Human papillomavirus and cervical cancer: Biomarkers for improved prevention efforts

Future Microbiology

Volumn 6, Issue 9, 2011, Pages 1083-1098

  Sahasrabuddhe, Vikrant V ^a   Luhn, Patricia ^a   Wentzensen, Nicolas ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

accuracy; biomarkers; cervical cancer; HPV; prevention; risk prediction; screening

Indexed keywords

BIOLOGICAL MARKER; PROTEIN E6; PROTEIN E7;

CANCER INCIDENCE; CANCER PREVENTION; CANCER SCREENING; CELL CYCLE S PHASE; COLPOSCOPY; CYTODIAGNOSIS; DIAGNOSTIC ACCURACY; DIAGNOSTIC APPROACH ROUTE; DIAGNOSTIC TEST ACCURACY STUDY; DNA HYBRIDIZATION; EMERGENCY HEALTH SERVICE; HUMAN; NONHUMAN; PAPANICOLAOU TEST; PAPILLOMAVIRUS INFECTION; PRECANCER; PRIORITY JOURNAL; REVIEW; SENSITIVITY AND SPECIFICITY; UTERINE CERVIX BIOPSY; UTERINE CERVIX CANCER; VALIDATION STUDY; VIRUS DETECTION; VIRUS GENOME; WART VIRUS;

ALPHAPAPILLOMAVIRUS; EARLY DETECTION OF CANCER; FEMALE; GENES, VIRAL; HUMANS; MASS SCREENING; MOLECULAR DIAGNOSTIC TECHNIQUES; PAPILLOMAVIRUS INFECTIONS; TUMOR MARKERS, BIOLOGICAL; UTERINE CERVICAL NEOPLASMS;

HUMAN PAPILLOMAVIRUS;

EID: 80053544244     PISSN: 17460913     EISSN: 17460921     Source Type: Journal    
DOI: 10.2217/fmb.11.87     Document Type: Review

References (149)

1. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int. J. Cancer 127(12), 2893-2917 (2010).
2. Walboomers JM, Jacobs MV, Manos MM, et al. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J. Pathol. 189(1), 12-19 (1999). (Pubitemid 29406813)
3. Munoz N, Bosch FX, de Sanjose S, et al. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N. Engl. J. Med. 348(6), 518-527 (2003). (Pubitemid 36159887)
4. Ferenczy A, Franco E. Cervical-cancer screening beyond the year 2000. Lancet Oncol. 2(1), 27-32 (2001). (Pubitemid 33585914)
5. Jordan J, Arbyn M, Martin-Hirsch P, et al. European guidelines for quality assurance in cervical cancer screening: recommendations for clinical management of abnormal cervical cytology, part 1. Cytopathology 19(6), 342-354 (2008).
6. Mitchell H. The price of guidelines: revising the national guidelines for managing Australian women with abnormal pap smears. Sex Health 3(1), 53-55 (2006). (Pubitemid 43269509)
7. Barzon L, Giorgi C, Buonaguro FM, Palu G. Guidelines of the Italian Society for Virology on HPV testing and vaccination for cervical cancer prevention. Infect. Agent. Cancer 3, 14 (2008).
8. Wright TC, Jr., 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. 197(4), 346-355 (2007). (Pubitemid 47464164)
9. Meijer CJ, Berkhof J, Castle PE, et al. Guidelines for human papillomavirus DNA test requirements for primary cervical cancer screening in women 30 years and older. Int. J. Cancer 124(3), 516-520 (2009).
10. Katki HA, Wacholder S, Solomon D, Castle PE, Schiffman M. Risk estimation for the next generation of prevention programmes for cervical cancer. Lancet Oncol. 10(11), 1022-1023 (2009).
11. Castle PE, Sideri M, Jeronimo J, Solomon D, Schiffman M. Risk assessment to guide the prevention of cervical cancer. Am. J. Obstet. Gynecol. 197(4), 356.e1-356.e6 (2007).
12. Castle PE, Schiffman M, Wheeler CM, Solomon D. Evidence for frequent regression of cervical intraepithelial neoplasia-grade 2. Obstet. Gynecol. 113(1), 18-25 (2009).
13. McCredie MR, Sharples KJ, Paul C, 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. 9(5), 425-434 (2008).
14. Schiffman M, Rodriguez AC. Heterogeneity in CIN3 diagnosis. Lancet Oncol. 9(5), 404-406 (2008). (Pubitemid 351618081)
15. Bouvard V, Baan R, Straif K, et al. A review of human carcinogens -Part B: biological agents. Lancet Oncol. 10(4), 321-322 (2009).
