Molecular biomarkers in cervical cancer diagnosis: a critical appraisal

Bibliography

• Cervical cancer. NIH Consens Statement 1996;14:1-38; quiz 4p
   PubMedGoogle Scholar
• Pierce Campbell CM, Menezes LJ, Paskett ED, Giuliano AR. Prevention of invasive cervical cancer in the United States: past, present, and future. Cancer Epidemiol Biomarkers Prev 2012;21:1402-8
   PubMed Web of Science ®Google Scholar
• Ferlay J, Shin HR, Bray F, et al. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 2010;127:2893-917
   PubMed Web of Science ®Google Scholar
• Papanicolaou GN. A new procedure for staining vaginal smears. Science 1942;95:438-9
   PubMedGoogle Scholar
• De Pokomandy A, Franco E. HPV infection and cervical carcinogenesis: epidemiology and prevention. In: Ayhan A, Reed N, Gultekin M, Dursun P, editors. Textbook of gynaecological oncology. Günes Publishing; Ankara, Turkey: 2011. p. 75
   Google Scholar
• 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 2009;302:1757-64
   PubMed Web of Science ®Google Scholar
• Arbyn M, Buntinx F, Van Ranst M, et al. 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 2004;96:280-93
   PubMed Web of Science ®Google Scholar
• Berkhof J, de Bruijne MC, Zielinski GD, et al. Evaluation of cervical screening strategies with adjunct high-risk human papillomavirus testing for women with borderline or mild dyskaryosis. Int J Cancer 2006;118:1759-68
   PubMed Web of Science ®Google Scholar
• 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 2007;370:1764-72
   PubMed Web of Science ®Google Scholar
• Naucler P, Ryd W, Tornberg S, et al. Human papillomavirus and Papanicolaou tests to screen for cervical cancer. N Engl J Med 2007;357:1589-97
   PubMed Web of Science ®Google Scholar
• 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 2008;100:492-501
   PubMed Web of Science ®Google Scholar
• Priebe AM. 2012 cervical cancer screening guidelines and the future role of HPV testing. Clin Obstet Gynecol 2013;56:44-50
   PubMed Web of Science ®Google Scholar
• Berkhof J, Coupe VM, Bogaards JA, et al. The health and economic effects of HPV DNA screening in The Netherlands. Int J Cancer 2010;127:2147-58
   PubMed Web of Science ®Google Scholar
• Dillner J. Primary human papillomavirus testing in organized cervical screening. Curr Opin Obstet Gynecol 2013;25:11-16
   PubMed Web of Science ®Google Scholar
• Pepe MS, Feng Z, Janes H, et al. Pivotal evaluation of the accuracy of a biomarker used for classification or prediction: standards for study design. J Natl Cancer Inst 2008;100:1432-8
   PubMed Web of Science ®Google Scholar
• Walboomers JM, Jacobs MV, Manos MM, et al. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 1999;189:12-19
   PubMed Web of Science ®Google Scholar
• Munoz N. Human papillomavirus and cancer: the epidemiological evidence. J Clin Virol 2000;19:1-5
   PubMed Web of Science ®Google Scholar
• zur Hausen H. Papillomaviruses and cancer: from basic studies to clinical application. Nat Rev Cancer 2002;2:342-50
   PubMed Web of Science ®Google Scholar
• zur Hausen H. Papillomaviruses causing cancer: evasion from host-cell control in early events in carcinogenesis. J Natl Cancer Inst 2000;92:690-8
   PubMed Web of Science ®Google Scholar
• van Muyden RC, ter Harmsel BW, Smedts FM, et al. Detection and typing of human papillomavirus in cervical carcinomas in Russian women: a prognostic study. Cancer 1999;85:2011-16
   PubMed Web of Science ®Google Scholar
• Zielinski GD, Snijders PJ, Rozendaal L, et al. The presence of high-risk HPV combined with specific p53 and p16INK4a expression patterns points to high-risk HPV as the main causative agent for adenocarcinoma in situ and adenocarcinoma of the cervix. J Pathol 2003;201:535-43
   PubMed Web of Science ®Google Scholar
• Bernard HU, Burk RD, Chen Z, et al. Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. Virology 2010;401:70-9
   PubMed Web of Science ®Google Scholar
• Lungu O, Sun XW, Felix J, et al. Relationship of human papillomavirus type to grade of cervical intraepithelial neoplasia. JAMA 1992;267:2493-6
