Skip to main content
Top
Published in: BMC Public Health 1/2019

Open Access 01-12-2019 | Human Papillomavirus | Research article

Budget impact analysis of cervical cancer screening in Portugal: comparison of cytology and primary HPV screening strategies

Authors: Angela Pista, Carlos Costa, Conceição Saldanha, José Alberto Fonseca Moutinho, José Maria Moutinho, Fernando Arrobas, Carlos Catalão, Jari Kempers

Published in: BMC Public Health | Issue 1/2019

Login to get access

Abstract

Background

Primary Human Papilloma Virus (HPV) testing is the currently recommended cervical cancer (CxCa) screening strategy by the Portuguese Society of Gynecology (SPG) clinical consensus. However, primary HPV testing has not yet been adopted by the Portuguese organized screening programs. This modelling study compares clinical benefits and costs of replacing the current practice, namely cytology with ASCUS HPV triage, with 2 comparative strategies: 1) HPV (pooled) test with cytology triage, or 2) HPV test with 16/18 genotyping and cytology triage, in organized CxCa screenings in Portugal.

Methods

A budget impact model compares screening performance, clinical outcomes and budget impact of the 3 screening strategies. A hypothetical cohort of 2,078,039 Portuguese women aged 25–64 years old women is followed for two screening cycles. Screening intervals are 3 years for cytology and 5 years for the HPV strategies. Model inputs include epidemiological, test performance and medical cost data. Clinical impacts are assessed with the numbers of CIN2–3 and CxCa detected. Annual costs, budget impact and cost of detecting one CIN2+ were calculated from a public healthcare payer’s perspective.

Results

HPV testing with HPV16/18 genotyping and cytology triage (comparator 2) shows the best clinical outcomes at the same cost as comparator 1 and is the most cost-effective CxCa screening strategy in the Portuguese context. Compared to screening with cytology, it would reduce annual CxCa incidence from 9.3 to 5.3 per 100,000, and CxCa mortality from 2.7 to 1.1 per 100,000. Further, it generates substantial cost savings by reducing the annual costs by €9.16 million (− 24%). The cost of detecting CIN2+ decreases from the current €15,845 to €12,795. On the other hand, HPV (pooled) test with cytology triage (comparator 1) reduces annual incidence of CxCa to 6.9 per 100,000 and CxCa mortality to 1.6 per 100,000, with a cost of €13,227 per CIN2+ detected with annual savings of €9.36 million (− 24%). The savings are mainly caused by increasing the length of routine screening intervals from three to five years.

