Comparing human papillomavirus prevalences in women with normal cytology or invasive cervical cancer to rank genotypes according to their oncogenic potential: a meta-analysis of observational studies

BMC Infectious Diseases

Anne CM Thiébaut²  Didier Guillemot⁴  Elisabeth Delarocque-Astagneau²  Isabelle Heard³  Michel Favre¹  Margarita Pons-Salort⁵  Erik Bernard² 

[1] Institut Pasteur, Genetics, Papillomavirus and Human Cancer Unit, 25-28 rue du Dr Roux, 75724 Paris Cedex 15 France;Univ Versailles–St-Quentin-en-Yvelines, EA 4499, UFR des Sciences de la Santé Simone Veil, 2 avenue de la Source de la Bièvre, 78180 Montigny Le Bretonneux France;INSERM, U943, Groupe Hospitalier Pitié–Salpêtrière, 91-105 boulevard de l’Hôpital, 75013 Paris, France;AP–HP, Hôpital Raymond Poincaré, 104 boulevard Raymond Poincaré, 92380 Garches, France;UPMC Univ Paris 06, Cellule Pasteur UPMC, 25-28 rue du Dr Roux, 75724 Paris Cedex 15 France

关键词: Meta-analysis;    Oncogenic potential;    Cervical cancer;    Genotype;    Human papillomavirus;   

Others  :  1146334
DOI  :  10.1186/1471-2334-13-373

 received in 2013-01-30, accepted in 2013-08-08,  发布年份 2013

【 摘 要 】

Background

Mucosal human papillomavirus (HPV) infection is a necessary cause of cervical cancer. Vaccine and non-vaccine genotype prevalences may change after vaccine introduction. Therefore, it appears essential to rank HPV genotypes according to their oncogenic potential for invasive cervical cancer, independently of their respective prevalences.

Methods

We performed meta-analyses of published observational studies and estimated pooled odds ratios with random-effects models for 32 HPV genotypes, using HPV-16 as the reference.

Results

Twenty-seven studies yielded 9,252 HPV-infected women: 2,902 diagnosed with invasive cervical cancer and 6,350 with normal cytology. Expressed as (odds ratio [95% confidence interval]), HPV-18 (0.63 [0.51, 0.78]) ranked closest to HPV-16, while other genotypes showed continuously decreasing relative oncogenic potentials: HPV-45 (0.35 [0.22, 0.55]), HPV-69 (0.28 [0.09, 0.92]), HPV-58 (0.24 [0.15, 0.38]), HPV-31 (0.22 [0.14, 0.35]), HPV-33 (0.22 [0.12, 0.38]), HPV-34 (0.21 [0.06, 0.80]), HPV-67 (0.21 [0.06, 0.67]), HPV-39 (0.17 [0.09, 0.30]), HPV-59 (0.17 [0.09, 0.31]), HPV-73 (0.16 [0.06, 0.41]), and HPV-52 (0.16 [0.11, 0.23]).

Conclusions

Our results support the markedly higher oncogenic potentials of HPV-16 and -18, followed by HPV-31, -33, -39, -45, -52, -58 and -59, and highlight the need for further investigation of HPV-34, -67, -69 and -73. Overall, these findings could have important implications for the prevention of cervical cancer.