   PubMed Web of Science ®Google Scholar
• Baak JP, Kruse AJ, Robboy SJ, et al. Dynamic behavioural interpretation of cervical intraepithelial neoplasia with molecular biomarkers. J Clin Pathol 2006;59:1017-28
   PubMed Web of Science ®Google Scholar
• Moody CA, Laimins LA. Human papillomavirus oncoproteins: pathways to transformation. Nat Rev Cancer 2010;10:550-60
   PubMed Web of Science ®Google Scholar
• Doorbar J, Quint W, Banks L, et al. The biology and life-cycle of human papillomaviruses. Vaccine 2012;30(Suppl 5):F55-70
   PubMed Web of Science ®Google Scholar
• Wentzensen N, von Knebel Doeberitz M. Biomarkers in cervical cancer screening. Dis Markers 2007;23:315-30
   PubMed Web of Science ®Google Scholar
• Stanley MA. Epithelial cell responses to infection with human papillomavirus. Clin Microbiol Rev 2012;25:215-22
   PubMed Web of Science ®Google Scholar
• Choo KB, Wang TS, Huang CJ. Analysis of relative binding affinity of E7-pRB of human papillomavirus 16 clinical variants using the yeast two-hybrid system. J Med Virol 2000;61:298-302
   PubMed Web of Science ®Google Scholar
• Baker CC, Phelps WC, Lindgren V, et al. Structural and transcriptional analysis of human papillomavirus type 16 sequences in cervical carcinoma cell lines. J Virol 1987;61:962-71
   PubMed Web of Science ®Google Scholar
• Schwarz E, Freese UK, Gissmann L, et al. Structure and transcription of human papillomavirus sequences in cervical carcinoma cells. Nature 1985;314:111-14
   PubMed Web of Science ®Google Scholar
• Vinokurova S, Wentzensen N, Kraus I, et al. Type-dependent integration frequency of human papillomavirus genomes in cervical lesions. Cancer Res 2008;68:307-13
   PubMed Web of Science ®Google Scholar
• Melsheimer P, Vinokurova S, Wentzensen N, et al. DNA aneuploidy and integration of human papillomavirus type 16 e6/e7 oncogenes in intraepithelial neoplasia and invasive squamous cell carcinoma of the cervix uteri. Clin Cancer Res 2004;10:3059-63
   PubMed Web of Science ®Google Scholar
• Hopman AH, Smedts F, Dignef W, et al. Transition of high-grade cervical intraepithelial neoplasia to micro-invasive carcinoma is characterized by integration of HPV 16/18 and numerical chromosome abnormalities. J Pathol 2004;202:23-33
   PubMed Web of Science ®Google Scholar
• Kadaja M, Isok-Paas H, Laos T, et al. Mechanism of genomic instability in cells infected with the high-risk human papillomaviruses. PLoS Pathog 2009;5:e1000397
   PubMedGoogle Scholar
• Mayeaux E Jr, Thomas Cox J. Modern colposcopy textbook and atlas. Lippincott Williams & Wilkins; Philadelphia, Pennsylvania (PA), USA: 2011
   Google Scholar
• Pett MR, Alazawi WO, Roberts I, et al. Acquisition of high-level chromosomal instability is associated with integration of human papillomavirus type 16 in cervical keratinocytes. Cancer Res 2004;64:1359-68
   PubMed Web of Science ®Google Scholar
• Schiffman M, Rodriguez AC, Chen Z, et al. A population-based prospective study of carcinogenic human papillomavirus variant lineages, viral persistence, and cervical neoplasia. Cancer Res 2010;70:3159-69
   PubMed Web of Science ®Google Scholar
• Ades S, Koushik A, Duarte-Franco E, et al. Selected class I and class II HLA alleles and haplotypes and risk of high-grade cervical intraepithelial neoplasia. Int J Cancer 2008;122:2820-6
   PubMed Web of Science ®Google Scholar
• Schiffman M, Kjaer SK. Chapter 2: natural history of anogenital human papillomavirus infection and neoplasia. J Natl Cancer Inst Monogr 2003(31):14-19
   PubMedGoogle Scholar
• Ovestad IT, Gudlaugsson E, Skaland I, et al. Local immune response in the microenvironment of CIN2-3 with and without spontaneous regression. Mod Pathol 2010;23:1231-40
   PubMed Web of Science ®Google Scholar
• de Boer MA, Jordanova ES, van Poelgeest MI, et al. Circulating human papillomavirus type 16 specific T-cells are associated with HLA Class I expression on tumor cells, but not related to the amount of viral oncogene transcripts. Int J Cancer 2007;121:2711-15
