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REVIEW ARTICLE

Geographic origin is a significant determinant of human papillomavirus prevalence in oesophageal squamous cell carcinoma: Systematic review and meta-analysis

Pages 1-18 | Received 23 Mar 2012, Accepted 05 Jun 2012, Published online: 25 Jul 2012

References

  • IARC monographs on the evaluation of carcinogenic risks to humans. Volume 64. Papillomaviruses. Lyon: IARC; 1995.
  • zur Hausen H. Papillomaviruses in the causation of human cancers—a brief historical account. Virology 2009;384: 260–5.
  • Syrjänen S, Syrjänen K. The history of papillomavirus research. Cent Eur J Public Health 2008;16(Suppl):S7–13.
  • Syrjänen K, Syrjänen S. Papillomavirus infections in human pathology. New York: Wiley & Sons; 2000. pp 1–615.
  • Coelho FR, Soares FA, Focchi J, Fregnani JH, de Andrade JM, Zeferino LC, . Câncer do colo do útero. Sao Paulo, Brazil: Tecmedd Editora; 2008. pp 1–678.
  • Syrjänen KJ. HPV infections and lung cancer. J Clin Pathol 2002;55:885–91.
  • Syrjänen KJ. HPV infections in benign and malignant sinonasal lesions. J Clin Pathol 2003;56:174–81.
  • Syrjänen KJ. Annual disease burden due to human papillomavirus (HPV) 6 and 11 infections in Finland. Scand J Infect Dis Suppl 2009;107:3–32.
  • Syrjänen KJ. Annual disease burden due to human papillomavirus (HPV) 16 and 18 infections in Finland. Scand J Infect Dis Suppl 2009;108:2–32.
  • Syrjänen KJ, Pyrhönen S, Syrjänen SM, Lamberg MA. Immunohistochemical demonstration of human papilloma virus (HPV) antigens in oral squamous cell lesions. Brit J Oral Surg 1983;21:147–53.
  • Syrjänen KJ, Pyrhönen S, Aukee S, Koskela E. Squamous cell papilloma of the oesophagus: a tumour probably caused by Human papilloma virus (HPV). Diagn Histopathol 1982;5:291–6.
  • Syrjänen KJ. Histological changes identical to those of condylomatous lesions found in esophageal squamous cell carcinomas. Arch Geschwulstforsch 1982;52:283–92.
  • Goldsmith MF. Papillomavirus invades esophagus, incidence seems to be increasing. JAMA 1984;251:2185–7.
  • Morris H, Price S. Langerhans’ cells, papillomaviruses and oesophageal carcinoma. A hypothesis. S Afr Med J 1986;69: 413–7.
  • Brooks LA, Steyn LM, Renan MJ. Oesophageal carcinoma. Search for a possible viral aetiology using molecular hybridisation techniques. S Afr Med J 1987;Suppl:6–8.
  • Syrjänen KJ. Human papillomavirus (HPV) infections and their associations with squamous cell neoplasia. Arch Geschwulstforsch 1987;57:417–44.
  • Syrjänen K, Chang F, Syrjänen S. Infectious agents as etiological factors in esophageal carcinogenesis. In: Tahara E, Sugimachi K, Oohara T, editors. Recent advances in gastroenterological carcinogenesis. Bologna: Monduzzi Editore; 1996. pp 29–43.
  • Syrjänen K. HPV infections of the oesophagus. In: Syrjänen K, Syrjänen S, editors. Papillomavirus infections in human pathology. New York: J. Wiley & Sons; 2000. pp 413–28.
  • Togawa Z, Rustgi AK. Human papillomavirus and esophageal squamous cell carcinoma. Gastroenterology 1995;108: 1605–6.
  • Poljak M, Cerar A, Seme K. Human papillomavirus infection in esophageal carcinomas: a study of 121 lesions using multiple broad-spectrum polymerase chain reactions and literature review. Hum Pathol 1998;29:266–71.
  • Matsha T, Erasmus R, Kafuko AB, Mugwanya D, Stepien A, Parker MI. Human papillomavirus associated with oesophageal cancer. J Clin Pathol 2002;55: 587–90.
  • Syrjänen K. HPV infections and oesophageal cancer. J Clin Pathol 2002;55:721–8.
  • Syrjänen KJ. HPV et tumeurs épidermoïdes bénignes et malignes de l’æsophage. Chapter 37. In: Aubin F, Pretet JL, Mougin C, editors. Papillomavirus humains. Biologie et pathologie tumorale. Paris: Editions TEC & DOC; 2003. pp 523–48.
  • Syrjänen K. HPV and oesophageal cancer. Chapter 15. In: Campo S, editor. Papillomavirus research: from natural history to vaccines and beyond. Norwich, UK: Caister Academic Press; 2006. pp 229–53.
  • Monk BJ, Tewari KS. The spectrum and clinical sequelae of human papillomavirus infection. Gynecol Oncol 2007;107:S6–13.
  • Syrjänen KJ. Human papillomavirus (HPV) involvement in esophageal carcinogenesis. New York, USA: Nova Science Publishing; 2010. pp 1–96.
  • Hardy RJ, Thompson SG. Detecting and describing heterogeneity in meta-analysis. Stat Med 1998;17:841–56.
