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Prevention of Cervical Cancer in Low-Resource African Settings

  • Masangu Mulongo
    Affiliations
    Clinical HIV Research Unit, Wits Health Consortium, Themba Lethu Clinic, Helen Joseph Hospital, Perth Road, Auckland Park, Johannesburg 2092, South Africa
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  • Carla J. Chibwesha
    Correspondence
    Corresponding author. Division of Global Women’s Health, Department of Obstetrics and Gynecology, University of North Carolina at Chapel Hill, 3009 Old Clinic Building, Campus Box 7577, Chapel Hill, NC 27599-7577.
    Affiliations
    Clinical HIV Research Unit, Wits Health Consortium, Themba Lethu Clinic, Helen Joseph Hospital, Perth Road, Auckland Park, Johannesburg 2092, South Africa

    Division of Global Women’s Health, Department of Obstetrics and Gynecology, University of North Carolina at Chapel Hill, 3009 Old Clinic Building, Campus Box 7577, Chapel Hill, NC, USA
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      References

        • Sung H.
        • Ferlay J.
        • Siegel R.L.
        • et al.
        Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries.
        CA Cancer J Clin. 2021; 71: 209-249
        • Bray F.
        • Ren J.S.
        • Masuyer E.
        • et al.
        Global estimates of cancer prevalence for 27 sites in the adult population in 2008.
        Int J Cancer. 2013; 132: 1133-1145
        • International Agency for Research on Cancer
        GLOBOCAN: Cancer Today.
        (Available at:) (Accessed August 12, 2022)
        • International Agency for Research on Cancer
        GLOBOCAN: Cancer Tomorrow.
        (Available at:) (Accessed August 12, 2022)
        • Denny L.
        Control of cancer of the cervix in low- and middle-income countries.
        Ann Surg Oncol. 2015; 22: 728-733
        • Sankaranarayanan R.
        Screening for cancer in low- and middle-income countries.
        Ann Glob Health. 2014; 80: 412-417
        • Oberlin A.M.
        • Rahangdale L.
        • Chinula L.
        • et al.
        Making HPV vaccination available to girls everywhere.
        Int J Gynaecol Obstet. 2018; 143: 267-276
        • Gakidou E.
        • Nordhagen S.
        • Obermeyer Z.
        Coverage of cervical cancer screening in 57 countries: low average levels and large inequalities.
        Plos Med. 2008; 5: e132
        • International Agency for Research on Cancer
        Cervical cancer elimination in Africa: where are we now and where do we need to be?.
        (Available at:) (Accessed August 12, 2022)
        • Stelzle D.
        • Tanaka L.F.
        • Lee K.K.
        • et al.
        Estimates of the global burden of cervical cancer associated with HIV.
        Lancet Glob Health. 2021; 9: e161-e169
        • Francis S.A.
        • Nelson J.
        • Liverpool J.
        • et al.
        Examining attitudes and knowledge about HPV and cervical cancer risk among female clinic attendees in Johannesburg, South Africa.
        Vaccine. 2010; 28: 8026-8032
        • Chirwa S.
        • Mwanahamuntu M.
        • Kapambwe S.
        • et al.
        Myths and misconceptions about cervical cancer among Zambian women: rapid assessment by peer educators.
        Glob Health Promot. 2010; 17: 47-50
        • Adewumi K.
        • Nishimura H.
        • Oketch S.Y.
        • et al.
        Barriers and Facilitators to Cervical Cancer Screening in Western Kenya: a Qualitative Study.
        J Cancer Educ. 2021; https://doi.org/10.1007/s13187-020-01928-6
        • World Health Organization
        Global strategy to accelerate the elimination of cervical cancer as a public health problem.
        (Available at:) (Accessed August 12, 2022)
        • Bosch F.X.
        • Manos M.M.
        • Munoz N.
        • et al.
        Prevalence of human papillomavirus in cervical cancer: a worldwide perspective. International biological study on cervical cancer (IBSCC) Study Group.
        J Natl Cancer Inst. 1995; 87: 796-802
        • Walboomers J.M.
        • Jacobs M.V.
        • Manos M.M.
        • et al.
