Comparison of oncogenic HPV type-specific viral DNA load and E6/E7 mRNA detection in cervical samples: Results from a multicenter study

Journal of Medical Virology

Volumn 85, Issue 3, 2013, Pages 472-482

  Broccolo, Francesco ^a   Fusetti, Lisa ^b   Rosini, Sandra ^c   Caraceni, Donatella ^d   Zappacosta, Roberta ^c   Ciccocioppo, Lucia ^d   Matteoli, Barbara ^b   Halfon, Philippe ^e   Malnati, Mauro S ^f   Ceccherini Nelli, Luca ^b  

^a UNIVERSITY OF MILANO BICOCCA   (Italy)

^b UNIVERSITY OF PISA   (Italy)

^c UNIVERSITY OF CHIETI   (Italy)

^d Renzetti Hospital   (Italy)

^e HÔPITAL AMBROISE PARÉ   (France)

^f SAN RAFFAELE HOSPITAL   (Italy)

Author keywords

Cervical cytological samples; E6 E7 mRNA; High risk HPV genotypes; Viral load

Indexed keywords

MESSENGER RNA; PROTEIN E6; PROTEIN E7; VIRUS DNA;

ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE SEVERITY; FEMALE; HUMAN; HUMAN PAPILLOMAVIRUS DNA TEST; HUMAN TISSUE; MAJOR CLINICAL STUDY; PREDICTIVE VALUE; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RNA ANALYSIS; SENSITIVITY ANALYSIS; UTERINE CERVIX CANCER; UTERINE CERVIX CARCINOMA IN SITU; VIRUS LOAD; WART VIRUS;

ADULT; AGED; DNA, VIRAL; FEMALE; GENOTYPE; HUMANS; MIDDLE AGED; MOLECULAR DIAGNOSTIC TECHNIQUES; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; PREDICTIVE VALUE OF TESTS; REAL-TIME POLYMERASE CHAIN REACTION; RETROSPECTIVE STUDIES; RNA, MESSENGER; RNA, VIRAL; SENSITIVITY AND SPECIFICITY; SEQUENCE ANALYSIS, DNA; UTERINE CERVICAL NEOPLASMS; YOUNG ADULT;

EID: 84873186012     PISSN: 01466615     EISSN: 10969071     Source Type: Journal    
DOI: 10.1002/jmv.23487     Document Type: Article

References (48)