   PubMed Web of Science ®Google Scholar
• Kobayashi A, Weinberg V, Darragh T, Smith-McCune K. Evolving immunosuppressive microenvironment during human cervical carcinogenesis. Mucosal Immunol 2008;1:412-20
   PubMed Web of Science ®Google Scholar
• Klingelhutz AJ, Roman A. Cellular transformation by human papillomaviruses: lessons learned by comparing high- and low-risk viruses. Virology 2012;424:77-98
   PubMed Web of Science ®Google Scholar
• Kruse AJ, Skaland I, Munk AC, et al. Low p53 and retinoblastoma protein expression in cervical intraepithelial neoplasia grade 3 lesions is associated with coexistent adenocarcinoma in situ. Hum Pathol 2008;39:573-8
   PubMed Web of Science ®Google Scholar
• Stanley M. Pathology and epidemiology of HPV infection in females. Gynecol Oncol 2010;117:S5-10
   PubMed Web of Science ®Google Scholar
• Keating JT, Cviko A, Riethdorf S, et al. Ki-67, cyclin E, and p16INK4 are complimentary surrogate biomarkers for human papilloma virus-related cervical neoplasia. Am J Surg Pathol 2001;25:884-91
   PubMed Web of Science ®Google Scholar
• von Knebel Doeberitz M, Reuschenbach M, Schmidt D, Bergeron C. Biomarkers for cervical cancer screening: the role of p16(INK4a) to highlight transforming HPV infections. Expert Rev Proteomics 2012;9:149-63
   PubMed Web of Science ®Google Scholar
• 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;92:276-84
   PubMed Web of Science ®Google Scholar
• Sano T, Oyama T, Kashiwabara K, et al. Expression status of p16 protein is associated with human papillomavirus oncogenic potential in cervical and genital lesions. Am J Pathol 1998;153:1741-8
   PubMed Web of Science ®Google Scholar
• Reuschenbach M, Seiz M, von Knebel Doeberitz C, et al. Evaluation of cervical cone biopsies for coexpression of p16INK4a and Ki-67 in epithelial cells. Int J Cancer 2012;130:388-94
   PubMed Web of Science ®Google Scholar
• 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;121:505-9
   PubMed Web of Science ®Google Scholar
• 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 Cytopathol 2011;119:158-66
   PubMed Web of Science ®Google Scholar
• Bergeron C, Schmidt D, Ikenberg H, Ridder R. High sensitivity and high specificity of p16/Ki-67 dual-stained cytology from screening and triage trials in over 28,000 women. Cancer Cytopathol 2010;118:305-6
   PubMed Web of Science ®Google Scholar
• Baak JP, Kruse AJ, Garland SM, et al. Combined p53 and retinoblastoma protein detection identifies persistent and regressive cervical high-grade squamous intraepithelial lesions. Am J Surg Pathol 2005;29:1062-6
   PubMed Web of Science ®Google Scholar
• Munk AC, Gudlaugsson E, Ovestad IT, et al. Interaction of epithelial biomarkers, local immune response and condom use in cervical intraepithelial neoplasia 2-3 regression. Gynecol Oncol 2012;127:489-94
   PubMed Web of Science ®Google Scholar
• Demers GW, Halbert CL, Galloway DA. Elevated wild-type p53 protein levels in human epithelial cell lines immortalized by the human papillomavirus type 16 E7 gene. Virology 1994;198:169-74
   PubMed Web of Science ®Google Scholar
• Huibregtse JM, Scheffner M, Howley PM. A cellular protein mediates association of p53 with the E6 oncoprotein of human papillomavirus types 16 or 18. EMBO J 1991;10:4129-35
   PubMed Web of Science ®Google Scholar
• Basile JR, Zacny V, Munger K. The cytokines tumor necrosis factor-alpha (TNF-alpha) and TNF-related apoptosis-inducing ligand differentially modulate proliferation and apoptotic pathways in human keratinocytes expressing the human papillomavirus-16 E7 oncoprotein. J Biol Chem 2001;276:22522-8
   PubMed Web of Science ®Google Scholar
• Filippova M, Song H, Connolly JL, et al. The human papillomavirus 16 E6 protein binds to tumor necrosis factor (TNF) R1 and protects cells from TNF-induced apoptosis. J Biol Chem 2002;277:21730-9
   PubMed Web of Science ®Google Scholar
• Garnett TO, Duerksen-Hughes PJ. Modulation of apoptosis by human papillomavirus (HPV) oncoproteins. Arch Virol 2006;151:2321-35
