MOLECULAR EPIDEMIOLOGY FEATURES OF HEPATITIS C VIRUS ISOLATES FROM DIFFERENT REGIONS OF THE REPUBLIC SAKHA (YAKUTIA)
- Authors: Semenov A.V.1, Ostankova J.V.2, Gerasimova V.V.3, Bichurina M.A.2, Kozlov A.V.4, Mukomolov S.L.2, Totolian A.A.5
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Affiliations:
- St. Petersburg Pasteur Institute, St. Petersburg, Russia Pavlov First St. Petersburg State Medical University, St. Petersburg, Russia North-West State Medical University n.a. I.I. Mechnikov, St. Petersburg, Russia
- St. Petersburg Pasteur Institute, St. Petersburg, Russia
- North-East Federal University n.a. M.K. Ammosov, Yakutsk, Russia
- North-West State Medical University n.a. I.I. Mechnikov, St. Petersburg, Russia
- St. Petersburg Pasteur Institute, St. Petersburg, Russia Pavlov First St. Petersburg State Medical University, St. Petersburg, Russia
- Issue: Vol 5, No 4 (2015)
- Pages: 359-372
- Section: ORIGINAL ARTICLES
- Submitted: 15.02.2016
- Accepted: 15.02.2016
- Published: 15.02.2016
- URL: https://iimmun.ru/iimm/article/view/353
- DOI: https://doi.org/10.15789/2220-7619-2015-4-359-372
- ID: 353
Cite item
Full Text
Abstract
According to WHO data about 3% of population are infected by hepatitic C virus (HCV) worldwide. Chronic hepatitis C is the leading cause of cirrhosis and hepatocellular carcinoma, thus it becoming one of the global public health problems. Clinical manifestations are varied and depend mainly of the virus biological properties and its interaction with the host immune system. Determination of virus genotype and subtype is important for a better understanding of the epidemiological and virological features of the disease. The prevalence genotypes hepatitis C virus is varies in different geographical regions of the world. The data about HCV genotypes distribution in some Russian Federation regions are very limited, especially about HCV genotypes prevalence in Siberia, Far East and some rural regions. One of such regions is Yakutia. In our study we identified genetic variants of HCV in chronic hepatitis C patients with moderate and high viral load from Yakutia by direct sequencing of HCV RNA NS5B region. Based on phylogenetic analysis we found the prevalent genotype 1 (88.3%), than genotype 2 (6.7%) and 3 (3.2%) among HCV patients with moderate and high viral load. Our results on the prevalence of subtype 1b are consistent with the data on the connection between this subtype with high levels of viremia, greater duration and severity of liver disease, as well as the development of chronic hepatits C in patients infected by HCV subtype 1b, compared with those infected with other subtypes of hepatitis virus C. The similarity of some Yakutian isolates with isolates from the United States, Brazil and Ireland was found. We discuss HCV subtype 2a isolates identified origin from isolates found in China. First in the territory of the Russian Federation HCV subtype 3g was identified, presumably imported from South Asia. Interconnected use of molecular, virological, demographic and epidemiological methods and information to monitor the infections will contribute to the understanding of the current HCV epidemiology in Russia.
About the authors
A. V. Semenov
St. Petersburg Pasteur Institute, St. Petersburg, RussiaPavlov First St. Petersburg State Medical University, St. Petersburg, Russia
North-West State Medical University n.a. I.I. Mechnikov, St. Petersburg, Russia
Email: fake@neicon.ru
PhD (Biology), Head of the Laboratory of Virology and Immunology HIV, St. Petersburg Pasteur Institute; Associate Professor, Pavlov First St. Petersburg State Medical University; Associate Professor, Department of Clinical Laboratory Diagnostics, North-West State Medical University named after I.I. Mechnikov, St. Petersburg, Russian Federation
РоссияJu. V. Ostankova
St. Petersburg Pasteur Institute, St. Petersburg, Russia
Author for correspondence.
