Detection of human papillomavirus in lung cancer: Systematic review and meta-analysis

Anticancer Research

Volumn 32, Issue 8, 2012, Pages 3235-3250

  Syrjänen, Kari ^a,b  

^a TURKU UNIVERSITY HOSPITAL   (Finland)

^b BARRETOS CANCER HOSPITAL   (Brazil)

Author keywords

Adenocarcinoma; Bronchus; Detection method; Geographic region; HPV; Lung; Meta analysis; Meta regression; Publication bias; Review; Squamous cell carcinoma; Study heterogeneity

Indexed keywords

WART VIRUS VACCINE;

ADENOCARCINOMA; ADENOSQUAMOUS CARCINOMA; ANAPLASTIC CARCINOMA; CANCER RISK; ELECTRON MICROSCOPY; FLUORESCENCE IN SITU HYBRIDIZATION; GEOGRAPHY; HISTOLOGY; HUMAN; HUMAN PAPILLOMAVIRUS TYPE 11; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN PAPILLOMAVIRUS TYPE 18; HUMAN PAPILLOMAVIRUS TYPE 6; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LARGE CELL CARCINOMA; LUNG BIOPSY; LUNG CANCER; LUNG SMALL CELL CANCER; LUNG SQUAMOUS CELL CARCINOMA; POLYMERASE CHAIN REACTION; PREVALENCE; PRIORITY JOURNAL; REVIEW; SENSITIVITY ANALYSIS; SMOKING; SOUTHERN BLOTTING; SQUAMOUS CELL METAPLASIA; SYSTEMATIC REVIEW; VIRUS DETECTION; WART VIRUS;

HUMANS; LUNG NEOPLASMS; PAPILLOMAVIRIDAE;

EID: 84865689536     PISSN: 02507005     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (145)

1. Ferlay J, Shin HR, Bray F, Forman D, Mathers C and Parkin DM. GLOBOCAN 2008, Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 10. Lyon, France: International Agency for Research on Cancer; 2010. Available from: http://globocan.iarc.fr last accessed April 19, 2012.
2. Thun MJ, Henley SJ and Calle EE: Tobacco use and cancer: an epidemiologic perspective for geneticists. Oncogene 21: 7307-7325, 2002.
3. Sun S, Schiller JH and Gazdar AF: Lung cancer in never smokers- a different disease. Nat Rev Cancer 7: 778-790, 2007.
4. Brownson R C, Alavanja MC, Caporaso N, Simoes EJ and Chang JC: Epidemiology and prevention of lung cancer in non-smokers. Epidemiol Rev 20: 218-236, 1998.
5. Subramanian J and Govindan R: Lung cancer in never smokers: a review. J Clin Oncol 25: 561-570, 2007.
6. Bilello KS, Murin S and Matthay RA: Epidemiology, etiology, and prevention of lung cancer. Clin Chest Med 23: 1-25, 2002.
7. Patel JD: Lung cancer: A biologically different disease in women? Women Health 5: 685-691, 2009.
8. Syrjänen KJ: Condylomatous changes in neoplastic bronchial epithelium. Report of a case. Respiration 38: 299-304, 1979.
9. Syrjänen KJ: Epithelial lesions suggestive of a condylomatous origin found closely associated with invasive bronchial squamous cell carcinomas. Respiration 40: 150-160, 1980.
10. Syrjänen KJ: Bronchial squamous cell carcinomas associated with epithelial changes identical to condylomatous lesions of the uterine cervix. Lung 158: 131-142, 1980.
11. Meisels A and Fortin R: Condylomatous lesions of the cervix and vagina. I. Cytologic patterns. Acta Cytol 20: 505-509, 1976.
12. Purola E and Savia E: Cytology of gynaecologic condyloma acuminata. Acta Cytol 21: 26-31, 1977.
13. Syrjänen KJ: Histological and cytological evidence of a condylomatous lesion in association with an invasive carcinoma of uterine cervix. Arch Geschwulstforsch 49: 436-443, 1979.
14. Syrjänen KJ: Morphologic survey of the condylomatous lesions in dysplastic and neoplastic epithelium of the uterine cervix. Arch Gynaecol 227: 153-161, 1979.
15. Syrjänen K: HPV infections in the respiratory tract. Chapter 16. In: Papillomavirus Infections in Human Pathology. Syrjänen K and Syrjänen S: (eds.). J. Wiley & Sons, New York, pp. 355-378, 2000.
