Sexual Health Sexual Health Society
Publishing on sexual health from the widest perspective
REVIEW

Models of cervical screening in the era of human papillomavirus vaccination

Karen Canfell
+ Author Affiliations
- Author Affiliations

Cancer Epidemiology Research Unit, Cancer Council NSW, 153 Dowling Street, Woolloomooloo, NSW 2010, Australia; School of Public Health, University of Sydney, Sydney, NSW 2006, Australia. Email: karenc@nswcc.org.au

Sexual Health 7(3) 359-367 https://doi.org/10.1071/SH10016
Submitted: 15 February 2010  Accepted: 28 May 2010   Published: 19 August 2010

Abstract

Epidemiologic and economic evaluation using simulation modelling can support complex policy decisions, and is an important tool in predicting the future interaction between human papillomavirus vaccination and cervical screening. Several categories of screening program evaluation are of interest, including: (1) changes to screening considered over the short term, over which the effects of vaccination should be confined to the youngest age groups (<30 years old); (2) the medium and long-term effect of vaccination on the screening program; and (3) changes to screening in context of vaccination. This review considers some of the policy questions in each category and discusses the modelling implications, with particular focus on the Australian context.

Additional keywords: Australia, Pap smear, simulation modelling.


Acknowledgements

I wish to thank the members of the research group Modellers Sans Frontières and collaborators, whose work is referenced here. These include Mark Clements, Jie-Bin Lew, Megan Smith, Carolyn Nickson, Robert Walker, Prudence Creighton, Rosa Legood, Kirsten Howard, Sally Lord, Suzanne Dyer, Yoon Jung Kang, Leonardo Simonella and Ruanne Barnabas. I would also like to thank the Advisory Panel for MSAC evaluations #1122/Reference #39, and Dr Jeffrey Tan for expert review and input into the model of cervical screening discussed here. My research group receives funding from a variety of non-commercial sources including the NHMRC (project grant #440200); screening program or government sources in Australia, New Zealand and the UK; Cancer Council NSW; and the UICC.


References


[1] Australian Institute of Health and Welfare. Cervical Screening in Australia 2006–2007. Report No.: Cat. No. CAN 43. Canberra: Australian Institute of Health and Welfare; 2009.

[2] Canfell K,  Sitas F,  Beral V. Cervical cancer in Australia and the United Kingdom: comparison of screening policy and uptake, and cancer incidence and mortality. Med J Aust 2006; 185 482–6.
PubMed |

[3] National Health and Medical Research Council. Screening to prevent cervical cancer: guidelines for the management of asymptomatic women with screen detected abnormalities. Canberra: NHMRC; 2005. Available online at: http://www.nhmrc.gov.au/publications/synopses/wh39syn.htm [verified July 2010].

[4] International Agency for Research on Cancer. GLOBOCAN 2002. Lyon: IARC; 2005. Available online at: http://www-dep.iarc.fr/ [verified July 2010].

[5] Curado MP , Edwards B , Shin HR , Storm H , Frelay J , Heanue M et al Cancer incidence in five continents, Vol. IX. Report No.: IARC Scientific Publications No. 160. Lyon: IARC; 2007.

[6] International Agency for Research on Cancer. WHO mortality database extracted from the World Health Organization (WHO) Databank. Lyon: IARC; 2005. Available online at: http://www-dep.iarc.fr/ [verified July 2010].

[7] Neville AM,  Quinn MA. An alternative cost effectiveness analysis of ThinPrep in the Australian setting. Aust N Z J Obstet Gynaecol 2005; 45 289–94.
CrossRef | PubMed |

[8] Anderson R,  Haas M,  Shanahan M. The cost-effectiveness of cervical screening in Australia: what is the impact of screening at different intervals or over a different age range? Aust N Z J Public Health 2008; 32 43–52.
CrossRef | PubMed |

[9] Kulasingam S,  Connelly L,  Conway E,  Hocking JS,  Myers E,  Regan DG, et al. A cost-effectiveness analysis of adding a human papillomavirus vaccine to the Australian National Cervical Cancer Screening Program. Sex Health 2007; 4 165–75.
CrossRef | PubMed |

[10] Medical Services Advisory Committee. Automation assisted and liquid based cytology for cervical cancer screening. MSAC reference 1122, Assessment report. Canberra: MSAC; 2009. Available online at: http://www.msac.gov.au/internet/msac/publishing.nsf/Content/2AD0E9BD12315EB9CA2575C5002872A9/$File/1122_MSAC_Assessment_Report.pdf [verified July 2010].

