HPV-associated cervical cancer: Current status and prospects
https://doi.org/10.29413/ABS.2023-8.3.4
Abstract
Every year, 570,000 new cases of cervical cancer (CC) are diagnosed in the world, and 311,000 people die from this disease. CC is the fourth most common type of cancer and therefore the fourth leading cause of cancer death in women worldwide. Numerous data on the occurrence and development of cervical cancer indicate an association in most cases (up to 90 %) with human papillomaviruses (HPV) of high carcinogenic risk (HCR).
CC prevention strategies are based on screening, and deaths from this oncopathology can be prevented through vaccination and treatment with early detection of the disease.
In this review, much attention is paid to current issues of detection and prevention of HPV-associated pathologies, and cervical cancer in particular, aiming to summarize and analyze the latest international literature data on this issue. As a result of this study, it was shown that for countries implementing the National program of vaccination against HPV of high carcinogenic risk, a decrease in the incidence of both cervical pathologies of varying severity and other cancers associated with the HPV carriage was registered.
While effective implementation of actual experience and future advances in human papillomavirus vaccine prophylaxis may make it possible for all countries to move to the high levels of vaccination coverage required to eliminate HPV-associated pathologies, the results also suggest that the path to complete cervical cancer elimination as a global public health problem can be extremely difficult due to a number of existing limitations.
About the Authors
E. A. KravtsovaRussian Federation
Ekaterina A. Kravtsova – Research Assistant at the Laboratory of Oncovirology; 1st year Master’s Degree Student at the Department of Human and Animal Physiology, Biological Institute
Kooperativniy lane 5, Tomsk 634009, Russian Federation
Lenina ave. 36, Tomsk 634050, Russian Federation
M. M. Tsyganov
Russian Federation
Matvei M. Tsyganov – Cand. Sc. (Biol.), Senior Research Officer at the Laboratory of Oncovirology; Associate Professor at the Department of Biochemistry and Molecular Biology with a Course of Clinical Laboratory Diagnostics
Kooperativniy lane 5, Tomsk 634009, Russian Federation
Moskovsky trakt 2, Tomsk 634050, Russian Federation
N. V. Litviakov
Russian Federation
Nikolay V. Litviakov – Dr. Sc. (Biol.), Head of the Laboratory of Oncovirology; Senior Researcher Officer at the Laboratory of Genetic Technologies, Central Research Laboratory
Kooperativniy lane 5, Tomsk 634009, Russian Federation
Moskovsky trakt 2, Tomsk 634050, Russian Federation
M. K. Ibragimova
Russian Federation
Marina K. Ibragimova – Cand. Sc. (Biol.), Senior Research Officer at the Laboratory of Oncovirology; Associate Professor at the Department of Biochemistry and Molecular Biology with a Course of Clinical Laboratory Diagnostics; Associate Professor at the Department of Vertebrate Zoology and Ecology, Biological Institute
Kooperativniy lane 5, Tomsk 634009, Russian Federation
Lenina ave. 36, Tomsk 634050, Russian Federation
Moskovsky trakt 2, Tomsk 634050, Russian Federation
References
1. Almeida AM, Queiroz JA, Sousa F, Sousa Â. Cervical cancer and HPV infection: Ongoing therapeutic research to counteract the action of E6 and E7 oncoproteins. Drug Discov Today. 2019; 24(10): 2044-2057. doi: 10.1016/j.drudis.2019.07.011
2. Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Сancer J Clin. 2021; 71(3): 209-249. doi: 10.3322/caac.21660
3. Jalil AT, Kadhum WR, Faryad Khan MU, Karevskiy A, Hanan ZK, Suksatan W, et al. Cancer stages and demographical study of HPV16 in gene L2 isolated from cervical cancer in DhiQar province, Iraq. Appl Nanosci. 2021; 13: 3627. doi: 10.1007/s13204-021-01947-9
4. Mutombo AB, Benoy I, Tozin R, Bogers J, van Geertruyden JP, Jacquemyn Y. Prevalence and distribution of human papillomavirus genotypes among women in Kinshasa, the Democratic Republic of the Congo. J Glob Oncol. 2019; 5:1-9. doi: 10. 1200/JGO.19.00110
5. Zoa Assoumou S, Ndjoyi Mbiguino A, Mabika Mabika B, Nguizi Ogoula S, El Mzibri M, Khattabi A, et al. Human papillomavirus genotypes distribution among Gabonese women with normal cytology and cervical abnormalities. Infect Agent Cancer. 2016; 11(1): 1-8. doi: 10.1186/s13027-016-0046-0
6. Khodakarami N, Hosseini SJ, Yavari P, Farzaneh F, Etemad K, Salehpour S, et al. Human papillomavirus infection prevalence in women referred to health clinic of Shahid Beheshti University of Medical Sciences, Tehran, Iran. Iranian Journal of Epidemiology. 2012; 7(4): 35-42.