【 授权许可】

   
2013 Bernard et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM: GLOBOCAN 2008 v1.2, Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 10 [Internet]. Lyon: International Agency for Research on Cancer; 2010.
• [2]Walboomers JMM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV, Snijders PJF, Peto J, Meijer CJLM, Muñoz N: Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 1999, 189:12-19.
• [3]Bosch FX, Lorincz A, Muñoz N, Meijer CJLM, Shah KV: The causal relation between human papillomavirus and cervical cancer. J Clin Pathol 2002, 55:244-265.
• [4]Muñoz N, Bosch FX, de Sanjosé S, Herrero R, Castellsagué X, Shah KV, Snijders PJF, Meijer CJLM: Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med 2003, 348:518-527.
• [5]Koshiol J, Lindsay L, Pimenta JM, Poole C, Jenkins D, Smith JS: Persistent human papillomavirus infection and cervical neoplasia: a systematic review and meta-analysis. Am J Epidemiol 2008, 168:123-137.
• [6]de Villiers EM, Fauquet C, Broker TR, Bernard HU, zur Hausen H: Classification of papillomaviruses. Virology 2004, 324:17-27.
• [7]Bernard HU, Burk RD, Chen Z, van Doorslaer K, zur Hausen H, de Villiers EM: Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. Virology 2010, 401:70-79.
• [8]Bouvard V, Baan R, Straif K, Grosse Y, Secretan B, El Ghissassi F, Benbrahim-Tallaa L, Guha N, Freeman C, Galichet L, Cogliano V: A review of human carcinogens – Part B: biological agents. Lancet Oncol 2009, 10:321-322.
• [9]Castle PE: The evolving definition of carcinogenic human papillomavirus. Infect Agent Cancer 2009, 4:7. BioMed Central Full Text
• [10]Muñoz N, Castellsagué X, Berrington De González A, Gissmann L: Chapter 1: HPV in the etiology of human cancer. Vaccine 2006, 24(Suppl 3):1-10.
• [11]IARC: Human Papillomaviruses. In IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. Volume 100: A Review of Human Carcinogens - Part B: Biological Agents. Lyon: International Agency for Research on Cancer; 2011:261-319.
• [12]Clifford G, Franceschi S, Diaz M, Muñoz N, Villa LL: Chapter 3: HPV type-distribution in women with and without cervical neoplastic diseases. Vaccine 2006, 24(Suppl 3):26-34.
• [13]de Sanjosé S, Quint WGV, Alemany L, Geraets DT, Klaustermeier JE, Lloveras B, Tous S, Felix A, Bravo LE, Shin HR, Vallejos CS, de Ruiz PA, Lima MA, Guimera N, Clavero O, Alejo M, Llombart-Bosch A, Cheng-Yang C, Tatti SA, Kasamatsu E, Iljazovic E, Odida M, Prado R, Seoud M, Grce M, Usubutun A, Jain A, Suarez GAH, Lombardi LE, Banjo A, Menéndez C, Domingo EJ, Velasco J, Nessa A, Chichareon SCB, Qiao YL, Lerma E, Garland SM, Sasagawa T, Ferrera A, Hammouda D, Mariani L, Pelayo A, Steiner I, Oliva E, Meijer CJLM, Al-Jassar WF, Cruz E, Wright TC, Puras A, Llave CL, Tzardi M, Agorastos T, Garcia-Barriola V, Clavel C, Ordi J, Andújar M, Castellsagué X, Sánchez GI, Nowakowski AM, Bornstein J, Muñoz N, Bosch FX: Human papillomavirus genotype attribution in invasive cervical cancer: a retrospective cross-sectional worldwide study. Lancet Oncol 2010, 11:1048-1056.
• [14]Durham DP, Poolman EM, Ibuka Y, Townsend JP, Galvani AP: Reevaluation of epidemiological data demonstrates that it is consistent with cross-immunity among human papillomavirus types. J Infect Dis 2012, 206:1291-1298.
• [15]Malagón T, Drolet M, Boily MC, Franco EL, Jit M, Brisson J, Brisson M: Cross-protective efficacy of two human papillomavirus vaccines: a systematic review and meta-analysis. Lancet Infect Dis 2012, 12:781-789.
• [16]Pons-Salort M, Letort V, Favre M, Heard I, Dervaux B, Opatowski L, Guillemot D: Exploring individual HPV coinfections is essential to predict HPV-vaccination impact on genotype distribution: a model-based approach. Vaccine 2013, 31:1238-1245.