Conclusion

The results support current clinical recommendations to replace cytology with HPV with 16/18 genotyping with cytology triage as screening algorithm.
Literature
2.
go back to reference Insinga RP, Dasbach EJ, Elbasha EH. Assessing the annual economic burden of preventing and treating anogenital human papillomavirus-related disease in the US: analytic framework and review of the literature. Pharmacoeconomics. 2005;23(11):1107–22.CrossRef Insinga RP, Dasbach EJ, Elbasha EH. Assessing the annual economic burden of preventing and treating anogenital human papillomavirus-related disease in the US: analytic framework and review of the literature. Pharmacoeconomics. 2005;23(11):1107–22.CrossRef
3.
go back to reference Ronco G, Dillner J, Elfström KM, Tunesi S, Snijders PJ, Arbyn M, et al. Efficacy of HPV-based screening for prevention of invasive cervical cancer: follow-up of four European randomised controlled trials. Lancet. 2014;383(9916):524–32.CrossRef Ronco G, Dillner J, Elfström KM, Tunesi S, Snijders PJ, Arbyn M, et al. Efficacy of HPV-based screening for prevention of invasive cervical cancer: follow-up of four European randomised controlled trials. Lancet. 2014;383(9916):524–32.CrossRef
4.
go back to reference Cuzick J, Thomas Cox J, Zhang G, Einstein MH, Stoler M, Trupin S, et al. Human papillomavirus testing for triage of women with low-grade squamous intraepithelial lesions. Int J Cancer. 2013 Feb 15;132(4):959–66.CrossRef Cuzick J, Thomas Cox J, Zhang G, Einstein MH, Stoler M, Trupin S, et al. Human papillomavirus testing for triage of women with low-grade squamous intraepithelial lesions. Int J Cancer. 2013 Feb 15;132(4):959–66.CrossRef
6.
go back to reference Diário da República, 2.ª série — N.° 183 — 21 de setembro de 2017. Diário da República, 2.ª série — N.° 183 — 21 de setembro de 2017.
8.
go back to reference Relatório de Monitorização e Avaliação dos Rastreios Oncológicos. Lisboa: Direcção-Geral da Saúde, 2017. Relatório de Monitorização e Avaliação dos Rastreios Oncológicos. Lisboa: Direcção-Geral da Saúde, 2017.
9.
go back to reference Del Mistro A, Frayle H, Ferro A, Callegaro S, et al. Cervical cancer screening by high risk HPV testing in routine practice: results at one year recall of high risk HPV-positive and cytology-negative women. J Med Screen. 2014 Mar;21(1):30–7.CrossRef Del Mistro A, Frayle H, Ferro A, Callegaro S, et al. Cervical cancer screening by high risk HPV testing in routine practice: results at one year recall of high risk HPV-positive and cytology-negative women. J Med Screen. 2014 Mar;21(1):30–7.CrossRef
10.
go back to reference Kulasingam SL, Havrilesky L, Ghebre R, Myers ER. Screening for Cervical Cancer: A Decision Analysis for the U.S. Preventive Services Task Force. Agency for Healthcare Research and Quality (US). 2011. Kulasingam SL, Havrilesky L, Ghebre R, Myers ER. Screening for Cervical Cancer: A Decision Analysis for the U.S. Preventive Services Task Force. Agency for Healthcare Research and Quality (US). 2011.
11.
go back to reference Insinga RP, Dasbach EJ, Elbasha EH, Liaw KL, Barr E. Progression and regression of incident cervical HPV 6, 11, 16 and 18 infections in young women. Infect Agent Cancer. 2007;2:15.CrossRef Insinga RP, Dasbach EJ, Elbasha EH, Liaw KL, Barr E. Progression and regression of incident cervical HPV 6, 11, 16 and 18 infections in young women. Infect Agent Cancer. 2007;2:15.CrossRef
12.
