Skip to main content
Top
Published in: Current Obstetrics and Gynecology Reports 4/2015

01-12-2015 | Management of HPV and Associated Cervical Lesions (L Denny, Section Editor)

Human Papillomavirus (HPV) Testing for Secondary Prevention of Cervical Cancer

Authors: Partha Basu, Smita Joshi, Rengaswamy Sankaranarayanan

Published in: Current Obstetrics and Gynecology Reports | Issue 4/2015

Login to get access

Abstract

The strong causal association between human papillomavirus (HPV) and cervical cancer led to the development of HPV detection tests as alternatives to cytology. Several cross-sectional studies evaluated the HPV detection tests in a variety of settings. The pooled sensitivity of HPV test for detection of cervical intraepithelial neoplasia (CIN) 2+ and 3+ diseases was 90 and 95 %, respectively, in these studies. Randomized controlled studies demonstrated substantially higher detection rates of CIN 2+ and 3+ lesions than cytology in the baseline round of screening. In subsequent rounds of screening, HPV-negative women had significantly lower risk of developing CIN 3 or invasive cancers compared to the cytology-negative women, thus proving the higher protective effect of HPV screening. The World Health Organization recommends HPV detection tests as the test of first choice for cervical cancer screening, if affordable. HPV tests are also recommended to triage minor cytological abnormalities and follow up women after treatment of high-grade lesions.
Literature
1.
go back to reference Ferlay J, Soerjomataram I, Ervik M, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F. GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 11 [Internet]. Lyon: International Agency for Research on Cancer; 2013. Ferlay J, Soerjomataram I, Ervik M, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F. GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 11 [Internet]. Lyon: International Agency for Research on Cancer; 2013.
2.
go back to reference IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Human papillomaviruses. IARC Monogr Eval Carcinog Risks Hum. 1995;64:1–378. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Human papillomaviruses. IARC Monogr Eval Carcinog Risks Hum. 1995;64:1–378.
3.
go back to reference Poljak M, Cuzick J, Kocjan BJ, Iftner T, Dillner J, Arbyn M. Nucleic acid tests for the detection of alpha human papillomaviruses. Vaccine. 2012;30 Suppl 5:F100–6.CrossRefPubMed Poljak M, Cuzick J, Kocjan BJ, Iftner T, Dillner J, Arbyn M. Nucleic acid tests for the detection of alpha human papillomaviruses. Vaccine. 2012;30 Suppl 5:F100–6.CrossRefPubMed
4.
go back to reference Arbyn M, Snijders PJ, Meijer CJ, Berkhof J, Cuschieri K, Kocjan BJ, et al. Which high-risk HPV assays fulfil criteria for use in primary cervical cancer screening? Clin Microbiol Infect. 2015;21:817–26.CrossRefPubMed Arbyn M, Snijders PJ, Meijer CJ, Berkhof J, Cuschieri K, Kocjan BJ, et al. Which high-risk HPV assays fulfil criteria for use in primary cervical cancer screening? Clin Microbiol Infect. 2015;21:817–26.CrossRefPubMed
5.
go back to reference Meijer CJ, Berkhof J, Castle PE, Hesselink AT, Franco EL, Ronco G, et al. Guidelines for human papillomavirus DNA test requirements for primary cervical cancer screening in women 30 years and older. Int J Cancer. 2009;124(3):516–20.PubMedCentralCrossRefPubMed Meijer CJ, Berkhof J, Castle PE, Hesselink AT, Franco EL, Ronco G, et al. Guidelines for human papillomavirus DNA test requirements for primary cervical cancer screening in women 30 years and older. Int J Cancer. 2009;124(3):516–20.PubMedCentralCrossRefPubMed
6.
go back to reference Sasieni PD, Cuzick J, Lynch-Farmery E. Estimating the efficacy of screening by auditing smear histories of women with and without cervical cancer. The National Co-ordinating Network for Cervical Screening Working Group. Br J Cancer. 1996;73(8):1001–5.PubMedCentralCrossRefPubMed Sasieni PD, Cuzick J, Lynch-Farmery E. Estimating the efficacy of screening by auditing smear histories of women with and without cervical cancer. The National Co-ordinating Network for Cervical Screening Working Group. Br J Cancer. 1996;73(8):1001–5.PubMedCentralCrossRefPubMed
7.
