Detection and quantification of human papillomavirus genital infections: Virological, epidemiological, and clinical applications.

Medecine et Maladies Infectieuses

Volumn 41, Issue 2, 2011, Pages 68-79

  Carcopino, X ^a,b,c   Henry, M ^b   Olive, D ^c   Boubli, L ^a   Tamalet, C ^b  

^a HÔPITAL NORD   (France)

^b TIMONE HOSPITAL   (France)

^c INSTITUT PAOLI CALMETTES   (France)

Author keywords

Cancer du col de l'ut rus; Cervical cancer; Charge virale; Human papillomavirus; Papillomavirus humain; Viral load

Indexed keywords

PROTEIN E6; PROTEIN E7; TELOMERASE; TUMOR SUPPRESSOR PROTEIN; DIAGNOSTIC AGENT; HUMAN PAPILLOMAVIRUS VACCINE L1, TYPE 6,11,16,18; WART VIRUS VACCINE;

ARTICLE; CANCER GRADING; CANCER RISK; COLPOSCOPY; FEMALE GENITAL TRACT INFECTION; HUMAN; INTERMETHOD COMPARISON; PAPILLOMAVIRUS INFECTION; QUANTITATIVE ANALYSIS; SCREENING TEST; SENSITIVITY AND SPECIFICITY; UTERINE CERVIX CARCINOMA IN SITU; UTERINE CERVIX CYTOLOGY; VIROLOGY; VIRUS DETECTION; VIRUS LOAD; WART VIRUS; WOMEN'S HEALTH; ALPHAPAPILLOMAVIRUS; CLASSIFICATION; DNA PROBE; FEMALE; GENETICS; ISOLATION AND PURIFICATION; MASS SCREENING; METHODOLOGY; PATHOGENICITY; POLYMERASE CHAIN REACTION; PREGNANCY; PREGNANCY COMPLICATION; PREVALENCE; REVIEW; UTERINE CERVICITIS; UTERINE CERVIX TUMOR; VACCINATION; VAGINA SMEAR; VIRUS LATENCY;

ALPHAPAPILLOMAVIRUS; CERVICAL INTRAEPITHELIAL NEOPLASIA; COLPOSCOPY; DNA PROBES, HPV; FEMALE; HUMANS; MASS SCREENING; PAPILLOMAVIRUS INFECTIONS; PAPILLOMAVIRUS VACCINES; POLYMERASE CHAIN REACTION; PREGNANCY; PREGNANCY COMPLICATIONS, INFECTIOUS; PREVALENCE; SENSITIVITY AND SPECIFICITY; UTERINE CERVICAL NEOPLASMS; UTERINE CERVICITIS; VACCINATION; VAGINAL SMEARS; VIRAL LOAD; VIRUS LATENCY;

EID: 79952188154     PISSN: 0399077X     EISSN: 17696690     Source Type: Journal    
DOI: 10.1016/j.medmal.2010.07.013     Document Type: Article

References (157)

