The Relationship between Human Papillomavirus and Oesophageal Squamous Cell Carcinoma in China—A Review of the Evidence
Surabhi S. Liyanage, Qian Li, Yang Zheng, Holly Seale, Philip J. Crowe, Anthony T. Newall, Bayzidur Rahman, Eva Segelov, Chenxu Qu, Fanghui Zhao, Junfeng Liu, Zhanhai Gao, Weixian Shi, Peng Yang, Aye Moa, Chandini Raina MacIntyre
Centre for Disease Control and Prevention, Beijing, China.
Department of Cancer Epidemiology, Cancer Institute, Chinese Academy of Medical Sciences, Peking Union Medical College, Beijing, China.
Department of Medicine, St. Vincent’s Hospital Clinical School, The University of New South Wales, Sydney, Australia.
Department of Surgery, Fourth Hospital, Shijiazhuang, China.
Department of Surgery, Prince of Wales Hospital Clinical School, The University of New South Wales, Sydney, Australia.
School of Public Health and Community Medicine, The University of New South Wales Medicine, The University of New South Wales, Sydney, Australia.
DOI: 10.4236/aid.2013.31003   PDF    HTML     5,568 Downloads   11,000 Views   Citations

Abstract

Background: China has one of the highest incidence rates of oesophageal cancer in the world. The role of human papillomavirus (HPV) has been extensively researched in oesophageal squamous cell carcinoma (OSCC) with indeterminate results. The majority of these studies have been conducted in the Chinese population. Evidence for a definitive HPV-OSCC association could potentially support prophylactic vaccination in target populations, highlighting the need for ongoing investigation. The aim of this review is to summarise the findings of HPV DNA in OSCC tissue in Chinese subjects, with a view to informing further research in this area. Methods: A systematic literature search of the Chinese National Knowledge Infrastructure (CNKI) database, Medline, Embase and PubMed was conducted for all studies in English and Chinese language, examining OSCC tissue for HPV DNA in China. Reference lists of retrieved articles were reviewed and hand searches of relevant, key journals were conducted, to source articles which were not electronically indexed. Sixty-four studies met our selection criteria. Data from case-control and cross-sectional studies were analysed separately for any HPV-OSCC association, using the Epi InfoTM 3.5.3 software program. Results: From all studies conducted in the Chinese population, 2166/5953 (36%) of all OSCC tissue and 478/1684 (28%) of healthy control tissue, tested positive for HPV. We found that 11/16 case-control and cross-sectional studies had a statistically significant crude odds ratio, which supported a potential HPV-OSCC association. The largest study, carried out in the high incidence County of Anyang in Henan Province, reported 207/265 (78%) OSCC tissues testing positive for HPV DNA against 203/357 (57%) controls and had an unadjusted odds ratio of 2.71 (p-value < 0.0001). Conclusion: A rigorous meta-analysis would improve interpretation of the data and a well-designed large-scale case-control study is warranted. If a link is found between HPV and OSCC, prophylactic HPV vaccines could be of significant benefit in China.

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S. S. Liyanage, Q. Li, Y. Zheng, H. Seale, P. J. Crowe, A. T. Newall, B. Rahman, E. Segelov, C. Qu, F. Zhao, J. Liu, Z. Gao, W. Shi, P. Yang, A. Moa and C. Raina MacIntyre, "The Relationship between Human Papillomavirus and Oesophageal Squamous Cell Carcinoma in China—A Review of the Evidence," Advances in Infectious Diseases, Vol. 3 No. 1, 2013, pp. 17-34. doi: 10.4236/aid.2013.31003.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] K. Syrjanen, “HPV and Oesophageal Carcinoma,” In: Papillomavirus Research: From Natural History to Vaccines and Beyond,” Caister Academic Press, Norfolk, 2006, pp. 229-253.
[2] “Smokeless Tobacco and Some Tobacco-specific N-Nitrosamines,” IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, Vol. 89, World Health Organisation and International Agency for Research on Cancer, Lyon, 2007.
[3] G. Brooks, K. Carroll, J. Butel, S. Morse, T. Mietzner, “Human Cancer Viruses,” In: M. A. Jawetz, Ed., Medical Microbiology, 24th Edition, The McGraw-Hill Companies, New York, 2007, pp. 597-600.
[4] P. Day and J. Schiller, “Early Events in the Papillomaviral Lifecycle,” In: C. M. Norfolk, Ed., Papillomavirus Research, Caister Academic Press, Norfolk, 2006, pp. 175-192.
[5] E. de Villiers, C. Fauquet, T. Broker, B. Hu and H. zur Hausen, “Classification of Papillomaviruses,” Virology, Vol. 324, No. 1, 2004, pp. 17-27. doi:10.1016/j.virol.2004.03.033
[6] J. Ferlay, H. Shin, F. Bray, D. Forman, C. Mathers and D. Parkin, “GLOBOCAN 2008, Cancer Incidence and Mortality Worldwide: IARC Cancer Base,” No. 10, International Agency for Research on Cancer, Lyon, 2010.
[7] D. M. Parkin, F. Bray, J. Ferlay and P. Pisani, “Global Cancer Statistics, 2002,” CA: A Cancer Journal for Clinicians, Vol. 55, No. 2, 2005, pp. 74-108. doi:10.3322/canjclin.55.2.74
[8] H. zur Hausen, “Human Papillomaviruses in the Pathogenesis of Anogenital Cancer,” Virology, Vol. 184, No. 1, 1991, pp. 9-13. doi:10.1016/0042-6822(91)90816-T
[9] H. Romanczuk and P. Howley, “Disruption of Either the E1 or the E2 Regulatory Gene of Human Papillomavirus Type 16 Increases Viral Immortalization Capacity,” Proceedings of the National Academy of Sciences, Vol. 89, No. 7, 1992, pp. 3159-3163.