  • Sterne JA, Gavaghan D, Egger M. Publication and related bias in meta-analysis: power of statistical tests and prevalence in the literature. J Clin Epidemiol 2000;53:1119–29.
  • Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics 1994;50: 1088–101.
  • Egger M, Davey SG, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997;315: 629–34.
  • Duval S, Tweedie R. Trim and fill: a simple funnel- plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics 2000;56:455–63.
  • Thompson SG, Sharp SJ. Explaining heterogeneity in meta-analysis: a comparison of methods. Stat Med 1999;18: 2693–708.
  • Hille JJ, Margolius KA, Markowitz S, Isaacson C. Human papillomavirus infection related to oesophageal carcinoma in black South Africans. A preliminary study. S Afr Med J 1986;69:417–20.
  • Hale MJ, Liptz TR, Paterson AC. Association between human papillomavirus and carcinoma of the oesophagus in South African blacks. A histochemical and immunohistochemical study. S Afr Med J 1989;76:329–30.
  • Matos M, Golindano C, Guirola E, Wright H, Capozzolo N, Nishimura M. Esophageal lesions caused by human papillomaviruses (HPV). G E N 1990;44:377–84.
  • Chang F, Syrjänen S, Shen Q, Ji HX, Syrjänen K. Human papillomavirus (HPV) DNA in esophageal precancer lesions and squamous cell carcinomas from China. Int J Cancer 1990;45:21–5.
  • Hippeläinen M, Eskelinen M, Lipponen P, Chang F, Syrjänen K. Mitotic activity index, volume corrected mitotic index and human papilloma-virus suggestive morphology are not prognostic factors in carcinoma of the oesophagus. Anticancer Res 1993;13:677–81.
  • Mori M, Shimono R, Inoue T, Kuwano H, Sugimachi K, Zhang RG. Papillomavirus and esophageal cancer in the Japanese and Chinese. Gastroenterology 1989;84:1126–7.
  • Nakamura T, Ide H, Eguchi IR, Hayashi K, Hanyu F, Nagasako K. Expression of p53 protein related to human papillomavirus and DNA ploidy in superficial esophageal carcinoma. Surg Today 1995;25:591–7.
  • van Cutsem E, Snoeck R, Van Ranst M, Fiten P, Opdenakker G, Geboes K, . Successful treatment of a squamous papilloma of the hypopharynx-esophagus by local injections of (S)-1-(3-hydroxy-2-phosphonylmethoxypropyl) cytosine. J Med Virol 1995;45:230–5.
  • Kuwano H, Sumiyoshi K, Sonoda K, Kitamura K, Toh Y, Nakashima H, Sugimachi K. Pathogenesis of esophageal squamous cell carcinoma with lymphoid stroma. Hepatogastroenterology 2001;48:458–61.
  • Xu CL, Qian XL, Zhou XS, Zhao QZ, Li YC. Expression of HPV16-E6 and E7 oncoproteins in squamous cell carcinoma tissues of esophageal cancer and non-cancer tissues. Ai Zheng 2004;23:165–8.
  • Yao PF, Li GC, Li J, Xia HS, Yang XL, Huang HY. Evidence of human papilloma virus infection and its epidemiology in esophageal squamous cell carcinoma. World J Gastroenterol 2006;12:1352–5.
  • Kulski J, Demeter T, Sterret GF, Shilkin KB. Human papillomavirus DNA in esophageal carcinoma. Lancet 1986;2:683–4.
  • Chang F, Shen Q, Zhou J, Wang C, Wang D, Syrjänen S, Syrjänen K. Detection of human papillomavirus DNA in cytologic specimens derived from esophageal precancer lesions and cancer. Scand J Gastroenterol 1990;25: 383–8.
  • Kulski JK, Demeter T, Mutavdzic S, Sterrett GF, Mitchell KM, Pixley EC. Survey of histologic specimens of human cancer for human papillomavirus types 6/11/16/18 by filter in situ hybridization. Am J Clin Pathol 1990;94: 566–70.
  • Loke SL, Ma L, Wong M, Srivastava G, Lo I, Bird CC. Human papillomavirus in oesophageal squamous cell carcinoma. J Clin Pathol 1990;43:909–12.
  • Benamouzig R, Pigot F, Quiroga G, Dalidire P, Chaussade S, Catalan F. Human papillomavirus infection in esophageal squamous cell carcinoma in Western countries. Int J Cancer 1992;50:549–52.
  • Li Y, Huang G, Xiao H, Huang Y, Mao T, Deng W. The status of human papillomavirus 16 DNA in the tissues of human esophagus carcinoma. Hua His I Ko Ta Hsueh Pao 1991;22:157–60.
  • Chang F, Syrjänen S, Shen Q, Wang L, Wang D, Syrjänen K. Human papillomavirus (HPV) involvement in esophageal precancer lesions and squamous cell carcinomas as evidenced by microscopy and different DNA techniques. Scand J Gastroenterol 1992;27:553–63.
  • Lu S, Luo F, Li H. Detection of human papilloma virus in esophageal squamous cell carcinoma and adjacent tissue specimens in Linxian. Zhonghua Zhong Liu Za Zhi 1995;17:321–4.
  • He D, Tsao SW, Bu H. Human papillomavirus infection and esophageal squamous cell carcinoma. Zhonghua Bing Li Xue Za Zhi 1996;25:351–4.