   PubMed Web of Science ®Google Scholar
• Amortegui AJ, Meyer MP, Elborne VL, Amin RM. p53, retinoblastoma gene product, and cyclin protein expression in human papillomavirus virus DNA-positive cervical intraepithelial neoplasia and invasive cancer. Mod Pathol 1995;8:907-12
   PubMed Web of Science ®Google Scholar
• Herbsleb M, Knudsen UB, Orntoft TF, et al. Telomerase activity, MIB-1, PCNA, HPV 16 and p53 as diagnostic markers for cervical intraepithelial neoplasia. APMIS 2001;109:607-17
   PubMed Web of Science ®Google Scholar
• Slagle BL, Kaufman RH, Reeves WC, Icenogle JP. Expression of ras, c-myc, and p53 proteins in cervical intraepithelial neoplasia. Cancer 1998;83:1401-8
   PubMed Web of Science ®Google Scholar
• Tringler B, Gup CJ, Singh M, et al. Evaluation of p16INK4a and pRb expression in cervical squamous and glandular neoplasia. Hum Pathol 2004;35:689-96
   PubMed Web of Science ®Google Scholar
• Howie HL, Katzenellenbogen RA, Galloway DA. Papillomavirus E6 proteins. Virology 2009;384:324-34
   PubMed Web of Science ®Google Scholar
• Klingelhutz AJ, Foster SA, McDougall JK. Telomerase activation by the E6 gene product of human papillomavirus type 16. Nature 1996;380:79-82
   PubMed Web of Science ®Google Scholar
• 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 2005;166:1229-38
   PubMed Web of Science ®Google Scholar
• Theelen W, Reijans M, Simons G, et al. A new multiparameter assay to assess HPV 16/18, viral load and physical status together with gain of telomerase genes in HPV-related cancers. Int J Cancer 2010;126:959-75
   PubMed Web of Science ®Google Scholar
• Theelen W, Speel EJ, Herfs M, et al. Increase in viral load, viral integration, and gain of telomerase genes during uterine cervical carcinogenesis can be simultaneously assessed by the HPV 16/18 MLPA-assay. Am J Pathol 2010;177:2022-33
   PubMed Web of Science ®Google Scholar
• Hopman AH, Theelen W, Hommelberg PP, et al. Genomic integration of oncogenic HPV and gain of the human telomerase gene TERC at 3q26 are strongly associated events in the progression of uterine cervical dysplasia to invasive cancer. J Pathol 2006;210:412-19
   PubMed Web of Science ®Google Scholar
• McQueen F, Duvall E. Using a quality control approach to define an 'adequately cellular' liquid-based cervical cytology specimen. Cytopathology 2006;17:168-74
   PubMed Web of Science ®Google Scholar
• Burger EA, Kornor H, Klemp M, et al. HPV mRNA tests for the detection of cervical intraepithelial neoplasia: a systematic review. Gynecol Oncol 2011;120:430-8
   PubMed Web of Science ®Google Scholar
• Bibbo M, Dytch HE, Alenghat E, et al. DNA ploidy profiles as prognostic indicators in CIN lesions. Am J Clin Pathol 1989;92:261-5
   PubMed Web of Science ®Google Scholar
• Steinbeck RG. Proliferation and DNA aneuploidy in mild dysplasia imply early steps of cervical carcinogenesis. Acta Oncol 1997;36:3-12
   PubMed Web of Science ®Google Scholar
• Duensing S, Duensing A, Crum CP, Munger K. Human papillomavirus type 16 E7 oncoprotein-induced abnormal centrosome synthesis is an early event in the evolving malignant phenotype. Cancer Res 2001;61:2356-60
   PubMed Web of Science ®Google Scholar
• Duensing S, Lee LY, Duensing A, et al. The human papillomavirus type 16 E6 and E7 oncoproteins cooperate to induce mitotic defects and genomic instability by uncoupling centrosome duplication from the cell division cycle. Proc Natl Acad Sci USA 2000;97:10002-7
   PubMed Web of Science ®Google Scholar
• Duensing S, Munger K. The human papillomavirus type 16 E6 and E7 oncoproteins independently induce numerical and structural chromosome instability. Cancer Res 2002;62:7075-82
   PubMed Web of Science ®Google Scholar
• Kessis TD, Connolly DC, Hedrick L, Cho KR. Expression of HPV16 E6 or E7 increases integration of foreign DNA. Oncogene 1996;13:427-31
   PubMed Web of Science ®Google Scholar
• Boulet GA, Horvath CA, Berghmans S, Bogers J. Human papillomavirus in cervical cancer screening: important role as biomarker. Cancer Epidemiol Biomarkers Prev 2008;17:810-17
