About this Journal Submit a Manuscript Table of Contents
Obstetrics and Gynecology International
Volume 2013 (2013), Article ID 912780, 15 pages
http://dx.doi.org/10.1155/2013/912780
Review Article

HPV-Based Screening, Triage, Treatment, and Followup Strategies in the Management of Cervical Intraepithelial Neoplasia

1Direction of Chronic Infections and Cancer, Research Center in Infection Diseases, National Institute of Public Health, Avenida Universidad 655, Cerrada Los Pinos y Caminera, Colonia Santa María Ahuacatitlán, Cuernavaca, 62100 Morelos, MEX, Mexico
2National Institute of Medical Sciences and Nutrition “Salvador Zubirán,” Vasco de Quiroga 15, Tlalpan, 14000 México, DF, Mexico

Received 8 October 2012; Accepted 12 March 2013

Academic Editor: W. T. Creasman

Copyright © 2013 Oscar Peralta-Zaragoza et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. WHO/ICO Information Centre on HPV and Cervical Cancer (HPV Information Centre), “Human papillomavirus and related cancers in world,” Summary Report, WHO/ICO, 2010, http://www.who.int/hpvcentre.
  2. J. Doorbar, “Molecular biology of human papillomavirus infection and cervical cancer,” Clinical Science, vol. 110, no. 5, pp. 525–541, 2006. View at Publisher · View at Google Scholar · View at Scopus
  3. D. Pyeon, S. M. Pearce, S. M. Lank, P. Ahlquist, and P. F. Lambert, “Establishment of human papillomavirus infection requires cell cycle progression,” PLoS Pathogens, vol. 5, no. 2, Article ID e1000318, pp. 1–9, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. R. Sankaranarayanan, A. M. Budukh, and R. Rajkumar, “Effective screening programmes for cervical cancer in low- and middle-income developing countries,” Bulletin of the World Health Organization, vol. 79, no. 10, pp. 954–962, 2001. View at Scopus
  5. M. Schiffman, N. Wentzensen, S. Wacholder, W. Kinney, J. C. Gage, and P. E. Castle, “Human papillomavirus testing in the prevention of cervical cancer,” Journal of the National Cancer Institute, vol. 103, no. 5, pp. 368–383, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. E. M. de Villiers, C. Fauquet, T. R. Broker, H. U. Bernard, and H. zur Hausen, “Classification of papillomaviruses,” Virology, vol. 324, no. 1, pp. 17–27, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. H. U. Bernard, “Gene expression of genital human papillomaviruses and considerations on potential antiviral approaches,” Antiviral Therapy, vol. 7, no. 4, pp. 219–237, 2002. View at Scopus
  8. Z. Zheng and C. Baker, “Papillomavirus genome structure, expression and post-transcription regulation,” NIH Public Access, vol. 11, pp. 2286–2302, 2006.
  9. N. Egawa, T. Nakahara, S. Ohno, et al., “The E1 protein of human papillomavirus type 16 is dispensable for maintenance replication of the viral genome,” Journal of Virology, vol. 86, no. 6, pp. 3276–3283, 2012. View at Publisher · View at Google Scholar
  10. E. Ramírez-Salazar, F. Centeno, K. Nieto, A. Valencia-Hernández, M. Salcedo, and E. Garrido, “HPV16 E2 could act as down-regulator in cellular genes implicated in apoptosis, proliferation and cell differentiation,” Virology Journal, vol. 8, article 247, pp. 1–10, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. S. M. Horner and D. DiMaio, “The DNA binding domain of a papillomavirus E2 protein programs a chimeric nuclease to cleave integrated human papillomavirus DNA in HeLa cervical carcinoma cells,” Journal of Virology, vol. 81, no. 12, pp. 6254–6264, 2007. View at Publisher · View at Google Scholar · View at Scopus
  12. J. You, “Papillomavirus interaction with cellular chromatin,” Biochimica et Biophysica Acta, vol. 1799, no. 3-4, pp. 192–199, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. F. Centeno, E. Ramírez-Salazar, E. García-Villa, P. Gariglio, and E. Garrido, “TAF1 interacts with and modulates human papillomavirus 16 E2-dependent transcriptional regulation,” Intervirology, vol. 51, no. 2, pp. 137–143, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. Q. Wang, H. Griffin, S. Souther, et al., “Functional analysis of the human papillomavirus type 16 E1E4 protein provides a mechanism for in vivo and in vitro keratin filament reorganization,” Journal of Virology, vol. 78, no. 2, pp. 821–833, 2004. View at Publisher · View at Google Scholar
  15. J. Khan, C. E. Davy, P. B. McIntosh, et al., “Role of calpain in the formation of human papillomavirus type 16 amyloid fibers and reorganization of the keratin network,” Journal of Virology, vol. 85, no. 19, pp. 9984–9997, 2011. View at Publisher · View at Google Scholar
