Prevalence of human papillomavirus in women attending cervical screening in the UK and Ireland: New data from northern Ireland and a systematic review and meta-analysis

Journal of Medical Virology

Volumn 85, Issue 2, 2013, Pages 295-308

  Anderson, Lesley ^a   O'Rorke, Michael ^a   Jamison, Jackie ^b   Wilson, Robbie ^b   Gavin, Anna ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b ANTRIM AREA HOSPITAL   (United Kingdom)

Author keywords

Human papillomavirus (HPV); Meta analysis; Normal cytology; Systematic review

Indexed keywords

ADULT; ARTICLE; FEMALE; HUMAN; HUMAN PAPILLOMAVIRUS TYPE 16; IMMUNIZATION; IRELAND; MAJOR CLINICAL STUDY; MASS SCREENING; PAPILLOMAVIRUS INFECTION; POLYMERASE CHAIN REACTION; PREVALENCE; SYSTEMATIC REVIEW; UNITED KINGDOM; UTERINE CERVIX CYTOLOGY; VIRUS DETECTION; VIRUS TYPING; WART VIRUS;

ADULT; CYTOLOGICAL TECHNIQUES; FEMALE; GREAT BRITAIN; HUMANS; IRELAND; MIDDLE AGED; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; PREVALENCE; VIROLOGY; YOUNG ADULT;

HUMAN PAPILLOMAVIRUS; HUMAN PAPILLOMAVIRUS TYPE 16;

EID: 84871167955     PISSN: 01466615     EISSN: 10969071     Source Type: Journal    
DOI: 10.1002/jmv.23459     Document Type: Article

References (75)

