Cervical cancer screening: on the way to a shift from cytology to full molecular screening

Annals of Oncology

Volumn 25, Issue 5, 2014, Pages 927-935

  Dijkstra, M G ^a,b   Snijders, P J F ^a   Arbyn, M ^c   Rijkaart, D C ^a   Berkhof, J ^a   Meijer, C J L M ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b Department of Gastroenterology   (Netherlands)

^c SCIENTIFIC INSTITUTE OF PUBLIC HEALTH   (Belgium)

Author keywords

cervical cancer screening; hrHPV DNA; self sampling; triage

Indexed keywords

VIRUS DNA;

CERVICAL INTRAEPITHELIAL NEOPLASIA; CYTODIAGNOSIS; EARLY DIAGNOSIS; FEMALE; GENETICS; GENOTYPING TECHNIQUE; HUMAN; HUMAN PAPILLOMAVIRUS TYPE 16; MASS SCREENING; MOLECULAR DIAGNOSIS; PAPILLOMAVIRUS INFECTIONS; SENSITIVITY AND SPECIFICITY; UTERINE CERVICAL NEOPLASMS; VIROLOGY;

CERVICAL INTRAEPITHELIAL NEOPLASIA; CYTODIAGNOSIS; DNA, VIRAL; EARLY DETECTION OF CANCER; FEMALE; GENOTYPING TECHNIQUES; HUMAN PAPILLOMAVIRUS 16; HUMANS; MASS SCREENING; MOLECULAR DIAGNOSTIC TECHNIQUES; PAPILLOMAVIRUS INFECTIONS; SENSITIVITY AND SPECIFICITY; UTERINE CERVICAL NEOPLASMS;

EID: 84904356042     PISSN: 09237534     EISSN: 15698041     Source Type: Journal    
DOI: 10.1093/annonc/mdt538     Document Type: Review

References (114)