[10] L. F. Garrote, R. Herrero, R. M. O. Reyes, S. Vaccarella, J. L. Anta, L. Ferbeye, N. Munoz and S. Franceschi, “Risk Factors for Cancer of the Oral Cavity and Oro-Pharynx in Cuba,” British Journal of Cancer, Vol. 85, No. 1, 2001, pp. 46-54. doi:10.1054/bjoc.2000.1825
[11] A. M. Hong, A. E. Grulich, D. Jones, C. S. Lee, S. M. Garland, T. A. Dobbins, J. R. Clark, G. B. Harnett, C. G. Milross, C. J. O’Brien, et al., “Squamous Cell Carcinoma of the Oropharynx in Australian Males Induced by Human Papillomavirus Vaccine Targets,” Vaccine, Vol. 28, No. 19, 2010, pp. 3269-3272. doi:10.1016/j.vaccine.2010.02.098
[12] R. Kreimer Aimee, J. Alberg Anthony, R. Daniel, E. Gravitt Patti, R. Viscidi, S. Garrett Elizabeth, V. Shah Keerti and L. Gillison Maura, “Oral Human Papillomavirus Infection in Adults Is Associated with Sexual Behavior and HIV Serostatus,” The Journal of Infectious Diseases, Vol. 189, No. 4, 2004, pp. 686-698. doi:10.1086/381504
[13] C. H. Shiboski, B. L. Schmidt and R. C. K. Jordan, “Tongue and Tonsil Carcinoma,” Cancer, Vol. 103, No. 9, 2005, pp. 1843-1849. doi:10.1002/cncr.20998
[14] E. Smith, S. Johnson, T. Cripe, S. Pignatari and L. Turek, “Perinatal Vertical Transmission of Human Papillomavirus and Subsequent Development of Respiratory Tract Papillomatosis,” Annals of Otology, Rhinology and Laryngology, Vol. 100, No. 6, 1991, pp. 478-483.
[15] F. Chang, S. Syrjanen, Q. Shen, L. Wang, D. Wang and K. Syrjanen, “Human Papillomavirus (HPV) Involvement in Esophageal Precancerous Lesions and Squamous Cell Carcinomas as Evidenced by Microscopy and Different DNA Techniques,” Scandinavian Journal of Gastroenterology, Vol. 27, No. 7, 1992, pp. 553-563. doi:10.3109/00365529209000119
[16] M. Curado, B. Edwards, H. Shin, H. Storm, J. Ferlay, M. Heanue and P. Boyle, “Cancer Incidence in Five Continents,” International Agency for Research on Cancer, Lyon, 2007.
[17] S. Mudan and J. Kang, “Epidemiology and Clinical Presentation in Esophageal Cancer,” In: S. Rankin, Ed., Carcinoma of the Esophagus, Cambridge University Press, New York, 2008, pp. 1-10.
[18] S. J. Spechler, “Squamous Cell Carcinoma of the Esophagus,” In: W. Scheppach, R. Bresalier and G. Tytgat, Eds., Gastrointestinal and Liver Tumors, Springer-Verlag, Berlin, 2004, pp. 5-11. doi:10.1007/978-3-642-18629-5_1
[19] Z. Wang, L. Tang, G. Sun, Y. Tang, Y. Xie, S. Wang, X. Hu, W. Gao, S. Cox and J.-S. Wang, “Etiological Study of Esophageal Squamous Cell Carcinoma in an Endemic Region: A Population-Based Case Control Study in Huaian, China,” BMC Cancer, Vol. 6, No. 1, 2006, p. 287. doi:10.1186/1471-2407-6-287
[20] D. Parkin, P. Pisani and J. Ferlay, “Estimates of Worldwide Incidence of 25 Major Cancers in 1990,” International Journal of Cancer, Vol. 80, No. 6, 1990, pp. 827-841. doi:10.1002/(SICI)1097-0215(19990315)80:6<827::AID-IJC6>3.0.CO;2-P
[21] Esophageal Cancer. http://www.merckmanuals.com/home/sec09/ch131/ch131c.html
[22] J. Ferlay, H. R. Shin, F. Bray, D. Forman, C. Mathers and D. M. Parkin, “Estimates of Worldwide Burden of Cancer in 2008: GLOBOCAN 2008,” International Journal of Cancer, Vol. 127, No. 12, 2010, pp. 2893-2917. doi:10.1002/ijc.25516
[23] P. Zhao, M. Dai, W. Chen and N. Li, “Cancer Trends in China,” Japanese Journal of Clinical Oncology, Vol. 40, No. 4, 2010, pp. 281-285. doi:10.1093/jjco/hyp187
[24] H. Zhang, Z. Chen, J. Cheng, X. Zhu, W. Guo, A. Hu, Y. Du, Y. Zhou and Y. Wang, “The High Incidence of Esophageal Cancer in Parts of China May Result Primarily from Genetic Rather than Environmental Factors,” Diseases of the Esophagus, Vol. 23, No. 5, 2010, pp. 392-397.
[25] D. He, D.-K. Zhang, K.-Y. Lam, L. Ma, H. Y.-S. Ngan, S. S. Liu and S.-W. Tsao, “Prevalence of HPV Infection in Esophageal Squamous Cell Carcinoma in Chinese Patients and Its Relationship to the p53 Gene Mutation,” International Journal of Cancer, Vol. 72, No. 6, 1997, pp. 959-964. doi:10.1002/(SICI)1097-0215(19970917)72:6<959::AID-IJC7>3.0.CO;2-O
[26] F. Kamangar, R. Malekzadeh, S. Dawsey and F. Saidi, “Esophageal Cancer in Northeastern Iran: A Review,” Archives of Iranian Medicine, Vol. 10, No. 1, 2007, pp. 70-82.
