Annals of the Russian academy of medical sciencesAnnals of the Russian academy of medical sciencesВестник Российской академии медицинских наук0869-60472414-3545"Paediatrician" Publishers LLC55010.15690/vramn.v70.i5.1444SCIENTIFIC REPORTSНАУЧНЫЕ СООБЩЕНИЯPhylodynamic of HCV PopulationsФилодинамика популяций вируса гепатита СKalininaO. V.КалининаО. В.
Russian Federation

доктор биологических наук, ведущий научный сотрудник лаборатории молекулярной микробиологии НИИ эпидемиологии и микробиологии им. Пастера Адрес: 197101, Санкт-Петербург, ул. Мира, д. 14, тел.: +7 (812) 233-21-49

olgakalinina@mail.ruZhebrunA. B.ЖебрунА. Б.
Russian Federation

доктор медицинских наук, профессор, член-корреспондент РАН, директор НИИ эпидемиологии и микробиологии им. Пастера Адрес: 197101, Санкт-Петербург, ул. Мира, д. 14

Saint-Petersburg Pasteur Institute, Saint-Petersburg, Russian FederationСанкт-Петербургский НИИ эпидемиологии и микробиологии им. Пастера, Санкт-Петербург, Российская Федерация031220157055735780312201503122015Copyright ©; 2015, "Paediatrician" Publishers LLCCopyright ©; 2015, Издательство "Педиатръ"2015"Paediatrician" Publishers LLCИздательство "Педиатръ"https://vestnikramn.spr-journal.ru/jour/about/submissionshttps://vestnikramn.spr-journal.ru/jour/article/view/550

Hepatitis C virus is an actual public health problem worldwide since its discovering in 1989. It is explained not only by the wide spreading andfrequent adverse outcomes of disease, the lack of effective preventive vaccine, but also by the high genetic variability of the virus. The current review summarizes the results of phylodynamic and phylogeographic studies of different HCV populations that allowed to characterize epidemic processes, to analyze the divergence of HCV into genotypes and subtypes, and to determine the geographic origin of the current HCV epidemic variants.

С момента открытия вируса гепатита С в 1989 г. он является актуальной проблемой здравоохранения во всем мире. Это связано не только с широким распространением инфекции, частыми неблагоприятными исходами заболевания, отсутствием эффективных профилактических вакцин, но также с высокой генетической изменчивостью вируса. В обзоре представлены результаты филодинамических и филогеографических исследований различных популяций вируса гепатита С, позволившие охарактеризовать развитие эпидемий, установить время дивергенции гено- / субтипов вируса, определить географическое происхождение его современных эпидемических вариантов.

