Population-level impact and herd effects following the introduction of human papillomavirus vaccination programmes: updated systematic review and meta-analysis

The Lancet

Volumn 394, Issue 10197, 2019, Pages 497-509

  Drolet, Mélanie ^a   Bénard, Élodie ^a,b   Perez N ^a   Brisson, Marc ^a,b,c   Ali, Hammad ^d   Boily, Marie Claude ^d   Baldo, Vincenzo ^d   Brassard, Paul ^d   Brotherton, Julia M L ^d   Callander, Denton ^d   Checchi, M ^d   Chow, Eric P F ^d   Cocchio, Silvia ^d   Dalianis, Tina ^d   Deeks, Shelley L ^d   Dehlendorff, Christian ^d   Donovan, B ^d   Fairley, Christopher K ^d   Flagg, Elaine W ^d   Gargano, Julia W ^d   Garland, Suzanne M ^d   Grün, Nathalie ^d   Hansen, Bo T ^d   Harrison, Christopher ^d   Herweijer, Eva ^d   Imburgia, Teresa M ^d   Johnson, Anne M ^d   Kahn, Jessica A ^d   Kavanagh, Kimberley ^d   Kjaer, Susanne K ^d   Kliewer, Erich V ^d   Liu, B ^d   Machalek, Dorothy A ^d   Markowitz, L ^d   Mesher, D ^d   Munk, Christian ^d   Niccolai, L ^d   Nygård, Mari ^d   Ogilvie, Gina ^d   Oliphant, Jeannie ^d   Pollock, Kevin G ^d   Purriños Hermida, Maria Jesús ^d   Smith, Megan A ^d   Steben, Marc ^d   Söderlund Strand, Anna ^d   Sonnenberg, Pam ^d   Sparen, Pär ^d   Tanton, C ^d   Wheeler, Cosette M ^d   Woestenberg, Petra J ^d   Yu, Bo Nancy ^d   more..

^a University Laval   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

^d NONE

Author keywords

[No Author keywords available]

Indexed keywords

WART VIRUS VACCINE;

ARTICLE; CONDYLOMA ACUMINATUM; HUMAN; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN PAPILLOMAVIRUS TYPE 18; HUMAN PAPILLOMAVIRUS TYPE 31; HUMAN PAPILLOMAVIRUS TYPE 33; HUMAN PAPILLOMAVIRUS TYPE 45; META ANALYSIS; PAPILLOMAVIRUS INFECTION; PREVALENCE; PRIORITY JOURNAL; SYSTEMATIC REVIEW; UTERINE CERVIX CARCINOMA IN SITU; VACCINATION; VACCINATION COVERAGE; ADOLESCENT; ADULT; AGE DISTRIBUTION; BIOASSAY; CLASSIFICATION; DRUG EFFECT; FEMALE; INCIDENCE; MALE; MASS IMMUNIZATION; PAPILLOMAVIRIDAE; UTERINE CERVIX TUMOR; VIROLOGY; YOUNG ADULT;

ADOLESCENT; ADULT; AGE DISTRIBUTION; CERVICAL INTRAEPITHELIAL NEOPLASIA; CONDYLOMATA ACUMINATA; ENDPOINT DETERMINATION; FEMALE; HUMANS; INCIDENCE; MALE; MASS VACCINATION; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; PAPILLOMAVIRUS VACCINES; PREVALENCE; UTERINE CERVICAL NEOPLASMS; YOUNG ADULT;

EID: 85068774013     PISSN: 01406736     EISSN: 1474547X     Source Type: Journal    
DOI: 10.1016/S0140-6736(19)30298-3     Document Type: Article

References (106)

