P16 expression in relation to human papillomavirus in liquid-based cervical smears

Gynecologic Oncology

Volumn 109, Issue 2, 2008, Pages 285-290

  Samama, Brigitte ^a,b,c   Schaeffer, Christiane ^a,b,c   Boehm, Nelly ^a,b,c  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b INSERM   (France)

^c UNIVERSITY HOSPITAL OF STRASBOURG   (France)

Author keywords

Cervical cancer screening; Human papillomavirus; Immunocytochemistry; In situ hybridization; P16

Indexed keywords

PROTEIN ANTIBODY; PROTEIN P16; VIRUS DNA;

ARTICLE; CANCER GRADING; CANCER GROWTH; CANCER RISK; CANCER SCREENING; CONTROLLED STUDY; DISEASE MARKER; DNA PROBE; EPISOME; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; IN SITU HYBRIDIZATION; NONHUMAN; PAPANICOLAOU TEST; PRIORITY JOURNAL; PROTEIN EXPRESSION; RELIABILITY; UTERINE CERVIX CANCER; UTERINE CERVIX CYTOLOGY; WART VIRUS;

ADULT; CYCLIN-DEPENDENT KINASE INHIBITOR P16; DNA, VIRAL; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; NEOPLASM PROTEINS; PAPILLOMAVIRUS INFECTIONS; STAINING AND LABELING; UP-REGULATION; UTERINE CERVICAL NEOPLASMS; VAGINAL SMEARS;

EID: 42749095849     PISSN: 00908258     EISSN: 10956859     Source Type: Journal    
DOI: 10.1016/j.ygyno.2008.01.043     Document Type: Article

References (63)

