© 1993 by Oxford University Press
Journal of the National Cancer Institute, Vol. 85, No. 12, 958-964,
June 16, 1993
© 1993 Oxford University Press
Epidemiologic Evidence Showing That Human Papillomavirus Infection Causes Most Cervical Intraepithelial Neoplasia
Epidemiology and Biostatistics Program, Division of Cancer Etiology, National Cancer Institute Bethesda, Md
Cetus Corporation Emeryville, Calif
Kaiser Permanente, Portland, Ore
Westat, Inc. Rockville, Md
Department of Pathology. The Johns Hopkins Medical Institutions Baltimore, Md
Correspondence to: Mark H. Schiffman, M.D., M.P.H., National Institutes of Health, Executive Plaza North, Rm. 443, Bethesda, MD 20892.
BACKGROUND:: Experimental studies have provided strong evidence that human papillomavirus (HPV) is the long-sought venereal cause of cervical neoplasia, but the epidemiologic evidence has been inconsistent. Purpose: Given improvements in HPV testing that have revealed a strong link between sexual activity history and cervical HPV infection, we conducted a large case-control study of HPV and cervical intraepithelial neoplasia (CIN) to evaluate whether sexual behavior and the other established risk factors for CIN influence risk primarily via HPV infection. Methods: We studied 500 women with CIN and 500 control subjects receiving cytologic screening at Kaiser Permanente, a large prepaid health plan, in Portland, Ore. The established epidemiologic risk factors for CIN were assessed by telephone interview. We performed HPV testing of cervicovaginal lavage specimens by gene amplification using polymerase chain reaction with a consensus primer to target the LI gene region of HPV. Unconditional logistic regression analysis was used to estimate relative risk of CIN and to adjust the epidemiologic associations for HPV test results to demonstrate whether the associations were mediated by HPV. Results: The case subjects demonstrated the typical epidemiologic profile of CIN: They had more sex partners, more cigarette smoking, earlier ages at first sexual intercourse, and lower socioeconomic status. Statistical adjustment for HPV infection substantially reduced the size of each of these case-control differences. Seventy-six percent of cases could be attributed to HPV infection; the results of cytologic review suggested that the true percentage was even higher. Once HPV infection was taken into account, an association of parity with risk of CIN was observed in both HPV-negative and HPV-positive women. Conclusion: The data show that the great majority of all grades of CIN can be attributed to HPV infection, particularly with the cancer-associated types of HPV. Implications: In light of this conclusion, the investigation of the natural history of HPV has preventive as well as etiologic importance. [J Natl Cancer Inst 85:958–964, 1993]
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- Epidemiologic Studies of a Necessary Causal Risk Factor: Human Papillomavirus Infection and Cervical Neoplasia
- Mark H. Schiffman and Philip Castle
J Natl Cancer Inst 2003 95: 2E.[Extract] [Full Text]
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M. Schiff, J. Miller, M. Masuk, L. van Asselt King, K. K Altobelli, C. M Wheeler, and T. M Becker Contraceptive and reproductive risk factors for cervical intraepithelial neoplasia in American Indian women Int. J. Epidemiol., December 1, 2000; 29(6): 983 - 990. [Abstract] [Full Text] [PDF]
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M. Ghaderi, L. Nikitina, C. S. Peacock, P. Hjelmström, G. Hallmans, F. Wiklund, P. Lenner, J. M. Blackwell, J. Dillner, and C. B. Sanjeevi Tumor Necrosis Factor a-11 and DR15-DQ6 (B*0602) Haplotype Increase the Risk for Cervical Intraepithelial Neoplasia in Human Papillomavirus 16 Seropositive Women in Northern Sweden Cancer Epidemiol. Biomarkers Prev., October 1, 2000; 9(10): 1067 - 1070. [Abstract] [Full Text]