1. Levêque J., Bergeron C., Boulanger J.C. Prevention of cervical cancer. Method and organization. J Gynecol Obstet Biol Reprod 2008, 37(Suppl. 1):S112-S113.
2. CNGOF. Recommandations pour la pratique clinique: prévention du cancer du col de l'utérus. Mises à jour en gynécologie médicale. Paris: Vigot; 2007. p. 527-41.
3. Rouzier R. Management of CIN1. J Gynecol Obstet Biol Reprod 2008, 37(Suppl. 1):S114-S120.
4. Belot A., Grosclaude P., Bossard N., Jougla E., Benhamou E., Delafosse P., et al. Cancer incidence and mortality in France over the period 1980-2005. Rev Epidemiol Sante Publique 2008, 56(3):159-175.
5. zur Hausen H. Papillomaviruses in the causation of human cancers - A brief historical account. Virology 2009, 384(2):260-265.
6. zur Hausen H. Papillomaviruses and cancer: from basic studies to clinical application. Nat Rev 2002, 2(5):342-350.
7. zur Hausen H. Papillomaviruses causing cancer: evasion from host-cell control in early events in carcinogenesis. J Natl Cancer Inst 2000, 92(9):690-698.
8. ACOG Practice Bulletin. Clinical management guidelines for obstetrician-gynecologists. Number 45, August 2003. Cervical cytology screening (replaces committee opinion 152, March 1995). Obstet Gynecol 2003;102(2):417-27.
9. Évaluation de l'intérêt de la recherche des Papillomavirus humains (HPV) dans le dépistage des lésions précancéreuses et cancéreuses du col de l'utérus. Anaes; 2004.
10. Mergui J.L., Polena V., David-Montefiore E., Uzan S. Guidelines for the follow-up of women treated for high-grade cervical neoplasia. J Gynecol Obstet Biol Reprod 2008, 37(Suppl. 1):S121-S130.
11. Arbyn M., Sasieni P., Meijer C.J., Clavel C., Koliopoulos G., Dillner J. Chapter 9: clinical applications of HPV testing: a summary of meta-analyses. Vaccine 2006, 24(Suppl. 3):S78-S89.
12. Arbyn M., Paraskevaidis E., Martin-Hirsch P., Prendiville W., Dillner J. Clinical utility of HPV-DNA detection: triage of minor cervical lesions, follow-up of women treated for high-grade CIN: an update of pooled evidence. Gynecol Oncol 2005, 99(3 Suppl. 1):S7-11.
13. Zielinski G.D., Bais A.G., Helmerhorst T.J., Verheijen R.H., de Schipper F.A., Snijders P.J., et al. HPV testing and monitoring of women after treatment of CIN 3: review of the literature and meta-analysis. Obstet Gynecol Surv 2004, 59(7):543-553.
14. Arbyn M., Buntinx F., Van Ranst M., Paraskevaidis E., Martin-Hirsch P., Dillner J. Virologic versus cytologic triage of women with equivocal Pap smears: a meta-analysis of the accuracy to detect high-grade intraepithelial neoplasia. J Natl Cancer Inst 2004, 96(4):280-293.
15. Koliopoulos G., Arbyn M., Martin-Hirsch P., Kyrgiou M., Prendiville W., Paraskevaidis E. Diagnostic accuracy of human papillomavirus testing in primary cervical screening: a systematic review and meta-analysis of non-randomized studies. Gynecol Oncol 2007, 104(1):232-246.
16. Yugawa T., Kiyono T. Molecular mechanisms of cervical carcinogenesis by high-risk human papillomaviruses: novel functions of E6 and E7 oncoproteins. Rev Med Virol 2009, 19(2):97-113.
17. Burchell A.N., Winer R.L., de Sanjose S., Franco E.L. Chapter 6: epidemiology and transmission dynamics of genital HPV infection. Vaccine 2006, 24(Suppl. 3). S3/52-61.
18. Munoz N., Bosch F.X., de Sanjose S., Herrero R., Castellsague X., Shah K.V., et al. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med 2003, 348(6):518-527.
19. Kjaer S.K., van den Brule A.J., Bock J.E., Poll P.A., Engholm G., Sherman M.E., et al. Human papillomavirus: the most significant risk determinant of cervical intraepithelial neoplasia. Int J Cancer 1996, 65(5):601-606.
20. Schiffman M.H., Bauer H.M., Hoover R.N., Glass A.G., Cadell D.M., Rush B.B., et al. Epidemiologic evidence showing that human papillomavirus infection causes most cervical intraepithelial neoplasia. J Natl Cancer Inst 1993, 85(12):958-964.
21. Munoz N., Bosch F.X., de Sanjose S., Tafur L., Izarzugaza I., Gili M., et al. The causal link between human papillomavirus and invasive cervical cancer: a population-based case-control study in Colombia and Spain. Int J Cancer 1992, 52(5):743-749.
22. Walboomers J.M., Jacobs M.V., Manos M.M., Bosch F.X., Kummer J.A., Shah K.V., et al. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 1999, 189(1):12-19.
23. Pretet J.L., Jacquard A.C., Carcopino X., Charlot J.F., Bouhour D., Kantelip B., et al. Human papillomavirus (HPV) genotype distribution in invasive cervical cancers in France: EDITH study. Int J Cancer 2008, 122(2):428-432.
24. Pretet J.L., Jacquard A.C., Carcopino X., Monnier-Benoit S., Averous G., Soubeyrand B., et al. Human papillomavirus genotype distribution in high grade cervical lesions (CIN 2/3) in France: EDITH study. Int J Cancer 2008, 122(2):424-427.