1. Bernstein S.J., Sanchez-Ramos L., and Ndubisi B. Liquid-based cervical cytologic smear and conventional Papanicolaou smears: a meta-analysis of prospective studies comparing cytologic diagnosis and sample adequacy. Am J Obstet Gynecol 185 (2001) 308-317
2. Solomon D., Davey D., Kurman R., Moriarty A., O'Connor D., Prey M., Raab S., Sherman M., Wilbur D., Wright T., and Young N. The 2001 Bethesda system: terminology for reporting results of cervical cytology. JAMA 287 (2002) 2114-2119
3. Wright T.C., Cox J.T., Massad L.S., Twiggs L.B., and Wilkinson E.J. 2001 consensus guidelines for the management of women with cervical cytological abnormalities. JAMA 287 (2002) 2120-2129
4. Dalstein V., Riethmuller D., Sautière J.L., Prétet J.L., Schaal J.P., and Mougin C. Detection of cervical precancer and cancer in a hospital population: benefits of testing for human papillomavirus. Eur J Cancer 40 (2004) 1225-1232
5. Cuzick J., Sasieni P., Davies P., Adams J., Normand C., Frater A., van Ballgooijen M., and van den Akker-van Marle E. A systematic review of the role of human papillomavirus (HPV) testing within a cervical screening programme: summary and conclusions. Br J Cancer 83 (2000) 561-565
6. Clavel C., Masure M., Bory J.P., Mangeonjean C., Lorenzato M., Nazeyrollas P., Gabriel R., Quereux C., and Birembaut P. Human papillomavirus testing in primary screening for the detection of high-grade cervical lesions: a study of 7932 women. Br J Cancer 84 (2001) 1616-1623
7. Kulasingam S.L., Hughes J.P., Kiviat N.B., Mao C., Weiss N.S., Kuypers J.M., and Koutsky L.A. Evaluation of human papillomavirus testing in primary screening for cervical abnormalities: comparison of sensitivity, specificity, and frequency of referral. JAMA 288 (2002) 1749-1757
8. Munoz N., Bosch F.X., de Sanjose S., Herrero R., Castellsague X., Shah K.V., Snijders P.J., and Meijer C.J. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med 348 (2003) 518-527
9. Sano T., Oyama T., Kashiwabara K., Fukuda T., and Nakajima T. Expression status of p16 protein is associated with human papillomavirus oncogenic potential in cervical and genital lesions. Am J Pathol 153 (1998) 1741-1748
10. Klaes R., Friedrich T., Spitkovsky D., Ridder R., Rudy W., Petry U., Dallenbach-Hellweg G., Schmidt D., and von Knebel Doeberitz M. Overexpression of p16INK4 as a specific marker for dysplastic and neoplastic epithelial cells of the cervix uteri. Int J Cancer 92 (2001) 276-284
11. Murphy N., Ring M., Killalea A.G., Uhlmann V., O'Donovan M., Mulcahy F., Turner M., McGuiness E., Griffin M., Martin C., Sheils O., and O'Leary J.J. P16INK4 as a marker for cervical dyskariosis: CIN and cGIN in cervical biopsies and ThinPrep TM smears. J Clin Pathol 56 (2003) 56-63
12. Yoshida T., Fukuda T., Sano T., Kanuma T., Owada N., and 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 Cytopathol 102 (2004) 100-108
13. Bose S., Evans H., Lantzy L., Scharre K., and Youssef E. p16INK4 is a surrogate biomarker for a subset of human papillomavirus-associated dysplasias of the uterine cervix as determined on the pap smear. Diagn Cytopathol 32 (2005) 21-24
14. Nieh S., Chen S.F., Chu T.Y., Lai H.C., Lin Y.S., Fu E., and Gau C.H. Is p16(INK4A) expression more useful than human papillomavirus test to determine the outcome of atypical squamous cells of undetermined significance-categorized Pap smear? A comparative analysis using abnormal cervical smears with follow-up biopsies. Gynecol Oncol 97 (2005) 35-40
15. Trunk M.J., Dallenbach-Hellweg G., Ridder R., Petry K.U., Ikenberg H., Schneider V., and von Knebel Doeberitz M. Morphological characteristics of p16INK4a-positive cells in cervical cytology samples. Acta Cytol 48 (2004) 771-782
16. Holladay E.B., Logan S., Arnold J., Knesel B., and Smith G.D. A comparison of the clinical utility of p16INK4 immunolocalization with the presence of human papillomavirus by hybrid capture 2 for the detection of cervical dysplasia/neoplasia. Cancer Cytopathol 108 (2006) 451-461
17. Samama B., Lipsker D., and Boehm N. p16 expression in relation to human papillomavirus anogenital lesions. Hum Pathol 37 (2006) 513-519
18. Kjaer S., Hogdall E., Frederiksen F., Munk C., van den Brule A., Svare E., Meijer C., Lorincz A., and Iftner T. The absolute risk of cervical abnormalities in high-risk human papillomavirus-positive, cytologically normal women over a 10-year period. Cancer Res 66 (2006) 10630-10636
19. Pientong C., Ekalaksananan T., Kongvingyoes B., Kritpetcharat O., Swadpanich U., Pengsa P., and Yuenyao P. Immunocytochemical staining of p16INK4a protein from conventional pap test and its association with human papillomavirus infection. Diagn Cytopathol 31 (2004) 235-242
20. Filho A.L., Utagawa M.L., Shirata N.K., Pereira S.M., Namiyama G.M., Kanamura C.T., Santos Gda de Oliveira M.A., Wakamatsu A., Nonogaky S., Roteli-Martins C., di Loreto C., Mattosinho de Castro Ferraz Mda G., Maeda M.Y., Alves V.A., and Syrjanen K. Immunocytochemical expression of p16INK4A and Ki-67 in cytologically negative and equivocal pap smears positive for oncogenic human papillomavirus. Int J Gynecol Pathol 24 (2005) 118-124
