Epidemiological profile of human papillomavirus infections and cervical cancer prevention among sexually active women in Burkina Faso: Literature Review

Main Article Content

Pierre Zabre Tani Sagna Rogomenoma Alice Ouedraogo Jacques Simpore

Abstract

Cervical cancer is one of the biggest public health challenges in developing countries. According to the Global Cancer Observation in 2022, Burkina Faso recorded 988 new cases, with 775 deaths. Caused mainly by the human papillomavirus (HPV), this cancer is a heavy burden on our populations. The aim of this review was to assess the current state of human papillomavirus infections and cervical cancer prevention among sexually active women in Burkina Faso. Original studies were extracted from PubMed/Medline, Google Scholar, semanticscholar, Hinari and Science Direct using appropriate MeSH terms. Results were extracted and reviewed using the Preferred Reporting Items for Systematic Reviews and Meta-Analyse method (PRISMA). Twenty-four studies from three regions of Burkina Faso were included in the systematic review, with most of the articles from the “Centre” region. Out of a total of 5480 participants for the pooled analyses, the review showed a prevalence of HPV, varying according to population type and region and ranging from 20.6% to 87.2%. In contrast, the overall prevalence of HPV 16 and 18 infections were low compared to the global trend. With a low screening rate, the prevalence of cancerous lesions ranged from 1.5% to 15.42%. The level of knowledge was lower among rural than urban residents. Bivalent and quadrivalent vaccines had low coverage for the genotypes identified. In the fight against cervical cancer in Burkina, concerted efforts are needed to strengthen screening programs, increase HPV vaccination coverage, and raise public awareness. Large-scale national studies are needed to map HPV genotypes in order to make appropriate decisions for cervical cancer control.

Keywords: Epidemiology, Prevention, Cervical cancer, HPV, Burkina Faso

Article Details

How to Cite
ZABRE, Pierre et al. Epidemiological profile of human papillomavirus infections and cervical cancer prevention among sexually active women in Burkina Faso: Literature Review. Medical Research Archives, [S.l.], v. 12, n. 11, nov. 2024. ISSN 2375-1924. Available at: <https://esmed.org/MRA/mra/article/view/5883>. Date accessed: 12 dec. 2024. doi: https://doi.org/10.18103/mra.v12i11.5883.
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Review Articles

References

1. Maria H, Dana H, Françoise M, Michael P, Jürgen W. Human papillomaviruses in Western Africa: prevalences and risk factors in Burkina Faso. Arch Gynecol Obstet. 2018;298(4):789-796. doi:10.1007/s00404-018-4860-z
2. Bernard HU, Burk RD, Chen Z, van Doorslaer K, zur Hausen H, de Villiers EM. Classification of Papillomaviruses (PVs) Based on 189 PV Types and Proposal of Taxonomic Amendments. Virology. 2010;401(1):70-79. doi:10.1016/j.virol.2010.02.002
3. Ouedraogo RA, Kande A, Nadembega WMC, Ouermi D, Zohoncon TM, Djigma FW, Ouedraogo CMRN, Lompo OM, Simpore J. Distribution of high- and low-risk human papillomavirus genotypes and their prophylactic vaccination coverage among West African women: systematic review. J Egypt Natl Cancer Inst. 2023;35(1):39. doi:10.1186/s43046-023-00196-x
4. Duport N. Données épidémiologiques sur le cancer du col de l’utérus. État Connaiss - Actual. Published online January 1, 2008:34.
