Cervical cancer control in the era of HPV vaccination and novel biomarkers

Pathobiology

Volumn 76, Issue 2, 2009, Pages 82-89

  Klug, Stefanie J ^b   Wentzensen, Nicolas ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

Author keywords

Biomarker; Cancer screening; Cervical cancer; Cytology; Human papillomavirus; Human papillomavirus vaccination

Indexed keywords

BIOLOGICAL MARKER; CYCLINE; KI 67 ANTIGEN; MITOGEN ACTIVATED PROTEIN KINASE; MYC PROTEIN; PROTEIN E6; PROTEIN E7; PROTEIN P16; WART VIRUS VACCINE;

CANCER GROWTH; CANCER RISK; COLPOSCOPY; CYTOLOGY; GENE EXPRESSION; HUMAN; HUMAN PAPILLOMAVIRUS TYPE 11; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN PAPILLOMAVIRUS TYPE 18; PRIORITY JOURNAL; REVIEW; TUMOR BIOPSY; UTERINE CERVIX CANCER; VACCINATION;

CERVICAL INTRAEPITHELIAL NEOPLASIA; DISEASE PROGRESSION; FEMALE; HUMANS; MASS SCREENING; MODELS, BIOLOGICAL; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; PAPILLOMAVIRUS VACCINES; TUMOR MARKERS, BIOLOGICAL; UTERINE CERVICAL NEOPLASMS; VAGINAL SMEARS;

HUMAN PAPILLOMAVIRUS; PAPILLOMAVIRIDAE;

EID: 65249107186     PISSN: 10152008     EISSN: None     Source Type: Journal    
DOI: 10.1159/000201676     Document Type: Review

References (87)