21. Ekalaksananan T., Pientong C., Sriamporn S., Kongyingyoes B., Pengsa P., Kleebkaow P., Kritpetcharat O., and Parkin D.M. Usefulness of combining testing for p16 protein and human papillomavirus (HPV) in cervical carcinoma screening. Gynecol Oncol 103 (2006) 62-66
22. Wentzensen N., Hampl M., Herkert M., Reichert A., Trunk M.J., Poremba C., Ridder R., and von Knebel Doeberitz M. Identification of high-grade cervical dysplasia by the detection of p16INK4 in cell lysates obtained from cervical samples. Cancer 107 (2006) 2307-2313
23. Meyer J.L., Hanlon D.W., Andersen B.T., Rasmussen O.F., and Bisgaard K. Evaluation of p16(INK4a) expression in ThinPrep cervical specimens with the CINtec p16(INK4a) assay: correlation with biopsy follow-up results. Cancer Cytopathol 111 (2007) 83-92
24. Samama B., Plas-Roser S., Schaeffer C., Chateau D., Fabre M., and Boehm N. HPV DNA detection by in situ hybridization with catalyzed signal amplification on thin-layer cervical smears. J Histochem Cytochem 50 (2002) 1417-1420
25. Evans M.F., and Cooper K. Human papillomavirus integration: detection by in situ hybridization and potential clinical application. J Pathol 202 (2004) 1-4
26. Saqi A., Pasha T.L., McGrath C.M., Yu G.H., Zhang P., and Gupta P. Overexpression of p16INK4A in liquid-based specimens (SurePath) as marker of cervical dysplasia and neoplasia. Diagn Cytopathol 27 (2002) 365-370
27. Tsuda H., Hashiguchi Y., Kawamura N., Inoue T., and Yamamoto K. Relationship between HPV typing and abnormality of G1 cell cycle regulators in cervical neoplasm. Gynecol Oncol 91 (2003) 476-485
28. Chen S.F., Yang S.F., Chu T.Y., Lai H.C., Lin Y.W., Bai C.Y., and Nieh S. Which test is a better strategy to determine the outcome of atypical glandular cell-categorized Pap smears? Immunocytochemical p16INK4 expression or human papillomavirus test-a retrospective study. Gynecol Oncol 99 (2005) 578-584
29. Carozzi F., Cecchini S., Confortini M., Becattini V., Cariaggi M.P., Pontenani G., Sani C., and Ciatto S. Role of P16(INK4a) expression in identifying CIN2 or more severe lesions among HPV-positive patients referred for colposcopy after abnormal cytology. Cancer 108 (2006) 119-123
30. Negri G., Moretto G., Menia E., Vittadello F., Kasal A., Mian C., and Egarter-Vigl E. Immunocytochemistry of p16INK4a in liquid-based cervicovaginal specimens with modified Papanicolaou counterstaining. J Clin Pathol 59 (2006) 827-830
31. Sahebali S., Depuydt C.E., Boulet G.A., Arbyn M., Moeneclaey L.M., Vereecken AJ Van Marck E.A., and Bogers J.J. Immunocytochemistry in liquid-based cervical cytology: analysis of clinical use following a cross-sectional study. Int J Cancer 118 (2006) 1254-1260
32. Cooper K., Herrington C.S., Stickland J.E., Evans M.F., and Jo M.G. Episomal and integrated human papillomavirus in cervical neoplasia shown by non-isotopic in situ hybridization. J Clin Pathol 44 (1991) 990-996
33. Ho G.Y., Bierman R., Beardsley L., Chang C.J., and Burk R.D. Natural history of cervicovaginal papillomavirus infection in young women. N Engl J Med 338 (1998) 423-428
34. Richardson H., Kelsall G., Tellier P., Vover H., Abrhamovicz M., Ferenczy A., Coutlee F., and Franco E.L. The natural history of type-specific human papillomavirus infections in female university students. Cancer Epidemiol Biomarkers Prev 12 (2003) 485-490
35. Munoz N., Mendez F., Posso H., Molano M., van den Brule A.J., Ronderos M., and Munoz A. Incidence, duration, and determinants of cervical human papillomavirus infection in a cohort of Colombian women with normal cytological results. J Infect Dis 190 (2004) 2077-2087
36. Mantovina F., and Banks L. The human papillomavirus E6 protein and its contribution to malignant progression. Oncogene 20 (2001) 7874-7887
37. Munger K., Basile J.R., Duensing S., Eichten A., Gonzales S.L., Grace M., and Zacny V.L. Biological activities and molecular targets of the human papillomavirus E7 oncoprotein. Oncogene 20 (2001) 7888-7898
38. Duensing S., and Munger K. Mechanisms of genomic instability in human cancer: insights from studies with human papillomavirus oncoproteins. Int J Cancer 109 (2004) 157-162
39. Jeon S., Allen-Hoffmann B.L., and Lambert P.F. Integration of human papillomavirus type 16 into the human genome correlates with a selective growth advantage of cells. J Virol 69 (1995) 2989-2997
40. Tonon S.A., Picconi M.A., Bos P.D., Zinivich J.B., Galuppo J., Alonio L.V., and Teyssie A.R. Physical status of the E2 human papillomavirus 16 viral gene in cervical preneoplastic and neoplastic lesions. J Clin Virol 21 (2001) 129-134
41. Peitsaro P., Johansson B., and Syrjanen S. Integrated human papillomavirus type 16 is frequently found in cervical cancer precursors as demonstrated by a novel quantitative real-time PCR technique. J Clin Microbiol 40 (2002) 886-891
