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. 1989 Apr;2(2):166–190. doi: 10.1128/cmr.2.2.166

Human papillomaviruses: are we ready to type?

A Roman 1, K H Fife 1
PMCID: PMC358109  PMID: 2539898

Abstract

The issue of determining which human papillomavirus (HPV) is present in a clinical specimen (typing specimens for HPVs) is receiving attention because HPVs cause condyloma acuminata and are associated with the continuum of disease which ranges from dysplasia to invasive genital cancer. Morphological inspection of precancerous lesions is not sufficient to determine which lesions will progress and which will not. A number of research tools based primarily on deoxyribonucleic acid hybridization have been developed. These permit identification and typing of HPV in genital tract scrapings or biopsies. Some HPV types (e.g., HPV-16 and HPV-18) have been identified in high-grade dysplasias and carcinomas more commonly than other types (e.g., HPV-6) and have been designated "high risk" types for cervical cancer. Thus, the question arises whether HPV typing would improve patient management by providing increased sensitivity for detection of patients at risk or by providing a prognostic indicator. In this review, the available typing methods are reviewed from the standpoint of their sensitivity, specificity, and ease of application to large-scale screening programs. Data implicating HPVs in the genesis of genital tract cancers are reviewed, as is the association of specific HPV types with specific outcomes. We conclude that there is currently no simple, inexpensive assay for HPV types, although such assays may be developed in the future. Analysis of the typing data indicates that, while HPV types can be designated high risk and low risk, these designations are not absolute and thus the low-risk group should not be ignored. In addition, interpretation of the data is complicated by finding high-risk types in individuals with no indication of disease. Insufficient data exist to indicate whether knowledge of the presence of a given HPV type is a better prognostic indicator than cytological or histological results. Thus, more research is needed before it can be determined whether typing information will augment the method currently in use for deciding treatment regimen and whether it warrants widespread use.

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Selected References

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  1. Alessandri L. M., Sterrett G. F., Pixley E. C., Kulski J. K. Comparison of peroxidase-antiperoxidase and avidin-biotin complex methods for the detection of papillomavirus in histological sections of the cervix uteri. Pathology. 1986 Oct;18(4):382–385. doi: 10.3109/00313028609087555. [DOI] [PubMed] [Google Scholar]
  2. Baker C. C., Phelps W. C., Lindgren V., Braun M. J., Gonda M. A., Howley P. M. Structural and transcriptional analysis of human papillomavirus type 16 sequences in cervical carcinoma cell lines. J Virol. 1987 Apr;61(4):962–971. doi: 10.1128/jvi.61.4.962-971.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barnes W., Delgado G., Kurman R. J., Petrilli E. S., Smith D. M., Ahmed S., Lorincz A. T., Temple G. F., Jenson A. B., Lancaster W. D. Possible prognostic significance of human papillomavirus type in cervical cancer. Gynecol Oncol. 1988 Mar;29(3):267–273. doi: 10.1016/0090-8258(88)90225-9. [DOI] [PubMed] [Google Scholar]
  4. Barrasso R., De Brux J., Croissant O., Orth G. High prevalence of papillomavirus-associated penile intraepithelial neoplasia in sexual partners of women with cervical intraepithelial neoplasia. N Engl J Med. 1987 Oct 8;317(15):916–923. doi: 10.1056/NEJM198710083171502. [DOI] [PubMed] [Google Scholar]
  5. Beaudenon S., Kremsdorf D., Croissant O., Jablonska S., Wain-Hobson S., Orth G. A novel type of human papillomavirus associated with genital neoplasias. Nature. 1986 May 15;321(6067):246–249. doi: 10.1038/321246a0. [DOI] [PubMed] [Google Scholar]
  6. Beaudenon S., Kremsdorf D., Obalek S., Jablonska S., Pehau-Arnaudet G., Croissant O., Orth G. Plurality of genital human papillomaviruses: characterization of two new types with distinct biological properties. Virology. 1987 Dec;161(2):374–384. doi: 10.1016/0042-6822(87)90130-9. [DOI] [PubMed] [Google Scholar]
  7. Beckmann A. M., Kiviat N. B., Daling J. R., Sherman K. J., McDougall J. K. Human papillomavirus type 16 in multifocal neoplasia of the female genital tract. Int J Gynecol Pathol. 1988;7(1):39–47. doi: 10.1097/00004347-198803000-00004. [DOI] [PubMed] [Google Scholar]
  8. Beckmann A. M., Myerson D., Daling J. R., Kiviat N. B., Fenoglio C. M., McDougall J. K. Detection and localization of human papillomavirus DNA in human genital condylomas by in situ hybridization with biotinylated probes. J Med Virol. 1985 Jul;16(3):265–273. doi: 10.1002/jmv.1890160307. [DOI] [PubMed] [Google Scholar]
  9. Boshart M., Gissmann L., Ikenberg H., Kleinheinz A., Scheurlen W., zur Hausen H. A new type of papillomavirus DNA, its presence in genital cancer biopsies and in cell lines derived from cervical cancer. EMBO J. 1984 May;3(5):1151–1157. doi: 10.1002/j.1460-2075.1984.tb01944.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Brinton L. A., Schairer C., Haenszel W., Stolley P., Lehman H. F., Levine R., Savitz D. A. Cigarette smoking and invasive cervical cancer. JAMA. 1986 Jun 20;255(23):3265–3269. [PubMed] [Google Scholar]
  11. Broker T. R. Structure and genetic expression of papillomaviruses. Obstet Gynecol Clin North Am. 1987 Jun;14(2):329–348. [PubMed] [Google Scholar]
  12. Butterworth C. E., Jr, Hatch K. D., Gore H., Mueller H., Krumdieck C. L. Improvement in cervical dysplasia associated with folic acid therapy in users of oral contraceptives. Am J Clin Nutr. 1982 Jan;35(1):73–82. doi: 10.1093/ajcn/35.1.73. [DOI] [PubMed] [Google Scholar]
  13. Campion M. J., McCance D. J., Cuzick J., Singer A. Progressive potential of mild cervical atypia: prospective cytological, colposcopic, and virological study. Lancet. 1986 Aug 2;2(8501):237–240. doi: 10.1016/s0140-6736(86)92067-2. [DOI] [PubMed] [Google Scholar]
  14. Campion M. J., Singer A. Vulval intraepithelial neoplasia: clinical review. Genitourin Med. 1987 Jun;63(3):147–152. doi: 10.1136/sti.63.3.147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Caussy D., Orr W., Daya A. D., Roth P., Reeves W., Rawls W. Evaluation of methods for detecting human papillomavirus deoxyribonucleotide sequences in clinical specimens. J Clin Microbiol. 1988 Feb;26(2):236–243. doi: 10.1128/jcm.26.2.236-243.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Choo K. B., Pan C. C., Liu M. S., Ng H. T., Chen C. P., Lee Y. N., Chao C. F., Meng C. L., Yeh M. Y., Han S. H. Presence of episomal and integrated human papillomavirus DNA sequences in cervical carcinoma. J Med Virol. 1987 Feb;21(2):101–107. doi: 10.1002/jmv.1890210202. [DOI] [PubMed] [Google Scholar]