16. Duensing S, Munger K. Mechanisms of genomic instability in human cancer: insights from studies with human papillomavirus oncoproteins. Int. J. Cancer 109(2), 157-162 (2004). (Pubitemid 38240914)
17. Arbyn M, Ronco G, Cuzick J, Wentzensen N, Castle PE. How to evaluate emerging technologies in cervical cancer screening? Int. J. Cancer 125(11), 2489-2496 (2009).
18. Solomon D, Breen N, McNeel T. Cervical cancer screening rates in the United States and the potential impact of implementation of screening guidelines. CA Cancer J. Clin. 57(2), 105-111 (2007). (Pubitemid 46535710)
19. Yabroff KR, Saraiya M, Meissner HI, et al. Specialty differences in primary care physician reports of papanicolaou test screening practices: a national survey, 2006 to 2007. Ann. Intern. Med. 151(9), 602-611 (2009).
20. Saraiya M, Berkowitz Z, Yabroff KR, Wideroff L, Kobrin S, Benard V. Cervical cancer screening with both human papillomavirus and Papanicolaou testing vs Papanicolaou testing alone: what screening intervals are physicians recommending? Arch. Intern. Med. 170(11), 977-985 (2010).
21. Tangka FK, OHara B, Gardner JG, et al. Meeting the cervical cancer screening needs of underserved women: the National Breast and Cervical Cancer Early Detection Program, 2004-2006. Cancer Causes Control 21(7), 1081-1090 (2010).
22. Nanda K, McCrory DC, Myers ER, et al. Accuracy of the Papanicolaou test in screening for and follow-up of cervical cytologic abnormalities: a systematic review. Ann. Intern. Med. 132(10), 810-819 (2000). (Pubitemid 30317797)
23. Cong X, Cox DD, Cantor SB. Bayesian meta-analysis of Papanicolaou smear accuracy. Gynecol. Oncol. 107(1 Suppl 1), S133-S137 (2007). (Pubitemid 47483890)
24. Myers ER, McCrory DC, Subramanian S, et al. Setting the target for a better cervical screening test: characteristics of a cost-effective test for cervical neoplasia screening. Obstet. Gynecol. 96(5 Pt 1), 645-652 (2000).
25. MacDonald CF. Assessing secondary prevention methods for cervical cancer: costs and benefits in managed care. Am. J. Manag. Care, 14(6 Suppl. 1), S185-S192 (2008). (Pubitemid 351898368)
26. Schiffman M, Wentzensen N, Wacholder S, Kinney W, Gage JC, Castle PE. Human papillomavirus testing in the prevention of cervical cancer. J. Natl. Cancer Inst. 103(5), 368-383 (2011).
27. Siebers AG, Klinkhamer PJ, Grefte JM, et al. Comparison of liquid-based cytology with conventional cytology for detection of cervical cancer precursors: a randomized controlled trial. JAMA 302(16), 1757-1764 (2009).
28. Kulasingam SL, Hughes JP, Kiviat NB, et al. Evaluation of human papillomavirus testing in primary screening for cervical abnormalities: comparison of sensitivity, specificity, and frequency of referral. JAMA 288(14), 1749-1757 (2002).
29. Arbyn M, Buntinx F, Van Ranst M, Paraskevaidis E, Martin-Hirsch P, Dillner J. Virologic versus cytologic triage of women with equivocal Pap smears: a meta-analysis of the accuracy to detect high-grade intraepithelial neoplasia. J. Natl. Cancer Inst. 96(4), 280-293 (2004). (Pubitemid 38256273)
30. Arbyn M, Paraskevaidis E, Martin-Hirsch P, Prendiville W, Dillner J. Clinical utility of HPV-DNA detection: triage of minor cervical lesions, follow-up of women treated for high-grade CIN: an update of pooled evidence. Gynecol. Oncol. 99(3 Suppl. 1), S7-S11 (2005). (Pubitemid 41774340)
31. Huh W, Einstein MH, Herzog TJ, Franco EL. What is the role of HPV typing in the United States now and in the next five years in a vaccinated population? Gynecol. Oncol. 117(3), 481-485 (2010).
32. 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, A1754 (2008).
33. 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(5), 303-315 (2006). (Pubitemid 43338210)
34. Arbyn M, Sasieni P, Meijer CJ, Clavel C, Koliopoulos G, Dillner J. Chapter 9: Clinical applications of HPV testing: a summary of meta-analyses. Vaccine 24(Suppl. 3), S3/78-89 (2006).
