Promising strategies for cervical cancer screening in the post-human papillomavirus vaccination era
Joseph Tota A B , Salaheddin M. Mahmud A C H , Alex Ferenczy D E F , François Coutlée A G and Eduardo L. Franco A B IA Department of Oncology, McGill University, 546 Pine Avenue West, Montreal, QC H2W 1S6, Canada.
B Department of Epidemiology and Biostatistics, McGill University, 546 Pine Avenue West, Montreal, QC H2W 1S6, Canada.
C Department of Surgery, McGill University, 546 Pine Avenue West, Montreal, QC H2W 1S6, Canada.
D Department of Pathology, McGill University, 546 Pine Avenue West, Montreal, QC H2W 1S6, Canada.
E Department of Obstetrics and Gynecology, McGill University, 546 Pine Avenue West, Montreal, QC H2W 1S6, Canada.
F Department of Pathology, Jewish General Hospital, 3755 Côte Ste-Catherine Road, Montreal, QC H3T 1E2, Canada.
G Département de Microbiologie et Infectiologie, Centre Hospitalier de l’Université de Montréal, Montreal, QC H2L 4M1, Canada.
H Department of Community Health Sciences, University of Manitoba, Winnipeg R3E 0W3, Canada.
I Corresponding author. Email: eduardo.franco@mcgill.ca
Sexual Health 7(3) 376-382 https://doi.org/10.1071/SH10022
Submitted: 19 February 2010 Accepted: 25 May 2010 Published: 19 August 2010
Abstract
Human papillomavirus (HPV) vaccination is expected to reduce the burden of cervical cancer in most settings; however, it is also expected to interfere with the effectiveness of screening. In the future, maintaining Pap cytology as the primary cervical screening test may become too costly. As the prevalence of cervical dysplasias decreases, the positive predictive value of the Pap test will also decrease, and, as a result, more women will be referred for unnecessary diagnostic procedures and follow-up. HPV DNA testing has recently emerged as the most likely candidate to replace cytology for primary screening. It is less prone to human error and much more sensitive than the Pap smear in detecting high-grade cervical lesions. Incorporating this test would improve the overall quality of screening programs and allow spacing out screening tests, while maintaining safety and lowering costs. Although HPV testing is less specific than Pap cytology, this issue could be resolved by reserving the latter for the more labour-efficient task of triaging HPV-positive cases. Because most HPV-positive smears would contain relevant abnormalities, Pap cytology would be expected to perform with sufficient accuracy under these circumstances. HPV Pap triage would also provide a low-cost strategy to monitor long-term vaccine efficacy. Although demonstration projects could start implementing HPV testing as a population screening tool, more research is needed to determine the optimal age to initiate screening, the role of HPV typing and other markers of disease progression, and appropriate follow-up algorithms for HPV-positive and Pap-negative women.
Additional keywords: cytology, HPV DNA, Pap smear.
Acknowledgements
Support for the authors’ research has been provided by a team grant on HPV and associated diseases by the Canadian Institutes of Health Research (grant 83320).
[1] Walboomers JM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah K, et al. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 1999; 189 12–9.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
[2] 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.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
[3] Munoz N, Bosch FX, Castellsague X, Díaz M, de Sanjose S, Hammouda D, et al. Against which human papillomavirus types shall we vaccinate and screen? The international perspective. Int J Cancer 2004; 111 278–85.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
[4] Harper DM, Franco EL, Wheeler CM, Moscicki A-B, Romanowski B, Roteli-Martins CM, et al. Sustained efficacy up to 4.5 years of a bivalent l1 virus-like particle vaccine against human papillomavirus types 16 and 18: follow-up from a randomised control trial. Lancet 2006; 367 1247–55.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
[5] Garland SM, Hernandez-Avila M, Wheeler CM, Perez G, Harper DM, Leodolter S, et al. Quadrivalent vaccine against human papillomavirus to prevent anogenital diseases. N Engl J Med 2007; 356 1928–43.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
[6] Taira AV, Neukermans CP, Sanders GD. Evaluating human papillomavirus vaccination programs. Emerg Infect Dis 2004; 10 1915–23.