25. Pretet J.L., Jacquard A.C., Saunier M., Clavel C., Dachez R., Gondry J., et al. Human papillomavirus genotype distribution in low-grade squamous intraepithelial lesions in France and comparison with CIN2/3 and invasive cervical cancer: the EDiTH III study. Gynecol Oncol 2008, 110(2):179-184.
26. Aubin F., Pretet J.L., Jacquard A.C., Saunier M., Carcopino X., Jaroud F., et al. Human papillomavirus genotype distribution in external acuminata condylomata: a Large French National Study (EDiTH IV). Clin Infect Dis 2008, 47(5):610-615.
27. Winer R.L., Feng Q., Hughes J.P., O'Reilly S., Kiviat N.B., Koutsky L.A. Risk of female human papillomavirus acquisition associated with first male sex partner. J Infect Dis 2008, 197(2):279-282.
28. Winer R.L., Hughes J.P., Feng Q., O'Reilly S., Kiviat N.B., Holmes K.K., et al. Condom use and the risk of genital human papillomavirus infection in young women. N Engl J Med 2006, 354(25):2645-2654.
29. Dalstein V., Riethmuller D., Pretet J.L., Le Bail Carval K., Sautiere J.L., Carbillet J.P., et al. Persistence and load of high-risk HPV are predictors for development of high-grade cervical lesions: a longitudinal French cohort study. Int J Cancer 2003, 106(3):396-403.
30. Woodman C.B., Collins S., Winter H., Bailey A., Ellis J., Prior P., et al. Natural history of cervical human papillomavirus infection in young women: a longitudinal cohort study. Lancet 2001, 357(9271):1831-1836.
31. Ho G.Y., Bierman R., Beardsley L., Chang C.J., Burk R.D. Natural history of cervicovaginal papillomavirus infection in young women. N Engl J Med 1998, 338(7):423-428.
32. Franco E.L., Villa L.L., Sobrinho J.P., Prado J.M., Rousseau M.C., Desy M., et al. Epidemiology of acquisition and clearance of cervical human papillomavirus infection in women from a high-risk area for cervical cancer. J Infect Dis 1999, 180(5):1415-1423.
33. Bosch F.X., Munoz N. The viral etiology of cervical cancer. Virus Res 2002, 89(2):183-190.
34. Schlecht N.F., Kulaga S., Robitaille J., Ferreira S., Santos M., Miyamura R.A., et al. Persistent human papillomavirus infection as a predictor of cervical intraepithelial neoplasia. JAMA 2001, 286(24):3106-3114.
35. Koutsky L. Epidemiology of genital human papillomavirus infection. Am J Med 1997, 102(5A):3-8.
36. Cibas E.S., Hong X., Crum C.P., Feldman S. Age-specific detection of high risk HPV DNA in cytologically normal, computer-imaged ThinPrep Pap samples. Gynecol Oncol 2007, 104(3):702-706.
37. Jacobs M.V., Walboomers J.M., Snijders P.J., Voorhorst F.J., Verheijen R.H., Fransen-Daalmeijer N., et al. Distribution of 37 mucosotropic HPV types in women with cytologically normal cervical smears: the age-related patterns for high-risk and low-risk types. Int J Cancer 2000, 87(2):221-227.
38. Agorastos T., Dinas K., Lloveras B., de Sanjose S., Kornegay J.R., Bonti H., et al. Human papillomavirus testing for primary screening in women at low risk of developing cervical cancer. The Greek experience. Gynecol Oncol 2005, 96(3):714-720.
39. Hildesheim A., Schiffman M.H., Gravitt P.E., Glass A.G., Greer C.E., Zhang T., et al. Persistence of type-specific human papillomavirus infection among cytologically normal women. J Infectious Dis 1994, 169(2):235-240.
40. Vernon S.D., Unger E.R., Williams D. Comparison of human papillomavirus detection and typing by cycle sequencing, line blotting, and hybrid capture. J Clin Microbiol 2000, 38(2):651-655.
41. Schneider A., Hoyer H., Lotz B., Leistritza S., Kuhne-Heid R., Nindl I., et al. Screening for high-grade cervical intra-epithelial neoplasia and cancer by testing for high-risk HPV, routine cytology or colposcopy. Int J Cancer 2000, 89(6):529-534.
42. Coutlee F., Gravitt P., Kornegay J., Hankins C., Richardson H., Lapointe N., et al. Use of PGMY primers in L1 consensus PCR improves detection of human papillomavirus DNA in genital samples. J Clin Microbiol 2002, 40(3):902-907.
43. van Doorn L.J., Quint W., Kleter B., Molijn A., Colau B., Martin M.T., et al. Genotyping of human papillomavirus in liquid cytology cervical specimens by the PGMY line blot assay and the SPF(10) line probe assay. J Clin Microbiol 2002, 40(3):979-983.
44. Kleter B., van Doorn L.J., ter Schegget J., Schrauwen L., van Krimpen K., Burger M., et al. Novel short-fragment PCR assay for highly sensitive broad-spectrum detection of anogenital human papillomaviruses. Am J Pathol 1998, 153(6):1731-1739.
45. Galan-Sanchez F., Rodriguez-Iglesias M.A. Comparison of human papillomavirus genotyping using commercial assays based on PCR and reverse hybridization methods. APMIS 2009, 117(10):708-715.
