Diagnostic accuracy of p16INK4a immunohistochemistry in oropharyngeal squamous cell carcinomas: A systematic review and meta-analysis

International Journal of Cancer

Volumn 140, Issue 5, 2017, Pages 1186-1198

  Prigge, Elena Sophie ^a   Arbyn, Marc ^b,c   von Knebel Doeberitz, Magnus ^a   Reuschenbach, Miriam ^a  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^b Scientific Institute of Public Healt   (Belgium)

^c UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

HPV; human papillomavirus; OPSCC; oropharyngeal squamous cell carcinoma; p16

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 2A; PROTEIN E6; PROTEIN E7; MESSENGER RNA; ONCOPROTEIN; P16 PROTEIN, HUMAN; TUMOR MARKER; TUMOR PROTEIN; VIRUS DNA; VIRUS RNA;

ARTICLE; DIAGNOSTIC ACCURACY; DIAGNOSTIC TEST ACCURACY STUDY; DIAGNOSTIC VALUE; GENE AMPLIFICATION; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN PAPILLOMAVIRUS DNA TEST; ICD-10; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; META ANALYSIS; NONHUMAN; OROPHARYNX SQUAMOUS CELL CARCINOMA; PAPILLOMAVIRUS INFECTION; PAPOVAVIRUS; POLYMERASE CHAIN REACTION; SENSITIVITY AND SPECIFICITY; SYSTEMATIC REVIEW; VIRUS DETECTION; CARCINOMA, SQUAMOUS CELL; CHEMISTRY; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; OROPHARYNGEAL NEOPLASMS; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; VIROLOGY; VIRUS CELL TRANSFORMATION;

BIOMARKERS, TUMOR; CARCINOMA, SQUAMOUS CELL; CELL TRANSFORMATION, VIRAL; CYCLIN-DEPENDENT KINASE INHIBITOR P16; DNA, VIRAL; HUMANS; IN SITU HYBRIDIZATION; NEOPLASM PROTEINS; ONCOGENE PROTEINS, VIRAL; OROPHARYNGEAL NEOPLASMS; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, VIRAL; SENSITIVITY AND SPECIFICITY;

EID: 85006285287     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.30516     Document Type: Article

References (72)

