Human papillomavirus testing and molecular markers of cervical dysplasia and carcinoma

Cancer

Volumn 111, Issue 1, 2007, Pages 1-14

  Dehn, Donna ^a   Torkko, Kathleen C ^a   Shroyer, Kenneth R ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

Cervix; CIN; Cytology; Dysplasia; HPV; p16INK4a

Indexed keywords

MESSENGER RNA; PROTEIN P16INK4A; TRANSFER RNA; VIRUS ANTIGEN; VIRUS DNA;

CANCER RISK; CANCER SCREENING; CLINICAL LABORATORY; COLPOSCOPY; DIAGNOSTIC ACCURACY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GOLD STANDARD; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; INTERMETHOD COMPARISON; LABORATORY TEST; MAJOR CLINICAL STUDY; MEDICAL TECHNOLOGY; NONHUMAN; PAPANICOLAOU TEST; POLYMERASE CHAIN REACTION; PREDICTION; PREVALENCE; PRIORITY JOURNAL; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; REVIEW; RNA PROBE; SCREENING TEST; UTERINE CERVIX BIOPSY; UTERINE CERVIX CARCINOMA; UTERINE CERVIX CYTOLOGY; UTERINE CERVIX DYSPLASIA; VIRUS DIAGNOSIS; VIRUS INFECTION; WART VIRUS;

ALPHAPAPILLOMAVIRUS; CYCLIN-DEPENDENT KINASE INHIBITOR P16; DNA, VIRAL; FEMALE; HUMANS; PAPILLOMAVIRUS INFECTIONS; SENSITIVITY AND SPECIFICITY; TUMOR MARKERS, BIOLOGICAL; UTERINE CERVICAL DYSPLASIA; UTERINE CERVICAL NEOPLASMS;

EID: 33847149582     PISSN: 0008543X     EISSN: 10970142     Source Type: Journal    
DOI: 10.1002/cncr.22425     Document Type: Review

References (142)

1. World Health Organization. Comprehensive cervical cancer control: a guide to essential practice. Geneva, Switzerland: WHO; 2006.
2. Jemal A, Siegel R, Ward E, et al. Cancer statistics, 2006. CA Cancer J Clin. 2006;56:106-130.
3. Schiffman M, Solomon D. Findings to date from the ASCUS-LSIL Triage Study (ALTS). Arch Pathol Lab Med. 2003;127:946-949.
4. DeFrancesco MA, Gargiulo F, Schreiber C, Ciravolo G, Salinaro F, Manca N. Detection and genotyping of human papillomavirus in cervical samples from Italian patients. J Med Virol. 2005;75:588-592.
5. Cates W Jr. Estimates of the incidence and prevalence of sexually transmitted diseases in the United States. American Social Health Association Panel. Sex Transm Dis. 1999;26:S2-S7.
6. Burk RD, Ho GY, Beardsley L, Lempa M, Peters M, Bierman R. Sexual behavior and partner characteristics are the predominant risk factors for genital human papillomavirus infection in young women. J Infect Dis. 1996;174:679-689.
7. Bauer HM, Ting Y, Greer CE, et al. Genital human papillomavirus infection in female university students as determined by a PCR-based method. JAMA. 1991;265:472-477.
8. Meijer CJ, Heimerhorst TJ, Rozendaal L, van der Linden JC, Voorhorst FJ, Walboomers JM. HPV typing and testing in gynaecological pathology: has the time come? Histopathology. 1998;33:83-86.
9. Plummer M, Herrero R, Franceschi S, et al. Smoking and cervical cancer: pooled analysis of the IARC multi-centric case-control study. Cancer Causes Control. 2003;14:805-814.
10. McIntyre-Seltman K, Castle PE, Guido R, Schiffman M, Wheeler CM, and the ALTS Group. Smoking is a risk factor for cervical intraepithelial neoplasia grade 3 among oncogenic human papillomavirus DNA-positive women with equivocal or mildly abnormal cytology. Cancer Epidemiol Biomarkers Prev. 2005;14:1165-1170.