1. Adams A, Jasani B, Fiander A. 2009. Prophylactic HPV vaccination for women over 18 years of age. Vaccine 27: 3391- 3394.
2. Baker D, Middleton E. 2003. Cervical screening and health inequality in England in the 1990s. J Epidemiol Community Health 57: 417- 423.
3. Bavin PJ, Giles JA, Hudson E, Williams D, Crow J, Griffiths PD, Emery VC, Walker PG. 1992. Comparison of cervical cytology and the polymerase chain reaction for HPV 16 to identify women with cervical disease in a general practice population. J Med Virol 37: 8- 12.
4. Berrens E, Van Renterghem L, Praet M. 2005. Human papillomavirus DNA detection in women with primary abnormal cytology of the cervix: Prevalence and distribution of HPV genotypes. Cytopathology 16: 199- 205.
5. Biswas C, Kell B, Mant C, Jewers RJ, Cason J, Muir P, Raju KS, Best JM. 1997. Detection of human papillomavirus type 16 early-gene transcription by reverse transcription-PCR is associated with abnormal cervical cytology. J Clin Microbiol 35: 1560- 1564.
6. Bosch XF, Manos MM, Munoz N, Sherman M, Jansen AM, Peto J, Schiffman MH, Moreno V, Kurman R, Shah KV. 1995. Prevalence of human papillomavirus in cervical cancer: A worldwide perspective. J Natl Cancer Inst 87: 796- 802.
7. Bosch FX, Lorincz A, Munoz N, Meijer CJLM, Shah K. 2002. The causal relation between human papillomavirus and cervical cancer. J Clin Pathol 55: 244- 265.
8. Bosch FX, Burchell AN, Schiffman M, Giuliano AR, de Sanjosé S, Bruni L, Tortolero-Luna G, Krugar Kjaer S, Munoz N. 2008. Epidemiology and natural history of human papillomavirus infections and type specific implications in cervical neoplasia. Vaccine 26S: K1- K16.
9. Bowring J, Walker P. 2010. The "Jade Goody effect": What now for cervical cancer prevention? J Fam Plann Reprod Health Care 36: 51- 54.
10. Bruni L, Diaz M, Castellsagué X, Ferrer E, Bosch X, de Sanjosé S. 2010. Cervical human papillomavirus prevalence in 5 Continents: Meta-analysis of 1 million women with normal cytological findings. J Infect Dis 202: 1789- 1799.
11. Burk RD, Kelly P, Feldman J, Bromberg J, Vermund SH, DeHovitz JA, Landesman SH. 1996. Declining prevalence of cervicovaginal human papillomavirus infection with age is independent of other risk factors. Sex Transm Dis 23: 333- 341.
12. Castellsagué X, Schneider A, Kaufmann AM, Bosch FX. 2009. HPV vaccination against cervical cancer in women above 25 years of age: Key considerations and current perspectives. Gynecol Oncol 115: S15- S23.
13. Castle PE, Schiffman M, Burk RD, Wacholder S, Hildesheim A, Herrero R, Bratti MC, Sherman ME, Lorincz A. 2002. Restricted cross-reactivity of Hybrid Capture 2 with non-oncogenic human papillomavirus types. Cancer Epidemiol Biomarkers Prev 11: 1394- 1399.
14. Clifford GM, Gallus S, Herrero R, Muñoz N, Snijders PJF, Vaccarella S, Anh PTH, Ferreccio C, Hieu NT, Matos E, Molano M, Rajkumar R, Ronco G, de Sanjosé S, Shin HR, Sukvirach S, Thomas JO, Tunsakul S, Meijer CJLM, Franceschi S, Group atIHPSS. 2005. Worldwide distribution of human papillomavirus types in cytologically normal women in the International Agency for Research on Cancer HPV prevalence surveys: A pooled analysis. Lancet 366: 991- 998.
15. Clifford G, Franceschi S, Diaz M, Muñoz N, Villa LL. 2006. Chapter 3: HPV type distribution in women with and without cervical neoplastic diseases. Vaccine 24: S26- S34.
16. Cotton SC, Sharp L, Seth R, Masson LF, Little J, Cruickshank ME, Neal K, Waugh N. 2007. Lifestyle and socio-demographic factors associated with high-risk HPV infection in UK women. Br J Cancer 97: 133- 139.
17. Currin LG, Jack RH, Linklater KM, Mak V, Møller H, Davies EA. 2009. Inequalities in the incidence of cervical cancer in South East England 2001-2005: An investigation of population risk factors. BMC Public Health 9: 62.