hepatitis C virusphylodinamicevolutiongenotypesrecombinant formsвирус гепатита Сфилодинамикаэволюциягенотипырекомбинантные формы1. Simmonds P., Bukh J., Combet C., Deléage G., Enomoto N., Feinstone S., Halfon P., Inchauspé G., Kuiken C., Maertens G., Mizokami M., Murphy D.G., Okamoto H., Pawlotsky J.M., Penin F., Sablon E., Shin I.T., Stuyver L.J., Thiel H.J., Viazov S., Weiner A.J., Widell A. Consensus proposals for a unified system of nomenclature of hepatitis C virus genotypes. Hepatology. 2005; 42(4): 962–973.2. Smith D.B., Bukh J., Kuiken C., Muerhoff A.S., Rice C.M., Stapleton J.T., Simmonds P. Expanded classification of hepatitis C virus into 7 genotypes and 67 subtypes: updated criteria and genotype assignment WEB resource. Hepatology. 2014; 59 (1): 318–327.3. Pybus O.G., Charleston M.A., Gupta S., Rambaut A., Holmes E.C., Harvey P.H. The epidemic behavior of the hepatitis C virus. Science. 2001; 292 (5525): 2323–2325.4. Pybus O.G., Markov P.V., Wu A., Tatem A.J. Investigating the endemic transmission of the hepatitis C virus. Int. J. Parasitol. 2007;37 (8): 839–849.5. Magiorkinis G., Magiorkinis E., Paraskevis D., Ho S.Y., Shapiro B., Pybus O.G., Allain J.P., Hatzakis A. The Global Spread of Hepatitis C Virus 1a and 1b: A Phylodynamic and Phylogeographic Analysis. PLoS Med. 2009; 6 (12): 1000198.6. Goedert J., Chen B., Preiss L., Aledort L.M., Rosenberg P.S. Reconstruction of the hepatitis C virus epidemic in the US haemophilia population, 1940–1990. Am. J. Epidemiol. 2007; 165 (12):1443–1453.7. Freeman A.J., Zekry A., Whybin L.R., Harvey C.E., van Beek I.A., de Kantzow S.L., Rawlinson W.D., Boughton C.R., Robertson P.W., Marinos G., Lloyd A.R. Hepatitis C prevalence among Australian injecting drug users in the 1970s and profiles of virus genotypes in the 1970s and 1990s. Med. J. Aust. 2000; 172 (12): 588–591.8. Pybus O.G., Holmes E.C., Simmonds P. The hepatitis C virus epidemic among injecting drug users. Infect. Genet. Evol. 2005; 5 (2): 131–139.9. Ciccozzi M., Ciccaglione A.R., Presti A.Lo, Yalcinkaya T., Taskan Z.P., Equestre M., Costantino A., Bruni R., Ebranati E., Salemi M., Gray R., Rezza G., Galli M., Zehender G. Reconstruction of the evolutionary dynamics of the hepatitis C virus 1b epidemic in Turkey. Infect. Genet. Evol. 2011; 11 (5): 863–868.10. Li C., Njouom R., Pépin J., Nakano T., Bennett P., Pybus O.G., Lu L. Characterization of full-length hepatitis C virus sequences for subtypes 1e, 1h and 1l, and a novel variant revealed Cameroon as an area in origin for genotype 1. J. Gen. Virol. 2013; 94 (Pt. 8): 1780–1790.11. Markov P.V., van de Laar T.J., Thomas X.V., Aronson S.J., Weegink C.J., van den Berk G.E., Prins M., Pybus O.G., Schinkel J. Colonial history and contemporary transmission shape the genetic diversity of hepatitis C virus genotype 2 in Amsterdam. J. Virol. 2012; 86 (14): 7677–7687.12. Li C., Cao H., Lu L., Murphy D. Full-length sequences of 11 hepatitis C virus genotype 2 isolates representing five subtypes and six unclassified lineages with unique geographical distributions and genetic variation patterns. J. Gen. Virol. 2012; 93 (6): 1173–1184.13. Pouillot R., Lachenal G., Pybus O.G., Rousset D., Njouom R. Variable epidemic histories of hepatitis C virus genotype 2 infection in West Africa and Cameroon. Infect. Genet. Evol. 2008; 8 (5):676–681.14. Thomas F., Nicot F., Sandres-Sauné K., Dubois M., Legrand-Abravanel F., Alric L., Peron J.M., Pasquier C., Izopet J. Genetic diversity of HCV genotype 2 strains in south western France. J. Med. Virol. 2007; 79 (1): 26–34.15. Cantaloube J.F., Gallian P., Laperche S., Elghouzzi M.H., Piquet Y., Bouchardeau F., Jordier F., Biagini P., Attoui H., de Micco P. Molecular characterization of genotype 2 and 4 hepatitis C virus isolates in French blood donors. J. Med. Virol. 