Human papillomavirus testing: The challenges of picking the right tools for the job

Expert Review of Obstetrics and Gynecology

Volumn 6, Issue 6, 2011, Pages 643-653

  Cuschieri, Kate ^a  

^a ROYAL INFIRMARY OF EDINBURGH   (United Kingdom)

Author keywords

cervical disease; clinical indications; HPV diagnostics; validation

Indexed keywords

BIOLOGICAL MARKER; CYCLIN DEPENDENT KINASE INHIBITOR 2A; VIRUS DNA; WART VIRUS VACCINE;

AGE; CANCER GRADING; CANCER PREVENTION; CANCER SCREENING; CLINICAL EFFECTIVENESS; CLINICAL PRACTICE; COLPOSCOPY; CONDYLOMA ACUMINATUM; CRYOTHERAPY; GENOTYPE; HEALTH PROGRAM; HIGH RISK PATIENT; HUMAN; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN PAPILLOMAVIRUS TYPE 18; IMMUNE STATUS; INFECTION PREVENTION; INTERMETHOD COMPARISON; LABORATORY DIAGNOSIS; NONHUMAN; PAPILLOMAVIRUS INFECTION; PATIENT SAFETY; PREDICTION; PRIMARY PREVENTION; PROCESS DEVELOPMENT; RESOURCE MANAGEMENT; REVIEW; RISK REDUCTION; SCREENING TEST; SENSITIVITY AND SPECIFICITY; TOTAL QUALITY MANAGEMENT; UTERINE CERVIX CARCINOMA IN SITU; UTERINE CERVIX CYTOLOGY; VACCINATION; VALIDATION PROCESS; VIRUS CARCINOGENESIS; VIRUS DIAGNOSIS; VIRUS IDENTIFICATION; WART VIRUS;

EID: 80455125983     PISSN: 17474108     EISSN: 17474116     Source Type: Journal    
DOI: 10.1586/eog.11.69     Document Type: Review

References (72)