1. Parkin DM, Bray F: The burden of HPV-re-lated cancers. Vaccine 2006;24(suppl 3):S11-S25.
2. Waggoner SE:Cervical cancer. Lancet 2003; 361:2217-2225.
3. Gustafsson L, Ponten J, Zack M, Adami HO: International incidence rates of invasive cervical cancer after introduction of cytological screening. Cancer Causes Control 1997;8: 755-763.
4. Munoz N, Bosch FX, de SanjoséS, Tafur L, Izarzugaza I, Gili M, Viladiu P, Navarro C, Martos C, Ascunce N:The causal link between human papillomavirus and invasive cervical cancer: a population-based case-control study in Colombia and Spain. Int J Cancer 1992;52:743-749.
5. Munoz N, Bosch FX, de SanjoséS, Herre-ro R, Castellsague X, Shah KV, Snijders PJ, Meijer CJ: Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med 2003;348:518-527.
6. Schiffman MH, Bauer HM, Hoover RN, Glass AG, Cadell DM, Rush BB, Scott DR, Sherman ME, Kurman RJ, Wacholder S:Ep-idemiologic evidence showing that human papillomavirus infection causes most cervical intraepithelial neoplasia. J Natl Cancer Inst 1993;85:958-964.
7. Walboomers JM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV, Snijders PJ, Peto J, Meijer CJ, Munoz N:Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 1999; 189:12-19.
8. zur Hausen H:Disrupted dichotomous in-tracellular control of human papillomavirus infection in cancer of the cervix. Lancet 1994;343:955-957.
9. zur Hausen H:Papillomaviruses and cancer: from basic studies to clinical application. Nat Rev Cancer 2002;2:342-350.
10. Cogliano V, Baan R, Straif K, Grosse Y, Secretan B, El Ghissassi F: Carcinogenicity of human papillomaviruses. Lancet Oncol 2005;6:204.
11. Dunne EF, Unger ER, Sternberg M, McQuillan G, Swan DC, Patel SS, Markowitz LE: Prevalence of HPV infection among females in the United States. JAMA 2007;297:813-819.
12. Syrjanen K, Hakama M, Saarikoski S, Vayrynen M, Yliskoski M, Syrjanen S, Kataja V, Castren O: Prevalence, incidence, and estimated life-time risk of cervical human papillomavirus infections in a nonselected Finnish female population. Sex Transm Dis 1990;17:15-19.
13. Schiffman M, Castle PE, Jeronimo J, Rodriguez AC, Wacholder S:Human papillomavirus and cervical cancer. Lancet 2007;370: 890-907.
14. Schlecht NF, Kulaga S, Robitaille J, Ferreira S, Santos M, Miyamura RA, Duarte-Franco E, Rohan TE, Ferenczy A, Villa LL, Franco EL:Persistent human papillomavirus infection as a predictor of cervical intraepithelial neoplasia. JAMA 2001;286:3106-3114.
15. Ostor AG: Natural history of cervical intraepithelial neoplasia: a critical review. Int J Gynecol Pathol 1993;12:186-192.
16. Schiffman M: Integration of human papillomavirus vaccination, cytology, and human papillomavirus testing. Cancer 2007;111: 145-153.
17. Doorbar J: Papillomavirus life cycle organization and biomarker selection. Dis Markers 2007;23:297-313.
18. von Knebel DM: New markers for cervical dysplasia to visualise the genomic chaos created by aberrant oncogenic papillomavirus infections. Eur J Cancer 2002;38:2229-2242.
19. Duensing S, Munger K: Centrosome abnormalities, genomic instability and carcinogenic progression. Biochim Biophys Acta 2001; 1471:M81-M88.
20. Wentzensen N, Vinokurova S, von Knebel DM:Systematic review of genomic integration sites of human papillomavirus genomes in epithelial dysplasia and invasive cancer of the female lower genital tract. Cancer Res 2004;64:3878-3884.
21. Papanicolaou GN:A survey of the actualities and potentialities of exfoliative cytology in cancer diagnosis. Ann Intern Med 1949;31:661-674.
22. Day NE: Effect of cervical cancer screening in Scandinavia. Obstet Gynecol 1984;63:714-718.
23. Franco EL, Duarte-Franco E, Ferenczy A: Cervical cancer: epidemiology, prevention and the role of human papillomavirus infection. CMAJ 2001;164:1017-1025.
24. Quinn M, Babb P, Jones J, Allen E: Effect of screening on incidence of and mortality from cancer of cervix in England: evaluation based on routinely collected statistics. BMJ 1999;318:904-908.
25. Janerich DT, Hadjimichael O, Schwartz PE, Lowell DM, Meigs JW, Merino MJ, Flannery JT, Polednak AP: The screening histories of women with invasive cervical cancer, Connecticut. Am J Public Health 1995;85:791-794.
26. Sasieni PD, Cuzick J, Lynch-Farmery E:Estimating the efficacy of screening by auditing smear histories of women with and without cervical cancer. The National Co-Ordinating Network for Cervical Screening Working Group. Br J Cancer 1996;73:10 01-10 05.