11. Moreno V, Bosch FX, Munoz N, et al, and the International Agency for Research on Cancer. Multicentric Cervical Cancer Study Group. Effect of oral contraceptives on risk of cervical cancer in women with human papillomavirus infection: the IARC multicentric case-control study. Lancet. 2002;359:1085-1092.
12. Munoz N, Franceschi S, Bosetti C, et al, and the International Agency for Research on Cancer. Multicentric Cervical Cancer Study Group. Role of parity and human papillomavirus in cervical cancer: the IARC multicentric case-control study. Lancet. 2002;359:1093-1101.
13. Castellsague X, Diaz M, de Sanjose S, et al, and the International Agency for Research on Cancer Multicenter Cervical Cancer Study Group. Worldwide human papillomavirus etiology of cervical adenocarcinoma and its cofactors: implications for screening and prevention. J Natl Cancer Inst. 2006;98:303-315.
14. Hildesheim A, Mann V, Brinton LA, Szklo M, Reeves WC, Rawls WE. Herpes simplex virus type 2: a possible interaction with human papillomavirus types 16/18 in the development of invasive cervical cancer. Int J Cancer. 1991;49:335-340.
15. Wolf JK, Ramirez PT. The molecular biology of cervical cancer. Cancer Invest. 2001;19:621-629.
16. zur Hausen H. Papillomaviruses in human cancers. Proc Assoc Am Physicians. 1999;111:581-587.
17. Stoler M. Human papillomavirus biology and cervical neoplasia, implications for diagnostic criteria and testing. Arch Pathol Lab Med. 2003;127:935-939.
18. Doorbar J. The papillomavirus life cycle. J Clin Virol. 2005;32(suppl 1):S7-15
19. Andersson S, Hansson B, Norman I, et al. Expression of E6/ E7 mRNA from 'high risk' human papillomavirus in relation to CIN grade, viral load and p16INK4a. Int J Oncol. 2006;29:705-711.
20. Scheurer ME, Tortolero-Luna G, Adler-Storthz K. Human papillomavirus infection: biology, epidemiology, and prevention. Int J Gynecol Cancer. 2005;15:727-746.
21. zur Hausen H. Papillomavirus infections-a major cause of human cancers. Biochim Biophys Acta. 1996;1288:F55-F78.
22. Martin CM, Astbury K, O'Leary JJ. Molecular profiling of cervical neoplasia. Expert Rev Mol Diagn. 2006;6:217-229.
23. Zhang HS, Postigo AA, Dean DC. Active transcriptional repression by the Rb-E2F complex mediates G1 arrest triggered by p16INK4a, TGFbeta, and contact inhibition. Cell. 1999;97:53-61.
24. Dyson N, Howley PM, Munger K, Harlow E. The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science. 1989;243:934-937.
25. Kobelin MH, Kobelin CG, Burke L, Lavin P, Niloff JM, Kim YB. Incidence and predictors of cervical dysplasia in patients with minimally abnormal Papanicolaou smears. Obstet Gynecol. 1998;92:356-359.
26. Crum CP, Genest DR, Krane JF, et al. Subclassifying atypical squamous cells in ThinPrep cervical cytology correlates with detection of high-risk human papillomavirus DNA. Am J Clin Pathol. 1999;112:384-390.
27. Schoolland M, Sterrett GF, Knowles SA, Mitchell KM, Kurinczuk JJ. The "Inconclusive-possible high grade epithelial abnormality" category in Papanicolaou smear reporting. Cancer. 1998;84:208-217.
28. Malik SN, Wilkinson EJ, Drew PA, Bennett BB, Hardt NS. Do qualifiers of ASCUS distinguish between low- and high-risk patients? Acta Cytol. 1999;43:376-380.
29. Chhieng DC, Elgert P, Cangiarella JF, Cohen JM. Variation in the incidence of AGUS between different patient populations. Acta Cytol. 2001;45:287-293.
30. Wright TC Jr, Cox JT, Massad LS, Twiggs LB, Wilkinson EJ, and the ASCCP-Sponsored Consensus Conference. 2001 Consensus Guidelines for the management of women with cervical cytological abnormalities. JAMA. 2002;287:2120-2129.
31. ASCUS-LSIL Triage Study (ALTS) Group. A randomized trial on the management of low-grade squamous intraepithelial lesion cytology interpretations [published comment appears in Am J Obstet Gynecol. 2003;188:1381-1382]. Am J Obstet Gynecol. 2003;188:1393-1400.