        Human papillomavirus is a necessary cause of invasive cervical cancer worldwide.
        J Pathol. 1999; 189: 12-19
        • Crosbie E.J.
        • Einstein M.H.
        • Franceschi S.
        • et al.
        Human papillomavirus and cervical cancer.
        Lancet. 2013; 382: 889-899
        • World Health Organization
        Human papillomavirus vaccines: WHO position paper, May 2017-Recommendations.
        Vaccine. 2017; 35: 5753-5755
        • Castellsague X.
        Natural history and epidemiology of HPV infection and cervical cancer.
        Gynecol Oncol. 2008; 110: S4-S7
        • Denny L.A.
        • Franceschi S.
        • de Sanjose S.
        • et al.
        Human papillomavirus, human immunodeficiency virus and immunosuppression.
        Vaccine. 2012; 30: F168-F174
        • Clifford G.M.
        • Goncalves M.A.
        • Franceschi S.
        • et al.
        Human papillomavirus types among women infected with HIV: a meta-analysis.
        AIDS. 2006; 20: 2337-2344
        • Denny L.
        • Boa R.
        • Williamson A.L.
        • et al.
        Human papillomavirus infection and cervical disease in human immunodeficiency virus-1-infected women.
        Obstet Gynecol. 2008; 111: 1380-1387
        • Singh D.K.
        • Anastos K.
        • Hoover D.R.
        • et al.
        Human papillomavirus infection and cervical cytology in HIV-infected and HIV-uninfected Rwandan women.
        J Infect Dis. 2009; 199: 1851-1861
        • Chirenje Z.M.
        HIV and cancer of the cervix.
        Best Pract Res Clin Obstet Gynaecol. 2005; 19: 269-276
        • Einstein M.H.
        • Phaeton R.
        Issues in cervical cancer incidence and treatment in HIV.
        Curr Opin Oncol. 2010; 22: 449-455
        • Castle P.E.
        • Einstein M.H.
        • Sahasrabuddhe V.V.
        Cervical cancer prevention and control in women living with human immunodeficiency virus.
        CA Cancer J Clin. 2021; 71: 505-526
        • Franceschi S.
        • Jaffe H.
        Cervical cancer screening of women living with HIV infection: a must in the era of antiretroviral therapy.
        Clin Infect Dis. 2007; 45: 510-513
        • UNAIDS. Global
        HIV Statistics 2022.
        (Available at:) (Accessed August 12, 2022)
        • Brower V.
        AIDS-related cancers increase in Africa.
        J Natl Cancer Inst. 2011; 103: 918-919
        • Casper C.
        The increasing burden of HIV-associated malignancies in resource-limited regions.
        Annu Rev Med. 2011; 62: 157-170
        • Ault K.A.
        • Future I.I.S.G.
        Effect of prophylactic human papillomavirus L1 virus-like-particle vaccine on risk of cervical intraepithelial neoplasia grade 2, grade 3, and adenocarcinoma in situ: a combined analysis of four randomised clinical trials.
        Lancet. 2007; 369: 1861-1868
        • Lehtinen M.
        • Paavonen J.
        • Wheeler C.M.
        • et al.
        Overall efficacy of HPV-16/18 AS04-adjuvanted vaccine against grade 3 or greater cervical intraepithelial neoplasia: 4-year end-of-study analysis of the randomised, double-blind PATRICIA trial.
        Lancet Oncol. 2012; 13: 89-99
        • Joura E.A.
        • Giuliano A.R.
        • Iversen O.E.
        • et al.
        A 9-valent HPV vaccine against infection and intraepithelial neoplasia in women.
        N Engl J Med. 2015; 372: 711-723
        • World Health Organization
        One-dose Human Papillomavirus (HPV) vaccine offers solid protection against cervical cancer.
        (Available at:) (Accessed August 12, 2022)
        • Jit M.
        • Brisson M.
        Potential lives saved in 73 countries by adopting multi-cohort vaccination of 9-14-year-old girls against human papillomavirus.
        Int J Cancer. 2018; 143: 317-323
        • Jit M.
        • Brisson M.
        • Portnoy A.
        • et al.
        Cost-effectiveness of female human papillomavirus vaccination in 179 countries: a PRIME modelling study.