go back to reference Khan MJ, Castle PE, Lorincz AT, Wacholder S, Sherman M, Scott DR, et al. The elevated 10-year risk of cervical precancer and cancer in women with human papillomavirus (HPV) type 16 or 18 and the possible utility of type-specific HPV testing in clinical practice. J Natl Cancer Inst. 2005 Jul 20;97(14):1072–9.CrossRef Khan MJ, Castle PE, Lorincz AT, Wacholder S, Sherman M, Scott DR, et al. The elevated 10-year risk of cervical precancer and cancer in women with human papillomavirus (HPV) type 16 or 18 and the possible utility of type-specific HPV testing in clinical practice. J Natl Cancer Inst. 2005 Jul 20;97(14):1072–9.CrossRef
13.
go back to reference Insinga RP, Dasbach EJ, Elbasha EH. Epidemiologic natural history and clinical management of human papillomavirus (HPV) disease: a critical and systematic review of the literature in the development of an HPV dynamic transmission model. BMC Infect Dis. 2009 Jul 29;9:119.CrossRef Insinga RP, Dasbach EJ, Elbasha EH. Epidemiologic natural history and clinical management of human papillomavirus (HPV) disease: a critical and systematic review of the literature in the development of an HPV dynamic transmission model. BMC Infect Dis. 2009 Jul 29;9:119.CrossRef
14.
go back to reference Kataja V, Syrjänen K, Mäntyjärvi R, Väyrynen M, Syrjänen S, Saarikoski S, et al. Prospective follow-up of cervical HPV infections: life table analysis of histopathological, cytological and colposcopic data. Eur J Epidemiol. 1989;5(1):1–7.CrossRef Kataja V, Syrjänen K, Mäntyjärvi R, Väyrynen M, Syrjänen S, Saarikoski S, et al. Prospective follow-up of cervical HPV infections: life table analysis of histopathological, cytological and colposcopic data. Eur J Epidemiol. 1989;5(1):1–7.CrossRef
15.
go back to reference Holowaty P, Miller AB, Rohan T, To T. Natural history of dysplasia of the uterine cervix. J Natl Cancer Inst. 1999;91(3):252–8.CrossRef Holowaty P, Miller AB, Rohan T, To T. Natural history of dysplasia of the uterine cervix. J Natl Cancer Inst. 1999;91(3):252–8.CrossRef
16.
go back to reference Matsumoto K, Yasugi T, Oki A, Fujii T, Nagata C, Sekiya S, et al. IgG antibodies to HPV16, 52, 58 and 6 L1-capsids and spontaneous regression of cervical intraepithelial neoplasia. Cancer Lett. 2006;231(2):309–13.CrossRef Matsumoto K, Yasugi T, Oki A, Fujii T, Nagata C, Sekiya S, et al. IgG antibodies to HPV16, 52, 58 and 6 L1-capsids and spontaneous regression of cervical intraepithelial neoplasia. Cancer Lett. 2006;231(2):309–13.CrossRef
17.
go back to reference Omori M, Hashi A, Nakazawa K, Yuminamochi T, Yamane T, Hirata S, et al. Estimation of prognoses for cervical intraepithelial neoplasia 2 by p16INK4a immunoexpression and high-risk HPV in situ hybridization signal types. Am J Clin Pathol. 2007;128(2):208–17.CrossRef Omori M, Hashi A, Nakazawa K, Yuminamochi T, Yamane T, Hirata S, et al. Estimation of prognoses for cervical intraepithelial neoplasia 2 by p16INK4a immunoexpression and high-risk HPV in situ hybridization signal types. Am J Clin Pathol. 2007;128(2):208–17.CrossRef
18.
go back to reference Guedes AC, Zeferino LC, Syrjänen KJ, Brenna SM. Short-term outcome of cervical intraepithelial neoplasia grade 2: considerations for management strategies and reproducibility of diagnosis. Anticancer Res. 2010;30(6):2319–23.PubMed Guedes AC, Zeferino LC, Syrjänen KJ, Brenna SM. Short-term outcome of cervical intraepithelial neoplasia grade 2: considerations for management strategies and reproducibility of diagnosis. Anticancer Res. 2010;30(6):2319–23.PubMed
19.
go back to reference 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(5):425–34.CrossRef 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(5):425–34.CrossRef
21.