1. zur Hausen H. Papillomaviruses in the causation of human cancers - a brief historical account. Virology 384(2), 260-265 (2009).
2. Bernard HU, Burk RD, Chen Z, van Doorslaer K, Hausen H, de Villiers EM. Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. Virology 401(1), 70-79 (2010).
3. Bouvard V, Baan R, Straif K et al.; WHO International Agency for Research on Cancer Monograph Working Group. A review of human carcinogens - Part B: biological agents. Lancet Oncol. 10(4), 321-322 (2009).
4. Khan MJ, Castle PE, Lorincz AT 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. J. Natl Cancer Inst. 97(14), 1072-1079 (2005). (Pubitemid 41417924)
5. Stoler MH, Wright TC Jr, Sharma A, Apple R, Gutekunst K, Wright TL; ATHENA (Addressing The Need for Advanced HPV Diagnostics) HPV Study Group. High-risk human papillomavirus testing in women with ASC-US cytology: results from the ATHENA HPV study. Am. J. Clin. Pathol. 135(3), 468-475 (2011).
6. Cuzick J, Ambroisine L, Cadman L et al. Performance of the Abbott RealTime high-risk HPV test in women with abnormal cervical cytology smears. J. Med. Virol. 82(7), 1186-1191 (2010).
7. Insinga RP, Perez G, Wheeler CM et al.; FUTURE I Investigators. Incidence, duration, and reappearance of type-specific cervical human papillomavirus infections in young women. Cancer Epidemiol. Biomarkers Prev. 19(6), 1585-1594 (2010).
8. Kjaer SK, Frederiksen K, Munk C, Iftner T. Long-term absolute risk of cervical intraepithelial neoplasia grade 3 or worse following human papillomavirus infection: role of persistence. J. Natl Cancer Inst. 102(19), 1478-1488 (2010).
9. Accardi R, Rubino R, Scalise M et al. E6 and E7 from human papillomavirus type 16 cooperate to target the PDZ protein Na/H exchange regulatory factor 1. J. Virol. 85(16), 8208-8216 (2011).
10. Pim D, Banks L. Interaction of viral oncoproteins with cellular target molecules: infection with high-risk vs low-risk human papillomaviruses. APMIS 118(6-7), 471-493 (2010).
11. Stanley M. HPV - immune response to infection and vaccination. Infect. Agent. Cancer 20, 5-19 (2010).
12. Poljak M, Kocjan BJ. Commercially available assays for multiplex detection of alpha human papillomaviruses. Expert Rev. Anti. Infect. Ther. 8(10), 1139-1162 (2010).
13. Arbyn M, Ronco G, Cuzick J, Wentzensen N, Castle PE. How to evaluate emerging technologies in cervical cancer screening? Int. J. Cancer 125(11), 2489-2496 (2009).
14. Meijer CJ, Berkhof J, Castle PE et al. Guidelines for human papillomavirus DNA test requirements for primary cervical cancer screening in women 30 years and older. Int. J. Cancer 124(3), 516-520 (2009).
15. Tabrizi SN. Quality assessment for human papillomavirus testing. Sex. Health 7(3), 335-337 (2010).
16. Fagan EJ, Moore C, Jenkins C, Rossouw A, Cubie HA, James VL. External quality assessment for molecular detection of human papillomaviruses. J. Clin. Virol. 48(4), 251-254 (2010).
17. Eklund C, Zhou T, Dillner J; WHO Human Papillomavirus Laboratory Network. Global proficiency study of human papillomavirus genotyping. J. Clin. Microbiol. 48(11), 4147-4155 (2010).
18. Cuzick J, Arbyn M, Sankaranarayanan Tsu V et al. Overview of human papillomavirus-based and other novel options for cervical cancer screening in developed and developing countries. Vaccine 26(Suppl. 19), K29-K41 (2008).
19. Nanda K, McCrory DC, Myers ER et al. Accuracy of the Papanicolaou test in screening for and follow-up of cervical cytologic abnormalities: a systematic review. Ann. Intern. Med. 132, 810-819 (2000). (Pubitemid 30317797)
20. Castle PE, Stoler MH, Wright TC, Sharma A, Wright TL, Behrens C. Performance of carcinogenic HPV testing and HPV16 or HPV18 genotyping for cervical cancer screening of women aged 25 years and older: a subanalysis of the ATHENA study. Lancet Oncol. 12(9), 880-890 (2011).
21. Melnikow J, Nuovo J, Willan AR, Chan BK, Howell LP. Natural history of cervical squamous intraepithelial lesions: a meta-analysis. Obstet. Gynecol. 92(4 Pt 2), 727-735 (1998). (Pubitemid 28440819)
22. Kyrgiou M, Koliopoulos G, Martin-Hirsch P et al. Management of minor cervical cytological abnormalities: a systematic review and a meta-analysis of the literature. Cancer Treat. Rev. 33(6), 514-520 (2007). (Pubitemid 47355339)
23. Arbyn M, Martin-Hirsch P, Buntinx F, Van Ranst M, Paraskevaidis E, Dillner J. Triage of women with equivocal or low-grade cervical cytology results: a meta-analysis of the HPV test positivity rate. J. Cell. Mol. Med. 13(4), 648-659 (2009).
24. Sargent A, Bailey A, Turner A et al. Optimal threshold for a positive hybrid capture 2 test for detection of human papillomavirus: data from the ARTISTIC trial. J. Clin. Microbiol. 48(2), 554-558 (2010).
25. Ratnam S, Coutlee F, Fontaine D et al. Aptima HPV E6/E7 mRNA test is as sensitive as Hybrid Capture 2 Assay butmore specific at detecting cervical precancer and cancer. J. Clin. Microbiol. 49(2), 557-564 (2011).