go back to reference Fahey MT, Irwig L, Macaskill P. Meta-analysis of Pap test accuracy. Am J Epidemiol. 1995;141(7):680–9.PubMed Fahey MT, Irwig L, Macaskill P. Meta-analysis of Pap test accuracy. Am J Epidemiol. 1995;141(7):680–9.PubMed
8.
go back to reference 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(10):810–9.CrossRefPubMed 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(10):810–9.CrossRefPubMed
9.
go back to reference Sankaranarayanan R, Chatterji R, Shastri SS, Wesley RS, Basu P, Mahe C, et al. Accuracy of human papillomavirus testing in primary screening of cervical neoplasia: results from a multicenter study in India. Int J Cancer. 2004;112(2):341–7.CrossRefPubMed Sankaranarayanan R, Chatterji R, Shastri SS, Wesley RS, Basu P, Mahe C, et al. Accuracy of human papillomavirus testing in primary screening of cervical neoplasia: results from a multicenter study in India. Int J Cancer. 2004;112(2):341–7.CrossRefPubMed
10.
go back to reference Arbyn M, Ronco G, Anttila A, Meijer CJ, Poljak M, Ogilvie G, et al. Evidence regarding human papillomavirus testing in secondary prevention of cervical cancer. Vaccine. 2012;30 Suppl 5:F88–99.CrossRefPubMed Arbyn M, Ronco G, Anttila A, Meijer CJ, Poljak M, Ogilvie G, et al. Evidence regarding human papillomavirus testing in secondary prevention of cervical cancer. Vaccine. 2012;30 Suppl 5:F88–99.CrossRefPubMed
11.
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.CrossRefPubMed 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.CrossRefPubMed
12.••
go back to reference Ronco G, Dillner J, Elfstrom 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. The pooled data from four large randomized controlled studies demonstrated the efficacy of HPV screening in prevention of cervical cancer.CrossRefPubMed Ronco G, Dillner J, Elfstrom 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. The pooled data from four large randomized controlled studies demonstrated the efficacy of HPV screening in prevention of cervical cancer.CrossRefPubMed
13.••
go back to reference 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(14):1385–94. The randomized controlled study demonstrated the reduction in mortality from cervical cancer by a single round of HPV screening in a low-resource setting.CrossRefPubMed 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(14):1385–94. The randomized controlled study demonstrated the reduction in mortality from cervical cancer by a single round of HPV screening in a low-resource setting.CrossRefPubMed
14.••
go back to reference Elfstrom KM, Smelov V, Johansson AL, Eklund C, Naucler P, Arnheim-Dahlstrom 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. The study demonstrated the long-term protection offered by HPV screening that justifies the prolongation of the screening interval even beyond 5 years.PubMedCentralCrossRefPubMed Elfstrom KM, Smelov V, Johansson AL, Eklund C, Naucler P, Arnheim-Dahlstrom 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. The study demonstrated the long-term protection offered by HPV screening that justifies the prolongation of the screening interval even beyond 5 years.PubMedCentralCrossRefPubMed
15.
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.PubMedCentralCrossRefPubMed 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.PubMedCentralCrossRefPubMed
16.
go back to reference Whitlock EP, Vesco KK, Eder M, Lin JS, Senger CA, Burda BU. Liquid-based cytology and human papillomavirus testing to screen for cervical cancer: a systematic review for the U.S. Preventive Services Task Force. Ann Intern Med. 2011;155(10):687–97. Whitlock EP, Vesco KK, Eder M, Lin JS, Senger CA, Burda BU. Liquid-based cytology and human papillomavirus testing to screen for cervical cancer: a systematic review for the U.S. Preventive Services Task Force. Ann Intern Med. 2011;155(10):687–97.
17.
go back to reference Cuzick J, Cadman L, Mesher D, Austin J, Ashdown-Barr L, Ho L, et al. Comparing the performance of six human papillomavirus tests in a screening population. Br J Cancer. 2013;108(4):908–13.PubMedCentralCrossRefPubMed Cuzick J, Cadman L, Mesher D, Austin J, Ashdown-Barr L, Ho L, et al. Comparing the performance of six human papillomavirus tests in a screening population. Br J Cancer. 2013;108(4):908–13.PubMedCentralCrossRefPubMed