  17. Collins J. E., Jenkins D., McCance D. J. Detection of human papillomavirus DNA sequences by in situ DNA-DNA hybridisation in cervical intraepithelial neoplasia and invasive carcinoma: a retrospective study. J Clin Pathol. 1988 Mar;41(3):289–295. doi: 10.1136/jcp.41.3.289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Cornelissen M. T., van der Velden K. J., Walboomers J. M., Briët M. A., Smits H. L., van der Noordaa J., ter Schegget J. Evaluation of different DNA-DNA hybridisation techniques in detection of HPV 16 DNA in cervical smears and biopsies. J Med Virol. 1988 May;25(1):105–114. doi: 10.1002/jmv.1890250114. [DOI] [PubMed] [Google Scholar]
  19. Cox M. F., Meanwell C. A., Maitland N. J., Blackledge G., Scully C., Jordan J. A. Human papillomavirus type-16 homologous DNA in normal human ectocervix. Lancet. 1986 Jul 19;2(8499):157–158. doi: 10.1016/s0140-6736(86)91965-3. [DOI] [PubMed] [Google Scholar]
  20. Crum C. P., Braun L. A., Shah K. V., Fu Y. S., Levine R. U., Fenoglio C. M., Richart R. M., Townsend D. E. Vulvar intraepithelial neoplasia: correlation of nuclear DNA content and the presence of a human papilloma virus (HPV) structural antigen. Cancer. 1982 Feb 1;49(3):468–471. doi: 10.1002/1097-0142(19820201)49:3<468::aid-cncr2820490313>3.0.co;2-7. [DOI] [PubMed] [Google Scholar]
  21. Crum C. P., Ikenberg H., Richart R. M., Gissman L. Human papillomavirus type 16 and early cervical neoplasia. N Engl J Med. 1984 Apr 5;310(14):880–883. doi: 10.1056/NEJM198404053101403. [DOI] [PubMed] [Google Scholar]
  22. Crum C. P., Mitao M., Levine R. U., Silverstein S. Cervical papillomaviruses segregate within morphologically distinct precancerous lesions. J Virol. 1985 Jun;54(3):675–681. doi: 10.1128/jvi.54.3.675-681.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Crum C. P., Nagai N., Levine R. U., Silverstein S. In situ hybridization analysis of HPV 16 DNA sequences in early cervical neoplasia. Am J Pathol. 1986 Apr;123(1):174–182. [PMC free article] [PubMed] [Google Scholar]
  24. Crum C. P., Nuovo G., Friedman D., Silverstein S. J. A comparison of biotin and isotope-labeled ribonucleic acid probes for in situ detection of HPV-16 ribonucleic acid in genital precancers. Lab Invest. 1988 Mar;58(3):354–359. [PubMed] [Google Scholar]
  25. Danos O., Engel L. W., Chen E. Y., Yaniv M., Howley P. M. Comparative analysis of the human type 1a and bovine type 1 papillomavirus genomes. J Virol. 1983 May;46(2):557–566. doi: 10.1128/jvi.46.2.557-566.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Danos O., Katinka M., Yaniv M. Human papillomavirus 1a complete DNA sequence: a novel type of genome organization among papovaviridae. EMBO J. 1982;1(2):231–236. doi: 10.1002/j.1460-2075.1982.tb01152.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Dekmezian R., Chen X., Kuo T., Ordóez N., Katz R. L. DNA hybridization for human papillomavirus (HPV) in cervical lesions. Relationship of the presence of various viral subtypes to expression of HPV structural proteins, involucrin, and carcinoembryonic antigen. Arch Pathol Lab Med. 1987 Jan;111(1):22–27. [PubMed] [Google Scholar]
  28. Della Torre G., Pilotti S., de Palo G., Rilke F. Viral particles in cervical condylomatous lesions. Tumori. 1978 Oct 31;64(5):549–553. doi: 10.1177/030089167806400513. [DOI] [PubMed] [Google Scholar]
  29. Dürst M., Gissmann L., Ikenberg H., zur Hausen H. A papillomavirus DNA from a cervical carcinoma and its prevalence in cancer biopsy samples from different geographic regions. Proc Natl Acad Sci U S A. 1983 Jun;80(12):3812–3815. doi: 10.1073/pnas.80.12.3812. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Dürst M., Kleinheinz A., Hotz M., Gissmann L. The physical state of human papillomavirus type 16 DNA in benign and malignant genital tumours. J Gen Virol. 1985 Jul;66(Pt 7):1515–1522. doi: 10.1099/0022-1317-66-7-1515. [DOI] [PubMed] [Google Scholar]
  31. Ferenczy A., Braun L., Shah K. V. Human papillomavirus (HPV) in condylomatous lesions of cervix. Am J Surg Pathol. 1981 Oct;5(7):661–670. doi: 10.1097/00000478-198110000-00008. [DOI] [PubMed] [Google Scholar]
  32. Ferenczy A., Mitao M., Nagai N., Silverstein S. J., Crum C. P. Latent papillomavirus and recurring genital warts. N Engl J Med. 1985 Sep 26;313(13):784–788. doi: 10.1056/NEJM198509263131304. [DOI] [PubMed] [Google Scholar]
  33. Fife K. H., Rogers R. E., Zwickl B. W. Symptomatic and asymptomatic cervical infections with human papillomavirus during pregnancy. J Infect Dis. 1987 Dec;156(6):904–911. doi: 10.1093/infdis/156.6.904. [DOI] [PubMed] [Google Scholar]
  34. Firzlaff J. M., Kiviat N. B., Beckmann A. M., Jenison S. A., Galloway D. A. Detection of human papillomavirus capsid antigens in various squamous epithelial lesions using antibodies directed against the L1 and L2 open reading frames. Virology. 1988 Jun;164(2):467–477. doi: 10.1016/0042-6822(88)90561-2. [DOI] [PubMed] [Google Scholar]
  35. Fu Y. S., Braun L., Shah K. V., Lawrence W. D., Robboy S. J. Histologic, nuclear DNA, and human papillomavirus studies of cervical condylomas. Cancer. 1983 Nov 1;52(9):1705–1711. doi: 10.1002/1097-0142(19831101)52:9<1705::aid-cncr2820520926>3.0.co;2-d. [DOI] [PubMed] [Google Scholar]
  36. Fuchs P. G., Girardi F., Pfister H. Human papillomavirus DNA in normal, metaplastic, preneoplastic and neoplastic epithelia of the cervix uteri. Int J Cancer. 1988 Jan 15;41(1):41–45. doi: 10.1002/ijc.2910410109. [DOI] [PubMed] [Google Scholar]
  37. Fukushima M., Okagaki T., Twiggs L. B., Clark B. A., Zachow K. R., Ostrow R. S., Faras A. J. Histological types of carcinoma of the uterine cervix and the detectability of human papillomavirus DNA. Cancer Res. 1985 Jul;45(7):3252–3255. [PubMed] [Google Scholar]
  38. Gissmann L., Boshart M., Dürst M., Ikenberg H., Wagner D., zur Hausen H. Presence of human papillomavirus in genital tumors. J Invest Dermatol. 1984 Jul;83(1 Suppl):26s–28s. doi: 10.1111/1523-1747.ep12281143. [DOI] [PubMed] [Google Scholar]
  39. Gissmann L., Diehl V., Schultz-Coulon H. J., zur Hausen H. Molecular cloning and characterization of human papilloma virus DNA derived from a laryngeal papilloma. J Virol. 1982 Oct;44(1):393–400. doi: 10.1128/jvi.44.1.393-400.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Gissmann L., Wolnik L., Ikenberg H., Koldovsky U., Schnürch H. G., zur Hausen H. Human papillomavirus types 6 and 11 DNA sequences in genital and laryngeal papillomas and in some cervical cancers. Proc Natl Acad Sci U S A. 1983 Jan;80(2):560–563. doi: 10.1073/pnas.80.2.560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Gissmann L., deVilliers E. M., zur Hausen H. Analysis of human genital warts (condylomata acuminata) and other genital tumors for human papillomavirus type 6 DNA. Int J Cancer. 1982 Feb 15;29(2):143–146. doi: 10.1002/ijc.2910290205. [DOI] [PubMed] [Google Scholar]