1. Bruni L, Diaz M, Barrionuevo-Roses L, et al. Worldwide female and male HPV vaccination coverage from 2006 to 2016. International Papillomavirus Conference; Cape Town; Feb 28–March 4, 2017.
2. Cervical Cancer Action. Global progress in HPV vaccination. http://www.cervicalcanceraction.org/comments/maps.php. (Accessed 23 May 2018)
3. Drolet, M, Bénard, É, Boily, MC, et al. Population-level impact and herd effects following human papillomavirus vaccination programmes: a systematic review and meta-analysis. Lancet Infect Dis 15 (2015), 565–580.
4. Franco, E, Schiffman, M, Wacholder, S, Stanley, M, Methodological issues for trials of vaccine efficacy against HPV types 16 and 18. ARC HPV Working Group, (eds.) Primary end-points for prophylactic vaccine trials, 2014, International Agency for Research on Cancer, Lyon, 39–45.
5. WHO. Human papillomavirus vaccines: WHO position paper, May 2017–recommendations. Vaccine 35 (2017), 5753–5755.
6. Liberati, A, Altman, DG, Tetzlaff, J, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ, 339, 2009, b2700.
7. Garland, SM, Steben, M, Sings, HL, et al. Natural history of genital warts: analysis of the placebo arm of 2 randomized phase III trials of a quadrivalent human papillomavirus (types 6, 11, 16, and 18) vaccine. J Infect Dis 199 (2009), 805–814.
8. DerSimonian, R, Laird, N, Meta-analysis in clinical trials. Control Clin Trials 7 (1986), 177–188.
9. Deeks, JJ, Higgins, JPT, on behalf of the Statistical Methods Group of the Cochrane Collaboration. Statistical algorithms in Review Manager 5. https://training.cochrane.org/handbook/statistical-methods-revman5. (Accessed 23 May 2014)
10. Deeks, JJ, Higgins, PT, Altman, DG, Analysing data and undertaking meta-analyses. Higgins, JPT, Green, S, (eds.) Cochrane handbook for systematic reviews of interventions version 5.1.0 (updated March 2011), 2011, The Cochrane Collaboration.
11. Dillner, J, Nygård, M, Munk, C, et al. Decline of HPV infections in Scandinavian cervical screening populations after introduction of HPV vaccination programs. Vaccine 36 (2018), 3820–3829.
12. Chow, EP, Danielewski, JA, Fehler, G, et al. Human papillomavirus in young women with Chlamydia trachomatis infection 7 years after the Australian human papillomavirus vaccination programme: a cross-sectional study. Lancet Infect Dis 15 (2015), 1314–1323.
13. Chow, EPF, Machalek, DA, Tabrizi, SN, et al. Quadrivalent vaccine-targeted human papillomavirus genotypes in heterosexual men after the Australian female human papillomavirus vaccination programme: a retrospective observational study. Lancet Infect Dis 17 (2017), 68–77.
14. Cummings, T, Zimet, GD, Brown, D, et al. Reduction of HPV infections through vaccination among at-risk urban adolescents. Vaccine 30 (2012), 5496–5499.
15. Dunne, EF, Naleway, A, Smith, N, et al. Reduction in human papillomavirus vaccine type prevalence among young women screened for cervical cancer in an integrated US healthcare delivery system in 2007 and 2012–2013. J Infect Dis 212 (2015), 1970–1975.
16. Grün, N, Ährlund-Richter, A, Franzén, J, et al. Follow-up on oral and cervical human papillomavirus prevalence 2013–2015 in youth at a youth clinic in Stockholm, Sweden. Infect Dis (Lond) 48 (2016), 169–170.
17. Kavanagh, K, Pollock, KG, Potts, A, et al. Introduction and sustained high coverage of the HPV bivalent vaccine leads to a reduction in prevalence of HPV 16/18 and closely related HPV types. Br J Cancer 110 (2014), 2804–2811.
18. Cameron, RL, Kavanagh, K, Pan, J, et al. Human papillomavirus prevalence and herd immunity after introduction of vaccination program, Scotland, 2009–2013. Emerg Infect Dis 22 (2016), 56–64.
19. Kavanagh, K, Pollock, KG, Cuschieri, K, et al. Changes in the prevalence of human papillomavirus following a national bivalent human papillomavirus vaccination programme in Scotland: a 7-year cross-sectional study. Lancet Infect Dis 17 (2017), 1293–1302.