27. McCrory DC, Matchar DB, Bastian L, Datta S, Hasselblad V, Hickey J, Myers E, Nanda K: Evaluation of cervical cytology. Evid Rep Technol Assess (Summ) 1999;1-6.
28. Golbang P, Scurry J, de Jong S, McKenzie D, Planner R, Pyman J, Davoren R:Investigation of 100 consecutive negative cone biopsies. Br J Obstet Gynaecol 1997;104:100-104.
29. Kyrgiou M, Koliopoulos G, Martin-Hirsch P, Arbyn M, Prendiville W, Paraskevaidis E: Obstetric outcomes after conservative treatment for intraepithelial or early invasive cervical lesions:systematic review and metaanalysis. Lancet 2006;367:489-498.
30. Jeronimo J, Schiffman M: Colposcopy at a crossroads. Am J Obstet Gynecol 2006;195: 349-353.
31. Gage JC, Hanson VW, Abbey K, Dippery S, Gardner S, Kubota J, Schiffman M, Solomon D, Jeronimo J:Number of cervical biopsies and sensitivity of colposcopy. Obstet Gynecol 2006;108:264-272.
32. Pretorius RG, Zhang WH, Belinson JL, Huang MN, Wu LY, Zhang X, Qiao YL: Colposcopically directed biopsy, random cervical biopsy, and endocervical curettage in the diagnosis of cervical intraepithelial neoplasia II or worse. Am J Obstet Gynecol 2004; 191:430-434.
33. Wentzensen N, Schiffman M, Dunn ST, Zuna RE, Walker J, Allen RA, Zhang R, Sherman ME, Wacholder S, Jeronimo J, Gold MA, Wang SS: Grading the severity of cervical neoplasia based on combined histopathology, cytopathology, and HPV genotype distribution among 1700 women referred to colposcopy in Oklahoma. Int J Cancer 2009; 124:964-969.
34. Schiller JT, Lowy DR: Prospects for cervical cancer prevention by human papillomavirus vaccination. Cancer Res 2006; 66: 10229-10232.
35. Franco EL, Cuzick J: Cervical cancer screening following prophylactic human papillomavirus vaccination. Vaccine 2008;26(suppl 1):A16-A23.
36. Clifford G, Franceschi S, Diaz M, Munoz N, Villa LL: HPV type-distribution in women with and without cervical neoplastic diseases. Vaccine 2006;24(suppl 3):S26 -S34.
37. Franco EL, Cuzick J, Hildesheim A, de San-jose S:Issues in planning cervical cancer screening in the era of HPV vaccination. Vaccine 2006;24(suppl 3):S171-S177.
38. Wright TC Jr, Schiffman M, Solomon D, Cox JT, Garcia F, Goldie S, Hatch K, Noller KL, Roach N, Runowicz C, Saslow D: Interim guidance for the use of human papillomavirus DNA testing as an adjunct to cervical cytology for screening. Obstet Gynecol 2004; 103:304-309.
39. Arbyn M: European Guidelines for Quality Assurance in Cervical Cancer Screening. 2008. http://bookshop.europa.eu/eubook-shop/FileCache/PUBPDF/ ND7007117ENC/ ND7007117ENC-002.pdf
40. Dudding N, Hewer EM, Lancucki L, Rice S: Rapid screening:a comparative study. Cytopathology 2001; 12:235-248.
41. American College of Pathologists: Commission on Laboratory Accreditation. Cytopathology Checklist. http://www.cap.org/apps/ cap.portal 2006.
42. SAC-Singlas Accreditation Scheme for Laboratories. MED002 Specific Criteria for Cytopathology Section. http://www.sac-ac-creditation.gov.sg/index. asp 2007.
43. Wiener HG, Klinkhamer P, Schenck U, Arbyn M, Bulten J, Bergeron C, Herbert A:European guidelines for quality assurance in cervical cancer screening:recommendations for cytology laboratories. Cytopathology 2007;18:67-78.
44. Davey E, Barratt A, Irwig L, Chan SF, Macaskill P, Mannes P, Saville AM: Effect of study design and quality on unsatisfactory rates, cytology classifications, and accuracy in liquid-based versus conventional cervical cytology:a systematic review. Lancet 2006; 367:122-132.
45. Karnon J, Peters J, Platt J, Chilcott J, Mc-Googan E, Brewer N:Liquid-based cytology in cervical screening:an updated rapid and systematic review and economic analysis. Health Technol Assess 2004;8:iii,1-iii,78.
46. Cuzick J, Szarewski A, Cubie H, Hu lman G, Kitchener H, Luesley D, McGoogan E, Menon U, Terry G, Edwards R, Brooks C, Desai M, Gie C, Ho L, Jacobs I, Pickles C, Sasieni P: Management of women who test positive for high-risk types of human papillomavirus: the HART study. Lancet 2003;362:1871-1876. 47 Ronco G, Segnan N, Giorgi-Rossi P, Zappa M, Casadei GP, Carozzi F, Dalla PP, Del Mistro A, Folicaldi S, Gillio-Tos A, Nardo G, Naldoni C, Schincaglia P, Zorzi M, Confortini M, Cuzick J: 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.