1. IARC, WHO/ICO information centre on HPV and cervical cancer (HPV Information Centre). Human papillomavirus and related cancers in World. 2010 Ref Type: Report.
2. Arbyn, M., Castellsague, X., de, S.S., et al. Worldwide burden of cervical cancer in 2008. Ann Oncol 22 (2011), 2675–2686.
3. Peto, J., Gilham, C., Fletcher, O., et al. The cervical cancer epidemic that screening has prevented in the UK. Lancet 364 (2004), 249–256.
4. de, K.I., van der Aa, M.A., van, B.M., et al. Trends in cervical cancer in the Netherlands until 2007: has the bottom been reached?. Int J Cancer 128 (2011), 2174–2181.
5. Gustafsson, L., Ponten, J., Zack, M., et al. International incidence rates of invasive cervical cancer after introduction of cytological screening. Cancer Causes Control 8 (1997), 755–763.
6. Arbyn, M., Raifu, A.O., Weiderpass, E., et al. Trends of cervical cancer mortality in the member states of the European Union. Eur J Cancer 45 (2009), 2640–2648.
7. Cuzick, J., Clavel, C., Petry, K.U., et al. Overview of the European and North American studies on HPV testing in primary cervical cancer screening. Int J Cancer 119 (2006), 1095–1101.
8. Nanda, K., McCrory, D.C., Myers, E.R., et al. Accuracy of the Papanicolaou test in screening for and follow-up of cervical cytologic abnormalities: a systematic review. Ann Intern Med 132 (2000), 810–819.
9. Fahey, M.T., Irwig, L., Macaskill, P., Meta-analysis of Pap test accuracy. Am J Epidemiol 141 (1995), 680–689.
10. Katki, H.A., Wentzensen, N., How might HPV testing be integrated into cervical screening?. Lancet Oncol 13 (2012), 8–10.
11. Bulk, S., Visser, O., Rozendaal, L., et al. Cervical cancer in the Netherlands 1989–1998: decrease of squamous cell carcinoma in older women, increase of adenocarcinoma in younger women. Int J Cancer 113 (2005), 1005–1009.
12. Anttila, A., Pukkala, E., Soderman, B., et al. Effect of organised screening on cervical cancer incidence and mortality in Finland, 1963–1995: recent increase in cervical cancer incidence. Int J Cancer 83 (1999), 59–65.
13. Walboomers, J.M., Jacobs, M.V., Manos, M.M., et al. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 189 (1999), 12–19.
14. Bouvard, V., Baan, R., Straif, K., et al. A review of human carcinogens—part B: biological agents. Lancet Oncol 10 (2009), 321–322.
15. Munoz, N., Bosch, F.X., Castellsague, X., et al. Against which human papillomavirus types shall we vaccinate and screen? The international perspective. Int J Cancer 111 (2004), 278–285.
16. Castellsague, X., Diaz, M., de Sanjose, S., et al. Worldwide human papillomavirus etiology of cervical adenocarcinoma and its cofactors: implications for screening and prevention. J Natl Cancer Inst 98 (2006), 303–315.
17. Franceschi, S., Monitoring HPV16/18 immunisation in England and elsewhere. Br J Cancer 103 (2010), 157–158.
18. Garland, S.M., Skinner, S.R., Brotherton, J.M., Adolescent and young adult HPV vaccination in Australia: achievements and challenges. Prev Med 53:Suppl 1 (2011), S29–S35.
19. Shearer, B.D., HPV vaccination: understanding the impact on HPV disease. Purple Papers 34 (2011), 1–18.
20. EA van Lier. Immunization coverage National Immunization programme in The NetherlandsRIVM report 210021014/2011. 1-1-2011. Ref Type: Report.
21. Bartlett, J.A., Peterson, J.A., The uptake of human papillomavirus (HPV) vaccine among adolescent females in the United States: a review of the literature. J Sch Nurs 27 (2011), 434–446.
22. Arbyn, M., de, S.S., Saraiya, M., et al. EUROGIN 2011 roadmap on prevention and treatment of HPV-related disease. Int J Cancer 131 (2012), 1969–1982.
23. Etter, D.J., Zimet, G.D., Rickert, V.I., Human papillomavirus vaccine in adolescent women: a 2012 update. Curr Opin Obstet Gynecol 24 (2012), 305–310.
24. Bulkmans, N.W., Berkhof, J., Rozendaal, L., 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 370 (2007), 1764–1772.
25. Kitchener, H.C., Almonte, M., Thomson, C., et al. HPV testing in combination with liquid-based cytology in primary cervical screening (ARTISTIC): a randomised controlled trial. Lancet Oncol 10 (2009), 672–682.
26. Naucler, P., Ryd, W., Tornberg, S., et al. Human papillomavirus and Papanicolaou tests to screen for cervical cancer. N Engl J Med 357 (2007), 1589–1597.
27. Naucler, P., Ryd, W., Tornberg, S., 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 101 (2009), 88–99.