20. Kahn, JA, Brown, DR, Ding, L, et al. Vaccine-type human papillomavirus and evidence of herd protection after vaccine introduction. Pediatrics 130 (2012), e249–e256.
21. Kahn, JA, Widdice, LE, Ding, L, et al. Substantial decline in vaccine-type human papillomavirus (HPV) among vaccinated young women during the first 8 years after HPV vaccine introduction in a community. Clin Infect Dis 63 (2016), 1281–1287.
22. Machalek, DA, Garland, SM, Brotherton, JML, et al. Very low prevalence of vaccine human papillomavirus types among 18- to 35-year old Australian women 9 years following implementation of vaccination. J Infect Dis 217 (2018), 1590–1600.
23. Markowitz, LE, Hariri, S, Lin, C, et al. Reduction in human papillomavirus (HPV) prevalence among young women following HPV vaccine introduction in the United States, National Health and Nutrition Examination Surveys, 2003–2010. J Infect Dis 208 (2013), 385–393.
24. Markowitz, LE, Liu, G, Hariri, S, Steinau, M, Dunne, EF, Unger, ER, Prevalence of HPV after introduction of the vaccination program in the United States. Pediatrics, 137, 2016, e20151968.
25. Oliver, SE, Unger, ER, Lewis, R, et al. Prevalence of human papillomavirus among females after vaccine introduction—National Health and Nutrition Examination Survey, United States, 2003–2014. J Infect Dis 216 (2017), 594–603.
26. Mesher, D, Panwar, K, Thomas, SL, Beddows, S, Soldan, K, Continuing reductions in HPV 16/18 in a population with high coverage of bivalent HPV vaccination in England: an ongoing cross-sectional study. BMJ Open, 6, 2016, e009915.
27. Mesher, D, Soldan, K, Howell-Jones, R, et al. Reduction in HPV 16/18 prevalence in sexually active young women following the introduction of HPV immunisation in England. Vaccine 32 (2013), 26–32.
28. Mesher, D, Panwar, K, Thomas, SL, et al. The impact of the national HPV vaccination program in England using the bivalent HPV vaccine: surveillance of type-specific HPV in young females, 2010–2016. J Infect Dis 218 (2018), 911–921.
29. Purriños-Hermida, MJ, Santiago-Pérez, MI, Treviño, M, et al. Direct, indirect and total effectiveness of bivalent HPV vaccine in women in Galicia, Spain. PLoS One, 13, 2018, e0201653.
30. Söderlund-Strand, A, Uhnoo, I, Dillner, J, Change in population prevalences of human papillomavirus after initiation of vaccination: the high-throughput HPV monitoring study. Cancer Epidemiol Biomarkers Prev 23 (2014), 2757–2764.
31. Sonnenberg, P, Clifton, S, Beddows, S, et al. Prevalence, risk factors, and uptake of interventions for sexually transmitted infections in Britain: findings from the National Surveys of Sexual Attitudes and Lifestyles (Natsal). Lancet 382 (2013), 1795–1806.
32. Tabrizi, SN, Brotherton, JML, Kaldor, JM, et al. Fall in human papillomavirus prevalence following a national vaccination program. J Infect Dis 206 (2012), 1645–1651.
33. Tabrizi, SN, Brotherton, JML, Kaldor, JM, et al. Assessment of herd immunity and cross-protection after a human papillomavirus vaccination programme in Australia: a repeat cross-sectional study. Lancet Infect Dis 14 (2014), 958–966.
34. Ali, H, Donovan, B, Wand, H, et al. Genital warts in young Australians five years into national human papillomavirus vaccination programme: national surveillance data. BMJ, 346, 2013, f2032.
35. Ali, H, McManus, H, O'Connor, CC, et al. Human papillomavirus vaccination and genital warts in young Indigenous Australians: national sentinel surveillance data. Med J Aust 206 (2017), 204–209.
36. Chow, EP, Read, TR, Wigan, R, et al. Ongoing decline in genital warts among young heterosexuals 7 years after the Australian human papillomavirus (HPV) vaccination programme. Sex Transm Infect 91 (2015), 214–219.
