Viral RNA patterns and high viral load reliably define oropharynx carcinomas with active HPV16 involvement

Cancer Research

Volumn 72, Issue 19, 2012, Pages 4993-5003

  Holzinger, Dana ^a,b   Schmitt, Markus ^b   Dyckhoff, Gerhard ^a   Benner, Axel ^b   Pawlita, Michael ^b   Bosch, Franz X ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 2A; VIRUS RNA;

ADULT; CARCINOGENIC ACTIVITY; CONTROLLED STUDY; DEATH; DISEASE ASSOCIATION; DNA MARKER; FEMALE; GENE OVEREXPRESSION; HUMAN; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; NONHUMAN; NOTE; OROPHARYNGEAL SQUAMOUS CELL CARCINOMA; OROPHARYNX CARCINOMA; OVERALL SURVIVAL; PAPILLOMAVIRUS INFECTION; PREVALENCE; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; RNA ANALYSIS; UTERINE CERVIX CARCINOMA; VIRUS LOAD;

CARCINOMA, SQUAMOUS CELL; CYCLIN-DEPENDENT KINASE INHIBITOR P16; DNA, VIRAL; FEMALE; HOST-PATHOGEN INTERACTIONS; HUMAN PAPILLOMAVIRUS 16; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MIDDLE AGED; MULTIVARIATE ANALYSIS; OROPHARYNGEAL NEOPLASMS; PAPILLOMAVIRUS INFECTIONS; REAL-TIME POLYMERASE CHAIN REACTION; RNA, VIRAL; SURVIVAL ANALYSIS; TISSUE ARRAY ANALYSIS; VIRAL LOAD;

EID: 84867116870     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-11-3934     Document Type: Note

References (45)

