© 2000 by Oxford University Press
Journal of the National Cancer Institute, Vol. 92, No. 9, 709-720,
May 3, 2000
© 2000 Oxford University Press
Evidence for a Causal Association Between Human Papillomavirus and a Subset of Head and Neck Cancers
Affiliations of authors: M. L. Gillison (Department of Medical Oncology), W. M. Koch, R. B. Capone, M. Spafford, L. Wu, D. Sidransky (Department of Otolaryngology–Head and Neck Surgery), W. H. Westra, M. Viglione (Department of Pathology), D. E. Symer (Department of Molecular Biology and Genetics), The Johns Hopkins University School of Medicine, Baltimore, MD; M. L. Zahurak, Department of Biostatistics, The Johns Hopkins Oncology Center, Baltimore; K. V. Shah, R. W. Daniel, Department of Molecular Microbiology and Immunology, The Johns Hopkins School of Hygiene and Public Health, Baltimore.
Correspondence to: Keerti V. Shah, M.D., Dr.P.H., The Johns Hopkins School of Hygiene and Public Health, 615 N. Wolfe St., Rm. E-5012, Baltimore, MD 21205 (e-mail: kvshah{at}jhsph.edu).
Background: High-risk human papillomaviruses (HPVs) are etiologic agents for anogenital tract cancers and have been detected in head and neck squamous cell carcinomas (HNSCCs). We investigated, retrospectively, an etiologic role for HPVs in a large series of patients with HNSCC. Methods: Tumor tissues from 253 patients with newly diagnosed or recurrent HNSCC were tested for the presence of HPV genome by use of polymerase chain reaction (PCR)-based assays, Southern blot hybridization, and in situ hybridization. The viral E6 coding region was sequenced to confirm the presence of tumor-specific viral isolates. Exons 5–9 of the TP53 gene were sequenced from 166 specimens. The hazard of death from HNSCC in patients with and without HPV-positive tumors was determined by proportional hazards regression analysis. Results: HPV was detected in 62 (25%) of 253 cases (95% confidence interval [CI] = 19%–30%). High-risk, tumorigenic type HPV16 was identified in 90% of the HPV-positive tumors. HPV16 was localized specifically by in situ hybridization within the nuclei of cancer cells in preinvasive, invasive, and lymph node disease. Southern blot hybridization patterns were consistent with viral integration. Poor tumor grade (odds ratio [OR] = 2.4; 95% CI = 1.2– 4.9) and oropharyngeal site (OR = 6.2; 95% CI = 3.1–12.1) independently increased the probability of HPV presence. As compared with HPV-negative oropharyngeal cancers, HPV-positive oropharyngeal cancers were less likely to occur among moderate to heavy drinkers (OR = 0.17; 95% CI = 0.05–0.61) and smokers (OR = 0.16; 95% CI = 0.02–1.4), had a characteristic basaloid morphology (OR = 18.7; 95% CI = 2.1–167), were less likely to have TP53 mutations (OR = 0.06; 95% CI = 0.01–0.36), and had improved disease-specific survival (hazard ratio [HR] = 0.26; 95% CI = 0.07–0.98). After adjustment for the presence of lymph node disease (HR = 2.3; 95% CI = 1.4– 3.8), heavy alcohol consumption (HR = 2.6; 95% CI = 1.4–4.7), and age greater than 60 years old (HR = 1.4; 95% CI = 0.8–2.3), all patients with HPV-positive tumors had a 59% reduction in risk of death from cancer when compared with HPV-negative HNSCC patients (HR = 0.41; 95% CI = 0.20–0.88). Conclusions: These data extend recent molecular and epidemiologic studies and strongly suggest that HPV-positive oropharyngeal cancers comprise a distinct molecular, clinical, and pathologic disease entity that is likely causally associated with HPV infection and that has a markedly improved prognosis.