16. Syrjänen KJ: HPV infections and lung cancer. J Clin Pathol 55: 885-891, 2002.
17. Klein F, Kotb WFM and Petersen I: Incidence of human papilloma virus in lung cancer. Lung Cancer 65: 13-18, 2009.
18. Srinivasan M, Taioli E and Ragin CC: Human papillomavirus type 16 and 18 in primary lung cancers - a meta-analysis. Carcinogenesis 30: 1722-1728, 2009.
19. Ciotti M, Giuliani L, Ambrogi V, Ronci C, Benedetto A, Mineo TC, Syrjänen K and Favalli C: Detection and expression of human papillomavirus oncogenes in non-small cell lung cancer. Oncol Rep 16: 183-189, 2006.
20. Giuliani L, Favalli C, Syrjanen K and Ciotti M: Human papillomavirus infections in lung cancer. Detection of E6 and E7 transcripts and review of the literature. Anticancer Res 27: 2697-2704, 2007.
21. Hsu NY, Cheng YW, Chan IP, Ho HC, Chen CY, Hsu CP, Lin MH and Chou MC: Association between expression of human papillomavirus 16/18 E6 oncoprotein and survival in patients with stage I non-small cell lung cancer. Oncol Rep 21: 81-87, 2009.
22. Giuliani L, Jaxmar T, Casadio C, Gariglio M, Manna A, D'Antonio D, Syrjanen K, Favalli C and Ciotti M: Detection of oncogenic viruses SV40, BKV, JCV, HCMV, HPV and p53 codon 72 polymorphism in lung carcinoma. Lung Cancer 57: 273-281, 2007.
23. Krikelis D, Tzimagiorgis G, Georgiou E, Destouni C, Agorastos T, Haitoglou C and Kouidou S: Frequent presence of incomplete HPV16 E7 ORFs in lung carcinomas: memories of viral infection. J Clin Virol 49: 169-174, 2010.
24. Koshiol J, Rotunno M, Gillison ML, Van Doorn LJ, Chaturvedi AK, Tarantini L, Song H, Quint WG, Struijk L, Goldstein AM, Hildesheim A, Taylor PR, Wacholder S, Bertazzi PA, Landi MT and Caporaso NE: Assessment of human papillomavirus in lung tumor tissue. J Natl Cancer Inst 103: 501-507, 2011.
25. Syrjänen KJ, Chang F and Syrjänen SM: HPV infections in etiology of benign and malignant sinonasal, bronchial and oesophageal squamous cell lesions. In: 4th International Multidisciplinary Congress EUROGIN 2000. Monsonego J: (ed.). Monduzzi Editore, Bologna, pp. 169-179, 2000.
26. Syrjänen KJ: Annual disease burden due to human papillomavirus (HPV) 6 and 11 infections in Finland. Scand J Infect Dis Suppl 107: 3-32, 2009.
27. Syrjänen KJ: Annual disease burden due to human papillomavirus (HPV) 16 and 18 infections in Finland. Scand J Infect Dis Suppl 108: 2-32, 2009.
28. Mammas IN, Sourvinos G, Zaravinos A and Spandidos DA: Vaccination against human papilloma virus (HPV): Epidemiological evidence of HPV in non-genital cancers. Pathol Oncol Res 17: 103-119, 2011.
29. Stanley M: Prospects for new human papillomavirus vaccines. Curr Opin Infect Dis 23: 70-75, 2010.
30. Hardy RJ and Thompson SG: Detecting and describing heterogeneity in meta-analysis. Stat Med 17: 841-856, 1998.
31. Sterne JA, Gavaghan D and Egger M: Publication and related bias in meta-analysis: power of statistical tests and prevalence in the literature. J Clin Epidemiol 53: 1119-1129, 2000.
32. Begg CB and Mazumdar M: Operating characteristics of a rank correlation test for publication bias. Biometrics 50: 1088-1101, 1994.
33. Egger M, Davey SG, Schneider M and Minder C: Bias in meta-analysis detected by a simple, graphical test. BMJ 315: 629-634, 1997.
34. Duval S and Tweedie R: Trim and fill: a simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics 56: 455-463, 2000.
35. Thompson SG and Sharp SJ: Explaining heterogeneity in meta-analysis: a comparison of methods. Stat Med 18: 2693-2708, 1999.
36. Yu Y, Yang A, Hu S, Zhang J and Yan H: Significance of human papillomavirus 16/18 infection in association with p53 mutation in lung carcinomas. Clin Respir J 2011. doi: 10.1111/j.1752-699X.2011.00277.x.
37. Bishop JA, Ogawa T, Chang X, Illei PB, Gabrielson E, Pai SI and Westra WH: HPV analysis in distinguishing second primary tumors from lung metastases in patients with head and neck squamous cell carcinoma. Am J Surg Pathol 36: 142-148, 2012.
