Genomic surveillance of HIV infection in the Russian Federation

Over the past 30 years, the amount of sequencing data has increased significantly, including for human immunodeficiency virus type 1 (HIV-1). Significant developments have also occurred in the field of bioinformatics. Because of this, first in science and then in practical healthcare, a new field has emerged — genomic surveillance. Currently, the possibilities of using bioinformatics methods are practically not described in Russian regulatory documents. This review outlines the main applications of genomic surveillance of HIV infection: analysis of HIV-1 drug resistance, investigation of HIV transmission, study of the characteristics of HIV occurrence and spread, assessment of the effectiveness of HIV prevention interventions, retrospective and operational analysis of the dynamics and structure of morbidity, and forecasting the development of the epidemic process. The review presents successful examples of domestic and international research, and makes proposals for the introduction of bioinformatics methods into the Russian system of epidemiological surveillance of HIV infection.

1. World Health Organization. HIV statistics, globally and by WHO region, 2023. Epidemiological fact sheet. https://cdn.who.int/media/docs/default-source/hq-hiv-hepatitis-and-stis-library/j0294-who-hiv-epi-factsheet-v7.pdf.

2. Sokolova E.V., Ladnaya N.N., Pokrovsky V.V., Kravchenko A.V., Kozyrina N.V., Yurin O.G., Chekryzhova D.G. The influence of antiretroviral therapy on the development of the HIV epidemic in the Russian Federation. Epidemiology and Infectious Diseases. Current Items, 2023, Vol. 13, No. 3, pp. 20–26 (In Russ.)]. doi: 10.18565/epidem.2023.13.3.20-6.

3. Pokrovsky V.V., Ladnaya N.N., Sokolova E.V. HIV infection. Information Bulletin No. 47. Moscow: Specialized Research Department for the Prevention and Control of AIDS of the Central Research Institute of Epidemiology of Rospotrebnadzor, 2023 (In Russ.)].

4. Kirichenko A., Kireev D., Lapovok I. et al. Prevalence of Pretreatment HIV-1 Drug Resistance in Armenia in 2017–2018 and 2020–2021 following a WHO Survey // Viruses. 2022. Vol. 14, No. 11. Р. 2320. doi: 10.3390/v14112320.

5. World Health Organization. Global genomic surveillance strategy for pathogens with pandemic and epidemic potential, 2022–2032. Geneva, 2022. https://www.who.int/publications/i/item/9789240046979.

6. Akimkin V.G., Semenenko T.A., Khafizov K.F. et al. Genomic surveillance strategy. Journal of microbiology, epidemiology and immunobiology, 2024, Vol. 101, No. 2, pp. 163– 172 (In Russ.)]. doi: 10.36233/0372-9311-507.

7. Poon A.F., Gustafson R., Daly P. et al. Near real-time monitoring of HIV transmission hotspots from routine HIV genotyping: an implementation case study // Lancet HIV. 2016. Vol. 3, No. 5. Р. e231–e238. doi: 10.1016/S2352–3018(16)00046-1.

8. Howison M., Gillani F.S., Novitsky V. et al. An Automated Bioinformatics Pipeline Informing Near-Real-Time Public Health Responses to New HIV Diagnoses in a Statewide HIV Epidemic // Viruses. 2023. Vol. 15, No. 3. Р. 737. doi: 10.3390/v15030737.

9. Hanke K., Rykalina V., Koppe U. et al. Developing a next level integrated genomic surveillance: Advances in the molecular epidemiology of HIV in Germany // International journal of medical microbiology, 2024. Vol. 314, No. 151606. doi: 10.1016/j.ijmm.2024.151606.

10. Guidelines MU 3.1.3342-16 «Epidemiological surveillance of HIV infection». Moscow, 2016 (In Russ.)].

11. Larder B.A., Darby G., Richman D.D. HIV with reduced sensitivity to zidovudine (AZT) isolated during prolonged therapy // Science. 1989. Vol. 243, No. 4899. Р. 1731–1734. doi: 10.1126/science.2467383.

