Advertisement

Eliminating Cervical Cancer: Progress and Challenges for High-income Countries

  • J.C. Davies-Oliveira
    Affiliations
    Gynaecological Oncology Research Group, Division of Cancer Sciences, University of Manchester, Faculty of Biology, Medicine and Health, Manchester, UK

    Department of Obstetrics and Gynaecology, St Mary's Hospital, Manchester University NHS Foundation Trust, Manchester Academic Health Science Centre, Manchester, UK
    Search for articles by this author
  • M.A. Smith
    Affiliations
    The Daffodil Centre, The University of Sydney, a joint venture with Cancer Council NSW, Sydney, New South Wales, Australia
    Search for articles by this author
  • S. Grover
    Affiliations
    The Daffodil Centre, The University of Sydney, a joint venture with Cancer Council NSW, Sydney, New South Wales, Australia

    Department of Radiation Oncology, University of Pennsylvania, Philadelphia, Pennsylvania, USA
    Search for articles by this author
  • K. Canfell
    Correspondence
    Author for correspondence: K. Canfell, The Daffodil Centre, 53 Dowling St, Woolloomooloo, NSW 2011, Australia. Tel: +61-2-9334-1726.
    Affiliations
    The Daffodil Centre, The University of Sydney, a joint venture with Cancer Council NSW, Sydney, New South Wales, Australia
    Search for articles by this author
  • E.J. Crosbie
    Affiliations
    Gynaecological Oncology Research Group, Division of Cancer Sciences, University of Manchester, Faculty of Biology, Medicine and Health, Manchester, UK

    Department of Obstetrics and Gynaecology, St Mary's Hospital, Manchester University NHS Foundation Trust, Manchester Academic Health Science Centre, Manchester, UK
    Search for articles by this author

      Abstract

      In 2020, the World Health Organization launched a major initiative to eliminate cervical cancer globally. The initiative is built around the three key pillars of human papillomavirus (HPV) vaccination, cervical screening and treatment, with associated intervention targets for the year 2030. The ‘90-70-90’ targets specify that 90% of adolescent girls receive prophylactic HPV vaccination, 70% of adult women receive a minimum twice-in-a-lifetime cervical HPV test and 90% receive appropriate treatment for preinvasive or invasive disease. Modelling has shown that if these targets are met, the elimination of cervical cancer, defined as fewer than four cases per 100 000 women per annum, will be achieved within a century. Many high-income countries are well positioned to eliminate cervical cancer within the coming decades, but few have achieved ‘90-70-90’ and many challenges must still be addressed to deliver these critical interventions effectively. This review considers the current status of cervical cancer control in relation to each of the three elimination pillars in high-income countries and discusses some of the developments that will assist countries in reaching these ambitious targets by 2030.

      Key words

      To read this article in full you will need to make a payment

      Subscribe:

      Subscribe to Clinical Oncology
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Simms K.T.
        • Steinberg J.
        • Caruana M.
        • Smith M.A.
        • Lew J.B.
        • Soerjomataram I.
        • et al.
        Impact of scaled up human papillomavirus vaccination and cervical screening and the potential for global elimination of cervical cancer in 181 countries, 2020–99: a modelling study.
        Lancet Oncol. 2019; 20: 394-407
        • Brisson M.
        • Kim J.J.
        • Canfell K.
        • Drolet M.
        • Gingras G.
        • Burger E.A.
        • et al.
        Impact of HPV vaccination and cervical screening on cervical cancer elimination: a comparative modelling analysis in 78 low-income and lower-middle-income countries.
        Lancet. 2020; 395: 575-590
        • World Health Organization
        Global strategy to accelerate the elimination of cervical cancer as a public health problem.
        WHO, Geneva2020 (Available at:)
        • Hall M.T.
        • Smith M.A.
        • Simms K.T.
        • Barnabas R.V.
        • Canfell K.
        • Murray J.M.
        The past, present and future impact of HIV prevention and control on HPV and cervical disease in Tanzania: a modelling study.
        PLoS One. 2020; 15e0231388
        • Hall M.T.
        • Simms K.T.
        • Lew J.B.
        • Smith M.A.
        • Brotherton J.M.
        • Saville M.
        • et al.
        The projected timeframe until cervical cancer elimination in Australia: a modelling study.
        Lancet Publ Health. 2019; 4: e19-e27
        • Burger E.A.
        • Smith M.A.
        • Killen J.
        • Sy S.
        • Simms K.T.
        • Canfell K.
        • et al.
        Projected time to elimination of cervical cancer in the USA: a comparative modelling study.
        Lancet Publ Health. 2020; 5: e213-e222https://doi.org/10.1016/S2468-2667(20)30006-2
        • Portnoy A.
        • Pedersen K.
        • Trogstad L.
        • Hansen B.T.
        • Feiring B.
        • Laake I.
        • et al.
        Impact and cost-effectiveness of strategies to accelerate cervical cancer elimination: a model-based analysis.
        Prevent Med. 2021; 144: 106276
        • de Sanjose S.
        • Quint W.G.
        • Alemany L.