35. Cuzick J, Arbyn M, Sankaranarayanan R, et al. Overview of human papillomavirus-based and other novel options for cervical cancer screening in developed and developing countries. Vaccine 26(Suppl. 10), K29-K41 (2008).
36. Eder PS, Lou J, Huff J, Macioszek J. The next-generation Hybrid Capture High-Risk HPV DNA assay on a fully automated platform. J. Clin. Virol. 45(Suppl. 1), S85-S92 (2009).
37. Bartholomew DA, Luff RD, Quigley NB, Curtis M, Olson MC. Analytical performance of Cervista® HPV 16/18 genotyping test for cervical cytology samples. J. Clin. Virol. 51(1), 38-43 (2011).
38. De Francesco MA, Gargiulo F, Schreiber C, Ciravolo G, Salinaro F, Manca N. Comparison of the AMPLICOR human papillomavirus test and the hybrid capture 2 assay for detection of high-risk human papillomavirus in women with abnormal PAP smear. J. Virol. Methods 147(1), 10-17 (2008). (Pubitemid 350253123)
39. Stoler MH, Wright TC, Jr., Sharma A, Apple R, Gutekunst K, Wright TL. High-risk human papillomavirus testing in women with ASC-US cytology: results from the ATHENA HPV study. Am. J. Clin. Pathol. 135(3), 468-475 (2011).
40. Mayrand MH, Duarte-Franco E, Rodrigues I, et al. Human papillomavirus DNA versus Papanicolaou screening tests for cervical cancer. N. Engl. J. Med. 357(16), 1579-1588 (2007). (Pubitemid 47598400)
41. Bulkmans NW, 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(9601), 1764-1772 (2007). (Pubitemid 350137476)
42. 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(2), 88-99 (2009).
43. 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(23), 1612-1623 (2009).
44. Sankaranarayanan R, Nene BM, Shastri SS, et al. HPV screening for cervical cancer in rural India. N. Engl. J. Med. 360(14), 1385-1394 (2009).
45. Kitchener HC, 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(7), 672-682 (2009).
46. 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(3), 249-257 (2010).
47. Koliopoulos G, Arbyn M, Martin-Hirsch P, Kyrgiou M, Prendiville W, Paraskevaidis E. Diagnostic accuracy of human papillomavirus testing in primary cervical screening: a systematic review and meta-analysis of non-randomized studies. Gynecol. Oncol. 104(1), 232-246 (2007). (Pubitemid 46054137)
48. Lynge E, Rebolj M. Primary HPV screening for cervical cancer prevention: results from European trials. Nat. Rev. Clin. Oncol. 6(12), 699-706 (2009).
49. Wentzensen N, Gravitt PE, Solomon D, Wheeler CM, Castle PE. A study of Amplicor human papillomavirus DNA detection in the atypical squamous cells of undetermined significance-low-grade squamous intraepithelial lesion triage study. Cancer Epidemiol. Biomarkers Prev. 18(5), 1341-1349 (2009).
50. Kinney W, Stoler MH, Castle PE. Special commentary: patient safety and the next generation of HPV DNA tests. Am. J. Clin. Pathol. 134(2), 193-199 (2010).
51. Katki HA, Kinney WK, 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(7), 663-672 (2011).
52. Moriarty AT, Schwartz MR, Eversole G, et al. Human papillomavirus testing and reporting rates: practices of participants in the College of American Pathologists Interlaboratory Comparison Program in Gynecologic Cytology in 2006. Arch. Pathol. Lab Med. 132(8), 1290-1294 (2008).
53. Human papillomavirus testing for triage of women with cytologic evidence of low-grade squamous intraepithelial lesions: baseline data from a randomized trial. The Atypical Squamous Cells of Undetermined Significance/Low-Grade Squamous Intraepithelial Lesions Triage Study (ALTS) Group. J. Natl. Cancer Inst. 92(5), 397-402 (2000).
54. Xi LF, Koutsky LA, Castle PE, et al. Human papillomavirus type 16 variants in paired enrollment and follow-up cervical samples: implications for a proper understanding of type-specific persistent infections. J. Infect. Dis. 202(11), 1667-1670 (2010).
55. Castle PE, Rodriguez AC, Burk RD, et al. Short term persistence of human papillomavirus and risk of cervical precancer and cancer: population based cohort study. BMJ 339, b2569 (2009).
