The impact of 10 years of human papillomavirus (HPV) vaccination in Australia: what additional disease burden will a nonavalent vaccine prevent?

Eurosurveillance - Tập 23 Số 41 - 2018
Cyra Patel1, Julia Brotherton2,3, Alexis Pillsbury1, Sanjay Jayasinghe4,1, Basil Donovan5,6, Kristine Macartney4,1, Helen Marshall7,8
1National Centre for Immunisation Research and Surveillance, Westmead, Australia
2School of Population and Global Health, University of Melbourne, Parkville, Australia
3VCS Population Health, VCS Foundation, East Melbourne, Australia
4Discipline of Child and Adolescent Health, Faculty of Medicine and Health, University of Sydney, Sydney, Australia
5Sydney Sexual Health Centre, Sydney Hospital, Sydney, Australia
6The Kirby Institute, University of New South Wales, Sydney, Australia
7Robinson Research Institute and Adelaide Medical School, University of Adelaide, North Adelaide, Australia
8Vaccinology and Immunology Research Trials Unit, Women’s and Children’s Hospital, North Adelaide, Australia

Tóm tắt

Background: A National human papilloma virus (HPV) Vaccination Programme for the prevention of HPV infection and associated disease using the quadrivalent HPV vaccine (4vHPV) has been funded and implemented in Australia since 2007, initially for girls only and extended to boys in 2013, with uptake rates among the highest observed worldwide. Aim: We report on the impact of this national programme on HPV prevalence and associated disease burden and estimate the potential impact of adopting a nonavalent HPV (9vHPV) vaccine. Methods: We performed a non-systematic literature review of studies measuring the burden of HPV-associated disease and infection in Australia before and after introduction of HPV vaccination. We also included key national reports with estimates of HPV-related disease burden. Results: Substantial declines in high-grade cervical disease and genital warts among vaccine-eligible women have been observed. Reductions in genital warts incidence and HPV prevalence among heterosexual men of similar age were observed before introduction of the male vaccination programme, indicating a substantial herd effect. 9vHPV vaccine is expected to prevent up to 90% of cervical and 96% of anal cancers. Of an estimated 1,544 HPV-associated cancers in 2012, 1,242 would have been preventable by the 4vHPV vaccine and an additional 187 anogenital cancers by the 9vHPV vaccine. Conclusions: Vaccination using 4vHPV vaccine has had a large demonstrable impact on HPV-related disease in Australia. A switch to 9vHPV could further reduce the HPV-associated cancer burden. With continued high coverage among both males and females, elimination of vaccine-type HPV disease seems achievable in Australia.

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Tài liệu tham khảo

Australian Institute of Health and Welfare (AIHW). Cervical screening in Australia 2018. Cat. no. CAN 111. Canberra: AIHW; 2018. Available from: https://www.aihw.gov.au/reports/cancer-screening/cervical-screening-in-australia-2018/contents/table-of-contents

Condon, 2016, Trends in cancer incidence and survival for Indigenous and non-Indigenous people in the Northern Territory., Med J Aust, 205, 454, 10.5694/mja16.00588

Jin, 2011, Trends in anal cancer in Australia, 1982-2005., Vaccine, 29, 2322, 10.1016/j.vaccine.2011.01.015

Australian Institute of Health and Welfare (AIHW). Australian cancer incidence and mortality (ACIM) books: Anal cancer. Canberra: AIHW; 2016.

Machalek, 2012, Anal human papillomavirus infection and associated neoplastic lesions in men who have sex with men: a systematic review and meta-analysis., Lancet Oncol, 13, 487, 10.1016/S1470-2045(12)70080-3

Vajdic, 2009, Anal human papillomavirus genotype diversity and co-infection in a community-based sample of homosexual men., Sex Transm Infect, 85, 330, 10.1136/sti.2008.034744

Poynten, 2017, Vaccine-preventable anal human papillomavirus in Australian gay and bisexual men., Papillomavirus Res, 3, 80, 10.1016/j.pvr.2017.02.003

Grulich, 2010, Cancers attributable to human papillomavirus infection., Sex Health, 7, 244, 10.1071/SH10020

Wakeham, 2014, The burden of HPV-associated anogenital cancers., Curr Oncol Rep, 16, 402, 10.1007/s11912-014-0402-4