        • Geraets D.T.
        • Klaustermeier J.E.
        • Lloveras B.
        • et al.
        Human papillomavirus genotype attribution in invasive cervical cancer: a retrospective cross-sectional worldwide study.
        Lancet Oncol. 2010; 11: 1048-1056
        • Garland S.M.
        • Steben M.
        • Sings H.L.
        • James M.
        • Lu S.
        • Railkar R.
        • 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. 2009; 199: 805-814
        • Naud P.S.
        • Roteli-Martins C.M.
        • De Carvalho N.S.
        • Teixeira J.C.
        • de Borba P.C.
        • Sanchez N.
        • et al.
        Sustained efficacy, immunogenicity, and safety of the HPV-16/18 AS04-adjuvanted vaccine: final analysis of a long-term follow-up study up to 9.4 years post-vaccination.
        Hum Vaccine Immunotherapeut. 2014; 10: 2147-2162
        • Ferris D.
        • Samakoses R.
        • Block S.L.
        • Lazcano-Ponce E.
        • Restrepo J.A.
        • Reisinger K.S.
        • et al.
        Long-term study of a quadrivalent human papillomavirus vaccine.
        Pediatrics. 2014; 134: e657-e665https://doi.org/10.1542/peds.2013-4144
        • Olsson S.E.
        • Villa L.L.
        • Costa R.L.
        • Petta C.A.
        • Andrade R.P.
        • Malm C.
        • et al.
        Induction of immune memory following administration of a prophylactic quadrivalent human papillomavirus (HPV) types 6/11/16/18 L1 virus-like particle (VLP) vaccine.
        Vaccine. 2007; 25: 4931-4939
        • Moscicki A.B.
        • Wheeler C.M.
        • Romanowski B.
        • Hedrick J.
        • Gall S.
        • Ferris D.
        • et al.
        Immune responses elicited by a fourth dose of the HPV-16/18 AS04-adjuvanted vaccine in previously vaccinated adult women.
        Vaccine. 2012; 31: 234-241
        • Kavanagh K.
        • Pollock K.G.
        • Cuschieri K.
        • Palmer T.
        • Cameron R.L.
        • Watt C.
        • 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. 2017; 17: 1293-1302
        • Malagon T.
        • Drolet M.
        • Boily M.C.
        • Franco E.L.
        • Jit M.
        • Brisson J.
        • et al.
        Cross-protective efficacy of two human papillomavirus vaccines: a systematic review and meta-analysis.
        Lancet Infect Dis. 2012; 12: 781-789
        • World Health Organization
        Meeting of the Strategic Advisory Group of Experts on immunization, April 2014 – conclusions and recommendations.
        Weekly Epidemiol Rec. 2014; 89: 221-236
        • GlaxoSmithKline Biologicals
        Package insert and product information - Cervarix 2016.
        (Available at:)
        • Merck & Co
        Package Insert - Gardasil 9 2016.
        (Available at:)
        • Merck & Co
        Package Insert - Gardasil 2015.
        (Available at:)
        • Basu P.
        • Muwonge R.
        • Bhatla N.
        • Nene B.M.
        • Joshi S.
        • Esmy P.O.
        • et al.
        Two-dose recommendation for human papillomavirus vaccine can be extended up to 18 years - updated evidence from Indian follow-up cohort study.
        Papillomavirus Res. 2019; 7: 75-81
        • Markowitz L.E.
        • Drolet M.
        • Perez N.
        • Jit M.
        • Brisson M.
        Human papillomavirus vaccine effectiveness by number of doses: systematic review of data from national immunization programs.
        Vaccine. 2018; 36: 4806-4815
        • Brotherton J.M.
        • Budd A.
        • Rompotis C.
        • Bartlett N.
        • Malloy M.J.
        • Andersen R.L.
        • et al.
        Is one dose of human papillomavirus vaccine as effective as three?: a national cohort analysis.
        Papillomavirus Res. 2019; 8: 100177
        • Sankaranarayanan R.
        • Joshi S.
        • Muwonge R.
        • Esmy P.O.
        • Basu P.
        • Prabhu P.
        • et al.
        Can a single dose of human papillomavirus (HPV) vaccine prevent cervical cancer? Early findings from an Indian study.
        Vaccine. 2018; 36: 4783-4791
        • Brisson M.
        • Benard E.
        • Drolet M.
        • Bogaards J.A.
        • Baussano I.
        • Vanska S.
        • et al.
        Population-level impact, herd immunity, and elimination after human papillomavirus vaccination: a systematic review and meta-analysis of predictions from transmission-dynamic models.
        Lancet Publ Health. 2016; 1: e8-e17
        • Drolet M.
        • É Bénard
        • Pérez N.
        • Brisson M.
        • Ali H.
        • Boily M.-C.
        • et al.
        Population-level impact and herd effects following the introduction of human papillomavirus vaccination programmes: updated systematic review and meta-analysis.
        Lancet. 2019; 394: 497-509https://doi.org/10.1016/S0140-6736(19)30298-3
        • Bruni L.
        • Saura-Lázaro A.
        • Montoliu A.