[27] S. Bai, S. Zhang and B. Li, “Primary Esophageal Adenocarcinoma,” Chinese Journal of Oncology, Vol. 11, No. 5, 1989, pp. 383-385.
[28] S. S. Liyanage, E. Segelov, S. M. Garland, S. N. Tabrizi, H. Seale, P. J. Crowe, D. E. Dwyer, A. Barbour, A. T. Newall, A. Malik, et al., “The Role of Human Papillomaviruses in Esophageal Squamous Cell Carcinoma,” Asia-Pacific Journal of Clinical Oncology, Vol. 9, No. 1, 2013, pp. 12-28.
[29] K. Syrjanen, “HPV Infections and Oesophageal Cancer,” Journal of Clinical Pathology, Vol. 55, No. 10, 2002, pp. 721-728. doi:10.1136/jcp.55.10.721
[30] L. Ke, “Mortality and Incidence Trends from Esophagus Cancer in Selected Geographic Areas of China circa 1970-90,” International Journal of Cancer, Vol. 102, No. 3, 2002, pp. 271-274. doi:10.1002/ijc.10706
[31] Y. Qin, L. Wang, Z. Fan, D. Kwong and X. Guan, “Comparative Genomic Hybridization Analysis of Genetic Aberrations Associated with Development of Esophageal Squamous Cell Carcinoma in Henan, China,” World Journal of Gastroenterology, Vol. 14, No. 12, 2008, pp. 1828-1835. doi:10.3748/wjg.14.1828
[32] C. Yang, “Research on Esophageal Cancer in China: A Review,” Cancer Research, Vol. 40, No. 8, 1980, pp. 2633-2644.
[33] X. Castellsagué, N. Munoz, E. De Stefani, C. Victora, R. Castelletto, P. Rolón and M. Quintana, “Independent and Joint Effects of Tobacco Smoking and Alcohol Drinking on the Risk of Esophageal Cancer in Men and Women,” International Journal of Cancer, Vol. 82, No. 5, 1999, pp. 657-664. doi:10.1002/(SICI)1097-0215(19990827)82:5<657::AID-IJC7>3.0.CO;2-C
[34] C. Han, G. Qiao, N. L. Hubbert, L. Li, C. Sun, Y. Wang, M. Yan, D. Xu, Y. Li, D. R. Lowy, et al., “Serologic Association Between Human Papillomavirus Type 16 Infection and Esophageal Cancer in Shaanxi Province, China,” Journal of the National Cancer Institute, Vol. 88, No. 20, 1996, pp. 1467-1471. doi:10.1093/jnci/88.20.1467
[35] J. Lagergren, Z. Wang, R. Bergstrom, J. Dillner and O. Nyren, “Human Papillomavirus Infection and Esophageal Cancer: A Nationwide Seroepidemiologic Case-Control Study in Sweden,” Journal of the National Cancer Institute, Vol. 91, No. 2, 1999, pp. 156-162. doi:10.1093/jnci/91.2.156
[36] C. Bosetti, C. La Vecchia, R. Talamini, L. Simonato, P. Zambon, E. Negri, D. Trichopoulos, P. Lagiou, R. Bardini and S. Franceschi, “Food Groups and Risk of Squamous Cell Esophageal Cancer in Northern Italy,” Journal of Cancer, Vol. 87, No. 2, 2000, pp. 289-294.
[37] G. Launoy, C. Milan, N. E. Day, M. P. Pienkowski, M. Gignoux and J. Faivre, “Diet and Squamous-Cell Cancer of the Oesophagus: A French Multicentre Case-Control Study,” International Journal of Cancer, Vol. 76, No. 1, 1998, pp. 7-12. doi:10.1002/(SICI)1097-0215(19980330)76:1<7::AID-IJC2>3.0.CO;2-4
[38] A. Ghavamzadeh, A. Moussavi, M. Jahani, M. Rastegarpanah and M. Iravani, “Esophageal Cancer in Iran,” Seminars in Oncology, Vol. 28, No. 2, 2001, pp. 153-157. doi:10.1016/S0093-7754(01)90086-7
[39] F. Islami, P. Boffetta, J.-S. Ren, L. Pedoeim, D. Khatib and F. Kamangar, “High-Temperature Beverages and Foods and Esophageal Cancer Risk—A Systematic Review,” International Journal of Cancer, Vol. 125, No. 3, 2009, pp. 491-524. doi:10.1002/ijc.24445
[40] F. Chang, S. Syrjanen, L. Wang and K. Syrjanen, “Infectious Agents in the Etiology of Esophageal Cancer,” Gastroenterology, Vol. 103, No. 4, 1992, pp. 1335-1348.