2008; 80 (10): 1732–1739.16. Choudhary M.C., Natarajan V., Pandey P., Gupta E., Sharma S., Tripathi R., Kumar M.S., Kazim S.N., Sarin S.K. Identification of Indian sub-continent as hotspot for HCV genotype 3a origin by Bayesian evolutionary reconstruction. Infect. Genet. Evol. 2014; 28: 87–94.17. Akkarathamrongsin S., Hacharoen P., Tangkijvanich P., Theamboonlers A., Tanaka Y., Mizokami M., Poovorawan Y. Molecular epidemiology and genetic history of hepatitis C virus subtype 3a infection in Thailand. Intervirology. 2013; 56 (5): 284–294.18. Li C., Lu L., Murphy D.G., Negro F., Okamoto H. Origin of hepatitis C virus genotype 3 in Africa as estimated through an evolutionary analysis of the full length genomes of nine subtypes, including the newly sequenced 3d and 3e. J. Gen. Virol. 2014; 95(Pt.8): 1677– 1688.19. Lu L., Murphy D., Li C., Xia X., Pham P.H., Jin Y., Hagedorn C.H., Abe K. Complete genomes of three subtype 6t isolates and analysis of many novel hepatitis C virus variants within genotype 6. J. Gen. Virol. 2008; 89 (2): 444–452.20. Pybus O.G., Barnes E., Taggart R., Lemey P., Markov P.V., Rasachak B., Syhavong B., Phetsouvanah R., Sheridan I., Humphreys I.S., Lu L., Newton P.N., Klenerman P. Genetic history of hepatitis C virus in East Asia. J. Virol. 2009; 83 (2): 1071–1082.21. Verbeeck J., Maes P., Lemey P., Pybus O.G., Wollants E., Song E., Nevens F., Fevery J., Delport W., Van der Merwe S., Van Ranst M. Investigating the origin and spread of hepatitis C virus genotype 5a. J. Virol. 2006; 80 (9): 4220–4226.22. Njouom R., Frost E., Deslandes S., Mamadou-Yaya F., Labbé A.C., Pouillot R., Mbélesso P., Mbadingai S., Rousset D., Pépin J. Predominance of hepatitis C virus genotype 4 infection and rapid transmission between 1935 and 1965 in the Central African Republic. J. Gen. Virol. 2009; 90 (Pt. 10): 2452–2456.23. Njouom R., Caron M., Besson G., Ndong-Atome G.R., Makuwa M., Pouillot R., Nkoghé D., Leroy E., Kazanji M. Phylogeography, risk factors and genetic history of hepatitis C virus in Gabon, central Africa. PLoS One. 2012; 7 (8): 42002.24. Njouom R., Nerrienet E., Dubois M., Lachenal G., Rousset D., Vessière A., Ayouba A., Pasquier C., Pouillot R. The hepatitis C virus epidemic in Cameroon: genetic evidence for rapid transmission between 1920 and 1960. Infect. Genet. Evol. 2007; 7 (3): 361–367.25. Cantaloube J., Gallian P., Bokilo A., Jordier F., Biagini P., Attoui H., Chiaroni J., de Micco P. Analysis of hepatitis C virus strains circulating in Republic of the Congo. J. Med. Virol. 2010; 82 (4): 562–567.26. Tanaka Y., Agha S., Saudy N., Kurbanov F., Orito E., Kato T., Abo-Zeid M., Khalaf M., Miyakawa Y., Mizokami M. Exponential spread of hepatitis C virus genotype 4a in Egypt. J. Mol. Evol. 2004;58 (2): 191–195.27. Mizokami M., Tanaka Y. Tracing the evolution of hepatitis C virus in the United States, Japan, and Egypt by using the molecular clock. Clin. Gastroenterol. Hepatol. 2005; 3 (10): 82–85.28. Henquell C., Guglielmini J., Verbeeck J., Mahul A., Thibault V., Lebray P., Laperche S., Trimoulet P., Foucher J., Le Guillou-Guillemette H., Fouchard-Hubert I., Legrand-Abravanel F., Métivier S., Gaudy C., D’Alteroche L., Rosenberg A.R., Podevin P., Plantier J.C., Riachi G., Saoudin H., Coppere H., André E., Gournay J., Feray C., Vallet S., Nousbaum J.B., Baazia Y., Roulot D., Alain S., Loustaud-Ratti V., Schvoerer E., Habersetzer F., Pérez- Serra R.J., Gourari S., Mirand A., Odent-Malaure H., Garraud O., Izopet J., Bommelaer G., Peigue-Lafeuille H., van Ranst M., Abergel A., Bailly J.L. Evolutionary history of hepatitis C virus genotype 5a in France, a multicenter ANRS study. Infect. Genet. Evol. 2011;11 (2): 496–503.29. Pybus O.G., Barnes E., Taggart R., Lemey P., Markov P.V., Rasachak B., Syhavong B., Phetsouvanah R., Sheridan I., Humphreys I.S., Lu L., Newton P.N., Klenerman P. Genetic history of hepatitis C virus in East Asia. J. Virol. 