• [17]Schiffman M, Herrero R, Desalle R, Hildesheim A, Wacholder S, Rodriguez AC, Bratti MC, Sherman ME, Morales J, Guillen D, Alfaro M, Hutchinson M, Wright TC, Solomon D, Chen Z, Schussler J, Castle PE, Burk RD: The carcinogenicity of human papillomavirus types reflects viral evolution. Virology 2005, 337:76-84.
• [18]Guan P, Howell-Jones R, Li N, Bruni L, de Sanjosé S, Franceschi S, Clifford GM: Human papillomavirus types in 115,789 HPV-positive women: a meta-analysis from cervical infection to cancer. Int J Cancer 2012, 131:2349-2359.
• [19]Vandenbroucke JP, von Elm E, Altman DG, Gøtzsche PC, Mulrow CD, Pocock SJ, Poole C, Schlesselman JJ, Egger M: Strengthening the reporting of observational studies in epidemiology (STROBE): explanation and elaboration. PLoS Med 2007, 4:e297.
• [20]DerSimonian R, Laird N: Meta-analysis in clinical trials. Control Clin Trials 1986, 7:177-188.
• [21]Plackett RL: The continuity correction in 2 × 2 tables. Biometrika 1964, 51:327-337.
• [22]Cox DR: The continuity correction. Biometrika 1970, 57:217-219.
• [23]Dickersin K, Berlin JA: Meta-analysis: state-of-the-science. Epidemiol Rev 1992, 14:154-176.
• [24]Higgins JPT, Thompson SG, Deeks JJ, Altman DG: Measuring inconsistency in meta-analyses. BMJ 2003, 327:557-560.
• [25]Chan PK: Human papillomavirus type 58: the unique role in cervical cancers in East Asia. Cell Biosci 2012, 2:17. BioMed Central Full Text
• [26]Egger M, Davey Smith G, Altman DG: Systematic Reviews in Health Care: Meta-analysis in context. London: BMJ; 2001.
• [27]Yusuf S, Peto R, Lewis J, Collins R, Sleight P: Beta blockade during and after myocardial infarction: an overview of the randomized trials. Prog Cardiovasc Dis 1985, 27:335-371.
• [28]StataCorp: Stata Statistical Software: Release 11. College Station, TX: StataCorp; 2009.
• [29]Sterne JAC, Newton HJ, Cox NJ: Meta-Analysis in Stata: An Updated Collection from the Stata Journal. College Station, TX: Stata Press; 2009.
• [30]Abba MC, Gomez MA, Golijow CD: Distribución de los genotipos del virus papiloma humano en infecciones cervicales en mujeres de La Plata, Argentina [Human papillomavirus genotype distribution in cervical infections among woman in La Plata, Argentina]. Rev Argent Microbiol 2003, 35:74-79.
• [31]Alibegashvili T, Clifford GM, Vaccarella S, Baidoshvili A, Gogiashvili L, Tsagareli Z, Kureli I, Snijders PJF, Heideman DAM, van Kemenade FJ, Meijer CJLM, Kordzaia D, Franceschi S: Human papillomavirus infection in women with and without cervical cancer in Tbilisi, Georgia. Cancer Epidemiol 2011, 35:465-470.
• [32]An HJ, Cho NH, Lee SY, Kim IH, Lee C, Kim SJ, Mun MS, Kim SH, Jeong JK: Correlation of cervical carcinoma and precancerous lesions with human papillomavirus (HPV) genotypes detected with the HPV DNA chip microarray method. Cancer 2003, 97:1672-1680.
• [33]Andersson S, Mints M, Sällström J, Wilander E: The relative distribution of oncogenic types of human papillomavirus in benign, pre-malignant and malignant cervical biopsies. A study with human papillomavirus deoxyribonucleic acid sequence analysis. Cancer Detect Prev 2005, 29:37-41.
• [34]Asato T, Maehama T, Nagai Y, Kanazawa K, Uezato H, Kariya K: A large case–control study of cervical cancer risk associated with human papillomavirus infection in Japan, by nucleotide sequencing-based genotyping. J Infect Dis 2004, 189:1829-1832.
