Asian Pacific Journal of Cancer Prevention

Asian Pacific Journal of Cancer Prevention (아시아태평양암예방학회)
권호 표지
DOI QR코드

DOI QR Code

Lack of Association between High-risk Human Papillomaviruses and Oral Squamous Cell Carcinoma in Young Japanese Patients

  • Rushatamukayanunt, Pradit (Oral and Maxillofacial Surgery, Department of Oral Health Sciences, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University) ;
  • Morita, Kei-Ichi (Oral and Maxillofacial Surgery, Department of Oral Health Sciences, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University) ;
  • Matsukawa, Sho (Oral and Maxillofacial Surgery, Department of Oral Health Sciences, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University) ;
  • Harada, Hiroyuki (Oral and Maxillofacial Surgery, Department of Oral Health Sciences, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University) ;
  • Shimamoto, Hiroaki (Oral and Maxillofacial Surgery, Department of Oral Health Sciences, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University) ;
  • Tomioka, Hirofumi (Oral and Maxillofacial Surgery, Department of Oral Health Sciences, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University) ;
  • Omura, Ken (Oral and Maxillofacial Surgery, Department of Oral Health Sciences, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University)
  • Published : 2014.05.30
Download PDF
⟨ Previous Next ⟩

Abstract

Background: Human papillomaviruses (HPV) may play an important role as one of the possible etiologies of oral squamous cell carcinoma (OSCC). The present study aimed to investigate the association between HPV and OSCC in young Japanese patients by examining the presence of HPV DNA and surrogate markers in OSCC tissues. Materials and Methods: Forty young patients with OSCC whose surgical specimens were available were analyzed and compared with 40 patients randomly recruited from a pool of patients aged >40 years. HPV DNA was detected using the polymerase chain reaction-based AMPLICOR$^{(R)}$ HPV test, and surrogate markers of HPV infection were analyzed using immunohistochemical techniques to detect $p16^{INK4a}$ and p53. Results: Only two (5%) young patients and one (2.5%) older patient were positive for HPV DNA. $p16^{INK4a}$ overexpression was identified in six (15%) young patients. p53 staining levels were not high in tissues of most young patients (27 patients, 67.5%). HPV DNA status did not significantly correlate with $p16^{INK4a}$ expression levels. Profiles of increased levels of $p16^{INK4a}$ expression with diminished levels of p53 staining were not associated with the presence of HPV DNA. The combined p53 with $p16^{INK4a}$ profiles were significantly correlated with alcohol consumption in younger patients (p=0.006). Conclusions: Results of the present study indicate that HPV is less likely to cause OSCC in young Japanese patients, and the $p16^{INK4a}$ expression level is not an appropriate surrogate marker for HPV infection in OSCC.