[11] Medical Services Advisory Committee. Human papillomavirus triage test for women with possible or definite low-grade squamous intraepithelial lesions. Canberra: MSAC; 2009. Available online at: http://www.msac.gov.au/internet/msac/publishing.nsf/Content/8FD1D98FE64C8A2FCA2575AD0082FD8F/$File/39_MSAC_Assessment_Report.pdf [verified July 2010].

[12] Drummond MF , Sculpher MJ , Torrance GW , O’Brien BJ , Stoddart GL . Methods for the economic evaluation of health care programmes. New York: Oxford University Press; 2005.

[13] Kim JJ,  Kuntz KM,  Stout NK,  Mahmud S,  Villa LL,  Franco EL, et al. Multiparameter calibration of a natural history model of cervical cancer. Am J Epidemiol 2007; 166 137–50.
CrossRef | PubMed |

[14] van de Velde N,  Brisson M,  Boily MC. Modeling human papillomavirus vaccine effectiveness: quantifying the impact of parameter uncertainty. Am J Epidemiol 2007; 165 762–75.
CrossRef | PubMed |

[15] Goldhaber-Fiebert JD,  Stout NK,  Ortendahl J,  Kuntz KM,  Goldie SJ,  Salomon JA. Modeling human papillomavirus and cervical cancer in the United States for analyses of screening and vaccination. Popul Health Metr 2007; 5 11.
CrossRef | PubMed |

[16] McIndoe WA,  McLean MR,  Jones RW,  Mullins PR. The invasive potential of carcinoma in situ of the cervix. Obstet Gynecol 1984; 64 451–8.
PubMed |

[17] McCredie MR,  Sharples KJ,  Paul C,  Baranyai J,  Medley G,  Jones RW, et al. Natural history of cervical neoplasia and risk of invasive cancer in women with cervical intraepithelial neoplasia 3: a retrospective cohort study. Lancet Oncol 2008; 9 425–34.
CrossRef | PubMed |

[18] Howard K,  Salkeld G,  McCaffery K,  Irwig L. HPV triage testing or repeat Pap smear for the management of atypical squamous cells (ASCUS) on Pap smear: is there evidence of process utility? Health Econ 2008; 17 593–605.
CrossRef | PubMed |

[19] Dickinson JA. Cervical screening: time to change the policy. Med J Aust 2002; 176 547–50.
PubMed |

[20] IARC Working Group on the Evaluation of Cancer. IARC handbooks of cancer prevention volume 10: cervix cancer screening (10th edition). Lyon: IARC Press; 2005.

[21] IARC Screening for squamous cervical cancer: duration of low risk after negative results of cervical cytology and its implication for screening policies. BMJ 1986; 293 659–64.
CrossRef | PubMed |

[22] Sasieni P,  Adams J,  Cuzick J. Benefit of cervical screening at different ages: evidence from the UK audit of screening histories. Br J Cancer 2003; 89 88–93.
CrossRef | PubMed |

[23] Sasieni P,  Castanon A,  Cuzick J. Effectiveness of cervical screening with age: population based case-control study of prospectively recorded data. BMJ 2009; 339 b2968.
CrossRef | PubMed |

[24] Cuzick J,  Clavel C,  Petry KU,  Meijer CJ,  Hoyer H,  Ratnam S, et al. Overview of the European and North American studies on HPV testing in primary cervical cancer screening. Int J Cancer 2006; 119 1095–101.
CrossRef | PubMed |

[25] Cuzick J,  Arbyn M,  Sankaranarayanan R,  Tsu V,  Ronco G,  Mayrand MH, et al. Overview of human papillomavirus-based and other novel options for cervical cancer screening in developed and developing countries. Vaccine 2008; 26(Suppl. 10): K29–K41.
CrossRef | PubMed |

[26] Canfell K,  Barnabas R,  Patnick J,  Beral V. The predicted effect of changes in cervical screening practice in the UK: results from a modelling study. Br J Cancer 2004; 91 530–6.
CrossRef | PubMed |

[27] Australian Bureau of Statistics (ABS). National Health Survey, summary of results, Australia, 2004–05. Cat. No. 4364.0. Canberra: ABS; 2006.