5. Ishida W, Singto Y, Yuenyao P, Tassaneeyakul W, Kanjanavirojkul N, Ishida T. Contribution of epigenetic risk factors but not p53 codon 72 polymorphism to the development of cervical cancer in Northeastern Thailand. Cancer Lett. 2004;210:205-211. doi:10.1016/j.canlet.2004.03.039
6. Muñoz N, Castellsagué X, Berrington de González A, Gissmann L. Chapter 1: HPV in the etiology of human cancer. Vaccine. 2006;24 Suppl 3:S3/1-10. doi:10.1016/j.vaccine.2006.05.115
7. Jain M, Yadav D, Jarouliya U, Chavda V, Yadav AK, Chaurasia B, Song M. Epidemiology, Molecular Pathogenesis, Immuno-Pathogenesis, Immune Escape Mechanisms and Vaccine Evaluation for HPV-Associated Carcinogenesis. Pathogens. 2023;12(12). doi:10.3390/pathogens12121380
8. Zohoncon TM, Ouedraogo TC, Brun LVC, Obiri-Yeboah D, Djigma WF, Kabibou S, Ouattara S, Gomina M, Yonli AT, Bazie VJTE, Ouedraogo C, Lompo O, Akpona SA, Simpore J. Molecular Epidemiology of High-Risk Human Papillomavirus in High-Grade Cervical Intraepithelial Neoplasia and in Cervical Cancer in Parakou, Republic of Benin. Pak J Biol Sci PJBS. 2016;19(2):49-56. doi:10.3923/pjbs.2016.49.56
9. Clifford GM, Gallus S, Herrero R, Muñoz N, Snijders PJF, Vaccarella S, Anh PTH, Ferreccio C, Hieu NT, Matos E, Molano M, Rajkumar R, Ronco G, de Sanjosé S, Shin HR, Sukvirach S, Thomas JO, Tunsakul S, Meijer CJLM, Franceschi S, IARC HPV Prevalence Surveys Study Group. Worldwide distribution of human papillomavirus types in cytologically normal women in the International Agency for Research on Cancer HPV prevalence surveys: a pooled analysis. Lancet Lond Engl. 2005;366(9490):991-998. doi:10.1016/S0140-6736(05)67069-9
10. Bhatla N, Aoki D, Sharma DN, Sankaranarayanan R. Cancer of the cervix uteri. Int J Gynecol Obstet. 2018;143:22-36. doi:10.1002/ijgo.12611
11. Ferlay J, Colombet M, Soerjomataram I, Mathers C, Parkin DM, Piñeros M, Znaor A, Bray F. Estimating the global cancer incidence and mortality in 2018: GLOBOCAN sources and methods. Int J Cancer. 2019;144(8):1941-1953. doi:10.1002/ijc.31937
12. Marie Tebeu P, Saint Saba Antaon J, Adjeba M, Pikop F, Tsuala Fouogue J, Ndom P. Connaissances, attitudes et pratiques des professionnels de santé sur le cancer du col de l’utérus au Cameroun: Santé Publique. 2021;Vol. 32(5):489-496. doi:10.3917/spub.205.0489
13. Mboumba Bouassa RS, Prazuck T, Lethu T, Meye JF, Bélec L. Cervical cancer in sub-Saharan Africa: an emerging and preventable disease associated with oncogenic human papillomavirus. Med Sante Trop. 2017;27(1):16-22. doi:10.1684/mst.2017.0648
14. Debrah O, Agyemang-Yeboah F, Donkoh ET, Asmah RH. Prevalence of vaccine and non-vaccine human papillomavirus types among women in Accra and Kumasi, Ghana: a cross-sectional study. BMC Womens Health. 2021;21(1):372. doi:10.1186/s12905-021-01511-1
15. Donkoh ET, Asmah RH, Agyemang-Yeboah F, Dabo EO, Wiredu EK. Prevalence and distribution of vaccine-preventable genital human papillomavirus (HPV) genotypes in Ghanaian women presenting for screening. Cancer Control. 2022;29:10732748221094721.
16. Seyoum A, Assefa N, Gure T, Seyoum B, Mulu A, Mihret A. Prevalence and Genotype Distribution of High-Risk Human Papillomavirus Infection Among Sub-Saharan African Women: A Systematic Review and Meta-Analysis. Front Public Health. 2022;10:890880. doi:10.3389/fpubh.2022.890880
17. Ogochukwu TN, Akabueze J, Ezeome IV, Aniebue UU, Oranu EO. Vaccination against human papilloma virus in adolescent girls: mother’s knowledge, attitude, desire and practice in Nigeria. J Infect Preve Med. 2017;5(151):2.
18. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. Int J Surg. 2010;8(5):336-341. doi:10.1016/j.ijsu.2010.02.007
19. Madeleine KK, Djénéba O, Mahoukèdè ZT, Traore Fatié Porzé Wilfried, Gnoumou Ouamini Pulchérie De Prisca, Alice OR, Théophane YA, Prosper B, Paul O, Clarisse OTW, Edwige YT, Akouélé KKP, Dorcas OY, Ouedraogo Charlemagne Marie Ragnag-Néwendé, Jacques S. Molecular epidemiology of human papillomavirus in pregnant women in Burkina Faso. Biomol Concepts. 2022;13(1):334-340. doi:10.1515/bmc-2022-0026
20. Djigma FW, Zohoncon TM, Douamba Z, Sorgho PA, Obiri-Yeboah D, Ouattara AK, Sagna T, Traore L, Ghilat-Avoid-Belem NW, Sanogo K, Sempore J, Yonli AT, Pietra V, Bisseye C, Ouedraogo C, Simpore J. Molecular Genotyping of Human Papillomavirus among HIV-infected and HIV- uninfected Women in Ouagadougou, Burkina Faso. Burkina Faso. 2020;8.
21. Ouedraogo CMR, Djigma FW, Bisseye C, Sagna T, Zeba M, Ouermi D, Karou SD, Pietra V, Buelli F, Ghilat-Avoid-Belem NW, Sanogo K, Sempore J, Moret R, Pignatelli S, Nikiema JB, Simpore J. Épidémiologie et caractérisation des génotypes de papillomavirus humain dans une population de femmes à Ouagadougou. J Gynécologie Obstétrique Biol Reprod. 2011;40(7):633-638. doi:10.1016/j.jgyn.2011.05.012
22. Salambanga C, Zohoncon TM, Traoré IMA, Ouedraogo RA, Djigma WF, Ouédraog C, Simpore J. High prevalence of high-risk human papillomavirus (HPV) infection among sexually active women in Ouagadougou. Médecine Santé Trop. 2019;29(3):302-305. doi:10.1684/mst.2019.0920
23. Djigma FW, Ouédraogo C, Karou DS, Sagna T, Bisseye C, Zeba M, Ouermi D, Gnoula C, Pietra V, Ghilat-Avoid-Belem NW, Sanogo K, Sempore J, Pignatelli S, Ferri AM, Nikiema JB, Simpore J. Prevalence and genotype characterization of Human Papillomaviruses among HIV-seropositive in Ouagadougou, Burkina Faso. Acta Trop. 2011;117(3):202-206. doi:10.1016/j.actatropica.2010.12.007
24. Zohoncon TM, Bisseye C, Djigma FW, Yonli AT, Compaore TR, Sagna T, Ouermi D, Ouédraogo CMR, Pietra V, Nikiéma JB, Akpona SA, Simpore J. Prevalence of HPV High-Risk Genotypes in Three Cohorts of Women in Ouagadougou (Burkina Faso). Mediterr J Hematol Infect Dis. 2013;5(1):e2013059. doi:10.4084/MJHID.2013.059
25. Ouedraogo RA, Zohoncon TM, Guigma SP, Angèle Traore IM. Oncogenic human papillomavirus infection and genotypes characterization among sexually active women in Tenkodogo at Burkina Faso, West Africa. Papillomavirus Res. 2018;6:22-26. doi:10.1016/j.pvr.2018.09.001
26. Ouedraogo RA, Zohoncon TM, Guigma SP, Ouattara AK, Simpore J. Prédominance du papillomavirus humain 56 dans une sous-population de femmes sexuellement actives à Garango, Centre-Est, Burkina Faso: Predominance of Human Papillomavirus 56 in a subpopulation of sexually active women in Garango, Central-East, Burkina Faso. J Appl Biosci. 2020;150(1):15499-15509.