  • Ashworth MT, McDicken IW, Southern SA, Nash JR. Human papillomavirus in squamous cell carcinoma of the oesophagus associated with tylosis. J Clin Pathol 1993;46:573–5.
  • Chang F, Syrjänen S, Shen Q, Wang L, Syrjänen K. Screening for human papillomavirus infections in esophageal squamous cell carcinomas by in situ hybridization. Cancer 1993;72:2525–30.
  • van Rensburg EJ, Venter EH, Simson IW. Human papillomavirus DNA in aerodigestive squamous carcinomas demonstrated by means of in situ hybridization. S Afr Med J 1993;83:516–8.
  • Furihata M, Ohtsuki Y, Ogoshi S, Takahashi A, Tamiya T, Ogata T. Prognostic significance of human papillomavirus genomes (type 16, 18) and aberrant expression of p53 protein in human esophageal cancer. Int J Cancer 1993;54: 226–30.
  • Ono H, Takahashi A, Ogoshi S, Furihata M, Ohtsuki Y. Relationship between h-ras p21 product and p53 protein or high-risk human papillomaviruses in esophageal cancer from Kochi, Japan. Am J Gastroenterol 1994;89:646–7.
  • Cooper K, Taylor L, Govind S. Human papillomavirus DNA in oesophageal carcinomas in South Africa. J Pathol 1995;175:273–7.
  • Li J, Zhang Y, Gao D. Study on the interrelationship between human papilloma virus infection and Langerhans cell in carcinogenesis of esophagus. Zhonghua Bing Li Xue Za Zhi 1996;25:83–5.
  • Woo YJ, Yoon HK. In situ hybridization study on human papillomavirus DNA expression in benign and malignant squamous lesions of the esophagus. J Korean Med Sci 1996;11:467–73.
  • Chang F, Syrjänen S, Wang L, Shen Q, Syrjänen K. p53 over-expression and human papillomavirus (HPV) infection in oesophageal squamous cell carcinomas derived from a high-incidence area in China. Anticancer Res 1997;17:709–15.
  • Agarwal SK, Chatterji A, Bhambhani S, Sharma BK. Immunohistochemical co-expression of human papillomavirus type 16/18 transforming (E6) oncoprotein and p53 tumour suppressor gene proteins in oesophageal cancer. Indian J Exp Biol 1998;36:559–63.
  • Takahashi A, Ogoshi S, Ono H, Ishikawa T, Toki T, Ohmori N, . High-risk human papillomavirus infection and overexpression of p53 protein in squamous cell carcinoma of the esophagus from Japan. Dis Esophag 1998;11:162–7.
  • Chang F, Syrjänen S, Shen Q, Cintorino M, Santopietro R, Tosi P, Syrjänen K. Detection of HPV DNA in oesophageal squamous cell carcinoma from the high-incidence area of Linxian, China. Scand J Gastroenterol 2000;35: 123–30.
  • Zhu LZ, Su XL, Chen KN, Yang RJ, Xing HP, Cui JG. Detection rate of human papillomavirus-16 in esophageal squamous cell carcinoma from different Chinese populations. Ai Zheng 2005;24:870–3.
  • De Petris G, Lewin M, Shoji T. Carcinoma cuniculatum of the esophagus. Ann Diagn Pathol 2005;9:134–8.
  • Qi ZL, Huo X, Xu XJ, Zhang B, Du MG, Yang HW. Relationship between HPV16/18 E6 and 53, 21WAF1, MDM2, Ki67 and cyclin D1 expression in esophageal squamous cell carcinoma: comparative study by using tissue microarray technology. Exp Oncol 2006;28:235–40.
  • Yao PF, Li GC, Li J, Xia HS, Yang XL, Huang HY. Evidence of human papilloma virus infection and its epidemiology in esophageal squamous cell carcinoma. World J Gastroenterol 2006;12:1352–5.
  • Kiyabu MT, Shibata D, Arnheim N, Martin WJ, Fitzgibbons PL. Detection of human papillomavirus in formalin-fixed, invasive squamous cell carcinoma using polymerase chain reaction. Am J Surg Pathol 1989;13:221–4.
  • Williamson AL, Jaskiesicz K, Gunning A. The detection of human papillomavirus in oesophageal lesions. Anticancer Res 1991;11:263–5.
  • Kim WH, Song SY, Kang JK, Park IS, Choi HJ. Detection of human papillomavirus DNA from esophageal cancer tissue using polymerase chain reaction. Gastroenterology 1991;100:A1272.
  • Toh Y, Kuwano H, Tanaka S, Baba K, Matsuda H, Sugimachi K, Mori R. Detection of human papillomavirus DNA in esophageal carcinoma in Japan by polymerase chain reaction. Cancer 1992;70:2234–8.
  • Chang F, Syrjänen S, Shen Q, Wang L, Wang D, Syrjänen K. Human papillomavirus (HPV) involvement in esophageal precancer lesions and squamous cell carcinomas as evidenced by microscopy and different DNA techniques. Scand J Gastroenterol 1992;27:553–63.
  • Chen BF. Polymerase chain reaction in detection of human papillomavirus DNA in esophageal carcinoma. Zhonghua Yi Xue Za Zhi 1993;73:667–9.