38. Stremlau A, Gissmann L, Ikenberg H, Stark M, Bannasch P and zur Hausen H: Human papillomavirus type 16 related DNA in an anaplastic carcinoma of the lung. Cancer 55: 1737-1740, 1985.
39. Helmuth RA and Strate RW: Squamous carcinoma of the lung in a nonirradiated, nonsmoking patient with juvenile laryngotracheal papillomatosis. Am J Surg Pathol 11: 643-650, 1987.
40. Ostrow RS, Manias DA, Fong WJ, Zachow KR and Faras AJ: A survey of human cancers for human papillomavirus DNA by filter hybridization. Cancer 59: 429-434, 1987.
41. Byrne JC, Tsao MS, Fraser RS and Howley PM: Human papillomavirus-11 DNA in a patient with chronic laryngotracheobronchial papillomatosis and metastatic squamous-cell carcinoma of the lung. N Engl J Med 317: 873-878, 1987.
42. Syrjänen KJ and Syrjänen SM: Human papillomavirus DNA in bronchial squamous cell carcinomas. Lancet 1: 168-169, 1987.
43. Trillo A and Guha A: Solitary condylomatous papilloma of the bronchus. Arch Pathol Lab Med 112: 731-733, 1988.
44. Syrjänen K, Syrjänen S, Kellokoski J, Kärjä J and Mäntyjärvi R: Human papillomavirus (HPV) type 6 and 16 DNA sequences in bronchial squamous cell carcinomas demonstrated by in situ DNA hybridization. Lung 167: 33-42, 1989.
45. Kerley SW, Buchon-Zalles C, Moran J and Fishback JL: Chronic cavitary respiratory papillomatosis. Arch Pathol Lab Med 113: 1166-1169, 1989.
46. Carey FA, Salter DM, Kerr KM and Lamb D: An investigation into the role of human papillomavirus in endobronchial papillary squamous tumours. Respir Med 84: 445-447, 1990.
47. Bejui-Thivolet F, Liagre N, Chignol MC, Chardonnet Y and Patricot LM: Detection of human papillomavirus DNA in squamous bronchial metaplasia and squamous cell carcinomas of the lung by in situ hybridization using biotinylated probes in paraffin-embedded specimens. Hum Pathol 21: 111-116, 1990.
48. Bejui-Thivolet F, Chardonnet Y and Patricot LM: Human papillomavirus type 11 DNA in papillary squamous cell lung carcinoma. Virchows Arch A Pathol Anat Histopathol 417: 457-461, 1990.
49. Kulski JK, Demeter T, Mutavdzic S, Sterrett GF, Mitchell KM and 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 94: 566-570, 1990.
50. Popper HH, Wirnsberger G, Juttner-Smolle FM, Pongratz MG and Sommersgutter M: The predictive value of human papilloma virus (HPV) typing in the prognosis of bronchial squamous cell papillomas. Histopathology 21: 323-330, 1992.
51. Guillou L, Sahli R, Chaubert P, Monnier P, Cuttat JF and Costa J: Squamous cell carcinoma of the lung in a nonsmoking, nonirradiated patient with juvenile laryngotracheal papillomatosis. Evidence of human papillomavirus-11 DNA in both carcinoma and papillomas. Am J Surg Pathol 15: 891-898, 1991.
52. DiLorenzo TP, Tamsen A, Abramson AL and Steinberg BM: Human papillomavirus type 6a DNA in the lung carcinoma of a patient with recurrent laryngeal papillomatosis is characterized by a partial duplication. J Gen Virol 73: 423-427, 1992.
53. Yousem SA, Ohori NP and Sonmez-Alpan E: Occurrence of human papillomavirus DNA in primary lung neoplasms. Cancer 69: 693-697, 1992.
54. Ogura H, Watanabe S, Fukushima K, Masuda Y, Fujiwara T and Yabe Y: Human papillomavirus DNA in squamous cell carcinomas of the respiratory and upper digestive tracts. Jpn J Clin Oncol 23: 221-225, 1993.
55. Xing LQ, Liu HR and Si JY: Detection of human papillomavirus DNA in squamous cell carcinomas of the lung by multiple polymerase chain reaction. Zhonghua Jie He He Hu Xi Za Zhi 16: 275-277, 1993. Article in Chinese.
56. Katial RK, Ranlett R and Whitlock WL: Human papilloma virus associated with solitary squamous papilloma complicated by bronchiectasis and bronchial stenosis. Chest 106: 1887-1889, 1994.
57. Liu HR, Xing LQ and Si JY: A study of human papillary virus infection by in situ hybridization and histopathology in squamous cell carcinoma of the lung. Chung Hua Ping Li Hsueh Tsa Chih 23: 299-301, 1994. Article I Chinese.