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S. Bodaghi, L. V. Wood, G. Roby, C. Ryder, S. M. Steinberg, and Z.-M. Zheng Could Human Papillomaviruses Be Spread through Blood? J. Clin. Microbiol., November 1, 2005; 43(11): 5428 - 5434. [Abstract] [Full Text] [PDF]
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G. D'Souza, E. Sugar, W. Ruby, P. Gravitt, and M. Gillison Analysis of the Effect of DNA Purification on Detection of Human Papillomavirus in Oral Rinse Samples by PCR J. Clin. Microbiol., November 1, 2005; 43(11): 5526 - 5535. [Abstract] [Full Text] [PDF]
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S. Begum, D. Cao, M. Gillison, M. Zahurak, and W. H. Westra Tissue Distribution of Human Papillomavirus 16 DNA Integration in Patients with Tonsillar Carcinoma Clin. Cancer Res., August 15, 2005; 11(16): 5694 - 5699. [Abstract] [Full Text] [PDF]
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B. P. Alter, H. Joenje, A. B. Oostra, and G. Pals Fanconi Anemia: Adult Head and Neck Cancer and Hematopoietic Mosaicism Arch Otolaryngol Head Neck Surg, July 1, 2005; 131(7): 635 - 639. [Full Text] [PDF]
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H. Yang, K. Yang, A. Khafagi, Y. Tang, T. E. Carey, A. W. Opipari, R. Lieberman, P. A. Oeth, W. Lancaster, H. P. Klinger, et al. Sensitive detection of human papillomavirus in cervical, head/neck, and schistosomiasis-associated bladder malignancies PNAS, May 24, 2005; 102(21): 7683 - 7688. [Abstract] [Full Text] [PDF]
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A. Baez, A. Cantor, S. Fonseca, M. Marcos-Martinez, L. A. Mathews, C. A. Muro-Cacho, and T. Munoz-Antonia Differences in Smad4 Expression in Human Papillomavirus Type 16-Positive and Human Papillomavirus Type 16-Negative Head and Neck Squamous Cell Carcinoma Clin. Cancer Res., May 1, 2005; 11(9): 3191 - 3197. [Abstract] [Full Text] [PDF]
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S. Bodaghi, K. Yamanegi, S.-Y. Xiao, M. Da Costa, J. M. Palefsky, and Z.-M. Zheng Colorectal Papillomavirus Infection in Patients with Colorectal Cancer Clin. Cancer Res., April 15, 2005; 11(8): 2862 - 2867. [Abstract] [Full Text] [PDF]
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D. Wang, J. M. Ritchie, E. M. Smith, Z. Zhang, L. P. Turek, and T. H. Haugen Alcohol Dehydrogenase 3 and Risk of Squamous Cell Carcinomas of the Head and Neck Cancer Epidemiol. Biomarkers Prev., March 1, 2005; 14(3): 626 - 632. [Abstract] [Full Text] [PDF]
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G. F. CANNICK, A. M. HOROWITZ, T. F. DRURY, S. G. REED, and T. A. DAY Assessing oral cancer knowledge among dental students in South Carolina J Am Dent Assoc, March 1, 2005; 136(3): 373 - 378. [Abstract] [Full Text] [PDF]
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H. J.T. van Zeeburg, P. J.F. Snijders, G. Pals, M. A.J.A. Hermsen, M. A. Rooimans, G. Bagby, J. Soulier, E. Gluckman, J. Wennerberg, C. R. Leemans, et al. Generation and Molecular Characterization of Head and Neck Squamous Cell Lines of Fanconi Anemia Patients Cancer Res., February 15, 2005; 65(4): 1271 - 1276. [Abstract] [Full Text] [PDF]
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A. R. Kreimer, G. M. Clifford, P. Boyle, and S. Franceschi Human Papillomavirus Types in Head and Neck Squamous Cell Carcinomas Worldwide: A Systematic Review Cancer Epidemiol. Biomarkers Prev., February 1, 2005; 14(2): 467 - 475. [Abstract] [Full Text] [PDF]
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S.C. Reshmi and S.M. Gollin Chromosomal Instability in Oral Cancer Cells Journal of Dental Research, February 1, 2005; 84(2): 107 - 117. [Abstract] [Full Text] [PDF]