  • Poljak M, Cerar A. Human papillomavirus type 16 DNA in oesophageal squamous cell carcinoma. Anticancer Res 1993;13:2113–6.
  • Chen B, Yin H, Dhurandhar N. Detection of human papillomavirus DNA in esophageal squamous cell carcinomas by the polymerase chain reaction using general consensus primers. Hum Pathol 1994;25:920–3.
  • Lewensohn-Fuchs I, Munck-Wikland E, Berke Z, Magnusson KP, Pallesen G, Auer G, Lindholm J, Linde A, Aberg B, Rubio C. Involvement of aberrant p53 expression and human papillomavirus in carcinoma of the head, neck and esophagus. Anticancer Res 1994;14:1281–5.
  • Togawa K, Jaskiewicz K, Takahashi H, Meltzer SJ, Rustgi AK. Human papillomavirus DNA sequences in esophagus squamous cell carcinoma. Gastroenterology 1994;107:128–36.
  • Cooper K. p53 mutations in human papillomavirus- associated oesophageal squamous cell carcinoma. Br J Cancer 1995;72:1337.
  • Benamouzig R, Jullian E, Chang FJ, Robaskiewicz M, Flejou JF, Raoul JL. Absence of human papillomavirus DNA detected by polymerase chain reaction in French patients with esophageal carcinoma. Gastroenterology 1995;109:1876–81.
  • Akutsu N, Shirasawa H, Nakano K, Tanzawa H, Asano T, Kobayashi S. Rare association of human papillomavirus DNA with esophageal cancer in Japan. J Infect Dis 1995;171:425–8.
  • Hosone M, Ishiwata T, Nomura N, Kawanami O. A molecular pathological study on the localization of the human papillomavirus using nested PCR and in situ hybridization methods in paraffin embedded tissues. Nippon Ika Daigaku Zasshi 1995;62:131–41.
  • Sugimachi K, Sumiyoshi K, Nozoe T, Yasuda M, Watanabe M, Kitamura K, . Carcinogenesis and histogenesis of esophageal carcinoma. Cancer 1995;75:1440–5.
  • Shibagaki I, Tanaka H, Shimada Y, Wagata T, Ikenaga M, Imamura M. p53 mutation, murine double minute 2 amplification, and human papillomavirus infection are frequently involved but not associated with each other in esophageal squamous cell carcinoma. Clin Cancer Res 1995;1: 769–73.
  • Smits HL, Tjong-A-Hung SP, ter-Schegget J, Nooter K, Kok T. Absence of human papillomavirus DNA from esophageal carcinoma as determined by multiple broad spectrum polymerase chain reactions. J Med Virol 1995;46:213–5.
  • Fidalgo PO, Cravo ML, Chaves PP, Leitao CN, Mira FC. High prevalence of human papillomavirus in squamous cell carcinoma and matched normal esophageal mucosa: assessment by polymerase chain reaction. Cancer 1995;76: 1522–8.
  • Suzuk L, Noffsinger AE, Hui YZ, Fenoglio-Preiser CM. Detection of human papillomavirus in esophageal squamous cell carcinoma. Cancer 1996;78:704–10.
  • West AB, Soloway GN, Lizarraga G, Tyrrell L, Longley JB. Type 73 human papillomavirus in esophageal squamous cell carcinoma: a novel association. Cancer 1996;77: 2440–4.
  • Benamouzig R, Jullian E, Pompidou A, Rautureau J. Are human papillomaviruses involved in esophageal carcinogenesis?Head and Neck Cancer Adv Basic Res 1996;114: 391–5.
  • He D, Zhang DK, Lam KY, Ma L, Ngan HY, Liu SS, Tsao SW. Prevalence of HPV infection in esophageal squamous cell carcinoma in Chinese patients and its relationship to the p53 gene mutation. Int J Cancer 1997;72:959–64.
  • Kok TC, Nooter K, Tjong-A-Hung SP, Smits HL, Ter Schegget J. No evidence of known types of human papillomavirus in squamous cell cancer of the oesophagus in a low-risk area. Eur J Cancer 1997;33:1865–8.
  • Lam KY, He D, Ma L, Zhang D, Ngan HY, Wan TS, Tsao SW. Presence of human papillomavirus in esophageal squamous cell carcinomas in Hong Kong Chinese and its relationship with p53 gene mutation. Hum Pathol 1997;28: 657–63.
  • Miller BA, Davidson M, Myerson D, Icenogle J, Lanier AP, Tan J, Beckmann AM. Human papillomavirus type 16 DNA in esophageal carcinomas from Alaska natives. Int J Cancer 1997;71:218–22.
  • Mizobuchi S, Sakamoto H, Tachimori Y, Kato H, Watanabe H, Terada M. Absence of human papillomavirus-16 and -18 DNA and Epstein–Barr virus DNA in esophageal squamous cell carcinoma. Jpn J Clin Oncol 1997;27:1–5.
  • Morgan RJ, Perry ACF, Newcomb PV, Hardwick RH, Alderson D. Human papillomavirus and oesophageal squamous cell carcinoma in the UK. Eur J Surg Oncol 1997;23: 513–7.
  • Paz IB, Cook N, Odom-Maryon T, Xie Y, Wilczynski SP. Human papillomavirus (HPV) in head and neck cancer. An association of HPV 16 with squamous cell carcinoma of Waldeyer's tonsillar ring. Cancer 1997;79:595–604.