  16. A. Venuti, F. Paolini, L. Nasir, et al., “Papillomavirus E5: the smallest oncoprotein with many functions,” Molecular Cancer, vol. 10, article 140, 2011. View at Publisher · View at Google Scholar
  17. M. S. Cortese, G. H. Ashrafi, and M. S. Campo, “All 4 di-leucine motifs in the first hydrophobic domain of the E5 oncoprotein of human papillomavirus type 16 are essential for surface MHC class I downregulation activity and E5 endomembrane localization,” International Journal of Cancer, vol. 126, no. 7, pp. 1675–1682, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. V. Bouvard, G. Matlashewski, Z. M. Gu, A. Storey, and L. Banks, “The human papillomavirus type 16 E5 gene cooperates with the E7 gene to stimulate proliferation of primary cells and increases viral gene expression,” Virology, vol. 203, no. 1, pp. 73–80, 1994. View at Publisher · View at Google Scholar · View at Scopus
  19. J. Ghai, R. S. Ostrow, J. Tolar et al., “The E5 gene product of rhesus papillomavirus is an activator of endogenous Ras and phosphatidylinositol-3′-kinase in NIH 3T3 cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 23, pp. 12879–12884, 1996. View at Scopus
  20. T. M. Wise-Draper and S. I. Wells, “Papillomavirus E6 and E7 proteins and their cellular targets,” Frontiers in Bioscience, vol. 13, no. 3, pp. 1003–1017, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. K. H. Vousden and D. P. Lane, “p53 in health and disease,” Nature Reviews Molecular Cell Biology, vol. 8, no. 4, pp. 275–283, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. F. A. Dick and N. J. Dyson, “Three regions of the pRB pocket domain affect its inactivation by human papillomavirus E7 proteins,” Journal of Virology, vol. 76, no. 12, pp. 6224–6234, 2002. View at Publisher · View at Google Scholar · View at Scopus
  23. C. A. Moody and L. A. Laimins, “Human papillomavirus oncoproteins: pathways to transformation,” Nature Reviews Cancer, vol. 10, no. 8, pp. 550–560, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. G. Alp-Avci, “Genomic organization and proteins of human papillomavirus,” Mikrobiyoloji Bülteni, vol. 46, no. 3, pp. 507–515, 2012.
  25. P. Melsheimer, S. Kaul, S. Dobeck, and G. Bastert, “Immunocytochemical detection of HPV high-risk type L1 capsid proteins in LSIL and HSIL as compared with detection of HPV L1 DNA,” Acta Cytologica, vol. 47, no. 2, pp. 124–128, 2003. View at Scopus
  26. M. Toro and A. Llombart-Bosch, “Immunohistochemical detection of the high risk Human Papillomavirus (HPV)-L1 protein in uterine cervix cytologies and biopsies,” Revista Española de Patología, vol. 38, no. 1, pp. 8–13, 2005.
  27. M. Molano, H. Posso, E. Weiderpass et al., “Prevalence and determinants of HPV infection among Colombian women with normal cytology,” British Journal of Cancer, vol. 87, no. 3, pp. 324–333, 2002. View at Publisher · View at Google Scholar · View at Scopus
  28. C. M. Roteli-Martins, N. S. de Carvalho, P. Naud et al., “Prevalence of human papillomavirus infection and associated risk factors in young women in Brazil, Canada, and the United States: a multicenter cross-sectional study,” International Journal of Gynecological Pathology, vol. 30, no. 2, pp. 173–184, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. H. Romanczuk and P. M. Howley, “Disruption of either the E1 or the E2 regulatory gene of human papillomavirus type 16 increases viral immortalization capacity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 89, no. 7, pp. 3159–3163, 1992. View at Scopus
  30. H. Trottier and A. N. Burchell, “Epidemiology of mucosal human papillomavirus infection and associated diseases,” Public Health Genomics, vol. 12, no. 5-6, pp. 291–307, 2009. View at Publisher · View at Google Scholar · View at Scopus
  31. K. Münger, A. Baldwin, K. M. Edwards et al., “Mechanisms of human papillomavirus-induced oncogenesis,” Journal of Virology, vol. 78, no. 21, pp. 11451–11460, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Manavi, G. Hudelist, A. Fink-Retter, D. Gschwantler-Kaulich, K. Pischinger, and K. Czerwenka, “Human papillomavirus DNA integration and messenger RNA transcription in cervical low- and high-risk squamous intraepithelial lesions in Austrian women,” International Journal of Gynecological Cancer, vol. 18, no. 2, pp. 285–294, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. American Congress of Obstetricians and Gynecologists, New Cervical Cancer Screening Recommendations from the U.S, Preventive Services Task Force and the American Cancer Society/American Society for Colposcopy and Cervical Pathology/American Society for Clinical Pathology, 2012, http://www.acog.org/About_ACOG/Announcements/New_Cervical_Cancer_Screening_Recommendations.