[41] V. Del, M. White, S. Enam, S. Oviedo, M. Bromer, R. Thomas, H. Parkman and K. Khalili, “Detection of JC Virus DNA Sequences and Expression of Viral T Antigen and Agnoprotein in Esophageal Carcinoma,” Cancer, Vol. 103, No. 3, 2005, pp. 516-527. doi:10.1002/cncr.20806
[42] M. Poljak, A. Cerar and K. Seme, “Human Papillomavirus Infection in Esophageal Carcinomas: A Study of 121 lesions Using Multiple Broad-Spectrum Polymerase Chain Reactions and Literature Review,” Human Pathology, Vol. 29, No. 3, 1998, pp. 266-271. doi:10.1016/S0046-8177(98)90046-6
[43] M. Selgrad, P. Malfertheiner, L. Fini, A. Goel, C. R. Boland and L. Ricciardiello, “The Role of Viral and Bacterial Pathogens in Gastrointestinal Cancer,” Journal of Cellular Physiology, Vol. 216, No. 2, 2008, pp. 378-388. doi:10.1002/jcp.21427
[44] M. Sur and K. Cooper, “The Role of the Human Papillomavirus in Esophageal Cancer,” Pathology, Vol. 30, No. 4, 1998, pp. 358-354. doi:10.1080/00313029800169616
[45] M. Tandi Matsha, R. Erasmus, A. Kafuko, D. Mugwanya, A. Stepien and M. I. Parker, “Human Papillomavirus Associated with Cancer,” Journal of Clinical Pathology, Vol. 55, No. 8, 2002, pp. 587-590. doi:10.1136/jcp.55.8.587
[46] K. Syrj?nen, “Histological Changes Identical to Those of Condylomatous Lesions Found in Esophageal Squamous Cell Carcinomas,” Archiv für Geschwulstforschung, Vol. 52, No. 4, 1982, pp. 283-292.
[47] L. Li, “Morbidity and Mortality of Malignant Tumours in Some Chinese Cities and Counties,” First Edition, People’s Medical Publishing House, Beijing, 2007.
[48] C. Hennekens and J. Buring, “Case-Control Studies,” In: S. M. Boston, Ed., Epidemiology in Medicine, First Edition, Little, Brown and Company, Toronto, 1987, pp. 132-152.
[49] R. Friis and T. Sellers, “Study Designs: Ecologic, Cross-Sectional, Case-Control,” In: Epidemiology for Public Health Practice, Fourth Edition, Jones and Bartlett Publishers, LLC, Sudbury, 2009, pp. 262-275.
[50] A. Dean, T. Arner, G. Sunki, R. Friedman, M. Lantinga, S. Sangam, J. Zubieta, K. Sullivan, K. Brendel, Z. Gao et al., “Epi Info, a Database and Statistics Program for Public Health Professionals,” 3.5.3 Edition, Centres for Diseas Control and Prevention (CDC), Atlanta, 2007.
[51] M. Mori, R. Shimono, T. Inoue, H. Kuwano, K. Sugimachi and R. Zhang, “Papillomavirus and esophageal cancer in the Japanese and Chinese,” The American Journal of Gastroenterology, Vol. 84, No. 9, 1989,pp. 1126-1127.
[52] G.-F. Gao, M. J. Roth, W.-Q. Wei, C. C. Abnet, F. Chen, N. Lu, F.-H. Zhao, X.-Q. Li, G.-Q. Wang, P. R. Taylor, et al., “No Association between HPV Infection and the Neoplastic Progression of Esophageal Squamous Cell Carcinoma: Result from a Cross-Sectional Study in a High-Risk Region of China,” International Journal of Cancer, Vol. 119, No. 6, 2006, pp. 1354-1359.
[53] S. Lu, F. Luo and H. Li, “Detection of Human Papillomavirus in Esophageal Squamous Cell Carcinoma and Adjacent Tissue Specimens in Linxian,” Chinese Journal of Oncology, 1995, Vol. 17, No. 5, pp. 321-324.
[54] C.-S. Song, J.-H. Cui, Z.-P. Wu, G. Yang and J.-J. Tan, “Relationship between Detection pf Human Papilloma Virus Genotypes and Esophageal Squamous Cell Carcinoma,” Chinese Journal of Cancer Prevention and Treatment, Vol. 16, No. 5, 2009, pp. 329-331.
[55] B. Cao, X. Tian, Y. Li, P. Jiang, T. Ning, H. Xing, Y. Zhao, C. Zhang, X. Shi, D. Chen, et al. , “LMP7/TAP2 Gene Polymorphisms and HPV Infection in Esophageal Carcinoma Patients from a High Incidence Area in China,” Carcinogenesis, Vol. 26, No. 7, 2005, pp. 1280-1284.
[56] B. Chen, “Polymerase Chain Reaction in Detection of Human Papillomavirus DNA in Esophageal Carcinoma,” Chinese Medical Journal, Vol. 73, No. 11, 1993, pp. 667-669.
[57] B. Chen, H. Yin and N. Dhurandhar, “Detection of Human Papillomavirus DNA in Esophageal Squamous Cell Carcinomas by the Polymerase Chain Reaction Using General Consensus Primers,” Human Pathology, Vol. 25, No. 9, 1994, pp. 920-923.
[58] M. Dai, W. Zhang, G. Clifford, T. Gheit, B. He, K. Michael, T. Waterboer, P. Hainaut, M. Tommasino and S. Franceschi, “Human Papillomavirus Infection among 100 Oesophageal Cancer Cases in the People’s Republic of China,” International Journal of Cancer, Vol. 121, No. 6, 2007, pp. 1396-1398.
[59] E. de Villiers, D. Lavergne, F. Chang, K. Syrjanen, P. Tosi, M. Cintorino, R. Santopietro and S. Syrjanen, “An Interlaboratory Study to Determine the Presence of Human Papillomavirus DNA in Esophageal Carcinoma from China,” International Journal of Cancer, Vol. 81, No. 2, 1999, pp. 225-228.
[60] D. He, S. Tsao and H. Bu, “Human Papillomavirus Infection and Esophageal Squamous Cell Carcinoma,” Chinese Journal of Pathology, Vol. 25, No. 6, 1996, pp. 351-354.