  • Rugge M, Bovo D, Busatto G, Parenti AR, Fawzy S, Guido M, . p53 alterations but no human papillomavirus infection in preinvasive and advanced squamous esophageal cancer in Italy. Cancer Epidemiol Biomarker Prev 1997;6:171–6.
  • Turner JR, Shen LH, Crum CP, Dean PJ, Odze RD. Low prevalence of human papillomavirus infection in esophageal squamous cell carcinomas from North America: analysis by a highly sensitive and specific polymerase chain reaction-based approach. Hum Pathol 1997;28:174–8.
  • Saegusa M, Hashimura M, Takano Y, Ohbu M, Okayasu I. Absence of human papillomavirus genomic sequences detected by the polymerase chain reaction in oesophageal and gastric carcinomas in Japan. Mol Pathol 1997;50:101–4.
  • Khurshid A, Kazuya N, Hanae I, Manabu I. Infection of human papillomavirus (HPV) and Epstein–Barr virus (EBV) and p53 expression in human esophageal carcinoma. J Pak Med Assoc 1998;48:138–42.
  • Lavergne D, de Villiers EM. Papillomavirus in esophageal papillomas and carcinomas. Int J Cancer 1999;80:681–4.
  • de Villiers EM, Lavergne D, Chang F, Syrjänen K, Tosi P, Cintorino M, . An interlaboratory study to determine the presence of human papillomavirus DNA in esophageal carcinoma from China. Int J Cancer 1999;81:225–8.
  • Wang LS, Chow KC, Wu YC, Li WY, Huang MH. Detection of Epstein–Barr virus in esophageal squamous cell carcinoma in Taiwan. Am J Gastroenterol 1999;94: 2834–9.
  • Talamini G, Capelli P, Zamboni G, Mastromauro M, Pasetto M, Castagnini A. Alcohol, smoking and papillomavirus infection as risk factors for esophageal squamous-cell papilloma and esophageal squamous-cell carcinoma in Italy. Int J Cancer 2000;86:874–8.
  • Kawaguchi H, Ohno S, Araki K, Miyazaki M, Saeki H, Watanabe M, . p53 polymorphism in human papillomavirus-associated esophageal cancer. Cancer Res 2000;60:2753–5.
  • Kamath AM, Wu TT, Heitmiller R, Daniel R, Shah KV. Investigation of the association of esophageal carcinoma with human papillomaviruses. Dis Esophag 2000;13: 122–4.
  • Lambot MA, Haot J, Peny MO, Fayt I, Noel JC. Evaluation of the role of human papillomavirus in oesophageal squamous cell carcinoma in Belgium. Acta Gastroenterol Belg 2000;63:154–6.
  • Lu Z, Chen K, Guo M. Detection of HPV in human esophageal cancer in high-incidence area and its correlation with p53 expression. Zhonghua Zhong Liu Za Zhi 2001;23: 220–3.
  • Peixoto-Guimaraes D, Hsin Lu S, Snijders P, Wilmotte R, Herrero R, Lenoir G, . Absence of association between HPV DNA, TP53 codon 72 polymorphism, and risk of oesophageal cancer in a high-risk area of China. Cancer Lett 2001;162:231–5.
  • Chang F, Syrjänen S, Shen Q, Cintorino M, Santopietro R, Tosi P, Syrjänen K. Presence of HPV, CMV, HSV and EBV in esophageal squamous cell carcinomas from a high- incidence area of China. Anticancer Res 2000;20: 3935–40.
  • Sobti RC, Kochar J, Singh K, Bhasin D, Capalash N. Telomerase activation and incidence of HPV in human gastrointestinal tumors in North Indian population. Mol Cell Biochem 2001;217:51–6.
  • Astori G, Merluzzi S, Arzese A, Brosolo P, de Pretis G, Maieron R, . Detection of human papillomavirus DNA and p53 gene mutations in esophageal cancer samples and adjacent normal mucosa. Digestion 2001;64:9–14.
  • Hasegawa M, Ohoka I, Yamazaki K, Hanami K, Sugano I, Nagao T, . Expression of p21/WAF-1, status of apoptosis and p53 mutation in esophageal squamous cell carcinoma with HPV infection. Pathol Int 2002;52:442–50.
  • Shen ZY, Hu SP, Lu LC, Tang CZ, Kuang ZS, Zhong SP, Zeng Y. Detection of human papillomavirus in esophageal carcinoma. J Med Virol 2002;68:412–6.
  • Awerkiew S, Bollschweiler E, Metzger R, Schneider PM, Holscher AH, Pfister H. Esophageal cancer in Germany is associated with Epstein–Barr virus but not with papillomaviruses. Med Microbiol Immunol (Berl) 2003;192:137–40.
  • Weston AC, Prolla JC. Association between esophageal squamous cell carcinoma and human papillomavirus detected by hybrid capture II assay. Dis Esophag 2003;16: 224–8.
  • Liu YL, Li XM, Jin GL, Yan X, Yang JZ, Wang JL, . HPV detection and FHIT expression in esophageal squamous carcinoma from high incidence area in Cixian County. Ai Zheng 2003;22:492–5.