56. Costa S, Negri G, Sideri M, et al. Human papillomavirus (HPV) test and PAP smear as predictors of outcome in conservatively treated adenocarcinoma in situ (AIS) of the uterine cervix. Gynecol. Oncol. 106(1), 170-176 (2007). (Pubitemid 46898589)
57. Einstein MH, Martens MG, Garcia FA, et al. Clinical validation of the Cervista HPV HR and 16/18 genotyping tests for use in women with ASC-US cytology. Gynecol. Oncol. 118(2), 116-122 (2010).
58. Geraets DT, Lenselink CH, Bekkers RL, van Doorn LJ, Quint WG, Melchers WJ. Universal human papillomavirus genotyping by the digene HPV Genotyping RH and LQ Tests. J. Clin. Virol. 50(4), 276-280 (2011).
59. Jamison J, Wilson RT, Carson J. The evaluation of human papillomavirus genotyping in cervical liquid-based cytology specimens; using the Roche Linear Array HPV genotyping assay. Cytopathology 20(4), 242-248 (2009).
60. Brismar-Wendel S, Froberg M, Hjerpe A, Andersson S, Johansson B. Age-specific prevalence of HPV genotypes in cervical cytology samples with equivocal or low-grade lesions. Br. J. Cancer 101(3), 511-517 (2009).
61. Wong AK, Chan RC, Nichols WS, Bose S. Human papillomavirus (HPV) in atypical squamous cervical cytology: the Invader HPV test as a new screening assay. J. Clin. Microbiol. 46(3), 869-875 (2008). (Pubitemid 351379971)
62. Arbyn M, Ronco G, Meijer CJ, Naucler P. Trials comparing cytology with human papillomavirus screening. Lancet Oncol. 10(10), 935-936 (2009).
63. Cuschieri K, Wentzensen N. Human papillomavirus mRNA and p16 detection as biomarkers for the improved diagnosis of cervical neoplasia. Cancer Epidemiol. Biomarkers Prev. 17(10), 2536-2545 (2008).
64. Wentzensen N, von Knebel Doeberitz M. Biomarkers in cervical cancer screening. Dis. Markers 23(4), 315-330 (2007). (Pubitemid 47015791)
65. Mayrand MH, Franco EL. Integrating novel primary-and secondary-prevention strategies: the next challenge for cervical cancer control. Future Oncol. 6(11), 1725-1733 (2010).
66. 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(11), 3033-3042 (2008).
67. Doorbar J. Papillomavirus life cycle organization and biomarker selection. Dis. Markers 23(4), 297-313 (2007). (Pubitemid 47015790)
68. Cattani P, Zannoni GF, Ricci C, et al. Clinical performance of human papillomavirus E6 and E7 mRNA testing for high-grade lesions of the cervix. J. Clin. Microbiol. 47(12), 3895-3901 (2009).
69. Dockter J, Schroder A, Hill C, Guzenski L, Monsonego J, Giachetti C. Clinical performance of the APTIMA HPV Assay for the detection of high-risk HPV and high-grade cervical lesions. J. Clin. Virol. 45(Suppl. 1), S55-S61 (2009).
70. Coquillard G, Palao B, Patterson BK. Quantification of intracellular HPV E6/E7 mRNA expression increases the specificity and positive predictive value of cervical cancer screening compared with HPV DNA. Gynecol. Oncol. 120(1), 89-93 (2011).
71. Keegan H, McInerney J, Pilkington L, et al. Comparison of HPV detection technologies: Hybrid capture 2, PreTect HPV-Proofer and analysis of HPV DNA viral load in HPV16, HPV18 and HPV33 E6/E7 mRNA positive specimens. J. Virol. Methods 155(1), 61-66 (2009).
72. Ratnam S, Coutlee F, Fontaine D, et al. Clinical performance of the PreTect HPV-Proofer E6/E7 mRNA assay in comparison with that of the Hybrid Capture 2 test for identification of women at risk of cervical cancer. J. Clin. Microbiol. 48(8), 2779-2785 (2010).
73. Reuschenbach M, Clad A, von Knebel Doeberitz C, et al. Performance of p16INK4a-cytology, HPV mRNA, and HPV DNA testing to identify high grade cervical dysplasia in women with abnormal screening results. Gynecol. Oncol. 119(1), 98-105 (2010).
74. Sorbye SW, Fismen S, Gutteberg TJ, Mortensen ES. HPV mRNA test in women with minor cervical lesions: experience of the University Hospital of North Norway. J. Virol. Methods 169(1), 219-222 (2010).