go back to reference Bulkmans NW, Berkhof J, Bulk S, Bleeker MC, van Kemenade FJ, Rozendaal L, et al. POBASCAM study group. High-risk HPV type-specific clearance rates in cervical screening. Br J Cancer. 2007;96(9):1419–24.CrossRef Bulkmans NW, Berkhof J, Bulk S, Bleeker MC, van Kemenade FJ, Rozendaal L, et al. POBASCAM study group. High-risk HPV type-specific clearance rates in cervical screening. Br J Cancer. 2007;96(9):1419–24.CrossRef
22.
go back to reference Matsumoto K, Oki A, Furuta R, Maeda H, Yasugi T, Takatsuka N, et al. Japan HPV and cervical cancer (JHACC) study group. Tobacco smoking and regression of low-grade cervical abnormalities. Cancer Sci. 2010;101(9):2065–73.CrossRef Matsumoto K, Oki A, Furuta R, Maeda H, Yasugi T, Takatsuka N, et al. Japan HPV and cervical cancer (JHACC) study group. Tobacco smoking and regression of low-grade cervical abnormalities. Cancer Sci. 2010;101(9):2065–73.CrossRef
23.
go back to reference Meyskens FL Jr, Surwit E, Moon TE, Childers JM, Davis JR, Dorr RT, et al. Enhancement of regression of cervical intraepithelial neoplasia II (moderate dysplasia) with topically applied all-trans-retinoic acid: a randomized trial. J Natl Cancer Inst. 1994;86(7):539–43.CrossRef Meyskens FL Jr, Surwit E, Moon TE, Childers JM, Davis JR, Dorr RT, et al. Enhancement of regression of cervical intraepithelial neoplasia II (moderate dysplasia) with topically applied all-trans-retinoic acid: a randomized trial. J Natl Cancer Inst. 1994;86(7):539–43.CrossRef
24.
go back to reference Castle PE, Rodríguez AC, Burk RD, Herrero R, Hildesheim A, Solomon D, et al. Neither one-time negative screening tests nor negative colposcopy provides absolute reassurance against cervical cancer. Int J Cancer. 2009;125(7):1649–56.CrossRef Castle PE, Rodríguez AC, Burk RD, Herrero R, Hildesheim A, Solomon D, et al. Neither one-time negative screening tests nor negative colposcopy provides absolute reassurance against cervical cancer. Int J Cancer. 2009;125(7):1649–56.CrossRef
25.
go back to reference Pista A, de Oliveira CF, Cunha MJ, Paixao MT, Real O. Prevalence of human papillomavirus infection in women in Portugal: the CLEOPATRE Portugal study. Int J Gynecol Cancer. 2011;21(6):1150–8.CrossRef Pista A, de Oliveira CF, Cunha MJ, Paixao MT, Real O. Prevalence of human papillomavirus infection in women in Portugal: the CLEOPATRE Portugal study. Int J Gynecol Cancer. 2011;21(6):1150–8.CrossRef
26.
go back to reference Pista A, de Oliveira CF, Lopes C, Cunha MJ. Human papillomavirus type distribution in cervical intraepithelial neoplasia grade 2/3 and cervical cancer in Portugal: a CLEOPATRE II study. Int J Gynecol Cancer. 2013;23(3):500–6.CrossRef Pista A, de Oliveira CF, Lopes C, Cunha MJ. Human papillomavirus type distribution in cervical intraepithelial neoplasia grade 2/3 and cervical cancer in Portugal: a CLEOPATRE II study. Int J Gynecol Cancer. 2013;23(3):500–6.CrossRef
27.
go back to reference Wright TC Jr, Stoler MH, Behrens CM, Apple R, Derion T, Wright TL. The ATHENA human papillomavirus study: design, methods, and baseline results. Am J Obstet Gynecol. 2012;206(1):46.e41–11.CrossRef Wright TC Jr, Stoler MH, Behrens CM, Apple R, Derion T, Wright TL. The ATHENA human papillomavirus study: design, methods, and baseline results. Am J Obstet Gynecol. 2012;206(1):46.e41–11.CrossRef
28.