Keywords

References

  1. Ang KK, Harris J, Wheeler R, et al (2010). Human papillomavirus and survival of patients with oropharyngeal cancer. N Engl J Med, 363, 24-35. https://doi.org/10.1056/NEJMoa0912217
  2. Annertz K, Anderson H, Biorklund A, et al (2002). Incidence and survival of squamous cell carcinoma of the tongue in Scandinavia, with special reference to young adults. Int J Cancer, 101, 95-9. https://doi.org/10.1002/ijc.10577
  3. Balz V, Scheckenbach K, Gotte K, et al (2003). Is the p53 inactivation frequency in squamous cell carcinomas of the head and neck underestimated? Analysis of p53 exons 2-11 and human papillomavirus 16/18 E6 transcripts in 123 unselected tumor specimens. Cancer Res, 63, 1188-91.
  4. Barnes L, Eveson J, Reihcart P, Sidransky D (2005). Pathology & genetics head and neck tumours-World Health Organization classification of tumours. v. 9. IARC press.
  5. Begum S, Gillison ML, Ansari-Lari MA, et al (2003). Detection of human papillomavirus in cervical lymph nodes: a highly effective strategy for localizing site of tumor origin. Clin Cancer Res, 9, 6469-75.
  6. Boy S, Van Rensburg EJ, Engelbrecht S, et al (2006). HPV detection in primary intra-oral squamous cell carcinomas--commensal, aetiological agent or contamination? J Oral Pathol Med, 35, 86-90. https://doi.org/10.1111/j.1600-0714.2006.00385.x
  7. Chaturvedi AK, Engels EA, Pfeiffer RM, et al (2011). Human papillomavirus and rising oropharyngeal cancer incidence in the United States. J Clin Oncol, 29, 4294-301. https://doi.org/10.1200/JCO.2011.36.4596
  8. Clifford GM, Smith JS, Plummer M, et al (2003). Human papillomavirus types in invasive cervical cancer worldwide: a meta-analysis. Br J Cancer, 88, 63-73. https://doi.org/10.1038/sj.bjc.6600688
  9. D'Souza G, Kreimer AR, Viscidi R, et al (2007). Case-control study of human papillomavirus and oropharyngeal cancer. N Engl J Med, 356, 1944-56. https://doi.org/10.1056/NEJMoa065497
  10. de Sanjose S, Quint WG, Alemany L, et al (2010). Human papillomavirus genotype attribution in invasive cervical cancer: a retrospective cross-sectional worldwide study. Lancet Oncol, 11, 1048-56. https://doi.org/10.1016/S1470-2045(10)70230-8
  11. Deng Z, Hasegawa M, Kiyuna A, et al (2013). Viral load, physical status, and E6/E7 mRNA expression of human papillomavirus in head and neck squamous cell carcinoma. Head Neck, 35, 800-8. https://doi.org/10.1002/hed.23034
  12. Duray A, Descamps G, Decaestecker C, et al (2012). Human papillomavirus DNA strongly correlates with a poorer prognosis in oral cavity carcinoma. Laryngoscope, 122, 1558-65. https://doi.org/10.1002/lary.23298
  13. El-Mofty SK, Lu DW (2003). Prevalence of human papillomavirus type 16 DNA in squamous cell carcinoma of the palatine tonsil, and not the oral cavity, in young patients: a distinct clinicopathologic and molecular disease entity. Am J Surg Pathol, 27, 1463-70. https://doi.org/10.1097/00000478-200311000-00010
  14. Elango KJ, Suresh A, Erode EM, et al (2011). Role of human papilloma virus in oral tongue squamous cell carcinoma. Asian Pac J Cancer Prev, 12, 889-96.
  15. Fakhry C, Westra WH, Li S, et al (2008). Improved survival of patients with human papillomavirus-positive head and neck squamous cell carcinoma in a prospective clinical trial. J Natl Cancer Inst, 100, 261-9. https://doi.org/10.1093/jnci/djn011
  16. Ferlay J, Shin HR, Bray F, et al (2010). Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer, 127, 2893-917. https://doi.org/10.1002/ijc.25516
  17. Finzer P, Aguilar-Lemarroy A, Rosl F (2002). The role of human papillomavirus oncoproteins E6 and E7 in apoptosis. Cancer Lett, 188, 15-24. https://doi.org/10.1016/S0304-3835(02)00431-7
  18. Gillison ML, Koch WM, Capone RB, et al (2000). Evidence for a causal association between human papillomavirus and a subset of head and neck cancers. J Natl Cancer Inst, 92, 709-20. https://doi.org/10.1093/jnci/92.9.709
  19. Goot-Heah K, Kwai-Lin T, Froemming GR, et al (2012). Human papilloma virus 18 detection in oral squamous cell carcinoma and potentially malignant lesions using saliva samples. Asian Pac J Cancer Prev, 13, 6109-13. https://doi.org/10.7314/APJCP.2012.13.12.6109