58. Popper HH, el-Shabrawi Y, Wockel W, Hofler G, Kenner L, Juttner-Smolle FM and Pongratz MG: Prognostic importance of human papilloma virus typing in squamous cell papilloma of the bronchus: comparison of in situ hybridization and the polymerase chain reaction. Hum Pathol 25: 1191-1197, 1994.
59. Shamanin V, Delius H and de Villiers EM: Development of a broad spectrum PCR assay for papillomaviruses and its application in screening lung cancer biopsies. J Gen Virol 75: 1149-1156, 1994.
60. Szabo I, Sepp R, Nakamoto K, Maeda M, Sakamoto H and Uda H: Human papillomavirus not found in squamous and large cell lung carcinomas by polymerase chain reaction. Cancer 73: 2740-2744, 1994.
61. Xing LQ, Liu HR and Si JY: Analysis of the characteristics of human papilloma virus infection in 85 neoplasms of the respiratory system in adult patients. Zhonghua Zhong Liu Za Zhi 16: 424-427, 1994. Article in Chinese.
62. Al-Ghamdi AA, Sanders CM, Keefe M, Coggon D and Maitland NJ: Human papillomavirus DNA and TP53 mutations in lung cancers from butchers. Br J Cancer 72: 293-297, 1995.
63. Kinoshita I, aka-Akita H, Shindoh M, Fujino M, Akie K, Kato M, Fujinaga K and Kawakami Y: Human papillomavirus type 18 DNA and E6-E7 mRNA are detected in squamous cell carcinoma and adenocarcinoma of the lung. Br J Cancer 71: 344-349, 1995.
64. Li Q, Hu K, Pan X, Cao Z, Yang J and Hu S: Detection of human papillomavirus types 16, 18 DNA related sequences in bronchogenic carcinoma by polymerase chain reaction. Chin Med J (Engl) 108: 610-614, 1995.
65. Nuorva K, Soini Y, Kamel D, Pöllänen R, Bloigu R, Vähäkangas K and Pääkkö P: p53 protein accumulation and the presence of human papillomavirus DNA in bronchiolo-alveolar carcinoma correlate with poor prognosis. Int J Cancer 64: 424-429, 1995.
66. Qingquan L, Xianguang P, Zuoyan C, Jiong Y and Suping H: Detection of human papillomavirus types 16, 18 DNA related sequences in bronchogenic carcinoma by polymerase chain reaction. Chin Med J (Engl) 108: 610-614, 1995.
67. Sagawa M, Saito Y, Endo C, Sato M, Usuda K, Kanma K, Takahashi S, Chin E, Sakurada A and Aikawa K: Detection of human papillomavirus type 16, 18 and 33 DNA in stage I (pT1N0M0) squamous cell carcinoma of the lung by polymerase chain reaction. Kyobu Geka 48: 360-362, 1995.
68. Thomas P, De L, X, Garbe L, Douagui H and Kleisbauer JP: Detection of human papillomavirus DNA in primary lung carcinoma by nested polymerase chain reaction. Cell Mol Biol 41: 1093-1097, 1995.
69. Zhang X, Zhu Y and Li L: Point mutation of p53 and detection of human papillomavirus DNA in bronchogenic carcinoma. Chung Hua Nei Ko Tsa Chih 34: 673-675, 1995. Article in Chinese.
70. Da J, Chen L and Hu Y: Human papillomavirus infection and p53 gene mutation in primary lung cancer. Chung Hua Chung Liu Tsa Chih 18: 27-29, 1996. Article in Chinese.
71. Thomas P, DeLamballerie X, Garbe L, Castelnau O and Kleisbauer JP: Detection of human papillomavirus by polymerase chain reaction in primary lung carcinoma. Bull Cancer 83: 842-846, 1996.
72. Hirayasu T, Iwamasa T, Kamada Y, Koyanagi Y, Usuda H and Genka K: Human papillomavirus DNA in squamous cell carcinoma of the lung. J Clin Pathol 49: 810-817, 1996.
73. Noutsou A, Koffa M, Ergazaki M, Siafakas NM and Spandidos DA: Detection of human papilloma virus (HPV) and K-RAS mutations in human lung carcinomas. Int J Oncol 8: 1089-1093, 1996.
74. Soini Y, Nuorva K, Kamel D, Pöllänen R, Vähäkangas K, Lehto VP and Pääkkö P: Presence of human papillomavirus DNA and abnormal p53 protein accumulation in lung carcinoma. Thorax 51: 887-893, 1996.
