Epidemiologic Classification of Human Papillomavirus Types Associated with Cervical Cancer
Nubia Muñoz, M.D., F. Xavier Bosch, M.D., Silvia de Sanjosé, M.D., Rolando Herrero, M.D., Xavier Castellsagué, M.D., Keerti V. Shah, Ph.D., Peter J.F. Snijders, Ph.D., Chris J.L.M. Meijer, M.D., for the International Agency for Research on Cancer Multicenter Cervical Cancer Study Group
Background Infection with human papilloma virus (HPV) is themain cause of cervical cancer, but the risk associated withthe various HPV types has not been adequately assessed.
Methods We pooled data from 11 case–control studies fromnine countries involving 1918 women with histologically confirmedsquamous-cell cervical cancer and 1928 control women. A commonprotocol and questionnaire were used. Information on risk factorswas obtained by personal interviews, and cervical cells werecollected for detection of HPV DNA and typing in a central laboratoryby polymerase-chain-reaction–based assays (with MY09/MY11and GP5+/6+ primers).
Results HPV DNA was detected in 1739 of the 1918 patients withcervical cancer (90.7 percent) and in 259 of the 1928 controlwomen (13.4 percent). With the GP5+/6+ primer, HPV DNA was detectedin 96.6 percent of the patients and 15.6 percent of the controls.The most common HPV types in patients, in descending order offrequency, were types 16, 18, 45, 31, 33, 52, 58, and 35. Amongcontrol women, types 16, 18, 45, 31, 6, 58, 35, and 33 werethe most common. For studies using the GP5+/6+ primer, the pooledodds ratio for cervical cancer associated with the presenceof any HPV was 158.2 (95 percent confidence interval, 113.4to 220.6). The odds ratios were over 45 for the most commonand least common HPV types. Fifteen HPV types were classifiedas high-risk types (16, 18, 31, 33, 35, 39, 45, 51, 52, 56,58, 59, 68, 73, and 82); 3 were classified as probable high-risktypes (26, 53, and 66); and 12 were classified as low-risk types(6, 11, 40, 42, 43, 44, 54, 61, 70, 72, 81, and CP6108). Therewas good agreement between our epidemiologic classificationand the classification based on phylogenetic grouping.
Conclusions In addition to HPV types 16 and 18, types 31, 33,35, 39, 45, 51, 52, 56, 58, 59, 68, 73, and 82 should be consideredcarcinogenic, or high-risk, types, and types 26, 53, and 66should be considered probably carcinogenic.
Source Information
From the International Agency for Research on Cancer, Lyons, France (N.M.); the Epidemiology and Cancer Registration Unit, Institut Català d'Oncologia, L'Hospitalet de Llobregat, Barcelona, Spain (F.X.B., S.S., X.C.); Costa Rican Foundation for Health Sciences, San José, Costa Rica (R.H.); the Department of Molecular Microbiology and Immunology, Johns Hopkins School of Public Health, Baltimore (K.V.S.); and the Department of Pathology, Vrije Universiteit Medical Center, Amsterdam (P.J.F.S., C.J.L.M.M.).
Address reprint requests to Dr. Muñoz at the Servei d'Epidemiologia i Registre del Càncer, Institut Català d'Oncologia, Hospital Duran i Reynals, Av. Gran Via, s/n km. 2,7, 08907 L'Hospitalet de Llobregat, Barcelona, Spain, or at cris{at}ico.scs.es.
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Naucler, P., Chen, H.-C., Persson, K., You, S.-L., Hsieh, C.-Y., Sun, C.-A., Dillner, J., Chen, C.-J.
(2007). Seroprevalence of human papillomaviruses and Chlamydia trachomatis and cervical cancer risk: nested case-control study. J. Gen. Virol.
88: 814-822
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Payan, C., Ducancelle, A., Aboubaker, M. H., Caer, J., Tapia, M., Chauvin, A., Peyronnet, D., Le Hen, E., Arab, Z., Legrand, M.-C., Tran, A., Postec, E., Tourmen, F., Avenel, M., Malbois, C., De Brux, M.-A., Descamps, P., Lunel, F.
(2007). Human Papillomavirus Quantification in Urine and Cervical Samples by Using the Mx4000 and LightCycler General Real-Time PCR Systems. J. Clin. Microbiol.
45: 897-901
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Fontaine, V., Mascaux, C., Weyn, C., Bernis, A., Celio, N., Lefevre, P., Kaufman, L., Garbar, C.
(2007). Evaluation of Combined General Primer-Mediated PCR Sequencing and Type-Specific PCR Strategies for Determination of Human Papillomavirus Genotypes in Cervical Cell Specimens. J. Clin. Microbiol.
45: 928-934
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Hasan, U. A., Bates, E., Takeshita, F., Biliato, A., Accardi, R., Bouvard, V., Mansour, M., Vincent, I., Gissmann, L., Iftner, T., Sideri, M., Stubenrauch, F., Tommasino, M.