• [35]Baay MFD, Tjalma WAA, Weyler J, Goovaerts G, Buytaert P, Van Marck EAE, Lardon F, Vermorken JB: Human papillomavirus infection in the female population of Antwerp, Belgium: prevalence in healthy women, women with premalignant lesions and cervical cancer. Eur J Gynaecol Oncol 2001, 22:204-208.
• [36]Bardin A, Vaccarella S, Clifford GM, Lissowska J, Rekosz M, Bobkiewicz P, Kupryjanczyk J, Krynicki R, Jonska-Gmyrek J, Danska-Bidzinska A, Snijders PJF, Meijer CJLM, Zatonski W, Franceschi S: Human papillomavirus infection in women with and without cervical cancer in Warsaw, Poland. Eur J Cancer 2008, 44:557-564.
• [37]Castellsagué X, Klaustermeier J, Carrilho C, Albero G, Sacarlal J, Quint W, Kleter B, Lloveras B, Ismail MR, de Sanjosé S, Bosch FX, Alonso P, Menéndez C: Vaccine-related HPV genotypes in women with and without cervical cancer in Mozambique: burden and potential for prevention. Int J Cancer 2008, 122:1901-1904.
• [38]Chang DY, Chen RJ, Lee SC, Huang SC: Prevalence of single and multiple infection with human papillomaviruses in various grades of cervical neoplasia. J Med Microbiol 1997, 46:54-60.
• [39]Chaouki N, Bosch FX, Muñoz N, Meijer CJLM, El Gueddari B, El Ghazi A, Deacon J, Castellsagué X, Walboomers JMM: The viral origin of cervical cancer in Rabat, Morocco. Int J Cancer 1998, 75:546-554.
• [40]Cho NH, An HJ, Jeong JK, Kang S, Kim JW, Kim YT, Park TK: Genotyping of 22 human papillomavirus types by DNA chip in Korean women: comparison with cytologic diagnosis. Am J Obstet Gynecol 2003, 188:56-62.
• [41]Ferrera A, Velema JP, Figueroa M, Bulnes R, Toro LA, Claros JM, De Barahona O, Melchers WJG: Human papillomavirus infection, cervical dysplasia and invasive cervical cancer in Honduras: a case–control study. Int J Cancer 1999, 82:799-803.
• [42]Hammouda D, Clifford GM, Pallardy S, Ayyach G, Chékiri A, Boudrich A, Snijders PJF, van Kemenade FJ, Meijer CJLM, Bouhadef A, Zitouni Z, Habib D, Ikezaren N, Franceschi S: Human papillomavirus infection in a population-based sample of women in Algiers, Algeria. Int J Cancer 2011, 128:2224-2229.
• [43]Herrero R, Castle PE, Schiffman M, Bratti MC, Hildesheim A, Morales J, Alfaro M, Sherman ME, Wacholder S, Chen S, Rodriguez AC, Burk RD: Epidemiologic profile of type-specific human papillomavirus infection and cervical neoplasia in Guanacaste, Costa Rica. J Infect Dis 2005, 191:1796-1807.
• [44]Hong D, Ye F, Chen H, Lu W, Cheng Q, Hu Y, Xie X: Distribution of human papillomavirus genotypes in the patients with cervical carcinoma and its precursors in Zhejiang Province, China. Int J Gynecol Cancer 2008, 18:104-109.
• [45]Illades-Aguiar B, Cortés-Malagón EM, Antonio-Véjar V, Zamudio-López N, Alarcón-Romero LDC, Fernández-Tilapa G, Hernández-Sotelo D, Terán-Porcayo MA, Flores-Alfaro E, Leyva-Vázquez MA: Cervical carcinoma in southern Mexico: human papillomavirus and cofactors. Cancer Detect Prev 2009, 32:300-307.
• [46]Illades-Aguiar B, Alarcón-Romero LDC, Antonio-Véjar V, Zamudio-López N, Sales-Linares N, Flores-Alfaro E, Fernández-Tilapa G, Vences-Velázquez A, Muñoz-Valle JF, Leyva-Vázquez MA: Prevalence and distribution of human papillomavirus types in cervical cancer, squamous intraepithelial lesions, and with no intraepithelial lesions in women from southern Mexico. Gynecol Oncol 2010, 117:291-296.
• [47]Keita N, Clifford GM, Koulibaly M, Douno K, Kabba I, Haba M, Sylla BS, van Kemenade FJ, Snijders PJF, Meijer CJLM, Franceschi S: HPV infection in women with and without cervical cancer in Conakry, Guinea. Br J Cancer 2009, 101:202-208.
• [48]Lee HS, Kim KM, Kim SM, Choi YD, Nam JH, Park CS, Choi HS: Human papillomavirus genotyping using HPV DNA chip analysis in Korean women. Int J Gynecol Cancer 2007, 17:497-501.