27. Ouedraogo RA, Zohoncon TM, Traore IMA, Ouattara AK, Guigma SP, Djigma FW, Obiri-Yeboah D, Ouedraogo C, Simpore J. Genotypic distribution of human oncogenic papillomaviruses in sexually active women in Burkina Faso: Central, Central-Eastern and Hauts-Bassins regions. Biomol Concepts. 2020;11(1):125-136. doi:10.1515/bmc-2020-0011
28. Sawadogo B, Gitta SN, Rutebemberwa E, Sawadogo M. Knowledge and beliefs on cervical cancer and practices on cervical cancer screening among women aged 20 to 50 years in Ouagadougou, Burkina Faso, 2012: a cross-sectional study. Pan Afr Med J. 2014;18(175). doi:10.11604/pamj.2014.18.175.3866
29. Compaore S, Ouedraogo CMR, Koanda S, Haynatzki G, Chamberlain RM, Soliman AS. Barriers to Cervical Cancer Screening in Burkina Faso: Needs for Patient and Professional Education. J Cancer Educ Off J Am Assoc Cancer Educ. 2016;31(4):760-766. doi:10.1007/s13187-015-0898-9
30. Kagoné TS, Paré PG, Dembélé A, Kania D, Zida S, Bonané/Thiéba B, Ouédraogo A, Testa J, Simporé J, Méda N. Cervical cancer in the Hauts-Bassins region of Burkina Faso: Results of a screening campaign by visual inspection with acetic acid (VIA screening in Burkina Faso). Afr J Reprod Health. 2022;26(6):97-103.
31. Tassembedo S, Winter CH, Traore IT, Ouattara A, Sawadogo M, Meda N. Cervical pre-cancer screening by visual inspection of the cervix after application of acetic acid in rural Burkina Faso: evaluation of women’s knowledge, screening practice habits, acceptability and prevalence of risk factors and lesions in Boussé health district. Pan Afr Med J. 2023;45:135. doi:10.11604/pamj.2023.45.135.36933
32. Diendéré J, Kiemtoré S, Coulibaly A, Tougri G, Ily NI, Kouanda S. Low attendance in cervical cancer screening, geographical disparities and sociodemographic determinants of screening uptake among adult women in Burkina Faso : results from the first nationwide population-based survey. Rev DÉpidémiologie Santé Publique. 2023;71(4):101845. doi:10.1016/j.respe.2023.101845
33. Traore IMA, Zohoncon TM, Dembele A, Djigma FW, Obiri-Yeboah D, Traore G, Bambara M, Ouedraogo C, Traore Y, Simpore J. Molecular Characterization of High-Risk Human Papillomavirus in Women in Bobo-Dioulasso, Burkina Faso. BioMed Res Int. 2016;2016:7092583. doi:10.1155/2016/7092583
34. Ouattara S, Somé DA, Dembélé A, Sanfo S, Zohoncon T, Ouattara AK, Bambara M, Dao B, Simporé J. Molecular Epidemiology of High-Risk Human Papilloma Virus Infection in Sexually Active Women at Bobo-Dioulasso University Teaching Hospital. Open J Obstet Gynecol. 2019;09(08):1178-1188. doi:10.4236/ojog.2019.98114
35. Tovo SF, Zohoncon TM, Dabiré AM, Ilboudo R, Tiemtoré RY, Obiri-Yeboah D, Yonli AT, Dovo EE, Ouédraogo RA, Ouattara AK, Sorgho PA, Ouermi D, Djigma FW, Ouédraogo C, Sangaré L, Simpore J. Molecular Epidemiology of Human Papillomaviruses, Neisseria gonorrhoeae, Chlamydia trachomatis and Mycoplasma genitalium among Female Sex Workers in Burkina Faso: Prevalence, Coinfections and Drug Resistance Genes. Trop Med Infect Dis. 2021;6(2):90. doi:10.3390/tropicalmed6020090
36. Ilboudo R, Traoré EM, Zohoncon TM, Ouédraogo RA, Traore MA, Bado P, Ouédraogo C, Djigma FW, Obiri D, Sakandé J, Simpore J, Ouedraogo C. Prevalence and Characterization of High-Risk Human Papillomavirus Genotypes among a Group of Sex Workers in Ouagadougou, Burkina Faso. Burkina Faso. Published online 2020.