  34. K. Nanda, D. C. McCrory, E. R. Myers et al., “Accuracy of the papanicolaou test in screening for and follow-up of cervical cytologic abnormalities: a systematic review,” Annals of Internal Medicine, vol. 132, no. 10, pp. 810–819, 2000. View at Scopus
  35. E. L. Franco, E. Duarte-Franco, and A. Ferenczy, “Prospects for controlling cervical cancer at the turn of the century,” Salud Publica de Mexico, vol. 45, no. 3, pp. S367–S375, 2003. View at Scopus
  36. P. de Cremoux, J. Coste, X. Sastre-Garau et al., “Efficiency of the hybrid capture 2 HPV DNA test in cervical cancer screening: a study by the French society of clinical cytology,” American Journal of Clinical Pathology, vol. 120, no. 4, pp. 492–499, 2003. View at Publisher · View at Google Scholar · View at Scopus
  37. M. Arbyn, F. Buntinx, M. van Ranst, E. Paraskevaidis, P. Martin-Hirsch, and J. Dillner, “Virologic versus cytologic triage of women with equivocal pap smears: a meta-analysis of the accuracy to detect high-grade intraepithelial neoplasia,” Journal of the National Cancer Institute, vol. 96, no. 4, pp. 280–293, 2004. View at Scopus
  38. J. Cuzick, M. H. Mayrand, G. Ronco, P. Snijders, and J. Wardle, “Chapter 10: new dimensions in cervical cancer screening,” Vaccine, vol. 24, no. 3, pp. S90–S97, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. W. Qu, G. Jiang, Y. Cruz et al., “PCR detection of human papillomavirus: comparison between MY09/MY11 and GP5+/GP6+ primer systems,” Journal of Clinical Microbiology, vol. 35, no. 6, pp. 1304–1310, 1997. View at Scopus
  40. S. Strauss, J. Z. Jordens, D. McBride et al., “Detection and typing of human papillomavirus DNA in paired urine and cervical scrapes,” European Journal of Epidemiology, vol. 15, no. 6, pp. 537–543, 1999. View at Publisher · View at Google Scholar · View at Scopus
  41. L. Giovannelli, A. Lama, G. Capra, V. Giordano, P. Aricò, and P. Ammatuna, “Detection of human papillomavirus DNA in cervical samples: analysis of the new PGMY-PCR compared to the hybrid capture II and MY-PCR assays and a two-step nested PCR assay,” Journal of Clinical Microbiology, vol. 42, no. 8, pp. 3861–3864, 2004. View at Publisher · View at Google Scholar · View at Scopus
  42. B. Kleter, L. J. van Doorn, J. ter Schegget et al., “Novel short-fragment PCR assay for highly sensitive broad-spectrum detection of anogenital human papillomaviruses,” American Journal of Pathology, vol. 153, no. 6, pp. 1731–1739, 1998. View at Scopus
  43. A. Josefsson, K. Livak, and U. Gyllensten, “Detection and quantitation of human papillomavirus by using the fluorescent 5′ exonuclease assay,” Journal of Clinical Microbiology, vol. 37, no. 3, pp. 490–496, 1999. View at Scopus
  44. M. Moberg, I. Gustavsson, and U. Gyllensten, “Real-time pcr-based system for simultaneous quantification of human papillomavirus types associated with high risk of cervical cancer,” Journal of Clinical Microbiology, vol. 41, no. 7, pp. 3221–3228, 2003. View at Publisher · View at Google Scholar · View at Scopus
  45. B. Gharizadeh, M. Ghaderi, D. Donnelly, B. Amini, K. L. Wallin, and P. Nyrén, “Multiple-primer DNA sequencing method,” Electrophoresis, vol. 24, no. 7-8, pp. 1145–1151, 2003. View at Scopus