        • Brotons M.
        • Alemany L.
        • Diallo M.S.
        • et al.
        HPV vaccination introduction worldwide and WHO and UNICEF estimates of national HPV immunization coverage 2010–2019.
        Prev Med. 2021; 144: 106399
        • Castellsague X.
        • Munoz N.
        • Pitisuttithum P.
        • Ferris D.
        • Monsonego J.
        • Ault K.
        • et al.
        End-of-study safety, immunogenicity, and efficacy of quadrivalent HPV (types 6, 11, 16, 18) recombinant vaccine in adult women 24-45 years of age.
        Br J Cancer. 2011; 105: 28-37
        • Wheeler C.M.
        • Skinner S.R.
        • Del Rosario-Raymundo M.R.
        • Garland S.M.
        • Chatterjee A.
        • Lazcano-Ponce E.
        • et al.
        Efficacy, safety, and immunogenicity of the human papillomavirus 16/18 AS04-adjuvanted vaccine in women older than 25 years: 7-year follow-up of the phase 3, double-blind, randomised controlled VIVIANE study.
        Lancet Infect Dis. 2016; 16: 1154-1168
        • Kim J.J.
        • Simms K.T.
        • Killen J.
        • Smith M.A.
        • Burger E.A.
        • Sy S.
        • et al.
        Human papillomavirus vaccination for adults aged 30 to 45 years in the United States: A cost-effectiveness analysis.
        PLoS Med. 2021; 18: e1003534https://doi.org/10.1371/journal.pmed.1003534
        • Laprise J.F.
        • Chesson H.W.
        • Markowitz L.E.
        • Drolet M.
        • Martin D.
        • É Bénard
        • et al.
        Effectiveness and cost-effectiveness of human papillomavirus vaccination through age 45 years in the United States.
        Ann Intern Med. 2020; 172: 22-29
        • World Health Organization
        Meeting of the Strategic Advisory Group of Experts on Immunization, October 2019: conclusions and recommendations.
        Weekly Epidemiol Rec. 2019; 94: 541-560
        • Garland S.M.
        • Stanley M.A.
        • Giuliano A.R.
        • Moscicki A.B.
        • Kaufmann A.
        • Bhatla N.
        • et al.
        IPVS statement on "Temporary HPV vaccine shortage: Implications globally to achieve equity".
        Papillomavirus Res. 2020; 9: 100195
        • Brotherton J.M.
        • Hawkes D.
        • Sultana F.
        • Malloy M.J.
        • Machalek D.A.
        • Smith M.A.
        • et al.
        Age-specific HPV prevalence among 116,052 women in Australia's renewed cervical screening program: a new tool for monitoring vaccine impact.
        Vaccine. 2019; 37: 412-416
        • Maver P.J.
        • Poljak M.
        Primary HPV-based cervical cancer screening in Europe: implementation status, challenges, and future plans.
        Clin Microbiol Infect. 2019; 26: 579-583https://doi.org/10.1016/j.cmi.2019.09.006
        • Lei J.
        • Ploner A.
        • Elfström K.M.
        • Wang J.
        • Roth A.
        • Fang F.
        • et al.
        HPV vaccination and the risk of invasive cervical cancer.
        New Engl J Med. 2020; 383: 1340-1348
        • Yuill S.
        • Egger S.
        • Smith M.
        • Velentzis L.
        • Wrede C.D.
        • Bateson D.
        • et al.
        Has human papillomavirus (HPV) vaccination prevented adverse pregnancy outcomes? Population-level analysis after 8 years of a national HPV vaccination program in Australia.
        J Infect Dis. 2020; 222: 499-508
        • Kalliala I.
        • Eriksson T.
        • Aro K.
        • Hokkanen M.
        • Lehtinen M.
        • Gissler M.
        • et al.
        Preterm birth rate after bivalent HPV vaccination: registry-based follow-up of a randomized clinical trial.
        Prev Med. 2021; 146: 106473
        • Kyrgiou M.
        • Athanasiou A.
        • Kalliala I.E.J.
        • Paraskevaidi M.
        • Mitra A.
        • Martin-Hirsch P.P.L.
        • et al.
        Obstetric outcomes after conservative treatment for cervical intraepithelial lesions and early invasive disease.
        Cochrane Database Syst Rev. 2017; 11: CD012847https://doi.org/10.1002/14651858.CD012847
        • Smith M.A.
        • 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. 2016; 16: 52
        • Smith M.A.
        • 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. 2015; 211: 91-99
        • Montano A.N.
        Sociodemographic differences in human papillomavirus vaccine impact: a systematic review.
        Publ Health Theses. 2016; : 1198
        • Crosbie E.J.
        • Einstein M.H.
        • Franceschi S.
        • Kitchener H.C.
        Human papillomavirus and cervical cancer.
        Lancet. 2013; 382: 889-899
        • Papanicolaou G.N.
        • Traut H.
        The diagnostic value of vaginal smears in carcinoma of the uterus.
        Am J Obstet Gynecol. 1941; 42: 193-206https://doi.org/10.1016/S0002-9378(16)40621-6
        • Shaw P.