37. Ouédraogo C, Zohoncon TM, Traoré EMA, Ouattara S, Bado P, Ouedraogo CT, Djigma FW, Ouermi D, Obiri-Yeboah D, Lompo O, Akpona SA, Simpore J. Distribution of High-Risk Human Papillomavirus Genotypes in Precancerous Cervical Lesions in Ouagadougou, Burkina Faso. Open J Obstet Gynecol. 2016;6(4):196-204. doi:10.4236/ojog.2016.64025
38. Zohoncon TM, Bado P, Ouermi D, Traoré EMA, Ouattara S, Djigma FW, Traore IMA, Yonli AT, Obiri-Yeboah D, Ouédraogo C, Akpona SA, Lompo O, Simpore J. Molecular characterization of high-risk human papillomavirus genotypes involved in invasive cervical cancer from formalin-fixed, paraffin-embedded tissues in Ouagadougou, Burkina Faso. Int J Curr Res. 2016;8(09):39314-39318.
39. Ouédraogo E, Zohoncon TM, Bayala B, Bado P, Da RPC, Ouedraogo RA, Traoré IMA, Kuassi-Kpede PA, Ouédraogo S, Dovo EE, Traoré L, Yonli AT, Djigma FW, Lompo OM, Simpore J. HPV/HBV or HPV/HCV Co-Infections in Women Treated for Chronic Hepatitis at Hôpital Saint Camille in Ouagadougou, Burkina Faso. Am J Mol Biol. 2024;14(01):1-12. doi:10.4236/ajmb.2024.141001
40. Chikandiwa A, Kelly H, Sawadogo B, Ngou J, Pisa PT, Gibson L, Didelot MN, Meda N, Weiss HA, Segondy M, Mayaud P, Delany-Moretlwe S, Group on behalf of the HS. Prevalence, incidence and correlates of low risk HPV infection and anogenital warts in a cohort of women living with HIV in Burkina Faso and South Africa. PLOS ONE. 2018;13(5):e0196018. doi:10.1371/journal.pone.0196018
41. Didelot-Rousseau MN, Nagot N, Costes-Martineau V, Vallès X, Ouedraogo A, Konate I, Weiss HA, Van de Perre P, Mayaud P, Segondy M, Yerelon Study Group. Human papillomavirus genotype distribution and cervical squamous intraepithelial lesions among high-risk women with and without HIV-1 infection in Burkina Faso. Br J Cancer. 2006;95(3):355-362. doi:10.1038/sj.bjc.6603252
42. Adams AR, Nortey PA, Dortey BA, Asmah RH, Wiredu EK. Cervical human papillomavirus prevalence, genotypes, and associated risk factors among female sex workers in Greater Accra, Ghana. J Oncol. 2019;2019.