32. Levine L, Lucci JA III, Dinh TV. Atypical glandular cells: new Bethesda Terminology and Management Guidelines. Obstet Gynecol Surv 2003;58:399-406.
33. Gage JC, Hanson VW, Abbey K, et al, and the ASCUS LSIL Triage Study (ALTS) Group. Number of cervical biopsies and sensitivity of colposcopy [published comment appears in Obstet Gynecol. 2006;108:246-247]. Obstet Gynecol. 2006;108:264-272.
34. Titus K. Making a valid point about HPV tests. CAP Today. 2005;19.
35. Naryshkin S. The false-negative fraction for Papanicolaou smears: how often are "abnormal" smears not detected by a "standard" screening cytologist? Arch Pathol Lab Med. 1997;121:270-272.
36. Krieger P, Naryshkin S. Random rescreening of cytologic smears: a practical and effective component of quality assurance programs in both large and small cytology laboratories. Acta Cytol. 1994;38:291-298.
37. Tabbara SO, Sidawy MK. Evaluation of the 5-year review of negative cervical smears in patients with high grade squamous intraepithelial lesions. Diagn Cytopathol. 1996;15:7-10.
38. Guo M, Hu L, Martin L, Liu S, Baliga M, Hughson MD. Accuracy of liquid-based Pap tests: comparison of concurrent liquid-based tests and cervical biopsies on 782 women with previously abnormal Pap smears. Acta Cytol. 2005;49:132-138.
39. DeMay RM. The Pap Smear. In: The art and science of cytopathology. Exfoliative cytology. Chicago: ASCP Press; 1996;61-205.
40. DeMay RM. Cytopathology of false negatives preceding cervical carcinoma. Am J Obstet Gynecol. 1996;175:1110-1113.
41. Benoit AG, Krepart GV, Lotocki RJ. Results of prior cytologic screening in patients with a diagnosis of Stage I carcinoma of the cervix. Am J Obstet Gynecol. 1984;148:690-694.
42. Berkeley AS, LiVolsi VA, Schwartz PE. Advanced squamous cell carcinoma of the cervix with recent normal Papanicolaou tests. Lancet. 1980;2:375-376.
43. Gay JD, Donaldson LD, Goellner JR. False-negative results in cervical cytologic studies. Acta Cytol. 1985;29:1043-1046.
44. Pairwuti S. False-negative Papanicolaou smears from women with cancerous and precancerous lesions of the uterine cervix. Acta Cytol. 1991;35:40-46.
45. Robertson JH, Woodend B. Negative cytology preceding cervical cancer: causes and prevention. J Clin Pathol. 1993;46:700-702.
46. van der Graaf Y, Vooijs GP, Gaillard HL, Go DM. Screening errors in cervical cytologic screening. Acta Cytol. 1987;31:434-438.
47. van der Graaf Y, Vooijs GE False-negative rate in cervical cytology. J Clin Pathol. 1987;40:438-442.
48. Lee KR, Minter LJ, Granter SR. Papanicolaou smear sensitivity for adenocarcinoma in situ of the cervix. A study of 34 cases. Am J Clin Pathol. 1997;107:30-35.
49. Krane JF, Granter SR, Trask CE, Hogan CL, Lee KR. Papanicolaou smear sensitivity for the detection of adenocarcinoma of the cervix: a study of 49 cases. Cancer. 2001;93:8-15.
50. Stoler MH. Testing for human papillomavirus: data driven implications for cervical neoplasia management. Clin Lab Med. 2003;23:569-583.
51. Cox JT. Human papillomavirus testing in primary cervical screening and abnormal Papanicolaou management. Obstet Gynecol Surv. 2006;61:S15-S25.
52. Carozzi FM, Del Mistro A, Confortini M, et al. Reproducibility of HPV DNA testing by Hybrid Capture 2 in a screening setting. Am J Clin Pathol. 2005;124:716-721.
53. Tarkowski TA, Rajeevan MS, Lee DR, Unger ER. Improved detection of viral RNA isolated from liquid-based cytology samples. Mol Diagn. 2001;6:125-130.
