Adolescent Health Series: HPV infection and vaccination in sub-Saharan Africa: 10 years of research in Tanzanian female adolescents - narrative review.
Human Papillomavirus
cervical cancer
narrative review
sexually transmitted infection
sub-Saharan Africa
vaccination
Journal
Tropical medicine & international health : TM & IH
ISSN: 1365-3156
Titre abrégé: Trop Med Int Health
Pays: England
ID NLM: 9610576
Informations de publication
Date de publication:
11 2021
11 2021
Historique:
pubmed:
27
7
2021
medline:
1
1
2022
entrez:
26
7
2021
Statut:
ppublish
Résumé
Cervical cancer is the leading cause of cancer-related morbidity and mortality in many sub-Saharan African (SSA) countries, including Tanzania. Most cervical cancer cases worldwide are attributable to infection of the cervix with Human Papillomavirus (HPV), a vaccine-preventable sexually transmitted infection (STI). Over the past 10 years, we have conducted a programme of HPV research in pre-adolescents and adolescents in Mwanza, the second-largest city in Tanzania, which is situated in a malaria-endemic region. In this narrative review article, we summarise the contribution of our work, alongside work of others, to improve the understanding of HPV epidemiology in SSA and development of setting-appropriate, evidence-based intervention strategies. We present evidence for very high prevalence and incidence of HPV infection among female SSA adolescents around the time of sexual debut, describe risk factors for HPV acquisition, and discuss associations between HPV, HIV and other STIs, which are also highly prevalent within this population. We summarise findings from early clinical trials of HPV vaccines in SSA, the first of which was an immunogenicity and safety trial conducted in Mwanza, Tanzania, and Dakar, Senegal. Within the trial, we evaluated for the first time the potential impact of malaria and helminth infection on vaccine-induced antibody responses in Tanzanian girls. We describe research evaluating optimal HPV vaccine delivery strategies within this setting, perceived requirements for and barriers to vaccine implementation among key informants from LMIC, vaccine acceptability among girls and parents, and opportunities for co-delivery of interventions alongside HPV vaccination to an adolescent population. Finally, we discuss country-level barriers to vaccine uptake in LMIC, and ongoing studies in Tanzania and other SSA countries of reduced-dose HPV vaccination schedules that may alleviate cost and logistical barriers to vaccine implementation.
Substances chimiques
Papillomavirus Vaccines
0
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
1345-1355Subventions
Organisme : Medical Research Council
ID : MR/N006135/1
Pays : United Kingdom
Informations de copyright
© 2021 John Wiley & Sons Ltd.
Références
WHO. International Agency for Research on Cancer. Global Cancer Observatory; 2018. Available at: https://gco.iarc.fr/today/home.
Villiers E-M, Schneider A, Miklaw H, Papendick U, Wagner D, Wesch H, et al. Human papillomavirus infections in women with and without abnormal cervical cytology. Lancet. 1987;2(8561):703-6.
Winer RL, Hughes JP, Feng Q, Xi LF, Cherne S, O'Reilly S, et al. Early natural history of incident, type-specific human papillomavirus infections in newly sexually active young women. Cancer Epidemiol Biomarkers Prev. 2011;20(4):699-707.
Houlihan CF, Baisley K, Bravo IG, Kapiga S, de Sanjosé S, Changalucha J, et al. Rapid acquisition of HPV around the time of sexual debut in adolescent girls in Tanzania. Int J Epidemiol. 2016;45(3):762-73.
Garland SM, Giuliano A, Brotherton J, Moscicki AB, Stanley M, Kaufmann AM, et al. IPVS statement moving towards elimination of cervical cancer as a public health problem. Papillomavirus Res. 2018;5:87-8.
Hall MT, Simms KT, Lew J-B, Smith MA, Brotherton JML, Saville M, et al. The projected timeframe until cervical cancer elimination in Australia: a modelling study. Lancet Public Health. 2019;4(1):e19-27.