go back to reference Castle PE, Stoler MH, Wright TC Jr, Sharma A, Wright TL, Behrens CM. Performance of carcinogenic human papillomavirus (HPV) testing and HPV16 or HPV18 genotyping for cervical cancer screening of women aged 25 years and older: a subanalysis of the ATHENA study. Lancet Oncol. 2011 Sep;12(9):880–90.CrossRef Castle PE, Stoler MH, Wright TC Jr, Sharma A, Wright TL, Behrens CM. Performance of carcinogenic human papillomavirus (HPV) testing and HPV16 or HPV18 genotyping for cervical cancer screening of women aged 25 years and older: a subanalysis of the ATHENA study. Lancet Oncol. 2011 Sep;12(9):880–90.CrossRef
30.
go back to reference Costa C. Quadrivalent HPV Vaccination Impact in Portugal: 2007-2010. Presentation, EUROGIN conference; 2011; Lisbon. Costa C. Quadrivalent HPV Vaccination Impact in Portugal: 2007-2010. Presentation, EUROGIN conference; 2011; Lisbon.
31.
go back to reference Santana R, Lopes S, Costa C. Human papillomavirus disease burden in Portugal. Lisbon: Poster presentation, EUROGIN; 2011. Santana R, Lopes S, Costa C. Human papillomavirus disease burden in Portugal. Lisbon: Poster presentation, EUROGIN; 2011.
32.
go back to reference Dijkstra MG, van Niekerk D, Rijkaart DC, van Kemenade FJ, Heideman DA, Snijders PJ, et al. primary hrHPV DNA testing in cervical cancer screening: how to manage screen-positive women? A POBASCAM trial substudy. Cancer Epidemiol Biomark Prev. 2014;23(1):55–63.CrossRef Dijkstra MG, van Niekerk D, Rijkaart DC, van Kemenade FJ, Heideman DA, Snijders PJ, et al. primary hrHPV DNA testing in cervical cancer screening: how to manage screen-positive women? A POBASCAM trial substudy. Cancer Epidemiol Biomark Prev. 2014;23(1):55–63.CrossRef
33.
go back to reference Stanczuk GA, Baxter GJ, Currie H, Forson W, Lawrence JR, Cuschieri K, et al. Defining optimal triage strategies for hrHPV screen-positive women-an evaluation of HPV 16/18 genotyping, cytology, and p16/Ki-67 Cytoimmunochemistry. Cancer Epidemiol Biomark Prev. 2017;8. Stanczuk GA, Baxter GJ, Currie H, Forson W, Lawrence JR, Cuschieri K, et al. Defining optimal triage strategies for hrHPV screen-positive women-an evaluation of HPV 16/18 genotyping, cytology, and p16/Ki-67 Cytoimmunochemistry. Cancer Epidemiol Biomark Prev. 2017;8.
34.
go back to reference Wright TC, Stoler MH, Behrens CM, Sharma A, Zhang G, Wright TL. Primary cervical cancer screening with human papillomavirus: end of study results from the ATHENA study using HPV as the first-line screening test. Gynecol Oncol. 2015;136(2):189–97.CrossRef Wright TC, Stoler MH, Behrens CM, Sharma A, Zhang G, Wright TL. Primary cervical cancer screening with human papillomavirus: end of study results from the ATHENA study using HPV as the first-line screening test. Gynecol Oncol. 2015;136(2):189–97.CrossRef
35.
go back to reference Wright TC Jr, Stoler MH, Behrens CM, Sharma A, Sharma K, Apple R. Interlaboratory variation in the performance of liquid-based cytology: insights from the ATHENA trial. Int J Cancer. 2014;134(8):1835–43.CrossRef Wright TC Jr, Stoler MH, Behrens CM, Sharma A, Sharma K, Apple R. Interlaboratory variation in the performance of liquid-based cytology: insights from the ATHENA trial. Int J Cancer. 2014;134(8):1835–43.CrossRef
36.
go back to reference Wright T, Huang J, Baker E, Garfield S, Hertz D, Cox JT. The budget impact of cervical cancer screening using HPV primary screening. Am J Manag Care. 2016;22(3):e95–105.PubMed Wright T, Huang J, Baker E, Garfield S, Hertz D, Cox JT. The budget impact of cervical cancer screening using HPV primary screening. Am J Manag Care. 2016;22(3):e95–105.PubMed
37.