  • Xu WG, Zhang LJ, Lu ZM, Li JY, Ke Y, Xu GW. Detection of human papillomavirus type 16 E6 mRNA in carcinomas of upper digestive tract. Zhonghua Yi Xue Za Zhi 2003;83: 1910–4.
  • Zhou XB, Guo M, Quan LP, Zhang W, Lu ZM, Wang QH, . Detection of human papillomavirus in Chinese esophageal squamous cell carcinoma and its adjacent normal epithelium. World J Gastroenterol 2003;9:1170–3.
  • Si HX, Tsao SW, Poon CS, Wang LD, Wong YC, Cheung AL. Viral load of HPV in esophageal squamous cell carcinoma. Int J Cancer 2003;103:496–500.
  • de Villiers EM, Gunst K, Stein H, Scherubl H. Esophageal squamous cell cancer in patients with head and neck cancer: prevalence of human papillomavirus DNA sequences. Int J Cancer 2004;109:253–8.
  • Acevedo-Nuno E, Gonzalez-Ojeda A, Vazquez-Camacho G, Balderas-Pena Luz MA, Moreno-Villa H, Montoya-Fuentes H. Human papillomavirus DNA and protein in tissue samples of oesophageal cancer, Barrett's oesophagus and oesophagitis. Anticancer Res 2004;24:1319–23.
  • Regragui A, Lakhdar H, Abderrahman Alaoui Balebbas M, Amrani M, Gamra L, Alaoui Belabbas M. Esophageal sarcomatoid carcinoma: report of a case with morphological, immunohistochemical and molecular study. Gastroenterol Clin Biol 2004;28:487–9.
  • Lu XM, Zhang YM, Lin RY, Liang XH, Zhang YL, Wang X. p53 polymorphism in human papillomavirus-associated Kazakh's esophageal cancer in Xinjiang, China. World J Gastroenterol 2004;10:2775–8.
  • White RE, Mungatana C, Mutuma G, Robert ME, Daniel RW, Topazian MD. Absence of human papillomavirus in esophageal carcinomas from southwestern Kenya. Dis Esophag 2005;18:28–30 .
  • Tampi C, Pai S, Doctor VM, Plumber S, Jagannath P. HPV-associated carcinoma of esophagus in the young: a case report and review of literature. Int J Gastrointest Cancer 2005;35:135–42.
  • Si HX, Tsao SW, Poon CS, Wong YC, Cheung AL. Physical status of HPV-16 in esophageal squamous cell carcinoma. J Clin Virol 2005;32:19–23.
  • Lyronis ID, Baritaki S, Bizakis I, Tsardi M, Spandidos DA. Evaluation of the prevalence of human papillomavirus and Epstein–Barr virus in esophageal squamous cell carcinomas. Int J Biol Markers 2005;20:5–10.
  • Liu WK, Chu YL, Zhang F, Chen P, Cheng F, Wang H. The relationship between HPV16 and expression of CD44v6, nm23H1 in esophageal squamous cell carcinoma. Arch Virol 2005;150:991–1001.
  • Liberale G, De Simone P, Snoeck R, Feron P, Gelin M, El Nakadi I. Verrucous carcinoma of the esophagus. A case report. Minerva Chir 2005;60:61–5.
  • Katiyar S, Hedau S, Jain N, Kar P, Khuroo MS, Mohanta J. p53 gene mutation and human papillomavirus (HPV) infection in esophageal carcinoma from three different endemic geographic regions of India. Cancer Lett 2005;218:69–79.
  • Farhadi M, Tahmasebi Z, Merat S, Kamangar F, Nasrollahzadeh D, Malekzadeh R. Human papillomavirus in squamous cell carcinoma of esophagus in a high-risk population. World J Gastroenterol 2005;11:1200–3.
  • Cao B, Tian X, Li Y, Jiang P, Ning T, Xing H. LMP7/TAP2 gene polymorphisms and HPV infection in esophageal carcinoma patients from a high incidence area in China. Carcinogenesis 2005;26:1280–4.
  • Baines JE, McGovern RM, Persing D, Gostout BS. Consensus-degenerate hybrid oligonucleotide primers (CODEHOP) for the detection of novel papillomaviruses and their application to esophageal and tonsillar carcinomas. J Virol Methods 2005;123:81–7.
  • Bahnassy AA, Zekri AR, Abdallah S, El-Shehaby AM, Sherif GM. Human papillomavirus infection in Egyptian esophageal carcinoma: correlation with p53, p21, mdm2, C-erbB2 and impact on survival. Pathol Int 2005;55: 53–62.
  • Souto Damin AP, Guedes Frazzon AP, de Carvalho Damin D, Beck Biehl H, Abruzzi de Oliveira L, Auler R. Detection of human papillomavirus DNA in squamous cell carcinoma of the esophagus by auto-nested PCR. Dis Esophag 2006;19:64–8.
  • Saravanan R, Youshya S, Campbell F, Ran H, Morris AI, Proby C. Unique expression of human papilloma virus type 5 and type 16 in esophageal squamous cell carcinoma—a case report. Am J Gastroenterol 2006;101:2423–6.
  • Gao GF, Roth MJ, Wei WQ, Abnet CC, Chen F, Lu N. 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. Int J Cancer 2006;119:1354–9.