2009; 83 (2): 1071–1082.30. Kalinina O., Norder H., Mukomolov S., Magnius L.O. A natural intergenotypic recombinant of hepatitis C virus identified in St. Petersburg. J. Virol. 2002; 76 (8): 4034–4043.31. Tallo T., Norder H., Tefanova V., Krispin T., Schmidt J., Ilmoja M., Orgulas K., Pruunsild K., Priimägi L., Magnius L.O. Genetic characterization of hepatitis C virus strains in Estonia: fluctuations in the predominating subtype with time. J. Med. Virol. 2007; 79 (4): 374–382.32. Samokhvalov E.I., Nikolaeva L.I., Al'khovskii S.V., Khlopova I.N., Makashova V.V., Petrova E.V., Sapronov G.V., Belyaeva N.M., L'vov D.K. Frequency of Detection of Different Hepatitis C Virus Subtypes in the Moscow Region. Voprosy virusologii = Problems of Virology. 2013;58(1):36–40.33. Chub E.V., Kochneva G.V., Granitov V.M., Netesov S.V. Recombinants of hepatitis C virus type 2k/1b in the population of the Altai region. Infektsionnye bolezni = Infectious diseases. 2007;5(4):5–11.34. Raghwani J., Thomas X.V., Koekkoek S.M., Schinkel J., Molenkamp R., van de Laar T.J., Takebe Y., Tanaka Y., Mizokami M., Rambaut A., Pybus O.G. Origin and evolution of the unique hepatitis C virus circulating recombinant form 2k/1b. J. Virol. 2012; 86 (4): 2212–2220.35. Kalinina O.V. Genome organization and geographical distribution of the natural intergenotypic recombinant of hepatitis c virus rf1_2k/1b. Infektsiya i immunitet = Infection and immunity = Russian Journal of Infection and Immunity. 2012;2(4):677-686. DOI:10.15789/2220-7619-2012-4-677-68636. Newman R.M., Kuntzen T., Weiner B., Berical A., Charlebois P., Kuiken C., Murphy D.G., Simmonds P., Bennett P., Lennon N.J., Birren B.W., Zody M.C., Allen T.M., Henn M.R. Whole Genome Pyrosequencing of Rare Hepatitis C Virus Genotypes Enhances Subtype Classification and Identification of Naturally Occurring Drug Resistance Variants. J. Infect. Dis. 2013; 208 (1): 17–31. .37. Hedskog C., Doehle B., Chodavarapu K., Gontcharova V., Crespo Garcia J., De Knegt R., Drenth J.P., McHutchison J.G., Brainard D., Stamm L.M, Miller M.D., Svarovskaia E., Mo H.Characterization of hepatitis C virus intergenotypic recombinant strains and associated virological response to sofosbuvir/ribavirin. Hepatology. 2015; 61 (2): 471–480.38. Kageyama S., Agdamag D.M., Alesna E.T., Leaño P.S., Heredia A.M., Abellanosa-Tac-An I.P., Jereza L.D., Tanimoto T., Yamamura J., Ichimura H. A natural inter genotypic (2b/1b) recombinant of hepatitis C virus in the Philippines. J. Med. Virol. 2006; 78 (11): 1423–1428.39. Yokoyama K., Takahashi M., Nishizawa T., Nagashima S., Jirintai S., Yotsumoto S., Okamoto H., Momoi M.Y. Identification and characterization of a natural inter-genotypic (2b/1b) recombinant hepatitis C virus in Japan. Arch. Virol. J. 2011; 156: 1591–1601.40. Hoshino H., Hino K., Miyakawa H., Takahashi K., Akbar S.M., Mishiro S. Inter genotypic recombinant hepatitis C virus strains in Japan noted by discrepancies between immunoassay and sequencing. J. Med. Virol. 2012; 1024: 1018–1024.41. Smith D.B., Pathirana S., Davidson F., Lawlor E., Power J., Yap P.L., Simmonds P. The origin of hepatitis C virus genotypes. J. Gen. Virol. 1997; 78 (2): 321–328.42. Simmonds P. Genetic diversity and evolution of hepatitis C virus 15 years on. J. Gen. Virol. 2004; 85 (11): 3173–3188.43. Lu L., Li C., Xu Y., Murphy D.G. Full-length genomes of 16 hepatitis C virus genotype 1 isolates representing subtypes 1c, 1d, 1e, 1g, 1h, 1i, 1j and 1k, and two new subtypes 1m and 1n, and four unclassified variants reveal ancestral relationships among subtypes. J. Gen. Virol. 2014, 95 (7): 1479–1487.