[28] Medical Services Advisory Committee. Completed assessments. 4-1-2010. Canberra: MSAC. Available online at: http://www.health.gov.au/internet/msac/publishing.nsf/content/app1122-1 [accessed February 2010].

[29] NPAAC. Performance measures for Australian laboratories reporting cervical cytology. Canberra: Department of Health and Ageing, National Pathology Accreditation Advisory Council; 2006.

[30] Williams AR. Liquid-based cytology and conventional smears compared over two 12-month periods. Cytopathology 2006; 17 82–5.
CrossRef | PubMed |

[31] Cuzick J,  Castanon A,  Sasieni P. Predicted impact of vaccination against human papillomavirus 16/18 on cancer incidence and cervical abnormalities in women aged 20–29 in the UK. Br J Cancer 2010; 102 933–39.
CrossRef | PubMed |

[32] Brotherton J,  Deeks S,  Campbell-Lloyd S,  Misrachi A,  Passaris I,  Peterson K, et al. Interim estimates of human papillomavirus vaccination coverage in the school-based program in Australia. Commun Dis Intell 2008; 32 457–61.
PubMed |

[33] Future II Study Group Quadrivalent vaccine against human papillomavirus to prevent high-grade cervical lesions. N Engl J Med 2007; 356 1915–27.
CrossRef | PubMed |

[34] Hildesheim A,  Herrero R,  Wacholder S,  Rodriguez AC,  Solomon D,  Bratti MC, et al. Effect of human papillomavirus 16/18 L1 viruslike particle vaccine among young women with preexisting infection: a randomized trial. JAMA 2007; 298 743–53.
CrossRef | PubMed |

[35] Riethmuller D , for the Quadrivalent HPV Vaccine Investigators. Quadrivalent HPV 6/11/16/18 vaccine efficacy against persistent infection or disease in subjects with prior HPV vaccine HPV type infection. Abstract presented at EUROGIN (SS 3–6). EUROGIN 2010 Meeting, Monte Carlo, Monaco 17–20 February 2010.

[36] Smith MA,  Canfell K,  Brotherton JM,  Lew JB,  Barnabas RV. The predicted impact of vaccination on human papillomavirus infections in Australia. Int J Cancer 2008; 123 1854–63.
CrossRef | PubMed |

[37] Anderson RM,  Garnett GP. Mathematical models of the transmission and control of sexually transmitted diseases. Sex Transm Dis 2000; 27 636–43.
CrossRef | PubMed |

[38] Garnett GP. An introduction to mathematical models in sexually transmitted disease epidemiology. Sex Transm Infect 2002; 78 7–12.
CrossRef | PubMed |

[39] Regan DG,  Philp DJ,  Hocking JS,  Law MG. Modelling the population-level impact of vaccination on the transmission of human papillomavirus type 16 in Australia. Sex Health 2007; 4 147–63.
CrossRef | PubMed |

[40] Garland SM , Brotherton J . The prevalence of human papillomavirus infection in Australia: analysis of data from the Women, Human Papillomavirus prevalence, Indigenous, Non-Indigenous, Urban, Rural (WHINURS) study. Proceedings of the 24th International Papillomavirus Society Conference, Beijing, China; 2007 Nov 9.