  42. Grunebaum A. N., Sedlis A., Sillman F., Fruchter R., Stanek A., Boyce J. Association of human papillomavirus infection with cervical intraepithelial neoplasia. Obstet Gynecol. 1983 Oct;62(4):448–455. [PubMed] [Google Scholar]
  43. Grussendorf-Conen E. I., Ikenberg H., Gissmann L. Demonstration of HPV-16 genomes in the nuclei of cervix carcinoma cells. Dermatologica. 1985;170(4):199–201. doi: 10.1159/000249531. [DOI] [PubMed] [Google Scholar]
  44. Guillet G., Braun L., Shah K., Ferenczy A. Papillomavirus in cervical condylomas with and without associated cervical intraepithelial neoplasia. J Invest Dermatol. 1983 Dec;81(6):513–516. doi: 10.1111/1523-1747.ep12522852. [DOI] [PubMed] [Google Scholar]
  45. Gupta J. W., Gupta P. K., Rosenshein N., Shah K. V. Detection of human papillomavirus in cervical smears. A comparison of in situ hybridization, immunocytochemistry and cytopathology. Acta Cytol. 1987 Jul-Aug;31(4):387–396. [PubMed] [Google Scholar]
  46. Gupta J. W., Gupta P. K., Shah K. V., Kelly D. P. Distribution of human papillomavirus antigen in cervicovaginal smears and cervical tissues. Int J Gynecol Pathol. 1983;2(2):160–170. doi: 10.1097/00004347-198302000-00007. [DOI] [PubMed] [Google Scholar]
  47. Gupta J., Gendelman H. E., Naghashfar Z., Gupta P., Rosenshein N., Sawada E., Woodruff J. D., Shah K. Specific identification of human papillomavirus type in cervical smears and paraffin sections by in situ hybridization with radioactive probes: a preliminary communication. Int J Gynecol Pathol. 1985;4(3):211–218. doi: 10.1097/00004347-198509000-00005. [DOI] [PubMed] [Google Scholar]
  48. Gupta J., Pilotti S., Rilke F., Shah K. Association of human papillomavirus type 16 with neoplastic lesions of the vulva and other genital sites by in situ hybridization. Am J Pathol. 1987 May;127(2):206–215. [PMC free article] [PubMed] [Google Scholar]
  49. Hills E., Laverty C. R. Electron microscopic detection of papilloma virus particles in selected koilocytotic cells in a routine cervical smear. Acta Cytol. 1979 Jan-Feb;23(1):53–56. [PubMed] [Google Scholar]
  50. Hsu S. M., Raine L., Fanger H. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem. 1981 Apr;29(4):577–580. doi: 10.1177/29.4.6166661. [DOI] [PubMed] [Google Scholar]
  51. Inagaki Y., Tsunokawa Y., Takebe N., Nawa H., Nakanishi S., Terada M., Sugimura T. Nucleotide sequences of cDNAs for human papillomavirus type 18 transcripts in HeLa cells. J Virol. 1988 May;62(5):1640–1646. doi: 10.1128/jvi.62.5.1640-1646.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Jarrett W. F., McNeil P. E., Grimshaw W. T., Selman I. E., McIntyre W. I. High incidence area of cattle cancer with a possible interaction between an environmental carcinogen and a papilloma virus. Nature. 1978 Jul 20;274(5668):215–217. doi: 10.1038/274215a0. [DOI] [PubMed] [Google Scholar]
  53. Jenkins D., Tay S. K., Maddox P. H. Routine papillomavirus antigen staining of cervical punch biopsy specimens. J Clin Pathol. 1987 Oct;40(10):1212–1216. doi: 10.1136/jcp.40.10.1212. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Jenson A. B., Rosenthal J. D., Olson C., Pass F., Lancaster W. D., Shah K. Immunologic relatedness of papillomaviruses from different species. J Natl Cancer Inst. 1980 Mar;64(3):495–500. [PubMed] [Google Scholar]
  55. Jenson A. B., Sommer S., Payling-Wright C., Pass F., Link C. C., Jr, Lancaster W. D. Human papillomavirus. Frequency and distribution in plantar and common warts. Lab Invest. 1982 Nov;47(5):491–497. [PubMed] [Google Scholar]
  56. KOSS L. G., DURFEE G. R. Unusual patterns of squamous epithelium of the uterine cervix: cytologic and pathologic study of koilocytotic atypia. Ann N Y Acad Sci. 1956 Mar 30;63(6):1245–1261. doi: 10.1111/j.1749-6632.1956.tb32134.x. [DOI] [PubMed] [Google Scholar]
  57. KOSS L. G., STEWART F., FOOTE F. W., JORDAN M. J., BADER G. M., DAY E. SOME HISTOLOGICAL ASPECTS OF BEHAVIOR OF EPIDERMOID CARCINOMA IN SITU AND RELATED LESIONS OF THE UTERINE CERVIX. A LONG-TERM PROSPECTIVE STUDY. Cancer. 1963 Sep;16:1160–1211. doi: 10.1002/1097-0142(196309)16:9<1160::aid-cncr2820160910>3.0.co;2-4. [DOI] [PubMed] [Google Scholar]
  58. Kadish A. S., Burk R. D., Kress Y., Calderin S., Romney S. L. Human papillomaviruses of different types in precancerous lesions of the uterine cervix: histologic, immunocytochemical and ultrastructural studies. Hum Pathol. 1986 Apr;17(4):384–392. doi: 10.1016/s0046-8177(86)80462-2. [DOI] [PubMed] [Google Scholar]
  59. Kahn T., Schwarz E., zur Hausen H. Molecular cloning and characterization of the DNA of a new human papillomavirus (HPV 30) from a laryngeal carcinoma. Int J Cancer. 1986 Jan 15;37(1):61–65. doi: 10.1002/ijc.2910370111. [DOI] [PubMed] [Google Scholar]
  60. Kanda T., Watanabe S., Yoshiike K. Human papillomavirus type 16 transformation of rat 3Y1 cells. Jpn J Cancer Res. 1987 Feb;78(2):103–108. [PubMed] [Google Scholar]
  61. Kasher M. S., Roman A. Characterization of human papillomavirus type 6b DNA isolated from an invasive squamous carcinoma of the vulva. Virology. 1988 Jul;165(1):225–233. doi: 10.1016/0042-6822(88)90676-9. [DOI] [PubMed] [Google Scholar]
  62. Kaufman R. H., Bornstein J., Adam E., Burek J., Tessin B., Adler-Storthz K. Human papillomavirus and herpes simplex virus in vulvar squamous cell carcinoma in situ. Am J Obstet Gynecol. 1988 Apr;158(4):862–871. doi: 10.1016/0002-9378(88)90086-5. [DOI] [PubMed] [Google Scholar]
  63. Kaur P., McDougall J. K. Characterization of primary human keratinocytes transformed by human papillomavirus type 18. J Virol. 1988 Jun;62(6):1917–1924. doi: 10.1128/jvi.62.6.1917-1924.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Kessler I. I. Human cervical cancer as a venereal disease. Cancer Res. 1976 Feb;36(2 Pt 2):783–791. [PubMed] [Google Scholar]
  65. Kjaer S. K., de Villiers E. M., Haugaard B. J., Christensen R. B., Teisen C., Møller K. A., Poll P., Jensen H., Vestergaard B. F., Lynge E. Human papillomavirus, herpes simplex virus and cervical cancer incidence in Greenland and Denmark. A population-based cross-sectional study. Int J Cancer. 1988 Apr 15;41(4):518–524. doi: 10.1002/ijc.2910410408. [DOI] [PubMed] [Google Scholar]
  66. Krieg P., Amtmann E., Sauer G. The simultaneous extraction of high-molecular-weight DNA and of RNA from solid tumors. Anal Biochem. 1983 Oct 15;134(2):288–294. doi: 10.1016/0003-2697(83)90299-3. [DOI] [PubMed] [Google Scholar]
  67. Kulski J. K., Howard M. J., Pixley E. C. DNA sequences of human papillomavirus types 11, 16 or 18 in invasive cervical carcinoma of Western Australian women. Immunol Cell Biol. 1987 Feb;65(Pt 1):77–84. doi: 10.1038/icb.1987.9. [DOI] [PubMed] [Google Scholar]
  68. Kurman R. J., Jenson A. B., Lancaster W. D. Papillomavirus infection of the cervix. II. Relationship to intraepithelial neoplasia based on the presence of specific viral structural proteins. Am J Surg Pathol. 1983 Jan;7(1):39–52. [PubMed] [Google Scholar]