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C. Hoyo, W. C Miller, B. M Newman, and J. A Fortney Selective screening for cervical neoplasia: an approach for resource-poor settings Int. J. Epidemiol., October 1, 2000; 29(5): 807 - 812. [Abstract] [Full Text] [PDF]
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I. Silins, I. Kallings, and J. Dillner Correlates of the Spread of Human Papillomavirus Infection Cancer Epidemiol. Biomarkers Prev., September 1, 2000; 9(9): 953 - 959. [Abstract] [Full Text]
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W. Ai, J. Narahari, and A. Roman Yin Yang 1 Negatively Regulates the Differentiation-Specific E1 Promoter of Human Papillomavirus Type 6 J. Virol., June 1, 2000; 74(11): 5198 - 5205. [Abstract] [Full Text]
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G. Romano, A. Sgambato, R. Mancini, G. Capelli, M. R. Giovagnoli, G. Flamini, A. Boninsegna, A. Vecchione, and A. Cittadini 8-Hydroxy-2'-deoxyguanosine in cervical cells: correlation with grade of dysplasia and human papillomavirus infection Carcinogenesis, June 1, 2000; 21(6): 1143 - 1147. [Abstract] [Full Text] [PDF]
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P. E. Gravitt, C. L. Peyton, T. Q. Alessi, C. M. Wheeler, F. Coutlée, A. Hildesheim, M. H. Schiffman, D. R. Scott, and R. J. Apple Improved Amplification of Genital Human Papillomaviruses J. Clin. Microbiol., January 1, 2000; 38(1): 357 - 361. [Abstract] [Full Text]
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R. T. Emeny, J. R. Herron, L. F. Xi, L. A. Koutsky, N. B. Kiviat, and C. M. Wheeler Comparison of Variant-Specific Hybridization and Single-Strand Conformational Polymorphism Methods for Detection of Mixed Human Papillomavirus Type 16 Variant Infections J. Clin. Microbiol., November 1, 1999; 37(11): 3627 - 3633. [Abstract] [Full Text]
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W. J. G. Melchers, J. M. J .E. Bakkers, J. Wang, P. C. M. de Wilde, H. Boonstra, W. G. V. Quint, and A. G. J. M. Hanselaar Short Fragment Polymerase Chain Reaction Reverse Hybridization Line Probe Assay to Detect and Genotype a Broad Spectrum of Human Papillomavirus Types : Clinical Evaluation and Follow-Up Am. J. Pathol., November 1, 1999; 155(5): 1473 - 1478. [Abstract] [Full Text] [PDF]
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 D. Ndisang, V. Budhram-Mahadeo, and D. S. Latchman The Brn-3a Transcription Factor Plays a Critical Role in Regulating Human Papilloma Virus Gene Expression and Determining the Growth Characteristics of Cervical Cancer Cells J. Biol. Chem., October 1, 1999; 274(40): 28521 - 28527. [Abstract] [Full Text] [PDF]
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K.-L. Liaw, A. G. Glass, M. M. Manos, C. E. Greer, D. R. Scott, M. Sherman, R. D. Burk, R. J. Kurman, S. Wacholder, B. B. Rush, et al. Detection of Human Papillomavirus DNA in Cytologically Normal Women and Subsequent Cervical Squamous Intraepithelial Lesions J Natl Cancer Inst, June 2, 1999; 91(11): 954 - 960. [Abstract] [Full Text] [PDF]
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F. Coutlée, P. Gravitt, H. Richardson, C. Hankins, E. Franco, N. Lapointe, H. Voyer, and The Canadian Women's HIV Study Group Nonisotopic Detection and Typing of Human Papillomavirus DNA in Genital Samples by the Line Blot Assay J. Clin. Microbiol., June 1, 1999; 37(6): 1852 - 1857. [Abstract] [Full Text]
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M. M. Manos, W. K. Kinney, L. B. Hurley, M. E. Sherman, J. Shieh-Ngai, R. J. Kurman, J. E. Ransley, B. J. Fetterman, J. S. Hartinger, K. M. McIntosh, et al. Identifying Women With Cervical Neoplasia: Using Human Papillomavirus DNA Testing for Equivocal Papanicolaou Results JAMA, May 5, 1999; 281(17): 1605 - 1610. [Abstract] [Full Text] [PDF]
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E. L. Franco, T. E. Rohan, and L. L. Villa Epidemiologic Evidence and Human Papillomavirus Infection as a Necessary Cause of Cervical Cancer J Natl Cancer Inst, March 17, 1999; 91(6): 506 - 511. [Full Text] [PDF]