Email: shenna1@yandex.ru
Researcher, Laboratory of Molecular Immunology and Seroepidemiology, St. Petersburg Pasteur Institute, St. Petersburg, Russian Federation
РоссияV. V. Gerasimova
North-East Federal University n.a. M.K. Ammosov, Yakutsk, Russia
Email: fake@neicon.ru
Researcher of the University Laboratory of Genome Medicine, Clinic of Medical Institute, Northeast Federal University named after M.K. Ammosov, Yakutsk, Russian Federation, Yakutsk, Russian Federation
РоссияM. A. Bichurina
St. Petersburg Pasteur Institute, St. Petersburg, Russia
Email: fake@neicon.ru
PhD, MD (Medicine), Head of the Laboratory of Etiology and Control of Viral Infections St. Petersburg Pasteur Institute, St. Petersburg, Russian Federation
РоссияA. V. Kozlov
North-West State Medical University n.a. I.I. Mechnikov, St. Petersburg, Russia
Email: fake@neicon.ru
PhD, MD (Medicine), Professor, Head of the Department of Clinical Laboratory Diagnostics North-West State Medical University named after I.I. Mechnikov, St. Petersburg, Russian Federation
РоссияS. L. Mukomolov
St. Petersburg Pasteur Institute, St. Petersburg, Russia
Email: fake@neicon.ru
PhD, MD (Medicine), Professor, Head of the Laboratory of Virus Hepatitis, St. Petersburg Pasteur Institute, St. Petersburg, Russian Federation
РоссияAreg A. Totolian
St. Petersburg Pasteur Institute, St. Petersburg, RussiaPavlov First St. Petersburg State Medical University, St. Petersburg, Russia
Email: fake@neicon.ru
Corresponding Member of RAS, PhD, MD (Medicine), Professor, Head of the Laboratory of Molecular Immunology and Seroepidemiology, St. Petersburg Pasteur Institute; Head of the Department of Immunology, Pavlov First St. Petersburg State Medical University, St. Petersburg, Russian Federation
РоссияReferences
- Вирусные гепатиты в Российской Федерации. Аналитический обзор. 9 выпуск / Под ред. Покровского В.И., Жебруна А.Б. СПб.: ФБУН НИИЭМ им. Пастера, 2013. 168 с. [Virusnye gepatity v Rossiiskoi Federatsii. Analiticheskii obzor. 9 vypusk. Pod red. Pokrovskogo V.I., Zhebruna A.B. [Viral hepatitis in the Russian Federation. Analytical review. 9th issue. Eds V.I. Pokrovskiy, A.B. Zhebrun]. St. Petersburg Pasteur Institute, 2013, 168 p.]
- О санитарно-эпидемиологической обстановке в Республике Саха (Якутия) в 2013 г.: Госуд. доклад. Якутск: Управление Роспотребнадзора по Республике Саха (Якутия). 2013. 282 c. [About sanitary and epidemiological situation in the Republic of Sakha (Yakutia) in 2013. Yakutsk: State report. Yakutsk Rospotrebnadzor for the Republic of Sakha (Yakutia). 2013, 282 p. (In Russ.)]
- Самохвалов Е.И., Николаева Л.И., Альховский С.В., Хлопова И.Н., Макашова В.В., Петрова Е.В., Сапронов Г.В., Беляева Н.М., Львов Д.К. Частота встречаемости отдельных субтипов вируса гепатита С в Московском регионе // Вопросы вирусологии. 2013. № 58 (1). С. 36–40. [Samokhvalov E.I., Nikolaeva L.I., Al’khovskii S.V., Khlopova V.V., Petrova E.V., Sapronov G.V., Beliaeva 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, vol. 58, no. 1, pp. 36–40. (In Russ.)]
- Семенов С.И., Терехова М.В., Индеева Л.Д., Павлов Н.Н., Тихонова Н.Н., Кузин С.Н., Писарева М.М., Грудинин М.П., Балахонцева Л.А., Серкина Т.П. Распространенность и генетическая характеристика вируса гепатита С в Якутии // Якутский медицинский журнал. 2009. № 2 (26). С. 129–132. [Semenov S.I., Terehova M.V., Indeeva L.D., Pavlov N.N., Tihonova N.N., Cusin S.N., Pisareva M.M., Grudinin M.P., Balahontseva L.A., Serkina T.P. Hepatitis C prevalence and genetic characteristic in Yakutia]. Yakutskii meditsinskii zhurnal = Yakut Medical Journal, 2009, vol. 2 no. 26, pp. 129–132. (In Russ.)]
- Степанова Г.И., Алексеева М.Н., Слепцова С.С. Клинические особенности хронического вирусного гепатита С в Республике (Саха) Якутия // Фундаментальные исследования. 2004. № 2. С. 97–98 [Stepanova G.I., Alekseeva M.N., Sleptsova S.S. Clinical features of chronic hepatitis C in the republic (Sakha) Yakutia]. Fundamental’nye issledovaniya = Basic Research, 2004, no. 2, pp. 97–98. (In Russ.)]
- Ahmed A.M., Hassan M.S., Abd-Elsayed A., Hassan H., Hasanain A.F., Helmy A. Insulin resistance, steatosis, and fibrosis in Egyptian patients with chronic hepatitis C virus infection. Saudi J. Gastroenterol., 2011, vol. 17 no. 4, pp. 245–251. doi: 10.4103/1319-3767.82578
- Ambrozaitis A., Agminas K.S., Balc I.G., Widell A. Hepatitis C in Lithuania: incidence, prevalence, risk factors and viral genotypes. Clin. Diagn. Virol., 1995, vol. 4 no. 4, pp. 273–284.