• [49]Liu X, Zhang S, Ruan Q, Ji Y, Ma L, Zhang Y: Prevalence and type distribution of human papillomavirus in women with cervical lesions in Liaoning Province, China. Int J Gynecol Cancer 2010, 20:147-153.
• [50]Maehama T: Epidemiological study in Okinawa, Japan, of human papillomavirus infection of the uterine cervix. Infect Dis Obstet Gynecol 2005, 13:77-80.
• [51]Park TC, Kim CJ, Koh YM, Lee KH, Yoon JH, Kim JH, Namkoong SE, Park JS: Human papillomavirus genotyping by the DNA chip in the cervical neoplasia. DNA Cell Biol 2004, 23:119-125.
• [52]Sasagawa T, Basha W, Yamazaki H, Inoue M: High-risk and multiple human papillomavirus infections associated with cervical abnormalities in Japanese women. Cancer Epidemiol Biomarkers Prev 2001, 10:45-52.
• [53]Sherpa ATL, Clifford GM, Vaccarella S, Shrestha S, Nygård M, Karki BS, Snijders PJF, Meijer CJLM, Franceschi S: Human papillomavirus infection in women with and without cervical cancer in Nepal. Cancer Causes Control 2010, 21:323-330.
• [54]Tachezy R, Hamsikova E, Hajek T, Mikyskova I, Smahel M, Van RM, Kanka J, Havrankova A, Rob L, Guttner V, Slavik V, Anton M, Kratochvil B, Kotrsova L, Vonka V: Human papillomavirus genotype spectrum in Czech women: correlation of HPV DNA presence with antibodies against HPV-16, 18, and 33 virus-like particles. J Med Virol 1999, 58:378-386.
• [55]Tornesello ML, Duraturo ML, Botti G, Greggi S, Piccoli R, De Palo G, Montella M, Buonaguro L, Buonaguro FM: Prevalence of alpha-papillomavirus genotypes in cervical squamous intraepithelial lesions and invasive cervical carcinoma in the Italian population. J Med Virol 2006, 78:1663-1672.
• [56]Wu D, Cai L, Huang M, Zheng Y, Yu J: Prevalence of genital human papillomavirus infection and genotypes among women from Fujian Province, PR China. Eur J Obstet Gynecol Reprod Biol 2010, 151:86-90.
• [57]Li N, Franceschi S, Howell-Jones R, Snijders PJF, Clifford GM: Human papillomavirus type distribution in 30,848 invasive cervical cancers worldwide: variation by geographical region, histological type and year of publication. Int J Cancer 2011, 128:927-935.
• [58]Schiffman M, Rodriguez AC, Chen Z, Wacholder S, Herrero R, Hildesheim A, Desalle R, Befano B, Yu K, Safaeian M, Sherman ME, Morales J, Guillen D, Alfaro M, Hutchinson M, Solomon D, Castle PE, Burk RD: A population-based prospective study of carcinogenic human papillomavirus variant lineages, viral persistence, and cervical neoplasia. Cancer Res 2010, 70:3159-3169.
• [59]Smith JS, Lindsay L, Hoots B, Keys J, Franceschi S, Winer R, Clifford GM: Human papillomavirus type distribution in invasive cervical cancer and high-grade cervical lesions: a meta-analysis update. Int J Cancer 2007, 121:621-632.
• [60]Insinga RP, Liaw KL, Johnson LG, Madeleine MM: A systematic review of the prevalence and attribution of human papillomavirus types among cervical, vaginal, and vulvar precancers and cancers in the United States. Cancer Epidemiol Biomarkers Prev 2008, 17:1611-1622.
• [61]Hammouda D, Muñoz N, Herrero R, Arslan A, Bouhadef A, Oublil M, Djedeat B, Fontanière B, Snijders P, Meijer C, Franceschi S: Cervical carcinoma in Algiers, Algeria: human papillomavirus and lifestyle risk factors. Int J Cancer 2005, 113:483-489.
• [62]de Sanjosé S, Diaz M, Castellsagué X, Clifford G, Bruni L, Muñoz N, Bosch FX: Worldwide prevalence and genotype distribution of cervical human papillomavirus DNA in women with normal cytology: a meta-analysis. Lancet Infect Dis 2007, 7:453-459.
• [63]Bruni L, Diaz M, Castellsagué X, Ferrer E, Bosch FX, de Sanjosé S: Cervical human papillomavirus prevalence in 5 continents: meta-analysis of 1 million women with normal cytological findings. J Infect Dis 2010, 202:1789-1799.