1. Andl T, Kahn T, Pfuhl A, Nicola T, Erber R, Conradt C, et al. Etiological involvement of oncogenic human papillomavirus in tonsillar squamous cell carcinomas lacking retinoblastoma cell cycle control. Cancer Res 1998;58:5-13. (Pubitemid 28027707)
2. Gillison ML, Koch WM, Capone RB, Spafford M, Westra WH, Wu L, et al. Evidence for a causal association between human papillomavirus and a subset of head and neck cancers. J Natl Cancer Inst 2000;92:709-20. (Pubitemid 30365531)
3. Paz IB, Cook N, Odom-Maryon T, Xie Y, Wilczynski SP. Human papillomavirus (HPV) in head and neck cancer. An association of HPV 16 with squamous cell carcinoma of Waldeyer's tonsillar ring. Cancer 1997;79:595-604. (Pubitemid 27051787)
4. Snijders PJ, Cromme FV, van den Brule AJ, Schrijnemakers HF, Snow GB, Meijer CJ, et al. Prevalence and expression of human papillomavirus in tonsillar carcinomas, indicating a possible viral etiology. Int J Cancer 1992;51:845-50.
5. Ang KK, Harris J, Wheeler R, Weber R, Rosenthal DI, Nguyen-Tan PF, et al. Human papillomavirus and survival of patients with oropharyngeal cancer. N Engl J Med 2010;363:24-35.
6. D'Souza G, Agrawal Y, Halpern J, Bodison S, Gillison ML. Oral sexual behaviors associated with prevalent oral human papillomavirus infection. J Infect Dis 2009;199:1263-9.
7. Gillison ML, D'Souza G, Westra W, Sugar E, Xiao W, Begum S, et al. Distinct risk factor profiles for human papillomavirus type 16-positive and human papillomavirus type 16-negative head and neck cancers. J Natl Cancer Inst 2008;100:407-20. (Pubitemid 351480511)
8. Hafkamp HC, Manni JJ, Haesevoets A, Voogd AC, Schepers M, Bot FJ, et al. Marked differences in survival rate between smokers and nonsmokers with HPV 16-associated tonsillar carcinomas. Int J Cancer 2008;122:2656-64. (Pubitemid 351631366)
9. Klussmann JP, Weissenborn SJ, Wieland U, Dries V, Kolligs J, Jungehuelsing M, et al. Prevalence, distribution, and viral load of human papillomavirus 16 DNA in tonsillar carcinomas. Cancer 2001; 92:2875-84.
10. Lindel K, Beer KT, Laissue J, Greiner RH, Aebersold DM. Human papillomavirus positive squamous cell carcinoma of the oropharynx: a radiosensitive subgroup of head and neck carcinoma. Cancer 2001;92:805-13. (Pubitemid 32783066)
11. Smith EM, Ritchie JM, Summersgill KF, Klussmann JP, Lee JH, Wang D, et al. Age, sexual behavior and human papillomavirus infection in oral cavity and oropharyngeal cancers. Int J Cancer 2004;108:766-72. (Pubitemid 38076410)
12. Fakhry C, Westra WH, Li S, Cmelak A, Ridge JA, Pinto H, et al. Improved survival of patients with human papillomavirus-positive head and neck squamous cell carcinoma in a prospective clinical trial. J Natl Cancer Inst 2008;100:261-9. (Pubitemid 351480538)
13. Shi W, Kato H, Perez-Ordonez B, Pintilie M, Huang S, Hui A, et al. Comparative prognostic value of HPV16 E6 mRNA compared with in situ hybridization for human oropharyngeal squamous carcinoma. J Clin Oncol 2009;27:6213-21.
14. Weinberger PM, Yu Z, Haffty BG, Kowalski D, Harigopal M, Brandsma J, et al. Molecular classification identi fies a subset of human papillomavirus- associated oropharyngeal cancers with favorable prognosis. J Clin Oncol 2006;24:736-47. (Pubitemid 46622040)
15. Attner P, Du J, Nasman A, Hammarstedt L, Ramqvist T, Lindholm J, et al. The role of human papillomavirus in the increased incidence of base of tongue cancer. Int J Cancer 2010;126:2879-84.
16. Braakhuis BJ, Snijders PJ, Keune WJ, Meijer CJ, Ruijter-Schippers HJ, Leemans CR, et al. Genetic patterns in head and neck cancers that contain or lack transcriptionally active human papillomavirus. J Natl Cancer Inst 2004;96:998-1006. (Pubitemid 39162642)
17. Jung AC, Briolat J, Millon R, de Reynies A, Rickman D, Thomas E, et al. Biological and clinical relevance of transcriptionally active human papillomavirus (HPV) infection in oropharynx squamous cell carcinoma. Int J Cancer 2010;126:1882-94.
18. Lindquist D, Romanitan M, Hammarstedt L, Nasman A, Dahlstrand H, Lindholm J, et al. Human papillomavirus is a favourable prognostic factor in tonsillar cancer and its oncogenic role is supported by the expression of E6 and E7. Mol Oncol 2007;1:350-5. (Pubitemid 350186274)
19. Mellin H, Dahlgren L, Munck-Wikland E, Lindholm J, Rabbani H, Kalantari M, et al. Human papillomavirus type 16 is episomal and a high viral load may be correlated to better prognosis in tonsillar cancer. Int J Cancer 2002;102:152-8.
20. van Houten VM, Snijders PJ, van den Brekel MW, Kummer JA, Meijer CJ, van Leeuwen B, et al. Biological evidence that human papillomaviruses are etiologically involved in a subgroup of head and neck squamous cell carcinomas. Int J Cancer 2001;93:232-5. (Pubitemid 32574279)