        The history of cervical screening I: the Pap. test.
        J Soc Obstet Gynecol Can. 2000; 22: 110-114
        • Löwy I.
        Cancer, women, and public health: the history of screening for cervical cancer.
        Historia, Ciencias, Saude-Manguinhos. 2010; 17: 53-67
        • Lynch-Farmery E.
        Cervical cancer screening in the United Kingdom, 1986 to 1996: a decade of change.
        J Obstet Gynecol Can. 1996; 18: 1251-1259
        • Karnon J.
        • Peters J.
        • Platt J.
        • Chilcott J.
        • McGoogan E.
        • Brewer N.
        Liquid-based cytology in cervical screening: an updated rapid and systematic review and economic analysis.
        Health Technol Assess. 2004; 8 (iii): 1-78
        • Rebolj M.
        • Rimmer J.
        • Denton K.
        • Tidy J.
        • Mathews C.
        • Ellis K.
        • et al.
        Primary cervical screening with high risk human papillomavirus testing: observational study.
        BMJ. 2019; 364: l240
        • Koliopoulos G.
        • Nyaga V.N.
        • Santesso N.
        • Bryant A.
        • Martin-Hirsch P.P.
        • Mustafa R.A.
        • et al.
        Cytology versus HPV testing for cervical cancer screening in the general population.
        Cochrane Database Syst Rev. 2017; 8: CD008587
        • Ronco G.
        • Dillner J.
        • Elfström K.M.
        • Tunesi S.
        • Snijders P.J.
        • Arbyn M.
        • et al.
        Efficacy of HPV-based screening for prevention of invasive cervical cancer: follow-up of four European randomised controlled trials.
        Lancet. 2014; 383: 524-532
        • Cuzick J.
        • Clavel C.
        • Petry K.U.
        • Meijer C.J.
        • Hoyer H.
        • Ratnam S.
        • et al.
        Overview of the European and North American studies on HPV testing in primary cervical cancer screening.
        Int J Cancer. 2006; 119: 1095-1101
        • Landy R.
        • Pesola F.
        • Castañón A.
        • Sasieni P.
        Impact of cervical screening on cervical cancer mortality: estimation using stage-specific results from a nested case-control study.
        Br J Cancer. 2016; 115: 1140-1146
        • Smith M.
        • Canfell K.
        Impact of the Australian National Cervical Screening Program in women of different ages.
        Med J Aust. 2016; 205: 359-364
        • Fontham E.T.H.
        • Wolf A.M.D.
        • Church T.R.
        • Etzioni R.
        • Flowers C.R.
        • Herzig A.
        • et al.
        Cervical cancer screening for individuals at average risk: 2020 guideline update from the American Cancer Society.
        CA Cancer J Clin. 2020; 70: 321-346
        • Pesola F.
        • Sasieni P.
        Impact of screening on cervical cancer incidence in England: a time trend analysis.
        BMJ Open. 2019; 9e026292
        • Landy R.
        • Birke H.
        • Castanon A.
        • Sasieni P.
        Benefits and harms of cervical screening from age 20 years compared with screening from age 25 years.
        Br J Cancer. 2014; 110: 1841-1846
        • Sasieni P.
        • Castanon A.
        • Cuzick J.
        Effectiveness of cervical screening with age: population based case-control study of prospectively recorded data.
        BMJ. 2009; 339: b2968
        • Hammer A.
        • Kahlert J.
        • Rositch A.
        • Pedersen L.
        • Gravitt P.
        • Blaakaer J.
        • et al.
        The temporal and age-dependent patterns of hysterectomy-corrected cervical cancer incidence rates in Denmark: a population-based cohort study.
        Acta Obstet Gynecol Scand. 2017; 96: 150-157
        • Tranberg M.
        • Petersen L.K.
        • Elfström K.M.
        • Hammer A.
        • Blaakær J.
        • Bennetsen M.H.
        • et al.
        Expanding the upper age limit for cervical cancer screening: a protocol for a nationwide non-randomised intervention study.
        BMJ Open. 2020; 10e039636
        • Gilham C.
        • Crosbie E.J.
        • Peto J.
        Cervical cancer screening in older women.
        BMJ. 2021; 372: n280
        • Lew J.B.
        • Simms K.T.
        • Smith M.A.
        • Hall M.
        • Kang Y.J.
        • Xu X.M.
        • et al.
        Primary HPV testing versus cytology-based cervical screening in women in Australia vaccinated for HPV and unvaccinated: effectiveness and economic assessment for the National Cervical Screening Program.
        Lancet Publ Health. 2017; 2: e96-e107
        • Kim J.J.
        • Burger E.A.
        • Sy S.
        • Campos N.G.
        Optimal cervical cancer screening in women vaccinated against human papillomavirus.
        J Natl Cancer Inst. 2017; 109: djw216https://doi.org/10.1093/jnci/djw216
        • Landy R.
        • Windridge P.
        • Gillman M.S.
        • Sasieni P.D.
        What cervical screening is appropriate for women who have been vaccinated against high risk HPV? A simulation study.