47. Ronco G, Giorgi-Rossi P, Carozzi F, Dalla PP, Del Mistro A, De Marco L, De Lillo M, Naldoni C, Pierotti P, Rizzolo R, Segnan N, Schincaglia P, Zorzi M, Confortini M, Cuzick J: 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 2006;7:547-555.
48. Khan MJ, Castle PE, Lorincz AT, Wacholder S, Sherman M, Scott DR, Rush BB, Glass AG, Schiffman M: The elevated 10-year risk of cervical precancer and cancer in women with human papillomavirus (HPV) type 16 or 18 and the possible utility of type-specific HPV testing in clinical practice. J Natl Cancer Inst 2005;97:1072-1079.
49. Brink AA, Snijders PJ, Meijer CJ: HPV detection methods. Dis Markers 2007;23:273-281.
50. Schiffman M, Solomon D: Findings to date from the ASCUS-LSIL Triage Study (ALTS). Arch Pathol Lab Med 2003;127:946-949.
51. Arbyn M, Buntinx F, van Ranst M, Paraske-vaidis 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 2004;96:280-293.
52. Bulkmans NW, Rozendaal L, Snijders PJ, Voorhorst FJ, Boeke AJ, Zandwijken GR, van Kemenade FJ, Verheijen RH, Groningen K, Boon ME, Keuning HJ, van Balleqooijen M, van den Brule AJ, Meijer CJ: 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 2004;110:94-101.
53. Mayrand MH, Duarte-Franco E, Rodrigues I, Walter SD, Hanley J, Ferenczy A, Ratnam S, Coutlee F, Franco EL: Human papillomavirus DNA versus Papanicolaou screening tests for cervical cancer. N Engl J Med 2007; 357:1579-1588.
54. Naucler P, Ryd W, Tornberg S, Strand A, Wadell G, Elfgren K, Radberg T, Strander B, Forslund O, Hansson BG, Rylander E, Dillner J: Human papillomavirus and Papanicolaou tests to screen for cervical cancer. N Engl J Med 2007;357:1589-1597.
55. Bais AG, van Kemenade FJ, Berkhof J, Verheijen RH, Snijders PJ, Voorhorst F, Babovic M, van Balleqooijen M, Helmerhorst TJ, Meijer CJ: Human papillomavirus testing on self-sampled cervicovaginal brushes: an effective alternative to protect nonresponders in cervical screening programs. Int J Cancer 2007;120:1505-1510.
56. von Knebel-Doeberitz M, Syrjanen KJ: Molecular markers:how to apply in practice. Gynecol Oncol 2006;103:18-20.
57. Wentzensen N, von Knebel DM: Biomarkers in cervical cancer screening. Dis Markers 2007;23:315-330.
58. Griesser H, Sander H, Hilfrich R, Moser B, Schenck U: Correlation of immunochemical detection of HPV L1 capsid protein in pap smears with regression of high-risk HPV positive mild/moderate dysplasia. Anal Quant Cytol Histol 2004;26:241-245.
59. Lie AK, Risberg B, Borge B, Sandstad B, Delabie J, Rimala R, Onsrud M, Thoresen S: DNA- versus RNA-based methods for human papillomavirus detection in cervical neoplasia. Gynecol Oncol 2005;97:908-915.
60. 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.
61. Molden T, Nygard JF, Kraus I, Karlsen F, Nygard M, Skare GB, Skomedal H, Thoresen SO, Hagmar B: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.
62. 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.
63. Abba MC, Laguens RM, Dulout FN, Golijow CD:The c-myc activation in cervical carcinomas and HPV 16 infections. Mutat Res 2004;557:151-158.
64. Branca M, Ciotti M, Santini D, Bonito LD, Benedetto A, Giorgi C, Paba P, Favalli C, Costa S, Agarossi A, Alderisio M, Syrjanen K:Activation of the ERK/MAP kinase pathway in cervical intraepithelial neoplasia is related to grade of the lesion but not to highrisk human papillomavirus, virus clearance, or prognosis in cervical cancer. Am J Clin Pathol 2004;122:902-911.
65. Branca M, Giorgi C, Santini D, Di Bonito L, Ciotti M, Costa S, Benedetto A, Casolati EA, Favalli C, Paba P, Di Bonito P, Mariani L, Syrjanen S, Bonifacio D, Accardi L, Zanconati F, Syrjanen K: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 2005;124:113-121.
66. Branca M, Giorgi C, Ciotti M, Santini D, Di Bonito L, Costa S, Benedetto A, Bonifacio D, Di Bonito P, Paba P, Accardi L, Mariani L, Ruutu M, Syrjanen SM, Favalli C, Syrjanen K:Over-expression of topoisomerase IIalpha is related to the grade of cervical intraepithe-lial neoplasia (CIN) and high-risk human papillomavirus (HPV), but does not predict prognosis in cervical cancer or HPV clearance after cone treatment. Int J Gynecol Pathol 2006;25:383-392.
67. El Ghobashy AA, Shaaban AM, Herod J, Innes J, Prime W, Herrington CS:Overex-pression of cyclins A and B as markers of neoplastic glandular lesions of the cervix. Gynecol Oncol 2004;92:628-634.