7. Zhang X, Li J, Xie B, Wu B, Lei S, Yao Y, et al. Comparative metabolomics analysis of cervicitis in human patients and a phenol mucilage-induced rat model using liquid chromatography tandem mass spectrometry. Front Pharmacol. 2018; 9: 282. doi: 10.3389/fphar.2018.00282
8. Li M, Du X, Lu M, Zhang W, Sun Z, Li L, et al. Prevalence characteristics of single and multiple HPV infections in women with cervical cancer and precancerous lesions in Beijing, China. J Med Virol. 2019; 91(3): 473-481. doi: 10.1002/jmv.25331
9. Korolenkova LI. Cervical intraepithelial neoplasia and early forms of cervical cancer: Clinical and morphological concept of cervical carcinogenesis. Moscow, 2017. (In Russ.).
10. Joshi S, Parikh R. PAP smear and HPV co-testing-need of the hour. Int J Health Sci Res. 2021; 11(1): 48-53.
11. Šarenac T, Mikov M. Cervical cancer, different treatments and importance of bile acids as therapeutic agents in this disease. Front Pharmacol. 2019; 10: 484. doi: 10.3389/fphar.2019.00484
12. Alkilani YG, Apodaca-Ramos I. Cervical polyps. StatPearls Publishing; 2020.
13. Kucukyıldız I, Karaca M, Akgor U, Turkyılmaz M, Keskinkılıc B, Kara F, et al. Endocervical polyps in high risk human papillomavirus infections. Ginekol Pol. 2022; 93(1): 7-10. doi: 10.5603/GP.a2021.0207
14. Major AL, 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(2): 501-511. doi: 10.1007/s00404-020-05816-8
15. Ye J, Cheng XD, Cheng B, Cheng YF, Chen XJ, Lu WG, et al. MiRNA detection in cervical exfoliated cells for missed high-grade lesions in women with LSIL/CIN1 diagnosis after colposcopyguided biopsy. BMC Cancer. 2019; 19(1): 1-9. doi: 10.1186/s12885-019-5311-3
16. Liu M, Yan X, Zhang M, Li X, Li S, Jing M. Influence of human papillomavirus infection on the natural history of cervical intraepithelial neoplasia 1: A meta-analysis. BioMed Res Int. 2017; 2017: 8971059. doi: 10.1155/2017/8971059
17. Santana BN, Baro RS, Orozco R, Arranz JP. Cervical vaporization in LSIL and persistent HPV infection. Taiwan J Obstet Gynecol. 2018; 57(4): 475-478. doi: 10.1016/j.tjog.2018.06.010
18. Tang Y, Zheng L, Yang S, Li B, Su H, Zhang LP. Epidemiology and genotype distribution of human papillomavirus (HPV) in Southwest China: A cross-sectional five years study in nonvaccinated women. Virol J. 2017; 14(1): 1-10. doi: 10.1186/s12985-017-0751-3
19. Yang W, Luo N, Ma L, Dai H, Cheng Z. The changes of surgical treatment for symptomatic uterine myomas in the past 15 years. Gynecol Minim Invasive Ther. 2018; 7(1): 10. doi: 10.4103/GMIT.GMIT_11_17
20. Bonde J, Bottari F, Parvu V, Pedersen H, Yanson K, Iacobone AD, et al. Bayesian analysis of baseline risk of CIN2 and CIN3 by HPV genotype in a European referral cohort. Int J Cancer. 2019; 145(4): 1033-1041. doi: 10.1002/ijc.32291
21. Sand FL, Munk C, Frederiksen K, Junge J, Iftner T, Dehlendorff C, et al. Risk of CIN3 or worse with persistence of 13 individual oncogenic HPV types. Int J Cancer. 2019; 144(80): 1975-1982. doi: 10.1002/ijc.31883
22. Celiešiūtė J, Vitkauskaitė A, Jusevičiūtė V, Paškauskas S, Jarienė K, Čižauskas A, et al. Low, medium and high-risk HPV type distribution in cervical carcinoma in situ. Int J Gynecol Cancer. 2017; 27(4): 1747.