        Int J Cancer. 2018; 142: 709-718
        • Simms K.T.
        • Smith M.A.
        • Lew J.B.
        • Kitchener H.C.
        • Castle P.E.
        • Canfell K.
        Will cervical screening remain cost-effective in women offered the next generation nonavalent HPV vaccine? Results for four developed countries.
        Int J Cancer. 2016; 139: 2771-2780
        • Obermair H.M.
        • Dodd R.H.
        • Bonner C.
        • Jansen J.
        • McCaffery K.
        'It has saved thousands of lives, so why change it?' Content analysis of objections to cervical screening programme changes in Australia.
        BMJ Open. 2018; 8e019171
        • Hill E.
        • Nemec M.
        • Marlow L.
        • Sherman S.M.
        • Waller J.
        Maximising the acceptability of extended time intervals between screens in the NHS Cervical Screening Programme: an online experimental study.
        J Med Screen. 2020; (969141320970591)
        • Sasieni P.
        • Castanon A.
        Research and analysis - audit report - cervical screening: invasive cervical cancer audit 2013–2016.
        Gov.UK: Public Health England, 2019
        • Wilding S.
        • Wighton S.
        • Halligan D.
        • West R.
        • Conner M.
        • O'Connor D.B.
        What factors are most influential in increasing cervical cancer screening attendance? An online study of UK-based women.
        Health Psychol Behav Med. 2020; 8: 314-328
        • Marlow L.
        • McBride E.
        • Varnes L.
        • Waller J.
        Barriers to cervical screening among older women from hard-to-reach groups: a qualitative study in England.
        BMC Womens Health. 2019; 19: 38
        • Rees I.
        • Jones D.
        • Chen H.
        • Macleod U.
        Interventions to improve the uptake of cervical cancer screening among lower socioeconomic groups: a systematic review.
        Prev Med. 2018; 111: 323-335
        • Bennett K.F.
        • Waller J.
        • Chorley A.J.
        • Ferrer R.A.
        • Haddrell J.B.
        • Marlow L.A.
        Barriers to cervical screening and interest in self-sampling among women who actively decline screening.
        J Med Screen. 2018; 25: 211-217
        • Castanon A.
        • Rebolj M.
        • Pesola F.
        • Sasieni P.
        Recovery strategies following COVID-19 disruption to cervical cancer screening and their impact on excess diagnoses.
        Br J Cancer. 2021; 124: 1361-1365https://doi.org/10.1038/s41416-021-01275-3
        • Smith M.A.
        • Burger E.A.
        • Castanon A.
        • de Kok I.
        • Hanley S.
        • Rebolj M.
        • et al.
        Impact of disruptions and recovery for established cervical screening programs across a range of high-income country program designs, using COVID-19 as an example: a modelled analysis.
        Prev Med. 2021; 159: 106623https://doi.org/10.1016/j.ypmed.2021.106623
        • Sargent A.
        • Fletcher S.
        • Bray K.
        • Kitchener H.C.
        • Crosbie E.J.
        Cross-sectional study of HPV testing in self-sampled urine and comparison with matched vaginal and cervical samples in women attending colposcopy for the management of abnormal cervical screening.
        BMJ Open. 2019; 9e025388
        • Arbyn M.
        • Peeters E.
        • Benoy I.
        • Vanden Broeck D.
        • Bogers J.
        • De Sutter P.
        • et al.
        VALHUDES: A protocol for validation of human papillomavirus assays and collection devices for HPV testing on self-samples and urine samples.
        J Clin Virol. 2018; 107: 52-56
        • Pathak N.
        • Dodds J.
        • Zamora J.
        • Khan K.
        Accuracy of urinary human papillomavirus testing for presence of cervical HPV: systematic review and meta-analysis.
        BMJ. 2014; 349: g5264
        • Yeh P.T.
        • Kennedy C.E.
        • de Vuyst H.
        • Narasimhan M.
        Self-sampling for human papillomavirus (HPV) testing: a systematic review and meta-analysis.
        BMJ Glob Health. 2019; 4e001351
        • Ernstson A.
        • Urdell A.
        • Forslund O.
        • Borgfeldt C.
        Cervical cancer prevention among long-term screening non-attendees by vaginal self-collected samples for hr-HPV mRNA detection.
        Infect Agent Cancer. 2020; 15: 10
        • Kellen E.
        • Benoy I.
        • Vanden Broeck D.
        • Martens P.
        • Bogers J.P.
        • Haelens A.
        • et al.
        A randomized, controlled trial of two strategies of offering the home-based HPV self-sampling test to non-participants in the Flemish cervical cancer screening program.
        Int J Cancer. 2018; 143: 861-868
        • Kitchener H.
        • Gittins M.
        • Cruickshank M.
        • Moseley C.
        • Fletcher S.
        • Albrow R.
        • et al.
        A cluster randomized trial of strategies to increase uptake amongst young women invited for their first cervical screen: the STRATEGIC trial.
        J Med Screen. 2018; 25: 88-98
        • Lilliecreutz C.
        • Karlsson H.
        • Spetz Holm A.C.