| PubMed |
[7] Kim JJ, Goldie SJ. Health and economic implications of HPV vaccination in the United States. N Engl J Med 2008; 359 821–32.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
[8] Kulasingam SL, Myers ER. Potential health and economic impact of adding a human papillomavirus vaccine to screening programs. JAMA 2003; 290 781–9.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[9] Rogoza RM, Ferko N, Bentley J, Meijer CJLM, Berkhof J, Wang K-L, et al. Optimization of primary and secondary cervical cancer prevention strategies in an era of cervical cancer vaccination: a multi-regional health economic analysis. Vaccine 2008; 26 F46–58.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[10] Brisson M, Van De Velde N, De Wals P, Boily MC. The potential cost-effectiveness of prophylactic human papillomavirus vaccines in Canada. Vaccine 2007; 25 5399–408.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[11] Kim JJ, Ortendahl J, Goldie SJ. Cost-effectiveness of human papillomavirus vaccination and cervical cancer screening in women older than 30 years in the United States. Ann Intern Med 2009; 151 538–45.
| PubMed |
[12] Goldie SJ, Kohli M, Grima D, Weinstein MC, Wright TC, Bosch FX, et al. Projected clinical benefits and cost-effectiveness of a human papillomavirus 16/18 vaccine. J Natl Cancer Inst 2004; 96 604–15.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[13] Miller AB, Nazeer S, Fonn S, Brandup-Lukanow A, Rehman R, Cronje H, et al. Report on consensus conference on cervical cancer screening and management. Int J Cancer 2000; 86 440–7.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
[14] Franco EL, Mahmud SM, Tota J, Ferenczy A, Coutlee F. The expected impact of HPV vaccination on the accuracy of cervical cancer screening: the need for a paradigm change. Arch Med Res 2009; 40 478–85.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[15] Sargent A, Bailey A, Almonte M, Turner A, Thomson C, Peto J, et al. Prevalence of type-specific HPV infection by age and grade of cervical cytology: data from the ARTISTIC trial. Br J Cancer 2008; 98 1704–9.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
[16] Coupé VM, Berkhof J, Bulkmans NW, Snijders PJ, Meijer CJ. Age-dependent prevalence of 14 high-risk HPV types in the Netherlands: implications for prophylactic vaccination and screening. Br J Cancer 2008; 98 646–51.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[17] Franco EL, Cuzick J, Hildesheim A, De Sanjose S. Chapter 20: issues in planning cervical cancer screening in the era of HPV vaccination. Vaccine 2006; 24 171–7.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[18] Cuzick J, Clavel C, Petry KU, Meijer CJLM, 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 | GoogleScholarGoogle Scholar | CAS | PubMed |
[19] Nanda K, Mccrory DC, Myers ER, Bastian LA, Hasselblad V, Hickey JD, et al. Accuracy of the Papanicolaou test in screening for and follow-up of cervical cytologic abnormalities: a systematic review. Ann Intern Med 2000; 132 810–9.
| CAS | PubMed |
[20] Franco EL, Cuzick J. Cervical cancer screening following prophylactic human papillomavirus vaccination. Vaccine 2008; 26 A16–23.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[21] Ratnam S, Franco EL, Ferenczy A. Human papillomavirus testing for primary screening of cervical cancer precursors. Cancer Epidemiol Biomarkers Prev 2000; 9 945–51.
| CAS | PubMed |
[22] Mayrand MH, Duarte-Franco E, Coutlee F, Rodrigues I, Walter SD, Ratnam S, et al. Randomized controlled trial of human papillomavirus testing versus Pap cytology in the primary screening for cervical cancer precursors: design, methods and preliminary accrual results of the Canadian Cervical Cancer Screening Trial (CCCaST). Int J Cancer 2006; 119 615–23.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
[23] Sankaranarayanan R, Thara S, Esmy PO, Basu P. Cervical cancer: screening and therapeutic perspectives. Med Princ Pract 2008; 17 351–64.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[24] Arbyn M, Bergeron C, Klinkhamer P, Martin-Hirsch P, Siebers AG, Bulten J. Liquid compared with conventional cervical cytology: a systematic review and meta-analysis. Obstet Gynecol 2008; 111 167–77.
| PubMed |
[25] Arbyn M, Sasieni P, Meijer CJ, Clavel C, Koliopoulos G, Dillner J. Chapter 9: clinical applications of HPV testing: a summary of meta-analyses. Vacci 2006; 24(Suppl 3): 78–89.
