A comprehensive natural history model of HPV infection and cervical cancer to estimate the clinical impact of a prophylactic HPV-16/18 vaccine

International Journal of Cancer

Volumn 106, Issue 6, 2003, Pages 896-904

  Goldie, Sue J ^a   Grima, Daniel ^b   Kohli, Michele ^b   Wright, Thomas C ^c   Weinstein, Milton ^a,b   Franco, Eduardo ^d  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b i3 Global   (Canada)

^c Columbia Univ School of Medicine ^*  (United States)

^d MCGILL UNIVERSITY   (Canada)

Author keywords

Cervical cancer precursors; HPV; Invasive cervical cancer; Modeling; Vaccine

Indexed keywords

UNCLASSIFIED DRUG; VIRUS VACCINE; WART VIRUS VACCINE;

ADULT; AGE; ARTICLE; CALIBRATION; CANCER INCIDENCE; CANCER INVASION; CARCINOGENESIS; DATA ANALYSIS; DISEASE COURSE; DRUG EFFECT; DRUG EFFICACY; FEMALE; HUMAN; IMMUNITY; INFECTION PREVENTION; MATHEMATICAL MODEL; PRECANCER; PREVALENCE; PRIORITY JOURNAL; PROBABILITY; UTERINE CERVIX CANCER; UTERINE CERVIX CARCINOMA IN SITU; VERRUCA VULGARIS; VIRUS STRAIN; WART VIRUS;

EID: 0042338783     PISSN: 00207136     EISSN: None     Source Type: Journal    
DOI: 10.1002/ijc.11334     Document Type: Article

References (84)