37. Callander, D, Ali, H, Donovan, B, Genital Warts Surveillance Network report 2004-2015. 2016, The Kirby Institute, Sydney, NSW.
38. Baandrup, L, Blomberg, M, Dehlendorff, C, Sand, C, Andersen, KK, Kjaer, SK, Significant decrease in the incidence of genital warts in young Danish women after implementation of a national human papillomavirus vaccination program. Sex Transm Dis 40 (2013), 130–135.
39. Bollerup, S, Baldur-Felskov, B, Blomberg, M, Baandrup, L, Dehlendorff, C, Kjaer, SK, Significant reduction in the incidence of genital warts in young men 5 years into the Danish human papillomavirus vaccination program for girls and women. Sex Transm Dis 43 (2016), 238–242.
40. Bauer, HM, Wright, G, Chow, J, Evidence of human papillomavirus vaccine effectiveness in reducing genital warts: an analysis of California public family planning administrative claims data, 2007–2010. Am J Public Health 102 (2012), 833–835.
41. Cocchio, S, Baldovin, T, Bertoncello, C, et al. Decline in hospitalization for genital warts in the Veneto region after an HPV vaccination program: an observational study. BMC Infect Dis, 17, 2017, 249.
42. Dominiak-Felden, G, Gobbo, C, Simondon, F, Evaluating the early benefit of quadrivalent HPV vaccine on genital warts in Belgium: a cohort study. PLoS One, 10, 2015, e0132404.
43. Flagg, EW, Schwartz, R, Weinstock, H, Prevalence of anogenital warts among participants in private health plans in the United States, 2003–2010: potential impact of human papillomavirus vaccination. Am J Public Health 103 (2013), 1428–1435.
44. Flagg, EW, Torrone, EA, Declines in anogenital warts among age groups most likely to be impacted by human papillomavirus vaccination, United States, 2006–2014. Am J Public Health 108 (2018), 112–119.
45. Guerra, FM, Rosella, LC, Dunn, S, Wilson, SE, Chen, C, Deeks, SL, Early impact of Ontario's human papillomavirus (HPV) vaccination program on anogenital warts (AGWs): a population-based assessment. Vaccine 34 (2016), 4678–4683.
46. Harrison, C, Britt, H, Garland, S, et al. Decreased management of genital warts in young women in Australian general practice post introduction of national HPV vaccination program: results from a nationally representative cross-sectional general practice study. PLoS One, 9, 2014, e105967.
47. Howell-Jones, R, Soldan, K, Wetten, S, et al. Declining genital warts in young women in England associated with HPV 16/18 vaccination: an ecological study. J Infect Dis 208 (2013), 1397–1403.
48. Canvin, M, Sinka, K, Hughes, G, Mesher, D, Decline in genital warts diagnoses among young women and young men since the introduction of the bivalent HPV (16/18) vaccination programme in England: an ecological analysis. Sex Transm Infect 93 (2017), 125–128.
49. Kliewer EV, Mahmud SM, Demers AA, Lambert P, Musto G. Quadrivalent HPV vaccination and the incidence of anogenital warts in Manitoba, Canada. 28th International Papillomavirus Conference; San Juan, Puerto Rico; Nov 30–Dec 6, 2012. Abstract E07–663.
50. Thompson, LH, Nugent, Z, Blanchard, JF, Ens, C, Yu, BN, Increasing incidence of anogenital warts with an urban-rural divide among males in Manitoba, Canada, 1990–2011. BMC Public Health, 16, 2016, 219.
51. Leval, A, Herweijer, E, Arnheim-Dahlström, L, et al. Incidence of genital warts in Sweden before and after quadrivalent human papillomavirus vaccine availability. J Infect Dis 206 (2012), 860–866.
52. Herweijer, E, Ploner, A, Sparén, P, Substantially reduced incidence of genital warts in women and men six years after HPV vaccine availability in Sweden. Vaccine 36 (2018), 1917–1920.
53. Liu, B, Donovan, B, Brotherton, JM, Saville, M, Kaldor, JM, Genital warts and chlamydia in Australian women: comparison of national population-based surveys in 2001 and 2011. Sex Transm Infect 90 (2014), 532–537.