  69. Kurman R. J., Schiffman M. H., Lancaster W. D., Reid R., Jenson A. B., Temple G. F., Lorincz A. T. Analysis of individual human papillomavirus types in cervical neoplasia: a possible role for type 18 in rapid progression. Am J Obstet Gynecol. 1988 Aug;159(2):293–296. doi: 10.1016/s0002-9378(88)80070-x. [DOI] [PubMed] [Google Scholar]
  70. Kurman R. J., Shah K. H., Lancaster W. D., Jenson A. B. Immunoperoxidase localization of papillomavirus antigens in cervical dysplasia and vulvar condylomas. Am J Obstet Gynecol. 1981 Aug 15;140(8):931–935. doi: 10.1016/0002-9378(81)90087-9. [DOI] [PubMed] [Google Scholar]
  71. Lancaster W. D., Castellano C., Santos C., Delgado G., Kurman R. J., Jenson A. B. Human papillomavirus deoxyribonucleic acid in cervical carcinoma from primary and metastatic sites. Am J Obstet Gynecol. 1986 Jan;154(1):115–119. doi: 10.1016/0002-9378(86)90405-9. [DOI] [PubMed] [Google Scholar]
  72. Laverty C. R., Russell P., Hills E., Booth N. The significance of noncondylomatous wart virus infection of the cervical transformation zone. A review with discussion of two illustrative cases. Acta Cytol. 1978 Jul-Aug;22(4):195–201. [PubMed] [Google Scholar]
  73. Law M. F., Lancaster W. D., Howley P. M. Conserved polynucleotide sequences among the genomes of papillomaviruses. J Virol. 1979 Oct;32(1):199–207. doi: 10.1128/jvi.32.1.199-207.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Lehn H., Krieg P., Sauer G. Papillomavirus genomes in human cervical tumors: analysis of their transcriptional activity. Proc Natl Acad Sci U S A. 1985 Aug;82(16):5540–5544. doi: 10.1073/pnas.82.16.5540. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Li C. C., Shah K. V., Seth A., Gilden R. V. Identification of the human papillomavirus type 6b L1 open reading frame protein in condylomas and corresponding antibodies in human sera. J Virol. 1987 Sep;61(9):2684–2690. doi: 10.1128/jvi.61.9.2684-2690.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Lorincz A. T., Lancaster W. D., Temple G. F. Cloning and characterization of the DNA of a new human papillomavirus from a woman with dysplasia of the uterine cervix. J Virol. 1986 Apr;58(1):225–229. doi: 10.1128/jvi.58.1.225-229.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Lorincz A. T., Quinn A. P., Lancaster W. D., Temple G. F. A new type of papillomavirus associated with cancer of the uterine cervix. Virology. 1987 Jul;159(1):187–190. doi: 10.1016/0042-6822(87)90366-7. [DOI] [PubMed] [Google Scholar]
  78. Lowy D. R., Dvoretzky I., Shober R., Law M. F., Engel L., Howley P. M. In vitro tumorigenic transformation by a defined sub-genomic fragment of bovine papilloma virus DNA. Nature. 1980 Sep 4;287(5777):72–74. doi: 10.1038/287072a0. [DOI] [PubMed] [Google Scholar]
  79. Lyon J. L., Gardner J. W., West D. W., Stanish W. M., Hebertson R. M. Smoking and carcinoma in situ of the uterine cervix. Am J Public Health. 1983 May;73(5):558–562. doi: 10.2105/ajph.73.5.558. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Lörincz A. T. Detection of human papillomavirus infection by nucleic acid hybridization. Obstet Gynecol Clin North Am. 1987 Jun;14(2):451–469. [PubMed] [Google Scholar]
  81. Lörincz A. T., Temple G. F., Patterson J. A., Jenson A. B., Kurman R. J., Lancaster W. D. Correlation of cellular atypia and human papillomavirus deoxyribonucleic acid sequences in exfoliated cells of the uterine cervix. Obstet Gynecol. 1986 Oct;68(4):508–512. [PubMed] [Google Scholar]
  82. Macnab J. C., Walkinshaw S. A., Cordiner J. W., Clements J. B. Human papillomavirus in clinically and histologically normal tissue of patients with genital cancer. N Engl J Med. 1986 Oct 23;315(17):1052–1058. doi: 10.1056/NEJM198610233151703. [DOI] [PubMed] [Google Scholar]
  83. Matlashewski G., Schneider J., Banks L., Jones N., Murray A., Crawford L. Human papillomavirus type 16 DNA cooperates with activated ras in transforming primary cells. EMBO J. 1987 Jun;6(6):1741–1746. doi: 10.1002/j.1460-2075.1987.tb02426.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. McCance D. J., Campion M. J., Clarkson P. K., Chesters P. M., Jenkins D., Singer A. Prevalence of human papillomavirus type 16 DNA sequences in cervical intraepithelial neoplasia and invasive carcinoma of the cervix. Br J Obstet Gynaecol. 1985 Nov;92(11):1101–1105. doi: 10.1111/j.1471-0528.1985.tb03019.x. [DOI] [PubMed] [Google Scholar]
  85. McCance D. J., Campion M. J., Singer A. Non-invasive detection of cervical papillomavirus DNA. Lancet. 1986 Mar 8;1(8480):558–559. doi: 10.1016/s0140-6736(86)90912-8. [DOI] [PubMed] [Google Scholar]
  86. McCance D. J., Kalache A., Ashdown K., Andrade L., Menezes F., Smith P., Doll R. Human papillomavirus types 16 and 18 in carcinomas of the penis from Brazil. Int J Cancer. 1986 Jan 15;37(1):55–59. doi: 10.1002/ijc.2910370110. [DOI] [PubMed] [Google Scholar]
  87. McCance D. J., Kopan R., Fuchs E., Laimins L. A. Human papillomavirus type 16 alters human epithelial cell differentiation in vitro. Proc Natl Acad Sci U S A. 1988 Oct;85(19):7169–7173. doi: 10.1073/pnas.85.19.7169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  88. McCance D. J., Walker P. G., Dyson J. L., Coleman D. V., Singer A. Presence of human papillomavirus DNA sequences in cervical intraepithelial neoplasia. Br Med J (Clin Res Ed) 1983 Sep 17;287(6395):784–788. doi: 10.1136/bmj.287.6395.784. [DOI] [PMC free article] [PubMed] [Google Scholar]
  89. McDougall J. K., Myerson D., Beckmann A. M. Detection of viral DNA and RNA by in situ hybridization. J Histochem Cytochem. 1986 Jan;34(1):33–38. doi: 10.1177/34.1.3001177. [DOI] [PubMed] [Google Scholar]
  90. Meisels A., Fortin R. Condylomatous lesions of the cervix and vagina. I. Cytologic patterns. Acta Cytol. 1976 Nov-Dec;20(6):505–509. [PubMed] [Google Scholar]
  91. Meisels A., Fortin R., Roy M. Condylomatous lesions of the cervix. II. Cytologic, colposcopic and histopathologic study. Acta Cytol. 1977 May-Jun;21(3):379–390. [PubMed] [Google Scholar]
  92. Meisels A., Roy M., Fortier M., Morin C., Casas-Cordero M., Shah K. V., Turgeon H. Human papillomavirus infection of the cervix: the atypical condyloma. Acta Cytol. 1981 Jan-Feb;25(1):7–16. [PubMed] [Google Scholar]
  93. Millan D. W., Davis J. A., Torbet T. E., Campo M. S. DNA sequences of human papillomavirus types 11, 16, and 18 in lesions of the uterine cervix in the west of Scotland. Br Med J (Clin Res Ed) 1986 Jul 12;293(6539):93–96. doi: 10.1136/bmj.293.6539.93. [DOI] [PMC free article] [PubMed] [Google Scholar]
  94. Mitchell H., Drake M., Medley G. Prospective evaluation of risk of cervical cancer after cytological evidence of human papilloma virus infection. Lancet. 1986 Mar 15;1(8481):573–575. doi: 10.1016/s0140-6736(86)92807-2. [DOI] [PubMed] [Google Scholar]