Condon, 2009, A cluster of vulvar cancer and vulvar intraepithelial neoplasia in young Australian indigenous women., Cancer Causes Control, 20, 67, 10.1007/s10552-008-9218-6

Ariyawardana, 2013, Trends of lip, oral cavity and oropharyngeal cancers in Australia 1982-2008: overall good news but with rising rates in the oropharynx., BMC Cancer, 13, 333, 10.1186/1471-2407-13-333

Hocking, 2011, Head and neck cancer in Australia between 1982 and 2005 show increasing incidence of potentially HPV-associated oropharyngeal cancers., Br J Cancer, 104, 886, 10.1038/sj.bjc.6606091

Hong, 2016, Rising prevalence of human papillomavirus-related oropharyngeal cancer in Australia over the last 2 decades., Head Neck, 38, 743, 10.1002/hed.23942

Elwood, 2014, Comparison of oropharyngeal and oral cavity squamous cell cancer incidence and trends in New Zealand and Queensland, Australia., Cancer Epidemiol, 38, 16, 10.1016/j.canep.2013.12.004

Chaturvedi, 2013, Worldwide trends in incidence rates for oral cavity and oropharyngeal cancers., J Clin Oncol, 31, 4550, 10.1200/JCO.2013.50.3870

Chow, 2015, 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, 1314, 10.1016/S1473-3099(15)00055-9

Tabrizi, 2012, Fall in human papillomavirus prevalence following a national vaccination program., J Infect Dis, 206, 1645, 10.1093/infdis/jis590

Tabrizi, 2014, Assessment of herd immunity and cross-protection after a human papillomavirus vaccination programme in Australia: a repeat cross-sectional study., Lancet Infect Dis, 14, 958, 10.1016/S1473-3099(14)70841-2

Osborne, 2015, Assessing genital human papillomavirus genoprevalence in young Australian women following the introduction of a national vaccination program., Vaccine, 33, 201, 10.1016/j.vaccine.2014.10.045

Tabrizi, 2014, HPV genotype prevalence in Australian women undergoing routine cervical screening by cytology status prior to implementation of an HPV vaccination program., J Clin Virol, 60, 250, 10.1016/j.jcv.2014.04.013

Machalek, 2018, 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, 1590, 10.1093/infdis/jiy075

Drolet, 2015, Population-level impact and herd effects following human papillomavirus vaccination programmes: a systematic review and meta-analysis., Lancet Infect Dis, 15, 565, 10.1016/S1473-3099(14)71073-4

Chow, 2017, 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, 68, 10.1016/S1473-3099(16)30116-5

Pillsbury, 2017, Population-level herd protection of males from a female human papillomavirus vaccination program: evidence from Australian serosurveillance., Clin Infect Dis, 65, 827, 10.1093/cid/cix436

Australian Institute of Health and Welfare (AIHW). Cervical screening in Australia 2013-2014. Cancer series no. 97. Cat. no. CAN 95. Canberra: AIHW; 2016.

Gertig, 2013, Impact of a population-based HPV vaccination program on cervical abnormalities: a data linkage study., BMC Med, 11, 227, 10.1186/1741-7015-11-227

Brotherton, 2015, Effectiveness of less than three doses of quadrivalent human papillomavirus vaccine against cervical intraepithelial neoplasia when administered using a standard dose spacing schedule: Observational cohort of young women in Australia., Papillomavirus Research., 1, 59, 10.1016/j.pvr.2015.05.005

Crowe, 2014, Effectiveness of quadrivalent human papillomavirus vaccine for the prevention of cervical abnormalities: case-control study nested within a population based screening programme in Australia., BMJ, 348, g1458, 10.1136/bmj.g1458

Smith, 2015, 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, 91, 10.1093/infdis/jiu370

Drolet, 2017, 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, 1205, 10.1093/infdis/jix476

Fairley, 2009, Rapid decline in presentations of genital warts after the implementation of a national quadrivalent human papillomavirus vaccination programme for young women., Sex Transm Infect, 85, 499, 10.1136/sti.2009.037788

Donovan, 2011, Quadrivalent human papillomavirus vaccination and trends in genital warts in Australia: analysis of national sentinel surveillance data., Lancet Infect Dis, 11, 39, 10.1016/S1473-3099(10)70225-5