23. Lu J, Song E, Ghoneim A, Alrashoud M. Machine learning for assisting cervical cancer diagnosis: An ensemble approach. Future Generation Computer Systems. 2020; 106: 199-205. doi: 10.1016/j.future.2019.12.033
24. Wang X, Huang X, Zhang Y. Involvement of human papillomaviruses in cervical cancer. Front Microbiol. 2018; 9: 2896. doi: 10.3389/fmicb.2018.02896
25. Wang R, Pan W, Jin L, Huang W, Li Y, Wu D, et al. Human papillomavirus vaccine against cervical cancer: Opportunity and challenge. Cancer Lett. 2020; 471: 88-102. doi: 10.1016/j.canlet.2019.11.039
26. Ono A, Koshiyama M, Nakagawa M, Watanabe Y, Ikuta E, Seki K, Oowaki M, et al. The preventive effect of dietary antioxidants on cervical cancer development. Medicina. 2020; 56(11): 604. doi: 10.3390/medicina56110604
27. Almeida AM, Queiroz JA, Sousa F, Sousa Â. Cervical cancer and HPV infection: Ongoing therapeutic research to counteract the action of E6 and E7 oncoproteins. Drug Discov Today. 2019;24(10): 2044-2057. doi: 10.1016/j.drudis.2019.07.011
28. Li W, Tian S, Wang P, Zang Y, Chen X, Yao Y, et al. The characteristics of HPV integration in cervical intraepithelial cells. J Cancer. 2019; 10(12): 2783. doi: 10.7150/jca.31450
29. Hu Z, Ma D. The precision prevention and therapy of HPV‐related cervical cancer: New concepts and clinical implications. Cancer Med. 2018; 7(10): 5217-5236. doi: 10.1002/cam4.1501
30. Zhou L, Qiu Q, Zhou Q, Li J, Yu M, Li K, et al. Long-read sequencing unveils high-resolution HPV integration and its oncogenic progression in cervical cancer. Nat Commun. 2022; 13(1):2563. doi: 10.1038/s41467-022-30190-1
31. Ribeiro J, Teixeira D, Marinho-Dias J, Monteiro P, Loureiro J, Baldaque I, et al. Characterization of human papillomavirus genotypes and HPV-16 physical status in cervical neoplasias of women from northern Portugal. Int J Gynecol Obstet. 2014; 125(2): 107-110. doi: 10.1016/j.ijgo.2013.10.011
32. Oyervides-Muñoz MA, Pérez-Maya AA, Rodríguez-Gutiérrez HF, Gómez-Macias GS, Fajardo-Ramírez OR, Treviño V, et al. Understanding the HPV integration and its progression to cervical cancer. Infect Genet Evol. 2018; 61: 134-144. doi: 10.1016/j.meegid.2018.03.003
33. Kamal M, Lameiras S, Deloger M, Morel A, Vacher S, Lecerf C, et al. Human papilloma virus (HPV) integration signature in cervical cancer: Identification of MACROD2 gene as HPV hot spot integration site. Br J Cancer. 2021; 124(4): 777-785. doi: 10.1038/s41416-020-01153-4
34. Bodelon C, Vinokurova S, Sampson JN, den Boon JA, Walker JL, Horswill MA, et al. Chromosomal copy number alterations and HPV integration in cervical precancer and invasive cancer. Carcinogenesis. 2016; 37(2): 188-196. doi: 10.1093/carcin/bgv171