21. Wiest T, Schwarz E, Enders C, Flechtenmacher C, Bosch FX. Involvement of intact HPV16 E6/E7 gene expression in head and neck cancers with unaltered p53 status and perturbed pRb cell cycle control. Oncogene 2002;21:1510-7. (Pubitemid 34226138)
22. Rischin D, Young RJ, Fisher R, Fox SB, Le QT, Peters LJ, et al. Prognostic significance of p16INK4A and human papillomavirus in patients with oropharyngeal cancer treated on TROG 02.02 phase III trial. J Clin Oncol 2010;28:4142-8.
23. Reimers N, Kasper HU, Weissenborn SJ, Stutzer H, Preuss SF, Hoffmann TK, et al. Combined analysis of HPV-DNA, p16 and EGFR expression to predict prognosis in oropharyngeal cancer. Int J Cancer 2007;120:1731-8. (Pubitemid 46399359)
24. Begum S, Cao D, Gillison M, Zahurak M, Westra WH. Tissue distribution of human papillomavirus 16 DNA integration in patients with tonsillar carcinoma. Clin Cancer Res 2005;11:5694-9. (Pubitemid 41170292)
25. Hoffmann M, Tribius S, Quabius ES, Henry H, Pfannenschmidt S, Burkhardt C, et al. HPV DNA, E6(*)I-mRNA expression and p16(INK4A) immunohistochemistry in head and neck cancer - how valid is p16 (INK4A) as surrogate marker? Cancer Lett 2012;323:88-96.
26. Smith EM, Wang D, Kim Y, Rubenstein LM, Lee JH, Haugen TH, et al. P16INK4a expression, human papillomavirus, and survival in head and neck cancer. Oral Oncol 2008;44:133-42. (Pubitemid 351179656)
27. Smeets SJ, Hesselink AT, Speel EJ, Haesevoets A, Snijders PJ, Pawlita M, et al. A novel algorithm for reliable detection of human papillomavirus in paraffin embedded head and neck cancer specimen. Int J Cancer 2007;121:2465-72. (Pubitemid 350022416)
28. Dyson N, Howley PM, Munger K, Harlow E. The human papillomavirus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science 1989;243:934-7. (Pubitemid 19066153)
29. Werness BA, Levine AJ, Howley PM. Association of human papillomavirus types 16 and 18 E6 proteins with p53. Science 1990;248:76-9.
30. Schmitt M, Dalstein V, Waterboer T, Clavel C, Gissmann L, Pawlita M. Diagnosing cervical cancer and high-grade precursors by HPV16 transcription patterns. Cancer Res 2010;70:249-56.
31. Schmitt M, Bravo IG, Snijders PJ, Gissmann L, Pawlita M, Waterboer T. Bead-based multiplex genotyping of human papillomaviruses. J Clin Microbiol 2006;44:504-12. (Pubitemid 43222244)
32. Schmitt M, Dondog B, Waterboer T, Pawlita M. Homogeneous amplification of genital human alpha papillomaviruses by PCR using novel broad-spectrum GP5+ and GP6+ primers. J Clin Microbiol 2008;46:1050-9. (Pubitemid 351380000)
33. Schmitt M, Dondog B, Waterboer T, Pawlita M, Tommasino M, Gheit T. Abundance of multiple high-risk human papillomavirus (HPV) infections found in cervical cells analyzed by use of an ultrasensitive HPV genotyping assay. J Clin Microbiol 2010;48:143-9.
34. Karsai S, Abel U, Roesch-Ely M, Affolter A, Hofele C, Joos S, et al. Comparison of p16(INK4a) expression with p53 alterations in head and neck cancer by tissue microarray analysis. J Pathol 2007;211:314-22. (Pubitemid 46172707)
35. Nasser W, Flechtenmacher C, Holzinger D, Hofele C, Bosch FX. Aberrant expression of p53, p16INK4a and Ki-67 as basic biomarker for malignant progression of oral leukoplakias. J Oral Pathol Med 2011;40:629-35.
36. Klaes R, Friedrich T, Spitkovsky D, Ridder R, Rudy W, Petry U, 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. (Pubitemid 32225381)
37. Korn EL. Censoring distributions as a measure of follow-up in survival analysis. Stat Med 1986;5:255-60.
38. Harrell F. Regression modeling strategies. 1st ed. New York: Springer; 2001.
39. Grambsch P, Therneau T. Proportional hazards tests and diagnostics based on weighted residuals. Biometrika 1994;81:515-26.
40. Heagerty PJ, Zheng Y. Survival model predictive accuracy and ROC curves. Biometrics 2005;61:92-105. (Pubitemid 40380968)
41. Gerds TA, Schumacher M. Efron-type measures of prediction error for survival analysis. Biometrics 2007;63:1283-7. (Pubitemid 350212588)
42. Efron B, Tibshirani R. Improvements on cross-validation: the 0.632+ bootstrap method. J Am Stat Assoc 1997;92:548-60.
43. Halec G, Schmitt M, Dondog B, Sharkhuu E, Wentzensen N, Gheit T, et al. Biological activity of probable/possible high-risk human papillomavirus types in cervical cancer. Int J Cancer. 2012 Apr 19. [Epub ahead of print].
44. Hoffmann M, Ihloff AS, Gorogh T, Weise JB, Fazel A, Krams M, et al. p16(INK4a) overexpression predicts translational active human papillomavirus infection in tonsillar cancer. Int J Cancer 2010;127:1595-602.
45. D'Souza G, Kreimer AR, Viscidi R, Pawlita M, Fakhry C, Koch WM, et al. Case-control study of human papillomavirus and oropharyngeal cancer. N Engl J Med 2007;356:1944-56. (Pubitemid 46740304)