75. Trope A, Sjoborg K, Eskild A, et al. Performance of human papillomavirus DNA and mRNA testing strategies for women with and without cervical neoplasia. J. Clin. Microbiol. 47(8), 2458-2464 (2009).
76. Wu R, Belinson SE, 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(8), 1411-1414 (2010).
77. Burger EA, Kornor H, Klemp M, Lauvrak V, Kristiansen IS. HPV mRNA tests for the detection of cervical intraepithelial neoplasia: a systematic review. Gynecol. Oncol. 120(3), 430-438 (2011).
78. Balasubramanian A, Hughes J, Mao C, et al. Evaluation of an ELISA for p16INK4a as a screening test for cervical cancer. Cancer Epidemiol. Biomarkers Prev. 18(11), 3008-3017 (2009).
79. Passamonti B, Gustinucci D, Recchia P, et al. Expression of p16 in abnormal pap-tests as an indicator of CIN2+ lesions: a possible role in the low grade ASC/US and L/SIL (Ig) cytologic lesions for screening prevention of uterine cervical tumours. Pathologica 102(1), 6-11 (2010).
80. Petry KU, 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. (2011).
81. Sung CO, Kim SR, Oh YL, Song SY. The use of p16(INK4A) immunocytochemistry in "Atypical squamous cells which cannot exclude HSIL" compared with "Atypical squamous cells of undetermined significance" in liquid-based cervical smears. Diagn. Cytopathol. 38(3), 168-171 (2010).
82. Guo M, Warriage I, Mutyala B, et al. Evaluation of p16 immunostaining to predict high-grade cervical intraepithelial neoplasia in women with Pap results of atypical squamous cells of undetermined significance. Diagn. Cytopathol. 39(7), 482-488 (2010).
83. Denton KJ, Bergeron C, Klement P, Trunk MJ, Keller T, Ridder R. 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(1), 12-21 (2010).
84. Schmidt D, Bergeron C, Denton KJ, Ridder R. 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 Cytopathology 119(3), 158-166 (2011).
85. Zeng WJ, Li Y, Fei HL, et al. The value of p16ink4a expression by fluorescence in situ hybridization in triage for high risk HPV positive in cervical cancer screening. Gynecol. Oncol. 120(1), 84-88 (2011).
86. Carozzi F, Confortini M, Dalla Palma 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(10), 937-945 (2008).
87. Tsoumpou I, Arbyn M, Kyrgiou M, et al. p16(INK4a) immunostaining in cytological and histological specimens from the uterine cervix: a systematic review and meta-analysis. Cancer Treat. Rev. 35(3), 210-220 (2009).
88. Halloush RA, Akpolat I, Jim Zhai Q, Schwartz MR, Mody DR. Comparison of ProEx C with p16INK4a and Ki-67 immunohistochemical staining of cell blocks prepared from residual liquid-based cervicovaginal material: a pilot study. Cancer 114(6), 474-480 (2008).
89. Siddiqui MT, Cohen C, Nassar A. Detecting high-grade cervical disease on ASC-H cytology: role of BD ProEx C and Digene Hybrid Capture II HPV DNA testing. Am. J. Clin. Pathol. 130(5), 765-770 (2008).
90. Siddiqui MT, Hornaman K, Cohen C, Nassar A. ProEx C immunocytochemistry and high-risk human papillomavirus DNA testing in papanicolaou tests with atypical squamous cell (ASC-US) cytology: correlation study with histologic biopsy. Arch. Pathol. Lab Med. 132(10), 1648-1652 (2008).
91. Guo M, Baruch AC, Silva EG, et al. Efficacy of p16 and ProExC immunostaining in the detection of high-grade cervical intraepithelial neoplasia and cervical carcinoma. Am. J. Clin. Pathol. 135(2), 212-220 (2011).
92. Kelly D, Kincaid E, Fansler Z, Rosenthal DL, Clark DP. Detection of cervical high-grade squamous intraepithelial lesions from cytologic samples using a novel immunocytochemical assay (ProEx C). Cancer 108(6), 494-500 (2006). (Pubitemid 46076970)
93. Tambouret RH. [Diagnostic importance of ProEx C in gynecologic cytopathology]. Ann. Pathol. 28 Spec No 1(1), S92-S93 (2008).