35. Wipperman J, Neil T, Williams T. Cervical cancer: Evaluation and management. Am Fam Physician. 2018; 97(7): 449-454.
36. Wang R, Pan W, Ji L, Huang W, Li Y, Wu D. Human papillomavirus vaccine against cervical cancer: Opportunity and challenge. Cancer Lett. 2020; 471: 88-102. doi: 10.1016/j.canlet.2019.11.039
37. Nagelhout G, Ebisch RM, van der Hel O, Meerkerk GJ, Magnée T, de Bruijn T, et al. Is smoking an independent risk factor for developing cervical intra-epithelial neoplasia and cervical cancer? A systematic review and meta-analysis. Expert Rev Anticancer Ther. 2021; 21(7): 781-794. doi: 10.1080/14737140.2021.1888719
38. Litviakov NV, Ibragimova MK, Tsyganov MM, Shpileva OV, Churuksaeva ON, Kolomiets LA. Changes in the genetic landscape
39. during the malignization of high grade squamous intraepithelial lesion into cervical cancer. Curr Probl Cancer. 2020; 44(5): 100567. doi: 10.1016/j.currproblcancer.2020.100567
40. Zhang H, Lu J, Lu Y, Cai Q, Liu H, Xu C. Cervical microbiome is altered in cervical intraepithelial neoplasia after loop electrosurgical excision procedure in china. Sci Rep. 2018; 8(1): 1-8. doi: 10.1038/s41598-018-23389-0
41. De Vincenzo R, Ricci C, Conte C, Scambia G. HPV vaccine cross-protection: Highlights on additional clinical benefit. Gynecol Oncol. 2013; 130(3): 642-651. doi: 10.1016/j.ygyno.2013.05.033
42. Ranjeva SL, Baskerville EB, Dukic V, Villa LL, LazcanoPonce E, Giuliano AR, et al. Recurring infection with ecologically distinct HPV types can explain high prevalence and diversity. Proceedings of the National Academy of Sciences. 2017; 114(51): 13573-13578. doi: 10.1073/pnas.1714712114
43. Wang R, Pan W, Jin L, Huang W, Li Y, Wu D, et al. Human papillomavirus vaccine against cervical cancer: Opportunity and challenge. Cancer Lett. 2020; 471: 88-102. doi: 10.1016/j.canlet.2019.11.039
44. Giorgi Rossi P, Carozzi F, Ronco G, Allia E, Bisanzi S, GillioTos A, et al. p16/ki67 and E6/E7 mRNA accuracy and prognostic value in triaging HPV DNA-positive women. JNCI: J Nati Cancer Inst. 2021; 113(3): 292-300. doi: 10.1093/jnci/djaa105
45. Zhao J, Cao H, Zhang W, Fan Y, Shi S, Wang R. SOX14 hypermethylation as a tumour biomarker in cervical cancer. BMC Cancer. 2021; 21(1): 1-10. doi: 10.1186/s12885-021-08406-2
46. Park S, Eom K, Kim J, Bang H, Wang HY, Ahn S, et al. MiR-9, miR-21, and miR-155 as potential biomarkers for HPV positive and negative cervical cancer. BMC Cancer. 2017; 17(1): 1-8. doi: 10.1186/s12885-017-3642-5
47. Kim HJ, Kim CY, Jin J, Bae MK, Kim YH, Ju W, et al. Aberrant single‐minded homolog 1 methylation as a potential biomarker for cervical cancer. Diagn Cytopathol. 2018; 46(1): 15-21. doi: 10.1002/dc.23838
48. Jiao X, Zhang S, Jiao J, Zhang T, Qu W, Muloye GM, et al. Promoter methylation of SEPT9 as a potential biomarker for early detection of cervical cancer and its overexpression predicts radioresistance. Clin Epigeneicst. 2019; 11(1): 1-14. doi: 10.1186/s13148-019-0719-9
49. Li N, He Y, Mi P, Hu Y. ZNF582 methylation as a potential biomarker to predict cervical intraepithelial neoplasia type III/worse:
50. A meta-analysis of related studies in Chinese population. Medicine. 2019; 98(6): e14297. doi: 10.1097/MD.0000000000014297
51. Fang C, Wang SY, Liou YL, Chen MH, Ouyang W, Duan KM. The promising role of PAX1 (aliases: HUP48, OFC2) gene methylation in ancer screening. Mol Genet Genomic Med. 2019; 7(3): e506. doi: 10.1002/mgg3.506
52. Zhang L, Yu J, Huang W, Zhang H, Xu J, Cai H. A. Sensitive and simplified classifier of cervical lesions based on a methylationspecific PCR assay: A Chinese cohort study. Cancer Manag Res. 2020; 12: 2567-2576. doi: 10.2147/CMAR.S246103