        Participation in interventions and recommended follow-up for non-attendees in cervical cancer screening – taking the women's own preferred test method into account – a Swedish randomised controlled trial.
        PLoS One. 2020; 15e0235202
        • Leeman A.
        • Del Pino M.
        • Molijn A.
        • Rodriguez A.
        • Torné A.
        • de Koning M.
        • et al.
        HPV testing in first-void urine provides sensitivity for CIN2+ detection comparable with a smear taken by a clinician or a brush-based self-sample: cross-sectional data from a triage population.
        Br J Obstet Gynaecol. 2017; 124: 1356-1363
        • Pattyn J.
        • Van Keer S.
        • Téblick L.
        • Van Damme P.
        • Vorsters A.
        HPV DNA detection in urine samples of women: 'an efficacious and accurate alternative to cervical samples?.
        Expert Rev Anti Infect Ther. 2019; 17: 755-757
        • Bonde J.H.
        • Sandri M.T.
        • Gary D.S.
        • Andrews J.C.
        Clinical utility of human papillomavirus genotyping in cervical cancer screening: a systematic review.
        J Low Genit Tract Dis. 2020; 24: 1-13
        • Wentzensen N.
        • Clarke M.A.
        • Bremer R.
        • Poitras N.
        • Tokugawa D.
        • Goldhoff P.E.
        • et al.
        Clinical evaluation of human papillomavirus screening with p16/Ki-67 dual stain triage in a large organized cervical cancer screening program.
        JAMA Intern Med. 2019; 179: 881-888
        • Tjalma W.A.A.
        Diagnostic performance of dual-staining cytology for cervical cancer screening: a systematic literature review.
        Eur J Obstet Gynecol Reprod Biol. 2017; 210: 275-280
        • Wentzensen N.
        • Lahrmann B.
        • Clarke M.A.
        • Kinney W.
        • Tokugawa D.
        • Poitras N.
        • et al.
        Accuracy and efficiency of deep-learning-based automation of dual stain cytology in cervical cancer screening.
        J Natl Cancer Inst. 2021; 113: 72-79
        • Snoek B.C.
        • Splunter A.P.V.
        • Bleeker M.C.G.
        • Ruiten M.C.V.
        • Heideman D.A.M.
        • Rurup W.F.
        • et al.
        Cervical cancer detection by DNA methylation analysis in urine.
        Sci Rep. 2019; 9: 3088
        • Cook D.A.
        • Krajden M.
        • Brentnall A.R.
        • Gondara L.
        • Chan T.
        • Law J.H.
        • et al.
        Evaluation of a validated methylation triage signature for human papillomavirus positive women in the HPV FOCAL cervical cancer screening trial.
        Int J Cancer. 2019; 144: 2587-2595
        • Ramírez A.T.
        • Sánchez G.I.
        • Nedjai B.
        • Agudelo M.C.
        • Brentnall A.R.
        • Cuschieri K.
        • et al.
        Effective methylation triage of HPV positive women with abnormal cytology in a middle-income country.
        Int J Cancer. 2021; 148: 1383-1393
        • McCredie M.R.
        • Sharples K.J.
        • Paul C.
        • Baranyai J.
        • Medley G.
        • Jones R.W.
        • et al.
        Natural history of cervical neoplasia and risk of invasive cancer in women with cervical intraepithelial neoplasia 3: a retrospective cohort study.
        Lancet Oncol. 2008; 9: 425-434
        • Lili E.
        • Chatzistamatiou K.
        • Kalpaktsidou-Vakiani A.
        • Moysiadis T.
        • Agorastos T.
        Low recurrence rate of high-grade cervical intraepithelial neoplasia after successful excision and routine colposcopy during follow-up.
        Medicine. 2018; 97e9719
        • Kyrgiou M.
        • Athanasiou A.
        • Paraskevaidi M.
        • Mitra A.
        • Kalliala I.
        • Martin-Hirsch P.
        • et al.
        Adverse obstetric outcomes after local treatment for cervical preinvasive and early invasive disease according to cone depth: systematic review and meta-analysis.
        BMJ. 2016; 354: i3633
        • Sauvaget C.
        • Muwonge R.
        • Sankaranarayanan R.
        Meta-analysis of the effectiveness of cryotherapy in the treatment of cervical intraepithelial neoplasia.
        Int J Gynaecol Obstet. 2013; 120: 218-223
        • Dolman L.
        • Sauvaget C.
        • Muwonge R.
        • Sankaranarayanan R.
        Meta-analysis of the efficacy of cold coagulation as a treatment method for cervical intraepithelial neoplasia: a systematic review.
        Br J Obstet Gynaecol. 2014; 121: 929-942
        • van de Sande A.J.M.
        • Koeneman M.M.
        • Gerestein C.G.
        • Kruse A.J.
        • van Kemenade F.J.
        • van Beekhuizen H.J.
        TOPical Imiquimod treatment of residual or recurrent cervical intraepithelial neoplasia (TOPIC-2 trial): a study protocol for a randomized controlled trial.
        BMC Cancer. 2018; 18: 655
        • Major A.L.
        • Dvořák V.