75. Welt A, Hummel M, Niedobitek G and Stein H: Human papillomavirus infection is not associated with bronchial carcinoma: evaluation by in situ hybridization and the polymerase chain reaction. J Pathol 181: 276-280, 1997.
76. Hu K, Li Q, Yang J and Hu S: Detection of human papillomavirus types 16 and 18 DNA-related sequences in bronchogenic carcinoma. Zhonghua Shi Yan He Lin Chuang Bing Du Xue Za Zhi 11: 147-149, 1997. Article in Chinese.
77. Bohlmeyer T, Le TN, Shroyer AL, Markham N and Shroyer KR: Detection of human papillomavirus in squamous cell carcinomas of the lung by polymerase chain reaction. Am J Respir Cell Mol Biol 18: 265-269, 1998.
78. Flieder DB, Koss MN, Nicholson A, Sesterhenn IA, Petras RE and Travis WD: Solitary pulmonary papillomas in adults: a clinicopathologic and in situ hybridization study of 14 cases combined with 27 cases in the literature. Am J Surg Pathol 22: 1328-1342, 1998.
79. Papadopoulou K, Labropoulou V, Davaris P, Mavromara P and Tsimara-Papastamatiou H: Detection of human papillomaviruses in squamous cell carcinomas of the lung. Virchows Arch 433: 49-54, 1998.
80. Tsuhako K, Nakazato I, Hirayasu T, Sunakawa H and Iwamasa T: Human papillomavirus DNA in adenosquamous carcinoma of the lung. J Clin Pathol 51: 741-749, 1998.
81. Wistuba II, Behrens C, Milchgrub S, Virmani AK, Jagirdar J, Thomas B, Ioachim HL, Litzky LA, Brambilla EM, Minna JD and Gazdar AF: Comparison of molecular changes in lung cancers in HIV-positive and HIV-indeterminate subjects. JAMA 279: 1554-1559, 1998.
82. Yang Y, Dong D, Peng L, Ling J, Xiao Y and Zhuang H: A study on the relationship between HPV infection and the oncogenesis of primary squamous carcinoma of the lung. Zhongguo Fei Ai Za Zhi 1: 35-36, 1998. Article in Chinese.
83. Gorgoulis VG, Zacharatos P, Kotsinas A, Kyroudi A, Rassidakis AN, Ikonomopoulos JA, Barbatis C, Herrington CS and Kittas C: Human papilloma virus (HPV) is possibly involved in laryngeal but not in lung carcinogenesis. Hum Pathol 30: 274-283, 1999.
84. Hennig EM, Suo Z, Karlsen F, Holm R, Thoresen S and Nesland JM: HPV 16 in multiple neoplastic lesions in women with CIN III. J Exp Clin Cancer Res 18: 369-377, 1999.
85. Hiroshima K, Toyozaki T, Iyoda A, Ohwada H, Kado S, Shirasawa H and Fujisawa T: Ultrastructural study of intranuclear inclusion bodies of pulmonary adenocarcinoma. Ultrastruct Pathol 23: 383-389, 1999.
86. Kawaguchi T, Matumura A, Iuchi K, Yamamoto S, Inoue Y, Sunami T, Naka N, Okishio K, Ueno K, Atagi S, Ogawara M, Hosoe S and Kawahara M: Solitary squamous papilloma of the bronchus associated with human papilloma virus type 11. Intern Med 38: 817-819, 1999.
87. Clavel CE, Nawrocki B, Bosseaux B, Poitevin G, Putaud IC, Mangeonjean CC, Monteau M and Birembaut PL: Detection of human papillomavirus DNA in bronchopulmonary carcinomas by hybrid capture II: a study of 185 tumors. Cancer 88: 1347-1352, 2000.
88. Harada H, Miura K, Tsutsui Y, Mineta H, Urano M, Abe M, Kuroda M and Kasahara M: Solitary squamous cell papilloma of the lung in a 40-year-old woman with recurrent laryngeal papillomatosis. Pathol Int 50: 431-439, 2000.
89. Iwamasa T, Miyagi J, Tsuhako K, Kinjo T, Kamada Y, Hirayasu T and Genka K: Prognostic implication of human papillomavirus infection in squamous cell carcinoma of the lung. Pathol Res Pract 196: 209-218, 2000.
90. Miyagi J, Tsuhako K, Kinjo T, Iwamasa T and Hirayasu T: Recent striking changes in histological differentiation and rate of human papillomavirus infection in squamous cell carcinoma of the lung in Okinawa, a subtropical island in southern Japan. J Clin Pathol 53: 676-684, 2000.
91. Niyaz H, Zhao C and Li Y: Detection and significance of HPV16, 18 infection, P53 overexpression and telomerase activity in patients with lung cancer. Zhonghua Jie He He Hu Xi Za Zhi 23: 679-682, 2000. Article in Chinese.