18. Cuschieri KS, Cubie HA, Whitley MW, Seagar AL, Arends MJ, Moore C, Gilkisson G. 2004. Multiple high risk HPV infections are common in cervical neoplasia and young women in a cervical screening population. J Clin Pathol 57: 68- 72.
19. Cuzick J, Terry G, Ho L, Hollingworth T, Anderson M. 1994. Type-specific human papillomavirus DNA in abnormal smears as a predictor of high-grade cervical intraepithelial neoplasia. Br J Cancer 69: 167- 171.
20. Cuzick J, Szarewski A, Terry G, Ho L, Hanby A, Maddox P, Anderson M, Kocjan G, Steele ST, Guillebaud J. 1995. Human papillomavirus testing in primary cervical screening. Lancet 345: 1533- 1536.
21. Cuzick J, Beverley E, Ho L, Terry G, Sapper H, Mielzynska I, Lorincz A, Chan WK, Krausz T, Soutter P. 1999. HPV testing in primary screening of older women. Br J Cancer 81: 554- 558.
22. Cuzick J, Szarewski A, Mesher D, Cadman L, Austin J, Perryman K, Ho L, Terry G, Sasieni P, Dina R, Soutter WP. 2008. Long-term follow-up of cervical abnormalities among women screened by HPV testing and cytology-results from the Hammersmith study. Int J Cancer 122: 2294- 2300.
23. Cuzick J, Castanon A, Sasieni P. 2010. Predicted impact of vaccination against human papillomavirus 16/18 on cancer incidence and cervical abnormalities in women aged 20-29 in the UK. Br J Cancer 102: 933- 939.
24. de Sanjosé S, Diaz M, Castellsagué X, Clifford G, Bruni L, Muñoz N, Bosch F. 2007. Worldwide prevalence and genotype distribution of cervical human papillomavirus DNA in women with normal cytology: A meta-analysis. Lancet Infect Dis 7: 453- 459.
25. DerSimonian R, Laird N. 1986. Meta-analysis in clinical trials. Control Clin Trials 7: 177- 188.
26. Evans DM, Hudson EA, Brown CL, Boddington MM, Hughes HE, Mackenzie EF, Marshall T. 1986. Terminology in gynaecological cytopathology: Report of the working party of the British society for clinical cytology. J Clin Pathol 39: 933- 944.
27. Franco EL, Villa LL, Sobrinho JP, Prado JM, Rousseau M-C, Desy M, Rohan TE. 1999. Epidemiology of acquisition and clearance of cervical human papillomavirus infection in women from a high-risk area for cervical cancer. J Infect Dis 180: 1415- 1423.
28. Freeman M, Tukey J. 1950. Transformations related to the angular and the square root. Ann Math Stat 4: 607- 611.
29. Grainge MJ, Seth R, Guo L, Neal KR, Coupland C, Vryenhoef P, Johnston J, Jenkins D. 2005. Cervical human papillomavirus screening among older women. Emerg Infect Dis 11: 1680- 1685.
30. Griffin NR, Bevan IS, Lewis FA, Wells M, Young LS. 1990. Demonstration of multiple HPV types in normal cervix and in cervical squamous cell carcinoma using the polymerase chain reaction on paraffin wax embedded material. J Clin Pathol 43: 52- 56.
31. Hallam N, Green J, Gibson P, Powis J, Bibby J. 1991. Prevalence of HPV cervical infection in a family planning clinic determined by polymerase chain reaction and dot blot hybridisation. J Med Virol 34: 154- 158.
32. Herbert A, Best JM, Chana P, Ktori E, Nowicki M, Dunsmore H, Culora G, Arbyn M, Kubba AA. 2007. Human papillomavirus testing with conventional Pap smear screening in three inner London community clinics. J Fam Plann Reprod Health Care 33: 171- 176.
33. Herrero R, Castle PE, Schiffman M, Bratti MC, Hildesheim A, Morales J, Alfaro M, Sherman ME, Wacholder S, Chen S, Rodriguez AC, Burk RD. 2005. Epidemiologic profile of type-specific human papillomavirus infection and cervical neoplasia in Guancastle, Costa Rica. J Infect Dis 191: 1796- 1807.
34. Hibbitts S, Rieck GC, Hart K, Powell NG, Beukenholdt R, Dallimore N, McRea J, Hauke A, Tristram A, Fiander AN. 2006. Human papillomavirus infection; an anonymous prevalence study in South Wales, UK. Br J Cancer 95: 226- 232.
35. Hibbitts S, Jones J, Powell N, Dallimore N, McRea J, Beer H, Tristram A, Fielder H, Fiander AN. 2008. Human papillomavirus prevalence in women attending routine cervical cancer screening in South Wales, UK: A cross-sectional study. Br J Cancer 99: 1929- 1933.