[61] J. Koshiol, W. Q. Wei, A. R. Kreimer, W. Chen, P. Gravitt, J. S. Ren, C. C. Abnet, J. B. Wang, F. Kamangar, D. M. Lin, et al., “No Role for Human Papillomavirus in Esophageal Squamous Cell Carcinoma in China,” International Journal of Cancer, Vol. 127, No. 1, 2010, pp. 93-100.
[62] D. Lavergne and E. M. de Villiers, “Papillomavirus in Esophageal Papillomas and Carcinomas,” International Journal of Cancer, Vol. 80, No. 5, 1999, pp. 681-684.
[63] S. Li, Y. Li, L. Wang, X. Wu, L. Zhou, X. Zhao, H. Liu and Y. Zeng, “Detection of Human Papillomavirus in Tissues of Esophageal Carcinomas by Polymerase Chain Reaction,” Chinese Journal of Experimental and Clinical Virology, Vol. 22, No. 4, 2008, pp. 251-253.
[64] T. Li, Z. M. Lu, M. Guo, Q. J. Wu, K. N. Chen, H. P. Xing, Q. Mei and Y. Ke, “p53 Codon 72 Polymorphism (C/G) and the Risk of Human Papillomavirus-Associated Carcinomas in China,” Cancer, Vol. 95, No. 12, 2002, pp. 2571-2576.
[65] T. Li, Z.-M. Lu, K.-N. Chen, M. Guo, H.-P. Xing, Q. Mei, H.-H. Yang, J. F. Lechner and Y. Ke, “Human Papillomavirus Type 16 is an Important Infectious Factor in the High Incidence of Esophageal Cancer in Anyang Area of China,” Carcinogenesis, Vol. 22, No. 6, 2001, pp. 929-934.
[66] P. Liao, J. Qin, T. Zeng, F. Li, J. Cai and L. He, “A 1:2 Matched Case-Control Study on the Interaction of HPV16E6 and HLA-DR9 Allele to Esophageal Cancer in Kazakh Ethnicity, Xinjiang,” Chinese Journal of Epidemiology, Vol. 30, No. 9, 2009, pp. 951-954.
[67] M. Liu, H. Zeng, X. Zhang, J. Zhu, J. Huang, X. Zhang and M. Xia, “Study on Human Papillomavirus Infection and Loss of Heterozygosity of Microsatellite in Esophageal Cancer,” Chinese Journal of Epidemiology, Vol. 28, No. 12, 2007, pp. 1203-1206.
[68] Y. Liu, X. Li, G. Jin, X. Yan, J. Yang, J. Wang, Y. Li, F. Wang and X. Zhang, “HPV Detection and FHIT Expression in Esophageal Squamous Carcinoma from High Incidence Area in Cixian County,” Chinese Journal of Cancer, Vol. 22, No. 5, 2003, pp. 492-495.
[69] X. Lu, Y. Zhang, R. Lin, X. Liang, Y. Zhang, X. Wang, Y. Zhang, Y. Wang and H. Wen, “p53 Polymorphism in Human Papillomavirus-Associated Kazakh’s Esophageal Cancer in Xinjiang, China,” World Journal of Gastroenterology, Vol. 10, No. 19, 2004, pp. 2775-2778.
[70] X. M. Lu, S. Monnier-Benoit, L. Z. Mo, S. Y. Xu, J. L. Prétet, Z. Liu, D. A. Vuitton and C. Mougin, “Human Papillomavirus in Esophageal Squamous Cell Carcinoma of the High-Risk Kazakh Ethnic Group in Xinjiang, China,” European Journal of Surgical Oncology, Vol. 34, No. 7, 2008, pp. 765-770.
[71] Z. Lu, K. Chen and M. Guo, “Detection of HPV in Human Oesophageal Cancer in High Incidence Area and Its Correlation with p53 Expression,” Chinese Journal of Oncology, Vol. 23, No. 3, 2001, pp. 220-223.
[72] D. Peixoto Guimaraes, S. Hsin Lu, P. Snijders, R. Wilmotte, R. Herrero, G. Lenoir, R. Montesano, C. J. L. M. Meijer, J. Walboomers and P. Hainaut, “Absence of Association between HPV DNA, TP53 Codon 72 Polymorphism, and Risk of Oesophageal Cancer in a High-Risk Area of China,” Cancer Letters, Vol. 162, No. 2, 2001, pp. 231-235.
[73] Z. Y. Shen, S. P. Hu, L. C. Lu, C. Z. Tang, Z. S. Kuang, S. P. Zhong and Y. Zeng, “Detection of Human Papillomavirus in Esophageal Carcinoma,” Journal of Medical Virology, Vol. 68, No. 3, 2002, pp. 412-416.
[74] K. Shuyama, A. Castillo, F. Aguayo, Q. Sun, N. Khan, C. Koriyama and S. Akiba, “Human Papillomavirus in High- and Low-Risk Areas of Oesophageal Squamous Cell Carcinoma in China,” British Journal of Cancer, Vol. 96, No. 10, 2007, pp. 1554-1559.
[75] H. Si, S. Tsao, C. Poon and A. Cheung, “Human Papillomavirus Infection and Loss of Heterozygosity in Esophageal Squamous Cell Carcinoma,” Cancer Letter, Vol. 213, No. 2, 2004, pp. 231-239.
[76] H. X. Si, S. W. Tsao, C. S. P. Poon, L. D. Wang, Y. C. Wong and A. L. Cheung, “Viral Load of HPV in Esophageal Squamous Cell Carcinoma,” International Journal of Cancer, Vol. 103, No. 4, 2003, pp. 496-500.