        • Schwarzová J.
        • Skřivánek A.
        • Malík T.
        • Pluta M.
        • et al.
        Efficacy and safety of an adsorbent and anti-oxidative vaginal gel on CIN1 and 2, on high-risk HPV, and on p16/Ki-67: a randomized controlled trial.
        Arch Gynecol Obstet. 2021; 303: 501-511
        • Zhao S.
        • Hu S.
        • Xu X.
        • Zhang X.
        • Pan Q.
        • Chen F.
        • et al.
        Impact of HPV-16/18 AS04-adjuvanted vaccine on preventing subsequent infection and disease after excision treatment: post-hoc analysis from a randomized controlled trial.
        BMC Infect Dis. 2020; 20: 846
        • Bhatla N.
        • Berek J.S.
        • Cuello Fredes M.
        • Denny L.A.
        • Grenman S.
        • Karunaratne K.
        • et al.
        Revised FIGO staging for carcinoma of the cervix uteri.
        Int J Gynaecol Obstet. 2019; 145: 129-135
        • Maduro J.H.
        • Pras E.
        • Willemse P.H.
        • de Vries E.G.
        Acute and long-term toxicity following radiotherapy alone or in combination with chemotherapy for locally advanced cervical cancer.
        Cancer Treat Rev. 2003; 29: 471-488
        • Liu B.
        • Gao S.
        • Li S.
        A comprehensive comparison of CT, MRI, positron emission tomography or positron emission tomography/CT, and diffusion weighted imaging-MRI for detecting the lymph nodes metastases in patients with cervical cancer: a meta-analysis based on 67 studies.
        Gynecol Obstet Invest. 2017; 82: 209-222
        • James R.M.
        • Cruickshank M.E.
        • Siddiqui N.
        • Group G.D.
        Management of cervical cancer: summary of SIGN guidelines.
        BMJ. 2008; 336: 41-43
        • Balaya V.
        • Mathevet P.
        • Magaud L.
        • Delomenie M.
        • Bonsang-Kitzis H.
        • Ngô C.
        • et al.
        Predictive factors of severe perioperative morbidity of radical hysterectomy with lymphadenectomy in early-stage cervical cancer: a French prospective multicentric cohort of 248 patients.
        Eur J Surg Oncol. 2019; 45: 650-658
        • Favre G.
        • Guani B.
        • Balaya V.
        • Magaud L.
        • Lecuru F.
        • Mathevet P.
        Sentinel lymph-node biopsy in early-stage cervical cancer: the 4-year follow-up results of the Senticol 2 trial.
        Front Oncol. 2020; 10: 621518
        • Reed N.
        • Balega J.
        • Barwick T.
        • Buckley L.
        • Burton K.
        • Eminowicz G.
        • et al.
        British Gynaecological Cancer Society (BGCS) cervical cancer guidelines: recommendations for practice.
        Eur J Obstet Gynecol Reprod Biol. 2021; 256: 433-465
        • Ramirez P.T.
        • Pareja R.
        • Rendón G.J.
        • Millan C.
        • Frumovitz M.
        • Schmeler K.M.
        Management of low-risk early-stage cervical cancer: should conization, simple trachelectomy, or simple hysterectomy replace radical surgery as the new standard of care?.
        Gynecol Oncol. 2014; 132: 254-259
        • Ramirez P.T.
        • Pareja R.
        • Eriksson A.G.Z.
        • Frumovitz M.
        International Gynecologic Cancer Society 2019 meeting summary.
        Int J Gynecol Cancer. 2020; 30: 167-173
        • Theofanakis C.
        • Haidopoulos D.
        • Thomakos N.
        • Rodolakis A.
        • Fotopoulou C.
        Minimizing fertility-sparing treatment for low volume early stage cervical cancer; is less the (r)evolution?.
        Anticancer Res. 2020; 40: 3651-3658
        • Ramirez P.T.
        • Frumovitz M.
        • Pareja R.
        • Lopez A.
        • Vieira M.
        • Ribeiro R.
        • et al.
        Minimally invasive versus abdominal radical hysterectomy for cervical cancer.
        N Engl J Med. 2018; 379: 1895-1904
        • Falconer H.
        • Palsdottir K.
        • Stalberg K.
        • Dahm-Kähler P.
        • Ottander U.
        • Lundin E.S.
        • et al.
        Robot-assisted approach to cervical cancer (RACC): an international multi-center, open-label randomized controlled trial.
        Int J Gynecol Cancer. 2019; 29: 1072-1076
        • Gupta S.
        Adjuvant chemotherapy in locally advanced cervical cancer: the ceiling remains unbroken.
        J Gynecol Oncol. 2019; 30: e97
        • Chemoradiotherapy for Cervical Cancer Meta-Analysis Collaboration
        Reducing uncertainties about the effects of chemoradiotherapy for cervical cancer: a systematic review and meta-analysis of individual patient data from 18 randomized trials.
        J Clin Oncol. 2008; 26: 5802-5812
        • Hong J.C.
        • Foote J.
        • Broadwater G.
        • Sosa J.A.