1. International Agency for Research on Cancer. IARC monographs on the evaluation of carcinogenic risks to humans. Vol. 64. Human Papillomaviruses. Lyon, France: International Agency for Research on Cancer. 1995.
2. Schiffman M. New epidemiology of human papillomavirus infection and cervical neoplasia. J Natl Cancer Inst. 1995;87:1345-1347.
3. Franco EL, Rohan TE, Villa LL. Epidemiologic evidence and human papillomavirus infection as a necessary cause of cervical cancer. J Natl Cancer Inst. 1999;91:506-11.
4. Pisani P, Parkin D, Munoz N, Ferlay J. Cancer and infection: estimates of the attributable fraction in 1990. Cancer Epidemiol Biomarkers and Prev 1997;6:387-400.
5. Sankaranarayanan R, Black RJ, Swaminathan R, Parkin DM. An overview of cancer survival in developing countries. IARC Sci Publ 1998;145:135-173
6. Pisani P, Parkin DM, Bray F, Ferlay J. Estimates of the worldwide mortality from 25 cancers in 1990. Int J Cancer. 1999;83:18-29.
7. Parkin DM, Pisani P, Ferlay J. Estimates of the worldwide incidence of 25 major cancers in 1990. Int J Cancer. 1999;80:827-41.
8. Ponten J, Adami HO, Bergstrom R, Dillner J, Friberg LG, Gustafsson L, Miller AB, Parkin DM, Sparen P. Trichopoulos D. Strategies for global control of cervical cancer. Int J Cancer. 1995;60:1-26.
9. Current status of development of prophylactic vaccines against human papillomavirus infection. Report of a technical meeting, Geneva. 16-18 February 1999. Department of Vaccines and other Biologicals, World Health Organization, and the International Agency for Research on Cancer, Geneva 1999. Available at www.who.int/gpvdocuments/
10. Schlecht NF, Kulaga S, Robitaille J, Ferreira S, Santos M, Miyamura RA, Duarte-Franco E, Rohan TE, Ferenczy A, Villa LL, Franco EL. Persistent human papillomavirus infection as a predictor of cervical intraepithelial neoplasia. JAMA. 2001;286:3106-3114.
11. Moscicki AB, Hills N, Shiboski S, Powell K, Jay N, Hanson E, Miller S, Clayton L, Farhat S, Broering J, Darragh T, Palefsky J. Risks for incident human papillomavirus infection and low-grade squamous intraepithelial lesions development in young females. JAMA. 2001; 285:2995-3002.
12. Woodman CB, Collins S, Winter H, Bailey A, Ellis J, Prior P, Yates M, Rollason TP, Young LS. Natural history of cervical human papillomavirus infection in young women: a longitudinal cohort study. Lancet 2001;357:1831-1836.
13. Ferenczy A, Franco EL. Persistent human papillomavirus infection and cervical neoplasia. Lancet Oncol. 2002:3:11-16.
14. Walboomers J, Jacobs M, Manos M, Bosch FX, Kummer JA, Shah KV, Snijders PJ, Peto J, Meijer CJ, Munoz N. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 1999;189:12-19.
15. Bosch F, Manos M, Munoz N, Sherman M, Jansen AM, Peto J, Schiffman MH, Moreno V, Kurman R, Shah KV. Prevalence of human papillomavirus in cervical cancer: a worldwide perspective. International biological study on cervical cancer (IBSCC) Study Group. J Natl Cancer Inst. 1995;87(11):796-802.
16. Galloway DA. Is vaccination against human papillomavirus a possibility? Lancet 1998;351 (suppl III):22-24, 1998
17. Lowy DR, Schiller JT. Papillomaviruses: prophylactic vaccine prospects. Biochimica et Biophysica Acta 1998;1423:M1-M8, 1998
18. Koutsky LA, Ault K, Wheeler CM, Brown DR, Barr E, Alvarez FB, Chiacchierini LM, Jansen KU. A controlled trial of a human papillomavirus type 16 vaccine. N Engl J Med. 2002;347:1645-51.
19. Gold MR, Siegel JE, Russel LB, Weinstein MC, eds. Cost-Effectiveness in Health and Medicine. New York: Oxford University Pr; 1996.
20. Halpern MT, Luce BR, Brown RE, Geneste B. Health and Economic Outcomes Modeling Practices: A Suggested Framework. Value in Health. 1998;2:131-147.
21. Weinstein MC, Toy EL, Sandberg EA, Neumann PJ, Evans JS, Kuntz KM, Graham JD, Hammitt JK. Modeling for health care and other policy decisions: Uses, Roles and Validity. Value in Health. 2001;4: 348-361.
22. Claxton K, Sculpher M, Drummond M. A rational framework for decision making by the National Institute for Clinical Excellence (NICE). Lancet 2002;360:711-15.
23. Schatzkin A. Intermediate markers as surrogate endpoints in cancer research. Hematol Oncol Clin North Am 2000;4:887-905.