1. Andersson S, Hansson B, Norman I, Gaberi V, Mints M, Hjerpe A, Karlsen F, Johansson B. 2006. Expression of E6/E7 mRNA from 'high risk' human papillomavirus in relation to CIN grade, viral load and p16INK4a. Int J Oncol 29: 705- 711.
2. Basu P, Roychowdhury S, Bafna UD, Chaudhury S, Kothari S, Sekhon R, Saranath D, Biswas S, Gronn P, Silva I, Siddiqi M, Ratnam S. 2009. Human papillomavirus genotype distribution in cervical cancer in India: Results from a multi-center study. Asian Pac J Cancer Prev 10: 27- 34.
3. Benevolo M, Vocaturo A, Caraceni D, French D, Rosini S, Zappacosta R, Terrenato I, Ciccocioppo L, Frega A, Giorgi Rossi P. 2011. Sensitivity, specificity, and clinical value of human papillomavirus (HPV) E6/E7 mRNA assay as a triage test for cervical cytology and HPV DNA test. J Clin Microbiol 49: 2643- 2650.
4. Beskow AH, Gyllensten UB. 2002. Host genetic control of HPV 16 titer in carcinoma in situ of the cervix uteri. Int J Cancer 101: 526- 531.
5. Broccolo F, Cocuzza CE. 2008. Automated extraction and quantitation of oncogenic HPV genotypes from cervical samples by real-time PCR-based system. J Virol Methods 148: 48- 57.
6. Broccolo F, Chiari S, Piana A, Castiglia P, Dell'Anna T, Garcia-Parra R, Maneo A, Villa A, Leone EB, Perego P, Maida A, Mangioni C, Cocuzza CE. 2009. Prevalence and viral load of oncogenic human papillomavirus types associated with cervical carcinoma in a population of north Italy. J Med Virol 81: 278- 287.
7. Burger EA, Kornør H, Klemp M, Lauvrak V, Kristiansen IS. 2011. HPV mRNA tests for the detection of cervical intraepithelial neoplasia: A systematic review. Gynecol Oncol 120: 430- 438. Review.
8. Calleja-Macias IE, Villa LL, Prado JC, Kalantari M, Allan B, Williamson AL, Chung LP, Collins RJ, Zuna RE, Dunn ST, Chu TY, Cubie HA, Cuschieri K, von Knebel-Doeberitz M, Martins CR, Sanchez GI, Bosch FX, Muñoz N, Bernard HU. 2005. Worldwide genomic diversity of the high-risk human papillomavirus types 31, 35 52, and 58, four close relatives of human papillomavirus type 16. J Virol 79: 30- 40.
9. Castle PE, Schiffman M, Scott DR, Sherman ME, Glass AG, Rush BB, Schussler JE, Wacholder S, Lorincz AT. 2005. Semiquantitative human papillomavirus type 16 viral load and the prospective risk of cervical precancer and cancer. Cancer Epidemiol Biomarkers Prev 14: 1311- 1314.
10. Cattani P, Siddu A, D'Onghia S, Marchetti S, Santangelo R, Vellone VG, Zannoni GF, Fadda G. 2009. RNA (E6 and E7) assays versus DNA (E6 and E7) assays for risk evaluation for women infected with human papillomavirus. J Clin Microbiol 47: 2136- 2141.
11. Cuschieri KS, Whitley MJ, Cubie HA. 2004. Human papillomavirus type specific DNA and RNA persistence-implications for cervical disease progression and monitoring. J Med Virol 73: 65- 70.
12. Dalstein V, Riethmuller D, Pretet JL, Le Bail Carval K, Sautiere JL, Carbillet JP, Kantelip B, Schaal J-P, Mougin C. 2003. Persistence and load of high-risk HPV are predictors for development of high-grade cervical lesions: A longitudinal French cohort study. Int J Cancer 106: 396- 403.
13. de Boer MA, Jordanova ES, Kenter GG, Peters AA, Corver WE, Trimbos JB, Fleuren GJ. 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.
14. de Roda Husman AM, Walboomers JMM, Van Den Brule AJC, Meijer CJLM, Snijders PJF. 1995. The use of general primers GP5 and GP6 elongated at their 39 ends with adjacent highly conserved sequences improves human papillomavirus detection by PCR. J Gen Virol 76: 1057- 1062.
15. Doorbar J. 2006. Molecular biology of human papillomavirus infection and cervical cancer. Clin Sci (Lond) 110: 525- 541.
16. Flores R, Papenfuss M, Klimecki WT, Giuliano AR. 2006. Cross-sectional analysis of oncogenic HPV viral load and cervical intraepithelial neoplasia. Int J Cancer 118: 1187- 1193.