  95. Morgan D., Pecoraro G., Rosenberg I., Defendi V. Transformation of C127 mouse fibroblasts by human papillomavirus 16. Cancer Res. 1988 May 1;48(9):2505–2511. [PubMed] [Google Scholar]
  96. Morin C., Braun L., Casas-Cordero M., Shah K. V., Roy M., Fortier M., Meisels A. Confirmation of the papillomavirus etiology of condylomatous cervix lesions by the peroxidase-antiperoxidase technique. J Natl Cancer Inst. 1981 May;66(5):831–835. [PubMed] [Google Scholar]
  97. Morin C., Meisels A. Human papilloma virus infection of the uterine cervix. Acta Cytol. 1980 Jan-Feb;24(1):82–84. [PubMed] [Google Scholar]
  98. Mullis K. B., Faloona F. A. Specific synthesis of DNA in vitro via a polymerase-catalyzed chain reaction. Methods Enzymol. 1987;155:335–350. doi: 10.1016/0076-6879(87)55023-6. [DOI] [PubMed] [Google Scholar]
  99. Muñoz N., Bosch X., Kaldor J. M. Does human papillomavirus cause cervical cancer? The state of the epidemiological evidence. Br J Cancer. 1988 Jan;57(1):1–5. doi: 10.1038/bjc.1988.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  100. Nagai N., Nuovo G., Friedman D., Crum C. P. Detection of papillomavirus nucleic acids in genital precancers with the in situ hybridization technique. Int J Gynecol Pathol. 1987;6(4):366–379. doi: 10.1097/00004347-198712000-00009. [DOI] [PubMed] [Google Scholar]
  101. Naghashfar Z. S., Rosenshein N. B., Lorincz A. T., Buscema J., Shah K. V. Characterization of human papillomavirus type 45, a new type 18-related virus of the genital tract. J Gen Virol. 1987 Dec;68(Pt 12):3073–3079. doi: 10.1099/0022-1317-68-12-3073. [DOI] [PubMed] [Google Scholar]
  102. Nakai Y., Lancaster W. D., Lim L. Y., Jenson A. B. Monoclonal antibodies to genus- and type-specific papillomavirus structural antigens. Intervirology. 1986;25(1):30–37. doi: 10.1159/000149652. [DOI] [PubMed] [Google Scholar]
  103. Nakajima T., Tsumuraya M., Morinaga S., Shimosato Y. Papillomavirus infection among Japanese: an immunohistochemical study for papillomavirus genus-specific antigen in human surface epithelial lesions. Jpn J Cancer Res. 1985 Jun;76(6):508–516. [PubMed] [Google Scholar]
  104. Nakajima T., Tsumuraya M., Morinaga S., Teshima S., Shimosato Y., Kishi K., Ohmi K., Sonoda T., Tsunematsu R., Tanemura K. The frequency of papillomavirus infection in cervical precancerous lesions in Japan: an immunoperoxidase study. Jpn J Cancer Res. 1986 Sep;77(9):891–895. [PubMed] [Google Scholar]
  105. Nash J. D., Burke T. W., Hoskins W. J. Biologic course of cervical human papillomavirus infection. Obstet Gynecol. 1987 Feb;69(2):160–162. [PubMed] [Google Scholar]
  106. Neumann R., Heiles B., Zippel C., Eggers H. J., Zippel H. H., Holzmann L., Schulz K. D. Use of biotinylated DNA probes in screening cells obtained from cervical swabs for human papillomavirus DNA sequences. Acta Cytol. 1986 Nov-Dec;30(6):603–607. [PubMed] [Google Scholar]
  107. Nuovo G. J., Crum C. P., De Villiers E. M., Levine R. U., Silverstein S. J. Isolation of a novel human papillomavirus (type 51) from a cervical condyloma. J Virol. 1988 Apr;62(4):1452–1455. doi: 10.1128/jvi.62.4.1452-1455.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  108. Okagaki T., Clark B. A., Zachow K. R., Twiggs L. B., Ostrow R. S., Pass F., Faras A. J. Presence of human papillomavirus in verrucous carcinoma (Ackerman) of the vagina. Immunocytochemical, ultrastructural, and DNA hybridization studies. Arch Pathol Lab Med. 1984 Jul;108(7):567–570. [PubMed] [Google Scholar]
  109. Oriel J. D., Whimster I. W. Carcinoma in situ associated with virus-containing anal warts. Br J Dermatol. 1971 Jan;84(1):71–73. doi: 10.1111/j.1365-2133.1971.tb14199.x. [DOI] [PubMed] [Google Scholar]
  110. Orth G., Breitburd F., Favre M. Evidence for antigenic determinants shared by the structural polypeptides of (Shope) rabbit papillomavirus and human papillomavirus type 1. Virology. 1978 Dec;91(2):243–255. doi: 10.1016/0042-6822(78)90373-2. [DOI] [PubMed] [Google Scholar]
  111. Orth G., Jablonska S., Jarzabek-Chorzelska M., Obalek S., Rzesa G., Favre M., Croissant O. Characteristics of the lesions and risk of malignant conversion associated with the type of human papillomavirus involved in epidermodysplasia verruciformis. Cancer Res. 1979 Mar;39(3):1074–1082. [PubMed] [Google Scholar]
  112. Oste C. Polymerase chain reaction. Biotechniques. 1988 Feb;6(2):162–167. [PubMed] [Google Scholar]
  113. Ostrow R. S., Bender M., Niimura M., Seki T., Kawashima M., Pass F., Faras A. J. Human papillomavirus DNA in cutaneous primary and metastasized squamous cell carcinomas from patients with epidermodysplasia verruciformis. Proc Natl Acad Sci U S A. 1982 Mar;79(5):1634–1638. doi: 10.1073/pnas.79.5.1634. [DOI] [PMC free article] [PubMed] [Google Scholar]
  114. Ostrow R. S., Manias D. A., Clark B. A., Okagaki T., Twiggs L. B., Faras A. J. Detection of human papillomavirus DNA in invasive carcinomas of the cervix by in situ hybridization. Cancer Res. 1987 Jan 15;47(2):649–653. [PubMed] [Google Scholar]
  115. Ostrow R. S., Manias D. A., Fong W. J., Zachow K. R., Faras A. J. A survey of human cancers for human papillomavirus DNA by filter hybridization. Cancer. 1987 Feb 1;59(3):429–434. doi: 10.1002/1097-0142(19870201)59:3<429::aid-cncr2820590313>3.0.co;2-1. [DOI] [PubMed] [Google Scholar]
  116. Parkin D. M., Stjernswärd J., Muir C. S. Estimates of the worldwide frequency of twelve major cancers. Bull World Health Organ. 1984;62(2):163–182. [PMC free article] [PubMed] [Google Scholar]
  117. Parkkinen S., Mäntyjärvi R., Syrjänen K., Ranki M. Detection of human papillomavirus DNA by the nucleic acid sandwich hybridization method from cervical scraping. J Med Virol. 1986 Nov;20(3):279–288. doi: 10.1002/jmv.1890200310. [DOI] [PubMed] [Google Scholar]
  118. Parkkinen S. Nucleic acid sandwich hybridization in detection of HPV 16 DNA: technique and its clinical application. J Virol Methods. 1988 Jan;19(1):69–77. doi: 10.1016/0166-0934(88)90008-0. [DOI] [PubMed] [Google Scholar]
  119. Pater M. M., Dunne J., Hogan G., Ghatage P., Pater A. Human papillomavirus types 16 and 18 sequences in early cervical neoplasia. Virology. 1986 Nov;155(1):13–18. doi: 10.1016/0042-6822(86)90163-7. [DOI] [PubMed] [Google Scholar]
  120. Pater M. M., Pater A. Human papillomavirus types 16 and 18 sequences in carcinoma cell lines of the cervix. Virology. 1985 Sep;145(2):313–318. doi: 10.1016/0042-6822(85)90164-3. [DOI] [PubMed] [Google Scholar]
  121. Pilotti S., Rilke F., Shah K. V., Delle Torre G., De Palo G. Immunohistochemical and ultrastructural evidence of papilloma virus infection associated with in situ and microinvasive squamous cell carcinoma of the vulva. Am J Surg Pathol. 1984 Oct;8(10):751–761. doi: 10.1097/00000478-198410000-00004. [DOI] [PubMed] [Google Scholar]