18.
go back to reference Schiffman M, Glass AG, Wentzensen N, Rush BB, Castle PE, Scott DR, et al. A long-term prospective study of type-specific human papillomavirus infection and risk of cervical neoplasia among 20,000 women in the Portland Kaiser Cohort Study. Cancer Epidemiol Biomarkers Prev. 2011;20(7):1398–409.PubMedCentralCrossRefPubMed Schiffman M, Glass AG, Wentzensen N, Rush BB, Castle PE, Scott DR, et al. A long-term prospective study of type-specific human papillomavirus infection and risk of cervical neoplasia among 20,000 women in the Portland Kaiser Cohort Study. Cancer Epidemiol Biomarkers Prev. 2011;20(7):1398–409.PubMedCentralCrossRefPubMed
19.
go back to reference Peto J, Gilham C, Deacon J, Taylor C, Evans C, Binns W, et al. Cervical HPV infection and neoplasia in a large population-based prospective study: the Manchester cohort. Br J Cancer. 2004;91(5):942–53.PubMedCentralPubMed Peto J, Gilham C, Deacon J, Taylor C, Evans C, Binns W, et al. Cervical HPV infection and neoplasia in a large population-based prospective study: the Manchester cohort. Br J Cancer. 2004;91(5):942–53.PubMedCentralPubMed
20.
go back to reference Cuzick J, Szarewski A, Mesher D, Cadman L, Austin J, Perryman K, et al. Long-term follow-up of cervical abnormalities among women screened by HPV testing and cytology-results from the Hammersmith study. Int J Cancer. 2008;122(10):2294–300.CrossRefPubMed Cuzick J, Szarewski A, Mesher D, Cadman L, Austin J, Perryman K, et al. Long-term follow-up of cervical abnormalities among women screened by HPV testing and cytology-results from the Hammersmith study. Int J Cancer. 2008;122(10):2294–300.CrossRefPubMed
21.
go back to reference Kjaer SK, Frederiksen K, Munk C, Iftner T. Long-term absolute risk of cervical intraepithelial neoplasia grade 3 or worse following human papillomavirus infection: role of persistence. J Natl Cancer Inst. 2010;102(19):1478–88.PubMedCentralCrossRefPubMed Kjaer SK, Frederiksen K, Munk C, Iftner T. Long-term absolute risk of cervical intraepithelial neoplasia grade 3 or worse following human papillomavirus infection: role of persistence. J Natl Cancer Inst. 2010;102(19):1478–88.PubMedCentralCrossRefPubMed
22.
go back to reference Mesher D, Szarewski A, Cadman L, Cubie H, Kitchener H, Luesley D, et al. Long-term follow-up of cervical disease in women screened by cytology and HPV testing: results from the HART study. Br J Cancer. 2010;102(9):1405–10.PubMedCentralCrossRefPubMed Mesher D, Szarewski A, Cadman L, Cubie H, Kitchener H, Luesley D, et al. Long-term follow-up of cervical disease in women screened by cytology and HPV testing: results from the HART study. Br J Cancer. 2010;102(9):1405–10.PubMedCentralCrossRefPubMed
23.••
go back to reference World Health Organization. Comprehensive cervical cancer prevention and control—a healthier future for girls and women: WHO guidance note. Geneva: WHO; 2013. WHO recommended the use of HPV test for primary screening and also recommended prolongation of screening interval to up to 10 years when such a sensitive test is used. World Health Organization. Comprehensive cervical cancer prevention and control—a healthier future for girls and women: WHO guidance note. Geneva: WHO; 2013. WHO recommended the use of HPV test for primary screening and also recommended prolongation of screening interval to up to 10 years when such a sensitive test is used.
24.•
go back to reference Arrossi S, Thouyaret L, Herrero R, Campanera A, Magdaleno A, Cuberli M, et al. Effect of self-collection of HPV DNA offered by community health workers at home visits on uptake of screening for cervical cancer (the EMA study): a population-based cluster-randomised trial. Lancet Glob Health. 2015;3(2):e85–94. The randomized controlled study demonstrated the efficacy of HPV test on self-collected vaginal samples to significantly improve the participation of the women.CrossRefPubMed Arrossi S, Thouyaret L, Herrero R, Campanera A, Magdaleno A, Cuberli M, et al. Effect of self-collection of HPV DNA offered by community health workers at home visits on uptake of screening for cervical cancer (the EMA study): a population-based cluster-randomised trial. Lancet Glob Health. 2015;3(2):e85–94. The randomized controlled study demonstrated the efficacy of HPV test on self-collected vaginal samples to significantly improve the participation of the women.CrossRefPubMed