Burger EA, Smith MA, Killen J, Sy S, Simms KT, Canfell K, et al. Projected time to elimination of cervical cancer in the USA: a comparative modelling study. Lancet Public Health. 2020;5(4):e213-22.
Brisson M, Kim JJ, Canfell K, Drolet M, Gingras G, Burger EA, 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(10224):575-90.
PopulationStat. World Statistical Data. Mwanza, Tanzania Population. Available from: https://populationstat.com/tanzania/mwanza. Accessed 27 Jun 2020.
Asiki G, Mpendo J, Abaasa A, Agaba C, Nanvubya A, Nielsen L, et al. HIV and syphilis prevalence and associated risk factors among fishing communities of Lake Victoria, Uganda. Sex Transm Infect. 2011;87(6):511-5.
Kapesa A, Basinda N, Nyanza EC, Mushi MF, Jahanpour O, Ngallaba SE, et al. Prevalence of HIV infection and uptake of HIV/AIDS services among fisherfolk in landing Islands of Lake Victoria, north western Tanzania. BMC Health Serv Res. 2018;18(1):980.
Kohli A, Kerrigan D, Brahmbhatt H, Likindikoki S, Beckham J, Mwampashi A, et al. Social and structural factors related to HIV risk among truck drivers passing through the Iringa region of Tanzania. AIDS Care. 2017;29(8):957-60.
Lemme F, Doyle AM, Changalucha J, Andreasen A, Baisley K, Maganja K, et al. HIV infection among young people in northwest Tanzania: the role of biological, behavioural and socio-demographic risk factors. PLoS One. 2013;8(6):e66287.
Francis SC, Ao TT, Vanobberghen FM, Chilongani J, Hashim R, Andreasen A, et al. Epidemiology of curable sexually transmitted infections among women at increased risk for HIV in northwestern Tanzania: inadequacy of syndromic management. PLoS One. 2014;9(7):e101221.
Watson-Jones D, Baisley K, Brown J, Kavishe B, Andreasen A, Changalucha J, et al. High prevalence and incidence of human papillomavirus in a cohort of healthy young African female subjects. Sex Transm Infect. 2013;89(5):358-65.
Baisley KJ, Andreasen A, Irani J, Nnko S, Changalucha J, Crucitti T, et al. HPV prevalence around the time of sexual debut in adolescent girls in Tanzania. Sex Transm Infect. 2020;96(3):211-9.
Houlihan CF, Baisley K, Bravo IG, Pavón MA, Changalucha J, Kapiga S, et al. Human papillomavirus DNA detected in fingertip, oral and bathroom samples from unvaccinated adolescent girls in Tanzania. Sex Transm Infect. 2019;95(5):374-9.
Houlihan CF, de Sanjosé S, Baisley K, Changalucha J, Ross DA, Kapiga S, et al. Prevalence of human papillomavirus in adolescent girls before reported sexual debut. J Infect Dis. 2014;210(6):837-45.
Mbulawa ZZA, van Schalkwyk C, Hu N-C, Meiring TL, Barnabas S, Dabee S, et al. High human papillomavirus (HPV) prevalence in South African adolescents and young women encourages expanded HPV vaccination campaigns. PLoS One. 2018;13(1):e0190166.
Ebrahim S, Mndende XK, Kharsany ABM, Mbulawa ZZA, Naranbhai V, Frohlich J, et al. High Burden of Human Papillomavirus (HPV) infection among young women in KwaZulu-Natal, South Africa. PLoS One. 2016;11(1):e0146603.
Ngabo F, Franceschi S, Baussano I, et al. Human papillomavirus infection in Rwanda at the moment of implementation of a national HPV vaccination programme. BMC Infect Dis. 2016;16:225.