  46. V. Fontaine, C. Mascaux, C. Weyn et al., “Evaluation of combined general primer-mediated PCR sequencing and type-specific PCR strategies for determination of human papillomavirus genotypes in cervical cell specimens,” Journal of Clinical Microbiology, vol. 45, no. 3, pp. 928–934, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. C. Baleriola, D. Millar, J. Melki et al., “Comparison of a novel HPV test with the Hybrid Capture II (hcII) and a reference PCR method shows high specificity and positive predictive value for 13 high-risk human papillomavirus infections,” Journal of Clinical Virology, vol. 42, no. 1, pp. 22–26, 2008. View at Publisher · View at Google Scholar · View at Scopus
  48. H. J. An, N. H. Cho, S. Y. Lee et al., “Correlation of cervical carcinoma and precancerous lesions with human papillomavirus (HPV) genotypes detected with the HPV DNA chip microarray method,” Cancer, vol. 97, no. 7, pp. 1672–1680, 2003. View at Publisher · View at Google Scholar · View at Scopus
  49. C. J. Kim, J. K. Jeong, M. Park et al., “HPV oligonucleotide microarray-based detection of HPV genotypes in cervical neoplastic lesions,” Gynecologic Oncology, vol. 89, no. 2, pp. 210–217, 2003. View at Publisher · View at Google Scholar · View at Scopus
  50. L. Kotaniemi-Talonen, P. Nieminen, A. Anttila, and M. Hakama, “Routine cervical screening with primary HPV testing and cytology triage protocol in a randomised setting,” British Journal of Cancer, vol. 93, no. 8, pp. 862–867, 2005. View at Publisher · View at Google Scholar · View at Scopus
  51. P. E. Castle, M. H. Stoler, T. C. Wright Jr., A. Sharma, T. L. Wright, and C. M. Behrens, “Performance of carcinogenic human papillomavirus (HPV) testing and HPV16 or HPV18 genotyping for cervical cancer screening of women aged 25 years and older: a subanalysis of the ATHENA study,” The Lancet Oncology, vol. 12, no. 9, pp. 880–890, 2011.
  52. S. de Sanjose, W. G. Quint, L. Alemany, et al., “Human papillomavirus genotype attribution in invasive cervical cancer: a retrospective cross-sectional worldwide study,” The Lancet Oncology, vol. 11, no. 11, pp. 1048–1056, 2010.
  53. D. C. Rijkaart, J. Berkhof, L. Rozendaal, et al., “Human papillomavirus testing for the detection of high-grade cervical intraepithelial neoplasia and cancer: final results of the POBASCAM randomised controlled trial,” The Lancet Oncology, vol. 13, no. 1, pp. 78–88, 2012.
  54. G. Ronco, P. Giorgi-Rossi, F. Carozzi et al., “Efficacy of human papillomavirus testing for the detection of invasive cervical cancers and cervical intraepithelial neoplasia: a randomised controlled trial,” The Lancet Oncology, vol. 11, no. 3, pp. 249–257, 2010. View at Publisher · View at Google Scholar · View at Scopus
  55. H. A. Katki, W. K. Kinney, B. Fetterman et al., “Cervical cancer risk for women undergoing concurrent testing for human papillomavirus and cervical cytology: a population-based study in routine clinical practice,” The Lancet Oncology, vol. 12, no. 7, pp. 663–672, 2011, Erratum in: The Lancet Oncology, vol. 12, no. 8, p. 722, 2011. View at Publisher · View at Google Scholar · View at Scopus
  56. R. Murillo, C. Wiesner, R. Cendales, M. Piñeros, and S. Tovar, “Comprehensive evaluation of cervical cancer screening programs: the case of Colombia,” Salud Pública de México, vol. 53, no. 6, pp. 469–477, 2011.