  • Gabor B, Imdahl A, Gyorgy L, Pal O. HPV-infection in esophageal cancer as possible predictive factor after neoadjuvant therapy. Magy Seb 2006;59:97–104.
  • Dreilich M, Bergqvist M, Moberg M, Brattström D, Gustavsson I, Bergström S, . High-risk human papilloma virus (HPV) and survival in patients with esophageal carcinoma: a pilot study. BMC Cancer 2006;6:94–101.
  • Castillo A, Aguayo F, Koriyama C, Torres M, Carrascal E, Corvalan A. Human papillomavirus in esophageal squamous cell carcinoma in Colombia and Chile. World J Gastroenterol 2006;12:6188–92.
  • Zhou Y, Pan Y, Zhang S, Shi X, Ning T, Ke Y. Increased phosphorylation of p70 S6 kinase is associated with HPV16 infection in cervical cancer and esophageal cancer. Br J Cancer 2007;97:218–22.
  • Shuyama K, Castillo A, Aguayo F, Sun Q, Khan N, Koriyama C. Human papillomavirus in high- and low-risk areas of oesophageal squamous cell carcinoma in China. Br J Cancer 2007;96:1554–9.
  • Pantelis A, Pantelis D, Ruemmele P, Hartmann A, Hofstaedter F, Buettner R. p53 Codon 72 polymorphism, loss of heterozygosity and high-risk human papillomavirus infection in a low-incidence German esophageal squamous cell carcinoma patient cohort. Oncol Rep 2007;17: 1243–8.
  • Matsha T, Donninger H, Erasmus RT, Hendricks D, Stepien A, Parker MI. Expression of p53 and its homolog, p73, in HPV DNA positive oesophageal squamous cell carcinomas. Virology 2007;369:182–90.
  • Liu M, Zeng HC, Zhang XL, Zhu J, Huang JF, Zhang X. Study on human papillomavirus infection and loss of heterozygosity of microsatellite in esophageal cancer. Zhonghua Liu Xing Bing Xue Za Zhi 2007;28:1203–6.
  • Far AE, Aghakhani A, Hamkar R, Ramezani A, Pishbigar HF, Mirmomen S. Frequency of human papillomavirus infection in oesophageal squamous cell carcinoma in Iranian patients. Scand J Infect Dis 2007;39:58–62.
  • Dai M, Zhang WD, Clifford GM, Gheit T, He BC, Michael KM, . Human papillomavirus infection among 100 oesophageal cancer cases in the People's Republic of China. Int J Cancer 2007;121:1396–8.
  • Lu XM, Monnier-Benoit S, Mo LZ, Xu SY, Pretet JL, Lium Z. Human papillomavirus in esophageal squamous cell carcinoma of the high-risk Kazakh ethnic group in Xinjiang, China. Eur J Surg Oncol 2008;34:765–70.
  • Koh JS, Lee SS, Baek HJ, Kim YI. No association of high-risk human papillomavirus with esophageal squamous cell carcinomas among Koreans, as determined by polymerase chain reaction. Dis Esophag 2008;21:114–7.
  • Yang W, Zhang Y, Tian X, Ning T, Ke Y. p53 Codon 72 polymorphism and the risk of esophageal squamous cell carcinoma. Mol Carcinog 2008;47:100–4.
  • Bognar G, Imdahl A, Ledniczky G, Ondrejka P. Possible role of human papilloma virus infection in response to neoadjuvant therapy in patients with esophageal cancer. Hepatogastroenterology 2008;55:93–7.
  • Tornesello ML, Monaco R, Nappi O, Buonauguro L, Buonauguro FM. Detection of mucosal and cutaneous human papillomaviruses in oesophagitis, squamous cell carcinoma and adenocarcinoma of the oesophagus. J Clin Virol 2009;45:28–33.
  • Zhao XY, Li SY, Li Y, Wang XL, Li YL, Wu XZ. Detection of human papillomavirus in esophageal carcinoma tissues from Baoding City of Hebei Province. Zhonghua Shi Yan He Lin Chuang Bing Du Xue Za Zhi 2009;23:91–3.
  • Hussain S, Bharti AC, Salam I, Bhat MA, Mir MM, Hedau S, . Transcription factor AP-1 in esophageal squamous cell carcinoma: alterations in activity and expression during human papillomavirus infection. BMC Cancer 2009;9:329–34.
  • Herrera-Goepfert R, Lizano M, Akiba S, Carrillo-Garcia A, Becker-D’Acosta M. Human papilloma virus and esophageal carcinoma in a Latin-American region. World J Gastroenterol 2009;15:3142–7.
  • Erol D, Bulut Y, Yuce H, Ozercan IH. Investigation of the presence of human papillomavirus DNA in various gastrointestinal carcinoma samples. Mikrobiyol Bul 2009;43:259–68.
  • Bellizzi AM, Woodford RL, Moskaluk CA, Jones DR, Kozower BD, Stelow EB. Basaloid squamous cell carcinoma of the esophagus: assessment for high-risk human papillomavirus and related molecular markers. Am J Surg Pathol 2009;33:1608–14.
  • Zhang D, Zhang Q, Zhou L, Huo L, Zhang Y, Shen Z. Comparison of prevalence, viral load, physical status and expression of human papillomavirus-16, -18 and -58 in esophageal and cervical cancer: a case–control study. BMC Cancer 2010;10:650.