12. World Health Organization. HIV drug resistance: brief report 2024. Geneva, 2024. https://www.who.int/publications/i/item/9789240086319.

13. Lazzari S., de Felici A., Sobel H., Bertagnolio S. HIV drug resistance surveillance: summary of an April 2003 WHO consultation // AIDS. 2004. Vol. 18. Р. S49–S53. doi: 10.1097/00002030-200406003-00010.

14. World Health Organization. HIV drug resistance strategy, 2021 update. Geneva, 2021.

15. Methodological recommendations MP 3.1.5.0075/1-13. 3.1.5. «Epidemiology. Prevention of infectious diseases. HIV infections. Surveillance of the spread of HIV strains resistant to antiretroviral drugs». Moscow, 2013 (In Russ.)].

16. Wertheim J.O., Kosakovsky Pond S.L., Forgione L.A. et al. Social and Genetic Networks of HIV-1 Transmission in New York City // PLoS pathogens. 2017. Vol. 13, No. 1. Р. e1006000. doi: 10.1371/journal.ppat.1006000.

17. Balfe P., Simmonds P., Ludlam C.A. et al. Concurrent evolution of human immunodeficiency virus type 1 in patients infected from the same source: rate of sequence change and low frequency of inactivating mutations // Journal of virology. 1990. Vol. 64, No. 12. Р. 6221–6233. doi: 10.1128/JVI.64.12.6221-6233.1990.

18. Ou C.Y., Ciesielski C.A., Myers G. et al. Molecular epidemiology of HIV transmission in a dental practice // Science. 1992. Vol. 256, No. 5060. Р. 1165–1171. doi: 10.1126/science.256.5060.1165.

19. Bernard E.J., Azad Y., Vandamme A.M. et al. HIV forensics: pitfalls and acceptable standards in the use of phylogenetic analysis as evidence in criminal investigations of HIV transmission // HIV medicine. 2007. Vol. 8, No. 6. Р. 382–387. doi: 10.1111/j.1468-1293.2007.00486.x.

20. Sandyreva T.P., Gerasimova N.A., Lopatukhin A.E. et al. Phylogenetic analysis in epidemiological investigations of cases of HIV infection. Epidemiology and infectious diseases, 2014, Vol. 19, No. 1, pp. 17–21 (In Russ.)].

21. Санитарно-эпидемиологические правила СП 3.1.5.2826–10 «Профилактика ВИЧ-инфекции». М., 2011.

22. Abecasis A.B., Pingarilho M., Vandamme A.M. Phylogenetic analysis as a forensic tool in HIV transmission investigations // AIDS. 2018. Vol. 32, No. 5. Р. 543–554. doi: 10.1097/QAD.0000000000001728.

23. Wymant C., Hall M., Ratmann O. et al. STOP-HCV Consortium, The Maela Pneumococcal Collaboration, The BEEHIVE Collaboration. PHY-LOSCANNER: Inferring Transmission from Within- and Between-Host Pathogen Genetic Diversity // Molecular biology and evolution. 2018. Vol. 35, No. 3. Р. 719–733. doi: 10.1093/molbev/msx304.

24. Shimotohno K., Golde D.W., Miwa M. et al. Nucleotide sequence analysis of the long terminal repeat of human T-cell leukemia virus type II // Proceedings of the National Academy of Sciences of the United States of America. 1984. Vol. 81, No. 4. Р. 1079–1083. doi: 10.1073/pnas.81.4.1079.

25. Ratner L., Haseltine W., Patarca R. et al. Complete nucleotide sequence of the AIDS virus, HTLV-III // Nature. 1985. Vol. 313, No. 6000. Р. 277–284. doi: 10.1038/313277a0.

26. Abecasis A., Vandamme A.M. Origin and Distribution of HIV-1 Subtypes // Encyclopedia of AIDS. N.Y.: Springer, 2015. doi: 10.1007/978-14614-9610-6_130-2.

