van Den Brule A.J.C., Van Bommel P.F.J., Meyer C.J.L.M., Voorhorst F.J., Kenemans P., Helmerhorst Th.J.M. Human papillomavirus DNA and genotypes: prognostic factors for progression of cervical intraepithelial neoplasia. Int J Gynecol Cancer. 1994 Mar;4(2):73–78. doi: 10.1046/j.1525-1438.1994.04020073.x. [DOI] [PubMed] [Google Scholar]
  8. Ho G. Y., Burk R. D., Klein S., Kadish A. S., Chang C. J., Palan P., Basu J., Tachezy R., Lewis R., Romney S. Persistent genital human papillomavirus infection as a risk factor for persistent cervical dysplasia. J Natl Cancer Inst. 1995 Sep 20;87(18):1365–1371. doi: 10.1093/jnci/87.18.1365. [DOI] [PubMed] [Google Scholar]
  9. Jenkins D., Sherlaw-Johnson C., Gallivan S. Can papilloma virus testing be used to improve cervical cancer screening? Int J Cancer. 1996 Mar 15;65(6):768–773. doi: 10.1002/(SICI)1097-0215(19960315)65:6<768::AID-IJC10>3.0.CO;2-0. [DOI] [PubMed] [Google Scholar]
  10. Jensen O. M., Estève J., Møller H., Renard H. Cancer in the European Community and its member states. Eur J Cancer. 1990;26(11-12):1167–1256. doi: 10.1016/0277-5379(90)90278-2. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Koopmanschap M. A., Lubbe K. T., van Oortmarssen G. J., van Agt H. M., van Ballegooijen M., Habbema J. K. Economic aspects of cervical cancer screening. Soc Sci Med. 1990;30(10):1081–1087. doi: 10.1016/0277-9536(90)90294-3. [DOI] [PubMed] [Google Scholar]
  13. Koopmanschap M. A., van Oortmarssen G. J., van Agt H. M., van Ballegooijen M., Habbema J. D., Lubbe K. T. Cervical-cancer screening: attendance and cost-effectiveness. Int J Cancer. 1990 Mar 15;45(3):410–415. doi: 10.1002/ijc.2910450305. [DOI] [PubMed] [Google Scholar]
  14. Lorincz A. T., Reid R., Jenson A. B., Greenberg M. D., Lancaster W., Kurman R. J. Human papillomavirus infection of the cervix: relative risk associations of 15 common anogenital types. Obstet Gynecol. 1992 Mar;79(3):328–337. doi: 10.1097/00006250-199203000-00002. [DOI] [PubMed] [Google Scholar]
  15. Melkert P. W., Hopman E., van den Brule A. J., Risse E. K., van Diest P. J., Bleker O. P., Helmerhorst T., Schipper M. E., Meijer C. J., Walboomers J. M. Prevalence of HPV in cytomorphologically normal cervical smears, as determined by the polymerase chain reaction, is age-dependent. Int J Cancer. 1993 Apr 1;53(6):919–923. doi: 10.1002/ijc.2910530609. [DOI] [PubMed] [Google Scholar]
  16. Morrison E. A., Ho G. Y., Vermund S. H., Goldberg G. L., Kadish A. S., Kelley K. F., Burk R. D. Human papillomavirus infection and other risk factors for cervical neoplasia: a case-control study. Int J Cancer. 1991 Aug 19;49(1):6–13. doi: 10.1002/ijc.2910490103. [DOI] [PubMed] [Google Scholar]
  17. Muñoz N., Bosch F. X., de Sanjosé S., Tafur L., Izarzugaza I., Gili M., Viladiu P., Navarro C., Martos C., Ascunce N. The causal link between human papillomavirus and invasive cervical cancer: a population-based case-control study in Colombia and Spain. Int J Cancer. 1992 Nov 11;52(5):743–749. doi: 10.1002/ijc.2910520513. [DOI] [PubMed] [Google Scholar]
  18. Parkin D. M., Pisani P., Ferlay J. Estimates of the worldwide incidence of eighteen major cancers in 1985. Int J Cancer. 1993 Jun 19;54(4):594–606. doi: 10.1002/ijc.2910540413. [DOI] [PubMed] [Google Scholar]