36. Higgins J, Thompson S, Decks J, Altman DG. 2003. Measuring inconsistency in meta-analyses. BMJ 327: 557- 560.
37. Ho GYF, 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.
38. Howell-Jones R, Bailey A, Beddows S, Sargent A, de Silva N, Wilson G, Anton J, Nichols T, Soldan K, Kitchener H, on behalf of the Study Group Collaborators. 2010. Multi-site study of HPV type-specific prevalence in women with cervical cancer, intraepithelial neoplasia and normal cytology in England. Br J Cancer 103: 209- 216.
39. JCVI. 2008. JCVI statement on human papillomavirus vaccines to protect against cervical cancer London Joint Committee on Vaccination and Immunisation.
40. Jones J, Powell NG, Tristram A, Fiander AN, Hibbitts S. 2009. Comparison of the PapilloCheck DNA micro-array human papillomavirus detection assay with Hybrid Capture II and PCR-enzyme immunoassay using the GP5/6+ primer set. J Clin Virol 45: 100- 104.
41. Keegan H, Ryan F, Malkin A, Griffin M, Lambkin H. 2007. Human papillomavirus prevalence and genotypes in an opportunistically screened Irish female population. Br J Biomed Sci 64: 18- 22.
42. Keegan H, Mc Inerney J, Pilkington L, Gronn 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.
43. Kelly RS, Patnick J, Kitchener HC, Moss SM, On behalf of the NHSCSP HPV Special Interest Group. 2011. HPV testing as a triage for borderline or mild dyskaryosis on cervical cytology: Results from the Sentinel study. Br J Cancer 105: 983- 988.
44. Kelly RS, Walker P, Kitchener H, Moss SM. 2012. Incidence of cervical intraepithelial neoplasia grade 2 or worse in colposcopy-negative/human papillomavirus-positive women with low-grade cytological abnormalities. BJOG 119: 20- 25.
45. Kitchener HC, Almonte M, Wheeler P, Desai M, Gilham C, Bailey A, Sargent A, Peto J, ARTISTIC Trial Study Group. 2006. HPV testing in routine cervical screening: Cross sectional data from the ARTISTIC trial. Br J Cancer 95: 56- 61.
46. Kitchener HC, Almonte M, Gilham C, Dowie R, Stoykova B, Sargent A, Roberts C, Desai M, Peto J, On behalf of the ARTISTIC Trial Study Group. 2009. ARTISTIC: A randomised trial of human papillomavirus (HPV) testing in primary cervical screening. Health Technol Assess 13: 1- 150.
47. Lu B, Kumar A, Castellsague X, Giuliano AR. 2011. Efficacy and safety of prophylactic vaccines against cervical HPV infection and diseases among women: A systematic review & meta-analysis. BMC Infect Dis 11: 13.
48. McCaffery K, Waller J, Forrest S, Cadman L, Szarewski A, Wardle J. 2004. Testing positive for human papillomavirus in routine cervical screening: Examination of psychosocial impact. BJOC 111: 1437- 1443.
49. Mesher D, Szarewski A, Cadman L, Cubie H, Kitchener H, Luesley D, Menon U, Hulman G, Desai M, Ho L, Terry G, Williams A, Sasieni P, Cuzick J. 2010. Long-term follow-up of cervical disease in women screened by cytology and HPV testing: Results from the HART study. Br J Cancer 102: 1405- 1410.
50. Metcalfe D, Price C, Powell J. 2011. Media coverage and public reaction to a celebrity cancer diagnosis. J Public Health 33: 80- 85.
51. Meyer T, Arndt R, Christophers E, Beckmann E-R, Schroder S, Gissmann L, Stockfleth E. 1998. Association of rare human papillomavirus types with genital premalignant and malignant lesions. J Infect Dis 178: 252- 255.
52. Moher D, Linberati A, Tetzlaff J, Altman DG, Group TP. 2009. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLoS Med 6: e1000097.
53. Muñoz N, Bosch XF, de Sanjosé S, Herrero R, Castellsagué X, Shah KV, Snijders PJF, Meijer CJLM, For the 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.
54. Newcombe RG. 1998. Two-sided confidence intervals for the single proportion: Comparison of seven methods. Stat Med 17: 857- 872.
55. Nielsen A, Kjaer SK, Muck C, Iftner T. 2008. Type-Specific HPV Infection and multiple HPV types: Prevalence and risk profile in Nearly 12, 000 younger and older Danish women. Sex Transm Dis 35: 276- 282.