        Lancet Glob Health. 2014; 2: e406-e414
        • Gelband H.
        • Sankaranarayanan R.
        • Gauvreau C.L.
        • et al.
        Costs, affordability, and feasibility of an essential package of cancer control interventions in low-income and middle-income countries: key messages from Disease Control Priorities, 3rd edition.
        Lancet. 2016; 387: 2133-2144
        • Wilailak S.
        • Kengsakul M.
        • Kehoe S.
        Worldwide initiatives to eliminate cervical cancer.
        Int J Gynaecol Obstet. 2021; 155: 102-106
        • Sawaya G.F.
        • Huchko M.J.
        Cervical Cancer Screening.
        Med Clin North Am. 2017; 101: 743-753
        • Saslow D.
        • Solomon D.
        • Lawson H.W.
        • et al.
        American Cancer Society, American Society for Colposcopy and Cervical Pathology, and American Society for Clinical Pathology screening guidelines for the prevention and early detection of cervical cancer.
        J Low Genit Tract Dis. 2012; 16: 175-204
        • Heard I.
        Prevention of cervical cancer in women with HIV.
        Curr Opin HIV AIDS. 2009; 4: 68-73
        • Maranga I.O.
        • Hampson L.
        • Oliver A.W.
        • et al.
        Analysis of factors contributing to the low survival of cervical cancer patients undergoing radiotherapy in Kenya.
        PLoS One. 2013; 8: e78411
        • Alfaro K.
        • Maza M.
        • Cremer M.
        • et al.
        Removing global barriers to cervical cancer prevention and moving towards elimination.
        Nat Rev Cancer. 2021; 21: 607-608
        • Sankaranarayanan R.
        • Anorlu R.
        • Sangwa-Lugoma G.
        • et al.
        Infrastructure requirements for human papillomavirus vaccination and cervical cancer screening in sub-Saharan Africa.
        Vaccine. 2013; 31: F47-F52
        • Parham G.P.
        • Sahasrabuddhe V.V.
        • Westfall A.O.
        • et al.
        Implementation of cervical cancer prevention services for HIV-infected women in Zambia: measuring program effectiveness.
        HIV Ther. 2010; 4: 713-722
        • Parham G.P.
        • Mwanahamuntu M.H.
        • Kapambwe S.
        • et al.
        Population-level scale-up of cervical cancer prevention services in a low-resource setting: development, implementation, and evaluation of the cervical cancer prevention program in Zambia.
        PLoS One. 2015; 10: e0122169
        • World Health Organization
        A practical manual on visual screening for cervical neoplasia.
        (Available at:) (Accessed August 12, 2022)
        • Sankaranarayanan R.
        • Basu P.
        • Wesley R.S.
        • et al.
        Accuracy of visual screening for cervical neoplasia: Results from an IARC multicentre study in India and Africa.
        Int J Cancer. 2004; 110: 907-913
        • Arbyn M.
        • Sankaranarayanan R.
        • Muwonge R.
        • et al.
        Pooled analysis of the accuracy of five cervical cancer screening tests assessed in eleven studies in Africa and India.
        Int J Cancer. 2008; 123: 153-160
        • Allanson E.R.
        • Phoolcharoen N.
        • Salcedo M.P.
        • et al.
        Accuracy of Smartphone Images of the Cervix After Acetic Acid Application for Diagnosing Cervical Intraepithelial Neoplasia Grade 2 or Greater in Women With Positive Cervical Screening: A Systematic Review and Meta-Analysis.
        JCO Glob Oncol. 2021; 7: 1711-1721
        • Sankaranarayanan R.
        • Nene B.M.
        • Dinshaw K.A.
        • et al.
        A cluster randomized controlled trial of visual, cytology and human papillomavirus screening for cancer of the cervix in rural India.
        Int J Cancer. 2005; 116: 617-623
        • Kuhn L.
        • Denny L.
        The time is now to implement HPV testing for primary screening in low resource settings.
        Prev Med. 2017; 98: 42-44
        • Bosch F.X.
        • Robles C.
        • Diaz M.
        • et al.
        HPV-FASTER: broadening the scope for prevention of HPV-related cancer.