  57. O. Andrés-Gamboa, L. Chicaíza, M. García-Molina, et al., “Cost-effectiveness of conventional cytology and HPV DNA testing for cervical cancer screening in Colombia,” Salud Pública de México, vol. 50, no. 4, pp. 276–285, 2008. View at Publisher · View at Google Scholar
  58. A. Vijayaraghavan, M. Efrusy, G. Lindeque, G. Dreyer, and C. Santas, “Cost effectiveness of high-risk HPV DNA testing for cervical cancer screening in South Africa,” Gynecologic Oncology, vol. 112, no. 2, pp. 377–383, 2009. View at Publisher · View at Google Scholar · View at Scopus
  59. Y. L. Qiao, J. W. Sellors, P. S. Eder et al., “A new HPV-DNA test for cervical-cancer screening in developing regions: a cross-sectional study of clinical accuracy in rural China,” The Lancet Oncology, vol. 9, no. 10, pp. 929–936, 2008. View at Publisher · View at Google Scholar · View at Scopus
  60. T. C. Wright Jr., L. S. Massad, C. J. Dunton, M. Spitzer, E. J. Wilkinson, and D. Solomon, “2006 consensus guidelines for the management of women with abnormal cervical cancer screening tests. 2006 American Society for Colposcopy and Cervical Pathology-sponsored Consensus Conference,” American Journal of Obstetrics and Gynecology, vol. 197, no. 4, pp. 346–355, 2007. View at Publisher · View at Google Scholar · View at Scopus
  61. N. F. Schlecht, R. W. Platt, E. Duarte-Franco et al., “Human papillomavirus infection and time to progression and regression of cervical intraepithelial neoplasia,” Journal of the National Cancer Institute, vol. 95, no. 17, pp. 1336–1343, 2003. View at Scopus
  62. A. B. Moscicki, S. Shiboski, N. K. Hills et al., “Regression of low-grade squamous intra-epithelial lesions in young women,” Lancet, vol. 364, no. 9446, pp. 1678–1683, 2004. View at Publisher · View at Google Scholar · View at Scopus
  63. M. J. Khan, P. E. Castle, A. T. Lorincz et al., “The elevated 10-year risk of cervical precancer and cancer in women with human papillomavirus (HPV) type 16 or 18 and the possible utility of type-specific HPV testing in clinical practice,” Journal of the National Cancer Institute, vol. 97, no. 14, pp. 1072–1079, 2005. View at Publisher · View at Google Scholar · View at Scopus
  64. J. D. Carreon, M. E. Sherman, D. Guillén et al., “CIN2 is a much less reproducible and less valid diagnosis than CIN3: results from a histological review of population-based cervical samples,” International Journal of Gynecological Pathology, vol. 26, no. 4, pp. 441–446, 2007. View at Publisher · View at Google Scholar · View at Scopus
  65. P. Mathevet, D. Dargent, M. Roy, and G. Beau, “A randomized prospective study comparing three techniques of conization: cold knife, laser, and LEEP,” Gynecologic Oncology, vol. 54, no. 2, pp. 175–179, 1994. View at Publisher · View at Google Scholar · View at Scopus
  66. M. Kyrgiou, G. Koliopoulos, P. Martin-Hirsch, M. Arbyn, W. Prendiville, and E. Paraskevaidis, “Obstetric outcomes after conservative treatment for intraepithelial or early invasive cervical lesions: systematic review and meta-analysis,” Lancet, vol. 367, no. 9509, pp. 489–498, 2006. View at Publisher · View at Google Scholar · View at Scopus
  67. M. Arbyn, M. Kyrgiou, C. Simoens et al., “Perinatal mortality and other severe adverse pregnancy outcomes associated with treatment of cervical intraepithelial neoplasia: meta-analysis,” British Medical Journal, vol. 337, no. 7673, article a1284, pp. 798–803, 2008. View at Publisher · View at Google Scholar · View at Scopus
  68. J. Nuovo, J. Melnikow, A. R. Willan, and B. K. S. Chan, “Treatment outcomes for squamous intraepithelial lesions,” International Journal of Gynecology and Obstetrics, vol. 68, no. 1, pp. 25–33, 2000. View at Publisher · View at Google Scholar · View at Scopus
  69. J. Melnikow, C. McGahan, G. F. Sawaya, T. Ehlen, and A. Coldman, “Cervical intraepithelial neoplasia outcomes after treatment: long-term follow-up from the British Columbia Cohort Study,” Journal of the National Cancer Institute, vol. 101, no. 10, pp. 721–728, 2009. View at Publisher · View at Google Scholar · View at Scopus
  70. E. Paraskevaidis, M. Arbyn, A. Sotiriadis et al., “The role of HPV DNA testing in the follow-up period after treatment for CIN: a systematic review of the literature,” Cancer Treatment Reviews, vol. 30, no. 2, pp. 205–211, 2004. View at Publisher · View at Google Scholar · View at Scopus
  71. J. Jones, A. Saleem, N. Rai, et al., “Human Papillomavirus genotype testing combined with cytology as a ‘test of cure’ post treatment: the importance of a persistent viral infection,” Journal of Clinical Virology, vol. 52, no. 2, pp. 88–92, 2011.