1. Gillison ML, Castellsague X, Chaturvedi A, et al. Eurogin Roadmap: comparative epidemiology of HPV infection and associated cancers of the head and neck and cervix. Int J Cancer 2014;134:497–507.
2. Arbyn M, de Sanjose S, Saraiya M, et al. EUROGIN 2011 roadmap on prevention and treatment of HPV-related disease. Int J Cancer 2012;131:1969–82.
3. Jemal A, Simard EP, Dorell C, et al. Annual Report to the Nation on the Status of Cancer, 1975–2009, featuring the burden and trends in human papillomavirus(HPV)-associated cancers and HPV vaccination coverage levels. J Natl Cancer Inst 2013;105:175–201.
4. Chaturvedi AK, Engels EA, Pfeiffer RM, et al. Human papillomavirus and rising oropharyngeal cancer incidence in the United States. J Clin Oncol 2011;29:4294–301.
5. Chaturvedi AK, Anderson WF, Lortet-Tieulent J, et al. Worldwide trends in incidence rates for oral cavity and oropharyngeal cancers. J Clin Oncol 2013;31:4550–9.
6. Dayyani F, Etzel CJ, Liu M, et al. Meta-analysis of the impact of human papillomavirus (HPV) on cancer risk and overall survival in head and neck squamous cell carcinomas (HNSCC). Head Neck Oncol 2010;2:15
7. Klussmann JP, Mooren JJ, Lehnen M, et al. Genetic signatures of HPV-related and unrelated oropharyngeal carcinoma and their prognostic implications. Clin Cancer Res 2009;15:1779–86.
8. Ragin CC, Taioli E. Survival of squamous cell carcinoma of the head and neck in relation to human papillomavirus infection: review and meta-analysis. Int J Cancer 2007;121:1813–20.
9. O'Rorke MA, Ellison MV, Murray LJ, et al. Human papillomavirus related head and neck cancer survival: a systematic review and meta-analysis. Oral Oncol 2012;48:1191–201.
10. Fakhry C, Westra WH, Li S, 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.
11. Mirghani H, Amen F, Blanchard P, et al. Treatment de-escalation in HPV-positive oropharyngeal carcinoma: ongoing trials, critical issues and perspectives. Int J Cancer 2015;136:1494–503.
12. Hellner K, Munger K. Human papillomaviruses as therapeutic targets in human cancer. J Clin Oncol 2011;29:1785–94.
13. 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.
14. von Knebel Doeberitz M. The causal role of human papillomavirus infections in non-anogenital cancers. It's time to ask for the functional evidence. Int J Cancer 2016;139:9–11.
15. Masuda N, Ohnishi T, Kawamoto S, et al. Analysis of chemical modification of RNA from formalin-fixed samples and optimization of molecular biology applications for such samples. Nucleic Acids Res 1999;27:4436–43.
16. von Ahlfen S, Missel A, Bendrat K, et al. Determinants of RNA quality from FFPE samples. PLoS One 2007;2:e1261
17. Benchekroun M, DeGraw J, Gao J, et al. Impact of fixative on recovery of mRNA from paraffin-embedded tissue. Diagn Mol Pathol 2004;13:116–25.
18. McLaughlin-Drubin ME, Crum CP, Munger K. Human papillomavirus E7 oncoprotein induces KDM6A and KDM6B histone demethylase expression and causes epigenetic reprogramming. Proc Natl Acad Sci U S A 2011;108:2130–5.
19. 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.
20. Bergeron C, Ronco G, Reuschenbach M, et al. The clinical impact of using p16 immunochemistry in cervical histopathology and cytology: an update of recent developments. Int J Cancer 2015;136:2741–517.
21. Roelens J, Reuschenbach M, von Knebel Doeberitz M, et al. p16INK4a immunocytochemistry versus human papillomavirus testing for triage of women with minor cytologic abnormalities: a systematic review and meta-analysis. Cancer Cytopathol 2012;120:294–307.
22. Jordan RC, Lingen MW, Perez-Ordonez B, et al. Validation of methods for oropharyngeal cancer HPV status determination in US cooperative group trials. Am J Surg Pathol 2012;36:945–54.
23. Klussmann JP, Gultekin E, Weissenborn SJ, et al. Expression of p16 protein identifies a distinct entity of tonsillar carcinomas associated with human papillomavirus. Am J Pathol 2003;162:747–53.
24. Prigge ES, Toth C, Dyckhoff G, et al. p16(INK4a)/Ki-67 co-expression specifically identifies transformed cells in the head and neck region. Int J Cancer 2015;136:1589–99. DOI: 10.1002/ijc.29130.
25. 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.
26. Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 2009;6:e1000097
27. Whiting P, Rutjes AW, Reitsma JB, et al. The development of QUADAS: a tool for the quality assessment of studies of diagnostic accuracy included in systematic reviews. BMC Med Res Methodol 2003;3:25.
28. Whiting PF, Rutjes AW, Westwood ME, et al. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med 2011;155:529–36.
29. Arbyn M, Roelens J, Cuschieri K, et al. The APTIMA HPV assay versus the Hybrid Capture 2 test in triage of women with ASC-US or LSIL cervical cytology: a meta-analysis of the diagnostic accuracy. Int J Cancer 2013;132:101–8.
30. Harbord RM, Deeks JJ, Egger M, et al. A unification of models for meta-analysis of diagnostic accuracy studies. Biostatistics 2007;8:239–51.
31. Reitsma JB, Glas AS, Rutjes AW, et al. Bivariate analysis of sensitivity and specificity produces informative summary measures in diagnostic reviews. J Clin Epidemiol 2005;58:982–90.
32. Nyaga VN, Arbyn M, Aerts M. Metaprop: a Stata command to perform meta-analysis of binomial data. Arch Pub Health 2014;72:39.
33. Higgins JP, Thompson SG, Deeks JJ, et al. Measuring inconsistency in meta-analyses. BMJ 2003;327:557–60.
34. Harris RJ, Bradburn MJ, Deeks JJ, et al. Metan: fixed- and random-effects meta-analysis. Stata J 2008;8:3–28.
35. Rietbergen MM, Leemans CR, Bloemena E, et al. Increasing prevalence rates of HPV attributable oropharyngeal squamous cell carcinomas in the Netherlands as assessed by a validated test algorithm. Int J Cancer 2013;132:1565–71.
36. Schache AG, Liloglou T, Risk JM, et al. Evaluation of human papilloma virus diagnostic testing in oropharyngeal squamous cell carcinoma: sensitivity, specificity, and prognostic discrimination. Clin Cancer Res 2011;17:6262–71.
