Sensitivity and specificity of antibodies against HPV16 E6 and other early proteins for the detection of HPV16-driven oropharyngeal squamous cell carcinoma

International Journal of Cancer

Volumn 140, Issue 12, 2017, Pages 2748-2757

  Holzinger, Dana ^a   Wichmann, Gunnar ^b   Baboci, Lorena ^a,c   Michel, Angelika ^a   Höfler, Daniela ^a   Wiesenfarth, Manuel ^a   Schroeder, Lea ^a   Boscolo Rizzo, Paolo ^c   Herold Mende, Christel ^d   Dyckhoff, Gerhard ^d   Boehm, Andreas ^b   Del Mistro, Annarosa ^e   Bosch, Franz X ^d   Dietz, Andreas ^b   Pawlita, Michael ^a   Waterboer, Tim ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY HOSPITAL LEIPZIG   (Germany)

^c UNIVERSITY OF PADOVA   (Italy)

^d UNIVERSITY OF HEIDELBERG   (Germany)

^e VENETO INSTITUTE OF ONCOLOGY IOV IRCCS   (Italy)

Author keywords

biomarker; diagnosis; early proteins; head and neck squamous cell carcinoma; human papillomavirus; oropharynx; serology

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 2A; GLYCOPROTEIN E1; L1 PROTEIN; PROTEIN E6; PROTEIN E6 ANTIBODY; PROTEIN E7; UNCLASSIFIED DRUG; VIRAL PROTEIN; VIRUS ANTIBODY; VIRUS DNA; VIRUS RNA; E6 PROTEIN, HUMAN PAPILLOMAVIRUS TYPE 16; ONCOPROTEIN; REPRESSOR PROTEIN;

ADULT; ADVANCED CANCER; AGED; ALCOHOL CONSUMPTION; ANTIBODY BLOOD LEVEL; ARTICLE; CANCER DIAGNOSIS; CONTROLLED STUDY; DIAGNOSTIC ACCURACY; DIAGNOSTIC TEST ACCURACY STUDY; FEMALE; GERMANY; HUMAN; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN TISSUE; HYPOPHARYNX CANCER; ITALY; LARYNX CANCER; LYMPHADENOPATHY; MAJOR CLINICAL STUDY; MALE; MOUTH CANCER; NONHUMAN; OROPHARYNX SQUAMOUS CELL CARCINOMA; PREDICTIVE VALUE; PREDICTOR VARIABLE; PROTEIN EXPRESSION; RELIABILITY; SENSITIVITY AND SPECIFICITY; SEROLOGY; SMOKING; BLOOD; CARCINOMA, SQUAMOUS CELL; CLINICAL TRIAL; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; MIDDLE AGED; MULTICENTER STUDY; OROPHARYNGEAL NEOPLASMS; PAPILLOMAVIRUS INFECTION; PHYSIOLOGY; VERY ELDERLY; VIROLOGY;

ADULT; AGED; AGED, 80 AND OVER; ANTIBODIES, VIRAL; CARCINOMA, SQUAMOUS CELL; FEMALE; HOST-PATHOGEN INTERACTIONS; HUMAN PAPILLOMAVIRUS 16; HUMANS; MALE; MIDDLE AGED; ONCOGENE PROTEINS, VIRAL; OROPHARYNGEAL NEOPLASMS; PAPILLOMAVIRUS INFECTIONS; REPRESSOR PROTEINS; SENSITIVITY AND SPECIFICITY;

EID: 85017477008     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.30697     Document Type: Article

References (51)