53. Gutiérrez-Hoya A, Soto-Cruz I. Role of the JAK/STAT pathway in cervical cancer: It’s relationship with HPV E6/E7 oncoproteins. Cells. 2020; 9(10): 2297. doi: 10.3390/cells9102297
54. Rodrigues C, Joy LR, Sachithanandan SP, Krishna S. Notch signalling in cervical cancer. Expl Cell Res. 2019; 385(2): 111682. doi: 10.1016/j.yexcr.2019.111682
55. Ramachandran D, Schürmann P, Mao Q, Wang Y, Bretschneider LM, Speith LM, et al. Association of genomic variants at the human leukocyte antigen locus with cervical cancer risk, HPV status and gene expression levels. Int J Cancer. 2020; 147(9): 2458-2468. doi: 10.1002/ijc.33171
56. Lei J, Ploner A, Elfström KM, Wang J, Roth A, Fang F, et al. HPV vaccination and the risk of invasive cervical cancer. N Engl J Med. 2020; 383(14): 1340-1348. doi: 10.1056/NEJMoa1917338
57. 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 modeling analysis in 78 low-income and lower-middle-income countries. Lancet. 2020; 395(10224): 575-590. doi: 10.1016/S0140-6736(20)30068-4
58. Ngoma M, Autier P. Cancer prevention: cervical cancer. Ecancermedicalscience. 2019; 13: 952. doi: 10.3332/ecancer.2019.952
59. Simms KT, Hanley SJ, Smith MA, Keane A, Canfell K. Impact of HPV vaccine hesitancy on cervical cancer in Japan: A modelling study. Lancet Public Health. 2020; 5(4): e223-e234. doi: 10.1016/S2468-2667(20)30010-4
60. Canfell K. Towards the global elimination of cervical cancer. Papillomavirus Res. 2019; 8: 100170. doi: 10.1016/j.pvr.2019.100170
61. Palmer T, Wallace L, Pollock KG, Cuschieri K, Robertson C, Kavanagh K, et al. Prevalence of cervical disease at age 20 after immunisation with bivalent HPV vaccine at age 12–13 in Scotland: Retrospective population study. BMJ. 2019; 365: 1161. doi: 10.1136/bmj.l1161
62. Tanaka H, Shirasawa H, Shimizu D, Sato N, Ooyama N, Takahashi O, et al. Preventive effect of human papillomavirus vaccination on the development of uterine cervical lesions in young Japanese women. J Obstet Gynaecol Res. 2017; 43(10): 1597-1601. doi: 10.1111/jog.13419
63. Gertig DM, Brotherton JM, Budd AC, Drennan K, Chappell G, Saville AM. Impact of a population-based HPV vaccination program on cervical abnormalities: A data linkage study. BMC Med. 2013; 11(1): 1-12. doi : 10.1186/1741-7015-11-227
64. Mahmud SM, Kliewer EV, Lambert P, Bozat-Emre S, Demers AA. Effectiveness of the quadrivalent human papillomavirus vaccine against cervical dysplasia in Manitoba, Canada. J Clin Oncol. 2014; 32(5): 438-443. doi: 10.1200/JCO.2013.52.4645
65. Wang R, Pan W, Jin L, Huang W, Li Y, Wu D, et al. Human papillomavirus vaccine against cervical cancer: Opportunity and challenge.Cancer Lett. 2020; 471: 88-102. doi: 10.1016/j.canlet.2019.11.039
66. Bruni L, Saura-Lázaro A, Montoliu A, Brotons M, Alemany L, Diallo MS, et al. HPV vaccination introduction worldwide and WHO and UNICEF estimates of national HPV immunization coverage 2010–2019. Prev Med. 2021; 144: 106399. doi: 10.1016/j.ypmed.2020.106399
67. Tsu VD, LaMontagne DS, Atuhebwe P, Bloem PN, Ndiaye C. National implementation of HPV vaccination programs in lowresource countries: Lessons, challenges, and future prospects. Prev Med. 2021; 144: 106335. doi: 10.1016/j.ypmed.2020.106335
68. Oyedeji O, Maples JM, Gregory S, Chamberlin SM, Gatwood JD, Wilson AQ, et al. Pharmacists’ perceived barriers to human papillomavirus (HPV) vaccination: A systematic literature review. Vaccines. 2021; 9(11): 1360. doi: 10.3390/vaccines9111360
69. Toh ZQ, Russell FM, Garland SM, Mulholland EK, Patton G, Licciardi PV. Human papillomavirus vaccination after COVID-19. JNCI Cancer Spectr. 2021; 5(2): pkab011. doi: 10.1093/jncics/pkab011
70. Coleman D, Day N, Douglas G, Farmery E, Lynge E, Philip J. European guidelines for quality assurance in cervical cancer screening. Europe against cancer programme. Part A. Eur J Cancer. 1993; 29: 298-299.