46. van Ham M.A., Bakkers J.M., Harbers G.K., Quint W.G., Massuger L.F., Melchers W.J. Comparison of two commercial assays for detection of human papillomavirus (HPV) in cervical scrape specimens: validation of the Roche AMPLICOR HPV test as a means to screen for HPV genotypes associated with a higher risk of cervical disorders. J Clin Microbiol 2005, 43(6):2662-2667.
47. Terry G., Ho L., Londesborough P., Cuzick J., Mielzynska-Lohnas I., Lorincz A. Detection of high-risk HPV types by the hybrid capture 2 test. J Med Virol 2001, 65(1):155-162.
48. Papachristou E., Sypsa V., Paraskevis D., Gkekas A., Politi E., Nicolaidou E., et al. Prevalence of different HPV types and estimation of prognostic risk factors based on the linear array HPV genotyping test. J Med Virol 2009, 81(12):2059-2065.
49. Ginocchio C.C., Barth D., Zhang F. Comparison of the Third Wave Invader human papillomavirus (HPV) assay and the digene HPV hybrid capture 2 assay for detection of high-risk HPV DNA. J Clin Microbiol 2008, 46(5):1641-1646.
50. Tang N., Huang S., Erickson B., Mak W.B., Salituro J., Robinson J., et al. High-risk HPV detection and concurrent HPV 16 and 18 typing with Abbott RealTime High Risk HPV test. J Clin Virol 2009, 45(Suppl. 1):S25-S28.
51. Lorincz A.T., Castle P.E., Sherman M.E., Scott D.R., Glass A.G., Wacholder S., et al. Viral load of human papillomavirus and risk of CIN3 or cervical cancer. Lancet 2002, 360(9328):228-229.
52. Carcopino X., Henry M., Benmoura D., Fallabregues A.S., Richet H., Boubli L., et al. Determination of HPV type 16 and 18 viral load in cervical smears of women referred to colposcopy. J Med Virol 2006, 78(8):1131-1140.
53. Saunier M., Monnier-Benoit S., Mauny F., Dalstein V., Briolat J., Riethmuller D., et al. Analysis of human papillomavirus type 16 (HPV16) DNA load and physical state for identification of HPV16-infected women with high-grade lesions or cervical carcinoma. J Clin Microbiol 2008, 46(11):3678-3685.
54. Gravitt P.E., Peyton C., Wheeler C., Apple R., Higuchi R., Shah K.V. Reproducibility of HPV 16 and HPV 18 viral load quantitation using TaqMan real-time PCR assays. J Virol Methods 2003, 112(1-2):23-33.
55. Pretet J.L., Dalstein V., Monnier-Benoit S., Delpeut S., Mougin C. High risk HPV load estimated by Hybrid Capture II correlates with HPV16 load measured by real-time PCR in cervical smears of HPV16-infected women. J Clin Virol 2004, 31(2):140-147.
56. Gravitt P.E., Burk R.D., Lorincz A., Herrero R., Hildesheim A., Sherman M.E., et al. A comparison between real-time polymerase chain reaction and hybrid capture 2 for human papillomavirus DNA quantitation. Cancer Epidemiol Biomarkers Prev 2003, 12(6):477-484.
57. Roberts I., Ng G., Foster N., Stanley M., Herdman M.T., Pett M.R., et al. Critical evaluation of HPV16 gene copy number quantification by SYBR green PCR. BMC Biotechnol 2008, 8:57.
58. Monnier-Benoît S., Dalstein V., Riethmuller D., Lalaoui N., Mougin C., Pretet J.L. Dynamics of HPV16 DNA load reflect the natural history of cervical HPV-associated lesions. J Clin Virol 2006, 35(3):270-277.
59. Quinn M., Babb P., Jones J., Allen E. Effect of screening on incidence of and mortality from cancer of cervix in England: evaluation based on routinely collected statistics. BMJ 1999, 318(7188):904-908.
60. Sasieni P.D., Cuzick J., Lynch-Farmery E. Estimating the efficacy of screening by auditing smear histories of women with and without cervical cancer. The National Co-ordinating Network for Cervical Screening Working Group. Br J Cancer 1996, 73(8):1001-1005.
61. Cuzick J., Clavel C., Petry K.U., Meijer C.J., Hoyer H., Ratnam S., et al. Overview of the European and North American studies on HPV testing in primary cervical cancer screening. Int J Cancer 2006, 119(5):1095-1101.
62. Stoler M.H., Schiffman M. Interobserver reproducibility of cervical cytologic and histologic interpretations: realistic estimates from the ASCUS-LSIL Triage Study. JAMA 2001, 285(11):1500-1505.
63. Boulanger J.C., Fauvet R., Urrutiaguer S., Drean Y., Sevestre H., Ganry O., et al. Cytological history of cases of invasive cervical cancer diagnosed in France in 2006. Gynecol Obstet Fertil 2007, 35(9):764-771.
64. Sankaranarayanan R., Nene B.M., Shastri S.S., Jayant K., Muwonge R., Budukh A.M., et al. HPV screening for cervical cancer in rural India. N Engl J Med 2009, 360(14):1385-1394.
65. Cuzick J., Szarewski A., Cubie H., Hulman G., Kitchener H., Luesley D., et al. Management of women who test positive for high-risk types of human papillomavirus: the HART study. Lancet 2003, 362(9399):1871-1876.