[41] Schiffman M. Integration of human papillomavirus vaccination, cytology, and human papillomavirus testing. Cancer 2007; 111 145–53.
CrossRef | PubMed |

[42] Mayrand MH,  Duarte-Franco E,  Rodrigues I,  Walter SD,  Hanley J,  Ferenczy A, et al. Human papillomavirus DNA versus Papanicolaou screening tests for cervical cancer. N Engl J Med 2007; 357 1579–88.
CrossRef | PubMed |

[43] Bulkmans NW,  Berkhof J,  Rozendaal L,  van Kemenade FJ,  Boeke AJ,  Bulk S, et al. Human papillomavirus DNA testing for the detection of cervical intraepithelial neoplasia grade 3 and cancer: 5-year follow-up of a randomised controlled implementation trial. Lancet 2007; 370 1764–72.
CrossRef | PubMed |

[44] Naucler P,  Ryd W,  Tornberg S,  Strand A,  Wadell G,  Elfgren K, et al. Human papillomavirus and Papanicolaou tests to screen for cervical cancer. N Engl J Med 2007; 357 1589–97.
CrossRef | PubMed |

[45] Cuzick J,  Szarewski A,  Cubie H,  Hulman G,  Kitchener H,  Luesley D, et al. Management of women who test positive for high-risk types of human papillomavirus: the HART study. Lancet 2003; 362 1871–6.
CrossRef | PubMed |

[46] Ronco G,  Giorgi-Rossi P,  Carozzi F,  Confortini M,  Palma PD,  Del MA, et al. Efficacy of human papillomavirus testing for the detection of invasive cervical cancers and cervical intraepithelial neoplasia: a randomised controlled trial. Lancet Oncol 2010; 11 249–57.
CrossRef | PubMed |

[47] Kitchener HC,  Almonte M,  Thomson C,  Wheeler P,  Sargent A,  Stoykova B, et al. HPV testing in combination with liquid-based cytology in primary cervical screening (ARTISTIC): a randomised controlled trial. Lancet Oncol 2009; 10 672–82.
CrossRef | PubMed |

[48] Kitchener HC,  Almonte M,  Gilham C,  Dowie R,  Stoykova B,  Sargent A, et al. ARTISTIC: a randomised trial of human papillomavirus (HPV) testing in primary cervical screening. Health Technol Assess 2009; 13 1–150.
PubMed |

[49] Myers ER,  McCrory DC,  Nanda K,  Bastian L,  Matchar DB. Mathematical model for the natural history of human papillomavirus infection and cervical carcinogenesis. Am J Epidemiol 2000; 151 1158–71.
PubMed |

[50] Schiffman M,  Castle PE,  Jeronimo J,  Rodriguez AC,  Wacholder S. Human papillomavirus and cervical cancer. Lancet 2007; 370 890–907.
CrossRef | PubMed |

[51] Eder PS,  Lou J,  Huff J,  Macioszek J. The next-generation Hybrid Capture High-Risk HPV DNA assay on a fully automated platform. J Clin Virol 2009; 45 S85–92.
CrossRef | PubMed |

[52] Coutlee F,  Mayrand MH,  Roger M,  Franco EL. Detection and typing of human papillomavirus nucleic acids in biological fluids. Public Health Genom 2009; 12 308–18.
CrossRef |

[53] Day SP,  Hudson A,  Mast A,  Sander T,  Curtis M,  Olson S, et al. Analytical performance of the Investigational Use Only Cervista HPV HR test as determined by a multi-center study. J Clin Virol 2009; 45 S63–72.
CrossRef | PubMed |

[54] Kurtycz DF,  Smith M,  He R,  Miyazaki K,  Shalkham J. Comparison of methods trial for high-risk HPV. Diagn Cytopathol 2010; 38 104–8.
PubMed |

[55] Thai H,  Rangwala S,  Gay T,  Keating K,  McLeod S,  Nazarenko I, et al. An HPV 16, 18, and 45 genotyping test based on Hybrid Capture technology. J Clin Virol 2009; 45(Suppl. 1): S93–7.
CrossRef | PubMed |

[56] Tsoumpou I,  Arbyn M,  Kyrgiou M,  Wentzensen N,  Koliopoulos G,  Martin-Hirsch P, et al. p16(INK4a) immunostaining in cytological and histological specimens from the uterine cervix: a systematic review and meta-analysis. Cancer Treat Rev 2009; 35 210–20.
CrossRef | PubMed |

[57] Koukari A . Renewal of the National Cervical Screening Program. Talk at Preventing Cervical Cancer 2009, Melbourne, March, 2009.



Rent Article (via Deepdyve) Export Citation Cited By (6)