Bule YP, Silva J, Carrilho C, Campos C, Sousa H, Tavares A, et al. Human papillomavirus prevalence and distribution in self-collected samples from female university students in Maputo. Int J Gynaecol Obstet. 2020;149(2):237-46.
Hegdahl HK, Fylkesnes KM, Sandøy IF. Sex differences in HIV prevalence persist over time: evidence from 18 countries in Sub-Saharan Africa. PLoS One. 2016;11(2):e0148502.
Pettifor AE, Hudgens MG, Levandowski BA, Rees HV, Cohen MS, et al. Highly efficient HIV transmission to young women in South Africa. AIDS. 2007;21(7):861-5.
Murenzi G, Kanyabwisha F, Murangwa A, Kubwimana G, Mutesa L, Burk RD, et al. Twelve-year trend in the prevalence of high-risk human papillomavirus infection among Rwandan women living with HIV. J Infect Dis. 2020;222(1):74-81.
Williamson AL. The Interaction between human immunodeficiency virus and human papillomaviruses in heterosexuals in Africa. J Clin Med. 2015;4(4):579-92.
Adler DH, Wallace M, Bennie T, et al. Cervical dysplasia and high-risk human papillomavirus infections among HIV-infected and HIV-uninfected adolescent females in South Africa. Infect Dis Obstet Gynecol. 2014;2014:498048.
Adler D, Wallace M, Bennie T, Abar B, Sadeghi R, Meiring T, et al. High risk human papillomavirus persistence among HIV-infected young women in South Africa. Int J Infect Dis. 2015;33:219-21.
Houlihan CF, Larke NL, Watson-Jones D, Smith-McCune KK, Shiboski S, Gravitt PE, et al. Human papillomavirus infection and increased risk of HIV acquisition. A systematic review and meta-analysis. AIDS. 2012;26(17):2211-22.
Gallagher KE, Baisley K, Grosskurth H, Vallely A, Kapiga S, Vandepitte J, et al. The association between cervical human papillomavirus infection and subsequent HIV acquisition in Tanzanian and Ugandan women: a nested case-control study. J Infect Dis. 2016;214(1):87-95.
Looker KJ, Rönn MM, Brock PM, Brisson M, Drolet M, Mayaud P, et al. Evidence of synergistic relationships between HIV and Human Papillomavirus (HPV): systematic reviews and meta-analyses of longitudinal studies of HPV acquisition and clearance by HIV status, and of HIV acquisition by HPV status. J Int AIDS Soc. 2018;21(6):e25110.
Torrone EA, Morrison CS, Chen P-L, Kwok C, Francis SC, Hayes RJ, et al. Prevalence of sexually transmitted infections and bacterial vaginosis among women in sub-Saharan Africa: An individual participant data meta-analysis of 18 HIV prevention studies. PLoS Medicine. 2018;15(2):e1002511.
van Schalkwyk C, Moodley J, Welte A, Johnson LF, et al. Are associations between HIV and human papillomavirus transmission due to behavioural confounding or biological effects? Sex Transm Infect. 2019;95(2):122-8.
Veldhuijzen NJ, Braunstein SL, Vyankandondera J, Ingabire C, Ntirushwa J, Kestelyn E, et al. The epidemiology of human papillomavirus infection in HIV-positive and HIV-negative high-risk women in Kigali, Rwanda. BMC Infect Dis. 2011;11:333.
Nakalembe M, Makanga P, Mubiru F, Swanson M, Martin J, Huchko M, et al. Prevalence, correlates, and predictive value of high-risk human papillomavirus mRNA detection in a community-based cervical cancer screening program in western Uganda. Infect Agent Cancer. 2019;14:14.
Ermel A, Tonui P, Titus M, Tong Y, Wong N, Ong’echa J, et al. A cross-sectional analysis of factors associated with detection of oncogenic human papillomavirus in human immunodeficiency virus-infected and uninfected Kenyan women. BMC Infect Dis. 2019;19(1):352.