25.
go back to reference Arbyn M, Verdoodt F, Snijders PJ, Verhoef VM, Suonio E, Dillner L, et al. Accuracy of human papillomavirus testing on self-collected versus clinician-collected samples: a meta-analysis. Lancet Oncol. 2014;15(2):172–83.CrossRefPubMed Arbyn M, Verdoodt F, Snijders PJ, Verhoef VM, Suonio E, Dillner L, et al. Accuracy of human papillomavirus testing on self-collected versus clinician-collected samples: a meta-analysis. Lancet Oncol. 2014;15(2):172–83.CrossRefPubMed
26.
go back to reference Lazcano-Ponce E, Lorincz AT, Cruz-Valdez A, Salmeron J, Uribe P, Velasco-Mondragon E, et al. Self-collection of vaginal specimens for human papillomavirus testing in cervical cancer prevention (MARCH): a community-based randomised controlled trial. Lancet. 2011;378(9806):1868–73.CrossRefPubMed Lazcano-Ponce E, Lorincz AT, Cruz-Valdez A, Salmeron J, Uribe P, Velasco-Mondragon E, et al. Self-collection of vaginal specimens for human papillomavirus testing in cervical cancer prevention (MARCH): a community-based randomised controlled trial. Lancet. 2011;378(9806):1868–73.CrossRefPubMed
27.
go back to reference Bhatla N, Dar L, Patro AR, Kumar P, Kriplani A, Gulati A, et al. Can human papillomavirus DNA testing of self-collected vaginal samples compare with physician-collected cervical samples and cytology for cervical cancer screening in developing countries? Cancer Epidemiol. 2009;33(6):446–50.CrossRefPubMed Bhatla N, Dar L, Patro AR, Kumar P, Kriplani A, Gulati A, et al. Can human papillomavirus DNA testing of self-collected vaginal samples compare with physician-collected cervical samples and cytology for cervical cancer screening in developing countries? Cancer Epidemiol. 2009;33(6):446–50.CrossRefPubMed
28.
go back to reference Belinson JL, Du H, Yang B, Wu R, Belinson SE, Qu X, et al. Improved sensitivity of vaginal self-collection and high-risk human papillomavirus testing. Int J Cancer. 2012;130(8):1855–60.CrossRefPubMed Belinson JL, Du H, Yang B, Wu R, Belinson SE, Qu X, et al. Improved sensitivity of vaginal self-collection and high-risk human papillomavirus testing. Int J Cancer. 2012;130(8):1855–60.CrossRefPubMed
29.
go back to reference Ronco G, Giorgi-Rossi P, Carozzi F, Confortini M, Dalla PP, Del MA, 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(7):492–501.CrossRefPubMed Ronco G, Giorgi-Rossi P, Carozzi F, Confortini M, Dalla PP, Del MA, 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(7):492–501.CrossRefPubMed
30.
go back to reference Muwonge R, Wesley RS, Nene BM, Shastri SS, Jayant K, Malvi SG, et al. Evaluation of cytology and visual triage of human papillomavirus-positive women in cervical cancer prevention in India. Int J Cancer. 2014;134(12):2902–9.CrossRefPubMed Muwonge R, Wesley RS, Nene BM, Shastri SS, Jayant K, Malvi SG, et al. Evaluation of cytology and visual triage of human papillomavirus-positive women in cervical cancer prevention in India. Int J Cancer. 2014;134(12):2902–9.CrossRefPubMed
31.
go back to reference Bergeron C, Giorgi-Rossi P, Cas F, Schiboni ML, Ghiringhello B, Dalla PP, et al. Informed cytology for triaging HPV-positive women: substudy nested in the NTCC randomized controlled trial. J Natl Cancer Inst. 2015;107(2):dju423.PubMedCentralCrossRefPubMed Bergeron C, Giorgi-Rossi P, Cas F, Schiboni ML, Ghiringhello B, Dalla PP, et al. Informed cytology for triaging HPV-positive women: substudy nested in the NTCC randomized controlled trial. J Natl Cancer Inst. 2015;107(2):dju423.PubMedCentralCrossRefPubMed
32.
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;97(14):1072–9.CrossRefPubMed 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;97(14):1072–9.CrossRefPubMed
33.
go back to reference Castle PE, Stoler MH, Wright Jr TC, 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;12(9):880–90.CrossRefPubMed Castle PE, Stoler MH, Wright Jr TC, 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;12(9):880–90.CrossRefPubMed
34.