  20. Hamid NA, Brown C, Gaston K (2009). The regulation of cell proliferation by the papillomavirus early proteins. Cell Mol Life Sci, 66, 1700-17. https://doi.org/10.1007/s00018-009-8631-7
  21. Harald ZH (2000). Papillomaviruses causing cancer: evasion from host-cell control in early events in carcinogenesis. J Natl Cancer I, 92, 690-8. https://doi.org/10.1093/jnci/92.9.690
  22. Harald ZH (2002). Papillomaviruses and cancer: From basic studies to clinical application. Nature Rev Cancer, 2, 342-50. https://doi.org/10.1038/nrc798
  23. Huang H, Zhang B, Chen W, et al (2012). Human papillomavirus infection and prognostic predictors in patients with oropharyngeal squamous cell carcinoma. Asian Pac J Cancer Prev, 13, 891-6. https://doi.org/10.7314/APJCP.2012.13.3.891
  24. Kabeya M, Furuta R, Kawabata K, et al (2012). Prevalence of human papillomavirus in mobile tongue cancer with particular reference to young patients. Cancer Sci, 103, 161-8. https://doi.org/10.1111/j.1349-7006.2011.02149.x
  25. Kaminagakura E, Villa LL, Andreoli MA, et al (2012). High-risk human papillomavirus in oral squamous cell carcinoma of young patients. Int J Cancer, 130, 1726-32. https://doi.org/10.1002/ijc.26185
  26. Khovidhunkit SO, Buajeeb W, Sanguansin S, et al (2008). Detection of human papillomavirus in oral squamous cell carcinoma, leukoplakia and lichen planus in Thai patients. Asian Pac J Cancer Prev, 9, 771-5.
  27. Kojima A, Maeda H, Sugita Y, et al (2002). Human papillomavirus type 38 infection in oral squamous cell carcinomas. Oral Oncol, 38, 591-6. https://doi.org/10.1016/S1368-8375(01)00112-9
  28. Krishna Rao SV, Mejia G, et al (2013). Epidemiology of oral cancer in Asia in the past decade--an update (2000-2012). Asian Pac J Cancer Prev, 14, 5567-77. https://doi.org/10.7314/APJCP.2013.14.10.5567
  29. Lingen MW, Xiao W, Schmitt A, et al (2013). Low etiologic fraction for high-risk human papillomavirus in oral cavity squamous cell carcinomas. Oral Oncol, 49, 1-8. https://doi.org/10.1016/j.oraloncology.2012.07.002
  30. Llewellyn CD, Johnson NW, Warnakulasuriya KA (2001). Risk factors for squamous cell carcinoma of the oral cavity in young people--a comprehensive literature review. Oral Oncol, 37, 401-18. https://doi.org/10.1016/S1368-8375(00)00135-4
  31. Llewellyn CD, Linklater K, Bell J, et al (2004). An analysis of risk factors for oral cancer in young people: a case-control study. Oral Oncol, 40, 304-13. https://doi.org/10.1016/j.oraloncology.2003.08.015
  32. Lopes V, Murray P, Williams H, et al (2011). Squamous cell carcinoma of the oral cavity rarely harbours oncogenic human papillomavirus. Oral Oncol, 47, 698-701. https://doi.org/10.1016/j.oraloncology.2011.04.022
  33. Matsuda T, Marugame T, Kamo K, et al (2010). Cancer incidence and incidence rates in Japan in 2004: based on data from 14 population-based cancer registries in the Monitoring of Cancer Incidence in Japan (MCIJ) Project. Jpn J Clin Oncol 40, 1192-200. https://doi.org/10.1093/jjco/hyq109
  34. Matsuda T, Marugame T, Kamo K, et al (2011). Cancer incidence and incidence rates in Japan in 2005: based on data from 12 population-based cancer registries in the Monitoring of Cancer Incidence in Japan (MCIJ) project. Jpn J Clin Oncol 41, 139-47. https://doi.org/10.1093/jjco/hyq169
  35. Matsuda T, Marugame T, Kamo K, et al (2012). Cancer incidence and incidence rates in Japan in 2006: based on data from 15 population-based cancer registries in the monitoring of cancer incidence in Japan (MCIJ) project. Jpn J Clin Oncol 42, 139-47. https://doi.org/10.1093/jjco/hyr184
  36. Matthews JB, Scully C, Jovanovic A, et al (1993). Relationship of tobacco/alcohol use to p53 expression in patients with lingual squamous cell carcinomas. Eur J Cancer B Oral Oncol, 29, 285-9 https://doi.org/10.1016/0964-1955(93)90049-K
  37. McLaughlin-Drubin ME, Munger K (2009). The human papillomavirus E7 oncoprotein. Virology, 384, 335-44. https://doi.org/10.1016/j.virol.2008.10.006
  38. Mehanna H, Beech T, Nicholson T, et al (2013). Prevalence of human papillomavirus in oropharyngeal and nonoropharyngeal head and neck cancer--systematic review and meta-analysis of trends by time and region. Head Neck 35, 747-55. https://doi.org/10.1002/hed.22015
