Genotypic diversity, prevalence and epidemiological assessment of various variants of human papillomavirus coinfection in patients with dermatovenereological profile

vaccination and screening are the most effective methods for reducing cervical cancer incidence and mortality. With high immunization coverage, there is a potential for changes in the pattern of HPV types circulating in the population, increasing the risk of reduced effectiveness of vaccination programs. Studying genotypic diversity, the prevalence of coinfections, and the interactions of HPV genotypes in different populations is a complex task for determining the oncogenic potential of the pathogen and assessing the effectiveness of vaccination.

Study objective. To study the genotypic diversity and prevalence of highly oncogenic HPV types and to conduct an epidemiological assessment of coinfection patterns in patients at risk for sexually transmitted infections (STIs).

Materials and methods. From 2005 to 2024, 9,056 patients were examined, including 1,269 women without complaints or clinical manifestations of disease and 751 patients with STIs. They were tested for STIs and identified 12 HPV genotypes. Research methods included PCR, clinical, epidemiological, and statistical methods.

Results and discussion. The prevalence of HPV among patients with dermatovenereological profile was 28.4 %. The most common HPV types in patients at risk for STIs are both vaccine-relevant (HPV 16) and non-vaccine-relevant (HPV 31, 33, 35, 45, 56, 58) genotypes of the virus, which is important to consider when developing screening and prevention programs. The prevalence of HPV and STI coinfections was revealed in 74.7 % of cases, including 74.9 % in mycoureaplasmosis. Multiple HPV infection was detected in 15 % of cases, while the most frequent combinations of HPV VCR included genotypes 16, 31, 33, 35 and 56. Based on statistical analysis, competitive interactions are suggested between certain pairs of HPV genotypes.

1. Bray F., Laversanne M., Sung H., Ferlay J., Siegel R. L., 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; (3): 229–263. https://doi.org/10.3322/caac.21834

2. Torre L. A., Bray F., Siegel R. L., Ferlay J., Lortet-Tieulent J., Jemal A. Global cancer statistics, 2012. CA Cancer J Clin. 2015; (2): 87–108. https://doi.org/10.3322/caac.21262

3. Biernat-Sudolska M., Szostek S., Rojek-Zakrzewska D., Klimek M., Kosz-Vnenchak M. Concomitant infections with human papillomavirus and various mycoplasma and ureaplasma species in women with abnormal cervical cytology. Adv Med Sci. 2011; (2): 299–303. https://doi.org/10.2478/v10039-011-0028-9

4. Discacciati M. G., Gimenes F., Pennacchi P. C., Faiao-Flores F., Zeferino L. C., Derchain S. M., Teixeira J. C., Costa M. C., Zonta M., Termini L. et al. MMP-9/RECK Imbalance: a mechanism associated with high-grade cervical lesions and genital infection by human papillomavirus and Chlamydia trachomatis. Cancer Epidemiol Biomarkers Prev. 2015; (10): 1539–1547. https://doi.org/10.1158/1055–9965.EPI-15–0420

5. Tantengco O. A. G., Nakura Y., Yoshimura M., Nishiumi F., Llamas-Clark E. F., Yanagihara I. Co-infection of human papillomavirus and other sexually transmitted bacteria in cervical cancer patients in the Philippines. Gynecol Oncol Rep. 2022; (40): 100943. https://doi.org/10.1016/j.gore.2022.100943

6. Comar M., Monasta L., Seraceni S., Colli C., Luska V., Morassut S., Clemente L., Drabeni M., Moise G., Fontana F., Suligoi B. Chlamydia trachomatis and HPV co-infections in HIV negative men from a multi-ethnic area of Northern Italy at high prevalence of cervical malignancies. J Med Virol. 2017; (9): 1654–1661. https://doi.org/10.1002/jmv.24811

7. Feng R. M., Z Wang M., Smith J. S., Dong L., Chen F., Pan Q. J., Zhang X., Qiao Y. L., Zhao F. H. Risk of high-risk human papillomavirus infection and cervical precancerous lesions with past or current trichomonas infection: a pooled analysis of 25,054 women in rural China. J Clin Virol. 2018; (99–100): 84–90. https://doi.org/10.1016/j.jcv.2017.12.015

8. Al-Awadhi R., Al-Mutairi N., Albatineh A. N., Chehadeh W. Association of HPV genotypes with external anogenital warts: a cross sectional study. BMC Infect Dis. 2019; (1): 375. https://doi.org/10.1186/s12879-019-4005-4

9. Marsela E., Fischbeck A. J., Hildebrand J. A., Aoki R., French L. E., Wollenberg A., Schmoeckel E., Reinholz M. Coexistence of Oncogenic Human Papillomavirus Genotypes in Condylomata Acuminata among Children and Adolescents. Acta Derm Venereol. 2020; (4): adv00061. https://doi.org/10.2340/00015555–3407

10. Correa R. M., Baena A., Valls J., Colucci M. C., Mendoza L., Rol M., Wiesner C., Ferrera A., Fellner M. D., González J. V., Basiletti J. A., Mongelos P., Rodriguez de la Peña M., Saino A., Kasamatsu E., Velarde C., Macavilca N., Martinez S., Venegas G., Calderón A. et al. Distribution of human papillomavirus genotypes by severity of cervical lesions in HPV screened positive women from the ESTAMPA study in Latin America. PLoS One. 2022; (7): e0272205. https://doi.org/10.1371/journal.pone.0272205

11. de Sanjose S., Quint W. G., Alemany L., Geraets D. T., Klaustermeier J. E., Lloveras B. и др. Human papillomavirus genotype attribution in invasive cervical cancer: a retrospective cross-sectional worldwide study. Lancet Oncol. 2010; (11): 1048–1056. https://doi.org/10.1016/S1470–2045 (10) 70230-8