54. Mikolajczyk, RT, Kraut, AA, Horn, J, Schulze-Rath, R, Garbe, E, Changes in incidence of anogenital warts diagnoses after the introduction of human papillomavirus vaccination in Germany —An ecologic study. Sex Transm Dis 40 (2013), 28–31.
55. Thöne, K, Horn, J, Mikolajczyk, R, Evaluation of vaccination herd immunity effects for anogenital warts in a low coverage setting with human papillomavirus vaccine-an interrupted time series analysis from 2005 to 2010 using health insurance data. BMC Infect Dis, 17, 2017, 564.
56. Oliphant, J, Perkins, N, Impact of the human papillomavirus (HPV) vaccine on genital wart diagnoses at Auckland Sexual Health Services. N Z Med J 124 (2011), 51–58.
57. Oliphant, J, Stewart, J, Saxton, P, Lo, M, Perkins, N, Ward, D, Trends in genital warts diagnoses in New Zealand five years following the quadrivalent human papillomavirus vaccine introduction. N Z Med J 130 (2017), 9–16.
58. Smith, MA, Liu, B, McIntyre, P, Menzies, R, Dey, A, Canfell, K, Fall in genital warts diagnoses in the general and indigenous Australian population following implementation of a national human papillomavirus vaccination program: analysis of routinely collected national hospital data. J Infect Dis 211 (2015), 91–99.
59. Smith, MA, Liu, B, McIntyre, P, Menzies, R, Dey, A, Canfell, K, Trends in genital warts by socioeconomic status after the introduction of the national HPV vaccination program in Australia: analysis of national hospital data. BMC Infect Dis, 16, 2016, 52.
60. Sonnenberg P, Tanton C, King E, et al. Genital warts & HPV 6/11 in the British population: data from the third National Survey of Sexual Attitudes and Lifestyles (Natsal-3). 31st International Papillomavirus Conference; Cape Town; Feb 28–March 4, 2017. Abstract 454.
61. Steben, M, Ouhoummane, N, Rodier, C, Sinyavskaya, L, Brassard, P, The early impact of human papillomavirus vaccination on anogenital warts in Québec, Canada. J Med Virol 90 (2018), 592–598.
62. Woestenberg, PJ, King, AJ, van der Sande, MA, et al. No evidence for cross-protection of the HPV-16/18 vaccine against HPV-6/11 positivity in female STI clinic visitors. J Infect 74 (2017), 393–400.
63. Sandø, N, Kofoed, K, Zachariae, C, Fouchard, J, A reduced national incidence of anogenital warts in young Danish men and women after introduction of a national quadrivalent human papillomavirus vaccination programme for young women – an ecological study. Acta Derm Venereol 94 (2014), 288–292.
64. Nsouli-Maktabi, H, Ludwig, SL, Yerubandi, UD, Gaydos, JC, Incidence of genital warts among U.S. service members before and after the introduction of the quadrivalent human papillomavirus vaccine. MSMR 20 (2013), 17–20.
65. Baldur-Felskov, B, Dehlendorff, C, Junge, J, Munk, C, Kjaer, SK, Incidence of cervical lesions in Danish women before and after implementation of a national HPV vaccination program. Cancer Causes Control 25 (2014), 915–922.
66. Baldur-Felskov, B, Munk, C, Nielsen, TSS, et al. Trends in the incidence of cervical cancer and severe precancerous lesions in Denmark, 1997–2012. Cancer Causes Control 26 (2015), 1105–1116.
67. Benard, VB, Castle, PE, Jenison, SA, et al. Population-based incidence rates of cervical intraepithelial neoplasia in the human papillomavirus vaccine era. JAMA Oncol 3 (2017), 833–837.
68. 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 (2011), 2085–2092.
69. Australian Institute of Health and Welfare. Cervical screening in Australia 2013–2014. National Cervical Screening Program. https://www.aihw.gov.au/getmedia/c5e7776b-907e-4467-b435-8d6863ef33e7/19750.pdf.aspx?inline=true. (Accessed 2 November 2018)
70. Australian Institute of Health and Welfare. Cervical screening in Australia: 2018. National Cervical Screening Program. https://www.aihw.gov.au/getmedia/8a26b34d-a912-4f01-b646-dc5d0ca54f03/aihw-can-111.pdf.aspx?inline=true. (Accessed 25 January 2019)