go back to reference Basu P, Mittal S, Banerjee D, Singh P, Panda C, Dutta S, et al. Diagnostic accuracy of VIA and HPV detection as primary and sequential screening tests in a cervical cancer screening demonstration project in India. Int J Cancer. 2015;137(4):859–67.CrossRefPubMed Basu P, Mittal S, Banerjee D, Singh P, Panda C, Dutta S, et al. Diagnostic accuracy of VIA and HPV detection as primary and sequential screening tests in a cervical cancer screening demonstration project in India. Int J Cancer. 2015;137(4):859–67.CrossRefPubMed
35.
go back to reference Qiao YL, Jeronimo J, Zhao FH, Schweizer J, Chen W, Valdez M, et al. Lower cost strategies for triage of human papillomavirus DNA-positive women. Int J Cancer. 2014;134(12):2891–901.PubMedCentralCrossRefPubMed Qiao YL, Jeronimo J, Zhao FH, Schweizer J, Chen W, Valdez M, et al. Lower cost strategies for triage of human papillomavirus DNA-positive women. Int J Cancer. 2014;134(12):2891–901.PubMedCentralCrossRefPubMed
36.
go back to reference Luttmer R, Berkhof J, Dijkstra MG, van Kemenade FJ, Snijders PJ, Heideman DA, et al. Comparing triage algorithms using HPV DNA genotyping, HPV E7 mRNA detection and cytology in high-risk HPV DNA-positive women. J Clin Virol. 2015;67:59–66.CrossRefPubMed Luttmer R, Berkhof J, Dijkstra MG, van Kemenade FJ, Snijders PJ, Heideman DA, et al. Comparing triage algorithms using HPV DNA genotyping, HPV E7 mRNA detection and cytology in high-risk HPV DNA-positive women. J Clin Virol. 2015;67:59–66.CrossRefPubMed
37.
go back to reference Carozzi F, Confortini M, Dalla PP, Del MA, Gillio-Tos A, De ML, et al. Use of p16-INK4A overexpression to increase the specificity of human papillomavirus testing: a nested substudy of the NTCC randomised controlled trial. Lancet Oncol. 2008;9(10):937–45.CrossRefPubMed Carozzi F, Confortini M, Dalla PP, Del MA, Gillio-Tos A, De ML, et al. Use of p16-INK4A overexpression to increase the specificity of human papillomavirus testing: a nested substudy of the NTCC randomised controlled trial. Lancet Oncol. 2008;9(10):937–45.CrossRefPubMed
38.
go back to reference Ghosh I, Mittal S, Banerjee D, Singh P, Dasgupta S, Chatterjee S, et al. Study of accuracy of colposcopy in VIA and HPV detection-based cervical cancer screening program. Aust N Z J Obstet Gynaecol. 2014;54(6):570–5.CrossRefPubMed Ghosh I, Mittal S, Banerjee D, Singh P, Dasgupta S, Chatterjee S, et al. Study of accuracy of colposcopy in VIA and HPV detection-based cervical cancer screening program. Aust N Z J Obstet Gynaecol. 2014;54(6):570–5.CrossRefPubMed
39.
go back to reference Yang B, Pretorius RG, Belinson JL, Zhang X, Burchette R, Qiao YL. False negative colposcopy is associated with thinner cervical intraepithelial neoplasia 2 and 3. Gynecol Oncol. 2008;110(1):32–6.CrossRefPubMed Yang B, Pretorius RG, Belinson JL, Zhang X, Burchette R, Qiao YL. False negative colposcopy is associated with thinner cervical intraepithelial neoplasia 2 and 3. Gynecol Oncol. 2008;110(1):32–6.CrossRefPubMed
40.
go back to reference Denny L, Kuhn L, De SM, Pollack AE, Dupree W, Wright Jr TC. Screen-and-treat approaches for cervical cancer prevention in low-resource settings: a randomized controlled trial. JAMA. 2005;294(17):2173–81.CrossRefPubMed Denny L, Kuhn L, De SM, Pollack AE, Dupree W, Wright Jr TC. Screen-and-treat approaches for cervical cancer prevention in low-resource settings: a randomized controlled trial. JAMA. 2005;294(17):2173–81.CrossRefPubMed
41.
go back to reference Denny L, Kuhn L, Hu CC, Tsai WY, Wright Jr TC. Human papillomavirus-based cervical cancer prevention: long-term results of a randomized screening trial. J Natl Cancer Inst. 2010;102(20):1557–67.CrossRefPubMed Denny L, Kuhn L, Hu CC, Tsai WY, Wright Jr TC. Human papillomavirus-based cervical cancer prevention: long-term results of a randomized screening trial. J Natl Cancer Inst. 2010;102(20):1557–67.CrossRefPubMed
42.
go back to reference Goldie SJ, Gaffikin L, Goldhaber-Fiebert JD, Gordillo-Tobar A, Levin C, Mahe C, et al. Cost-effectiveness of cervical-cancer screening in five developing countries. N Engl J Med. 2005;353(20):2158–68.CrossRefPubMed Goldie SJ, Gaffikin L, Goldhaber-Fiebert JD, Gordillo-Tobar A, Levin C, Mahe C, et al. Cost-effectiveness of cervical-cancer screening in five developing countries. N Engl J Med. 2005;353(20):2158–68.CrossRefPubMed
43.