  39. Monsonego J, Bohbot JM, Pollini G, et al (2005). Performance of the Roche AMPLICOR human papillomavirus (HPV) test in prediction of cervical intraepithelial neoplasia (CIN) in women with abnormal PAP smear. Gynecol Oncol, 99, 160-8. https://doi.org/10.1016/j.ygyno.2005.05.030
  40. Munger K, Baldwin A, Edwards KM, et al (2004). Mechanisms of human papillomavirus-induced oncogenesis. J Virol, 78, 11451-60. https://doi.org/10.1128/JVI.78.21.11451-11460.2004
  41. Narisawa-Saito M, Kiyono T (2007). Basic mechanisms of highrisk human papillomavirus-induced carcinogenesis: roles of E6 and E7 proteins. Cancer Sci, 98, 1505-11. https://doi.org/10.1111/j.1349-7006.2007.00546.x
  42. Ovestad IT, Vennestrom U, Andersen L, et al (2011). Comparison of different commercial methods for HPV detection in follow-up cytology after ASCUS/LSIL, prediction of CIN2-3 in follow up biopsies and spontaneous regression of CIN2-3. Gynecol Oncol, 123, 278-83. https://doi.org/10.1016/j.ygyno.2011.07.024
  43. Patel SC, Carpenter WR, Tyree S, et al (2011). Increasing incidence of oral tongue squamous cell carcinoma in young white women, age 18 to 44 years. J Clin Oncol, 29, 1488-94. https://doi.org/10.1200/JCO.2010.31.7883
  44. Reuschenbach M, Kansy K, Garbe K, et al (2013). Lack of evidence of human papillomavirus-induced squamous cell carcinomas of the oral cavity in southern Germany. Oral Oncol, 49, 937-42. https://doi.org/10.1016/j.oraloncology.2013.03.451
  45. Schantz SP, Yu GP (2002). Head and neck cancer incidence trends in young Americans, 1973-1997, with a special analysis for tongue cancer. Arch Otolaryngol Head Neck Surg, 128, 268-74. https://doi.org/10.1001/archotol.128.3.268
  46. Shima K, Kobayashi I, Saito I, et al (2000). Incidence of human papillomavirus 16 and 18 infection and p53 mutation in patients with oral squamous cell carcinoma in Japan. Br J Oral Maxillofac Surg, 38, 445-50. https://doi.org/10.1054/bjom.2000.0162
  47. Soerjomataram I, Lortet-Tieulent J, Parkin DM, et al (2012). Global burden of cancer in 2008: a systematic analysis of disability-adjusted life-years in 12 world regions. Lancet, 380, 1840-50. https://doi.org/10.1016/S0140-6736(12)60919-2
  48. Sugiyama M, Bhawal UK, Kawamura M, et al (2007). Human papillomavirus-16 in oral squamous cell carcinoma: clinical correlates and 5-year survival. Br J Oral Maxillofac Surg, 45, 116-22. https://doi.org/10.1016/j.bjoms.2006.04.012
  49. Thongsuksai P, Boonyaphiphat P, Sriplung H, Sudhikaran W (2003) p53 mutations in betel-associated oral cancer from Thailand. Cancer Lett, 201, 1-7. https://doi.org/10.1016/S0304-3835(03)00417-8
  50. Tural D, Elicin O, Batur S, et al (2013). Increase in the rate of HPV positive oropharyngeal cancers during 1996-2011 in a case study in Turkey. Asian Pac J Cancer Prev, 14, 6065-8. https://doi.org/10.7314/APJCP.2013.14.10.6065
  51. van Ham MA, Bakkers JM, Harbers GK, et al (2005). comparison of two commercial assays for detection of human papillomavirus (HPV) in cervical scrape specimens: validation of the Roche AMPLICOR HPV test as a means to screen for HPV genotypes associated with a higher risk of cervical disorders. J Clin Microbiol, 43, 2662-7. https://doi.org/10.1128/JCM.43.6.2662-2667.2005
  52. van Monsjou HS, Lopez-Yurda MI, Hauptmann M, et al (2013). Oral and oropharyngeal squamous cell carcinoma in young patients: the Netherlands Cancer Institute experience. Head Neck, 35, 94-102. https://doi.org/10.1002/hed.22935
  53. Wentzensen N, Gravitt PE, Solomon D, et al (2009). A study of Amplicor human papillomavirus DNA detection in the atypical squamous cells of undetermined significance-lowgrade squamous intraepithelial lesion triage study. Cancer Epidemiol Biomarkers Prev, 18, 1341-9. https://doi.org/10.1158/1055-9965.EPI-08-1180
  54. Westra WH, Taube JM, Poeta ML, et al (2008). Inverse relationship between human papillomavirus-16 infection and disruptive p53 gene mutations in squamous cell carcinoma of the head and neck. Clin Cancer Res, 14, 366-9. https://doi.org/10.1158/1078-0432.CCR-07-1402
  55. Yamakawa-Kakuta Y, Kawamata H, Doi Y, et al (2009). Does the expression of HPV16/18 E6/E7 in head and neck squamous cell carcinomas relate to their clinicopathological characteristics? Int J Oncol, 35, 983-8.