   PubMed Web of Science ®Google Scholar
• Park JS, Hwang ES, Park SN, et al. Physical status and expression of HPV genes in cervical cancers. Gynecol Oncol 1997;65:121-9
   PubMed Web of Science ®Google Scholar
• Pett M, Coleman N. Integration of high-risk human papillomavirus: a key event in cervical carcinogenesis? J Pathol 2007;212:356-67
   PubMed Web of Science ®Google Scholar
• Litjens RJ, Theelen W, Van de Pas Y, et al. Use of the HPV MLPA assay in cervical cytology for the prediction of high grade lesions. J Med Virol 2013; In press
   PubMed Web of Science ®Google Scholar
• Carcopino X, Henry M, Mancini J, et al. Significance of HPV 16 and 18 viral load quantitation in women referred for colposcopy. J Med Virol 2012;84:306-13
   PubMed Web of Science ®Google Scholar
• Dalstein V, Riethmuller D, Pretet JL, et al. Persistence and load of high-risk HPV are predictors for development of high-grade cervical lesions: a longitudinal French cohort study. Int J Cancer 2003;106:396-403
   PubMed Web of Science ®Google Scholar
• Hesselink AT, Berkhof J, Heideman DA, et al. High-risk human papillomavirus DNA load in a population-based cervical screening cohort in relation to the detection of high-grade cervical intraepithelial neoplasia and cervical cancer. Int J Cancer 2009;124:381-6
   PubMed Web of Science ®Google Scholar
• Moberg M, Gustavsson I, Gyllensten U. Type-specific associations of human papillomavirus load with risk of developing cervical carcinoma in situ. Int J Cancer 2004;112:854-9
   PubMed Web of Science ®Google Scholar
• Cuzick J, Mayrand MH, Ronco G, et al. Chapter 10: new dimensions in cervical cancer screening. Vaccine 2006;24(Suppl 3):S3/90-7
   Google Scholar
• 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 2009;112:293-9
   PubMed Web of Science ®Google Scholar
• Spathis A, Aga E, Alepaki M, et al. Promoter methylation of p16(INK4A), hMLH1, and MGMT in liquid-based cervical cytology samples compared with clinicopathological findings and HPV presence. Infect Dis Obstet Gynecol 2011;2011:927861
   PubMedGoogle Scholar
• 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 2011;129:2218-25
   PubMed Web of Science ®Google Scholar
• 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 2011;17:2459-65
   PubMed Web of Science ®Google Scholar
• Ostor AG. Natural history of cervical intraepithelial neoplasia: a critical review. Int J Gynecol Pathol 1993;12:186-92
   PubMed Web of Science ®Google Scholar
• Luhn P, Walker J, Schiffman M, et al. The role of co-factors in the progression from human papillomavirus infection to cervical cancer. Gynecol Oncol 2013;128:265-70
   PubMed Web of Science ®Google Scholar
• 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 2008;9:425-34
   PubMed Web of Science ®Google Scholar
• Munk AC, Kruse AJ, van Diermen B, et al. Cervical intraepithelial neoplasia grade 3 lesions can regress. APMIS 2007;115:1409-14
   PubMed Web of Science ®Google Scholar
• Carreon JD, Sherman ME, Guillen D, et al. CIN2 is a much less reproducible and less valid diagnosis than CIN3: results from a histological review of population-based cervical samples. Int J Gynecol Pathol 2007;26:441-6
   PubMed Web of Science ®Google Scholar
• Darragh TM, Colgan TJ, Cox JT, et al. The lower anogenital squamous terminology standardization project for HPV-associated lesions: background and consensus recommendations from the College of American Pathologists and the American Society for Colposcopy and Cervical Pathology. J Low Genit Tract Dis 2012;16:205-42
   PubMed Web of Science ®Google Scholar
• Trimble CL, Piantadosi S, Gravitt P, et al. Spontaneous regression of high-grade cervical dysplasia: effects of human papillomavirus type and HLA phenotype. Clin Cancer Res 2005;11:4717-23
   PubMed Web of Science ®Google Scholar
• Snijders PJ, Verhoef VM, 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 2013;132:2223-36
   PubMed Web of Science ®Google Scholar