54. Castle PE, Solomon D, Hildesheim A, et al. Stability of archived liquid-based cervical cytologic specimens. Cancer. 2003;99:89-96.
55. Hopman AH, Kamps MA, Smedts F, Speel EJ, Herrington CS, Ramaekers FC. HPV in situ hybridization: impact of different protocols on the detection of integrated HPV. Int J Cancer. 2005;115:419-428.
56. Hacker GW, Su H, Hauser-Kronberger C, Hainfeld JF, Tubbs R. Sensitive in situ hybridization with catalyzed reporter deposition, streptavidin-Nanogold, and silver acetate autometallography: detection of single-copy human papillomavirus [published comment appears in Am J Pathol. 1997;151:1172-1173]. Am J Pathol. 1997;150:1553-1561.
57. Davies P, Kornegay J, Iftner T. Current methods of testing for human papillomavirus. Best Pract Res Clin Obstet Cynaecol. 2001;15:677-700.
58. Peyton CL, Schiffman M, Lorincz AT, et al. Comparison of PCR- and hybrid capture-based human papillomavirus detection systems using multiple cervical specimen collection strategies [published correction appears in J Clin Microbiol. 1999;37:478]. J Clin Microbiol. 1998;36:3248-3254.
59. Schiffman M, Wheeler CM, Dasgupta A, Solomon D, Castle PE, and The ALTS Group. A comparison of a prototype PCR assay and Hybrid Capture 2 for detection of carcinogenic human papillomavirus DNA in women with equivocal or mildly abnormal Papanicolaou smears. Am J Clin Pathol. 2005;124:722-732.
60. Ronco G, Segnan N, Giorgi-Rossi P, et al, and the New Technologies for Cervical Cancer Working Group. Human papillomavirus testing and liquid-based cytology: results at recruitment from the new technologies for cervical cancer randomized controlled trial. J Natl Cancer Inst. 2006;98:765-774.
61. Malloy C, Sherris J, Herdman C. HPV DNA testing: technical and programmatic issues for cervical cancer prevention in low-resource settings. Seattle: PATH; 2000.
62. van Doorn LJ, Kleter B, Quint WG. Molecular detection and genotyping of human papillomavirus. Expert Rev Mol Diagn. 2001;1:394-402.
63. Gravitt PE, Peyton CL, Alessi TQ, et al. Improved amplification of genital human papillomaviruses. J Clin Microbiol. 2000;38:357-361.
64. van Doom LJ, Quint W, Kleter B, et al. Genotyping of human papillomavirus in liquid cytology cervical specimens by the PGMY line blot assay and the SPF(10) line probe assay. J Clin Microbiol. 2002;40:979-983.
65. Morris BJ. Cervical human papillomavirus screening by PCR: advantages of targeting the E6/E7 region. Clin Chem Lab Med. 2005;43:1171-1177.
66. Brink AA, Snijders PJ, Meijer CJ, Berkhof J, Verheijen RH. HPV testing in cervical screening. Best Pract Res Clin Obstet Gynaecol. 2006;20:253-266.
67. Fujii T, Masumoto N, Saito M, et al. Comparison between in situ hybridization and real-time PCR technique as a means of detecting the integrated form of human papillomavirus 16 in cervical neoplasia. Diagn Mol Pathol. 2005;14:103-108.
68. Gheit T, Landi S, Gemignani F, et al. Development of a sensitive and specific assay combining multiplex PCR and DNA microarray primer extension to detect high-risk mucosal human papillomavirus types. J Clin Microbiol. 2006;44:2025-2031.
69. Kleter B, van Doom LJ, ter Schegget J, et al. Novel short-fragment PCR assay for highly sensitive broad-spectrum detection of anogenital human papillomaviruses [published comment appears in Am J Pathol. 1998;153:1667-1671]. Am J Pathol. 1998;153:1731-1739.
70. Gravitt PE, Peyton CL, Apple RJ, Wheeler CM. Genotyping of 27 human papillomavirus types by using L1 consensus PCR products by a single-hybridization, reverse line blot detection method. J Clin Microbiol. 1998;36:3020-3027.