37. Bussu F, Sali M, Gallus R, et al. Human papillomavirus (HPV) infection in squamous cell carcinomas arising from the oropharynx: detection of HPV DNA and p16 immunohistochemistry as diagnostic and prognostic indicators – a pilot study. Int J Radiat Oncol Biol Phys 2014;89:1115–20.
38. Bussu F, Sali M, Gallus R, et al. HPV infection in squamous cell carcinomas arising from different mucosal sites of the head and neck region. Is p16 immunohistochemistry a reliable surrogate marker? Br J Cancer 2013;108:1157–62.
39. Cerezo L, Lopez C, de la Torre A, et al. Incidence of human papillomavirus-related oropharyngeal cancer and outcomes after chemoradiation in a population of heavy smokers. Head Neck 2014;36:782–6.
40. Mirghani H, Casiraghi O, Amen F, et al. Diagnosis of HPV-driven head and neck cancer with a single test in routine clinical practice. Mod Pathol 2015;28:1518–27.
41. 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.
42. 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.
43. Lukesova E, Boucek J, Rotnaglova E, et al. High level of Tregs is a positive prognostic marker in patients with HPV-positive oral and oropharyngeal squamous cell carcinomas. BioMed Res Int 2014;2014:303929.
44. Vojtechova Z, Sabol I, Salakova M, et al. Analysis of the integration of human papillomaviruses in head and neck tumours in relation to patients' prognosis. Int J Cancer 2016;138:386–95.
45. Masterson L, Sorgeloos F, Winder D, et al. Deregulation of SYCP2 predicts early stage human papillomavirus-positive oropharyngeal carcinoma: a prospective whole transcriptome analysis. Cancer Sci 2015;106:1568–75.
46. Shi W, Kato H, Perez-Ordonez B, 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.
47. Schlecht NF, Brandwein-Gensler M, Nuovo GJ, et al. A comparison of clinically utilized human papillomavirus detection methods in head and neck cancer. Mod Pathol 2011;24:1295–305.
48. Perrone F, Gloghini A, Cortelazzi B, et al. Isolating p16-positive/HPV-negative oropharyngeal cancer: an effort worth making. Am J Surg Pathol 2011;35:774–7. Author reply 7–8.
49. Hoffmann M, Tribius S, Quabius ES, et al. HPV DNA, E6*I-mRNA expression and p16INK4A immunohistochemistry in head and neck cancer – how valid is p16INK4A as surrogate marker? Cancer Lett 2012;323:88–96.
50. Gao G, Chernock RD, Gay HA, et al. A novel RT-PCR method for quantification of human papillomavirus transcripts in archived tissues and its application in oropharyngeal cancer prognosis. Int J Cancer 2013;132:882–90.
51. Salazar CR, Anayannis N, Smith RV, et al. Combined P16 and human papillomavirus testing predicts head and neck cancer survival. Int J Cancer 2014;135:2404–12.
52. Mehrad M, Zhao H, Gao G, et al. Transcriptionally-active human papillomavirus is consistently retained in the distant metastases of primary oropharyngeal carcinomas. Head and Neck Pathol 2014;8:157–63.
53. Deng Z, Hasegawa M, Aoki K, et al. A comprehensive evaluation of human papillomavirus positive status and p16INK4a overexpression as a prognostic biomarker in head and neck squamous cell carcinoma. Int J Oncol 2014;45:67–76.
54. Isayeva T, Xu J, Dai Q, et al. African Americans with oropharyngeal carcinoma have significantly poorer outcomes despite similar rates of human papillomavirus-mediated carcinogenesis. Hum Pathol 2014;45:310–9.
55. Quabius ES, Haag J, Kuhnel A, et al. Geographical and anatomical influences on human papillomavirus prevalence diversity in head and neck squamous cell carcinoma in Germany. Int J Oncol 2015;46:414–22.
56. Medema RH, Herrera RE, Lam F, et al. Growth suppression by p16ink4 requires functional retinoblastoma protein. Proc Natl Acad Sci U S A 1995;92:6289–93.
57. Collado M, Blasco MA, Serrano M. Cellular senescence in cancer and aging. Cell 2007;130:223–33.
58. Campisi J. Cellular senescence as a tumor-suppressor mechanism. Trends Cell Biol 2001;11:S27–S31.
59. Munger K, Basile JR, Duensing S, et al. Biological activities and molecular targets of the human papillomavirus E7 oncoprotein. Oncogene 2001;20:7888–98.
60. Munger K, Werness BA, Dyson N, et al. Complex formation of human papillomavirus E7 proteins with the retinoblastoma tumor suppressor gene product. EMBO J 1989;8:4099–105.
61. Kreimer AR, Clifford GM, Boyle P, et al. Human papillomavirus types in head and neck squamous cell carcinomas worldwide: a systematic review. Cancer Epidemiol Biomarkers Prev 2005;14:467–75.
62. 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.
63. 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.
64. 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.
65. 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.
66. Jewell SD, Srinivasan M, McCart LM, et al. Analysis of the molecular quality of human tissues: an experience from the Cooperative Human Tissue Network. Am J Clin Pathol 2002;118:733–41.
67. Forslund O, Lindqvist P, Haadem K, et al. HPV 16 DNA and mRNA in cervical brush samples quantified by PCR and microwell hybridization. J Virol Methods 1997; 69:209–22.
68. McNicol P, Guijon F, Wayne S, et al. Expression of human papillomavirus type 16 E6-E7 open reading frame varies quantitatively in biopsy tissue from different grades of cervical intraepithelial neoplasia. J Clin Microbiol 1995;33:1169–73.
69. Shirasawa H, Tanzawa H, Matsunaga T, et al. Quantitative detection of spliced E6-E7 transcripts of human papillomavirus type 16 in cervical premalignant lesions. Virology 1991;184:795–8.
70. Smotkin D, Prokoph H, Wettstein FO. Oncogenic and nononcogenic human genital papillomaviruses generate the E7 mRNA by different mechanisms. J Virol 1989;63:1441–7.
71. 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.
72. Lingen MW, Xiao W, Schmitt A, et al. Low etiologic fraction for high-risk human papillomavirus in oral cavity squamous cell carcinomas. Oral Oncol 2013;49:1–8.