Read, 2011, The near disappearance of genital warts in young women 4 years after commencing a national human papillomavirus (HPV) vaccination programme., Sex Transm Infect, 87, 544, 10.1136/sextrans-2011-050234

Ali, 2013, Genital warts in young Australians five years into national human papillomavirus vaccination programme: national surveillance data., BMJ, 346, f2032, 10.1136/bmj.f2032

Ali, 2013, Decline in in-patient treatments of genital warts among young Australians following the national HPV vaccination program., BMC Infect Dis, 13, 140, 10.1186/1471-2334-13-140

Chow, 2015, Ongoing decline in genital warts among young heterosexuals 7 years after the Australian human papillomavirus (HPV) vaccination programme., Sex Transm Infect, 91, 214, 10.1136/sextrans-2014-051813

Ali, 2017, Human papillomavirus vaccination and genital warts in young Indigenous Australians: national sentinel surveillance data., Med J Aust, 206, 204, 10.5694/mja16.00597

Larson, 2010, Epidemiology of recurrent respiratory papillomatosis., APMIS, 118, 450, 10.1111/j.1600-0463.2010.02619.x

Novakovic, 2018, A prospective study of the incidence of juvenile-onset recurrent respiratory papillomatosis after implementation of a national HPV vaccination program., J Infect Dis, 217, 208

Brotherton, 2017, Looking beyond human papillomavirus (HPV) genotype 16 and 18: Defining HPV genotype distribution in cervical cancers in Australia prior to vaccination., Int J Cancer, 141, 1576, 10.1002/ijc.30871

Baricevic, 2015, High-sensitivity human papilloma virus genotyping reveals near universal positivity in anal squamous cell carcinoma: different implications for vaccine prevention and prognosis., Eur J Cancer, 51, 776, 10.1016/j.ejca.2015.01.058

Hillman, 2014, Human papillomavirus (HPV) genotypes in an Australian sample of anal cancers., Int J Cancer, 135, 996, 10.1002/ijc.28730

De Vuyst, 2009, Prevalence and type distribution of human papillomavirus in carcinoma and intraepithelial neoplasia of the vulva, vagina and anus: a meta-analysis., Int J Cancer, 124, 1626, 10.1002/ijc.24116

Saraiya, 2015, US assessment of HPV types in cancers: implications for current and 9-valent HPV vaccines., J Natl Cancer Inst, 107, djv086, 10.1093/jnci/djv086

Antonsson, 2015, Human papillomavirus status and p16(INK4A) expression in patients with mucosal squamous cell carcinoma of the head and neck in Queensland, Australia., Cancer Epidemiol, 39, 174, 10.1016/j.canep.2015.01.010

Simms, 2017, Optimal management strategies for primary HPV testing for cervical screening: cost-effectiveness evaluation for the National Cervical Screening Program in Australia., PLoS One, 12, e0163509, 10.1371/journal.pone.0163509

Simms, 2016, Will cervical screening remain cost-effective in women offered the next generation nonavalent HPV vaccine? Results for four developed countries., Int J Cancer, 139, 2771, 10.1002/ijc.30392

Simms, 2016, Cost-effectiveness of the next generation nonavalent human papillomavirus vaccine in the context of primary human papillomavirus screening in Australia: a comparative modelling analysis., Lancet Public Health, 1, e66, 10.1016/S2468-2667(16)30019-6

Korostil, 2013, Near elimination of genital warts in Australia predicted with extension of human papillomavirus vaccination to males., Sex Transm Dis, 40, 833, 10.1097/OLQ.0000000000000030

Brotherton, 2016, Primary prevention of HPV through vaccination: update on the current global status., Curr Obstet Gynecol Rep, 5, 210, 10.1007/s13669-016-0165-z

Mesher, 2018, 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, 911, 10.1093/infdis/jiy249

Carozzi, 2016, Effectiveness of HPV vaccination in women reaching screening age in Italy., J Clin Virol, 84, 74, 10.1016/j.jcv.2016.09.011

Feiring, 2018, Substantial decline in prevalence of vaccine-type and non-vaccine type HPV in vaccinated and unvaccinated girls 5 years after implementing HPV vaccine in Norway., J Infect Dis, 10.1093/infdis/jiy432

Jeannot, 2018, Prevalence of vaccine type infections in vaccinated and non-vaccinated young women: HPV-IMPACT, a self-sampling study., Int J Environ Res Public Health, 15, E1447, 10.3390/ijerph15071447