  19. Remmink A. J., Walboomers J. M., Helmerhorst T. J., Voorhorst F. J., Rozendaal L., Risse E. K., Meijer C. J., Kenemans P. The presence of persistent high-risk HPV genotypes in dysplastic cervical lesions is associated with progressive disease: natural history up to 36 months. Int J Cancer. 1995 May 4;61(3):306–311. doi: 10.1002/ijc.2910610305. [DOI] [PubMed] [Google Scholar]
  20. Rozendaal L., Walboomers J. M., van der Linden J. C., Voorhorst F. J., Kenemans P., Helmerhorst T. J., van Ballegooijen M., Meijer C. J. PCR-based high-risk HPV test in cervical cancer screening gives objective risk assessment of women with cytomorphologically normal cervical smears. Int J Cancer. 1996 Dec 11;68(6):766–769. doi: 10.1002/(SICI)1097-0215(19961211)68:6<766::AID-IJC13>3.0.CO;2-Z. [DOI] [PubMed] [Google Scholar]
  21. Van Den Brule A. J., Walboomers J. M., Du Maine M., Kenemans P., Meijer C. J. Difference in prevalence of human papillomavirus genotypes in cytomorphologically normal cervical smears is associated with a history of cervical intraepithelial neoplasia. Int J Cancer. 1991 May 30;48(3):404–408. doi: 10.1002/ijc.2910480317. [DOI] [PubMed] [Google Scholar]
  22. Walboomers J. M., de Roda Husman A. M., Snijders P. J., Stel H. V., Risse E. K., Helmerhorst T. J., Voorhorst F. J., Meijer C. J. Human papillomavirus in false negative archival cervical smears: implications for screening for cervical cancer. J Clin Pathol. 1995 Aug;48(8):728–732. doi: 10.1136/jcp.48.8.728. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. de Sanjosé S., Muñoz N., Bosch F. X., Reimann K., Pedersen N. S., Orfila J., Ascunce N., González L. C., Tafur L., Gili M. Sexually transmitted agents and cervical neoplasia in Colombia and Spain. Int J Cancer. 1994 Feb 1;56(3):358–363. doi: 10.1002/ijc.2910560311. [DOI] [PubMed] [Google Scholar]
  24. van Ballegooijen M., Habbema J. D., van Oortmarssen G. J., Koopmanschap M. A., Lubbe J. T., van Agt H. M. Preventive Pap-smears: balancing costs, risks and benefits. Br J Cancer. 1992 Jun;65(6):930–933. doi: 10.1038/bjc.1992.195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. van Ballegooijen M., Koopmanschap M. A., Habbema J. D. The management of cervical intra-epithelial neoplasia (CIN): extensiveness and costs in The Netherlands. Eur J Cancer. 1995 Sep;31A(10):1672–1676. doi: 10.1016/0959-8049(95)00243-c. [DOI] [PubMed] [Google Scholar]
  26. van Ballegooijen M., Koopmanschap M. A., Tjokrowardojo A. J., van Oortmarssen G. J. Care and costs for advanced cervical cancer. Eur J Cancer. 1992;28A(10):1703–1708. doi: 10.1016/0959-8049(92)90072-a. [DOI] [PubMed] [Google Scholar]
  27. van Oortmarssen G. J., Habbema J. D. Duration of preclinical cervical cancer and reduction in incidence of invasive cancer following negative pap smears. Int J Epidemiol. 1995 Apr;24(2):300–307. doi: 10.1093/ije/24.2.300. [DOI] [PubMed] [Google Scholar]
  28. van Oortmarssen G. J., Habbema J. D. Epidemiological evidence for age-dependent regression of pre-invasive cervical cancer. Br J Cancer. 1991 Sep;64(3):559–565. doi: 10.1038/bjc.1991.350. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from British Journal of Cancer are provided here courtesy of Cancer Research UK

RESOURCES