27. Lapovok I.A., Lopatukhin A.E., Kireev D.E. et al. Molecular epidemiological analysis of HIV-1 variants circulating in Russia in 1987–2015, Ter. Arkh., 2017, Vol. 89, No. 11, рр. 44–49 (In Russ.)]. doi: 10.17116/terarkh2017891144-49.

28. Baryshev P.B., Bogachev V.V., Gashnikova N.M. HIV-1 genetic diversity in Russia: CRF63_02A1, a new HIV type 1 genetic variant spreading in Siberia // AIDS research and human retroviruses. 2014. Vol. 30, No. 6. Р. 592–597. doi: 10.1089/aid.2013.0196.

29. Sivay M.V., Ekushov V.E., Zyryanova D.P. et al. Reconstruction of the epidemic caused by CRF63_02A HIV-1. Molecular diagnostics and biosafety 2022: collection of materials from the congress with international participation, Moscow, April 27–28, 2022. Moscow: FBUN Central Research Institute of Epidemiology of Rospotrebnadzor, 2022. P. 107 (In Russ.)].

30. Murzakova A., Kireev D., Baryshev P. et al. Molecular Epidemiology of HIV-1 Subtype G in the Russian Federation // Viruses. 2019. Vol. 11, No. 4. Р. 348. doi: 10.3390/v11040348.

31. Akimkin V.G., Khafizov K.F., Dubodelov D.V. et al. Molecular Genetic Monitoring and Digital Transformation Technologies in Modern Epidemiology. Annals of the Russian academy of medical sciences, 2023, Vol. 78, No. 4, рр. 363–369 (In Russ.)]. doi: 10.15690/vramn13672.

32. Kuleshov K.V., Vodop’ianov S.O., Dedkov V.G. et al. Travel-Associated Vibrio cholerae O1 El Tor, Russia // Emerging infectious diseases. 2016. Vol. 22, No. 11. Р. 2006–2008. doi: 10.3201/eid2211.151727.

33. Kuleshov K.V., Pavlova A.S., Egorova A.E. et al. Phylogenomic analysis of Salmonella enterica subsp. isolates. enterica serovar Enteritidis associated with sporadic and group morbidity in Russia. Epidemiology and Infectious Diseases. Current Items, 2023, Vol. 13, No. 2, рр. 76–82 (In Russ.)]. doi: 10.18565/epidem.2023.13.2.76-82.

34. Kireev D.E., Kirichenko A.A., Osadchaya O.A. et al. Connectivity of HIV epidemics in the republic of Armenia and the Russian Federation. Epidemiology and Infectious Diseases. Current Items, 2023. Vol. 13, No. 3, рр. 27–34 (In Russ.)]. doi: 10.18565/epidem.2023.13.3.27-34.

35. Worobey M., Watts T.D., McKay R.A. et al. 1970s and ‚Patient 0’ HIV-1 genomes illuminate early HIV/AIDS history in North America // Nature. 2016. Vol. 539, No. 7627. Р. 98–101. doi: 10.1038/nature19827.

36. Díez-Fuertes F., Cabello M., Thomson M.M. Bayesian phylogeographic analyses clarify the origin of the HIV-1 subtype A variant circulating in former Soviet Union’s countries. Infection, genetics and evolution // Infect. Genet Evol. 2015. Vol. 33, Р. 197–205. doi: 10.1016/j.meegid.2015.05.003

37. Paraskevis D., Pybus O., Magiorkinis G. et al. SPREAD Programme. Tracing the HIV-1 subtype B mobility in Europe: a phylogeographic approach // Retrovirology. 2009. Vol. 6, No. 49. doi: 10.1186/1742-4690-6-49.

38. Du L., Wu J., Qian P. et al. Phylogeographical Analysis Reveals Distinct Sources of HIV-1 and HCV Transmitted to Former Blood Donors in China // AIDS research and human retroviruses. 2017. Vol. 33, No. 3. Р. 284–289. doi: 10.1089/AID.2016.0147.