66. Mayrand M.H., Duarte-Franco E., Rodrigues I., Walter S.D., Hanley J., Ferenczy A., et al. Human papillomavirus DNA versus Papanicolaou screening tests for cervical cancer. N Engl J Med 2007, 357(16):1579-1588.
67. Bulkmans N.W., Berkhof J., Rozendaal L., van Kemenade F.J., Boeke A.J., Bulk S., et al. Human papillomavirus DNA testing for the detection of cervical intraepithelial neoplasia grade 3 and cancer: 5-year follow-up of a randomised controlled implementation trial. Lancet 2007, 370(9601):1764-1772.
68. Hoyer H., Scheungraber C., Kuehne-Heid R., Teller K., Greinke C., Leistritz S., et al. Cumulative 5-year diagnoses of CIN2, CIN3 or cervical cancer after concurrent high-risk HPV and cytology testing in a primary screening setting. Int J Cancer 2005, 116(1):136-143.
69. Clavel C., Cucherousset J., Lorenzato M., Caudroy S., Nou J.M., Nazeyrollas P., et al. Negative human papillomavirus testing in normal smears selects a population at low risk for developing high-grade cervical lesions. Br J Cancer 2004, 90(9):1803-1808.
70. Dalstein V., Riethmuller D., Sautiere J.L., Pretet J.L., Kantelip B., Schaal J.P., et al. Detection of cervical precancer and cancer in a hospital population; benefits of testing for human papillomavirus. Eur J Cancer 2004, 40(8):1225-1232.
71. Salmeron J., Lazcano-Ponce E., Lorincz A., Hernandez M., Hernandez P., Leyva A., et al. Comparison of HPV-based assays with Papanicolaou smears for cervical cancer screening in Morelos State, Mexico. Cancer Causes Control 2003, 14(6):505-512.
72. Naucler P., Ryd W., Tornberg S., Strand A., Wadell G., Elfgren K., et al. Human papillomavirus and Papanicolaou tests to screen for cervical cancer. N Engl J Med 2007, 357(16):1589-1597.
73. Kotaniemi-Talonen L., Nieminen P., Anttila A., Hakama M. Routine cervical screening with primary HPV testing and cytology triage protocol in a randomised setting. Br J Cancer 2005, 93(8):862-867.
74. Cuzick J., Szarewski A., Mesher D., Cadman L., Austin J., Perryman K., et al. Long-term follow-up of cervical abnormalities among women screened by HPV testing and cytology-Results from the Hammersmith study. Int J Cancer 2008, 122(10):2294-2300.
75. Riethmuller D., Pretet J.L., Denis F., Aubin F., Pradat P., Clavel C., et al. Expected impact of a quadrivalent HPV vaccine in France. J Gynecol Obstet Biol Reprod 2009, 38(5):389-395.
76. Bergeron C., Breugelmans J.G., Bouee S., Lorans C., Bernard S., Remy V. Cervical cancer, screening and associated treatment costs in France. Gynecol Obstet Fertil 2006, 34(11):1036-1042.
77. Levêque J, Morcel K, Harlicot JP, Foucher F, Coiffic J, Bauville E. Quelles recommandations du CNGOF pour le vaccin et le dépistage de demain ? In: CNGOF, editor. Mises à jour en gynécologie médicale. Paris: Vigot; 2007. p. 193-206.
78. Boulet G.A., Horvath C.A., Berghmans S., Bogers J. Human papillomavirus in cervical cancer screening: important role as biomarker. Cancer Epidemiol Biomarkers Prev 2008, 17(4):810-817.
79. Sun C.A., Lai H.C., Chang C.C., Neih S., Yu C.P., Chu T.Y. The significance of human papillomavirus viral load in prediction of histologic severity and size of squamous intraepithelial lesions of uterine cervix. Gynecol Oncol 2001, 83(1):95-99.
80. Damay A., Didelot-Rousseau M.N., Costes V., Konate I., Ouedraogo A., Nagot N., et al. Viral load and physical status of human papillomavirus (HPV) 18 in cervical samples from female sex workers infected with HPV 18 in Burkina Faso. J Med Virol 2009, 81(10):1786-1791.
81. Lefevre J., Hankins C., Money D., Rachlis A., Pourreaux K., Coutlee F. Human papillomavirus type 16 viral load is higher in human immunodeficiency virus-seropositive women with high-grade squamous intraepithelial lesions than in those with normal cytology smears. J Clin Microbiol 2004, 42(5):2212-2215.
82. Andersson S., Safari H., Mints M., Lewensohn-Fuchs I., Gyllensten U., Johansson B. Type distribution, viral load and integration status of high-risk human papillomaviruses in pre-stages of cervical cancer (CIN). Br J Cancer 2005, 92(12):2195-2200.
83. Cricca M., Morselli-Labate A.M., Venturoli S., Ambretti S., Gentilomi G.A., Gallinella G., et al. Viral DNA load, physical status and E2/E6 ratio as markers to grade HPV16 positive women for high-grade cervical lesions. Gynecol Oncol 2007, 106(3):549-557.
84. Gravitt P.E., Kovacic M.B., Herrero R., Schiffman M., Bratti C., Hildesheim A., et al. High load for most high risk human papillomavirus genotypes is associated with prevalent cervical cancer precursors but only HPV16 load predicts the development of incident disease. Int J Cancer 2007, 121(12):2787-2793.
85. Kovacic M.B., Castle P.E., Herrero R., Schiffman M., Sherman M.E., Wacholder S., et al. Relationships of human papillomavirus type, qualitative viral load, and age with cytologic abnormality. Cancer Res 2006, 66(20):10112-10119.