(2007). TLR9 Expression and Function Is Abolished by the Cervical Cancer-Associated Human Papillomavirus Type 16. J. Immunol.
178: 3186-3197
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Radivojac, P., Iakoucheva, L. M., Oldfield, C. J., Obradovic, Z., Uversky, V. N., Dunker, A. K.
(2007). Intrinsic Disorder and Functional Proteomics. Biophys. J
92: 1439-1456
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Ragin, C.C.R., Modugno, F., Gollin, S.M.
(2007). The Epidemiology and Risk Factors of Head and Neck Cancer: a Focus on Human Papillomavirus. J. Dent. Res.
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Carozzi, F., Bisanzi, S., Sani, C., Zappa, M., Cecchini, S., Ciatto, S., Confortini, M.
(2007). Agreement between the AMPLICOR Human Papillomavirus Test and the Hybrid Capture 2 Assay in Detection of High-Risk Human Papillomavirus and Diagnosis of Biopsy-Confirmed High-Grade Cervical Disease. J. Clin. Microbiol.
45: 364-369
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Halfon, P., Trepo, E., Antoniotti, G., Bernot, C., Cart-Lamy, P., Khiri, H., Thibaud, D., Marron, J., Martineau, A., Penaranda, G., Benmoura, D., Blanc, B., and RBML (Reseau de Biologie Moleculaire Liberale),
(2007). Prospective Evaluation of the Hybrid Capture 2 and AMPLICOR Human Papillomavirus (HPV) Tests for Detection of 13 High-Risk HPV Genotypes in Atypical Squamous Cells of Uncertain Significance. J. Clin. Microbiol.
45: 313-316
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Mbwana, J, Viscidi, R, Lyamuya, E, Mhalu, F, Chalamilla, G, Liljeqvist, J-A, Lagergard, T
(2007). Prevalence of serum antibodies to human papilloma virus in patients with genital ulcer disease in an urban population of Tanzania. Sex. Transm. Infect.
83: 64-65
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Xi, L. F., Koutsky, L. A., Hildesheim, A., Galloway, D. A., Wheeler, C. M., Winer, R. L., Ho, J., Kiviat, N. B.
(2007). Risk for High-Grade Cervical Intraepithelial Neoplasia Associated with Variants of Human Papillomavirus Types 16 and 18. Cancer Epidemiol. Biomarkers Prev.
16: 4-10
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Kreimer, A. R., Katki, H. A., Schiffman, M., Wheeler, C. M., Castle, P. E., for the ASCUS-LSIL Triage Study Group,
(2007). Viral Determinants of Human Papillomavirus Persistence following Loop Electrical Excision Procedure Treatment for Cervical Intraepithelial Neoplasia Grade 2 or 3. Cancer Epidemiol. Biomarkers Prev.
16: 11-16
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Saslow, D., Castle, P. E., Cox, J. T., Davey, D. D., Einstein, M. H., Ferris, D. G., Goldie, S. J., Harper, D. M., Kinney, W., Moscicki, A.-B., Noller, K. L., Wheeler, C. M., Ades, T., Andrews, K. S., Doroshenk, M. K., Kahn, K. G., Schmidt, C., Shafey, O., Smith, R. A., Partridge, E. E., (for The Gynecologic Cancer Advisory Group), , Garcia, F.
(2007). American Cancer Society Guideline for Human Papillomavirus (HPV) Vaccine Use to Prevent Cervical Cancer and Its Precursors. CA Cancer J Clin
57: 7-28
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Piersma, S. J., Jordanova, E. S., van Poelgeest, M. I.E., Kwappenberg, K. M.C., van der Hulst, J. M., Drijfhout, J. W., Melief, C. J.M., Kenter, G. G., Fleuren, G. J., Offringa, R., van der Burg, S. H.
(2007). High Number of Intraepithelial CD8+ Tumor-Infiltrating Lymphocytes Is Associated with the Absence of Lymph Node Metastases in Patients with Large Early-Stage Cervical Cancer. Cancer Res.
67: 354-361
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de Boer, M. A., Jordanova, E. S., Kenter, G. G., Peters, A. A., Corver, W. E., Trimbos, J. B., Fleuren, G. J.
(2007). High Human Papillomavirus Oncogene mRNA Expression and Not Viral DNA Load Is Associated with Poor Prognosis in Cervical Cancer Patients. Clin. Cancer Res.
13: 132-138
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Fakhry, C., D'souza, G., Sugar, E., Weber, K., Goshu, E., Minkoff, H., Wright, R., Seaberg, E., Gillison, M.
(2006). Relationship between Prevalent Oral and Cervical Human Papillomavirus Infections in Human Immunodeficiency Virus-Positive and -Negative Women. J. Clin. Microbiol.