1. Andl T, Kahn T, Pfuhl A, et al. Etiological involvement of oncogenic human papillomavirus in tonsillar squamous cell carcinomas lacking retinoblastoma cell cycle control. Cancer Res 1998;58:5–13.
2. Gillison ML, Koch WM, Capone RB, 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.
3. Snijders PJ, Cromme FV, van den Brule AJ, et al. Prevalence and expression of human papillomavirus in tonsillar carcinomas, indicating a possible viral etiology. Int J Cancer 1992;51:845–50.
4. Castellsague X, Alemany L, Quer M, et al. HPV involvement in head and neck cancers: comprehensive assessment of biomarkers in 3680 patients. J Natl Cancer Inst 2016;108:djv403.
5. Halec G, Holzinger D, Schmitt M, et al. Biological evidence for a causal role of HPV16 in a small fraction of laryngeal squamous cell carcinoma. Br J Cancer 2013;109:172–83.
6. Jung AC, Briolat J, Millon R, 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.
7. Klussmann JP, Weissenborn SJ, Wieland U, et al. Prevalence, distribution, and viral load of human papillomavirus 16 DNA in tonsillar carcinomas. Cancer 2001;92:2875–84.
8. Smeets SJ, Hesselink AT, Speel EJ, 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.
9. Ang KK, Harris J, Wheeler R, et al. Human papillomavirus and survival of patients with oropharyngeal cancer. N Engl J Med 2010;363:24–35.
10. Braakhuis BJ, Snijders PJ, Keune WJ, 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.
11. Holzinger D, Schmitt M, Dyckhoff G, et al. Viral RNA patterns and high viral load reliably define oropharynx carcinomas with active HPV16 involvement. Cancer Res 2012;72:4993–5003.
12. van Houten VM, Snijders PJ, van den Brekel MW, 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. CrossRef][10.1002/ijc.1313]
13. Wiest T, Schwarz E, Enders C, et al. 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.
14. Weinberger PM, Yu Z, Haffty BG, et al. Molecular classification identifies a subset of human papillomavirus–associated oropharyngeal cancers with favorable prognosis. J Clin Oncol 2006;24:736–47.
15. Prigge ES, Arbyn M, von Knebel Doeberitz M, et al. Diagnostic accuracy of p16INK4a immunohistochemistry in oropharyngeal squamous cell carcinomas: a systematic review and meta-analysis. Int J Cancer 2017;140:1186–1198.
16. Dahlstrom KR, Adler-Storthz K, Etzel CJ, et al. Human papillomavirus type 16 infection and squamous cell carcinoma of the head and neck in never-smokers: a matched pair analysis. Clin Cancer Res 2003;9:2620–6.
17. D'Souza G, Kreimer AR, Viscidi R, et al. Case-control study of human papillomavirus and oropharyngeal cancer. N Engl J Med 2007;356:1944–56.
18. 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;95:1772–83.
19. Zumbach K, Hoffmann M, Kahn T, et al. Antibodies against oncoproteins E6 and E7 of human papillomavirus types 16 and 18 in patients with head-and-neck squamous-cell carcinoma. Int J Cancer 2000;85:815–8.
20. Kreimer AR, Johansson M, Waterboer T, et al. Evaluation of human papillomavirus antibodies and risk of subsequent head and neck cancer. J Clin Oncol 2013;31:2708–15.
21. Anantharaman D, Gheit T, Waterboer T, et al. Human papillomavirus infections and upper aero-digestive tract cancers: the ARCAGE study. J Natl Cancer Inst 2013;105:536–45.
22. Anderson KS, Dahlstrom KR, Cheng JN, et al. HPV16 antibodies as risk factors for oropharyngeal cancer and their association with tumor HPV and smoking status. Oral Oncol 2015;51:662–7.
23. Anderson KS, Wong J, D'Souza G, et al. Serum antibodies to the HPV16 proteome as biomarkers for head and neck cancer. Br J Cancer 2011;104:1896–905.
24. Lang Kuhs KA, Pawlita M, Gibson SP, et al. Characterization of human papillomavirus antibodies in individuals with head and neck cancer. Cancer Epidemiol 2016;42:46–52.
25. Kelsey KT, Nelson HH, Kim S, et al. Human papillomavirus serology and tobacco smoking in a community control group. BMC Infect Dis 2015;15:8.
26. Kreimer AR, Brennan P, Lang Kuhs KA, et al. Human papillomavirus antibodies and future risk of anogenital cancer: a nested case-control study in the European prospective investigation into cancer and nutrition study. J Clin Oncol 2015;33:877–84.
27. Lang Kuhs KA, Anantharaman D, Waterboer T, et al. Human papillomavirus 16 E6 antibodies in individuals without diagnosed cancer: a pooled analysis. Cancer Epidemiol Biomarkers Prev 2015;24:683–9.