  • Wang X, Tian X, Liu F, Zhao Y, Sun M, Chen D. Detection of HPV DNA in esophageal cancer specimens from different regions and ethnic groups: a descriptive study. BMC Cancer 2010;10:19.
  • Tonna J, Palefsky JM, Rabban J, Campos GM, Theodore P, Ladabaum U. Esophageal verrucous carcinoma arising from hyperkeratotic plaques associated with human papilloma virus type 51. Dis Esophag 2010;23:E17–20.
  • Liu WK, Jiang XY, Zhang MP, Zhang ZX. The relationship between HPV16 and expression of cyclooxygenase-2, p53 and their prognostic roles in esophageal squamous cell carcinoma. Eur J Gastroenterol Hepatol 2010;22:67–74.
  • Koshiol J, Wei WQ, Kreimer AR, Chen W, Gravitt P, Ren JS, . No role for human papillomavirus in esophageal squamous cell carcinoma in China. Int J Cancer 2010;127:93–100.
  • Ding GC, Ren JL, Chang FB, Li JL, Yuan L, Song X. Human papillomavirus DNA and P16(INK4A) expression in concurrent esophageal and gastric cardia cancers. World J Gastroenterol 2010;16:5901–6.
  • Antonsson A, Nancarrow DJ, Brown IS, Green AC, Drew PA, Watson DI. High-risk human papillomavirus in esophageal squamous cell carcinoma. Cancer Epidemiol Biomarkers Prev 2010;19:2080–7.
  • Malik SM, Nevin DT, Cohen S, Hunt JL, Palazzo JP. Assessment of immunohistochemistry for p16INK4 and high-risk HPV DNA by in situ hybridization in esophageal squamous cell carcinoma. Int J Surg Pathol 2011;19: 31–4.
  • Zhang QY, Zhang DH, Shen ZY, Xu LY, Li EM, Au WW. Infection and integration of human papillomavirus in esophageal carcinoma. Int J Hyg Environ Health 2011;214: 156–61.
  • Wang WC, Wu TT, Chandan VS, Lohse CM, Zhang L. Ki-67 and ProExC are useful immunohistochemical markers in esophageal squamous intraepithelial neoplasia. Hum Pathol 2011;42:1430–7.
  • Hussain S, Singh N, Salam I, Bandil K, Yuvaraj M, Akbar BM. Methylation-mediated gene silencing of suppressor of cytokine signaling-1 (SOCS-1) gene in esophageal squamous cell carcinoma patients of Kashmir valley. J Recept Signal Transduct Res 2011;31:147–56.
  • Goto A, Li CP, Ota S, Niki T, Ohtsuki Y, Kitajima S. Human papillomavirus infection in lung and esophageal cancers: analysis of 485 Asian cases. J Med Virol 2011;83:1383–90.
  • Cui MC, Li Y, He X, Wang XL, Wang LD, Liu HT. Study of human papillomavirus in biopsy tissue specimens of esophageal carcinomas in Linzhou city. Zhonghua Shi Yan He Lin Chuang Bing Du Xue Za Zhi 2011;25:39–41.
  • Castillo A, Koriyama C, Higashi M, Anwar M, Bukhari MH, Carrascal E. Human papillomavirus in upper digestive tract tumors from three countries. World J Gastroenterol 2011;17:5295–304.
  • Landau M, Goldblum JR, Deroche T, Dumot J, Downs-Kelly E, Rice TW, . Esophageal carcinoma cuniculatum: report of 9 cases. Am J Surg Pathol 2012;36:8–17.
  • Doxtader EE, Katzenstein AL. The relationship between p16 expression and high-risk human papillomavirus infection in squamous cell carcinomas from sites other than uterine cervix: a study of 137 cases. Hum Pathol 2012;43:327–32.
  • Abdirad A, Eram N, Behzadi AH, Koriyama C, Parvaneh N, Akiba S. Human papillomavirus detected in esophageal squamous cell carcinoma in Iran. Eur J Intern Med 2012;23:e59–62.
  • Gupta N, Barwad A, Rajwanshi A, Kochhar R. Prevalence of human papillomavirus in esophageal carcinomas: a polymerase chain reaction-based study. Acta Cytol 2012;56:80–4.
  • Huedo-Medina T, Sanchez-Meca J, Marin-Martinez F, Botella J. Assessing heterogeneity in meta-analysis: Q statistic or I2 index? CHIP Documents. Paper 19. University of Connecticut; 2006. Available at: http://digitalcommons.uconn.edu/chip_docs/19 (accessed March 20, 2012).
  • Field AP. Meta-analysis of correlation coefficients: a Monte Carlo comparison of fixed- and random-effects methods. Psychol Methods 2001;6:161–80.
  • Field AP. The problems in using fixed-effects models of meta-analysis on real-world data. Understand Stat 2003;2: 77–96.
  • Cochran WG. The combination of estimates from different experiments. Biometrics 1954;10:101–29.
  • Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ 2003;327:557–60.
  • Sitas F, Egger S, Urban, MI, Taylor PR, Abnet CC, Boffetta P, on behalf of the InterSCOPE Collaboration. InterSCOPE study: associations between esophageal squamous cell carcinoma and human papillomavirus serological markers. J Natl Cancer Inst 2012;104:147–58.

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