43. Tounkara FK, Téguété I, Guédou FA, Goma-Matsétsé E, Koné A, Béhanzin L, Traoré S, Aza-Gnandji M, Keita B, Guenoun J, Coutlée F, Alary M. Human papillomavirus genotype distribution and factors associated among female sex workers in West Africa. Grce M, ed. PloS One. 2020;15(11):e0242711-e0242711. doi:10.1371/journal.pone.0242711
44. Diop-Ndiaye H, Beiter K, Gheit T, Sow Ndoye A, Dramé A, McKay-Chopin S, Tommasino M, Bouh Boye CS, Sylla B, Kane CT. Human Papillomavirus infection in senegalese female sex workers. Papillomavirus Res Amst Neth. 2019;7:97-101. doi:10.1016/j.pvr.2019.02.003
45. Morhason-Bello IO, Baisley K, Pavon MA, Adewole IF, Bakare RA, de Sanjosé S, Francis SC, Watson-Jones D. Oral, genital and anal human papillomavirus infections among female sex workers in Ibadan, Nigeria. PloS One. 2022;17(3):e0265269. doi:10.1371/journal.pone.0265269
46. Kelly HA, Ngou J, Chikandiwa A, Sawadogo B. Associations of Papillomavirus humain (HPV) génotypes avec néoplasie cervicale de haut grade (CIN2 ) dans une cohorte de femmes vivant avec le VIH au Burkina Faso et Afrique du Sud. PloS One. 2017;12(3):e0174117. doi:10.1371/journal.pone.0174117
47. Clifford GM, Gonçalves MAG, Franceschi S, Group for the H and HS. Human papillomavirus types among women infected with HIV: a meta-analysis. AIDS. 2006;20(18):2337. doi:10.1097/01.aids.0000253361.63578.14
48. Nweke IG, Banjo AAF, Abdulkareem FB, Nwadike VU. Prevalence of human papilloma virus DNA in HIV positive women in Lagos University Teaching Hospital (LUTH) Lagos, Nigeria. Published online 2013.
49. Yakub MM, Fowotade A, Anaedobe CG, Manga MM, Bakare RA, Abimiku BA. Human papillomavirus correlates of high grade cervical dysplasia among HIV-Infected women at a major treatment centre in Nigeria: a cross-sectional study. Pan Afr Med J. 2019;33:125. doi:10.11604/pamj.2019.33.125.17589
50. Zinzendorf NY, Asher CM, Sandrine AT, Pierre B, Timotée O, Agathe DK, Joseph LS, Thérèse AKB. Prevalence and Human Papillomavirus Genotypes Distribution among HIV-Positive and -Negative Young Women Aged 20 to 37-Years-Old with Cervical Cancer in Abidjan, Côte d’Ivoire. In: ; 2022. https://api.semanticscholar.org/CorpusID:247861170
51. Chachage M, Parikh AP, Mahenge A, Bahemana E, Mnkai J, Mbuya W, Mcharo R, Maganga L, Mwamwaja J, Gervas R, Kibuuka H, Maswai J, Singoei V, Iroezindu M, Fasina A, Esber A, Dear N, Imbach M, Crowell TA, Hern J, Song X, Hoelscher M, Polyak CS, Ake JA, Geldmacher C, AFRICOS Study Group. High-risk human papillomavirus genotype distribution among women living with and at risk for HIV in Africa. AIDS Lond. 2023;37(4):625-635. doi:10.1097/QAD.0000000000003437
52. Nyasenu YT, Gbeasor-Komlanvi FA, Ehlan A, Issa SAR, Dossim S, Kolou M, Yambiyo BM, Prince-david M, Salou M, Ekouevi DK, Dagnra A. Prevalence and distribution of Human Papillomavirus (HPV) genotypes among HIV infected women in Lomé, Togo. PLoS ONE. 2019;14. https://api.semanticscholar.org/CorpusID:71714850
53. Heard I, Palefsky JM, Kazatchkine MD. The Impact of HIV Antiviral Therapy on Human Papillomavirus (Hpv) Infections and Hpv-Related Diseases. Antivir Ther. 2004;9(1):13-22. doi:10.1177/135965350400900117
54. Bratcher LF, Sahasrabuddhe VV. The impact of antiretroviral therapy on HPV and cervical intraepithelial neoplasia: current evidence and directions for future research. Infect Agent Cancer. 2010;5:8. doi:10.1186/1750-9378-5-8
55. Ogembo RK, Gona PN, Seymour AJ, Park HSM, Bain PA, Maranda L, Ogembo JG. Prevalence of human papillomavirus genotypes among African women with normal cervical cytology and neoplasia: a systematic review and meta-analysis. PloS One. 2015;10(4):e0122488.
56. Kabir AS, Bukar M, Nggada HA, Rann HB, Gidado A, Musa AB. Prevalence of human papillomavirus genotypes in cervical cancer in Maiduguri, Nigeria. Pan Afr Med J. 2019;33. https://api.semanticscholar.org/CorpusID:201172653
57. Attoh S, Asmah R, Wiredu EK, Gyasi R, Tettey Y. Human papilloma virus genotypes in Ghanaian women with cervical carcinoma. East Afr Med J. 2010;87(8).