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A Eriksson, J. Herron, T Yamada, and C. Wheeler Human papillomavirus type 16 variant lineages characterized by nucleotide sequence analysis of the E5 coding segment and the E2 hinge region J. Gen. Virol., March 1, 1999; 80(3): 595 - 600. [Abstract]
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J. G. Joyce, J.-S. Tung, C. T. Przysiecki, J. C. Cook, E. D. Lehman, J. A. Sands, K. U. Jansen, and P. M. Keller The L1 Major Capsid Protein of Human Papillomavirus Type 11 Recombinant Virus-like Particles Interacts with Heparin and Cell-surface Glycosaminoglycans on Human Keratinocytes J. Biol. Chem., February 26, 1999; 274(9): 5810 - 5822. [Abstract] [Full Text] [PDF]
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L Kjellberg, Z Wang, F Wiklund, K Edlund, T Angstrom, P Lenner, I Sjoberg, G Hallmans, K. Wallin, M Sapp, et al. Sexual behaviour and papillomavirus exposure in cervical intraepithelial neoplasia: a population-based case-control study J. Gen. Virol., February 1, 1999; 80(2): 391 - 398. [Abstract]
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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 J Natl Cancer Inst, January 20, 1999; 91(2): 156 - 162. [Abstract] [Full Text] [PDF]
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C. L. Peyton, M. Schiffman, A. T. Lörincz, W. C. Hunt, I. Mielzynska, C. Bratti, S. Eaton, A. Hildesheim, L. A. Morera, A. C. Rodriguez, et al. Comparison of PCR- and Hybrid Capture-Based Human Papillomavirus Detection Systems Using Multiple Cervical Specimen Collection Strategies J. Clin. Microbiol., November 1, 1998; 36(11): 3248 - 3254. [Abstract] [Full Text]
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P. E. Gravitt, C. L. Peyton, R. J. Apple, and C. M. Wheeler Genotyping of 27 Human Papillomavirus Types by Using L1 Consensus PCR Products by a Single-Hybridization, Reverse Line Blot Detection Method J. Clin. Microbiol., October 1, 1998; 36(10): 3020 - 3027. [Abstract] [Full Text]
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P. Zazove, B. D. Reed, L. Gregoire, A. Ferenczy, D. W. Gorenflo, and W. D. Lancaster Low False-Negative Rate of PCR Analysis for Detecting Human Papillomavirus-Related Cervical Lesions J. Clin. Microbiol., September 1, 1998; 36(9): 2708 - 2713. [Abstract] [Full Text]
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F. Coutlée and H. Voyer Effect of Nonionic Detergents on Amplification of Human Papillomavirus DNA with Consensus Primers MY09 and MY11 J. Clin. Microbiol., April 1, 1998; 36(4): 1164 - 1164. [Full Text]
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D. R. Lowy and J. T. Schiller Papillomaviruses and Cervical Cancer: Pathogenesis and Vaccine Development J Natl Cancer Inst Monographs, April 1, 1998; 1998(23): 27 - 30. [Abstract] [Full Text]
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J Dillner, P Knekt, J T Schiller, and T Hakulinen Prospective seroepidemiological evidence that human papillomavirus type 16 infection is a risk factor for oesophageal squamous cell carcinoma BMJ, November 18, 1995; 311(7016): 1346 - 1346. [Full Text]
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R. J. Kurman, D. E. Henson, A. L. Herbst, K. L. Noller, M. H. Schiffman, the 1992 National Cancer Institute Workshop, R. J. Kurman, T. Bonfiglio, H. Buck, C. Crum, et al. Interim Guidelines for Management of Abnormal Cervical Cytology JAMA, June 15, 1994; 271(23): 1866 - 1869. [Abstract] [PDF]
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 M. T. Ruffin Cervical Cancer Screening-Reply Arch Fam Med, November 1, 1993; 2(11): 1114 - 1115. [Abstract] [PDF]
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 X. Hu, T. Pang, A. Asplund, J. Ponten, and M. Nister Clonality Analysis of Synchronous Lesions of Cervical Carcinoma Based on X Chromosome Inactivation Polymorphism, Human Papillomavirus Type 16 Genome Mutations, and Loss of Heterozygosity J. Exp. Med., March 25, 2002; 195(7): 845 - 854. [Abstract] [Full Text] [PDF]
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