| Crossref | GoogleScholarGoogle Scholar |
[26] Naucler P, Ryd W, Tornberg S, Strand A, Wadell G, Elfgren K, et al. Efficacy of HPV DNA testing with cytology triage and/or repeat HPV DNA testing in primary cervical cancer screening. J Natl Cancer Inst 2009; 101 88–99.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[27] Bulkmans NW, Rozendaal L, Snijders PJ, Voorhorst FJ, Boeke AJP, Zandwijken GRJ, et al. POBASCAM, a population-based randomized controlled trial for implementation of high-risk HPV testing in cervical screening: design, methods and baseline data of 44 102 women. Int J Cancer 2004; 110 94–101.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
[28] Bulkmans NW, Berkhof J, Rozendaal L, van Kemenade FJ, Boeke AJP, 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 | GoogleScholarGoogle Scholar | CAS | PubMed |
[29] Elfgren K, Rylander E, Radberg T, Strander B, Strand A, Paajanen K, et al. Colposcopic and histopathologic evaluation of women participating in population-based screening for human papillomavirus deoxyribonucleic acid persistence. Am J Obstet Gynecol 2005; 193 650–7.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[30] Kotaniemi-Talonen L, Nieminen P, Anttila A, Hakama M. Routine cervical screening with primary HPV testing and cytology triage protocol in a randomised setting. Br J Cancer 2005; 93 862–7.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
[31] Sankaranarayanan R, Nene BM, Shastri SS, Jayant K, Muwonge R, Budukh AM, et al. HPV screening for cervical cancer in rural India. N Engl J Med 2009; 360 1385–94.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
[32] 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 | GoogleScholarGoogle Scholar | PubMed |
[33] Leinonen M, Nieminen P, Kotaniemi-Talonen L, Malila N, Tarkkanen J, Laurila P, et al. Age-specific evaluation of primary human papillomavirus screening vs conventional cytology in a randomized setting. J Natl Cancer Inst 2009; 101 1612–23.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
[34] Ronco G, Giorgi-Rossi P, Carozzi F, Dalla Palma P, Del Mistro A, De Marco L, et al. Human papillomavirus testing and liquid-based cytology in primary screening of women younger than 35 years: results at recruitment for a randomised controlled trial. Lancet Oncol 2006; 7 547–55.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[35] Ronco G, Giorgi-Rossi P, Carozzi F, Confortini M, Dalla Palma P, Del Mistro A, et al. Results at recruitment from a randomized controlled trial comparing human papillomavirus testing alone with conventional cytology as the primary cervical cancer screening test. J Natl Cancer Inst 2008; 100 492–501.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[36] Naucler P, Ryd W, Tornberg S, Walter SD, Hanley J, Ferenczy A, et al. Human papillomavirus and Papanicolaou tests to screen for cervical cancer. N Engl J Med 2007; 357 1589–97.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
[37] Mayrand MH, Duarte-Franco E, Rodrigues I, et al. Human papillomavirus DNA versus Papanicolaou screening tests for cervical cancer. N Engl J Med 2007; 357 1579–88.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
[38] Bulkmans NW, Berkhof J, Bulk S, Bleeker MCG, van Kemenade FJ, Rozendaal L, et al. High-risk HPV type-specific clearance rates in cervical screening. Br J Cancer 2007; 96 1419–24.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
[39] Dillner J, Rebolj M, Birembaut P, Petry K-U, Szarewski A, Munk C, et al. Long term predictive values of cytology and human papillomavirus testing in cervical cancer screening: joint European cohort study. BMJ 2008; 337 a1754.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[40] Coutlee F, Rouleau D, Ferenczy A, Franco E. The laboratory diagnosis of genital human papillomavirus infections. Canadian J Infect Dis Med Microbiol 2005; 16 83–91.
[41] Depuydt CE, Arbyn M, Benoy IH, Vandepitte J, Vereecken AJ, Bogers JJ. Quality control for normal liquid based cytology: rescreening, high risk HPV targeted reviewing and/or high risk HPV detection? J Cell Mol Med 2009; 13 4051–60.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[42] Franco EL. A new generation of studies of human papillomavirus DNA testing in cervical cancer screening. J Natl Cancer Inst 2009; 101 1600–1.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
[43] Cuzick J, Arbyn M, Sankaranarayanan R, Tsu V, Ronco G, Mayrand M-H, 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): K29–41.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[44] 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 | GoogleScholarGoogle Scholar | PubMed |
[45] Saslow D, Runowicz CD, Solomon D, Moscicki A-B, Smith RA, Eyre HJ, et al. American Cancer Society guideline for the early detection of cervical neoplasia and cancer. CA Cancer J Clin 2002; 52 342–62.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[46] Wright TC, Massad LS, Dunton CJ, Spitzer M, Wilkinson EJ, Solomon D. 2006 consensus guidelines for the management of women with abnormal cervical cancer screening tests. Am J Obstet Gynecol 2007; 197 346–55.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[47] Spitzer M. Screening and management of women and girls with human papillomavirus infection. Gynecol Oncol 2007; 107 S14–8.
| Crossref | GoogleScholarGoogle Scholar | PubMed |