Sow PS, Watson-Jones D, Kiviat N, Changalucha J, Mbaye KD, Brown J, et al. Safety and immunogenicity of human papillomavirus-16/18 AS04-adjuvanted vaccine: a randomized trial in 10-25-year-old HIV-Seronegative African girls and young women. J Infect Dis. 2013;207(11):1753-63.
Brown J, Baisley K, Kavishe B, Changalucha J, Andreasen A, Mayaud P, et al. Impact of malaria and helminth infections on immunogenicity of the human papillomavirus-16/18 AS04-adjuvanted vaccine in Tanzania. Vaccine. 2014;32(5):611-7.
Nakalembe M, Banura C, Namujju PB, Mirembe FM. Immunogenicity to the bivalent HPV-16/18 vaccine among adolescent African students exposed to helminths and malaria. J Infect Dev Ctries. 2015;9(2):197-205.
Denny L, Hendricks B, Gordon C, Thomas F, Hezareh M, Dobbelaere K, et al. Safety and immunogenicity of the HPV-16/18 AS04-adjuvanted vaccine in HIV-positive women in South Africa: a partially-blind randomised placebo-controlled study. Vaccine. 2013;31(48):5745-53.
Mugo N, Ansah NA, Marino D, Saah A, Garner EIO, et al. Evaluation of safety and immunogenicity of a quadrivalent human papillomavirus vaccine in healthy females between 9 and 26 years of age in Sub-Saharan Africa. Hum Vaccin Immunother. 2015;11(6):1323-30.
Kojic EM, Kang M, Cespedes MS, Umbleja T, Godfrey C, Allen RT, et al. Immunogenicity and safety of the quadrivalent human papillomavirus vaccine in HIV-1-infected women. Clin Infect Dis. 2014;59(1):127-35.
Mugo NR, Eckert L, Magaret AS, Cheng A, Mwaniki L, Ngure K, et al. Quadrivalent HPV vaccine in HIV-1-infected early adolescent girls and boys in Kenya: Month 7 and 12 post vaccine immunogenicity and correlation with immune status. Vaccine. 2018;36(46):7025-32.
WHO. Human papillomavirus vaccines: WHO position paper, October 2014. Wkly Epidemiol Rec 2014;89:465-91.
Iversen O-E, Miranda MJ, Ulied A, Soerdal T, Lazarus E, Chokephaibulkit K, et al. Immunogenicity of the 9-valent HPV vaccine using 2-dose regimens in girls and boys vs a 3-dose regimen in women. JAMA. 2016;316(22):2411-21.
Watson-Jones D, Baisley K, Ponsiano R, Lemme F, Remes P, Ross D, et al. Human papillomavirus vaccination in Tanzanian schoolgirls: cluster-randomized trial comparing 2 vaccine-delivery strategies. J Infect Dis. 2012;206(5):678-86.
Quentin W, Terris-Prestholt F, Changalucha J, Soteli S, Edmunds WJ, Hutubessy R, et al. Costs of delivering human papillomavirus vaccination to schoolgirls in Mwanza Region. Tanzania. BMC Med. 2012;10:137.
Remes P, Selestine V, Changalucha J, Ross DA, Wight D, de Sanjosé S, et al. A qualitative study of HPV vaccine acceptability among health workers, teachers, parents, female pupils, and religious leaders in northwest Tanzania. Vaccine. 2012;30(36):5363-7.
Watson-Jones D, Tomlin K, Remes P, Baisley K, Ponsiano R, Soteli S, et al. Reasons for receiving or not receiving HPV vaccination in primary schoolgirls in Tanzania: a case control study. PLoS One. 2012;7(10):e45231.
Cunningham MS, Davison C, Aronson KJ. HPV vaccine acceptability in Africa: a systematic review. Prev Med. 2014;69:274-9.