68. Goel MM, Mehrotra A, Singh U, Gupta HP, Misra JS:MIB-1 and PCNA immunostain-ing as a diagnostic adjunct to cervical Pap smear. Diagn Cytopathol 2005;33:15-19.
69. Golijow CD, Abba MC, Mouron SA, Gomez MA, Dulout FN: c-myc gene amplification detected in preinvasive intraepithelial cervical lesions. Int J Gynecol Cancer 2001;11: 62-465.
70. Keating JT, Cviko A, Riethdorf S, Riethdorf L, Quade BJ, Sun D, Duensing S, Sheets EE, Munger K, Crum CP:Ki-67, cyclin E, and p16INK4 are complimentary surrogate bio-markers for human papilloma virus-related cervica l neoplasia. Am J Surg Pathol 2001;25: 84-891.
71. Syrjanen KJ: Immunohistochemistry in assessment of molecular pathogenesis of cervical carcinogenesis. Eur J Gynaecol Oncol 2005;26:5-19.
72. Weaver EJ, Kovatich AJ, Bibbo M:Cyclin E expression and early cervical neoplasia in ThinPrep specimens. A feasibility study. Acta Cytol 2000;44:301-304.
73. 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 2006;108: 324-330.
74. Heselmeyer-Haddad K, Sommerfeld K, White NM, Chaudhri N, Morrison LE, Palanisamy N, Wang ZY, Auer G, Steinberg W, Ried T:Genomic amplification of the human telomerase gene (TERC) in pap smears predicts the development of cervical cancer. Am J Pathol 2005;166:1229-1238.
75. Heselmeyer K, Schrock E, du Manoir S, Ble-gen H, Shah K, Steinbeck R, Auer G, Ried T: Gain of chromosome 3q defines the transition from severe dysplasia to invasive carcinoma of the uterine cervix. Proc Natl Acad Sci USA 1996;93:479-484.
76. Khleif SN, DeGregori J, Yee CL, Otterson GA, Kaye FJ, Nevins JR, Howley PM: Inhibition of cyclin D-CDK4/CDK6 activity is associated with an E2F-mediated induction of cyclin kinase inhibitor activity. Proc Natl Acad Sci USA 1996;93:4350-4354.
77. Sano T, Oyama T, Kashiwabara K, Fukuda T, Nakajima T:Expression status of p16 protein is associated with human papillomavirus oncogenic potential in cervical and genital lesions. Am J Pathol 1998;153:1741-1748.
78. Klaes R, Friedrich T, Spitkovsky D, Ridder R, Rudy W, Petry U, Dallenbach-Hellweg G, Schmidt D, von Knebel DM: Overexpression of p16(INK4A) as a specific marker for dys-plastic and neoplastic epithelial cells of the cervix uteri. Int J Cancer 2001;92:276-284.
79. Horn LC, Reichert A, Oster A, Arndal SF, Trunk MJ, Ridder R, Rassmussen OF, Bjelkenkrantz K, Christiansen P, Eck M, Lorey T, Skovlund VR, Ruediger T, Schneider V, Schmidt D: Immunostaining for p16INK4a used as a conjunctive tool improves interob-server agreement of the histologic diagnosis of cervical intraepithelial neoplasia. Am J Surg Pathol 2008;32:502-512.
80. Klaes R, Benner A, Friedrich T, Ridder R, Herrington S, Jenkins D, Kurman RJ, Schmidt D, Stoler M, von Knebel DM: p16INK4a immunohistochemistry improves interobserver agreement in the diagnosis of cervical intraepithelial neoplasia. Am J Surg Pathol 2002;26:1389-1399.
81. Zhang Q, Kuhn L, Denny LA, De Souza M, Taylor S, Wright TC Jr:Impact of utilizing p16INK4A immunohistochemistry on estimated performance of three cervical cancer screening tests. Int J Cancer 2007;120:351-356.
82. Dehn D, Torkko KC, Shroyer KR: Human papillomavirus testing and molecular markers of cervical dysplasia and carcinoma. Cancer 2007;111:1-14.
83. Wentzensen N, Bergeron C, Cas F, Vinokurova S, von Knebel DM: Triage of women with ASCUS and LSIL cytology:use of qualitative assessment of p16INK4a positive cells to identify patients with high-grade cervical intraepithelial neoplasia. Cancer 2007;111: 58-66.
84. Ziemke P: Immunocytochemistry (p16IN K4a) a s a n addit iona l exa m i nat ion for cytological specimens Class III D (Munich Classification II) (in German). Zentralbl Gynaekol 2005;127:140 -145.
85. Mao C, Balasubramanian A, Yu M, Kiviat N, Ridder R, Reichert A, Herkert M, von Knebel DM, Koutsky LA: Evaluation of a new p16(INK4A) ELISA test and a high-risk HPV DNA test for cervical cancer screening: results from proof-of-concept study. Int J Cancer 2007;120:2435-2438.
86. Wentzensen N, Hampl M, Herkert M, Reichert A, Trunk MJ, Poremba C, Ridder R, von Knebel DM: Identification of high-grade cervical dysplasia by the detection of p16INK4a in cell lysates obtained from cervical samples. Cancer 2006;107:2307-2313.
87. Castle PE, Sideri M, Jeronimo J, Solomon D, Schiffman M: Risk assessment to guide the prevention of cervical cancer. Am J Obstet Gynecol 2007; 197:356.