  72. S. Venturoli, S. Ambretti, M. Cricca et al., “Correlation of high-risk human papillomavirus genotypes persistence and risk of residual or recurrent cervical disease after surgical treatment,” Journal of Medical Virology, vol. 80, no. 8, pp. 1434–1440, 2008. View at Publisher · View at Google Scholar · View at Scopus
  73. ABEDIA, Database of clinical trials, June 2012, http://www.abedia.com/wiley/index.html.
  74. US National Institutes of Health, Database of clinical trials, July 2012, http://www.nlm.nih.gov/copyright.html, http://clinicaltrials.gov/ct2/home.
  75. X. Y. Niu, Z. L. Peng, W. Q. Duan, H. Wang, and P. Wang, “Inhibition of HPV 16 E6 oncogene expression by RNA interference in vitro and in vivo,” International Journal of Gynecological Cancer, vol. 16, no. 2, pp. 743–751, 2006. View at Publisher · View at Google Scholar · View at Scopus
  76. J. Salazar-León, F. Reyes-Román, A. Meneses-Acosta, et al., “Silencing of HPV16 E6 and E7 oncogenic activities by small interference RNA induces autophagy and apoptosis in human cervical cancer cells,” Journal of Nucleic Acids Investigation, vol. 2, article e10, pp. 59–69, 2011.
  77. M. Jiang and J. Milner, “Selective silencing of viral gene expression in HPV-positive human cervical carcinoma cells treated with siRNA, a primer of RNA interference,” Oncogene, vol. 21, no. 39, pp. 6041–6048, 2002. View at Publisher · View at Google Scholar · View at Scopus
  78. J. T. C. Chang, T. F. Kuo, Y. J. Chen et al., “Highly potent and specific siRNAs against E6 or E7 genes of HPV16-or HPV18-infected cervical cancers,” Cancer Gene Therapy, vol. 17, no. 12, pp. 827–836, 2010. View at Publisher · View at Google Scholar · View at Scopus
  79. T. Fujii, M. Saito, E. Iwasaki et al., “Intratumor injection of small interfering RNA-targeting human papillomavirus 18 E6 and E7 successfully inhibits the growth of cervical cancer,” International Journal of Oncology, vol. 29, no. 3, pp. 541–548, 2006. View at Scopus
  80. S. Y. Wu, A. Singhania, M. Burgess et al., “Systemic delivery of E6/7 siRNA using novel lipidic particles and its application with cisplatin in cervical cancer mouse models,” Gene Therapy, vol. 18, no. 1, pp. 14–22, 2011. View at Publisher · View at Google Scholar · View at Scopus
  81. H. W. Chesson, J. M. Blandford, T. L. Gift, G. Tao, and K. L. Irwin, “The estimated direct medical cost of sexuality transmitted diseases among American youth, 2000,” Perspectives on Sexual and Reproductive Health, vol. 36, no. 1, pp. 11–19, 2004. View at Scopus
  82. D. Blumenthal, “Performance improvement in health care—seizing the moment,” The New England Journal of Medicine, vol. 366, pp. 1953–1955, 2012. View at Publisher · View at Google Scholar
  83. J. A. Aguilar-Pérez, A. G. Leyva-López, D. Angulo-Nájera, A. Salinas, and E. C. Lazcano-Ponce, “Tamizaje en cáncer cervical: conocimiento de la utilidad y uso de citología cervical en México,” Revista de Saúde Pública, vol. 37, no. 1, pp. 100–106, 2003. View at Publisher · View at Google Scholar
  84. M. A. Madrigal-Campa, E. D. Lazcano-Ponce, and C. Infante-Catañeda, “Sobreutilización del servicio de colposcopia en México,” Ginecología y Obstetricia de México, vol. 73, pp. 637–647, 2005.
  85. A. Mahdavi and B. J. Monk, “Vaccines against human papillomavirus and cervical cancer: promises and challenges,” Oncologist, vol. 10, no. 7, pp. 528–538, 2005. View at Publisher · View at Google Scholar · View at Scopus