94. Pinto AP, Schlecht NF, Woo TY, Crum CP, Cibas ES. Biomarker (ProEx C, p16(INK4A), and MiB-1) distinction of high-grade squamous intraepithelial lesion from its mimics. Mod. Pathol. 21(9), 1067-1074 (2008).
95. Baak JP, Kruse AJ, Robboy SJ, Janssen EA, van Diermen B, Skaland I. Dynamic behavioural interpretation of cervical intraepithelial neoplasia with molecular biomarkers. J. Clin. Pathol. 59(10), 1017-1028 (2006). (Pubitemid 44570323)
96. Murphy N, Ring M, Heffron CC, et al. Quantitation of CDC6 and MCM5 mRNA in cervical intraepithelial neoplasia and invasive squamous cell carcinoma of the cervix. Mod. Pathol. 18(6), 844-849 (2005). (Pubitemid 40780519)
97. Branca M, Giorgi C, Santini D, et al. Survivin as a marker of cervical intraepithelial neoplasia and high-risk human papillomavirus and a predictor of virus clearance and prognosis in cervical cancer. Am. J. Clin. Pathol. 124(1), 113-121 (2005). (Pubitemid 40944383)
98. Liang J, Mittal KR, Wei JJ, Yee H, Chiriboga L, Shukla P. Utility of p16INK4a, CEA, Ki67, P53 and ER/PR in the differential diagnosis of benign, premalignant, and malignant glandular lesions of the uterine cervix and their relationship with Silverberg scoring system for endocervical glandular lesions. Int. J. Gynecol. Pathol. 26(1), 71-75 (2007). (Pubitemid 46036962)
99. Yu L, Wang L, Zhong J, Chen S. Diagnostic value of p16INK4A, Ki-67, and human papillomavirus L1 capsid protein immunochemical staining on cell blocks from residual liquid-based gynecologic cytology specimens. Cancer Cytopathol. 118(1), 47-55 (2010).
100. Huang MZ, Li HB, Nie XM, Wu XY, Jiang XM. An analysis on the combination expression of HPV L1 capsid protein and p16INK4a in cervical lesions. Diagn. Cytopathol. 38(8), 573-578 (2010).
101. Hoshikawa S, Sano T, Yoshida T, Ito H, Oyama T, Fukuda T. Immunohistological analysis of HPV L1 capsid protein and p16 protein in low-grade dysplastic lesions of the uterine cervix. Pathol. Res. Pract. 206(12), 816-820 (2010).
102. Schweizer J, Lu PS, Mahoney CW, et al. Feasibility study of a human papillomavirus E6 oncoprotein test for diagnosis of cervical precancer and cancer. J. Clin. Microbiol. 48(12), 4646-4648 (2010).
103. Yang HP, Walmer DK, Merisier D, et al. A pilot analytic study of a research-level, lower-cost human papillomavirus 16, 18, and 45 test. J. Virol. Methods 176(1-2), 112-114 (2011).
104. Sankaranarayanan R, Boffetta P. Research on cancer prevention, detection and management in low-and medium-income countries. Ann. Oncol. 21(10), 1935-1943 (2010).
105. Sauvaget C, Fayette JM, Muwonge R, Wesley R, Sankaranarayanan R. Accuracy of visual inspection with acetic acid for cervical cancer screening. Int. J. Gynaecol. Obstet. 113(1), 14-24 (2011).
106. Sankaranarayanan R, Esmy PO, Rajkumar R, et al. Effect of visual screening on cervical cancer incidence and mortality in Tamil Nadu, India: a cluster-randomised trial. Lancet 370(9585), 398-406 (2007). (Pubitemid 47176655)
107. Zhao FH, Lin MJ, Chen F, et al. Performance of high-risk human papillomavirus DNA testing as a primary screen for cervical cancer: a pooled analysis of individual patient data from 17 population-based studies from China. Lancet Oncol. 11(12), 1160-1171 (2010).
108. Goldie SJ, Gaffikin L, Goldhaber-Fiebert JD, et al. Cost-effectiveness of cervical-cancer screening in five developing countries. N. Engl. J. Med. 353(20), 2158-2168 (2005). (Pubitemid 41653107)
109. Qiao YL, Sellors JW, Eder PS, 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(10), 929-936 (2008).
110. Clifford G, Franceschi S, Diaz M, Munoz N, Villa LL. Chapter 3: HPV type-distribution in women with and without cervical neoplastic diseases. Vaccine 24(Suppl. 3), S3/26-34 (2006).