go back to reference Skroumpelos A, Agorastos T, Chatzistamatiou K, Akalestos T, Poulios N, Kyriopoulos J. Budget impact analysis of high-risk Hpv Dna (Hrhpv) test with 16/18 genotyping as a primary screening method for cervical cancer in Greece. Value Health. 2015;18(7):A349.CrossRef Skroumpelos A, Agorastos T, Chatzistamatiou K, Akalestos T, Poulios N, Kyriopoulos J. Budget impact analysis of high-risk Hpv Dna (Hrhpv) test with 16/18 genotyping as a primary screening method for cervical cancer in Greece. Value Health. 2015;18(7):A349.CrossRef
38.
go back to reference Petry KU, Barth C, Wasem J, Neumann A. A model to evaluate the costs and clinical effectiveness of human papilloma virus screeningcompared with annual papanicolaou cytology in Germany. Eur J Obstet Gynecol Reprod Biol. 2017;212:132–9.CrossRef Petry KU, Barth C, Wasem J, Neumann A. A model to evaluate the costs and clinical effectiveness of human papilloma virus screeningcompared with annual papanicolaou cytology in Germany. Eur J Obstet Gynecol Reprod Biol. 2017;212:132–9.CrossRef
39.
go back to reference Tjalma WAA, Kim E, Vandeweyer K. The impact on women's health and the cervical cancer screening budget of primary HPV screening with dual-stain cytology triage in Belgium. Eur J Obstet Gynecol Reprod Biol. 2017;212:171-81. Tjalma WAA, Kim E, Vandeweyer K. The impact on women's health and the cervical cancer screening budget of primary HPV screening with dual-stain cytology triage in Belgium. Eur J Obstet Gynecol Reprod Biol. 2017;212:171-81.
40.
go back to reference Elfström KM, Smelov V, Johansson AL, Eklund C, Nauclér P, Arnheim-Dahlström L, et al. Long term duration of protective effect for HPV negative women: follow-up of primary HPV screening randomised controlled trial. BMJ. 2014;348:g130.CrossRef Elfström KM, Smelov V, Johansson AL, Eklund C, Nauclér P, Arnheim-Dahlström L, et al. Long term duration of protective effect for HPV negative women: follow-up of primary HPV screening randomised controlled trial. BMJ. 2014;348:g130.CrossRef
41.
go back to reference Bulkmans NW, Rozendaal L, Snijders PJ, Voorhorst FJ, Boeke AJ, Zandwijken GR, 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(1):94–101.CrossRef Bulkmans NW, Rozendaal L, Snijders PJ, Voorhorst FJ, Boeke AJ, Zandwijken GR, 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(1):94–101.CrossRef
42.
go back to reference 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. Health Technol Assess. 2009;13(51):1–150 iii-iv.CrossRef 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. Health Technol Assess. 2009;13(51):1–150 iii-iv.CrossRef
43.
go back to reference Ronco G, Giorgi-Rossi P, Carozzi F, Confortini M, Dalla Palma P, Del Mistro A, 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(3):249–57.CrossRef Ronco G, Giorgi-Rossi P, Carozzi F, Confortini M, Dalla Palma P, Del Mistro A, 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(3):249–57.CrossRef
44.
go back to reference Canfell K, Caruana M, Gebski V, Darlington-Brown J, Heley S, Brotherton J, et al. Cervical screening with primary HPV testing or cytology in a population of women in which those aged 33 years or younger had previously been offered HPV vaccination: results of the Compasspilot randomised trial. PLoS Med. 2017;14(9):e1002388.CrossRef Canfell K, Caruana M, Gebski V, Darlington-Brown J, Heley S, Brotherton J, et al. Cervical screening with primary HPV testing or cytology in a population of women in which those aged 33 years or younger had previously been offered HPV vaccination: results of the Compasspilot randomised trial. PLoS Med. 2017;14(9):e1002388.CrossRef
45.