44: 4479-4485
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Hampl, M., Sarajuuri, H., Wentzensen, N., Bender, H. G., Kueppers, V.
(2006). Effect of Human Papillomavirus Vaccines on Vulvar, Vaginal, and Anal Intraepithelial Lesions and Vulvar Cancer. Obstet Gynecol
108: 1361-1368
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Daley, M. F., Liddon, N., Crane, L. A., Beaty, B. L., Barrow, J., Babbel, C., Markowitz, L. E., Dunne, E. F., Stokley, S., Dickinson, L. M., Berman, S., Kempe, A.
(2006). A National Survey of Pediatrician Knowledge and Attitudes Regarding Human Papillomavirus Vaccination. Pediatrics
118: 2280-2289
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Garcia-Pineres, A. J., Hildesheim, A., Herrero, R., Trivett, M., Williams, M., Atmetlla, I., Ramirez, M., Villegas, M., Schiffman, M., Rodriguez, A. C., Burk, R. D., Hildesheim, M., Freer, E., Bonilla, J., Bratti, C., Berzofsky, J. A., Pinto, L. A.
(2006). Persistent Human Papillomavirus Infection Is Associated with a Generalized Decrease in Immune Responsiveness in Older Women.. Cancer Res.
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Vaccarella, S., Herrero, R., Dai, M., Snijders, P. J.F., Meijer, C. J.L.M., Thomas, J. O., Hoang Anh, P. T., Ferreccio, C., Matos, E., Posso, H., de Sanjose, S., Shin, H.-R., Sukvirach, S., Lazcano-Ponce, E., Ronco, G., Rajkumar, R., Qiao, Y.-L., Munoz, N., Franceschi, S., and IARC HPV Prevalence Surveys Study Group,
(2006). Reproductive Factors, Oral Contraceptive Use, and Human Papillomavirus Infection: Pooled Analysis of the IARC HPV Prevalence Surveys.. Cancer Epidemiol. Biomarkers Prev.
15: 2148-2153
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Castle, P. E., Sadorra, M., Garcia, F., Holladay, E. B., Kornegay, J.
(2006). Pilot Study of a Commercialized Human Papillomavirus (HPV) Genotyping Assay: Comparison of HPV Risk Group to Cytology and Histology. J. Clin. Microbiol.
44: 3915-3917
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Han, J., Swan, D. C., Smith, S. J., Lum, S. H., Sefers, S. E., Unger, E. R., Tang, Y.-W.
(2006). Simultaneous Amplification and Identification of 25 Human Papillomavirus Types with Templex Technology. J. Clin. Microbiol.
44: 4157-4162
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Wieland, U., Brockmeyer, N. H., Weissenborn, S. J., Hochdorfer, B., Stucker, M., Swoboda, J., Altmeyer, P., Pfister, H., Kreuter, A., for the Competence Network HIV/AIDS,
(2006). Imiquimod Treatment of Anal Intraepithelial Neoplasia in HIV-Positive Men.. Arch Dermatol
142: 1438-1444
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Herdman, M.T., Pett, M. R., Roberts, I., Alazawi, W. O.F., Teschendorff, A. E., Zhang, X.-Y., Stanley, M. A., Coleman, N.
(2006). Interferon-{beta} treatment of cervical keratinocytes naturally infected with human papillomavirus 16 episomes promotes rapid reduction in episome numbers and emergence of latent integrants. Carcinogenesis
27: 2341-2353
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Kovacic, M. B., Castle, P. E., Herrero, R., Schiffman, M., Sherman, M. E., Wacholder, S., Rodriguez, A. C., Hutchinson, M. L., Bratti, M. C., Hildesheim, A., Morales, J., Alfaro, M., Burk, R. D.
(2006). Relationships of human papillomavirus type, qualitative viral load, and age with cytologic abnormality.. Cancer Res.
66: 10112-10119
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Hesselink, A. T., Bulkmans, N. W. J., Berkhof, J., Lorincz, A. T., Meijer, C. J. L. M., Snijders, P. J. F.
(2006). Cross-Sectional Comparison of an Automated Hybrid Capture 2 Assay and the Consensus GP5+/6+ PCR Method in a Population-Based Cervical Screening Program.. J. Clin. Microbiol.
44: 3680-3685
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Branca, M, Giorgi, C, Ciotti, M, Santini, D, Di Bonito, L, Costa, S, Benedetto, A, Bonifacio, D, Di Bonito, P, Paba, P, Accardi, L, Mariani, L, Ruutu, M, Favalli, C, Syrjanen, K, on behalf of the HPV-Pathogen Istituto Superiore d,
(2006). Down-regulated nucleoside diphosphate kinase nm23-H1 expression is unrelated to high-risk human papillomavirus but associated with progression of cervical intraepithelial neoplasia and unfavourable prognosis in cervical cancer. J. Clin. Pathol.
59: 1044-1051
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