111. Esteller M. Epigenetics in cancer. N. Engl. J. Med. 358(11), 1148-1159 (2008).
112. Lai HC, Lin YW, Huang TH, et al. Identification of novel DNA methylation markers in cervical cancer. Int. J. Cancer 123(1), 161-167 (2008). (Pubitemid 351705204)
113. Sova P, Feng Q, Geiss G, et al. Discovery of novel methylation biomarkers in cervical carcinoma by global demethylation and microarray analysis. Cancer Epidemiol. Biomarkers Prev. 15(1), 114-123 (2006).
114. Wang SS, Smiraglia DJ, Wu YZ, et al. Identification of novel methylation markers in cervical cancer using restriction landmark genomic scanning. Cancer Res. 68(7), 2489-2497 (2008). (Pubitemid 351521825)
115. Wentzensen N, Sherman ME, Schiffman M, Wang SS. Utility of methylation markers in cervical cancer early detection: appraisal of the state-of-the-science. Gynecol. Oncol. 112(2), 293-299 (2009).
116. de Wilde J, Kooter JM, Overmeer RM, et al. hTERT promoter activity and CpG methylation in HPV-induced carcinogenesis. BMC Cancer 10, 271 (2010).
117. Flatley JE, McNeir K, Balasubramani L, et al. Folate status and aberrant DNA methylation are associated with HPV infection and cervical pathogenesis. Cancer Epidemiol. Biomarkers Prev. 18(10), 2782-2789 (2009).
118. Neyaz MK, Kumar RS, Hussain S, et al. Effect of aberrant promoter methylation of FHIT and RASSF1A genes on susceptibility to cervical cancer in a North Indian population. Biomarkers 13(6), 597-606 (2008).
119. Overmeer RM, Henken FE, Bierkens M, et al. Repression of MAL tumour suppressor activity by promoter methylation during cervical carcinogenesis. J. Pathol. 219(3), 327-336 (2009).
120. Yang N, Nijhuis ER, Volders HH, et al. Gene promoter methylation patterns throughout the process of cervical carcinogenesis. Cell Oncol. 32(1-2), 131-143 (2010).
121. Brandsma JL, Sun Y, Lizardi PM, et al. Distinct human papillomavirus type 16 methylomes in cervical cells at different stages of premalignancy. Virology 389(1-2), 100-107 (2009).
122. Hublarova P, Hrstka R, Rotterova P, et al. Prediction of human papillomavirus 16 e6 gene expression and cervical intraepithelial neoplasia progression by methylation status. Int. J. Gynecol. Cancer 19(3), 321-325 (2009).
123. Kalantari M, Calleja-Macias IE, Tewari D, et al. Conserved methylation patterns of human papillomavirus type 16 DNA in asymptomatic infection and cervical neoplasia. J. Virol. 78(23), 12762-12772 (2004). (Pubitemid 39507784)
124. Turan T, Kalantari M, Calleja-Macias IE, et al. Methylation of the human papillomavirus-18 L1 gene: a biomarker of neoplastic progression? Virology 349(1), 175-183 (2006).
125. Kalantari M, Chase DM, Tewari KS, Bernard HU. Recombination of human papillomavirus-16 and host DNA in exfoliated cervical cells: a pilot study of L1 gene methylation and chromosomal integration as biomarkers of carcinogenic progression. J. Med. Virol. 82(2), 311-320 (2010).
126. Hidalgo A, Schewe C, Petersen S, et al. Human papilloma virus status and chromosomal imbalances in primary cervical carcinomas and tumour cell lines. Eur. J. Cancer 36(4), 542-548 (2000). (Pubitemid 30136236)
127. Umayahara K, Numa F, Suehiro Y, et al. Comparative genomic hybridization detects genetic alterations during early stages of cervical cancer progression. Genes Chromosomes Cancer 33(1), 98-102 (2002).
128. Yang YC, Shyong WY, Chang MS, et al. Frequent gain of copy number on the long arm of chromosome 3 in human cervical adenocarcinoma. Cancer Genet. Cytogenet. 131(1), 48-53 (2001).
129. Jiang J, Wei LH, Li YL, et al. Detection of TERC amplification in cervical epithelial cells for the diagnosis of high-grade cervical lesions and invasive cancer: a multicenter study in China. J. Mol. Diagn. 12(6), 808-817 (2010).