71. Coutlee F, Gravitt P, Kornegay J, et al. Use of PGMY primers in L1 consensus PCR improves detection of human papillomavirus DNA in genital samples. J Clin Microbiol. 2002;40:902-907.
72. Melchers WJ, Bakkers JM, Wang J, et al. Short fragment polymerase chain reaction reverse hybridization line probe assay to detect and genotype a broad spectrum of human papillomavirus types. Clinical evaluation and follow-up. Am J Pathol. 1999;155:1473-1478.
73. Kleter B, van Doom LJ, Schrauwen L, et al. Development and clinical evaluation of a highly sensitive PCR-reverse hybridization line probe assay for detection and identification of anogenital human papillomavirus. J Clin Microbiol. 1999;37:2508-2517.
74. Gillio-Tos A, De Marco L, Ghisetti V, et al. Human papillomavirus typing with GP5+/6+ polymerase chain reaction reverse line blotting and with commercial type-specific PCR kits. J Clin Virol. 2006;36:126-132.
75. Monsonego J, Bohbot JM, Pollini G, et al. Performance of the Roche AMPLICOR human papillomavirus (HPV) test in prediction of cervical intraepithelial neoplasia (CIN) in women with abnormal PAP smear. Gynecol Oncol. 2005;99:160-168.
76. Sandri MT, Lentati P, Benini E, et al. Comparison of the Digene HC2 Assay and the Roche AMPLICOR human papillomavirus (HPV) test for detection of high-risk HPV genotypes in cervical samples. J Clin Microbiol 2006;44:2141-2146.
77. van Ham MA, Bakkers JM, Harbers GK, Quint WG, Massuger LF, Melchers WJ. Comparison of two commercial assays for detection of human papillomavirus (HPV) in cervical scrape specimens: validation of the Roche AMPLICOR HPV test as a means to screen for HPV genotypes associated with a higher risk of cervical disorders. J Clin Microbiol. 2005;43:2662-2667.
78. Klaassen CH, Prinsen CF, de Valk HA, Horrevorts AM, Jeunink MA, Thunnissen FB. DNA microarray format for detection and subtyping of human papillomavirus. J Clin Microbiol. 2004;42:2152-2160.
79. Oh TJ, Kim CJ, Woo SK, et al. Development and clinical evaluation of a highly sensitive DNA microarray for detection and genotyping of human papillomaviruses. J Clin Microbiol. 2004;42:3272-3280.
80. Kim CJ, Jeong JK, Park M, et al. HPV oligonucleotide microarray-based detection of HPV genotypes in cervical neoplastic lesions. Gynecol Oncol. 2003;89:210-217.
81. Choi YD, Jung WW, Nam JH, Choi HS, Park CS. Detection of HPV genotypes in cervical lesions by the HPV DNA Chip and sequencing. Gynecol Oncol. 2005;98:369-375.
82. Kim KH, Yoon MS, Na YJ, Park CS, Oh MR, Moon WC. Development and evaluation of a highly sensitive human papillomavirus genotyping DNA chip. Gynecol Oncol. 2006;100:38-43.
83. Chen S, Tabrizi SN, Fairley CK, Borg AJ, Garland SM. Simultaneous detection and typing strategy for human papillomaviruses based on PCR and restriction endonuclease mapping. Biotechniques. 1994;17:138-40,142-143.
84. Lungu O, Wright TC Jr, Silverstein S. Typing of human papillomaviruses by polymerase chain reaction amplification with L1 consensus primers and RFLP analysis. Mol Cell Probes. 1992;6:145-152.
85. Arens M. Clinically relevant sequence-based genotyping of HBV, HCV, CMV, and HIV. J Clin Virol. 2001;22:11-29.
86. Dunbar SA, Vander Zee CA, Oliver KG, Karem KL, Jacobson JW. Quantitative, multiplexed detection of bacterial pathogens: DNA and protein applications of the Luminex Lab-MAP system. J Microbiol Methods. 2003;53:245-252.
87. Jiang HL, Zhu HH, Zhou LF, Chen F, Chen Z. Genotyping of human papillomavirus in cervical lesions by Ll consensus PCR and the Luminex xMAP system. J Med Microbiol. 2006;55(pt 6):715-720.