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Z. Yu, P. M. Weinberger, B. G. Haffty, C. Sasaki, C. Zerillo, J. Joe, D. Kowalski, J. Dziura, R. L. Camp, D. L. Rimm, et al. Cyclin D1 Is a Valuable Prognostic Marker in Oropharyngeal Squamous Cell Carcinoma Clin. Cancer Res., February 1, 2005; 11(3): 1160 - 1166. [Abstract] [Full Text] [PDF]
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S Mitra, C Misra, R K Singh, C K Panda, and S Roychoudhury Association of specific genotype and haplotype of p53 gene with cervical cancer in India J. Clin. Pathol., January 1, 2005; 58(1): 26 - 31. [Abstract] [Full Text] [PDF]
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M. Rodriguez-Pinilla, J. L. Rodriguez-Peralto, R. Hitt, J. J. Sanchez, C. Ballestin, A. Diez, L. Sanchez-Verde, F. Alameda, and M. Sanchez-Cespedes Cyclin A as a Predictive Factor for Chemotherapy Response in Advanced Head and Neck Cancer Clin. Cancer Res., December 15, 2004; 10(24): 8486 - 8492. [Abstract] [Full Text] [PDF]
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K. Munger, A. Baldwin, K. M. Edwards, H. Hayakawa, C. L. Nguyen, M. Owens, M. Grace, and K. Huh Mechanisms of Human Papillomavirus-Induced Oncogenesis J. Virol., November 1, 2004; 78(21): 11451 - 11460. [Full Text] [PDF]
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J. R. Grandis, J. A. Pietenpol, J. S. Greenberger, R. A. Pelroy, and S. Mohla Head and Neck Cancer: Meeting Summary and Research Opportunities Cancer Res., November 1, 2004; 64(21): 8126 - 8129. [Abstract] [Full Text] [PDF]
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N. Sirianni, P. K. Ha, M. Oelke, J. Califano, W. Gooding, W. Westra, T. L. Whiteside, W. M. Koch, J. P. Schneck, A. DeLeo, et al. Effect of Human Papillomavirus-16 Infection on CD8+ T-Cell Recognition of a Wild-Type Sequence p53264-272 Peptide in Patients with Squamous Cell Carcinoma of the Head and Neck Clin. Cancer Res., October 15, 2004; 10(20): 6929 - 6937. [Abstract] [Full Text] [PDF]
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L. Mao and W. K. Hong How Does Human Papillomavirus Contribute to Head and Neck Cancer Development? J Natl Cancer Inst, July 7, 2004; 96(13): 978 - 980. [Full Text] [PDF]
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B. J. M. Braakhuis, P. J. F. Snijders, W.-J. H. Keune, C. J. L. M. Meijer, H. J. Ruijter-Schippers, C. R. Leemans, and R. H. Brakenhoff Genetic Patterns in Head and Neck Cancers That Contain or Lack Transcriptionally Active Human Papillomavirus J Natl Cancer Inst, July 7, 2004; 96(13): 998 - 1006. [Abstract] [Full Text] [PDF]
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H. J. T. van Zeeburg, P. J. F. Snijders, H. Joenje, and R. H. Brakenhoff Re: Human Papillomavirus DNA and p53 Polymorphisms in Squamous Cell Carcinomas From Fanconi Anemia Patients J Natl Cancer Inst, June 16, 2004; 96(12): 968 - 968. [Full Text] [PDF]
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E. M. Smith, J. M. Ritchie, K. F. Summersgill, H. T. Hoffman, D. H. Wang, T. H. Haugen, and L. P. Turek Human Papillomavirus in Oral Exfoliated Cells and Risk of Head and Neck Cancer J Natl Cancer Inst, March 17, 2004; 96(6): 449 - 455. [Abstract] [Full Text] [PDF]
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M. Dai, G. M. Clifford, F. le Calvez, X. Castellsague, P. J. F. Snijders, M. Pawlita, R. Herrero, P. Hainaut, and S. Franceschi Human Papillomavirus Type 16 and TP53 Mutation in Oral Cancer: Matched Analysis of the IARC Multicenter Study Cancer Res., January 15, 2004; 64(2): 468 - 471. [Abstract] [Full Text] [PDF]
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