        • Gaillard S.
        • Havrilesky L.J.
        • et al.
        Data-derived treatment duration goal for cervical cancer: should 8 weeks remain the target in the era of concurrent chemoradiation?.
        JCO Clin Cancer Inform. 2017; 1: 1-15
        • Han K.
        • Milosevic M.
        • Fyles A.
        • Pintilie M.
        • Viswanathan A.N.
        Trends in the utilization of brachytherapy in cervical cancer in the United States.
        Int J Radiat Oncol Biol Phys. 2013; 87: 111-119
        • Gupta S.
        • Maheshwari A.
        • Parab P.
        • Mahantshetty U.
        • Hawaldar R.
        • Sastri Chopra S.
        • et al.
        Neoadjuvant chemotherapy followed by radical surgery versus concomitant chemotherapy and radiotherapy in patients with stage IB2, IIA, or IIB squamous cervical cancer: a randomized controlled trial.
        J Clin Oncol. 2018; 36: 1548-1555
        • Kenter G.
        • Greggi S.
        • Vergote I.
        • Katsaros D.
        • Kobierski J.
        • Massuger L.
        • et al.
        Results from neoadjuvant chemotherapy followed by surgery compared to chemoradiation for stage Ib2-IIb cervical cancer, EORTC 55994.
        J Clin Oncol. 2019; 37
        • Tangjitgamol S.
        • Tharavichitkul E.
        • Tovanabutra C.
        • Rongsriyam K.
        • Asakij T.
        • Paengchit K.
        • et al.
        A randomized controlled trial comparing concurrent chemoradiation versus concurrent chemoradiation followed by adjuvant chemotherapy in locally advanced cervical cancer patients: ACTLACC trial.
        J Gynecol Oncol. 2019; 30: e82
      1. Mileshkin L. Moore K.N. Barnes E. Gebski V. Narayan K. Bradshaw N. Adjuvant chemotherapy following chemoradiation as primary treatment for locally advanced cervical cancer compared to chemoradiation alone: the randomized phase III OUTBACK Trial (ANZGOG 0902, RTOG 1174, NRG 0274). 2021 ASCO Annual Meeting. 2021 (Available at:)
        • Tewari K.S.
        • Sill M.W.
        • Penson R.T.
        • Huang H.
        • Ramondetta L.M.
        • Landrum L.M.
        • et al.
        Bevacizumab for advanced cervical cancer: final overall survival and adverse event analysis of a randomised, controlled, open-label, phase 3 trial (Gynecologic Oncology Group 240).
        Lancet. 2017; 390: 1654-1663
        • Orbegoso C.
        • Murali K.
        • Banerjee S.
        The current status of immunotherapy for cervical cancer.
        Rep Pract Oncol Radiother. 2018; 23: 580-588
        • Maringe C.
        • Spicer J.
        • Morris M.
        • Purushotham A.
        • Nolte E.
        • Sullivan R.
        • et al.
        The impact of the COVID-19 pandemic on cancer deaths due to delays in diagnosis in England, UK: a national, population-based, modelling study.
        Lancet Oncol. 2020; 21: 1023-1034
        • Hanna T.P.
        • King W.D.
        • Thibodeau S.
        • Jalink M.
        • Paulin G.A.
        • Harvey-Jones E.
        • et al.
        Mortality due to cancer treatment delay: systematic review and meta-analysis.
        BMJ. 2020; 371: m4087
        • Martei Y.M.
        • Rick T.J.
        • Fadelu T.
        • Ezzi M.S.
        • Hammad N.
        • Quadri N.S.
        • et al.
        Impact of COVID-19 on cancer care delivery in Africa: a cross-sectional survey of oncology providers in Africa.
        JCO Glob Oncol. 2021; 7: 368-377
        • Nnaji C.A.
        • Moodley J.
        Impact of the COVID-19 pandemic on cancer diagnosis, treatment and research in African health systems: a review of current evidence and contextual perspectives.
        Ecancermedicalscience. 2021; 15: 1170
        • Burger E.A.
        • Jansen E.E.
        • Killen J.
        • Kok I.M.
        • Smith M.A.
        • Sy S.
        • et al.
        Impact of COVID-19-related care disruptions on cervical cancer screening in the United States.
        J Med Screen. 2021; (9691413211001097)
        • Castanon Alejandra
        • Rebolj Matejka
        • Burger Emily
        • de Kok Inge
        • Smith Megan
        • Hanley Sharon
        • et al.
        Cervical screening during the COVID-19 pandemic: optimising recovery strategie.
        Lancet Public Health. 2021; 6: e522-e527https://doi.org/10.1016/S2468-2667(21)00078-5
        • Pötter R.
        • Georg P.
        • Dimopoulos J.C.
        • Grimm M.
        • Berger D.
        • Nesvacil N.
        • et al.
        Clinical outcome of protocol based image (MRI) guided adaptive brachytherapy combined with 3D conformal radiotherapy with or without chemotherapy in patients with locally advanced cervical cancer.
        Radiother Oncol. 2011; 100: 116-123https://doi.org/10.1016/j.radonc.2011.07.012