88. Schmitt M, Bravo IG, Snijders PJ, Gissmann L, Pawlita M, Waterboer T. Bead-based multiplex genotyping of human papillomaviruses. J Clin Microbiol. 2006;44:504-512.
89. Germer JJ, Majewski DW, Yung B, Mitchell PS, Yao JD. Evaluation of the invader assay for genotyping hepatitis C virus. J Clin Microbiol. 2006;44:318-323.
90. Thyagarajan B, Anderson KE, Kong F, Selk FR, Lynch CF, Gross MD. New approaches for genotyping paraffin wax embedded breast tissue from patients with cancer: the Iowa women's health study. J Clin Pathol. 2005;58:955-961.
91. Hjertner B, Meehan B, McKillen J, McNeilly F, Belak S. Adaptation of an Invader assay for the detection of African swine fever virus DNA. J Virol Methods. 2005;124:1-10.
92. Snijders PJ, van den Brule AJ, Meijer CJ. The clinical relevance of human papillomavirus testing: relationship between analytical and clinical sensitivity. J Pathol. 2003;201:1-6.
93. Gravitt PE, Peyton C, Wheeler C, Apple R, Higuchi R, Shah KV. Reproducibility of HPV 16 and HPV 18 viral load quantitation using TaqMan real-time PCR assays. J Virol Methods. 2003;112:23-33.
94. Carcopino X, Henry M, Benmoura D, et al. Determination of HPV type 16 and 18 viral load in cervical smears of women referred to colposcopy. J Med Virol 2006;78:1131-1140.
95. Gravitt PE, Burk RD, Lorincz A, et al. A comparison between real-time polymerase chain reaction and Hybrid Capture 2 for human papillomavirus DNA quantitation. Cancer Epidemiol Biomarkers Prev. 2003;12:477-484.
96. Hudson JB, Bedell MA, McCance DJ, Laiminis LA. Immortalization and altered differentiation of human keratinocytes in vitro by the E6 and E7 open reading frames of human papillomavirus type 18. J Virol. 1990;64:519-526.
97. Molden T, Kraus I, Karlsen F, Skomedal H, Hagmar B. Human papillomavirus E6/E7 mRNA expression in women younger than 30 years of age. Gynecol Oncol. 2006;100:95-100.
98. Lie AK, Risberg B, Borge B, et al. DNA- versus RNA-based methods for human papillomavirus detection in cervical neoplasia. Gynecol Oncol. 2005;97:908-915.
99. Molden T, Nygard JF, Kraus I, et al. Predicting CIN2+ when detecting HPV mRNA and DNA by PreTect HPV-proofer and consensus PCR: a 2-year follow-up of women with ASCUS or LSIL Pap smear. Int J Cancer. 2005;114:973-976.
100. Schachter J, Chernesky MA, Willis DE, et al. Vaginal swabs are the specimens of choice when screening for Chlamydia trachomatis and Neisseria gonorrhoeae: results from a multicenter evaluation of the APTIMA assays for both infections. Sex Transm Dis. 2005;32:725-728.
101. Chernesky MA, Jang DE. APTIMA transcription-mediated amplification assays for Chlamydia trachomatis and Neisseria gonorrhoeae. Expert Rev Mol Diagn. 2006;6:519-525.
102. Santin AD, Zhan F, Bignotti E, et al. Gene expression profiles of primary HPV16- and HPV18-infected early stage cervical cancers and normal cervical epithelium: identification of novel candidate molecular markers for cervical cancer diagnosis and therapy. Virology. 2005;331:269-291.
103. Jarboe EA, Liaw KL, Thompson LC, et al. Analysis of telomerase as a diagnostic biomarker of cervical dysplasia and carcinoma. Oncogene. 2002;21:664-673.
104. Jarboe EA, Thompson LC, Heinz D, McGregor JA, Shroyer KR. Telomerase and human papillomavirus as diagnostic adjuncts for cervical dysplasia and carcinoma. Hum Pathol. 2004;35:396-402.
105. Sherr CJ. Cancer cell cycles. Science. 1996;274:1672-1677.
106. Kamb A, Gruis NA, Weaver-Feldhaus J, et al. A cell cycle regulator potentially involved in genesis of many tumor types. Science. 1994;264:436-440.