28. Ronco, G., Giorgi-Rossi, P., Carozzi, F., et al. Efficacy of human papillomavirus testing for the detection of invasive cervical cancers and cervical intraepithelial neoplasia: a randomised controlled trial. Lancet Oncol 11 (2010), 249–257.
29. Mayrand, M.H., Duarte-Franco, E., Rodrigues, I., et al. Human papillomavirus DNA versus Papanicolaou screening tests for cervical cancer. N Engl J Med 357 (2007), 1579–1588.
30. Cuzick, J., Szarewski, A., Mesher, D., 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 122 (2008), 2294–2300.
31. Arbyn, M., Ronco, G., Meijer, C.J., et al. Trials comparing cytology with human papillomavirus screening. Lancet Oncol 10 (2009), 935–936.
32. Sasieni, P., Castle, P.E., Cuzick, J., Further analysis of the ARTISTIC trial. Lancet Oncol 10 (2009), 841–842.
33. Rijkaart, D.C., Berkhof, J., Rozendaal, L., 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 13 (2012), 78–88.
34. Dillner, J., Rebolj, M., Birembaut, P., et al. Long term predictive values of cytology and human papillomavirus testing in cervical cancer screening: joint European cohort study. BMJ, 337, 2008, a1754.
35. Katki, H.A., Kinney, W.K., Fetterman, B., 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 12 (2011), 663–672.
36. Ronco G, Dillner J, Elfström KM, et al. Efficacy of HPV-based screening for prevention of invasive cervical cancer: follow-up of four European randomised controlled trials. The International HPV screening working group. Lancet. 2013 November 1. doi:pii: S0140-6736(13)62218-7. 10.1016/S0140-6736(13)62218-7. [epub ahead of print].
37. Berkhof, J., Coupe, V.M., Bogaards, J.A., et al. The health and economic effects of HPV DNA screening in The Netherlands. Int J Cancer 127 (2010), 2147–2158.
38. Rijkaart, D.C., Berkhof, J., van Kemenade, F.J., et al. HPV DNA testing in population-based cervical screening (VUSA-Screen study): results and implications. Br J Cancer 106 (2012), 975–981.
39. Dijkstra, M., van, N.D., Rijkaart, D., et al. Primary hrHPV DNA testing in cervical cancer screening: how to manage screen positive women? A POBASCAM trial substudy. Cancer Epidemiol Biomarkers Prev, 2013 June 3 [epub ahead of print], doi: 10.1158/1055-9965.EPI-13-0173.
40. Arbyn, M., Ronco, G., Anttila, A., et al. Evidence regarding human papillomavirus testing in secondary prevention of cervical cancer. Vaccine 30:Suppl 5 (2012), F88–F99.
41. Saslow, D., Solomon, D., Lawson, H.W., et al. American cancer society, American society for colposcopy and cervical pathology, and American society for clinical pathology screening guidelines for the prevention and early detection of cervical cancer. Am J Clin Pathol 137 (2012), 516–542.
42. Sankaranarayanan, R., Nene, B.M., Shastri, S.S., et al. HPV screening for cervical cancer in rural India. N Engl J Med 360 (2009), 1385–1394.
43. +-PCR and SPF10-line blot assays for detection of high-risk human papillomavirus in samples from women with normal cytology results who develop grade 3 cervical intraepithelial neoplasia. J Clin Microbiol 46 (2008), 3215–3221.
44. Meijer, C.J., Berkhof, J., Castle, P.E., et al. Guidelines for human papillomavirus DNA test requirements for primary cervical cancer screening in women 30 years and older. Int J Cancer 124 (2009), 516–520.
45. Meijer, C.J., Berkhof, H., Heideman, D.A., et al. Validation of high-risk HPV tests for primary cervical screening. J Clin Virol 46:Suppl 3 (2009), S1–S4.
46. Castle, P.E., Sadorra, M., Lau, T., et al. Evaluation of a prototype real-time PCR assay for carcinogenic human papillomavirus (HPV) detection and simultaneous HPV genotype 16 (HPV16) and HPV18 genotyping. J Clin Microbiol 47 (2009), 3344–3347.
47. Snijders, P.J., Heideman, D.A., Meijer, C.J., Methods for HPV detection in exfoliated cell and tissue specimens. APMIS 118 (2010), 520–528.
48. +-PCR-enzyme immunoassay in population-based cervical screening. J Clin Microbiol 48 (2010), 797–801.
49. Heideman, D.A., Hesselink, A.T., Berkhof, J., et al. Clinical validation of the cobas 4800 HPV test for cervical screening purposes. J Clin Microbiol 49 (2011), 3983–3985.
50. Carozzi, F.M., Burroni, E., Bisanzi, S., et al. Comparison of clinical performance of Abbott RealTime High Risk HPV test with that of hybrid capture 2 assay in a screening setting. J Clin Microbiol 49 (2011), 1446–1451.