Herweijer, 2018, Substantially reduced incidence of genital warts in women and men six years after HPV vaccine availability in Sweden., Vaccine, 36, 1917, 10.1016/j.vaccine.2018.02.097

Dominiak-Felden, 2015, Evaluating the early benefit of quadrivalent HPV vaccine on genital warts in Belgium: a cohort study., PLoS One, 10, e0132404, 10.1371/journal.pone.0132404

Pollock, 2014, Reduction of low- and high-grade cervical abnormalities associated with high uptake of the HPV bivalent vaccine in Scotland., Br J Cancer, 111, 1824, 10.1038/bjc.2014.479

Joura, 2015, A 9-valent HPV vaccine against infection and intraepithelial neoplasia in women., N Engl J Med, 372, 711, 10.1056/NEJMoa1405044

Moreira, 2016, Safety profile of the 9-valent HPV vaccine: a combined analysis of 7 phase III clinical trials., Pediatrics, 138, e20154387, 10.1542/peds.2015-4387

Cuschieri, 2016, Impact of partial bivalent HPV vaccination on vaccine-type infection: a population-based analysis., Br J Cancer, 114, 1261, 10.1038/bjc.2016.97

Kreimer, 2015, Efficacy of fewer than three doses of an HPV-16/18 AS04-adjuvanted vaccine: combined analysis of data from the Costa Rica Vaccine and PATRICIA Trials., Lancet Oncol, 16, 775, 10.1016/S1470-2045(15)00047-9

Zhai, 2016, Gardasil-9: A global survey of projected efficacy., Antiviral Res, 130, 101, 10.1016/j.antiviral.2016.03.016

2017, Human papillomavirus vaccines: WHO position paper, May 2017., Wkly Epidemiol Rec, 92, 241

Brotherton, 2017, HPV vaccine coverage is increasing in Australia., Med J Aust, 206, 262, 10.5694/mja16.00958

Brotherton, 2013, Human papillomavirus vaccine coverage among female Australian adolescents: success of the school-based approach., Med J Aust, 199, 614, 10.5694/mja13.10272

Marshall, 2007, A cross-sectional survey to assess community attitudes to introduction of Human papillomavirus vaccine., Aust N Z J Public Health, 31, 235, 10.1111/j.1467-842X.2007.00054.x

Marshall, 2013, Parental and societal support for adolescent immunization through school based immunization programs., Vaccine, 31, 3059, 10.1016/j.vaccine.2013.04.064

National Statistics. HPV immunisation statistics Scotland - school year 2015/16. Glasgow: National Services Scotland; 2016. Available from: https://www.isdscotland.org/Health-Topics/Child-Health/Publications/2016-11-08/2016-11-08-HPV-Immunisation-Report.pdf

Brisson, 2016, Population-level impact, herd immunity, and elimination after human papillomavirus vaccination: a systematic review and meta-analysis of predictions from transmission-dynamic models., Lancet Public Health, 1, e8, 10.1016/S2468-2667(16)30001-9

Stevens, 2009, HPV genotype prevalence in women with abnormal pap smears in Melbourne, Australia., J Med Virol, 81, 1283, 10.1002/jmv.21515

Garland, 2008, Human papillomavirus and cervical cancer in Australasia and Oceania: risk-factors, epidemiology and prevention., Vaccine, 26, M80, 10.1016/j.vaccine.2008.05.041

Callegari, 2014, How best to interpret mixed human papillomavirus genotypes in high-grade cervical intraepithelial neoplasia lesions., Vaccine, 32, 4082, 10.1016/j.vaccine.2014.05.041

Antonsson, 2015, Cancers in Australia in 2010 attributable to infectious agents., Aust N Z J Public Health, 39, 446, 10.1111/1753-6405.12445

Australian Institute of Health and Welfare (AIHW). Cancer in Australia: an overview, 2012. Canberra: AIHW; 2012. Available from; https://www.aihw.gov.au/reports/cancer/cancer-in-australia-an-overview-2012/contents/table-of-contents

Australian institute of Health and Welfare (AIHW). Gynaecological cancers in Australia: an overview. Canberra: AIHW; 2012. Available from: https://www.aihw.gov.au/reports/cancer/gynaecological-cancers-in-australia-an-overview/contents/summary