107. Khleif SN, DeGregori J, Yee CL, 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 U S A. 1996;93:4350-1354.
108. Jones DL, Munger K. Interactions of the human papillomavirus E7 protein with cell cycle regulators. Semin Cancer Biol. 1996;7:327-337.
109. Keating JT, Cviko A, Riethdorf S, et al. Ki-67, cyclin E, and p16INK4 are complementary surrogate biomarkers for human papilloma virus-related cervical neoplasia. Am J Surg Pathol. 2001;25:884-891.
110. 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. 2001;92:276-284.
111. Klaes R, Benner A, Friedrich T, et al. p16INK4a immunohistochemistry improves interobserver agreement in the diagnosis of cervical intraepithelial neoplasia [published comment appears in Am J Surg Pathol. 2003;27:1284; author reply 1284]. Am J Surg Pathol. 2002;26:1389-1399.
112. Murphy N, Ring M, Killalea AG, et al. p16INK4A as a marker for cervical dyskaryosis: CIN and cGIN in cervical biopsies and ThinPrep smears. J Clin Pathol. 2003;56:56-63.
113. Cameron RI, Maxwell P, Jenkins D, McCluggage WG. Immunohistochemical staining with MIB1, bcl2 and p16 assists in the distinction of cervical glandular intraepithelial neoplasia from tubo-endometrial metaplasia, endometriosis and microglandular hyperplasia. Histopathology. 2002;41:313-321.
114. Negri G, Egarter-Vigl E, Kasal A, Romano F, Haitel A, Mian C. p16INK4a is a useful marker for the diagnosis of adenocarcinoma of the cervix uteri and its precursors: an immunohistochemical study with immunocytochemical correlations. Am J Surg Pathol. 2003;27:187-193.
115. Yoshida T, Fukuda T, Sano T, Kanuma T, Owada N, Nakajima T. 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. 2004;102:100-108.
116. Ekalaksananan T, Pientong C, Sriamporn S, et al. Usefulness of combining testing for p16 protein and human papillomavirus (HPV) in cervical carcinoma screening. Gynecol Oncol. 2006;103:62-66.
117. Nieh S, Chen SF, Chu TY, 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. 2005;97:35-40.
118. Guo M, Hu L, Baliga M, He Z, Hughson MD. The predictive value of p16INK4a and Hybrid Capture 2 human papillomavirus testing for high-grade cervical intraepithelial neoplasia. Am J Clin Pathol 2004;122:894-901.
119. Wang SS, Trunk M, Schiffman M et al. Validation of p16INK4a as a marker of oncogenic human papillomavirus infection in cervical biopsies from a population-based cohort in Costa Rica. Cancer Epidemiol Biomarkers Prev 2004;13:1355-1360.
120. Malinowski DP. Molecular diagnostic assays for cervical neoplasia: emerging markers for the detection of high-grade cervical disease. Biotechniques. 2005;(suppl):17-23.
121. Shroyer KR, Homer P, Heinz D, Singh M. Validation of a novel immunocytochemical assay for topoisomerase II-alpha and minichromosome maintenance protein 2 expression in cervical cytology. Cancer Cytopathol. 2006;108:324-330.
122. Kjaer SK, Chackerian B, van den Brule AJ, et al. High-risk human papillomavirus is sexually transmitted: evidence from a follow-up study of virgins starting sexual activity (intercourse). Cancer Epidemiol Biomarkers Prev. 2001;10:101-106.
123. Winer RL, Lee SK, Hughes JP, Adam DE, Kiviat NB, Koutsky LA. Genital human papillomavirus infection: incidence and risk factors in a cohort of female university students [published correction appears in Am J Epidemiol. 2003;157:858]. Am J Epidemiol. 2003;157:218-226.
124. Fairley CK, Gay NJ, Forbes A, Abramson M, Garland SM. Hand-genital transmission of genital warts? An analysis of prevalence data. Epidemiol Infect. 1995;115:169-176.
125. Herrero R, Castellsague X, Pawlita M, et al. Human papillomavirus and oral cancer: the International Agency for Research on Cancer multicenter study. J Natl Cancer Inst. 2003;95:1772-1783.