go back to reference Campos NG, Maza M, Alfaro K, Gage JC, Castle PE, Felix JC, et al. The comparative and cost-effectiveness of HPV-based cervical cancer screening algorithms in El Salvador. Int J Cancer. 2015;137(4):893–902.CrossRefPubMed Campos NG, Maza M, Alfaro K, Gage JC, Castle PE, Felix JC, et al. The comparative and cost-effectiveness of HPV-based cervical cancer screening algorithms in El Salvador. Int J Cancer. 2015;137(4):893–902.CrossRefPubMed
44.
go back to reference World Health Organization. WHO guidelines for screening and treatment of precancerous lesions for cervical cancer prevention. Geneva: WHO; 2013. World Health Organization. WHO guidelines for screening and treatment of precancerous lesions for cervical cancer prevention. Geneva: WHO; 2013.
45.
go back to reference Cox JT, Lorincz AT, Schiffman MH, Sherman ME, Cullen A, Kurman RJ. Human papillomavirus testing by hybrid capture appears to be useful in triaging women with a cytologic diagnosis of atypical squamous cells of undetermined significance. Am J Obstet Gynecol. 1995;172(3):946–54.CrossRefPubMed Cox JT, Lorincz AT, Schiffman MH, Sherman ME, Cullen A, Kurman RJ. Human papillomavirus testing by hybrid capture appears to be useful in triaging women with a cytologic diagnosis of atypical squamous cells of undetermined significance. Am J Obstet Gynecol. 1995;172(3):946–54.CrossRefPubMed
46.
go back to reference Nygard JF, Sauer T, Skjeldestad FE, Skare GB, Thoresen SO. CIN 2/3 and cervical cancer after an ASCUS pap smear. A 7-year, prospective study of the Norwegian population-based, coordinated screening program. Acta Cytol. 2003;47(6):991–1000.CrossRefPubMed Nygard JF, Sauer T, Skjeldestad FE, Skare GB, Thoresen SO. CIN 2/3 and cervical cancer after an ASCUS pap smear. A 7-year, prospective study of the Norwegian population-based, coordinated screening program. Acta Cytol. 2003;47(6):991–1000.CrossRefPubMed
47.
go back to reference Solomon D, Schiffman M, Tarone R. Comparison of three management strategies for patients with atypical squamous cells of undetermined significance: baseline results from a randomized trial. J Natl Cancer Inst. 2001;93(4):293–9.CrossRefPubMed Solomon D, Schiffman M, Tarone R. Comparison of three management strategies for patients with atypical squamous cells of undetermined significance: baseline results from a randomized trial. J Natl Cancer Inst. 2001;93(4):293–9.CrossRefPubMed
48.
go back to reference Lytwyn A, Sellors JW, Mahony JB, Daya D, Chapman W, Ellis N, et al. Comparison of human papillomavirus DNA testing and repeat Papanicolaou test in women with low-grade cervical cytologic abnormalities: a randomized trial. HPV effectiveness in Lowgrade Paps (HELP) Study No. 1 Group. CMAJ. 2000;163(6):701–7.PubMedCentralPubMed Lytwyn A, Sellors JW, Mahony JB, Daya D, Chapman W, Ellis N, et al. Comparison of human papillomavirus DNA testing and repeat Papanicolaou test in women with low-grade cervical cytologic abnormalities: a randomized trial. HPV effectiveness in Lowgrade Paps (HELP) Study No. 1 Group. CMAJ. 2000;163(6):701–7.PubMedCentralPubMed
49.
go back to reference Arbyn M, Roelens J, Simoens C, Buntinx F, Paraskevaidis E, Martin-Hirsch PP, et al. Human papillomavirus testing versus repeat cytology for triage of minor cytological cervical lesions. Cochrane Database Syst Rev. 2013;3:CD008054.PubMed Arbyn M, Roelens J, Simoens C, Buntinx F, Paraskevaidis E, Martin-Hirsch PP, et al. Human papillomavirus testing versus repeat cytology for triage of minor cytological cervical lesions. Cochrane Database Syst Rev. 2013;3:CD008054.PubMed
50.
go back to reference Soutter WP, Sasieni P, Panoskaltsis T. Long-term risk of invasive cervical cancer after treatment of squamous cervical intraepithelial neoplasia. Int J Cancer. 2006;118(8):2048–55.CrossRefPubMed Soutter WP, Sasieni P, Panoskaltsis T. Long-term risk of invasive cervical cancer after treatment of squamous cervical intraepithelial neoplasia. Int J Cancer. 2006;118(8):2048–55.CrossRefPubMed
51.
go back to reference Albrow R, Kitchener H, Gupta N, Desai M. Cervical screening in England: the past, present, and future. Cancer Cytopathol. 2012;120(2):87–96.CrossRefPubMed Albrow R, Kitchener H, Gupta N, Desai M. Cervical screening in England: the past, present, and future. Cancer Cytopathol. 2012;120(2):87–96.CrossRefPubMed