51. Poljak, M., Cuzick, J., Kocjan, B.J., et al. Nucleic acid tests for the detection of alpha human papillomaviruses. Vaccine 30:Suppl 5 (2012), F100–F106.
52. Hesselink, A.T., Meijer, C.J., Poljak, M., et al. Clinical validation of the Abbott RealTime High Risk (HR) HPV assay according to the guidelines for HPV DNA test requirements for cervical screening. J Clin Microbiol 51 (2013), 2409–2410.
53. Getman, D., Aiyer, A., Dockter, J., et al. Efficiency of the APTIMA HPV Assay for detection of HPV RNA and DNA targets. J Clin Virol 45:Suppl 1 (2009), S49–S54.
54. Wu, R., Belinson, S.E., Du, H., et al. Human papillomavirus messenger RNA assay for cervical cancer screening: the Shenzhen Cervical Cancer Screening Trial I. Int J Gynecol Cancer 20 (2010), 1411–1414.
55. Monsonego, J., Hudgens, M.G., Zerat, L., et al. Evaluation of oncogenic human papillomavirus RNA and DNA tests with liquid-based cytology in primary cervical cancer screening: the FASE study. Int J Cancer 129 (2011), 691–701.
56. Heideman, D.A., Hesselink, A.T., van Kemenade, F.J., et al. The Aptima HPV assay fulfills the cross-sectional clinical and reproducibility criteria of international guidelines for human papillomavirus test requirements for cervical screening. J Clin Microbiol 51 (2013), 3653–3657.
57. Cuzick, J., Cadman, L., Mesher, D., et al. Comparing the performance of six human papillomavirus tests in a screening population. Br J Cancer 108 (2013), 908–913.
58. Szarewski, A., Mesher, D., Cadman, L., et al. Comparison of seven tests for high-grade cervical intraepithelial neoplasia in women with abnormal smears: the Predictors 2 study. J Clin Microbiol 50 (2012), 1867–1873.
59. Rijkaart, D.C., Berkhof, J., van Kemenade, F.J., et al. Evaluation of 14 triage strategies for HPV DNA-positive women in population-based cervical screening. Int J Cancer 130 (2012), 602–610.
60. Clifford, G.M., Smith, J.S., Plummer, M., et al. Human papillomavirus types in invasive cervical cancer worldwide: a meta-analysis. Br J Cancer 88 (2003), 63–73.
61. Khan, M.J., Castle, P.E., Lorincz, A.T., 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 97 (2005), 1072–1079.
62. Castle, P.E., Stoler, M.H., Wright, T.C. Jr, et al. 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 12 (2011), 880–890.
63. Meijer, C.J., Berkhof, J., Screening: cervical cancer—should we abandon cytology for screening?. Nat Rev Clin Oncol 9 (2012), 558–559.
64. von Knebel, D.M., New markers for cervical dysplasia to visualise the genomic chaos created by aberrant oncogenic papillomavirus infections. Eur J Cancer 38 (2002), 2229–2242.
65. Duensing, S., Duensing, A., Flores, E.R., et al. Centrosome abnormalities and genomic instability by episomal expression of human papillomavirus type 16 in raft cultures of human keratinocytes. J Virol 75 (2001), 7712–7716.
66. Duensing, S., Munger, K., The human papillomavirus type 16 E6 and E7 oncoproteins independently induce numerical and structural chromosome instability. Cancer Res 62 (2002), 7075–7082.
67. Sotlar, K., Stubner, A., Diemer, D., et al. Detection of high-risk human papillomavirus E6 and E7 oncogene transcripts in cervical scrapes by nested RT-polymerase chain reaction. J Med Virol 74 (2004), 107–116.
68. Molden, T., Kraus, I., Skomedal, H., et al. PreTect HPV-Proofer: real-time detection and typing of E6/E7 mRNA from carcinogenic human papillomaviruses. J Virol Methods 142 (2007), 204–212.
69. Rijkaart, D.C., Heideman, D.A., Coupe, V.M., et al. High-risk human papillomavirus (hrHPV) E6/E7 mRNA testing by PreTect HPV-Proofer for detection of cervical high-grade intraepithelial neoplasia and cancer among hrHPV DNA-positive women with normal cytology. J Clin Microbiol 50 (2012), 2390–2396.
70. Klaes, R., Friedrich, T., Spitkovsky, D., et al. Overexpression of p16(INK4A) as a specific marker for dysplastic and neoplastic epithelial cells of the cervix uteri. Int J Cancer 92 (2001), 276–284.
71. Khleif, S.N., DeGregori, J., Yee, C.L., et al. Inhibition of cyclin D-CDK4/CDK6 activity is associated with an E2F-mediated induction of cyclin kinase inhibitor activity. Proc Natl Acad Sci USA 93 (1996), 4350–4354.
72. McLaughlin-Drubin, M.E., Crum, C.P., Munger, K., Human papillomavirus E7 oncoprotein induces KDM6A and KDM6B histone demethylase expression and causes epigenetic reprogramming. Proc Natl Acad Sci USA 108 (2011), 2130–2135.