126. Bosch FX, Lorincz A, Munoz N, Meijer CJ, Shah KV. The causal relation between human papillomavirus and cervical cancer [published comment appears in J Clin Pathol. 2002;55:241-242]. J Clin Pathol. 2002;55:244-265.
127. Durst M, Gissmann L, Ikenberg H, zur Hausen H. A papillomavirus DNA from a cervical carcinoma and its prevalence in cancer biopsy samples from different geographic regions. Proc Natl Acad Sci U S A. 1983;80:3812-3815.
128. Boshart M, Gissmann L, Ikenberg H, Kleinheinz A, Scheurlen W, zur Hausen H. A new type of papillomavirus DNA, its presence in genital cancer biopsies and in cell lines derived from cervical cancer. EMBO J. 1984;3:1151-1157.
129. Magnusson PK, Lichtenstein P, Gyllensten UB. Heritability of cervical tumours. Int J Cancer. 2000;88:698-701.
130. Ginocchio CC. Assays for the detection of human papillomavirus. Pan American Society for Clinical Virology Newsletter. March 2004;31(1):1-3. Published online at: http:// www.virology.org/newsletters/2004march.pdf
131. Qureshi MN, Rudelli RD, Tubbs RR, Biscotti CV, Layfield LJ. Role of HPV DNA testing in predicting cervical intraepithelial lesions: comparison of HC HPV and ISH HPV Diagn Cytopathol 2003;29:149-155.
132. Jin XW, Brainard J, Nielsen C, Yen-Lieberman B. New advances transform the management of women with abnormal pap tests. Pan American Society for Clinical Virology Newsletter. March 2004;31(1):4-5. Published online at: http:// www.virology.org/newsletters/2004march.pdf
133. Molden T, Kraus I, Karlsen F, Skomedal H, Nygard JF, Hagmar B. Comparison of human papillomavirus messenger RNA and DNA detection: A cross-sectional study of 4,136 women >30 years of age with a 2-year follow-up of high-grade squamous intraepithelial lesion. Cancer Epidemiol Biomarkers Prev. 2005;14:367-372.
134. Schorge JO, Lea JS, Elias KJ, et al. P16 as a molecular biomarker of cervical adenocarcinoma. Am J Obstet Gynecol. 2004;190:668-673.
135. Saqi A, Pasha TL, McGrath CM, Yu GH, Zhang P, Gupta R Overexpression of p16INK4A in liquid-based specimens (SurePath) as marker of cervical dysplasia and neoplasia. Diagn Cytopathol. 2002;27:365-370.
136. Pientong C, Ekalaksananan T, Swadpanich U, et al. Immunocytochemical detection of p16INK4a protein in scraped cervical cells. Acta Cytol. 2003;47:616-623.
137. Pientong C, Ekalaksananan T, Kongyingyoes B, et al. Immunocytochemical staining of p16INK4a protein from conventional Pap test and its association with human papillomavirus infection. Diagn Cytopathol. 2004;31:235-242.
138. Bose S, Evans H, Lantzy L, Scharre K, Youssef E. p16(INK4A) is a surrogate biomarker for a subset of human papilloma virus-associated dysplasias of the uterine cervix as determined on the Pap smear. Diagn Cytopathol. 2005;32:21-24.
139. Moore GD, Lear SC, Wills-Frank LA, Martin AW, Snyder JW, Helm CW. Differential expression of cdk inhibitors p16, p21cip1, p27kip1, and cyclin E in cervical cytological smears prepared by the ThinPrep method. Diagn Cytopathol. 2005;32:82-87.
140. Nieh S, Chen SF, Chu TY, Lai HC, Fu E. Expression of p16 INK4A in Papanicolaou smears containing atypical squamous cells of undetermined significance from the uterine cervix. Gynecol Oncol. 2003;91:201-208.
141. Wentzensen N, Bergeron C, Cas F, Eschenbach D, Vinokurova S, von Knebel Doeberitz M. Evaluation of a nuclear score for p16INK4a-stained cervical squamous cells in liquid-based cytology samples. Cancer. 2005;105:461-467.
142. Lambert AP, Anschau F, Schmitt VM. p16INK4A expression in cervical premalignant and malignant lesions. Exp Mol Pathol. 2006;80:192-196.