86. Kulmala S.M., Syrjanen S.M., Gyllensten U.B., Shabalova I.P., Petrovichev N., Tosi P., et al. Early integration of high copy HPV16 detectable in women with normal and low grade cervical cytology and histology. J Clin Pathol 2006, 59(5):513-517.
87. Payan C., Ducancelle A., Aboubaker M.H., Caer J., Tapia M., Chauvin A., et al. Human papillomavirus quantification in urine and cervical samples by using the Mx4000 and LightCycler general real-time PCR systems. J Clin Microbiol 2007, 45(3):897-901.
88. Tsai H.T., Wu C.H., Lai H.L., Li R.N., Tung Y.C., Chuang H.Y., et al. Association between quantitative high-risk human papillomavirus DNA load and cervical intraepithelial neoplasm risk. Cancer Epidemiol Biomarkers Prev 2005, 14(11 Pt 1):2544-2549.
89. van Duin M., Snijders P.J., Schrijnemakers H.F., Voorhorst F.J., Rozendaal L., Nobbenhuis M.A., et al. Human papillomavirus 16 load in normal and abnormal cervical scrapes: an indicator of CIN II/III and viral clearance. Int J Cancer 2002, 98(4):590-595.
90. Ylitalo N., Sorensen P., Josefsson A.M., Magnusson P.K., Andersen P.K., Ponten J., et al. Consistent high viral load of human papillomavirus 16 and risk of cervical carcinoma in situ: a nested case-control study. Lancet 2000, 355(9222):2194-2198.
91. Zerbini M., Venturoli S., Cricca M., Gallinella G., De Simone P., Costa S., et al. Distribution and viral load of type specific HPVs in different cervical lesions as detected by PCR-ELISA. J Clin Pathol 2001, 54(5):377-380.
92. Wu Y., Chen Y., Li L., Yu G., Zhang Y., He Y. Associations of high-risk HPV types and viral load with cervical cancer in China. J Clin Virol 2006, 35(3):264-269.
93. Snijders P.J., Hogewoning C.J., Hesselink A.T., Berkhof J., Voorhorst F.J., Bleeker M.C., et al. Determination of viral load thresholds in cervical scrapings to rule out CIN 3 in HPV 16, 18, 31 and 33-positive women with normal cytology. Int J Cancer 2006, 119(5):1102-1107.
94. Fiander A.N., Hart K.W., Hibbitts S.J., Rieck G.C., Tristram A.J., Beukenholdt R.W., et al. Variation in human papillomavirus type-16 viral load within different histological grades of cervical neoplasia. J Med Virol 2007, 79(9):1366-1369.
95. Song S.H., Lee J.K., Oh M.J., Hur J.Y., Park Y.K., Saw H.S. Risk factors for the progression or persistence of untreated mild dysplasia of the uterine cervix. Int J Gynecol Cancer 2006, 16(4):1608-1613.
96. Moberg M., Gustavsson I., Gyllensten U. Type-specific associations of human papillomavirus load with risk of developing cervical carcinoma in situ. Int J Cancer 2004, 112(5):854-859.
97. Castle P.E., Schiffman M., Scott D.R., Sherman M.E., Glass A.G., Rush B.B., et al. Semiquantitative human papillomavirus type 16 viral load and the prospective risk of cervical precancer and cancer. Cancer Epidemiol Biomarkers Prev 2005, 14(5):1311-1314.
98. Lai C.H., Chao A., Chang C.J., Chao F.Y., Huang H.J., Hsueh S., et al. Host and viral factors in relation to clearance of human papillomavirus infection: a cohort study in Taiwan. Int J Cancer 2008, 123(7):1685-1692.
99. Munoz N., Hernandez-Suarez G., Mendez F., Molano M., Posso H., Moreno V., et al. Persistence of HPV infection and risk of high-grade cervical intraepithelial neoplasia in a cohort of Colombian women. Br J Cancer 2009, 100(7):1184-1190.
100. Fontaine J., Hankins C., Money D., Rachlis A., Pourreaux K., Ferenczy A., et al. Human papillomavirus type 16 (HPV-16) viral load and persistence of HPV-16 infection in women infected or at risk for HIV. J Clin Virol 2008, 43(3):307-312.
101. Bae J., Seo S.S., Park Y.S., Dong S.M., Kang S., Myung S.K., et al. Natural history of persistent high-risk human papillomavirus infections in Korean women. Gynecol Oncol 2009, 115(1):75-80.
102. Moberg M., Gustavsson I., Wilander E., Gyllensten U. High viral loads of human papillomavirus predict risk of invasive cervical carcinoma. Br J Cancer 2005, 92(5):891-894.
103. Ho C.M., Cheng W.F., Chu T.Y., Chen C.A., Chuang M.H., Chang S.F., et al. Human papillomaviral load changes in low-grade squamous intraepithelial lesions of the uterine cervix. Br J Cancer 2006, 95(10):1384-1389.
104. Trimble C.L., Piantadosi S., Gravitt P., Ronnett B., Pizer E., Elko A., et al. Spontaneous regression of high-grade cervical dysplasia: effects of human papillomavirus type and HLA phenotype. Clin Cancer Res 2005, 11(13):4717-4723.
105. Hesselink A.T., Berkhof J., Heideman D.A., Bulkmans N.W., van Tellingen J.E., Meijer C.J., et al. High-risk human papillomavirus DNA load in a population-based cervical screening cohort in relation to the detection of high-grade cervical intraepithelial neoplasia and cervical cancer. Int J Cancer 2009, 124(2):381-386.