42. Hopman A.H., Smedts F., Dignef W., Ummelen M., Sonke G., Mravunac M., Vooijs G.P., Speel E.J., and Ramaekers F.C. Transition of high-grade cervical intraepithelial neoplasia to micro-invasive carcinoma is characterized by integration of HPV 16/18 and numerical chromosome. J Pathol 202 (2004) 23-33
43. Munger K., and Howley P.M. Human papillomavirus immortalization and transformation functions. Virus Res 89 (2002) 213-228
44. Doorbar J. Molecular biology of human papillomavirus infection and cervical cancer. Clin Sci (Lond) 110 (2006) 525-541
45. Woodman C.B., Collins S.I., and Young L.S. The natural history of cervical HPV infection: unresolved issues. Nat Rev Cancer 7 (2007) 11-22
46. Kalof A.N., Evans M.F., Simmons-Arnold L., Beatty B.G., and Cooper K. p16INK4A immunoexpression and HPV in situ hybridization signal patterns: potential markers of high-grade cervical intraepithelial neoplasia. Am J Surg Pathol 29 (2005) 674-679
47. INK4A immunohistochemistry is superior to HPV in situ hybridization for the detection of high-risk HPV in atypical squamous metaplasia. Am J Surg Pathol 31 (2007) 33-43
48. Masumoto N., Fujii T., Ishikawa M., Iwata T., Fukuchi T., Susumu N., Mukai M., Kubushiro K., Tsukazaki K., and Nozawa S. P16 overexpression and human papillomavirus infection in small cell carcinoma of the uterine cervix. Hum Pathol 34 (2003) 778-783
49. Begum S., Cao D., Gillison M., Zahurac M., and Westra W.H. Tissue distribution of human papillomavirus 16 DNA integration in patients with tonsillar carcinoma. Clin Cancer Res 11 (2005) 5694-5699
50. Sahebali S., Depuydt C.E., Segers K., Moeneclaey L.M., Vereecken A.J., Van Marck E., and Bogers J.J. P16INK4a as an adjunct marker in liquid-based cervical cytology. Int J Cancer 108 (2004) 871-876
51. Ansari-Lari M., Staebler A., Zaino R., Shah K., and Ronnett B. Distinction of endocervical and endometrial adenocarcinomas: immunohistochemical p16 expression correlated with human papillomavirus (HPV) DNA detection. Am J Surg Pathol 28 (2004) 160-167
52. Murphy N., Heffron C.C., King B., Ganuguapati U.G., Ring M., McGuiness E., Sheils O., and O'Leary J.J. P16INK4A positivity in benign, premalignant and malignant cervical glandular lesions: a potential diagnostic problem. Virchows Arch 445 (2004) 610-615
53. Conscience I., Jovenin N., Coissard C., Lorenzato M., Durlach A., Grange F., Birembaut P., Clavel C., and Bernard P. P16 is overexpressed in cutaneous carcinomas located on sun-exposed areas. Eur J Dermatol 16 (2006) 518-522
54. Pavey S., Conroy S., Russell T., and Gabrielli B. Ultraviolet radiation induces p16CDKN2A expression in human skin. Cancer Res 59 (1999) 4185-4189
55. Natarajan E., Saeb M., Crum C.P., Woo S.B., McKee P.H., and Rheinwald J.G. Co-expression of p16 (INK4A) and laminin 5 gamma2 by microinvasive and superficial squamous cell carcinomas in vivo and by migrating wound and senescent keratinocytes in culture. Am J Pathol 163 (2003) 477-491
56. Milde-Langosch K., Riethdorf S., Kraus-Poppinghaus A., Riethdorf L., and Loning T. Expression of cyclin-dependent kinase inhibitors p16MTS1, p21WAF1, and p27KIP1 in HPV-positive and HPV-negative adenocarcinomas. Virchows Arch 439 (2001) 55-61
57. Nindl I., Meyer T., Schmook T., Ulrich C., Ridder R., Audring H., Sterry W., and Stockfleth E. Human papillomavirus and overexpression of p16INK4 in nonmelanoma skin cancer. Dermatol Surg 30 (2004) 409-414
58. Negri G., Rigo B., Vittadello E., Egarter-Vigl E., and Mian C. Human papillomavirus typing with hybrid capture II on archived liquid-based cytologic specimens: is HPV typing always reproducible?. Am J Clin Pathol 122 (2004) 90-93
59. Branca M., Ciotti M., Santini D., Di Bonito L., Giorgi C., Benedetto A., Paba P., Favalli C., Costa S., Agarossi A., Alderisio M., and Syrjanen K. P16(INK4) expression is related to grade of cin and high-risk human papillomavirus but does not predict virus clearance after conization or disease outcome. Int J Gynecol Oncol 23 (2004) 354-365
60. Negri G., Vittadello F., Romano F., Kasal A., Rivasi F., Girlando S., Mian C., and Egarter-Vigl E. p16INK4a expression and progression risk of low-grade intraepithelial neoplasia of the cervix uteri. Virchows Arch 445 (2004) 616-620
61. Nuovo G.J., Plaia T.W., Belinsky S.A., Baylin S.B., and Herman G.J. In situ detection of the hypermethylation-induced inactivation of the p16 gene as an early event in oncogenesis. Proc Natl Acad Sci U S A 96 (1999) 12754-12759
62. Virmani A.K., Muller C., Rathi A., Zoechbauer-Mueller S., Mathis M., and Gazdar A.F. Aberrant methylation during cervical carcinogenesis. Clin Cancer Res 7 (2001) 584-589
63. Kang S., Kim H.B., Shim J.W., Nam E., Kim S.H., Ahn H.J., Cfhoi Y.P., Ding B., Song K., and Cho N.H. Methylation of p16INK4a is a non-rare event in cervical intraepithelial neoplasia. Diagn Mol Cytopathol 15 (2006) 74-82