  122. Pirisi L., Yasumoto S., Feller M., Doniger J., DiPaolo J. A. Transformation of human fibroblasts and keratinocytes with human papillomavirus type 16 DNA. J Virol. 1987 Apr;61(4):1061–1066. doi: 10.1128/jvi.61.4.1061-1066.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  123. Portolani M., Borgatti M. A., Bartoletti A. M., Mariuzzi M. G., Beltrami C. A., Di Loreto C., De Nictolis M., Stramazzotti D. Papillomavirus genus-antigens in vulvar and cervical condylomatous lesions. Microbiologica. 1983 Apr;6(2):115–120. [PubMed] [Google Scholar]
  124. Ranki M., Palva A., Virtanen M., Laaksonen M., Söderlund H. Sandwich hybridization as a convenient method for the detection of nucleic acids in crude samples. Gene. 1983 Jan-Feb;21(1-2):77–85. doi: 10.1016/0378-1119(83)90149-x. [DOI] [PubMed] [Google Scholar]
  125. Reeves W. C., Caussy D., Brinton L. A., Brenes M. M., Montalvan P., Gomez B., de Britton R. C., Morice E., Gaitan E., de Lao S. L. Case-control study of human papillomaviruses and cervical cancer in Latin America. Int J Cancer. 1987 Oct 15;40(4):450–454. doi: 10.1002/ijc.2910400403. [DOI] [PubMed] [Google Scholar]
  126. Reid R., Fu Y. S., Herschman B. R., Crum C. P., Braun L., Shah K. V., Agronow S. J., Stanhope C. R. Genital warts and cervical cancer. VI. The relationship between aneuploid and polyploid cervical lesions. Am J Obstet Gynecol. 1984 Sep 15;150(2):189–199. doi: 10.1016/s0002-9378(84)80015-0. [DOI] [PubMed] [Google Scholar]
  127. Reid R., Laverty C. R., Coppleson M., Isarangkul W., Hills E. Noncondylomatous cervical wart virus infection. Obstet Gynecol. 1980 Apr;55(4):476–483. [PubMed] [Google Scholar]
  128. Reid R., Stanhope C. R., Herschman B. R., Booth E., Phibbs G. D., Smith J. P. Genital warts and cervical cancer. I. Evidence of an association between subclinical papillomavirus infection and cervical malignancy. Cancer. 1982 Jul 15;50(2):377–387. doi: 10.1002/1097-0142(19820715)50:2<377::aid-cncr2820500236>3.0.co;2-a. [DOI] [PubMed] [Google Scholar]
  129. Richart R. M., Barron B. A. A follow-up study of patients with cervical dysplasia. Am J Obstet Gynecol. 1969 Oct 1;105(3):386–393. doi: 10.1016/0002-9378(69)90268-3. [DOI] [PubMed] [Google Scholar]
  130. Richart R. M. Cervical intraepithelial neoplasia. Pathol Annu. 1973;8:301–328. [PubMed] [Google Scholar]
  131. Rigby P. W., Dieckmann M., Rhodes C., Berg P. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977 Jun 15;113(1):237–251. doi: 10.1016/0022-2836(77)90052-3. [DOI] [PubMed] [Google Scholar]
  132. Roman A., Fife K. Human papillomavirus DNA associated with foreskins of normal newborns. J Infect Dis. 1986 May;153(5):855–861. doi: 10.1093/infdis/153.5.855. [DOI] [PubMed] [Google Scholar]
  133. Saiki R. K., Gelfand D. H., Stoffel S., Scharf S. J., Higuchi R., Horn G. T., Mullis K. B., Erlich H. A. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 1988 Jan 29;239(4839):487–491. doi: 10.1126/science.2448875. [DOI] [PubMed] [Google Scholar]
  134. Saiki R. K., Scharf S., Faloona F., Mullis K. B., Horn G. T., Erlich H. A., Arnheim N. Enzymatic amplification of beta-globin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia. Science. 1985 Dec 20;230(4732):1350–1354. doi: 10.1126/science.2999980. [DOI] [PubMed] [Google Scholar]
  135. Sasson I. M., Haley N. J., Hoffmann D., Wynder E. L., Hellberg D., Nilsson S. Cigarette smoking and neoplasia of the uterine cervix: smoke constituents in cervical mucus. N Engl J Med. 1985 Jan 31;312(5):315–316. doi: 10.1056/nejm198501313120516. [DOI] [PubMed] [Google Scholar]
  136. Sato S., Okagaki T., Clark B. A., Twiggs L. B., Fukushima M., Ostrow R. S., Faras A. J. Sensitivity of koilocytosis, immunocytochemistry, and electron microscopy as compared to DNA hybridization in detecting human papillomavirus in cervical and vaginal condyloma and intraepithelial neoplasia. Int J Gynecol Pathol. 1986;5(4):297–307. doi: 10.1097/00004347-198612000-00002. [DOI] [PubMed] [Google Scholar]
  137. Schneider A., Hotz M., Gissmann L. Increased prevalence of human papillomaviruses in the lower genital tract of pregnant women. Int J Cancer. 1987 Aug 15;40(2):198–201. doi: 10.1002/ijc.2910400212. [DOI] [PubMed] [Google Scholar]
  138. Schneider A., Kraus H., Schuhmann R., Gissmann L. Papillomavirus infection of the lower genital tract: detection of viral DNA in gynecological swabs. Int J Cancer. 1985 Apr 15;35(4):443–448. doi: 10.1002/ijc.2910350405. [DOI] [PubMed] [Google Scholar]
  139. Schneider A., Oltersdorf T., Schneider V., Gissmann L. Distribution pattern of human papilloma virus 16 genome in cervical neoplasia by molecular in situ hybridization of tissue sections. Int J Cancer. 1987 Jun 15;39(6):717–721. doi: 10.1002/ijc.2910390611. [DOI] [PubMed] [Google Scholar]
  140. Schwarz E., Freese U. K., Gissmann L., Mayer W., Roggenbuck B., Stremlau A., zur Hausen H. Structure and transcription of human papillomavirus sequences in cervical carcinoma cells. Nature. 1985 Mar 7;314(6006):111–114. doi: 10.1038/314111a0. [DOI] [PubMed] [Google Scholar]
  141. Shibata D. K., Arnheim N., Martin W. J. Detection of human papilloma virus in paraffin-embedded tissue using the polymerase chain reaction. J Exp Med. 1988 Jan 1;167(1):225–230. doi: 10.1084/jem.167.1.225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  142. Shirasawa H., Tomita Y., Kubota K., Kasai T., Sekiya S., Takamizawa H., Simizu B. Transcriptional differences of the human papillomavirus type 16 genome between precancerous lesions and invasive carcinomas. J Virol. 1988 Mar;62(3):1022–1027. doi: 10.1128/jvi.62.3.1022-1027.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  143. Shirasawa H., Tomita Y., Sekiya S., Takamizawa H., Simizu B. Integration and transcription of human papillomavirus type 16 and 18 sequences in cell lines derived from cervical carcinomas. J Gen Virol. 1987 Feb;68(Pt 2):583–591. doi: 10.1099/0022-1317-68-2-583. [DOI] [PubMed] [Google Scholar]
  144. Smotkin D., Berek J. S., Fu Y. S., Hacker N. F., Major F. J., Wettstein F. O. Human papillomavirus deoxyribonucleic acid in adenocarcinoma and adenosquamous carcinoma of the uterine cervix. Obstet Gynecol. 1986 Aug;68(2):241–244. [PubMed] [Google Scholar]
  145. Smotkin D., Wettstein F. O. Transcription of human papillomavirus type 16 early genes in a cervical cancer and a cancer-derived cell line and identification of the E7 protein. Proc Natl Acad Sci U S A. 1986 Jul;83(13):4680–4684. doi: 10.1073/pnas.83.13.4680. [DOI] [PMC free article] [PubMed] [Google Scholar]
  146. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  147. Spence R. P., Murray A., Banks L., Kelland L. R., Crawford L. Analysis of human papillomavirus sequences in cell lines recently derived from cervical cancers. Cancer Res. 1988 Jan 15;48(2):324–328. [PubMed] [Google Scholar]
  148. Stanbridge C. M., Butler E. B. Human papillomavirus infection of the lower female genital tract: association with multicentric neoplasia. Int J Gynecol Pathol. 1983;2(3):264–274. doi: 10.1097/00004347-198303000-00004. [DOI] [PubMed] [Google Scholar]