24. Goldie SJ, Weinstein MC, Kuntz KM, Freedberg KA. The costs, clinical benefits, and cost-effectiveness of screening for cervical cancer in HIV-infected women. Ann Intern Med. 1999;130:97-107.
25. Goldie SJ, Kuhn L, Denny L, Pollack, Wright TC. Policy analysis of cervical cancer screening strategies in low-resource settings: clinical benefits and cost-effectiveness. JAMA 2001;285(24):3107-3115.
26. Sherlaw-Johnson C, Gallivan S, Jenkins D. Evaluating cervical cancer screening programmes for developing countries. Int J Cancer. 1997; 72(2):210-216.
27. Jenkins D, Sherlaw-Johnson C, Gallivan S. Can papilloma virus testing be used to improve cervical cancer screening? Int J Cancer 1996;65(6):768-773.
28. van Ballegooijen M, van den Akker-van Marle ME, Warmerdam PG, Meijer CJ, Walboomers JM, Habbema JD. Present evidence on the value of HPV testing for cervical cancer screening: a model-based exploration of the (cost-) effectiveness. Br J Cancer. 1997;76(5): 651-657.
29. Cuzick J, Sasieni P, Davies P, Adams J, Normand C, Frater A, van Ballegooijen M, van den Akker E. A systematic review of the role of human papillomavirus testing within a cervical screening programme. Health Technol Assess. 1999;3:14.
30. Myers E, McCrory D, Nanda K, Matchar D. Mathematical model for the natural history of human papillomavirus infection and cervical carcinogenesis. Am J Epidemiol. 2000;151:1158-1171.85.
31. Brown AD, Garber AM: Cost-effectiveness of 3 methods to enhance the sensitivity of Papanicolaou testing. JAMA. 1999;281:347-353.
32. Eddy DM. Screening for cervical cancer. Ann Intern Med. 1990;113: 214-226.
33. Fahs MC, Mandelblatt J, Schechter C, Muller C. Cost effectiveness of cervical cancer screening for the elderly. Ann Intern Med. 1992;117: 520-527.
34. van der Akker-van Marle ME, van Ballegooijen M, van Oortmarssen GJ, Boer R, Habbema JD. Cost-effectiveness of cervical cancer screening: comparison of screening policies. J Natl Cancer Inst. 2002; 94:193-204.
35. Pecorelli S, Benedet JL, Creasman WT, Shepherd JH. FIGO staging of gynecologic cancer. 1994-1997 FIGO Committee on Gynecologic Oncology. International Federation of Gynecology and Obstetrics. In. J. Gynaecol. Obstet. 1999;65:243-9.
36. Wallin KL, Wiklund F, Angstrom T, Bergman F, Stendahl U, Wadell G, Hallmans G, Dillner J. Type-specific persistence of human papillomavirus DNA before the development of invasive cervical cancer. N Engl J Med 1999;341(22):1633-1638.
37. Nobbenhuis MA, Walboomers JM, Helmerhorst TJ, Rozendaal L, Remmink AJ, Risse EK, van der Linden HC, Voorhorst FJ, Kenemans P, Meijer CJ. Relation of human papillomavirus status to cervical lesions and consequences for cervical cancer screening: a prospective study. Lancet. 1999;354:20-25.
38. Ho GY, Bierman R, Beardsley L, Chang CJ, Burk RD. Natural history of cervicovaginal papillomavirus infection in young women. N Engl J Med. 1998;338:423-8.
39. Remmink AJ, Walboomers JM, Helmerhorst TJ, Voorhorst FJ, Rozendaal L, Risse EK, Meijer CJ, 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;61:306-311.
40. Ellerbrock TV, Chiasson MA, Bush TJ, Sun XW, Sawo D, Brudney K, Wright TC. Incidence of cervical squamous intraepithelial lesions in HIV-infected women. JAMA. 2000;283(8):1031-1037.
41. Londesborough P, Ho L, Terry G, Cuzick J, Wheeler C, Singer A. Human papillomavirus genotype as a predictor of persistence and development of high-grade lesions in women with minor cervical abnormalities. Int J Cancer. 1996;69:364-8.
42. Rozendaal L, Walboomers JM, van der Linden JC, Voorhorst FJ, Kenemans P, Helmerhorst TJ, van Ballegooijen M, Meijer CJ. PCR-based high-risk HPV test in cervical cancer screening gives objective risk assessment of women with cytomorphologically normal cervical smears. Int J of Cancer. 1996;68:766-769.
43. Ho G, Burk R, Klein S, Kadish AS, Chang CJ, Balan P, Basu J, Tachezy R, Lewis R, Romney S. Persistent genital human papilloma-virus infection as a risk factor for persistent cervical dysplasia. J Natl Cancer Inst. 1995;87(18):1365-1371.