56. Olsson SE, Kjaer SK, Sigurdsson K, Iverson OE, Hernandez-Avila M, Wheeler CM, Perez G, Brown DR, Koutsky LA, Tay EH. 2009. Evaluation of quadrivalent HPV 6/11/16/18 vaccine efficacy against cervical and angiogenital disease in subjects with serological evidence of prior vaccine type HPV infection. Hum Vaccin 5: 696- 704.
57. Perrons C, Brink N, Jalal H, Watts P, Jelley R. 2005. The impact of high risk human papillomavirus testing in an inner London colposcopy clinic. J Med Virol 76: 576- 582.
58. Peto J, Gilham C, Deacon J, Taylor C, Evans C, Binns W, Haywood M, Elanko N, Coleman D, Yule R, Desai M. 2004. Cervical HPV infection and neoplasia in a large population-based prospective study: The Manchester cohort. Br J Cancer 91: 942- 953.
59. Pisani P, Parkin M, Munoz N, Ferlay J. 1997. Cancer and infection: Estimates of the attributable fraction in 1990. Cancer Epidemiol Biomarkers Prev 6: 387- 400.
60. Quality Assurance Reference Centre. 2010. Northern Ireland cervical screening programme Public Health Agency.
61. Richardson H, Kelsall G, Tellier P, Voyer H, Abrahamowicz H, Ferency A, Coutlee F, Franco E. 2003. Human papillomavirus infections in female university students. Cancer Epidemiol Biomarkers Prev 12: 485- 490.
62. Roberts SA, Brabin L, Stretch R, Baxter D, Elton P, Kitchener H, McCann R. 2011. Human papillomavirus vaccination and social inequality: Results from a prospective cohort study. Epidemiol Infect 139: 400- 405.
63. Sargent A, Bailey A, Almonte M, Turner A, Thomson C, Peto J, Desai M, Mather J, Moss S, Roberts C, Kitchener HC, ARTISTIC Study Group. 2008. Prevalence of type-specific HPV infection by age and grade of cervical cytology: Data from the ARTISTIC trial. Br J Cancer 98: 1704- 1709.
64. Schiffman M, Castle PE, Jeronimo J, Rodriguez AC, Wacholder S. 2007. Human papillomavirus and cervical cancer. Lancet 370: 890- 907.
65. Scholl SM, Pillers EM, Robinson RE, Farrell PJ. 1985. Prevalence of human papillomavirus type 16 DNA in cervical carcinoma samples in East Anglia. Int J Cancer 35: 215- 218.
66. Simon P. 2008. Prophylactic efficacy of GSK AS04-adjuvanted HPV vaccine in adult women. 8th International multidisciplinary congress of the European Research Organization on Genital Infection and Neoplasia (EUROGIN) Nice pTC2-9.
67. Smith JS, Melendy A, Rana RK, Pimenta JM. 2008. Age-specific prevalence of infection with human papillomavirus in females: A global review. J Adolesc Health 43: S5- S25.
68. Tidy JA, Parry GC, Ward P, Coleman DV, Peto J, Malcolm AD, Farrell PJ. 1989a. High rate of human papillomavirus type 16 infection in cytologically normal cervices. Lancet 1: 434.
69. Tidy JA, Vousden KA, Farrell PJ. 1989b. Relation between infection with a subtype of HPV16 and cervical neoplasia. Lancet 1: 1225- 1227.
70. Vernon SD, Unger ER, Williams D. 2000. Comparison of human papillomavirus detection and typing by cycle sequencing, line blotting and hybrid capture. J Clin Microbiol 38: 651- 655.
71. Villa LL, Denny L. 2006. Methods for detection of HPV infection and it's clinical utility. Int J Gynecol Obstet 94: S71- S80.
72. Walboomers JMM, Jacobs MV, Manos MM, Bosch X, Kummer A, Shah K, Snijders PJF, Peto J, Meijer CJL, Munoz N. 1999. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 189: 12- 19.
73. WHO/ICO. 2010. Human papillomavirus and related cancers in United Kingdom. Information Centre on HPV and Cervical Cancer (HPV Information Centre).
74. Wilson E. 1927. Probable inference, the law of succession and statistical inference. J Am Stat Assoc 22: 209- 212.
75. Woodman CBJ, Collins S, Winter H, Bailey A, Ellis J, Prior P, Yates M, Rollason TP. 2001. Natural history of cervical human papillomavirus infection in young women: A longitudinal cohort study. Lancet 357: 1831- 1836.