71. Flagg, EW, Torrone, EA, Weinstock, H, Ecological Association of Human Papillomavirus Vaccination with Cervical Dysplasia Prevalence in the United States, 2007–2014. Am J Public Health 106 (2016), 2211–2218.
72. Gargano, JW, Park, IU, Griffin, MR, et al. Trends in high-grade cervical lesions and cervical cancer screening in five states, 2008–2015. Clin Infect Dis, 2018 published online Aug 23. DOI:10.1093/cid/ciy707.
73. Niccolai, LM, Julian, PJ, Meek, JI, McBride, V, Hadler, JL, Sosa, LE, Declining rates of high-grade cervical lesions in young women in Connecticut, 2008–2011. Cancer Epidemiol Biomarkers Prev 22 (2013), 1446–1450.
74. Niccolai, LM, Meek, JI, Brackney, M, Hadler, JL, Sosa, LE, Weinberger, DM, Declines in human papillomavirus (HPV)–associated high-grade cervical lesions after introduction of HPV vaccines in Connecticut, United States, 2008–2015. Clin Infect Dis 65 (2017), 884–889.
75. Liaw, KL, Kjaer, S, Nygard, M, Dillner, J, Utilization of nordic countries national registries to monitor the impact of HPV vaccination. Pharmacoepidemiol Drug Saf, 23, 2014, 356.
76. Ogilvie, GS, Naus, M, Money, DM, et al. Reduction in cervical intraepithelial neoplasia in young women in British Columbia after introduction of the HPV vaccine: an ecological analysis. Int J Cancer 137 (2015), 1931–1937.
77. Pollock, KG, Kavanagh, K, Potts, A, et al. Reduction of low- and high-grade cervical abnormalities associated with high uptake of the HPV bivalent vaccine in Scotland. Br J Cancer 111 (2014), 1824–1830.
78. Chen, HY, Kessler, CL, Mori, N, Chauhan, SP, Cervical cancer screening in the United States, 1993–2010: characteristics of women who are never screened. J Womens Health (Larchmt) 21 (2012), 1132–1138.
79. Jemal, A, Simard, EP, Dorell, C, et al. Annual report to the nation on the status of cancer, 1975–2009, featuring the burden and trends in human papillomavirus (HPV)-associated cancers and HPV vaccination coverage levels. J Natl Cancer Inst 105 (2013), 175–201.
80. Tiro, JA, Tsui, J, Bauer, HM, Yamada, E, Kobrin, S, Breen, N, Human papillomavirus vaccine use among adolescent girls and young adult women: an analysis of the 2007 California Health Interview Survey. J Womens Health (Larchmt) 21 (2012), 656–665.
81. Chao, C, Silverberg, MJ, Becerra, TA, et al. Human papillomavirus vaccination and subsequent cervical cancer screening in a large integrated healthcare system. Am J Obstet Gynecol 216 (2017), 151.e1–151.e9.
82. Drolet, M, Laprise, JF, Brotherton, JML, et al. The impact of human papillomavirus catch-up vaccination in Australia: implications for introduction of multiple age cohort vaccination and postvaccination data interpretation. J Infect Dis 216 (2017), 1205–1209.
83. Chaiyakunapruk N, Ng SS. Summary of evidence. Human papillomavirus (HPV) vaccination: an updated systematic review of cost-effectiveness analyses. Meeting of the Strategic Advisory Group of Experts on Immunization (SAGE); Geneva; October, 2016.
84. WHO. Human papillomavirus vaccines: WHO position paper, October 2014. Wkly Epidemiol Rec 89 (2014), 465–491.
85. Meites, E, Kempe, A, Markowitz, LE, Use of a 2-dose schedule for human papillomavirus vaccination —updated recommendations of the Advisory Committee on Immunization Practices. MMWR Morb Mortal Wkly Rep 65 (2016), 1405–1408.
86. Pagliusi, SR, Teresa Aguado, M, Efficacy and other milestones for human papillomavirus vaccine introduction. Vaccine 23 (2004), 569–578.
87. National Advisory Committee on Immunization (NACI). Statement on human papillomavirus vaccine. An advisory committee statement (ACS). Can Commun Dis Rep 33:ACS-2 (2007), 1–31.
88. US Food and Drug Administration. Vaccines, blood & biologics: Gardasil. https://www.fda.gov/BiologicsBloodVaccines/Vaccines/ApprovedProducts/ucm094042.htm. (Accessed 2 May 2019)