17. Gravitt PE, Burk RD, Lorincz A, Herrero R, Hildesheim A, Sherman ME, Bratti MC, Rodriguez AC, Helzlsouer KJ, Schiffman M. 2003. A comparison between real-time polymerase chain reaction and hybrid capture 2 for human papillomavirus DNA quantitation. Cancer Epidemiol Biomarkers Prev 12: 477- 484.
18. Halfon P, Benmoura D, Agostini A, Khiri H, Marineau A, Penaranda G, Blanc B. 2010. Relevance of HPV mRNA detection in a population of ASCUS plus women using the NucliSENS EasyQ HPV assay. J Clin Virol 47: 177- 181.
19. Ho GY, Bierman R, Beardsley L, Chang CJ, Burk RD. 1998. Natural history of cervicovaginal papillomavirus infection in young women. N Engl J Med 338: 423- 428.
20. Hovland S, Muller S, Skomedal H, Mints M, Bergstrom J, Wallin KL, Karlsen F, Johansson B, Andersson S. 2010. E6/E7 mRNA expression analysis: A test for the objective assessment of cervical adenocarcinoma in clinical prognostic procedure. Int J Oncol 36: 1533- 1539.
21. Jacobs MV, de Roda Husman AM, van den Brule AJ, Snijders PJ, Meijer CJ, Walboomers JM. 1995. Group-specific differentiation between high- and low-risk human papillomavirus genotypes by general primer-mediated PCR and two cocktails of oligonucleotide probes. J Clin Microbiol 33: 901- 905.
22. Josefsson AM, Magnusson PK, Ylitalo N, Sorensen P, Qwarforth-Tubbin P, Andersen PK, Melbye M, Adami HO, Gyllensten UB. 2000. Viral load of human papilloma virus 16 as a determinant for development of cervical carcinoma in situ: A nested case-control study. Lancet 355: 2189- 2193.
23. Kalantari M, Calleja-Macias IE, Tewari D, Hagmar B, Lie K, Barrera-Saldana HA, Wiley DJ, Bernard H-U. 2004. Conserved methylation patterns of human papillomavirus type 16 DNA in asymptomatic infection and cervical neoplasia. J Virol 78: 12762- 12772.
24. Keegan H, Mc Inerney J, Pilkington L, Grønn P, Silva I, Karlsen F, Bolger N, Logan C, Furuberg L, O'Leary J, Martin C. 2009. Comparison of HPV detection technologies: Hybrid capture 2, PreTect HPV-Proofer and analysis of HPV DNA viral load in HPV16, HPV18 and HPV33 E6/E7 mRNA positive specimens. J Virol Methods 155: 61- 66.
25. Kjaer SK, Van Den Brule AJ, Paull G, Svare EI, Sherman ME, Thomsen BL, Suntum M, Bock JE, Poll PA, Meijer CJ. 2002. Type specific persistence of high risk human papillomavirus (HPV) as indicator of high grade cervical squamous intraepithelial lesions in young women: Population based prospective follow up study. BMJ 325: 572.
26. Koliopoulos G, Chrelias C, Pappas A, Makridima S, Kountouris E, Alepaki M, Spathis A, Stathopoulou V, Panayiotides I, Panagopoulos P, Karakitsos P, Kassanos D. 2012. The diagnostic accuracy of two methods for E6&7 mRNA detection in women with minor cytological abnormalities. Acta Obstet Gynecol Scand 91: 794- 801.
27. Kraus I, Molden T, Erno LE, Skomedal H, Karlsen F, Hagmar B. 2004. Human papillomavirus oncogenic expression in the dysplastic portio; an investigation of biopsies from 190 cervical cones. Br J Cancer 90: 1407- 1413.
28. Kraus I, Molden T, Holm R, Lie AK, Karlsen F, Kristensen GB, Skomedal H. 2006. Presence of E6 and E7 mRNA from human papillomavirus types 16, 18 31, 33 and 45 in the majority of cervical carcinomas. J Clin Microbiol 44: 1310- 1317.
29. Lie AK, Risberg B, Borge B, Sandstad B, Delabie J, Rimala R, Onsrud M, Thoresen S. 2005. DNA-versus RNA-based methods for human papillomavirus detection in cervical neoplasia. Gynecol Oncol 97: 908- 915.
30. Middleton K, Peh W, Southern SA, Griffin H, Sotlar K, Nakahara T, El-Sherif A, Morris L, Seth R, Hibma M, Jenkins D, Lambert P, Coleman N, Doorbar J. 2003. Organisation of the human papillomavirus productive cell cycle during neoplastic progression provides a basis for the selection of diagnostic markers. J Virol 77: 10186- 10201.
31. Moberg M, Gustavsson I, Gyllensten U. 2003. Real-time PCR-based system for simultaneous quantitation of human papillomavirus types associated with high risk of cervical cancer. J Clin Microbiol 41: 3221- 3228.