• [64]Borenstein M, Hedges LV, Higgins JPT, Rothstein HR: Introduction to Meta-Analysis. Chichester: John Wiley & Sons; 2009.
• [65]Sweeting MJ, Sutton AJ, Lambert PC: What to add to nothing? Use and avoidance of continuity corrections in meta-analysis of sparse data. Stat Med 2004, 23:1351-1375.
• [66]Wang SS, Zuna RE, Wentzensen N, Dunn ST, Sherman ME, Gold MA, Schiffman M, Wacholder S, Allen RA, Block I, Downing K, Jeronimo J, Carreon JD, Safaeian M, Brown D, Walker JL: Human papillomavirus cofactors by disease progression and human papillomavirus types in the study to understand cervical cancer early endpoints and determinants. Cancer Epidemiol Biomarkers Prev 2009, 18:113-120.
• [67]Castle PE, Shaber R, Lamere BJ, Kinney W, Fetterma B, Poitras N, Lorey T, Schiffman M, Dunne A, Ostolaza JM, McKinney S, Burk RD: Human papillomavirus (HPV) genotypes in women with cervical precancer and cancer at Kaiser Permanente Northern California. Cancer Epidemiol Biomarkers Prev 2011, 20:946-953.
• [68]FUTURE II Study Group: Quadrivalent vaccine against human papillomavirus to prevent high-grade cervical lesions. N Engl J Med 2007, 356:1915-1927.
• [69]Paavonen J, Naud P, Salmeron J, Wheeler CM, Chow SN, Apter D, Kitchener H, Castellsague X, Teixeira JC, Skinner SR, Hedrick J, Jaisamrarn U, Limson G, Garland S, Szarewski A, Romanowski B, Aoki FY, Schwarz TF, Poppe WAJ, Bosch FX, Jenkins D, Hardt K, Zahaf T, Descamps D, Struyf F, Lehtinen M, Dubin G: Efficacy of human papillomavirus (HPV)-16/18 AS04-adjuvanted vaccine against cervical infection and precancer caused by oncogenic HPV types (PATRICIA): final analysis of a double-blind, randomised study in young women. Lancet 2009, 374:301-314.
• [70]Schiffman M, Castle PE: The promise of global cervical-cancer prevention. N Engl J Med 2005, 353:2101-2104.
• [71]Ostör AG: Natural history of cervical intraepithelial neoplasia: a critical review. Int J Gynecol Pathol 1993, 12:186-192.
• [72]van der Graaf Y, Molijn A, Doornewaard H, Quint W, van Doorn LJ, van den Tweel J: Human papillomavirus and the long-term risk of cervical neoplasia. Am J Epidemiol 2002, 156:158-164.
• [73]Katki HA, Kinney WK, Fetterman B, Lorey T, Poitras NE, Cheung L, Demuth F, Schiffman M, Wacholder S, Castle PE: Cervical cancer risk for women undergoing concurrent testing for human papillomavirus and cervical cytology: a population-based study in routine clinical practice. Lancet Oncol 2011, 12:663-672.
• [74]Franco EL, Schlecht NF, Saslow D: The epidemiology of cervical cancer. Cancer J 2003, 9:348-359.
• [75]Choi YH, Chapman R, Gay N, Jit M: Potential overestimation of HPV vaccine impact due to unmasking of non-vaccine types: quantification using a multi-type mathematical model. Vaccine 2012, 30:3383-3388.
• [76]Schiffman M, Clifford G, Buonaguro FM: Classification of weakly carcinogenic human papillomavirus types: addressing the limits of epidemiology at the borderline. Infect Agent Cancer 2009, 4:8. BioMed Central Full Text
• [77]Opalka D, Matys K, Bojczuk P, Green T, Gesser R, Saah A, Haupt R, Dutko F, Esser MT: Multiplexed serologic assay for nine anogenital human papillomavirus types. Clin Vaccine Immunol 2010, 17:818-827.
• [78]Franceschi S, Denny L, Irwin KL, Jeronimo J, Lopalco PL, Monsonego J, Peto J, Ronco G, Sasieni P, Wheeler CM: EUROGIN 2010 roadmap on cervical cancer prevention. Int J Cancer 2011, 128:2765-2774.
• [79]Peres J: For cancers caused by HPV, two vaccines were just the beginning. J Natl Cancer Inst 2011, 103:360-362.