39. Lai A., Bozzi G., Franzetti M. et al. HIV-1 A1 Subtype Epidemic in Italy Originated from Africa and Eastern Europe and Shows a High Frequency of Transmission Chains Involving Intravenous Drug Users // PloS One. 2016. Vol. 11, No. 1. Р. e0146097. doi: 10.1371/journal.pone.0146097.

40. Phillips A.N., Sabin C., Pillay D., Lundgren J.D. HIV in the UK 1980–2006: reconstruction using a model of HIV infection and the effect of anti-retroviral therapy // HIV medicine. 2007. Vol. 8, No. 8. Р. 536–546. doi: 10.1111/j.1468–1293.2007.00507.x.

41. Volz E.M., Kosakovsky Pond S.L., Ward M.J. et al. Phylodynamics of infectious disease epidemics // Genetics. 2009. Vol. 183, No. 4. Р. 1421– 1430. doi: 10.1534/genetics.109.106021.

42. Dennis A. M., Hué S., Billock R. et al. Human Immunodeficiency Virus Type 1 Phylodynamics to Detect and Characterize Active Transmission Clusters in North Carolina // The Journal of infectious diseases. 2020. Vol. 221, No. 8, Р. 1321–1330. doi: 10.1093/infdis/jiz176.

43. Jovanović L., Šiljić, M., Ćirković V. et al. Exploring Evolutionary and Transmission Dynamics of HIV Epidemic in Serbia: Bridging Socio-Demographic With Phylogenetic Approach // Frontiers in microbiology. 2019. Vol. 10, No. 287. doi: 10.3389/fmicb.2019.00287.

44. Volz E.M., Ionides E., Romero-Severson E.O. et al. HIV-1 transmission during early infection in men who have sex with men: a phylodynamic analysis // PLoS medicine. 2013. Vol. 10, No. 12. Р. e1001568. doi: 10.1371/journal.pmed.1001568.

45. Novitsky V., Kühnert D., Moyo S. et al. Phylodynamic analysis of HIV sub-epidemics in Mochudi, Botswana // Epidemics. 2015. Vol. 13. Р. 44–55. doi: 10.1016/j.epidem.2015.07.002.

46. Stadler T., Kouyos R., von Wyl V. et al. Swiss HIV Cohort Study. Estimating the basic reproductive number from viral sequence data // Molecular biology and evolution. 2012. Vol. 29, No. 1. Р. 347–357. doi: 10.1093/molbev/msr217.

47. Gray R.R., Tatem A.J., Lamers S. et al. Spatial phylodynamics of HIV-1 epidemic emergence in east Africa // AIDS. 2009. Vol. 23, No. 14. Р. F9– F17. doi: 10.1097/QAD.0b013e32832faf61.

48. Skar H., Axelsson M., Berggren I. et al. Dynamics of two separate but linked HIV-1 CRF01_AE outbreaks among injection drug users in Stockholm, Sweden, and Helsinki, Finland // Journal of virology, 2011. Vol. 85, No. 1. Р. 510–518. doi: 10.1128/JVI.01413–10.

49. Peters P.J., Pontones P., Hoover K.W. et al. Indiana HIV Outbreak Investigation Team. HIV Infection Linked to Injection Use of Oxymorphone in Indiana, 2014–2015 // The New England journal of medicine. 2016. Vol. 375, No. 3. Р. 229–239. doi: 10.1056/NEJMoa1515195.

50. Golden M.R., Lechtenberg R., Glick S.N. et al. Outbreak of Human Immunodeficiency Virus Infection Among Heterosexual Persons Who Are Living Homeless and Inject Drugs — Seattle, Washington, 2018 // MMWR. Morbidity and mortality weekly report. 2019. Vol. 68, No. 15. Р. 344–349. doi: 10.15585/mmwr.mm6815a2.