92. Cheng YW, Chiou HL, Sheu GT, Hsieh LL, Chen JT, Chen CY, Su JM and Lee H: The association of human papillomavirus 16/18 infection with lung cancer among nonsmoking Taiwanese women. Cancer Res 61: 2799-2803, 2001.
93. Kaya H, Kotiloglu E, Inanli S, Ekicioglu G, Bozkurt SU, Tutkun A and Kullu S: Prevalence of human papillomavirus (HPV) DNA in larynx and lung carcinomas. Pathologica 93: 531-534, 2001.
94. Miasko A, Niklinska W, Niklinski J, Chyczewska E, Naumnik W and Chyczewski L: Detection of human papillomavirus in non-small cell lung carcinoma by polymerase chain reaction. Folia Histochem Cytobiol 39: 127-128, 2001.
95. Miyagi J, Kinjo T, Tsuhako K, Higa M, Iwamasa T, Kamada Y and Hirayasu T: Extremely high Langerhans cell infiltration contributes to the favourable prognosis of HPV-infected squamous cell carcinoma and adenocarcinoma of the lung. Histopathology 38: 355-367, 2001.
96. Papadakis ED, Soulitzis N and Spandidos DA: Association of p53 codon 72 polymorphism with advanced lung cancer: the Arg allele is preferentially retained in tumours arising in Arg/Pro germline heterozygotes. Br J Cancer 87: 1013-1018, 2002.
97. Plunkett M, Brestovac B, Thompson J, Sterrett G, Filion P, Smith D and Frost F: The value of HPV DNA typing in the distinction between adenocarcinoma of endocervical and endometrial origin. Pathology 35: 397-401, 2003.
98. Aaron S, Wong E, Tyrrell D, Duggan M, Vallieres E, Jewell L, Romanowski B and Doe PJ: Interferon treatment of multiple pulmonary malignancies associated with papilloma virus. Can Respir J 11: 443-446, 2004.
99. Cheng YW, Chiou HL, Chen JT, Chou MC, Lin TS, Lai WW, Chen CY, Tsai YY and Lee H: Gender difference in human papillomarvirus infection for non-small cell lung cancer in Taiwan. Lung Cancer 46: 165-170, 2004.
100. Xu H, Lu DW, El-Mofty SK and Wang HL: Metachronous squamous cell carcinomas evolving from independent oropharyngeal and pulmonary squamous papillomas: association with human papillomavirus 11 and lack of aberrant p53, Rb, and p16 protein expression. Hum Pathol 35: 1419-1422, 2004.
101. Zafer E, Ergun MA, Alver G, Sahin FI, Yavuzer S and Ekmekci A: Detection and typing of human papillomavirus in non-small cell lung cancer. Respiration 71: 88-90, 2004.
102. Brouchet L, Valmary S, Dahan M, Didier A, Galateau-Salle F, Brousset P and Degano B: Detection of oncogenic virus genomes and gene products in lung carcinoma. Br J Cancer 92: 743-746, 2005.
103. Coissard CJ, Besson G, Polette MC, Monteau M, Birembaut PL and Clavel CE: Prevalence of human papillomaviruses in lung carcinomas: a study of 218 cases. Mod Pathol 18: 1606-1609, 2005.
104. Jain N, Singh V, Hedau S, Kumar S, Daga MK, Dewan R, Murthy NS, Husain SA and Das BC: Infection of human papillomavirus type 18 and p53 codon 72 polymorphism in lung cancer patients from India. Chest 128: 3999-4007, 2005.
105. Wu MF, Cheng YW, Lai JC, Hsu MC, Chen JT, Liu WS, Chiou MC, Chen CY and Lee H: Frequent p16INK4a promoter hypermethylation in human papillomavirus- infected female lung cancer in Taiwan. Int J Cancer 113: 440-445, 2005.
106. Castillo A, Aguayo F, Koriyama C, Shuyama K, Akiba S, Herrera-Goepfert R, Carrascal E, Klinge G, Sanchez J and Eizuru Y: Human papillomavirus in lung carcinomas among three Latin American countries. Oncol Rep 15: 883-888, 2006.
107. Fei Y, Yang J, Hsieh WC, Wu JY, Wu TC, Goan YG, Lee H and Cheng YW: Different human papillomavirus 16/18 infection in Chinese non-small cell lung cancer patients living in Wuhan, China. Jpn J Clin Oncol 36: 274-279, 2006.
108. Wang J, Cheng YW, Wu DW, Chen JT, Chen CY, Chou MC and Lee H: Frequent FHIT gene loss of heterozygosity in human papillomavirus-infected non-smoking female lung cancer in Taiwan. Cancer Lett 235: 18-25, 2006.