32. Moberg M, Gustavsson I, Gyllenstein U. 2004. Type-specific associations of human papillomavirus load with risk of developing cervical carcinoma in situ. Int J Cancer 112: 854- 859.
33. Moberg M, Gustavsson I, Wilander E, Gyllensten U. 2005. High viral loads of human papillomavirus predict risk of invasive cervical carcinoma. Br J Cancer 92: 891- 894.
34. Molden T, Nygård JF, Kraus I, Karlsen F, Nygård M, Skare GB, Skomedal H, Thoresen SO, Hagmar B. 2005. Predicting CIN2+ when detecting HPV mRNA and DNA by PreTect HPV-Proofer and consensus PCR: A 2-year follow-up of women with ASCUS or L-SIL Pap smear. Int J Cancer 114: 973- 976.
35. Munoz N, Bosch FX, de Sanjose S, Herrero R, Castellsague X, Shah KV, Snijders PJ, Meijer CJ, International Agency for Research on Cancer Multicenter Cervical Cancer Study Group. 2003. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med 348: 518- 527.
36. Qu W, Jiang G, Cruz Y, Chang CJ, Ho GY, Klein RS, Burk RD. 1997. PCR detection of human papillomavirus: comparison between MY09/MY11 and GP5+/GP6+ primer systems. J Clin Microbiol 35: 1304- 1310.
37. Ratnam SF, Coutlee D, Fontaine J, Bentley N, Escott P, Ghatage P, Gadag V, Holloway G, Bartellas E, Kum N, Giede C, Lear A. 2010. Clinical performance of the PreTect HPV-Proofer E6/E7 mRNA assay in comparison with that of the hybrid capture 2 test for identification of women at risk of cervical cancer. J Clin Microbiol 48: 2779- 2785.
38. Sherman ME, Wang SS, Wheeler CM, Rich L, Gravitt PE, Tarone R, Schiffman M. 2003. Determinants of human papillomavirus load among women with histological cervical intraepithelial neoplasia 3: Dominant impact of surrounding low-grade lesions. Cancer Epidemiol Biomarkers Prev 12: 1038- 1044.
39. Snijders PJF, Steenbergen RDM, Heideman DAM, Meijer CJLM. 2006. HPV-mediated cervical carcinogenesis: Concepts and clinical implications. J Pathol 208: 152- 164.
40. Sørbye SW, Fismen S, Gutteberg T, Mortensen ES. 2010. Triage of women with minor cervical lesions: Data suggesting a "test and treat" approach for HPV E6/E7 mRNA testing. PLoS ONE 5: e12724.
41. Stanley MA. 2001. Human papillomavirus and cervical carcinogenesis. Best Pract Res Clin Obstet Gynaecol 15: 663- 676.
42. Sun CA, Liu JF, Wu DM, Nieh S, Yu CP, Chu TY. 2002. Viral load of high risk human papillomavirus in cervical squamous intraepithelial lesions. Int J Gynaecol Obstet 76: 41- 47.
43. Swan DC, Tucker RA, Tortolero-Luna G, Follen Mitchell M, Wideroff L, Unger ER, Nisenbaum RA, Reeves WC, Icenogle JP. 1999. Human papillomavirus (HPV) DNA copy number is dependent on grade of cervical disease and HPV type. J Clin Microbiol 37: 1030- 1034.
44. Szarewski A, Mesher D, Cadman L, Austin J, Ashdown-Barr L, Ho L, Terry G, Liddle S, Young M, Stoler M, McCarthy J, Wright C, Bergeron C, Soutter WP, Lyons D, Cuzick J. 2012. Comparison of seven tests for high-grade cervical intraepithelial neoplasia in women with abnormal smears: The Predictors 2 study. J Clin Microbiol 50: 1867- 1873.
45. Ylitalo N, Josefsson A, Melbye M, Sorensen P, Frisch M, Andersen PK, Sparén P, Gustafsson M, Magnusson P, Ponten J, Gyllensten U, Adami HO. 2000. A prospective study showing long-term infection with human papillomavirus 16 before the development of cervical carcinoma in situ. Cancer Res 60: 6027- 6032.
46. Tropé A, Sjøborg K, Eskild A, Cuschieri K, Eriksen T, Thoresen S, Steinbakk M, Laurak V, Jonassen CM, Westerhagen U, Jacobsen MB, Lie AK. 2009. Performance of human papillomavirus DNA and mRNA testing strategies for women with and without cervical neoplasia. J Clin Microbiol 47: 2458- 2464.
47. Zerbini M, Venturoli S, Cricca M, Gallinella G, De Simone P, Costa S, Santini D, Musiani M. 2001. Distribution and viral load of type specific HPVs in different cervical lesions as detected by PCR-ELISA. J Clin Pathol 54: 377- 380.
48. Zur Hausen H. 2002. Papillomaviruses and cancer: From basic studies to clinical application. Nat Rev Cancer 2: 342- 350. Review.