go back to reference Ogilvie GS, van Niekerk D, Krajden M, Smith LW, Cook D, Gondara L, et al. Effect of screening with primary cervical HPV testing vs cytology testing on high-grade cervical intraepithelial neoplasia at 48 months: the HPV FOCAL randomized clinical trial. JAMA. 2018;320(1):43–52.CrossRef Ogilvie GS, van Niekerk D, Krajden M, Smith LW, Cook D, Gondara L, et al. Effect of screening with primary cervical HPV testing vs cytology testing on high-grade cervical intraepithelial neoplasia at 48 months: the HPV FOCAL randomized clinical trial. JAMA. 2018;320(1):43–52.CrossRef
46.
go back to reference Katki HA, Kinney WK, Fetterman B, Lorey T, Poitras NE, Cheung L, et al. Cervical cancer risk for women undergoing concurrent testing for human papillomavirus and cervical cytology: a population-based study in routine clinical practice. Lancet Oncol. 2011;12(7):663–72.CrossRef Katki HA, Kinney WK, Fetterman B, Lorey T, Poitras NE, Cheung L, et al. Cervical cancer risk for women undergoing concurrent testing for human papillomavirus and cervical cytology: a population-based study in routine clinical practice. Lancet Oncol. 2011;12(7):663–72.CrossRef
47.
go back to reference 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(5):1095–101.CrossRef 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(5):1095–101.CrossRef
48.
go back to reference Richardson LA, El-Zein M, Ramanakumar AV, Ratnam S, Sangwa-Lugoma G, Longatto-Filho A, et al. HPV DNA testing with cytology triage in cervical cancer screening: influence of revealing HPV infection status. Cancer Cytopathol. 2015;123(12):745–54.CrossRef Richardson LA, El-Zein M, Ramanakumar AV, Ratnam S, Sangwa-Lugoma G, Longatto-Filho A, et al. HPV DNA testing with cytology triage in cervical cancer screening: influence of revealing HPV infection status. Cancer Cytopathol. 2015;123(12):745–54.CrossRef
49.
go back to reference Bergeron C, Giorgi-Rossi P, Cas F, Schiboni ML, Ghiringhello B, Dalla Palma P, et al. Informed cytology for triaging HPV-positive women: substudy nested in the NTCC randomized controlled trial. J Natl Cancer Inst. 2015;7:107(2). Bergeron C, Giorgi-Rossi P, Cas F, Schiboni ML, Ghiringhello B, Dalla Palma P, et al. Informed cytology for triaging HPV-positive women: substudy nested in the NTCC randomized controlled trial. J Natl Cancer Inst. 2015;7:107(2).
50.
go back to reference Bianchi FP, Gallone MS, Fortunato F, Boccalini S, Martinelli D, Prato R, et al. Epidemiology and cost of cervical cancer care and prevention in Apulia (Italy), 2007/2016. Ann Ig. 2018;30(6):490–501.PubMed Bianchi FP, Gallone MS, Fortunato F, Boccalini S, Martinelli D, Prato R, et al. Epidemiology and cost of cervical cancer care and prevention in Apulia (Italy), 2007/2016. Ann Ig. 2018;30(6):490–501.PubMed
51.
go back to reference Arbyn M, Snijders PJ, Meijer CJ, Berkhof J, Cuschieri K, Kocjan BJ, Poljak M. Which high-risk HPV assays fulfil criteria for use in primary cervical cancer screening? Clin Microbiol Infect. 2015;21(9):817–26.CrossRef Arbyn M, Snijders PJ, Meijer CJ, Berkhof J, Cuschieri K, Kocjan BJ, Poljak M. Which high-risk HPV assays fulfil criteria for use in primary cervical cancer screening? Clin Microbiol Infect. 2015;21(9):817–26.CrossRef
Metadata
Title
Budget impact analysis of cervical cancer screening in Portugal: comparison of cytology and primary HPV screening strategies
Authors
Angela Pista
Carlos Costa
Conceição Saldanha
José Alberto Fonseca Moutinho
José Maria Moutinho
Fernando Arrobas
Carlos Catalão
Jari Kempers
Publication date
01-12-2019
Publisher
BioMed Central
Published in
BMC Public Health / Issue 1/2019
Electronic ISSN: 1471-2458
DOI
https://doi.org/10.1186/s12889-019-6536-4

Other articles of this Issue 1/2019

BMC Public Health 1/2019 Go to the issue