  149. Stanbridge C. M., Mather J., Curry A., Butler E. B. Demonstration of papilloma virus particles in cervical and vaginal scrape material: a report of 10 cases. J Clin Pathol. 1981 May;34(5):524–531. doi: 10.1136/jcp.34.5.524. [DOI] [PMC free article] [PubMed] [Google Scholar]
  150. Statement of caution in the interpretation of papillomavirus-associated lesions of the epithelium of uterine cervix. Am J Obstet Gynecol. 1983 May 15;146(2):125–125. doi: 10.1016/0002-9378(83)91038-4. [DOI] [PubMed] [Google Scholar]
  151. Steinberg B. M., Topp W. C., Schneider P. S., Abramson A. L. Laryngeal papillomavirus infection during clinical remission. N Engl J Med. 1983 May 26;308(21):1261–1264. doi: 10.1056/NEJM198305263082104. [DOI] [PubMed] [Google Scholar]
  152. Sterrett G. F., Alessandri L. M., Pixley E., Kulski J. K. Assessment of precancerous lesions of the uterine cervix for evidence of human papillomavirus infection: a histological and immunohistochemical study. Pathology. 1987 Jan;19(1):84–90. doi: 10.3109/00313028709065144. [DOI] [PubMed] [Google Scholar]
  153. Stoler M. H., Broker T. R. In situ hybridization detection of human papillomavirus DNAs and messenger RNAs in genital condylomas and a cervical carcinoma. Hum Pathol. 1986 Dec;17(12):1250–1258. doi: 10.1016/s0046-8177(86)80569-x. [DOI] [PubMed] [Google Scholar]
  154. Storey A., Pim D., Murray A., Osborn K., Banks L., Crawford L. Comparison of the in vitro transforming activities of human papillomavirus types. EMBO J. 1988 Jun;7(6):1815–1820. doi: 10.1002/j.1460-2075.1988.tb03013.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  155. Sutherland I. H., Arulkumaran S., Kitchener H. C. Atypical condylomas of the cervix uteri in Singapore women: a histopathological and immunohistochemical study. Aust N Z J Obstet Gynaecol. 1986 May;26(2):151–154. doi: 10.1111/j.1479-828x.1986.tb01554.x. [DOI] [PubMed] [Google Scholar]
  156. Sutton G. P., Stehman F. B., Ehrlich C. E., Roman A. Human papillomavirus deoxyribonucleic acid in lesions of the female genital tract: evidence for type 6/11 in squamous carcinoma of the vulva. Obstet Gynecol. 1987 Oct;70(4):564–568. [PubMed] [Google Scholar]
  157. Swan S. H., Brown W. L. Oral contraceptive use, sexual activity, and cervical carcinoma. Am J Obstet Gynecol. 1981 Jan;139(1):52–57. doi: 10.1016/0002-9378(81)90411-7. [DOI] [PubMed] [Google Scholar]
  158. Syrjanen K., Parkkinen S., Mantyjarvi R., Vayrynen M., Syrjanen S., Holopainen H., Saarikoski S., Castren O. Human papillomavirus (HPV) type as an important determinant of the natural history of HPV infections in uterine cervix. Eur J Epidemiol. 1985 Sep;1(3):180–187. doi: 10.1007/BF00234092. [DOI] [PubMed] [Google Scholar]
  159. Syrjänen K. J. Human papillomavirus lesions in association with cervical dysplasias and neoplasias. Obstet Gynecol. 1983 Nov;62(5):617–624. [PubMed] [Google Scholar]
  160. Syrjänen K. J. Morphologic survey of the condylomatous lesions in dysplastic and neoplastic epithelium of the uterine cervix. Arch Gynecol. 1979 Aug;227(2):153–161. doi: 10.1007/BF02103290. [DOI] [PubMed] [Google Scholar]
  161. Syrjänen K. J., Mäntyjärvi R., Väyrynen M., Yliskoski M., Syrjänen S. M., Saarikoski S., Nurmi T., Parkkinen S., Castrén O. Cervical smears in assessment of the natural history of human papillomavirus infections in prospectively followed women. Acta Cytol. 1987 Nov-Dec;31(6):855–865. [PubMed] [Google Scholar]
  162. Syrjänen K. J., Pyrhönen S. Demonstration of human papilloma virus antigen in the condylomatous lesions of the uterine cervix by immunoperoxidase technique. Gynecol Obstet Invest. 1982;14(2):90–96. doi: 10.1159/000299456. [DOI] [PubMed] [Google Scholar]
  163. Syrjänen K. J., Pyrhönen S. Immunoperoxidase demonstration of human papilloma virus (HPV) in dysplastic lesions of the uterine cervix. Arch Gynecol. 1982;233(1):53–61. doi: 10.1007/BF02110679. [DOI] [PubMed] [Google Scholar]
  164. Syrjänen K., Väyrynen M., Castrén O., Mäntyjärvi R., Pyrhönen S., Yliskoski M. Morphological and immunohistochemical evidence of human papilloma virus (HPV) involvement in the dysplastic lesions of the uterine cervix. Int J Gynaecol Obstet. 1983 Aug;21(4):261–269. doi: 10.1016/0020-7292(83)90015-2. [DOI] [PubMed] [Google Scholar]
  165. Syrjänen K., Väyrynen M., Mäntyjärvi R., Holopainen H., Saarikoski S., Syrjänen S., Parkkinen S., Castrén O. Electron microscopy in assessment of the biological behavior of human papillomavirus infections in the uterine cervix. Neoplasma. 1986;33(4):493–505. [PubMed] [Google Scholar]
  166. Syrjänen K., Väyrynen M., Saarikoski S., Mäntyjärvi R., Parkkinen S., Hippeläinen M., Castren O. Natural history of cervical human papillomavirus (HPV) infections based on prospective follow-up. Br J Obstet Gynaecol. 1985 Nov;92(11):1086–1092. [PubMed] [Google Scholar]
  167. Syrjänen S., Partanen P., Mäntyjärvi R., Syrjänen K. Sensitivity of in situ hybridization techniques using biotin- and 35S-labeled human papillomavirus (HPV) DNA probes. J Virol Methods. 1988 Mar-Apr;19(3-4):225–238. doi: 10.1016/0166-0934(88)90017-1. [DOI] [PubMed] [Google Scholar]
  168. Syrjänen S., Syrjänen K. An improved in situ DNA hybridization protocol for detection of human papillomavirus (HPV) DNA sequences in paraffin-embedded biopsies. J Virol Methods. 1986 Nov;14(3-4):293–304. doi: 10.1016/0166-0934(86)90031-5. [DOI] [PubMed] [Google Scholar]
  169. Syrjänen S., Syrjänen K., Mäntyjärvi R., Parkkinen S., Väyrynen M., Saarikoski S., Castren O. Human papillomavirus (HPV) DNA sequences demonstrated by in situ DNA hybridization in serial paraffin-embedded cervical biopsies. Arch Gynecol. 1986;239(1):39–48. doi: 10.1007/BF02134287. [DOI] [PubMed] [Google Scholar]
  170. Thompson G. H., Roman A. Expression of human papillomavirus type 6 E1, E2, L1 and L2 open reading frames in Escherichia coli. Gene. 1987;56(2-3):289–295. doi: 10.1016/0378-1119(87)90146-6. [DOI] [PubMed] [Google Scholar]
  171. Toki T., Oikawa N., Tase T., Satoh S., Wada Y., Yajima A. Immunohistochemical demonstration of papillomavirus antigen in cervical dysplasia and vulvar condyloma. Gynecol Obstet Invest. 1986;22(2):97–101. doi: 10.1159/000298898. [DOI] [PubMed] [Google Scholar]
  172. Tomita Y., Shirasawa H., Simizu B. Expression of human papillomavirus types 6b and 16 L1 open reading frames in Escherichia coli: detection of a 56,000-dalton polypeptide containing genus-specific (common) antigens. J Virol. 1987 Aug;61(8):2389–2394. doi: 10.1128/jvi.61.8.2389-2394.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  173. Toon P. G., Arrand J. R., Wilson L. P., Sharp D. S. Human papillomavirus infection of the uterine cervix of women without cytological signs of neoplasia. Br Med J (Clin Res Ed) 1986 Nov 15;293(6557):1261–1264. doi: 10.1136/bmj.293.6557.1261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  174. Trevathan E., Layde P., Webster L. A., Adams J. B., Benigno B. B., Ory H. Cigarette smoking and dysplasia and carcinoma in situ of the uterine cervix. JAMA. 1983 Jul 22;250(4):499–502. [PubMed] [Google Scholar]