73. Guo, M., Hu, L., Baliga, M., et al. The predictive value of p16(INK4a) and hybrid capture 2 human papillomavirus testing for high-grade cervical intraepithelial neoplasia. Am J Clin Pathol 122 (2004), 894–901.
74. Nieh, S., Chen, S.F., Chu, T.Y., et al. Is p16(INK4A) expression more useful than human papillomavirus test to determine the outcome of atypical squamous cells of undetermined significance-categorized Pap smear? A comparative analysis using abnormal cervical smears with follow-up biopsies. Gynecol Oncol 97 (2005), 35–40.
75. Yoshida, T., Fukuda, T., Sano, T., et al. Usefulness of liquid-based cytology specimens for the immunocytochemical study of p16 expression and human papillomavirus testing: a comparative study using simultaneously sampled histology materials. Cancer 102 (2004), 100–108.
76. Carozzi, F., Confortini, M., Dalla, P.P., 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 9 (2008), 937–945.
77. Denton, K.J., Bergeron, C., Klement, P., et al. The sensitivity and specificity of p16(INK4a) cytology vs HPV testing for detecting high-grade cervical disease in the triage of ASC-US and LSIL pap cytology results. Am J Clin Pathol 134 (2010), 12–21.
78. Carozzi, F., Gillio-Tos, A., Confortini, M., et al. Risk of high-grade cervical intraepithelial neoplasia during follow-up in HPV-positive women according to baseline p16-INK4A results: a prospective analysis of a nested substudy of the NTCC randomised controlled trial. Lancet Oncol 14 (2013), 168–176.
79. Szarewski, A., Ambroisine, L., Cadman, L., et al. Comparison of predictors for high-grade cervical intraepithelial neoplasia in women with abnormal smears. Cancer Epidemiol Biomarkers Prev 17 (2008), 3033–3042.
80. Wentzensen, N., Bergeron, C., Cas, F., et al. Evaluation of a nuclear score for p16(INK4a)-stained cervical squamous cells in liquid-based cytology samples. Cancer 105 (2005), 461–467.
81. Schmidt, D., Bergeron, C., Denton, K.J., et al. p16/ki-67 dual-stain cytology in the triage of ASCUS and LSIL papanicolaou cytology: results from the European equivocal or mildly abnormal Papanicolaou cytology study. Cancer Cytopathol 119 (2011), 158–166.
82. Wentzensen, N., Schwartz, L., Zuna, R.E., et al. Performance of p16/Ki-67 immunostaining to detect cervical cancer precursors in a colposcopy referral population. Clin Cancer Res 18 (2012), 4154–4162.
83. Petry, K.U., Schmidt, D., Scherbring, S., et al. Triaging Pap cytology negative, HPV positive cervical cancer screening results with p16/Ki-67 Dual-stained cytology. Gynecol Oncol 121 (2011), 505–509.
84. Mesher, D., Szarewski, A., Cadman, L., et al. Comparison of human papillomavirus testing strategies for triage of women referred with low-grade cytological abnormalities. Eur J Cancer, 2013 February 26 [epub ahead of print].
85. Herman, J.G., Baylin, S.B., Gene silencing in cancer in association with promoter hypermethylation. N Engl J Med 349 (2003), 2042–2054.
86. Henken, F.E., Wilting, S.M., Overmeer, R.M., et al. Sequential gene promoter methylation during HPV-induced cervical carcinogenesis. Br J Cancer 97 (2007), 1457–1464.
87. Steenbergen, R.D., Kramer, D., Braakhuis, B.J., et al. TSLC1 gene silencing in cervical cancer cell lines and cervical neoplasia. J Natl Cancer Inst 96 (2004), 294–305.
88. Esteller, M., Epigenetics in cancer. N Engl J Med 358 (2008), 1148–1159.
89. Bierkens, M., Hesselink, A.T., Meijer, C.J., et al. CADM1 and MAL promoter methylation levels in hrHPV-positive cervical scrapes increase proportional to degree and duration of underlying cervical disease. Int J Cancer 133 (2013), 1293–1299.
90. Hesselink, A.T., Heideman, D.A., Steenbergen, R.D., et al. Combined promoter methylation analysis of CADM1 and MAL: an objective triage tool for high-risk human papillomavirus DNA-positive women. Clin Cancer Res 17 (2011), 2459–2465.
91. Dijkstra. Long-term CIN3+ risks following primary hrHPV DNA and triage testing in Cervical Cancer screening. submitted.
92. Bais, A.G., van Kemenade, F.J., Berkhof, J., et al. Human papillomavirus testing on self-sampled cervicovaginal brushes: an effective alternative to protect nonresponders in cervical screening programs. Int J Cancer 120 (2007), 1505–1510.