[77] L. Suzuk, A. Noffsinger, Y. Hui and C. Fenoglio-Preiser, “Detection of Human Papillomavirus in Esophageal Squamous Cell Carcinoma,” Cancer, Vol. 78, No. 4, 1996, pp. 704-710.
[78] W. Xu, L. Zhang, Z. Lu, J. Li, Y. Ke and G. Xu, “Detection of Human Papillomavirus Type 16 E6 mRNA in Carcinomas of the Upper Digestive Tract,” Chinese Medical Journal, Vol. 83, No. 21, 2003, pp. 1910-1914.
[79] X. Zhao, S. Li, Y. Li, X. Wang, Y. Li, X. Wu, L. Zhou, H. Liu and Y. Zeng, “Detection of Human Papillomavirus in Esophageal Carcinoma Tissues from Baoding City of Hebei Province,” Chinese Journal of Experimental and Clinical Virology, Vol. 23, No. 2, 2009, pp. 91-93.
[80] X. Zhou, M. Guo, L. Quan, W. Zhang, Z. Lu, Q. Wang, Y. Ke and N. Xu, “Detection of Human Papillomavirus in Chinese Esophageal Squamous Cell Carcinoma and Its Adjacent Normal Epithelium,” World Journal of Gastroenterology, Vol. 9, No. 6, 2003, pp. 1170-1173.
[81] Y. Zhou, Y. Pan, S. Zhang, X. Shi, T. Ning and Y. Ke, “Increased Phosphorylation of p70 S6 Kinase is Associated with HPV16 Infection in Cervical Cancer and Esophageal Cancer,” British Journal of Cancer, Vol. 97, No. 2, 2007, pp. 218-222.
[82] F. Chang, S. Syrj?nen, Q. Shen, M. Cintorino, R. Santopietro, P. Tosi and K. Syrj?nen, “Detection of HPV DNA in Esophageal Squamous Cell Carcinoma from the High Incidence Area of Linxian, China,” Scandinavian Journal of Gastroenterology, Vol. 35, No. 2, 2000, pp. 123-130.
[83] J. Chen, Y. Zhou, J. Li and P. Wu, “Effect of HPV16 Infection on the Esophageal Carcinoma and the Gene Expressions of p53 and p16,” China Journal of Laboratory Diagnosis, Vol. 8, No. 2, 2004,pp. 182-185.
[84] L. Chen, L. Yang, Z. Sun, H. Zhang, T. Ren, B. Chang, L. Pang, Y. Qi, H. Li, J. Jiang, et al., “Correlation between HPV16 and Esophageal Cancer of Kazakh People in Xinjiang,” Journal of Nongken Medicine, Vol. 30, No. 1, 2008, pp. 15-22.
[85] M. Duan, R. Tian and X. Cao, “The Relationship between HPV and Esophageal Carcinoma,” Journal of Practical Medical Techniques, Vol. 14, No. 1A, 2005, pp. 11-12.
[86] L. Y. Gu, L. M. Sai, X. L. Hou, G. Chen, F. Li, C. X. Liu, Y. Z. Chen, B. Chang, L. Yang, W. H. Liang, et al. , “Correlation between HPV16 Infection and Esophageal Carcinoma of Kazakh People in Xinjiang,” China Oncology, Vol. 21, No. 9, 2010, pp. 668-672.
[87] B. He, G. Duan and L. Cai, “Study on the Relationship between High Risk HPV Infection and p53 Polymorphisms in Esophageal Cancer,” Strait Journal of Preventive Medicine, Vol. 13, No. 3, 2007, pp. 8-10.
[88] M. Liu, X. Zhang, W. Fu, J. Yang and X. Zhu, “Study of Association between HPV Infection and Squamous Cell Carinoma as well as Dysplastic Tissue of the Oesophagus,” China Journal of Modern Medicine, Vol. 18, No. 14, 2008, pp. 2084-2086.
[89] W. Liu, X. Jiang, M. Zhang and Z. Zhang, “The Relationship between HPV16 and Expression of Cyclooxygenase-2, P53 and Their Prognostic Roles in Esophageal Squamous Cell Carcinoma,” European Journal of Gastroenterology & Hepatology, Vol. 22, No. 1, 2010, pp. 67-74. doi:10.1097/MEG.0b013e32832c7e76
[90] X. Wang, X. Tian, F. Liu, Y. Zhao, M. Sun, D. Chen, C. Lu, Z. Wang, X. Shi, Q. Zhang, et al., “Detection of HPV DNA in Esophageal Cancer Specimens from Different Regions and Ethnic Groups: A Descriptive Study,” BMC Cancer, Vol. 10, No. 1, 2010, p. 19. doi:10.1186/1471-2407-10-19
[91] S. Zhou, I. Sheyhidin, T. Yang, L. Zhang, A. Hasim, X. Lu, M. Niyaz and T. Liu, “Relationship between Human Papillomavirus 16 and Esophageal Squamous Cell Carcinoma in Uygur Population in Xinjiang Uygur Autonomous Region,” World Chinese Journal of Digestology, 2009, Vol. 17, No. 31, pp. 3214-3217.
[92] M.-C. Cui, Y. Li, X. He, X.-L. Wang, L.-D. Wang and H.-S. Liu, “Study of Human Papillomavirus in Biospy Tissue Specimens of Esophageal Carcinomas in Linzhou City,” Chinese Journal of Experimental and Clinical Virology, Vol. 25, No. 1, 2011, pp. 39-41.