58. Nartey Y, Amo-Antwi K, Hill PC, Dassah ET, Asmah RH, Nyarko KM, Agambire R, Konney TO, Yarney J, Damale N. Human papillomavirus genotype distribution among women with and without cervical cancer: Implication for vaccination and screening in Ghana. PloS One. 2023;18(1):e0280437.
59. Obiri-Yeboah D, Akakpo PK, Mutocheluh M, Adjei-Danso E, Allornuvor G, Amoako-Sakyi D, Adu-Sarkodie Y, Mayaud P. Epidemiology of cervical human papillomavirus (HPV) infection and squamous intraepithelial lesions (SIL) among a cohort of HIV-infected and uninfected Ghanaian women. BMC Cancer. 2017;17(1):688. doi:10.1186/s12885-017-3682-x
60. Louie KS, De Sanjose S, Mayaud P. Epidemiology and prevention of human papillomavirus and cervical cancer in sub-Saharan Africa: a comprehensive review. Trop Med Int Health. 2009;14(10):1287-1302. doi:10.1111/j.1365-3156.2009.02372.x
61. Safaeian M, Kemp TJ, Pan DY, Porras C, Rodriguez AC, Schiffman M, Cortes B, Katki H, Wacholder S, Schiller JT, Gonzalez P, Penrose K, Lowy DR, Quint W, van Doorn LJ, Herrero R, Hildesheim A, Pinto LA. Cross-protective vaccine efficacy of the bivalent HPV vaccine against HPV31 is associated with humoral immune responses. Hum Vaccines Immunother. 2013;9(7):1399-1406. doi:10.4161/hv.24340
62. Diallo MH. Connaissances, attitudes et pratiques des femmes en matière de dépistage du cancer du col de l’utérus (CCU) au centre médical communal de Coronthie Conakry- Guinée. J SAGO Gynécologie – Obstétrique Santé Reprod. 2021;22(1). Accessed February 13, 2024. http://www.jsago.org/index.php/jsago/article/view/88
63. OMS. Vaccins contre les papillomavirus humains: note de synthèse de l’OMS, mai 2017.May 12, 2017:28.
64. Sampson CN, Nkpeebo SD, Degley TA. Knowledge, attitude and health beliefs on cervical cancer screening in Ajumako-Eyan-Essiam District, Ghana. Can Oncol Nurs J Rev Can Nurs Oncol. 2021;31(3):285-290. doi:10.5737/23688076313285290
65. OMS. La lutte contre le cancer du col de l’utérus: guide des pratiques essentielles.; 2017. Accessed January 7, 2021. http://apps.who.int/iris/bitstream/10665/254713/1/9789242548952-fre.pdf?ua=1
66. OMS. Stratégie mondiale en vue d’accélérer l’élimination du cancer du col de l’utérus en tant que problème de santé publique. Accessed July 6, 2024. https://www.who.int/fr/publications/i/item/9789240014107
67. Bray F, Laversanne M, Sung H, Ferlay J, Siegel RL, Soerjomataram I, Jemal A. Global cancer statistics 2022: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2024;74(3):229-263. doi:10.3322/caac.21834
68. Perrin A. Connaissance des femmes sur les modalités de prévention et de dépistage du cancer du col de l’utérus. Published online 1991.
69. Ketevi AA, Logbo-Akey E, Andele A, Adou R, Tipoh AA, Aboubakari AS, Akpadza K. Connaissances, attitudes et pratiques des femmes en âge de procréer sur le cancer du col de l’utérus à l’hôpital de Bé (Togo): Knowledge, attitudes and practices of women of childbearing age concerning cervical cancer at be hospital (Togo). J Rech Sci L’Université Lomé. 2023;25(3):175-181.