Watson-Jones D, Lees S, Mwanga J, Neke N, Changalucha J, Broutet N, et al. Feasibility and acceptability of delivering adolescent health interventions alongside HPV vaccination in Tanzania. Health Policy Plan. 2016;31(6):691-9.
Gallagher KE, Howard N, Kabakama S, Mounier-Jack S, Burchett HED, LaMontagne DS, et al. Human papillomavirus (HPV) vaccine coverage achievements in low and middle-income countries 2007-2016. Papillomavirus Res. 2017;4:72-8.
Gallagher KE, Howard N, Kabakama S, Mounier-Jack S, Griffiths UK, Feletto M, et al. Lessons learnt from human papillomavirus (HPV) vaccination in 45 low- and middle-income countries. PLoS One. 2017;12(6):e0177773.
Watson-Jones D, Mugo N, Lees S, Mathai M, Vusha S, Ndirangu G, et al. Access and attitudes to HPV vaccination amongst hard-to-reach populations in Kenya. PLoS One. 2015;10(6):e0123701.
Kabakama S, Gallagher KE, Howard N, Mounier-Jack S, Burchett HED, Griffiths UK, et al. Social mobilisation, consent and acceptability: a review of human papillomavirus vaccination procedures in low and middle-income countries. BMC Public Health. 2016;16(1):834.
Gallagher KE, Erio T, Baisley K, Lees S, Watson-Jones D, et al. The impact of a human papillomavirus (HPV) vaccination campaign on routine primary health service provision and health workers in Tanzania: a controlled before and after study. BMC Health Serv Res. 2018;18(1):173.
Gallagher KE, LaMontagne DS, Watson-Jones D. Status of HPV vaccine introduction and barriers to country uptake. Vaccine. 2018;36(32):4761-7.
Perlman S, Wamai RG, Bain PA, Welty T, Welty E, Ogembo JG, et al. Knowledge and awareness of HPV vaccine and acceptability to vaccinate in sub-Saharan Africa: a systematic review. PLoS One. 2014;9(3):e90912.
Sankaranarayanan R, Joshi S, Muwonge R, Esmy PO, 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(32):4783-91.
Kreimer AR, Sampson JN, Porras C, Schiller JT, Kemp T, Herrero R, et al. Evaluation of durability of a single-dose of the bivalent HPV vaccine: the CVT Trial. J Natl Cancer Inst. 2020;112(10):1038-46.
Whitworth HS, Gallagher KE, Howard N, Mounier-Jack S, Mbwanji G, Kreimer AR, et al. Efficacy and immunogenicity of a single dose of human papillomavirus vaccine compared to no vaccination or standard three and two-dose vaccination regimens: A systematic review of evidence from clinical trials. Vaccine. 2020;38(6):1302-14.
Gallagher KE, Kelly H, Cocks N, Dixon S, Mounier-Jack S, Howard N, et al. Vaccine programme stakeholder perspectives on a hypothetical single-dose human papillomavirus (HPV) vaccine schedule in low and middle-income countries. Papillomavirus Res. 2018;6:33-40.
Baisley KJ, Whitworth HS, Changalucha J, Pinto L, Dillner J, Kapiga S, et al. A dose-reduction HPV vaccine immunobridging trial of two HPV vaccines among adolescent girls in Tanzania (the DoRIS trial) - Study protocol for a randomised controlled trial. Contemp Clin Trials. 2021;101:106266.
Mitchell KR, Erio T, Whitworth HS, Marwerwe G, Changalucha J, Baisley K, et al. Does the number of doses matter? A qualitative study of HPV vaccination acceptability nested in a dose reduction trial in Tanzania. Tumour. Virus Res. 2021;12:200217.
Houlihan CF, Baisley K, Bravo IG, Kapiga S, de Sanjosé S, Changalucha J, et al. The Incidence of Human Papillomavirus in Tanzanian Adolescent Girls Before Reported Sexual Debut. J Adolesc Health. 2016;58(3):295-301.