106. Lombard I., Vincent-Salomon A., Validire P., Zafrani B., de la Rochefordiere A., Clough K., et al. Human papillomavirus genotype as a major determinant of the course of cervical cancer. J Clin Oncol 1998, 16(8):2613-2619.
107. Burger R.A., Monk B.J., Kurosaki T., Anton-Culver H., Vasilev S.A., Berman M.L., et al. Human papillomavirus type 18: association with poor prognosis in early stage cervical cancer. J Natl Cancer Inst 1996, 88(19):1361-1368.
108. Wanram S., Limpaiboon T., Leelayuwat C., Yuenyao P., Guiney D.G., Lulitanond V., et al. The use of viral load as a surrogate marker in predicting disease progression for patients with early invasive cervical cancer with integrated human papillomavirus type 16. Am J Obstet Gynecol 2009, 201(1). 79 e1-7.
109. Kim J.Y., Park S., Nam B.H., Roh J.W., Lee C.H., Kim Y.H., et al. Low initial human papillomavirus viral load implicates worse prognosis in patients with uterine cervical cancer treated with radiotherapy. J Clin Oncol 2009, 27(30):5088-5093.
110. de Boer M.A., Jordanova E.S., Kenter G.G., Peters A.A., Corver W.E., Trimbos J.B., et al. High human papillomavirus oncogene mRNA expression and not viral DNA load is associated with poor prognosis in cervical cancer patients. Clin Cancer Res 2007, 13(1):132-138.
111. Kim Y.M., Park J.Y., Lee K.M., Kong T.W., Yoo S.C., Kim W.Y., et al. Does pretreatment HPV viral load correlate with prognosis in patients with early stage cervical carcinoma?. J Gynecol Oncol 2008, 19(2):113-116.
112. Bae J.H., Kim C.J., Park T.C., Namkoong S.E., Park J.S. Persistence of human papillomavirus as a predictor for treatment failure after loop electrosurgical excision procedure. Int J Gynecol Cancer 2007, 17(6):1271-1277.
113. Bar-Am A., Gamzu R., Levin I., Fainaru O., Niv J., Almog B. Follow-up by combined cytology and human papillomavirus testing for patients post-cone biopsy: results of a long-term follow-up. Gynecol Oncol 2003, 91(1):149-153.
114. Nam K., Chung S., Kim J., Jeon S., Bae D. Factors associated with HPV persistence after conization in patients with negative margins. J Gynecol Oncol 2009, 20(2):91-95.
115. Song S.H., Lee J.K., Oh M.J., Hur J.Y., Na J.Y., Park Y.K., et al. Persistent HPV infection after conization in patients with negative margins. Gynecol Oncol 2006, 101(3):418-422.
116. Park J.Y., Lee S.M., Yoo C.W., Kang S., Park S.Y., Seo S.S. Risk factors predicting residual disease in subsequent hysterectomy following conization for cervical intraepithelial neoplasia (CIN) III and microinvasive cervical cancer. Gynecol Oncol 2007, 107(1):39-44.
117. Alonso I., Torne A., Puig-Tintore L.M., Esteve R., Quinto L., Campo E., et al. Pre- and post-conization high-risk HPV testing predicts residual/recurrent disease in patients treated for CIN 2-3. Gynecol Oncol 2006, 103(2):631-636.
118. Rigoni-Stern D. Fatti statistici relative alla mallatie cancrosi che servirono de base alla poche cose dette dal dott. G Service Propr Pathol Terap Ser 1842, 2:507-517.
119. Ciuffo G. Inesto positive con filtrato di verruca volgare. G Ital Mal Vene Pelle 1907, 48:12-17.
120. Strauss MJ, Shaw EW, et al. Crystalline virus-like particles from skin papillomas characterized by intranuclear inclusion bodies. Proc Soc Exp Biol Med 1949;72(1):46-50 [New York, NY].
121. Nahmias A.J., Josey W.E., Naib Z.M., Luce C.F., Guest B.A. Antibodies to Herpesvirus hominis types 1 and 2 in humans. II. Women with cervical cancer. Am J Epidemiol 1970, 91(6):547-552.
122. Naib Z.M., Nahmias A.J., Josey W.E., Kramer J.H. Genital herpetic infection. Association with cervical dysplasia and carcinoma. Cancer 1969, 23(4):940-945.
123. Rawls WE, Tompkins WA, Figueroa ME, Melnick JL. Herpesvirus type 2: association with carcinoma of the cervix. Science 1968;161(847):1255-6 [New York, NY].
124. Klug A., Finch J.T. Structure of viruses of the papilloma-polyoma type. I. Human Wart Virus. J Mol Biol 1965, 11:403-423.
125. Crawford L.V. A study of human papilloma virus DNA. J Mol Biol 1965, 13(2):362-372.
126. 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, 13(5):650-656.
127. zur Hausen J., Schulte-Holthausen H., Wolf H., Dorries K., Egger H. Attempts to detect virus-specific DNA in human tumors. II. Nucleic acid hybridizations with complementary RNA of human herpes group viruses. Int J Cancer 1974, 13(5):657-664.
128. Almeida J.D., Oriel J.D., Stannard L.M. Characterization of the virus found in human genital warts. Microbiops 1969, 3:225-232.
129. Gissmann L., Hausen H.Z. Human papilloma virus DNA: physical mapping and genetic heterogeneity. Proc Natl Acad Sci U S A 1976, 73(4):1310-1313.