93. Raab, S.S., Grzybicki, D.M., Zarbo, R.J., et al. Frequency and outcome of cervical cancer prevention failures in the United States. Am J Clin Pathol 128 (2007), 817–824.
94. Sasieni, P., Adams, J., Cuzick, J., Benefit of cervical screening at different ages: evidence from the UK audit of screening histories. Br J Cancer 89 (2003), 88–93.
95. Petignat, P., Faltin, D.L., Bruchim, I., et al. Are self-collected samples comparable to physician-collected cervical specimens for human papillomavirus DNA testing? A systematic review and meta-analysis. Gynecol Oncol 105 (2007), 530–535.
96. Brink, A.A., Meijer, C.J., Wiegerinck, M.A., et al. High concordance of results of testing for human papillomavirus in cervicovaginal samples collected by two methods, with comparison of a novel self-sampling device to a conventional endocervical brush. J Clin Microbiol 44 (2006), 2518–2523.
97. Gok, M., Heideman, D.A., van Kemenade, F.J., et al. HPV testing on self collected cervicovaginal lavage specimens as screening method for women who do not attend cervical screening: cohort study. BMJ, 340, 2010, c1040.
98. Virtanen, A., Nieminen, P., Luostarinen, T., et al. Self-sample HPV tests as an intervention for nonattendees of cervical cancer screening in Finland: a randomized trial. Cancer Epidemiol Biomarkers Prev 20 (2011), 1960–1969.
99. Snijders, P.J., Verhoef, V.M., Arbyn, M., et al. High-risk HPV testing on self-sampled versus clinician-collected specimens: a review on the clinical accuracy and impact on population attendance in cervical cancer screening. Int J Cancer 32 (2012), 2223–2236.
100. Holanda, F. Jr, Castelo, A., Veras, T.M., et al. Primary screening for cervical cancer through self sampling. Int J Gynaecol Obstet 95 (2006), 179–184.
101. Qiao, Y.L., Sellors, J.W., Eder, P.S., 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 9 (2008), 929–936.
102. Lazcano-Ponce, E., Lorincz, A.T., Cruz-Valdez, A., et al. Self-collection of vaginal specimens for human papillomavirus testing in cervical cancer prevention (MARCH): a community-based randomised controlled trial. Lancet 378 (2011), 1868–1873.
103. Ogilvie, G.S., Patrick, D.M., Schulzer, M., et al. Diagnostic accuracy of self collected vaginal specimens for human papillomavirus compared to clinician collected human papillomavirus specimens: a meta-analysis. Sex Transm Infect 81 (2005), 207–212.
104. Dannecker, C., Siebert, U., Thaler, C.J., et al. Primary cervical cancer screening by self-sampling of human papillomavirus DNA in internal medicine outpatient clinics. Ann Oncol 15 (2004), 863–869.
105. Khanna, N., Mishra, S.I., Tian, G., et al. Human papillomavirus detection in self-collected vaginal specimens and matched clinician-collected cervical specimens. Int J Gynecol Cancer 17 (2007), 615–622.
106. Castle, P.E., Schiffman, M., Burk, R.D., et al. Restricted cross-reactivity of hybrid capture 2 with nononcogenic human papillomavirus types. Cancer Epidemiol Biomarkers Prev 11 (2002), 1394–1399.
107. Baldwin, S., Santos, C., Mendez, B.E., et al. Comparison of type-specific human papillomavirus data from self and clinician directed sampling. Gynecol Oncol 97 (2005), 612–617.
108. Nobbenhuis, M.A., Helmerhorst, T.J., van den Brule, A.J., et al. Primary screening for high risk HPV by home obtained cervicovaginal lavage is an alternative screening tool for unscreened women. J Clin Pathol 55 (2002), 435–439.
109. Bulkmans, N.W., Rozendaal, L., Snijders, P.J., 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 110 (2004), 94–101.
110. Kitchener, H.C., Almonte, M., Wheeler, P., et al. HPV testing in routine cervical screening: cross sectional data from the ARTISTIC trial. Br J Cancer 95 (2006), 56–61.
111. Ronco, G., Giorgi-Rossi, P., Carozzi, F., 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 7 (2006), 547–555.
112. Ronco, G., Giorgi-Rossi, P., Carozzi, F., 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 100 (2008), 492–501.
113. Leinonen, M., Nieminen, P., Kotaniemi-Talonen, L., et al. Age-specific evaluation of primary human papillomavirus screening vs conventional cytology in a randomized setting. J Natl Cancer Inst 101 (2009), 1612–1623.
114. Schmeink, C.E., Bekkers, R.L., Massuger, L.F., et al. The potential role of self-sampling for high-risk human papillomavirus detection in cervical cancer screening. Rev Med Virol 21 (2011), 139–153.