26. Cuschieri K, Wentzensen N. Human papillomavirus mRNA and p16 detection as biomarkers for the improved diagnosis of cervical neoplasia. Cancer Epidemiol. Biomarkers Prev. 17(10), 2536-2545 (2008).
27. Tsoumpou I, Arbyn M, Kyrgiou M et al. p16(INK4a) immunostaining in cytological and histological specimens from the uterine cervix: a systematic review and meta-analysis. Cancer Treat. Rev. 35(3), 210-220 (2009).
28. Szarewski A, Ambroisine L, Cadman L et al. Comparison of predictors for high-grade cervical intraepithelial neoplasia in women with abnormal smears. Cancer Epidemiol. Biomarkers Prev. 17(11), 3033-3042 (2008).
29. Katki HA, Kinney WK, Fetterman B et al. Cervical cancer risk for women undergoing concurrent testing for human papillomavirus and cervical cytology: a population-based study in routine clinical practice. Lancet Oncol. 12(7), 663-672 (2011).
30. Kitchener HC, Almonte M, Thomson C et al. HPV testing in combination with liquid-based cytology in primary cervical screening (ARTISTIC): a randomized controlled trial. Lancet Oncol. 10(7), 672-682 (2009).
31. Arbyn M. HPV testing to monitor outcome after treatment of high-grade CIN. Presented at: 28th International Papillomavirus Meeting. Malmo, Sweden, 8-14 May 2009.
32. Strander B, Andersson-Ellstrom A, Milsom I, Sparen P. Long term risk of invasive cancer after treatment for cervical intraepithelial neoplasia grade 3: a population based cohort study. BMJ 335(7629), 1077 (2007).
33. Kocken M, Helmerhorst TJM, Berkhof J et al. Risk of recurrent high-grade cervical intraepithelial neoplasia after successful treatment: a long-term multi-cohort study. Lancet Oncol. 12, 441-450 (2011).
34. Valasoulis G, Koliopoulos G, Founta C et al. Alterations in human papillomavirus-related biomarkers after treatment of cervical intraepithelial neoplasia. Gynecol. Oncol. 121(1), 43-48 (2011).
35. Venturoli S, Ambretti S, Cricca M et al Correlation of high-risk human papillomavirus genotypes persistence and risk of residual or recurrent cervical disease after surgical treatment. J. Med. Virol. 80(8), 1434-1440 (2008). (Pubitemid 351897416)
36. Brismar S, Johansson B, Borjesson M, Arbyn M, Andersson S. Follow-up after treatment of cervical intraepithelial neoplasia by human papillomavirus genotyping. Am. J. Obstet. Gynecol. 201(1), 17.e1-8 (2009).
37. Kotaniemi-Talonen L, Nieminen P, Anttila A, Hakama M. Routine cervical screening with primary HPV testing and cytology triage protocol in a randomized setting. Br. J. Cancer 93(8), 862-867 (2005). (Pubitemid 41487010)
38. Sankaranarayanan R, Nene BM, Dinshaw KA et al. A cluster randomized controlled trial of visual, cytology and human papillomavirus screening for cancer of the cervix in rural India. Int. J. Cancer 116, 617-623 (2005). (Pubitemid 41099199)
39. Ronco G, Segnan N, Giorgi-Rossi P et al. Human papillomavirus testing and liquid-based cytology: results at recruitment from the New Technologies for Cervical Cancer Randomized Controlled Trial. J. Natl Cancer Inst. 98, 765-774 (2006). (Pubitemid 43983300)
40. Ronco G, Giorgi-Rossi P, Carozzi F et al. Human papillomavirus testing and liquid-based cytology in primary screening of women younger than 35 years: results at recruitment for a randomized controlled trial. Lancet Oncol. 7, 547-555 (2006). (Pubitemid 43923665)
41. Bulkmans NWJ, Berkhof J, Rozendaal L et al. Human papillomavirus DNA testing for the detection of cervical intraepithelial neoplasia grade 3 and cancer: 5-year follow-up of a randomized controlled implementation trial. Lancet 370, 1764-1772 (2007). (Pubitemid 350137476)
42. Naucler P, Ryd W, Tornberg S et al. Human papillomavirus and papanicolaou tests to screen for cervical cancer. N. Engl. J. Med. 357, 1589-1597 (2007). (Pubitemid 47598401)
43. Ogilvie GS, van Niekerk DJ, Krajden M et al. A randomized controlled trial of Human Papillomavirus (HPV) testing for cervical cancer screening: trial design and preliminary results (HPV FOCAL trial).BMC Cancer 10, 111 (2010).
44. Almonte M, Sasieni P, Cuzick J. Incorporating human papillomavirus testing into cytological screening in the era of prophylactic vaccines. Best Pract. Res. Clin. Obstet. Gynaecol. 25(5), 617-629 (2011).
45. Cuzick J, Clavel C, Petry KU et al. Overview of the European and North American studies on HPV testing in primary cervical cancer screening. Int. J. Cancer 119(5), 1095-1101 (2006). (Pubitemid 44116919)
46. Saraiya M, Berkowitz Z, Yabroff KR, Wideroff L, Kobrin S, Benard V. Cervical cancer screening with both human papillomavirus and Papanicolaou testing vs Papanicolaou testing alone: what screening intervals are physicians recommending? Arch. Intern. Med. 170(11), 977-985 (2010).
47. Schmeink CE, Bekkers RL, Massuger LF, Melchers WJ. The potential role of self-sampling for high-risk human papillomavirus detection in cervical cancer screening. Rev. Med. Virol. 3, 139-153 (2011).