130. Heselmeyer-Haddad K, Sommerfeld K, White NM, et al. Genomic amplification of the human telomerase gene (TERC) in pap smears predicts the development of cervical cancer. Am. J. Pathol. 166(4), 1229-1238 (2005). (Pubitemid 40524445)
131. Jalali GR, Herzog TJ, Dziura B, Walat R, Kilpatrick MW. Amplification of the chromosome 3q26 region shows high negative predictive value for nonmalignant transformation of LSIL cytologic finding. Am. J. Obstet. Gynecol. 202(6), 581 E581-E585 (2010).
132. Fitzpatrick MA, Funk MC, Gius D, et al. Identification of chromosomal alterations important in the development of cervical intraepithelial neoplasia and invasive carcinoma using alignment of DNA microarray data. Gynecol. Oncol. 103(2), 458-462 (2006). (Pubitemid 44602151)
133. Cortez MA, Ivan C, Zhou P, Wu X, Ivan M, Calin GA. microRNAs in cancer: from bench to bedside. Adv. Cancer Res. 108, 113-157 (2010).
134. Lee JW, Choi CH, Choi JJ, et al. Altered MicroRNA expression in cervical carcinomas. Clin. Cancer Res. 14(9), 2535-2542 (2008).
135. Lui WO, Pourmand N, Patterson BK, Fire A. Patterns of known and novel small RNAs in human cervical cancer. Cancer Res. 67(13), 6031-6043 (2007). (Pubitemid 47037482)
136. Martinez I, Gardiner AS, Board KF, Monzon FA, Edwards RP, Khan SA. Human papillomavirus type 16 reduces the expression of microRNA-218 in cervical carcinoma cells. Oncogene 27(18), 2575-2582 (2008). (Pubitemid 351550884)
137. Li B, Hu Y, Ye F, Li Y, Lv W, Xie X. Reduced miR-34a expression in normal cervical tissues and cervical lesions with high-risk human papillomavirus infection. Int. J. Gynecol. Cancer 20(4), 597-604 (2010).
138. Li Y, Liu J, Yuan C, Cui B, Zou X, Qiao Y. High-risk human papillomavirus reduces the expression of microRNA-218 in women with cervical intraepithelial neoplasia. J. Int. Med. Res. 38(5), 1730-1736 (2010).
139. Liu C, Pan C, Shen J, Wang H, Yong L, Zhang R. Discrimination analysis of mass spectrometry proteomics for cervical cancer detection. Med. Oncol. 20(4), 597-604 (2010).
140. Panicker G, Ye Y, Wang D, Unger ER. Characterization of the human cervical mucous proteome. Clin. Proteomics 6(1-2), 18-28 (2010).
141. Zegels G, Van Raemdonck GA, Coen EP, Tjalma WA, Van Ostade XW. Comprehensive proteomic analysis of human cervical-vaginal fluid using colposcopy samples. Proteome Sci. 7, 17 (2009).
142. Lai HC, Lin YW, Huang RL, et al. Quantitative DNA methylation analysis detects cervical intraepithelial neoplasms type 3 and worse. Cancer 116(18), 4266-4274 (2010).
143. Huang TH, Lai HC, Liu HW, et al. Quantitative analysis of methylation status of the PAX1 gene for detection of cervical cancer. Int. J. Gynecol. Cancer 20(4), 513-519 (2010).
144. Kim JH, Choi YD, Lee JS, Lee JH, Nam JH, Choi C. Assessment of DNA methylation for the detection of cervical neoplasia in liquid-based cytology specimens. Gynecol. Oncol. 116(1), 99-104 (2010).
145. Apostolidou S, Hadwin R, Burnell M, et al. DNA methylation analysis in liquid-based cytology for cervical cancer screening. Int. J. Cancer 125(12), 2995-3002 (2009).
146. Yang N, Eijsink JJ, Lendvai A, et al. Methylation markers for CCNA1 and C13ORF18 are strongly associated with high-grade cervical intraepithelial neoplasia and cervical cancer in cervical scrapings. Cancer Epidemiol. Biomarkers Prev. 18(11), 3000-3007 (2009).
147. Overmeer RM, Louwers JA, Meijer CJ, et al. Combined CADM1 and MAL promoter methylation analysis to detect (pre-) malignant cervical lesions in high-risk HPV-positive women. Int. J. Cancer doi: 10.1002/ijc.25890 (2010) (Epub ahead of print).
148. Hesselink AT, Heideman DA, Steenbergen RD, 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(8), 2459-2465 (2011).
149. Feng Q, Balasubramanian A, Hawes SE, et al. Detection of hypermethylated genes in women with and without cervical neoplasia. J. Natl. Cancer Inst. 97(4), 273-282 (2005). (Pubitemid 40310275)