[93] A. Goto, C.-P. Li, S. Ota, T. Niki, Y. Ohtsuki, S. Kitajima, S. Yonezawa, C. Koriyama, S. Akiba, H. Uchima, et al. , “Human Papillomavirus Infection in Lung and Esophageal Cancers: Analysis of 485 Asian Cases,” Journal of Medical Virology, Vol. 83, No. 8, 2011, pp. 1383-1390. doi:10.1002/jmv.22150
[94] H. Kawaguchi, S. Ohno, K. Araki, M. Miyazaki, H. Saeki, M. Watanabe, S. Tanaka and K. Sugimachi, “p53 Polymorphism in Human Papillomavirus-Associated Esophageal,” Cancer Cancer Researchearch, Vol. 60, No. 2000, pp. 2753-2755.
[95] Q. Ma, H. Jiang, Y. Feng, X. Wang, Y. Zhou, K. Liu and Z. KJia, “Detection of Human Papillomavirus DNA in Squamus Cell Carcinoma of the Esophagus,” World Chinese Journal of Digestology, Vol. 8, No. 11, 2000, pp. 1218-1224.
[96] L. Yang, L. Chen, Z.-Z. Sun, H.-Y. Zhang, X.-Y. Tian, Y. Qi, J. Zhu, L. Yang, J.-M. Qin and F. Li, “Analysis of Human Papillomavirus DNA Infection in Kazakh Esophageal Carcinomas in Xinjiang Province,” World Chinese Journal of Digestology, Vol. 15, No. 9, 2007, pp. 2114-2119.
[97] G. Ding, L. Wang, S.-H. Li, C. Feng, Y.-R. Zhang, J.-L. Ren, Z. Fan, R. Wang, X. He and T. Guo, “Correlation between Papillomavirus Infection and Esophageal Squamous Cell Carcinoma and Gastric Adenocarcinoma in High-Incidence Area of Henan Province,” Chinese Journal of Cancer Prevention and Treatment, Vol. 16, No. 4, 2009, pp. 252-255.
[98] G.-C. Ding, J.-L. Ren, F.-B. Chang, J.-L. Li, L. Yaun, X. Song, S.-L. Zhou, T. Guo, Z.-M. Fa, Y. Zeng, et al., “Human Papillomavirus DNA and p16 INK4A Expression in Concurrent Esophageal and Gastric Cardia Cancers,” World Journal of Gastroenterology, Vol. 16, No. 46, 2010, pp. 5901-5906. doi:10.3748/wjg.v16.i46.5901
[99] D. Zhang, Q. Zhang, L. Zhou, L. Huo, Y.-R. Zhang, Z. Shen and Y. Zhu, “Comparison of Prevalence, Viral Load, Physical Status and Expression of Human Papillimavirus-16, -18 and -58 in Esophageal and Cervical Cancer: A Case-Control Study,” BMC Cancer, Vol. 10, No. 650, 2010, p. 650. doi:10.1186/1471-2407-10-650
[100] C. Xu, X. Qian, X. Zhou, Q. Zhao and Y. Li, “Expression HPV 16-E6 and E7 Oncoproteins in Squamous Cell Carcinoma Tissues of Esophageal Cancer and Non-Cancer Tissues,” Chinese Journal of Oncology, Vol. 23, No. 2, 2004, pp. 165-168.
[101] J. Liu, S. Qin and W. Zhang, “Relationship between HPVE6 p53 Protein and Esophageal Squamous Cell Carcinoma,” World Chinese Journal of Digestology, Vol. 8, No. 5, 2000, pp. 494-496.
[102] F. Chang, S. Syrj?nen, Q. Shen, H. Ji and K. Syrj?nen, “Human Papillomavirus (HPV) DNA in Esophageal Precancer Lesions and Squamous Cell Carcinomas from China,” International Journal of Cancer, Vol. 45, No. 1, 1990, pp. 21-25. doi:10.1002/ijc.2910450106
[103] Y. Li, G. Huang, H. Xiao, Y. Huang, T. Mao and W. Deng, “The Status of Human Papillomavirus 16 DNA in the Tissues of Human Esophagus Carcinoma,” Journal of West China University of Medical Sciences, Vol. 22, No. 2, 1991, pp. 157-160.
[104] J. Li, Y. Zhang and D. Gao, “Study on the Interrelationship between Human Papilloma Virus Infection and Langerhans Cells in Carcinogenesis of Esophagus,” Chinese Journal of Pathology, Vol. 25, No. 2, 1996, pp. 83-85.
[105] F. Chang, S. Syrj?nen, L. Wang, Q. Shen and K. Syrj?nen, “p53 Overexpression and Human Papillomavirus (HPV) Infection in Oesophageal Squamous Cell Carcinomas Derived from a High-Incidence Area in China,” AntiCancer Researchearch, Vol. 17, No. 1B, 1997, pp. 709-715.
[106] L. Zhu, X. Su, K. Chen, R. Yang, H. Xing, J. Cui and Y. Ke, “Detection Rate of Human Papillomavirus-16 in Esophageal Squamous Cell Carcinoma from Different Chinese Populations,” Chinese Journal of Cancer, Vol. 24, No. 7, 2005, pp. 870-873.
[107] P. Yao, G. Li, J. Li, H. Xia, X. Yang, H. Huang, Y. Fu, R. Wang, X. Wang and J. Sha, “Evidence of Human Papilloma Virus Infection and Its Epidemiology in Esophageal Squamous Cell Carcinoma,” World Journal of Gastroenterology, Vol. 12, No. 9, 2006, pp. 1352-1355.