  175. Tsunokawa Y., Takebe N., Nozawa S., Kasamatsu T., Gissmann L., zur Hausen H., Terada M., Sugimura T. Presence of human papillomavirus type-16 and type-18 DNA sequences and their expression in cervical cancers and cell lines from Japanese patients. Int J Cancer. 1986 Apr 15;37(4):499–503. doi: 10.1002/ijc.2910370405. [DOI] [PubMed] [Google Scholar]
  176. Vessey M. P., Lawless M., McPherson K., Yeates D. Neoplasia of the cervix uteri and contraception: a possible adverse effect of the pill. Lancet. 1983 Oct 22;2(8356):930–934. doi: 10.1016/s0140-6736(83)90451-8. [DOI] [PubMed] [Google Scholar]
  177. Villa L. L., Lopes A. Human papillomavirus DNA sequences in penile carcinomas in Brazil. Int J Cancer. 1986 Jun 15;37(6):853–855. doi: 10.1002/ijc.2910370610. [DOI] [PubMed] [Google Scholar]
  178. Vonka V., Kanka J., Hirsch I., Závadová H., Krcmár M., Suchánková A., Rezácová D., Broucek J., Press M., Domorázková E. Prospective study on the relationship between cervical neoplasia and herpes simplex type-2 virus. II. Herpes simplex type-2 antibody presence in sera taken at enrollment. Int J Cancer. 1984 Jan 15;33(1):61–66. doi: 10.1002/ijc.2910330111. [DOI] [PubMed] [Google Scholar]
  179. Wagner D., Ikenberg H., Boehm N., Gissmann L. Identification of human papillomavirus in cervical swabs by deoxyribonucleic acid in situ hybridization. Obstet Gynecol. 1984 Dec;64(6):767–772. [PubMed] [Google Scholar]
  180. Wahl G. M., Berger S. L., Kimmel A. R. Molecular hybridization of immobilized nucleic acids: theoretical concepts and practical considerations. Methods Enzymol. 1987;152:399–407. doi: 10.1016/0076-6879(87)52046-8. [DOI] [PubMed] [Google Scholar]
  181. Walker P. G., Singer A., Dyson J. L., Shah K. V., To A., Coleman D. V. The prevalence of human papillomavirus antigen in patients with cervical intraepithelial neoplasia. Br J Cancer. 1983 Jul;48(1):99–101. doi: 10.1038/bjc.1983.163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  182. Watanabe S., Yoshiike K. Transformation of rat 3Y1 cells by human papillomavirus type-18 DNA. Int J Cancer. 1988 Jun 15;41(6):896–900. doi: 10.1002/ijc.2910410622. [DOI] [PubMed] [Google Scholar]
  183. Webb D. H., Rogers R. E., Fife K. H. A one-step method for detecting and typing human papillomavirus DNA in cervical scrape specimens from women with cervical dysplasia. J Infect Dis. 1987 Dec;156(6):912–919. doi: 10.1093/infdis/156.6.912. [DOI] [PubMed] [Google Scholar]
  184. Wickenden C., Malcolm A. D., Byrne M., Smith C., Anderson M. C., Coleman D. V. Prevalence of HPV DNA and viral copy numbers in cervical scrapes from women with normal and abnormal cervices. J Pathol. 1987 Oct;153(2):127–135. doi: 10.1002/path.1711530206. [DOI] [PubMed] [Google Scholar]
  185. Wickenden C., Steele A., Malcolm A. D., Coleman D. V. Screening for wart virus infection in normal and abnormal cervices by DNA hybridisation of cervical scrapes. Lancet. 1985 Jan 12;1(8420):65–67. doi: 10.1016/s0140-6736(85)91963-4. [DOI] [PubMed] [Google Scholar]
  186. Wilbur D. C., Reichman R. C., Stoler M. H. Detection of infection by human papillomavirus in genital condylomata. A comparison study using immunocytochemistry and in situ nucleic acid hybridization. Am J Clin Pathol. 1988 Apr;89(4):505–510. doi: 10.1093/ajcp/89.4.505. [DOI] [PubMed] [Google Scholar]
  187. Woodruff J. D., Braun L., Cavalieri R., Gupta P., Pass F., Shah K. V. Immunologic identification of papillomavirus antigen in condyloma tissues from the female genital tract. Obstet Gynecol. 1980 Dec;56(6):727–732. [PubMed] [Google Scholar]
  188. Yasumoto S., Burkhardt A. L., Doniger J., DiPaolo J. A. Human papillomavirus type 16 DNA-induced malignant transformation of NIH 3T3 cells. J Virol. 1986 Feb;57(2):572–577. doi: 10.1128/jvi.57.2.572-577.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  189. Yee C., Krishnan-Hewlett I., Baker C. C., Schlegel R., Howley P. M. Presence and expression of human papillomavirus sequences in human cervical carcinoma cell lines. Am J Pathol. 1985 Jun;119(3):361–366. [PMC free article] [PubMed] [Google Scholar]
  190. Yoshikawa H., Matsukura T., Yamamoto E., Kawana T., Mizuno M., Yoshiike K. Occurrence of human papillomavirus types 16 and 18 DNA in cervical carcinomas from Japan: age of patients and histological type of carcinomas. Jpn J Cancer Res. 1985 Aug;76(8):667–671. [PubMed] [Google Scholar]
  191. Zachow K. R., Ostrow R. S., Bender M., Watts S., Okagaki T., Pass F., Faras A. J. Detection of human papillomavirus DNA in anogenital neoplasias. Nature. 1982 Dec 23;300(5894):771–773. doi: 10.1038/300771a0. [DOI] [PubMed] [Google Scholar]
  192. Zarod A. P., Rutherford J. D., Corbitt G. Malignant progression of laryngeal papilloma associated with human papilloma virus type 6 (HPV-6) DNA. J Clin Pathol. 1988 Mar;41(3):280–283. doi: 10.1136/jcp.41.3.280. [DOI] [PMC free article] [PubMed] [Google Scholar]
  193. de Villiers E. M., Gissmann L., zur Hausen H. Molecular cloning of viral DNA from human genital warts. J Virol. 1981 Dec;40(3):932–935. doi: 10.1128/jvi.40.3.932-935.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  194. de Villiers E. M., Neumann C., Le J. Y., Weidauer H., zur Hausen H. Infection of the oral mucosa with defined types of human papillomaviruses. Med Microbiol Immunol. 1986;174(6):287–294. doi: 10.1007/BF02123681. [DOI] [PubMed] [Google Scholar]
  195. de Villiers E. M., Schneider A., Gross G., zur Hausen H. Analysis of benign and malignant urogenital tumors for human papillomavirus infection by labelling cellular DNA. Med Microbiol Immunol. 1986;174(6):281–286. doi: 10.1007/BF02123680. [DOI] [PubMed] [Google Scholar]
  196. de Villiers E. M., Wagner D., Schneider A., Wesch H., Miklaw H., Wahrendorf J., Papendick U., zur Hausen H. Human papillomavirus infections in women with and without abnormal cervical cytology. Lancet. 1987 Sep 26;2(8561):703–706. doi: 10.1016/s0140-6736(87)91072-5. [DOI] [PubMed] [Google Scholar]
  197. zur Hausen H. Human genital cancer: synergism between two virus infections or synergism between a virus infection and initiating events? Lancet. 1982 Dec 18;2(8312):1370–1372. doi: 10.1016/s0140-6736(82)91273-9. [DOI] [PubMed] [Google Scholar]
  198. zur Hausen H., Meinhof W., Scheiber W., Bornkamm G. W. Attempts to detect virus-secific DNA in human tumors. I. Nucleic acid hybridizations with complementary RNA of human wart virus. Int J Cancer. 1974 May 15;13(5):650–656. doi: 10.1002/ijc.2910130509. [DOI] [PubMed] [Google Scholar]

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