Cited by

  1. Alcohol and Tobacco Increases Risk of High Risk HPV Infection in Head and Neck Cancer Patients: Study from North-East Region of India vol.10, pp.10, 2015, https://doi.org/10.1371/journal.pone.0140700
  2. Expression and Response to Therapy and Survival in Selected Head and Neck Cancers vol.16, pp.1, 2015, https://doi.org/10.7314/APJCP.2015.16.1.253
  3. Saliva-Based Screening of High-Risk Human Papillomavirus Strains: Detection in Female Indonesian and Thai Dental Students vol.16, pp.13, 2015, https://doi.org/10.7314/APJCP.2015.16.13.5525
  4. Do Human Papilloma Viruses Play Any Role in Oral Squamous Cell Carcinoma in North Indians? vol.16, pp.16, 2015, https://doi.org/10.7314/APJCP.2015.16.16.7077
  5. Head and Neck Squamous Cell Carcinoma - Comparative Evaluation of Pathological Parameters in Young and Old Patients vol.16, pp.9, 2015, https://doi.org/10.7314/APJCP.2015.16.9.4061
  6. p16 and p53 in HPV-positive versus HPV-negative oral squamous cell carcinoma: do pathways differ? vol.46, pp.9, 2017, https://doi.org/10.1111/jop.12562
  7. Molecular basis of oral squamous cell carcinoma in young patients: Is it any different from older patients? vol.47, pp.6, 2018, https://doi.org/10.1111/jop.12642