52.
go back to reference Kitchener HC, Walker PG, Nelson L, Hadwin R, Patnick J, Anthony GB, et al. HPV testing as an adjunct to cytology in the follow up of women treated for cervical intraepithelial neoplasia. BJOG. 2008;115(8):1001–7.CrossRefPubMed Kitchener HC, Walker PG, Nelson L, Hadwin R, Patnick J, Anthony GB, et al. HPV testing as an adjunct to cytology in the follow up of women treated for cervical intraepithelial neoplasia. BJOG. 2008;115(8):1001–7.CrossRefPubMed
53.
go back to reference Costa S, Venturoli S, Origoni M, Preti M, Mariani L, Cristoforoni P, et al. Performance of HPV DNA testing in the follow-up after treatment of high-grade cervical lesions, adenocarcinoma in situ (AIS) and microinvasive carcinoma. Ecancermedicalscience. 2015;9:528.PubMedCentralCrossRefPubMed Costa S, Venturoli S, Origoni M, Preti M, Mariani L, Cristoforoni P, et al. Performance of HPV DNA testing in the follow-up after treatment of high-grade cervical lesions, adenocarcinoma in situ (AIS) and microinvasive carcinoma. Ecancermedicalscience. 2015;9:528.PubMedCentralCrossRefPubMed
54.
go back to reference Serati M, Siesto G, Carollo S, Formenti G, Riva C, Cromi A, et al. Risk factors for cervical intraepithelial neoplasia recurrence after conization: a 10-year study. Eur J Obstet Gynecol Reprod Biol. 2012;165(1):86–90.CrossRefPubMed Serati M, Siesto G, Carollo S, Formenti G, Riva C, Cromi A, et al. Risk factors for cervical intraepithelial neoplasia recurrence after conization: a 10-year study. Eur J Obstet Gynecol Reprod Biol. 2012;165(1):86–90.CrossRefPubMed
55.
go back to reference Ghaem-Maghami S, Sagi S, Majeed G, Soutter WP. Incomplete excision of cervical intraepithelial neoplasia and risk of treatment failure: a meta-analysis. Lancet Oncol. 2007;8(11):985–93.CrossRefPubMed Ghaem-Maghami S, Sagi S, Majeed G, Soutter WP. Incomplete excision of cervical intraepithelial neoplasia and risk of treatment failure: a meta-analysis. Lancet Oncol. 2007;8(11):985–93.CrossRefPubMed
56.
go back to reference Qiao YL, Sellors JW, Eder PS, Bao YP, Lim JM, Zhao FH, et al. A new HPV-DNA test for cervical-cancer screening in developing regions: a cross-sectional study of clinical accuracy in rural China. Lancet Oncol. 2008;9(10):929–36.CrossRefPubMed Qiao YL, Sellors JW, Eder PS, Bao YP, Lim JM, Zhao FH, et al. A new HPV-DNA test for cervical-cancer screening in developing regions: a cross-sectional study of clinical accuracy in rural China. Lancet Oncol. 2008;9(10):929–36.CrossRefPubMed
57.
go back to reference Boers A, Slagter-Menkema L, van Hemel BM, Belinson JL, Ruitenbeek T, Buikema HJ, et al. Comparing the Cervista HPV HR test and Hybrid Capture 2 assay in a Dutch screening population: improved specificity of the Cervista HPV HR test by changing the cut-off. PLoS One. 2014;9(7):e101930.PubMedCentralCrossRefPubMed Boers A, Slagter-Menkema L, van Hemel BM, Belinson JL, Ruitenbeek T, Buikema HJ, et al. Comparing the Cervista HPV HR test and Hybrid Capture 2 assay in a Dutch screening population: improved specificity of the Cervista HPV HR test by changing the cut-off. PLoS One. 2014;9(7):e101930.PubMedCentralCrossRefPubMed
58.
go back to reference Einstein MH, Smith KM, Davis TE, Schmeler KM, Ferris DG, Savage AH, et al. Clinical evaluation of the cartridge-based GeneXpert human papillomavirus assay in women referred for colposcopy. J Clin Microbiol. 2014;52(6):2089–95.PubMedCentralCrossRefPubMed Einstein MH, Smith KM, Davis TE, Schmeler KM, Ferris DG, Savage AH, et al. Clinical evaluation of the cartridge-based GeneXpert human papillomavirus assay in women referred for colposcopy. J Clin Microbiol. 2014;52(6):2089–95.PubMedCentralCrossRefPubMed
59.
go back to reference Du H, Yi J, Wu R, Belinson SE, Qu X, Yang B, et al. A new PCR-based mass spectrometry system for high-risk HPV, part II: clinical trial. Am J Clin Pathol. 2011;136(6):920–3.CrossRefPubMed Du H, Yi J, Wu R, Belinson SE, Qu X, Yang B, et al. A new PCR-based mass spectrometry system for high-risk HPV, part II: clinical trial. Am J Clin Pathol. 2011;136(6):920–3.CrossRefPubMed
60.