70. Bouslah S, Soltani MS, Ben Salah A, Sriha A. Connaissances, attitudes et pratiques des femmes tunisiennes en matière de dépistage du cancer du sein et de celui du col de l’utérus. Psycho-Oncol. 2014;8(2):123-132. doi:10.1007/s11839-014-0460-8
71. Olubodun T, Odukoya OO, Balogun MR. Knowledge, attitude and practice of cervical cancer prevention, among women residing in an urban slum in Lagos, South West, Nigeria. Pan Afr Med J. 2019;32(130):130-130. doi:10.11604/pamj.2019.32.130.14432
72. Ahmed SA, Sabitu K, Idris SH, Ahmed R. Knowledge, attitude and practice of cervical cancer screening among market women in Zaria, Nigeria. Niger Med J J Niger Med Assoc. 2013;54(5):316-319. doi:10.4103/0300-1652.122337
73. Daka M, Ngoma C, Kalusopa VM, Banda Y, Chikwanda EK, Mulumba A. Knowledge, Attitudes and Perceptions Influencing Cervical Cancer Screening among Women in Kitwe District, Copperbelt Province, Zambia. Open J Obstet Gynecol. Published online 2022. https://api.semanticscholar.org/CorpusID:250157220
74. Nyambe A, Kampen JK, Baboo SK, Van Hal G. Knowledge, attitudes and practices of cervical cancer prevention among Zambian women and men. BMC Public Health. 2019;19:1-15.
75. O O, J TG. Knowledge, attitudes and practices of cervical cancer screening among rural women in KwaZulu-Natal, South Africa. Pan Afr Med J. 2022;42. doi:10.11604/pamj.2022.42.188.26172
76. Shu NE, Abiola AHO, Akodu BA, Bassey BA, Misago N. Knowledge, attitudes and preventive practices for human Papilloma virus infection among female sex workers in Lagos metropolis. Pan Afr Med J. 2020;36:278. doi:10.11604/pamj.2020.36.278.17912
77. De Groot AS, Tounkara K, Rochas M, Beseme S, Yekta S, Diallo FS, Tracy JK, Teguete I, Koita OA. Knowledge, attitudes, practices and willingness to vaccinate in preparation for the introduction of HPV vaccines in Bamako, Mali. Seale H, ed. PloS One. 2017;12(2):e0171631-e0171631. doi:10.1371/journal.pone.0171631
78. Osborne A, James PB, Bangura C, Williams SMT, Wadsworth R, Lebbie A. Knowledge, prevalence, and risk factors for self-reported sexually transmitted diseases among University Students in Sierra Leone. Sierra Leone J Biomed Res. 2023;14(2):81-91.
79. Dickson KS, Boateng ENK, Acquah E, Ayebeng C, Addo IY. Screening for cervical cancer among women in five countries in sub-saharan Africa: analysis of the role played by distance to health facility and socio-demographic factors. BMC Health Serv Res. 2023;23(1):61-61. doi:10.1186/s12913-023-09055-w
80. Biaye B, Gassama O, Dieme MEF, Toure Y, Cissé M, Wade M, Diop D, Assane B, Guèye M, Diouf AA, Moreau JC. Screening for Cervical Cancer by Visual Inspection with Acetic Acid (VIA) in Nabil Choucair Health Center—Dakar (Senegal). Open J Obstet Gynecol. Published online 2019. https://api.semanticscholar.org/CorpusID:86405742
81. Gnatou GYS, Onivogui Z, Adoli LK, Gbeasor-Komlanvi FA, Sadio AJ, Konu YR, Tchankoni MK, Zida-Compaore WIC, Agbonon A, Ekouevi DK. Screening for Precancerous Cervical Lesions in Women of Reproductive Age in the Kara Region of Togo in 2022. Open J Epidemiol. 2023;13(04):293-305.
82. Chigbu CO, Onyebuchi AK, Onyeka TC, Odugu BU, Dim CC. The impact of community health educators on uptake of cervical and breast cancer prevention services in Nigeria. Int J Gynecol Obstet. 2017;137(3):319-324. doi:10.1002/ijgo.12150