28. Tachezy R, Klozar J, Rubenstein L, et al. Demographic and risk factors in patients with head and neck tumors. J Med Virol 2009;81:878–87.
29. Koslabova E, Hamsikova E, Salakova M, et al. Markers of HPV infection and survival in patients with head and neck tumors. Int J Cancer 2013;133:1832–9.
30. Rotnaglova E, Tachezy R, Salakova M, et al. HPV involvement in tonsillar cancer: prognostic significance and clinically relevant markers. Int J Cancer 2011;129:101–10.
31. Smith EM, Ritchie JM, Pawlita M, et al. Human papillomavirus seropositivity and risks of head and neck cancer. Int J Cancer 2007;120:825–32.
32. Smith EM, Pawlita M, Rubenstein LM, et al. Risk factors and survival by HPV-16 E6 and E7 antibody status in human papillomavirus positive head and neck cancer. Int J Cancer 2010;127:111–7.
33. Smith EM, Rubenstein LM, Haugen TH, et al. Complex etiology underlies risk and survival in head and neck cancer human papillomavirus, tobacco, and alcohol: a case for multifactor disease. J Oncol 2012;2012:571862.
34. Wichmann G, Rosolowski M, Krohn K, et al. The role of HPV RNA transcription, immune response-related gene expression and disruptive TP53 mutations in diagnostic and prognostic profiling of head and neck cancer. Int J Cancer 2015;137:2846–57.
35. Baboci L, Holzinger D, Boscolo-Rizzo P, et al. Low prevalence of HPV-driven head and neck squamous cell carcinoma in North-East Italy. Papillomavirus Res 2016;2:133–40. CrossRef][10.1016/j.pvr.2016.07.002]
36. Schmitt M, Bravo IG, Snijders PJ, et al. Beadbased multiplex genotyping of human papillomaviruses. J Clin Microbiol 2006;44:504–12.
37. Schmitt M, Dondog B, Waterboer T, et al. Homogeneous amplification of genital human alpha papillomaviruses by PCR using novel broad-spectrum GP5+ and GP6+ primers. J Clin Microbiol 2008;46:1050–9.
38. Hofler D, Bohmer G, von Wasielewski R, et al. HPV16 RNA patterns defined by novel high-throughput RT-qPCR as triage marker in HPV-based cervical cancer precursor screening. Gynecol Oncol 2015;138:676–82.
39. Schmitt M, Dalstein V, Waterboer T, et al. Diagnosing cervical cancer and high-grade precursors by HPV16 transcription patterns. Cancer Res 2010;70:249–56.
40. Waterboer T, Sehr P, Michael KM, et al. Multiplex human papillomavirus serology based on in situ-purified glutathione s-transferase fusion proteins. Clin Chem 2005;51:1845–53.
41. Ribeiro KB, Levi JE, Pawlita M, et al. Low human papillomavirus prevalence in head and neck cancer: results from two large case-control studies in high-incidence regions. Int J Epidemiol 2011;40:489–502.
42. Sitas F, Egger S, Urban MI, et al. InterSCOPE study: Associations between esophageal squamous cell carcinoma and human papillomavirus serological markers. J Natl Cancer Inst 2012;104:147–58.
43. Castro F, Dirks WG, Fahnrich S, et al. High-throughput SNP-based authentication of human cell lines. Int J Cancer 2013;132:308–14.
44. Holzinger D, Flechtenmacher C, Henfling N, et al. Identification of oropharyngeal squamous cell carcinomas with active HPV16 involvement by immunohistochemical analysis of the retinoblastoma protein pathway. Int J Cancer 2013;133:1389–99.
45. Ndiaye C, Mena M, Alemany L, et al. HPV DNA, E6/E7 mRNA, and p16INK4a detection in head and neck cancers: a systematic review and meta-analysis. Lancet Oncol 2014;15:1319–31.
46. Bertisch B, Franceschi S, Lise M, et al. Risk factors for anal cancer in persons infected with HIV: a nested case-control study in the Swiss HIV Cohort Study. Am J Epidemiol 2013;178:877–84.
47. Dillner J. The serological response to papillomaviruses. Semin Cancer Biol 1999;9:423–30.
48. Heideman DA, Waterboer T, Pawlita M, et al. Human papillomavirus-16 is the predominant type etiologically involved in penile squamous cell carcinoma. J Clin Oncol 2007;25:4550–6.
49. Meschede W, Zumbach K, Braspenning J, et al. Antibodies against early proteins of human papillomaviruses as diagnostic markers for invasive cervical cancer. J Clin Microbiol 1998;36:475–80.
50. Zumbach K, Kisseljov F, Sacharova O, et al. Antibodies against oncoproteins E6 and E7 of human papillomavirus types 16 and 18 in cervical-carcinoma patients from Russia. Int J Cancer 2000;85:313–8.
51. Baboci L, Boscolo-Rizzo P, Holzinger D, et al. Evidence of the causal role of human papillomavirus type 58 in an oropharyngeal carcinoma. Virol J 2013;10:334. CrossRef][10.1186/1743-422X-10-334]