71. Chrysostomou AC, Stylianou DC, Constantinidou A, Kostrikis LG. Cervical cancer screening programs in Europe: The transition towards HPV vaccination and population-based HPV testing. Viruses. 2018; 10(12): 729. doi: 10.3390/v10120729
72. Cervical intraepithelial neoplasia, erosion and ectropion of the cervix: Clinical guidelines. 2022. (In Russ.).
73. Sroczynski G, Esteban E, Widschwendter A, Oberaigner W, Borena W, von Laer D, et al. Reducing overtreatment associated with overdiagnosis in cervical cancer screening – A model-based benefit-harm analysis for Austria. Int J Cancer. 2020; 147(4): 1131-1142. doi: 10.1002/ijc.32849
74. Jolidon V, De Prez V, Willems B, Bracke P, Cullati S, BurtonJeangros C. Never and under cervical cancer screening in Switzerland and Belgium: Trends and inequalities. BMC Public Health. 2020; 20(1): 1-11. doi: 10.1186/s12889-020-09619-z
75. Altova A, Kulhánová I, Bruha L, Lustigova M. Breast and cervical cancer screening attendance among Czech women. Cent Eur J Public Health. 2021; 29(2): 90-95. doi: 10.21101/cejph.a6623
76. Pedersen K, Fogelberg S, Thamsborg LH, Clements M, Nygård M, Kristiansen IS, et al. An overview of cervical cancer epidemiology and prevention in Scandinavia. Acta Obstet GynecolScand. 2018; 97(7): 795-807. doi: 10.1111/aogs.13313
77. Ojamaa K, Innos K, Baburin A, Everaus H, Veerus P. Trends in cervical cancer incidence and survival in Estonia from 1995 to 2014. BMC Cancer. 2018; 18(1): 1-9. doi: 10.1186/s12885-018-5006-1
78. De Rycke Y, Tubach F, Lafourcade A, Guillo S, Dalichampt M, Dahlab A, et al. Cervical cancer screening coverage, management of squamous intraepithelial lesions and related costs in France. PloS One. 2020; 15(2): e0228660. doi: 10.1371/journal.pone.0228660
79. de Munter AC, Klooster TM, van Lier A, Akkermans R, de Melker HE, Ruijs WLM. Determinants of HPV-vaccination uptake and subgroups with a lower uptake in the Netherlands. BMC Public Health. 2021; 21(1): 1-13. doi: 10.1186/s12889-021-11897-0
80. Osowiecka K, Yahuza S, Szwiec M, Gwara A, Kasprzycka K, Godawska M, et al. Students’ knowledge about cervical cancer prevention in Poland. Medicina. 2021; 57(10): 1045. doi: 10.3390/medicina57101045
81. Kramer J. Eradicating cervical cancer: Lessons learned from Rwanda and Australia. Int J Gynecol Obstet. 2021; 154(2): 270-276. doi: 10.1002/ijgo.13601
82. Fernandes C, Alves J, Rodrigues A, Azevedo J. Group for the study of HPV vaccines. Epidemiological impact of the human papillomavirus vaccination program on genital warts in Portugal: A retrospective, chart review study. Vaccine. 2022; 40(2): 275-281. doi: 10.1016/j.vaccine.2021.11.070
83. Maver PJ, Poljak M. Primary HPV-based cervical cancer screening in Europe: Implementation status, challenges, and future plans. Clin Microbiol Infect. 2020; 26(5): 579-583. doi: 10.1016/j.cmi.2019.09.006
Review
For citations:
Kravtsova E.A., Tsyganov M.M., Litviakov N.V., Ibragimova M.K. HPV-associated cervical cancer: Current status and prospects. Acta Biomedica Scientifica. 2023;8(3):42-54. https://doi.org/10.29413/ABS.2023-8.3.4