130. Gissmann L., Pfister H., Zur Hausen H. Human papilloma viruses (HPV): characterization of four different isolates. Virology 1977, 76(2):569-580.
131. Orth G., Favre M., Croissant O. Characterization of a new type of human papillomavirus that causes skin warts. J Virol 1977, 24(1):108-120.
132. Meisels A., Fortin R., Roy M. Condylomatous lesions of the cervix. II. Cytologic, colposcopic and histopathologic study. Acta Cytol 1977, 21(3):379-390.
133. Meisels A., Fortin R. Condylomatous lesions of the cervix and vagina. I. Cytologic patterns. Acta Cytol 1976, 20(6):505-509.
134. Hills E., Laverty C.R. Electron microscopic detection of papilloma virus particles in selected koilocytotic cells in a routine cervical smear. Acta Cytol 1979, 23(1):53-56.
135. Della Torre G., Pilotti S., de Palo G., Rilke F. Viral particles in cervical condylomatous lesions. Tumori 1978, 64(5):549-553.
136. 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, 29(2):143-146.
137. 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, 44(1):393-400.
138. Gissmann L., zur Hausen H. Partial characterization of viral DNA from human genital warts (Condylomata acuminata). Int J Cancer 1980, 25(5):605-609.
139. de Villiers E.M., Gissmann L., zur Hausen H. Molecular cloning of viral DNA from human genital warts. J Virol 1981, 40(3):932-935.
140. Durst 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, 80(12):3812-3815.
141. Ikenberg H., Gissmann L., Gross G., Grussendorf-Conen E.I., zur Hausen H. Human papillomavirus type-16-related DNA in genital Bowen's disease and in Bowenoid papulosis. Int J Cancer 1983, 32(5):563-565.
142. 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, 3(5):1151-1157.
143. Crum C.P., Ikenberg H., Richart R.M., Gissman L. Human papillomavirus type 16 and early cervical neoplasia. N Engl J Med 1984, 310(14):880-883.
144. Vonka V., Kanka J., Hirsch I., Zavadova H., Krcmar M., Suchankova A., et al. 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, 33(1):61-66.
145. Vonka V., Kanka J., Jelinek J., Subrt I., Suchanek A., Havrankova A., et al. Prospective study on the relationship between cervical neoplasia and herpes simplex type-2 virus. I. Epidemiological characteristics. Int J Cancer 1984, 33(1):49-60.
146. Schwarz E., Freese U.K., Gissmann L., Mayer W., Roggenbuck B., Stremlau A., et al. Structure and transcription of human papillomavirus sequences in cervical carcinoma cells. Nature 1985, 314(6006):111-114.
147. 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, 57(2):572-577.
148. Durst M., Dzarlieva-Petrusevska R.T., Boukamp P., Fusenig N.E., Gissmann L. Molecular and cytogenetic analysis of immortalized human primary keratinocytes obtained after transfection with human papillomavirus type 16 DNA. Oncogene 1987, 1(3):251-256.
149. 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, 61(4):1061-1066.
150. Werness BA, Levine AJ, Howley PM. Association of human papillomavirus types 16 and 18 E6 proteins with p53. Science 1990;248(4951):76-9 [New York, NY].
151. Zhou J., Sun X.Y., Stenzel D.J., Frazer I.H. Expression of vaccinia recombinant HPV 16 L1 and L2 ORF proteins in epithelial cells is sufficient for assembly of HPV virion-like particles. Virology 1991, 185(1):251-257.
152. Dyson N., Guida P., Munger K., Harlow E. Homologous sequences in adenovirus E1A and human papillomavirus E7 proteins mediate interaction with the same set of cellular proteins. J Virol 1992, 66(12):6893-6902.
153. Bosch F.X., Munoz N., de Sanjose S., Izarzugaza I., Gili M., Viladiu P., et al. Risk factors for cervical cancer in Colombia and Spain. Int J Cancer 1992, 52(5):750-758.
154. Koutsky L.A., Ault K.A., Wheeler C.M., Brown D.R., Barr E., Alvarez F.B., et al. A controlled trial of a human papillomavirus type 16 vaccine. N Engl J Med 2002, 347(21):1645-1651.
155. Harper D.M., Franco E.L., Wheeler C., Ferris D.G., Jenkins D., Schuind A., et al. Efficacy of a bivalent L1 virus-like particle vaccine in prevention of infection with human papillomavirus types 16 and 18 in young women: a randomised controlled trial. Lancet 2004, 364(9447):1757-1765.
156. Villa L.L., Costa R.L., Petta C.A., Andrade R.P., Ault K.A., Giuliano A.R., et al. Prophylactic quadrivalent human papillomavirus (types 6, 11, 16, and 18) L1 virus-like particle vaccine in young women: a randomised double-blind placebo-controlled multicentre phase II efficacy trial. Lancet Oncol 2005, 6(5):271-278.
157. Bergeron C., Breugelmans J.G., Bouee S., Lorans C., Benard S., Remy V. Cervical cancer screening and associated treatment costs in France. Gynecol Obstet Fertil 2006, 34(11):1036-1042.