12. Guan P., Howell-Jones R., Bruni L., de Sanjose S., Franceschi S., Clifford G. M. Human papillomavirus types in 115,789 HPV-positive women: a meta-analysis from cervical infection to cancer. Int J Cancer. 2012; (10): 2349–2359. https://doi.org/10.1002/ijc.27485

13. Bruno M. T., Scalia G., Cassaro N., Boemi S. Multiple HPV 16 infection with two strains: a possible marker of neoplastic progression. BMC Cancer. 2020; (1): 444. https://doi.org/10.1186/s12885-020-06946-7

14. Zhao M., Zhou D., Zhang M., Kang P., Cui M., Zhu L., Luo L. Characteristic of persistent human papillomavirus infection in women worldwide: a meta-analysis. PeerJ. 2023; (11): e16247. https://doi.org/10.7717/peerj.16247

15. Na J., Li Y., Wang J., Wang X., Lu J., Han S. The correlation between multiple HPV infections and the occurrence, development, and prognosis of cervical cancer. Front Microbiol. 2023; (14): 1220522. https://doi.org/10.3389/fmicb.2023.1220522

16. Dillner J., Sparén P., Andrae B., Strander B. Cervical cancer has increased in Sweden in women who had a normal cell sample. Lakartidningen. 2018; (115): E 9FD.

17. NORDCAN, Association of Nordic Cancer Registries. In WHO IARC. 2022. Доступно по ссылке: https://nordcan.iarc.fr/en/dataviz/trends?cancers=190&sexes=1_2&populations=0&mode=-cancer&multiple_populations=0&multiple_cancers=1 (дата обращения: 28.11.2025)

18. CRUK Cervical Cancer Incidence Statistics. Доступно по ссылке: https://www.cancerresearchuk.org/health-professional/cancer-statistics/statistics-by-cancer-type/cervical-cancer/incidence#heading-Two (дата обращения: 28.11.2025).

19. Hampson I. N. Effects of the Prophylactic HPV Vaccines on HPV Type Prevalence and Cervical Pathology. Viruses. 2022; (4): 757. https://doi.org/10.3390/v14040757

20. Man I., Auranen K., Wallinga J., Bogaards J. A. Capturing multiple-type interactions into practical predictors of type replacement following human papillomavirus vaccination. Philos Trans R Soc Lond B Biol Sci. 2019; (1773): 20180298. https://doi.org/10.1098/rstb.2018.0298

21. Tota J. E., Struyf F., Merikukka M., Gonzalez P., Kreimer A. R., Bi D., Castellsagué X., de Carvalho N. S., Garland S. M., Harper D. M., Karkada N., Peters K., Pope W. A. J., Porras C., Quint W., Rodriguez A. C., Schiffman M., Schussler J., Skinner S. R., Teixeira J. C. et al. Evaluation of Type Replacement Following HPV16/18 Vaccination: Pooled Analysis of Two Randomized Trials. J Natl Cancer Inst. 2017; (7): djw300. https://doi.org/10.1093/jnci/djw300

22. Weinberger D. M., Malley R., Lipsitch M. Serotype replacement in disease after pneumococcal vaccination. Lancet. 2011; (9807): 1962–1973. https://doi.org/10.1016/S0140–6736(10)62225-8

23. Merikukka M., Kaasila M., Namujju P. B., Palmroth J., Kirnbauer R., Paavonen J., Surcel H. M., Lehtinen M. Differences in incidence and co-occurrence of vaccine and nonvaccine human papillomavirus types in Finnish population before human papillomavirus mass vaccination suggest competitive advantage for HPV33. Int J Cancer. 2011; (5): 1114–1119. https://doi.org/10.1002/ijc.25675

24. Tota J. E., Ramanakumar A. V., Jiang M., Dillner J., Walter S. D., Kaufman J. S., Coutlée F., Villa L. L., Franco E. L. Epidemiologic approaches to evaluating the potential for human papillomavirus type replacement postvaccination. Am J Epidemiol. 2013; (4): 625–634. https://doi.org/10.1093/aje/kwt018

25. Su Y., Zheng T., Bi Z., Jia X., Li Y., Kuang X., Yang Y., Chen Q., Lin H., Huang Y., Huang S., Qiao Y., Wu T., Zhang J., Xia N. Pattern of multiple human papillomavirus infection and type competition: An analysis in healthy Chinese women aged 18–45 years. Hum Vaccin Immunother. 2024; (1): 2334474. https://doi.org/10.1080/21645515.2024.2334474

26. Chen Y., Li Q., Du L., Du Z., Zhou Y., Huang Y., Zhang J., Wang W., Zhang L., Xie J., Xu C., Ge Y., Yao X., Zhou Y. Epidemiologic evaluation of human papillomavirus type competition in unvaccinated women from Xiamen, China. Front Microbiol. 2025; (16): 1546166. https://doi.org/10.3389/fmicb.2025.1546166

27. Man I., Wallinga J., Bogaards J. A. Inferring pathogen type interactions using cross-sectional prevalence data: opportunities and pitfalls for predicting type replacement. Epidemiology. 2018; (5): 666–674. https://doi.org/10.1097/EDE.0000000000000870

28. Dickson E. L., Vogel R. I., Bliss R. L., Downs L. S. Jr. Multiple-type human papillomavirus (HPV) infections: a cross-sectional analysis of the prevalence of specific types in 309,000 women referred for HPV testing at the time of cervical cytology. Int J Gynecol Cancer. 2013; (7): 1295–1302. https://doi.org/10.1097/IGC.0b013e31829e9fb4