109. Zhao M, Rasmussen S, Perry J and Kiev J: The human papillomavirus as a possible cause of squamous cell carcinoma: A case study with a review of the medical literature. Am Surg 72: 49-50, 2006.
110. Aguayo F, Castillo A, Koriyama C, Higashi M, Itoh T, Capetillo M, Shuyama K, Corvalan A, Eizuru Y and Akiba S: Human papillomavirus-16 is integrated in lung carcinomas: a study in Chile. Br J Cancer 97: 85-91, 2007.
111. Carlson JW, Nucci MR, Brodsky J, Crum CP and Hirsch MS: Biomarker-assisted diagnosis of ovarian, cervical and pulmonary small cell carcinomas: the role of TTF-1, WT-1 and HPV analysis. Histopathology 51: 305-312, 2007.
112. Cheng YW, Wu MF, Wang J, Yeh KT, Goan YG, Chiou HL, Chen CY and Lee H: Human papillomavirus 16/18 E6 oncoprotein is expressed in lung cancer and related with p53 inactivation. Cancer Res 67: 10686-10693, 2007.
113. Nadji SA, Mahmoodi M, Ziaee AA, Naghshvar F, Torabizadeh J, Yahyapour Y, Nategh R and Mokhtari-Azad T: Relationship between lung cancer and human papillomavirus in north of Iran, Mazandaran province. Cancer Lett 248: 41-46, 2007.
114. Park MS, Chang YS, Shin JH, Kim DJ, Chung KY, Shin DH, Moon JW, Kang SM, Hahn CH, Kim YS, Chang J, Kim SK and Kim SK: The prevalence of human papillomavirus infection in Korean non-small cell lung cancer patients. Yonsei Med J 48: 69-77, 2007.
115. Buyru N, Altinisik J, Isin M and Dalay N: p53 codon 72 polymorphism and HPV status in lung cancer. Med Sci Monit 14: CR493-CR497, 2008.
116. Wang Y, Wang A, Jiang R, Pan H, Huang B, Lu Y and Wu C: Human papillomavirus type 16 and 18 infection is associated with lung cancer patients from the central part of China. Oncol Rep 20: 333-339, 2008.
117. Lim WT, Chuah KL, Leong SS, Tan EH and Toh CK: Assessment of human papillomavirus and Epstein-Barr virus in lung adenocarcinoma. Oncol Rep 21: 971-975, 2009.
118. Weichert W, Schewe C, Denkert C, Morawietz L, Dietel M and Petersen I: Molecular HPV typing as a diagnostic tool to discriminate primary from metastatic squamous cell carcinoma of the lung. Am J Surg Pathol 33: 513-520, 2009.
119. Xu Y, Cheng B, Pan H, Wu A and Zhang L: The Relationship between the status of human papillomavirus 16/18 infection and the expression of BCL-2 and BAX in squamous cell carcinomas of the lung. Zhongguo Fei Ai Za Zhi 12: 849-852, 2009. Article in Chinese.
120. Yu Y, Yang A, Hu S and Yan H: Correlation of HPV-16/18 infection of human papillomavirus with lung squamous cell carcinomas in Western China. Oncol Rep 21: 1627-1632, 2009.
121. Aguayo F, Anwar M, Koriyama C, Castillo A, Sun Q, Morewaya J, Eizuru Y and Akiba S: Human papillomavirus-16 presence and physical status in lung carcinomas from Asia. Infect Agent Cancer 5: 20-28, 2010.
122. Baba M, Castillo A, Koriyama C, Yanagi M, Matsumoto H, Natsugoe S, Shuyama KY, Khan N, Higashi M, Itoh T, Eizuru Y, Aikou T and Akiba S: Human papillomavirus is frequently detected in gefitinib-responsive lung adenocarcinomas. Oncol Rep 23: 1085-1092, 2010.
123. Branica BV, Smojver-Jezek S, Juros Z, Grgic S, Srpak N, Mitrecic D and Gajovic S: Detection of human papillomaviruses type 16, 18 and 33 in bronchial aspirates of lung carcinoma patients by polymerase chain reaction: a study of 84 cases in Croatia. Coll Anthropol 34: 159-162, 2010.
124. Iwakawa R, Kohno T, Enari M, Kiyono T and Yokota J: Prevalence of human papillomavirus 16/18/33 infection and p53 mutation in lung adenocarcinoma. Cancer Sci 101: 1891-1896, 2010.