48. Rebolj M, Bonde J, Njor SH, Lynge E. Human papillomavirus testing in primary cervical screening and the cutoff level for hybrid capture 2 tests: systematic review. BMJ 342, d2757 (2011).
49. Rijkaart DC, Berkhof J, van Kemenade FJ et al. Evaluation of 14 triage strategies for HPV DNA-positive women in population-based cervical screening. Int. J. Cancer DOI: 10.1002/ijc.26056 (2011) (Epub ahead of print).
50. Carozzi F, Confortini M, Dalla Palma P et al. New Technologies for Cervical Cancer Screening (NTCC) Working Group. Use of p16-INK4A overexpression to increase the specificity of human papillomavirus testing: a nested substudy of the NTCC randomized controlled trial. Lancet Oncol. 10, 937-945 (2008).
51. Hoots BE, Palefsky JM, Pimenta JM, Smith JS. Human papillomavirus type distribution in anal cancer and anal intraepithelial lesions. Int. J. Cancer 124(10), 2375-2383 (2009).
52. Miralles-Guri C, Bruni L, Cubilla AL, Castellsagué X, Bosch FX, de Sanjosé S. Human papillomavirus prevalence and type distribution in penile carcinoma. J. Clin. Pathol. 62(10), 870-878 (2009).
53. Chung CH, Gillison ML. Human papillomavirus in head and neck cancer: its role in pathogenesis and clinical implications. Clin. Cancer Res. 15(22), 6758-6762 (2009).
54. Salit IE, Lytwyn A, Raboud J et al. The role of cytology (Pap tests) and human papillomavirus testing in anal cancer screening. AIDS 24(9), 1307-1131 (2010).
55. Elbasha EH, Dasbach EJ. Impact of vaccinating boys and men against HPV in the United States. Vaccine 28(42), 6858-6867 (2010).
56. Giuliano AR, Lee JH, Fulp W et al. Incidence and clearance of genital human papillomavirus infection in men (HIM): a cohort study. Lancet 377(9769), 932-940 (2011).
57. 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. 202(12), 1789-1799 (2010).
58. Zhao FH, Lin MJ, Chen F et al.; Cervical Cancer Screening Group in China. Performance of high-risk human papillomavirus DNA testing as a primary screen for cervical cancer: a pooled analysis of individual patient data from 17 population-based studies from China. Lancet Oncol. 12, 1160-1171 (2010).
59. Sasieni P, Castanon A, Cuzick J. Effectiveness of cervical screening with age: population based case-control study of prospectively recorded data. BMJ 339, b2968 (2009).
60. Sankaranarayanan R, Boffetta P. Research on cancer prevention, detection and management in low- and medium-income countries. Ann Oncol. 21(10), 1935-1943 (2010).
61. Denny L, Kuhn L, De Souza M, Pollack AE, Dupree W, Wright TC Jr. Screen-and-treat approaches for cervical cancer prevention in low-resource settings: a randomized controlled trial. JAMA 294(17), 2173-2181 (2005). (Pubitemid 41571134)
62. Shi JF, Canfell K, Lew JB et al. Evaluation of primary HPV-DNA testing in relation to visual inspection methods for cervical cancer screening in rural China: an epidemiologic and cost-effectiveness modelling study. BMC Cancer 11, 239 (2011).
63. Sankaranarayanan R, Nene BM, Shastri SS et al. HPV screening for cervical cancer in rural India. N. Engl. J. Med. 360(14), 1385-1394 (2009).
64. Qiao YL, Sellors JW, Eder PS et al. A new HPV-DNA test for cervical-cancer screening in developing regions: a cross-sectional study of clinical accuracy in rural China. Lancet Oncol. 9(10), 929-936 (2008).
65. Virtanen A, Nieminen P, Luostarinen T, Anttila A. Self-sample HPV tests as an intervention for nonattendees of cervical cancer screening in Finland: a randomized trial. Cancer Epidemiol. Biomarkers Prev. 9, 1960-1969 (2011).
66. Wikström I, Lindell M, Sanner K, Wilander E. Self-sampling and HPV testing or ordinary Pap-smear in women not regularly attending screening: a randomized study. Br. J. Cancer 105 (3), 337-339 (2011).
67. Szarewski A, Cadman L, Mesher D et al. HPV self-sampling as an alternative strategy in non-attenders for cervical screening - a randomized controlled trial. Br. J. Cancer 104(6), 915-920 (2011).
68. Howard M, Lytwyn A, Lohfeld L, Redwood-Campbell L, Fowler N, Karwalajtys T. Barriers to acceptance of self-sampling for human papillomavirus across ethnolinguistic groups of women. Can. J. Public Health. 100(5), 365-369 (2009).
69. Waller J, McCaffery K, Forrest S et al. Acceptability of unsupervised HPV self-sampling using written instructions. J. Med. Screen. 13(4), 208-213 (2006). (Pubitemid 46057729)
70. Brotherton JM, Fridman M, May CL, Chappell G, Saville AM, Gertig DM. Early effect of the HPV vaccination programme on cervical abnormalities in Victoria, Australia: an ecological study. Lancet 377(9783), 2085-2092 (2011).
71. Franco EL, Cuzick J. Cervical cancer screening following prophylactic human papillomavirus vaccination. Vaccine 26(Suppl. 1), A16-A23 (2008). (Pubitemid 351312311)
72. Almonte M, Murillo R, Sánchez GI et al. New paradigms and challenges in cervical cancer prevention and control in Latin America. Salud. Publica Mex. 52(6), 544-559 (2010).