[108] F. Chang, S. Syrjanen, Q. Shen, L. Wang and K. Syrjanen, “Screening for Human Papillomavirus Infections in Esophageal Squamous Cell Carcinomas by in Situ Hybridization,” Cancer, Vol. 72, No. 9, 1993, pp. 2525-2530. doi:10.1002/1097-0142(19931101)72:9<2525::AID-CNCR 2820720902>3.0.CO;2-L
[109] P. Zhou, X.-Z. Wang, Z.-L. Zhu, J. Liu and X. Li, “Expression of HPV16/18 in Esophageal Squamous Carcinoma in Taixing Area,” Journal of China Medical University, Vol. 40, No. 2, 2011, pp. 172-174.
[110] L. Jin and Q. Cao, “Expression and Effect of Human Papillomavirus in Esophageal Carcinoma,” Chinese Journal of Gastroenterology, Vol. 12, No. 1, 2007, pp. 36-39.
[111] Z. X. Qi, X. Xu, B. Zhang, M. Du, H. Yang, L. Zheng, J. Li and Z. Shen, “Relationship between HPV 16/18 and p53, p21WAF1, MDM2, Ki67 and Cyclin D1 Expression in Esophageal Squamous Cell Carcinoma: Comparative Study by Using Tissue Microarray Technology,” Experimental Oncology, Vol. 28, No. 3, 2006, pp. 235-240.
[112] P. O. Fidalgo, M. L. Cravo, P. P. Chaves, C. N. Leitao and F. C. Mira, “High Prevalence of Human Papillomavirus in Squamous Cell Carcinoma and Matched Normal Esophageal Mucosa. Assessment by Polymerase Chain Reaction,” Cancer, Vol. 76, No. 9, 1995, pp. 1522-1528. doi:10.1002/1097-0142(19951101)76:9<1522::AID-CNCR2820760904>3.0.CO;2-3
[113] T. Kahn, E. Schwarz and H. zur Hausen, “Molecular Cloning and Characterization of the DNA of a New Human Papillomavirus (HPV 30) from a Laryngeal Carcinoma,” International Journal of Cancer, Vol. 37, No. 1, 1986, pp. 61-65. doi:10.1002/ijc.2910370111
[114] V. Furrer, M. Benitez, M. Furnes, H. Lanfranchi and N. Modesti, “Biopsy vs. Superficial Scraping: Detection of Human Papillomavirus 6, 11, 16, and 18 in Potentially Malignant and Malignant Oral Lesions,” Journal of Oral Pathology & Medicine, Vol. 35, No. 6, 2006, pp. 338-344. doi:10.1111/j.1600-0714.2006.00423.x
[115] HPV Vaccination, “Should it be Recommended or Required?” Rapid Public Health Policy Response Project, Jacobs Institute of Women’s Health, School of Public Health and Health Services, The George Washington University, Washington DC, 2007.
[116] J. Li, L. Li, J. Ma, L. Wei, M. Niyazi, C. Li, A. Xuh, J. Wanga, H. Lianga and J. Belinsoni, et al., “Knowledge and Attitudes about Human Papillomavirus (HPV) and HPV Vaccines among Women Living in Metropolitan and Rural Regions of China,” Vaccine, Vol. 27, No. 8, 2009, pp. 1210-1215. doi:10.1016/j.vaccine.2008.12.020
[117] J. Shi, Y. Qiao, J. Smith, B. Dondog, Y. Bao, M. Dai, G. Clifford and S. Franceschi, “Epidemiology and Prevention of Human Papillomavirus and Cervical Cancer in China and Mongolia,” Vaccine, Vol. 26S, No. 12, 2008, pp. M53-M59. doi:10.1016/j.vaccine.2008.05.009
[118] http://www.merck.com/newsroom/press_releases/product/2006_0608.html
[119] M. Chang, S. You, C. Chen, C. Liu, C. Lee, S. Lin, H. Chu, T. Wu, S. Yang, H. Kuo, et al., “Decreased Incidence of Hepatocellular Carcinoma in Hepatitis B Vaccinees: A 20-Year Follow-Up Study,” Journal of the National Cancer Institute, Vol. 101, 2009, pp. 1348-1355. doi:10.1093/jnci/djp288
[120] H. Chen, M. Chang, Y. Ni, H. Hsu, P. Lee, C. Lee and D. Chen, “Seroepidemiology of Hepatitis B Virus Infection in Children: Ten Years of Mass Vaccination in Taiwan,” Journal of the American Medical Association, Vol. 276, No. 11, 1996, pp. 906-908. doi:10.1001/jama.1996.03540110060032
[121] M. Campo, “Papillomas and Cancer in Cattle,” Cancer Survivors, Vol. 6, No. 1, 1987, pp. 39-54.
[122] D. Xing, W. Tan and D. Lin, “Genetic Polymorphisms and Susceptibility to Esophageal Cancer among Chinese Population,” Oncology Reports, Vol. 10, No. 5, 2003, pp. 1615-1623.
[123] F. Chang, S. Syrjanen, Q. Shen, M. Cintorino, R. Santopietro, P. Tosi and K. Syrjanen, “Evaluation of HPV, CMV, HSV and EBV in Esophageal Squamous Cell Carcinomas from a High-Incidence Area of China,” AntiCancer Research, Vol. 20, No. 5C, 2000, pp. 3935-3940.
[124] X. Wang, X. Tian, F. Liu, Y. Zhao, M. Sun, D. Chen, C. Lu, Z. Wang, X. Shi, Q. Zhang, et al., “Detection of HPV DNA in Esophageal Cancer Specimens from Different Regions and Ethnic Groups: A Descriptive Study,” BMC Cancer, Vol. 10, No. 19, 2010, p. 19.

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