125. Joh J, Jenson AB, Moore GD, Rezazedeh A, Slone SP, Ghim SJ and Kloecker GH: Human papillomavirus (HPV) and Merkel cell polyomavirus (MCPyV) in non small cell lung cancer. Exp Mol Pathol 89: 222-226, 2010.
126. Wang YH, Chen DJ, Yi TN and Liu XH: The relationship among human papilloma virus infection, survivin, and p53 gene in lung squamous carcinoma tissue. Saudi Med J 31: 1331-1336, 2010.
127. Zhang J, Wang T, Han M, Yang ZH, Liu LX, Chen Y, Zhang L, Hu HZ and Xi MR: Variation of human papillomavirus 16 in cervical and lung cancers in Sichuan, China. Acta Virol 54: 247-253, 2010.
128. Carpagnano GE, Koutelou A, Natalicchio MI, Martinelli D, Ruggieri C, Di TA, Antonetti R, Carpagnano F and Foschino-Barbaro MP: HPV in exhaled breath condensate of lung cancer patients. Br J Cancer 105: 1183-1190, 2011.
129. Goto A, Li CP, Ota S, Niki T, Ohtsuki Y, Kitajima S, Yonezawa S, Koriyama C, Akiba S, Uchima H, Lin YM, Yeh KT, Koh JS, Kim CW, Kwon KY, Nga ME and Fukayama M: Human papillomavirus infection in lung and esophageal cancers: analysis of 485 Asian cases. J Med Virol 83: 1383-1390, 2011.
130. Halimi M and Morshedi AS: Human papillomavirus infection in lung vs. oral squamous cell carcinomas: a polymerase chain reaction study. Pak J Biol Sci 14: 641-646, 2011.
131. Inamura K, Kumasaka T, Furuta R, Shimada K, Hiyama N, Furuhata Y, Tanaka I and Takemura T: Mixed squamous cell and glandular papilloma of the lung: A case study and literature review. Pathol Int 61: 252-258, 2011.
132. Lagana SM, Hanna RF and Borczuk AC: Pleomorphic (spindle and squamous cell) carcinoma arising in a peripheral mixed squamous and glandular papilloma in a 70-year-old man. Arch Pathol Lab Med 135: 1353-1356, 2011.
133. Mammas IN, Zaravinos A, Sourvinos G and Spandidos DA: Detection of human papillomavirus in bronchoalveolar lavage samples in immunocompetent children. Pediatr Infect Dis J 30: 384-386, 2011.
134. Saumet L, Damay A, Jeziorski E, Cartier C, Rouleau C, Margueritte G, Rodiere M and Segondy M: Bronchopulmonary squamous cell carcinoma associated with HPV 11 in a 15-year-old girl with a history of severe recurrent respiratory papillomatosis: a case report. Arch Pediatr 18: 754-757, 2011.
135. Doxtader EE and Katzenstein ALA: 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 43: 327-332, 2012.
136. Syrjänen K, Silvoniemi M, Salminen E, Vasankari T and Syrjänen S: Detection of human papillomavirus genotypes in bronchial cancer using sensitive multimetrix assay. Anticancer Res 32: 625-631, 2012.
137. Huedo-Medina T, Sanchez-Meca J, Marin-Martinez F and Botella J: Assessing heterogeneity in meta-analysis: Q statistic or I2 index? CHIP Documents. 2006; Paper 19. http://digitalcommons.uconn.edu/chip-docs/19 Last accessed April 19, 2012.
138. Field AP: Meta-analysis of correlation coefficients: A Monte-Carlo comparison of fixed- and random-effects methods. Psychol Meth 6: 161-180, 2001.
139. Field AP: The problems in using fixed-effects models of meta-analysis on real-world data. Understand Stat 2: 77-96, 2003.
140. Cochran WG: The combination of estimates from different experiments. Biometrics 10: 101-129, 1954.
141. Higgins JPT, Thompson SG, Deeks JJ and Altman DG: Measuring inconsistency in meta-analyses. Brit Med J 327: 557-560, 2003.
142. Syrjänen KJ: Human Papillomavirus (HPV) Involvement in Esophageal Carcinogenesis. Nova Science Publishing, New York, USA, pp. 1-96, 2010.
143. Li YJ, Tsai YC, Chen YC and Christiani DC: Human papilloma virus and female lung adenocarcinoma. Semin Oncol 36: 542-552, 2009.
144. Rezazadeh A, Laber DA, Ghim SJ, Jenson AB and Kloecker G: The role of human papilloma virus in lung cancer: a review of the evidence. Am J Med Sci 338: 64-67, 2009.
145. Kountouri MP, Mammas IN and Spandidos DA: Human papilloma virus (HPV) in lung cancer: Unanswered questions. Lung Cancer 67: 125-126, 2010.