89. European Centre for Disease Prevention and Control. Guidance for the introduction of HPV vaccines in EU countries. Stockholm. https://ecdc.europa.eu/sites/portal/files/media/en/publications/Publications/0801_GUI_Introduction_of_HPV_Vaccines_in_EU.pdf, January, 2008. (Accessed 2 May 2019)
90. Richardson, LA, Tota, J, Franco, EL, Optimizing technology for cervical cancer screening in high-resource settings. Expert Rev Obstet Gynecol 6 (2011), 343–353.
91. Canfell, K, Caruana, M, Gebski, V, et al. Cervical screening with primary HPV testing or cytology in a population of women in which those aged 33 years or younger had previously been offered HPV vaccination: results of the compass pilot randomised trial. PLoS Med, 14, 2017, e1002388.
92. Drolet, M, Boily, MC, Greenaway, C, et al. Sociodemographic inequalities in sexual activity and cervical cancer screening: implications for the success of human papillomavirus vaccination. Cancer Epidemiol Biomarkers Prev 22 (2013), 641–652.
93. Herweijer, E, Feldman, AL, Ploner, A, et al. The participation of HPV-vaccinated women in a national cervical screening program: population-based cohort study. PLoS One, 10, 2015, e0134185.
94. Tanton, C, Soldan, K, Beddows, S, et al. High-risk human papillomavirus (HPV) infection and cervical cancer prevention in Britain: Evidence of differential uptake of interventions from a probability survey. Cancer Epidemiol Biomarkers Prev 24 (2015), 842–853.
95. Brotherton, JML, Gertig, DM, May, C, Chappell, G, Saville, M, HPV vaccine impact in Australian women: ready for an HPV-based screening program. Med J Aust, 204, 2016, 184.
96. Liu, G, Hariri, S, Bradley, H, Gottlieb, SL, Leichliter, JS, Markowitz, LE, Trends and patterns of sexual behaviors among adolescents and adults aged 14 to 59 years, United States. Sex Transm Dis 42 (2015), 20–26.
97. Lewis, R, Tanton, C, Mercer, CH, et al. Heterosexual practices among young people in Britain: evidence from three national surveys of sexual attitudes and lifestyles. J Adolesc Health 61 (2017), 694–702.
98. Mercer, CH, Tanton, C, Prah, P, et al. Changes in sexual attitudes and lifestyles in Britain through the life course and over time: findings from the National Surveys of Sexual Attitudes and Lifestyles (Natsal). Lancet 382 (2013), 1781–1794.
99. Rissel, C, Badcock, PB, Smith, AM, et al. Heterosexual experience and recent heterosexual encounters among Australian adults: the Second Australian Study of Health and Relationships. Sex Health 11 (2014), 416–426.
100. Jensen, KE, Munk, C, Sparen, P, et al. Women's sexual behavior. Population-based study among 65,000 women from four Nordic countries before introduction of human papillomavirus vaccination. Acta Obstet Gynecol Scand 90 (2011), 459–467.
101. Stenhammar, C, Ehrsson, YT, Åkerud, H, Larsson, M, Tydén, T, Sexual and contraceptive behavior among female university students in Sweden—repeated surveys over a 25-year period. Acta Obstet Gynecol Scand 94 (2015), 253–259.
102. Herlitz, CA, Forsberg, M, Sexual behaviour and risk assessment in different age cohorts in the general population of Sweden (1989–2007). Scand J Public Health 38 (2010), 32–39.
103. Cocchio, S, Bertoncello, C, Baldovin, T, Buja, A, Majori, S, Baldo, V, Self-reported genital warts among sexually-active university students: a cross-sectional study. BMC Infect Dis, 18, 2018, 41.
104. Marino, C, Vieno, A, Lenzi, M, Santinello, M, Time trends in adolescent sexual behaviour in Italy. Sex Health 11 (2014), 379–380.
105. Mori, S, Nakao, S, Kukimoto, I, Kusumoto-Matsuo, R, Kondo, K, Kanda, T, Biased amplification of human papillomavirus DNA in specimens containing multiple human papillomavirus types by PCR with consensus primers. Cancer Sci 102 (2011), 1223–1227.
106. Tota, JE, Ramanakumar, AV, Jiang, M, et al. Epidemiologic approaches to evaluating the potential for human papillomavirus type replacement postvaccination. Am J Epidemiol 178 (2013), 625–634.