44. Hildesheim A, Schiffman MH, Gravitt PE, Glass AG, Greer CE, Zhang T, Scott DR, Rush BB, Lawler P, Sherman ME, Kurman RG, Manos MM. Persistence of type-specific human papillomavirus infection among cytologically normal women. J Infect Dis. 1994;169:235-240.
45. Koutsky LA, Holmes KK, Critchlow CW, Stevens CE, Paavonen J, Beckmann AM, DeRouen TA, Galloway DA, Vernon D, Kiviat NB. A cohort study of the risk of cervical intraepithelial neoplasia grade 2 or 3 in relation to papillomavirus infection. N Engl J Med. 1992;327: 1272-1278.
46. Rousseau MC, Pereira JS, Prado JCM, Villa LL, Rohan TE, Franco EL Cervical coinfection with human papillomavirus (HPV) types as a predictor of acquisition and persistence of HPV infection. J Infect Dis 2001;184:1508-17.
47. Franco E, Villa L, Rohan T, Ferenczy A, Petzl-Erler M, Matlashewski G. Design and methods of the Ludwig-McGill longitudinal study of the natural history of human papillomavirus infection and cervical neoplasia in Brazil. Rev Panam Salud Publica. 1999;6(4):223-33
48. The 1988 Bethesda System for reporting cervical/vaginal cytological diagnoses. National Cancer Institute Workshop. JAMA. 1989;262: 931-4.
49. Luff RD. The Bethesda System for reporting cervical/vaginal cytologic diagnoses: report of the 1991 Bethesda workshop. The Bethesda System Editorial Committee. Hum Pathol. 1992;23(7):719-721.
50. Franco E, Villa L, Sobrinho J, Prado JM, Rousseau MC, Desy 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.
51. Moscicki AB, Shiboski S, Broering J, Powell K, Clayton L, Jay N, Darragh TM, Brescia R, Kanowitz S, Miller SB, Stone J, Hanson E, Palefsky J. The natural history of human papillomavirus infection as measured by repeated DNA testing in adolescent and young women. J Pediatrics. 1998;132(2):277-284.
52. Sun XW, Kuhn L, Ellerbrock TV, Chiasson MA, Bush TJ, Wright TC. Human papillomavirus infection in women infected with the human immunodeficiency virus. N Engl J Med 1997;337:1343-9.
53. Walboomers JMM, Meijer CJLM. Do HPV-negative cervical carcinomas exist? J Pathol 1997;181:253-7.
54. Franco EL. Measurement errors in epidemiological studies of human papillomavirus an cervical cancer. IARC Sci Publ; 119:181-97.
55. Franco EL. Statistical issues in human papillomavirus testing and screening. Clinics in Laboratory Med. 2000;20:346-367.
56. World Health Organization Statistical Information System (WHO-SIS). 1997-1999 World Health Statistics Annual. Available: http://www-nt.who.int/whosis/statistics/menu.cfm (Accessed July 2001)
57. McCrory D, Mather D, Bastain L, Datta S, Hasselblad V, Hickey J, Myers E, Nanda K. Evaluation of Cervical Cytology. Evidence Report/Technology Assessment No.5 (Prepared by Duke University under Contract No. 290-97-0014). AHCPR Publication No. 99-E010. Rockville, MD: Agency for Health Care Policy and Research. February 1999. Available: http://www.ahrq.gov/clinic/epcsums/cervsumm.htm
58. Hopman EH, Rozendaal L, Voorhorst FJ, Walboomers JM, Kenemans P, Helmerhorst TJ. High risk human papillomavirus in women with normal cervical cytology prior to the development of abnormal cytology and colposcopy. Br J Obstet Gynaecol 2000;107:600-604.
59. Ostor AG. Natural history of cervical intraepithelial neoplasia: a critical review. Int J Gynecol Pathol. 1993;12(2):186-192.
60. Melnikow J, Nuovo J, Willan AR, Chan BK, Howell LP. Natural history of cervical squamous intraepithelial lesions: a meta-analysis. Obstet Gynecol. 1998;92(4 Pt 2):727-735.
61. Holowaty P, Miller AB, Rohan T, To, T. Natural history of dysplasia of the uterine cervix. J Nat Cancer Instit 1999;91:252-258.
62. Syrjanen K, Kataja V, Yliskoski M Chang F, Syrjanen S, Saarikoski S. Natural history of cervical human papillomavirus lesions does not substantiate the biologic relevance of the Bethesda System. Obstet Gynecol 1992;79:675-682.
63. Burk RD, Kelly P, Feldman J, Bromberg J, Vermund SH, DeHovitz JA, Landesman SH. Declining prevalence of cervicovaginal human papillomavirus infection with age is independent of other risk factors. Sex Transm Dis. 1996;23:333-341.
64. Melkert PJ, Hopman E, van den Brule J, Risse E, Van Diest P, Bleker O. Prevalence of HPV in cytomorphlogically normal cervical smears, as determined by the polymerase chain reaction, is age-dependent. Int J Cancer. 1993;53:919-923.