go back to reference Kitchener HC, Almonte M, Wheeler P, Desai M, Gilham C, Bailey A, et al. HPV testing in routine cervical screening: cross sectional data from the ARTISTIC trial. Br J Cancer. 2006;95(1):56–61.PubMedCentralCrossRefPubMed Kitchener HC, Almonte M, Wheeler P, Desai M, Gilham C, Bailey A, et al. HPV testing in routine cervical screening: cross sectional data from the ARTISTIC trial. Br J Cancer. 2006;95(1):56–61.PubMedCentralCrossRefPubMed
61.
go back to reference Leinonen MK, Nieminen P, Lonnberg S, Malila N, Hakama M, Pokhrel A, et al. Detection rates of precancerous and cancerous cervical lesions within one screening round of primary human papillomavirus DNA testing: prospective randomised trial in Finland. BMJ. 2012;345:e7789.PubMedCentralCrossRefPubMed Leinonen MK, Nieminen P, Lonnberg S, Malila N, Hakama M, Pokhrel A, et al. Detection rates of precancerous and cancerous cervical lesions within one screening round of primary human papillomavirus DNA testing: prospective randomised trial in Finland. BMJ. 2012;345:e7789.PubMedCentralCrossRefPubMed
62.
go back to reference Ogilvie GS, van Niekerk DJ, Krajden M, Martin RE, Ehlen TG, Ceballos K, et al. A randomized controlled trial of Human Papillomavirus (HPV) testing for cervical cancer screening: trial design and preliminary results (HPV FOCAL Trial). BMC Cancer. 2010;10:111.PubMedCentralCrossRefPubMed Ogilvie GS, van Niekerk DJ, Krajden M, Martin RE, Ehlen TG, Ceballos K, et al. A randomized controlled trial of Human Papillomavirus (HPV) testing for cervical cancer screening: trial design and preliminary results (HPV FOCAL Trial). BMC Cancer. 2010;10:111.PubMedCentralCrossRefPubMed
63.
go back to reference Ronco G, Brezzi S, Carozzi F, Dalla PP, Giorgi-Rossi P, Minucci D, et al. The New Technologies for Cervical Cancer Screening randomised controlled trial. An overview of results during the first phase of recruitment. Gynecol Oncol. 2007;107(1 Suppl 1):S230–2.CrossRefPubMed Ronco G, Brezzi S, Carozzi F, Dalla PP, Giorgi-Rossi P, Minucci D, et al. The New Technologies for Cervical Cancer Screening randomised controlled trial. An overview of results during the first phase of recruitment. Gynecol Oncol. 2007;107(1 Suppl 1):S230–2.CrossRefPubMed
64.
go back to reference Ronco G, Giorgi-Rossi P, Carozzi F, Confortini M, Dalla PP, 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(3):249–57.CrossRefPubMed Ronco G, Giorgi-Rossi P, Carozzi F, Confortini M, Dalla PP, 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(3):249–57.CrossRefPubMed
65.
go back to reference Rijkaart DC, Berkhof J, Rozendaal L, van Kemenade FJ, Bulkmans NW, Heideman DA, et al. Human papillomavirus testing for the detection of high-grade cervical intraepithelial neoplasia and cancer: final results of the POBASCAM randomised controlled trial. Lancet Oncol. 2012;13(1):78–88.CrossRefPubMed Rijkaart DC, Berkhof J, Rozendaal L, van Kemenade FJ, Bulkmans NW, Heideman DA, et al. Human papillomavirus testing for the detection of high-grade cervical intraepithelial neoplasia and cancer: final results of the POBASCAM randomised controlled trial. Lancet Oncol. 2012;13(1):78–88.CrossRefPubMed
66.
go back to reference 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(2):88–99.CrossRefPubMed 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(2):88–99.CrossRefPubMed
Metadata
Title
Human Papillomavirus (HPV) Testing for Secondary Prevention of Cervical Cancer
Authors
Partha Basu
Smita Joshi
Rengaswamy Sankaranarayanan
Publication date
01-12-2015
Publisher
Springer US
Published in
Current Obstetrics and Gynecology Reports / Issue 4/2015
Electronic ISSN: 2161-3303
DOI
https://doi.org/10.1007/s13669-015-0133-z

Other articles of this Issue 4/2015

Current Obstetrics and Gynecology Reports 4/2015 Go to the issue

Gynecologic Oncology (R Salani, Section Editor)

Tobacco Use and Outcomes in Gynecologic Malignancy

Management of HPV and Associated Cervical Lesions (L Denny, Section Editor)

Immunology of HPV Infection

Management of HPV and Associated Cervical Lesions (L Denny, Section Editor)

Epidemiology and Burden of Disease Associated with HPV Infection

Gynecologic Oncology (R Salani, Section Editor)

Nutrition in Gynecologic Cancer

Management of HPV and Associated Cervical Lesions (L Denny, Section Editor)

Natural History of Human Papilloma Virus Infection of the Cervix