        Nat Rev Clin Oncol. 2016; 13: 119-132
        • Ronco G.
        • Dillner J.
        • Elfstrom K.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
        • Zhao Y.
        • Bao H.
        • Ma L.
        • et al.
        Real-world effectiveness of primary screening with high-risk human papillomavirus testing in the cervical cancer screening programme in China: a nationwide, population-based study.
        BMC Med. 2021; 19: 164
        • Aitken C.A.
        • van Agt H.M.E.
        • Siebers A.G.
        • et al.
        Introduction of primary screening using high-risk HPV DNA detection in the Dutch cervical cancer screening programme: a population-based cohort study.
        BMC Med. 2019; 17: 228
        • Arrossi S.
        • Thouyaret L.
        • Laudi R.
        • et al.
        Implementation of HPV-testing for cervical cancer screening in programmatic contexts: The Jujuy demonstration project in Argentina.
        Int J Cancer. 2015; 137: 1709-1718
        • Denny L.
        • Kuhn L.
        • De Souza M.
        • et al.
        Screen-and-treat approaches for cervical cancer prevention in low-resource settings: a randomized controlled trial.
        JAMA. 2005; 294: 2173-2181
        • Kuhn L.
        • Wang C.
        • Tsai W.Y.
        • et al.
        Efficacy of human papillomavirus-based screen-and-treat for cervical cancer prevention among HIV-infected women.
        AIDS. 2010; 24: 2553-2561
        • World Health Organization
        WHO guideline for screening and treatment of cervical precancer lesions for cervical cancer prevention.
        (Available at:) (Accessed August 12, 2022)
        • Jeronimo J.
        • Castle P.E.
        • Temin S.
        • et al.
        Secondary Prevention of Cervical Cancer: ASCO Resource-Stratified Clinical Practice Guideline.
        J Glob Oncol. 2017; 3: 635-657
        • U.S. Preventive Services Task Force
        Cervical cancer screening.
        (Accessed at:) (Accessed August 12, 2022)
        • Arbyn M.
        • Simon M.
        • Peeters E.
        • et al.
        2020 list of human papillomavirus assays suitable for primary cervical cancer screening.
        Clin Microbiol Infect. 2021; 27: 1083-1095
        • Jeronimo J.
        • Bansil P.
        • Lim J.
        • et al.
        A multicountry evaluation of careHPV testing, visual inspection with acetic acid, and papanicolaou testing for the detection of cervical cancer.
        Int J Gynecol Cancer. 2014; 24: 576-585
        • Einstein M.H.
        • Smith K.M.
        • Davis T.E.
        • et al.
        Clinical evaluation of the cartridge-based GeneXpert human papillomavirus assay in women referred for colposcopy.
        J Clin Microbiol. 2014; 52: 2089-2095
        • Zhang W.
        • Du H.
        • Huang X.
        • et al.
        Evaluation of an isothermal amplification HPV detection assay for primary cervical cancer screening.
        Infect Agent Cancer. 2020; 15: 65
        • Arbyn M.
        • Smith S.B.
        • Temin S.
        • et al.
        Detecting cervical precancer and reaching underscreened women by using HPV testing on self samples: updated meta-analyses.
        BMJ. 2018; 363: k4823
        • Nelson E.J.
        • Maynard B.R.
        • Loux T.
        • et al.
        The acceptability of self-sampled screening for HPV DNA: a systematic review and meta-analysis.
        Sex Transm Infect. 2017; 93: 56-61
        • Gupta S.
        • Palmer C.
        • Bik E.M.
        • et al.
        Self-Sampling for Human Papillomavirus Testing: Increased Cervical Cancer Screening Participation and Incorporation in International Screening Programs.
        Front Public Health. 2018; 6: 77
        • Yeh P.T.
        • Kennedy C.E.
        • de Vuyst H.
        • et al.
        Self-sampling for human papillomavirus (HPV) testing: a systematic review and meta-analysis.
        BMJ Glob Health. 2019; 4: e001351
        • Unitaid
        Cervical cancer screening and treatment of precancerous lesions for secondary prevention of cervical cancer: technology landscape.
        (Available at:) (Accessed August 12, 2022)