65. Bauer HM, Hildesheim A, Schiffman MH, Glass AG, Rush BB, Scott DR, Cadell DM, Kurman RJ, Manos MM. Determinants of genital human papillomavirus infection in low-risk women in Portland, Oregon. Sex Transm Dis. 1993;20(5):274-278.
66. Kotloff KL, Wasserman SS, Russ K, Shapiro S, Daniel R, Brown W, Frost A, Tabaro SO, Shah K. Detection of genital human papillomavirus and associated cytological abnormalities among college women. Sex Transm Dis 1998;25:243-250.
67. Liaw K, Glass AG, Manos MM, Greer CE, Scott DR, Sherman M, Burk RD, Kurman RJ, Wacholder S, Rush BB, Cadell DM, Lawler P, Tabor D, Schiffman M. Detection of human papillomavirus DNA in cytologically normal women and subsequent cervical squamous intraepithelial lesions. J Natl Cancer Inst. 1999;91:954-960.
68. Liu T, Soong SJ, Alvarez RD, Butterworth CE. A longitudinal analysis of human papillomavirus 16 infection, nutritional status, and cervical dysplasia progression. Cancer Epidemiology, Biomarkers, and Prevention. 1995;4:373-380.
69. Nasiell K, Roger V, Nasiell M. Behavior of mild cervical dysplasia during long-term follow-up. Obstet Gynecol 1986;67:665-669.
70. Pretorius R, Semrad N, Watring W, Fotheringham N. Presentation of cervical cancer. Gynecol Oncol 1991;42:48-53.
71. Surveillance, Epidemiology, End Results (SEER) Cancer Statistics Review, 1973-1994. US Dept of Health and Human Services. PHS, NIH, NCI, Bethesda, Maryland. SEER Home Page, http://www-seer. ims.nci.nih.gov/: National Cancer Institute: 1997.
72. Robles SC, White F, Peruga A. Trends in cervical cancer mortality in the Americas. Bull Pan AM Health Organ 1996;30 (4):290-301.
73. Ferlay J, Bray F, Pisani P, Parkin D. GLOBOCAN 2000: Cancer Incidence, Mortality and Prevalence Worldwide, Version 1.0. IARC CancerBase No. 5. Lyon, IARC Press, 2001.
74. Herrero R, Schiffman MH, Bratti C, Hildesheim A, Balmaceda I, Sherman ME, Greenberg M, Cardenas F, Gomez V, Helgesen K, Morales, J, Hutchinson M et al. 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; 1:362-75.).
75. Herrero R, Hildesheim A, Bratti C, Sherman ME, Hutchinson M, Morales J, Balmaceda I, Greenberg MD, Alfaro M, Burk RD, Wacholder S, Plummer M, Schiffman M. Population-based study of human papillomavirus infection and cervical neoplasia in rural Costa Rica. J Natl Cancer Inst. 2000;92(6):464-474.
76. Gustafsson L, Ponten J, Bergstrom R, Adami HO. International incidence rates of invasive cervical cancer before cytological screening. Int J Cancer 1997;71(2):159-165.
77. Parkin DM, Whelan SL, Ferlay J, Raymond L, Young J (Eds.) Cancer Incidence in Five Continents Vol. VII. International Agency for Research on Cancer Scientific Publications No. 143. IARC 1997; Lyon, France.
78. Sierra R, Barrantes R, Munoz Leiva G, Parkin D, Bieber C, Munoz C. Cancer in Costa Rica. International Agency for Research on Cancer Technical Report No. 1. 1998: Lyon France.
79. Fidler HK, Boyes DA, Worth AJ. Cervical cancer detection in British Columbia: A progress report. J Obstet Gynaec Brit Cwlth 1968; 75:392-404.
80. Rousseau MC, Franco EL. A cumulative case-control study of risk factor profiles for oncogenic and nononcogenic cervical human papillomavirus infections. Cancer Epidemiol Biomarkers Prev. 2000; 9:469-76.
81. Castle PE, Schiffman M, Gravitt PE, Kendall H, Fishman S, Dong H, Hildesheim A, Herrero R, Bratti M, Sherman M, Lorincz A, Schussler J, Burk RD. Comparisons of HPV DNA detection by MY09/11 PCR Methods. Journal of Medical Virology. 2002;68:417-423.
82. Castle PE, Schiffman M, Burk RD, Wacholder S, Hildesheim A, Herrero R, Bratti MC, Sherman ME, Lorincz A. Restricted Cross-Reactivity of Hybrid Capture 2 with Nononcogenic Human Papillomavirus Types. Cancer Epidemiology, Biomarkers, and Prevention. 2002;11:1394-1399
83. Highes JP, Garnett GP, Koutsky LA. The theoretical population level impact of a prophylactic human papillomavirus vaccine. Epidemiol 2002;13:631-9.
84. Sanders G, Taira AI. Cost effectiveness of a potential vaccine for human papillomavirus. Emerging Infectious Diseases. 2003;9:37-48.