51. Alpren C., Dawson E. L., John B. et al. Opioid Use Fueling HIV Transmission in an Urban Setting: An Outbreak of HIV Infection Among People Who Inject Drugs-Massachusetts, 2015–2018 // American journal of public health. 2020. Vol. 110, No. 1. Р. 37–44. doi: 10.2105/AJPH.2019.305366.

52. Tookes H., Bartholomew T.S., Geary S. et al. Rapid Identification and Investigation of an HIV Risk Network Among People Who Inject Drugs-Miami, FL, 2018 // AIDS and behavior, 2020. Vol. 24, No. 1. Р. 246–256. doi: 10.1007/s10461-019-02680-9.

53. Metcalfe R., Ragonnet-Cronin M., Bradley-Stewart A. et al. From hospital to the community: redesigning the human immunodeficiency virus (HIV) clinical service model to respond to an outbreak of HIV among people who inject drugs // The Journal of infectious diseases. 2020. Vol. 222. Р. S410–S419. doi: 10.1093/infdis/jiaa336.

54. Bavinton B.R., Jin F., Prestage G. et al.; Opposites Attract Study Group. The Opposites Attract Study of viral load, HIV treatment and HIV transmission in serodiscordant homosexual male couples: design and methods // BMC public health. 2014. Vol. 14, No. 917. doi: 10.1186/1471-2458-14-917.

55. Cohen M. S., Chen Y. Q., McCauley M. et al.; HPTN 052 Study Team. Antiretroviral Therapy for the Prevention of HIV-1 Transmission // The New England journal of medicine. 2016. Vol. 375, No. 9. Р. 830–839. doi: 10.1056/NEJMoa1600693.

56. Rodger A.J., Cambiano V., Bruun T. et al.; PARTNER Study Group. Risk of HIV transmission through condomless sex in serodifferent gay couples with the HIV-positive partner taking suppressive antiretroviral therapy (PARTNER): final results of a multicentre, prospective, observational study // Lancet. 2019. Vol. 393, No. 10189. Р. 2428–2438. doi: 10.1016/S0140-6736(19)30418-0.

57. EACS Guidelines version 12.0, October 2023

58. CDC. Detecting and responding to HIV transmission clusters. A guide for health departments. Draft version 2.0. June 2018.

59. Lou J., Wu J., Chen L., Ruan Y., Shao Y. A sex-role-preference model for HIV transmission among men who have sex with men in China // BMC public health. 2009. Vol. 9, No. 1. Р. S10. doi: 10.1186/1471-2458-9-S1-S10.

60. Kwon Y. M., Yeun E. J., Kim H. Y., Youn M. S., Cho J. Y., Lee H. J. Application of the transtheoretical model to identify aspects influencing condom use among Korean college students // Western journal of nursing research. 2008. Vol. 30, No. 8. Р. 991–1004. doi: 10.1177/0193945908319988.

61. Wang Z., Zhang Z., Zhang C., Jin X., Wu J., Su B., Shen Y., Ruan Y., Xing H., Lou J. Trace the History of HIV and Predict Its Future through Genetic Sequences // Tropical medicine and infectious disease. 2022. Vol. 7, No. 8, Р. 190. doi: 10.3390/tropicalmed7080190.

62. Novitsky V., Moyo S., Le, Q., DeGruttola V., Essex M. Impact of sampling density on the extent of HIV clustering // AIDS research and human retroviruses. 2014. Vol. 30, No. 12. Р. 1226–1235. doi: 10.1089/aid.2014.0173.

63. Mazrouee S., Hallmark C. J., Mora R., Del Vecchio N., Carrasco Hernandez R., Carr M., McNeese M., Fujimoto K., Wertheim J. O. Impact of molecular sequence data completeness on HIV cluster detection and a network science approach to enhance detection // Scientific reports. 2022. Vol. 12, No. 1. Р. 19230. doi: 10.1038/s41598-022-21924-8.