- Batash S., Khaykis I., Raicht R.F., Bini E.J. High prevalence of hepatitis C virus infection among immigrants from the former Soviet Union in the New York City metropolitan area: results of a community based screening program. Am. J. Gastroenterol., 2008, vol. 103, no. 4, pp. 922–927. doi: 10.1111/j.15720241.2008.01789.x
- Blatt L.M., Mutchnick M.G., Tong M.J., Klion F.M., Lebovics E., Freilich B., Bach N., Smith C., Herrera J., Tobias H., Conrad A., Schmid P., McHutchison J.G. Assessment of hepatitis C virus RNA and genotype from 6807 patients with chronic hepatitis C in the United States. J. Viral. Hepat., 2000, vol. 7, no. 3, pp. 196–202. doi: 10.1046/j.1365-2893.2000.00221.x
- Bracho M.A., Saludes V., Martró E., Bargalló A., González-Candelas F., Ausina V. Complete genome of a european hepatitis C virus subtype 1g isolate: phylogenetic and genetic analyses. Virol. J., 2008, vol. 5, pp. 72–79. doi: 10.1186/1743-422X-5-72
- Cavalheiro Nde P., De La Rosa A., Elagin S., Tengan F.M., Araújo E.S., Barone A.A. Hepatitis C: sexual or intrafamilial transmission? Epidemiological and phylogenetic analysis of hepatitis C virus in 24 infected couples. Rev. Soc. Bras. Med. Trop., 2009, vol. 42, no. 3, pp. 239–244.
- Chamberlain R.W., Adams N.J., Taylor L.A., Simmonds P., Elliott R.M. The complete coding sequence of hepatitis C virus genotype 5a, the predominant genotype in South Africa. Biochem. Biophys. Res. Commun., 1997, vol. 236, pp. 44–49.
- Chuang W.L., Yu M.L. Host factors determining the efficacy of hepatitis C treatment. J. Gastroenterol., 2013, vol. 48, no. 1, pp. 22–30. doi: 10.1007/s00535-012-0669-x
- Cramp M.E., Rosenberg W.M., Ryder S.D., Blach S., Parkes J. Modelling the impact of improving screening and treatment of chronic hepatitis C virus infection on future hepatocellular carcinoma rates and liverrelated mortality. BMC Gastroenterol., 2014, vol. 14, pp. 137–47. doi: 10.1186/1471-230X-14-137
- De Bruijne J., Schinkel J., Prins M., Koekkoek S.M., Aronson S.J., van Ballegooijen M.W., Reesink H.W., Molenkamp R., van de Laar T.J. Emergence of hepatitis C virus genotype 4: phylogenetic analysis reveals three distinct epidemiological profiles. J. Clin. Microbiol., 2009, vol. 47, no. 12, pp. 3832–3838. doi: 10.1128/JCM.01146-09
- Debojyoti B., Kheya M., Goutam C., Ranadeep G., Nabarun M., Mohua B. Correlation study between HCV genotypes distribution pattern and viral load in a tertiary care hospital in Kolkata, India. J. Clin. Diagn. Res., 2015, vol. 9 no. 5, pp. DC15–17. doi: 10.7860/JCDR/2015/12701.5977
- Demetriou V.L., Kostrikis L.G. Nearfull genome characterization of unclassified hepatitis C virus strains relating to genotypes 1 and 4. J. Med. Virol., 2011, vol. 83, pp. 2119–2127. doi: 10.1002/jmv.22237
- Dustin L.B., Rice C.M. Flying under the radar: the immunobiology of hepatitis C. Annu. Rev. Immunol., 2013, vol. 25, pp. 71–99.
- EASL clinical practice guidelines: management of hepatitis C virus infection. J. Hepatol., 2011, vol. 55, pp. 245–264. doi: 10.1016/j.jhep.2011.02.023
- Esmat G., Hashem M., El-Raziky M., El-Akel W., El-Naghy S., El-Koofy N. Risk factors for hepatitis C virus acquisition and predictors of persistence among Egyptian children. Liver Int., 2012, vol. 32, no. 3, pp. 449–456. doi: 10.1111/j.1478-3231.2011.02643.x
- Gededzha M.P., Selabe S.G., Kyaw T., Rakgole J.N., Blackard J.T., Mphahlele M.J. Introduction of new subtypes and variants of hepatitis C virus genotype 4 in South Africa. J. Med. Virol., 2012, vol. 84. no. 4, pp. 601–607. doi: 10.1002/jmv.23215
- Ghany M.G., Strader D.B., Thomas D.L., Seeff L.B., American association for the study of liver diseases. Diagnosis, management, and treatment of hepatitis C: an update. Hepatology, 2009, vol. 49, no. 4, pp. 1335–1374. doi: 10.1002/hep.22759
- Higgins D.G., Bleasby A.J., Fuchs R. CLUSTAL V: improved software for multiple sequence alignment. Comput. Appl. Biosci., 1992, vol. 8, no. 2, pp. 189–191.
- Karchava M., Waldenström J., Parker M., Hallack R., Sharvadze L., Gatserelia L., Chkhartishvili N., Dvali N., Dzigua L., Dolmazashvili E., Norder H., Tsertsvadze T. High incidence of the hepatitis C virus recombinant 2k/1b in Georgia: Recommendations for testing and treatment. Hepatol. Res., 2015. doi: 10.1111/hepr.12505
- Kavita S.L., Jyotsna A.J., Sandhya P.S., Badri N.T., Mohan Prasad V.G., Vidya A.A. Comparison of hepatitis C virus genotyping by 5 noncoding regionand corebased reverse transcriptase PCR assay with sequencing and use of the assay for determining subtype distribution in India. J. Clin. Microbiol., 2003, vol. 41, no. 11, pp. 5240–5244.
- Kuiken C., Combet C., Bukh J., Shin I., Deleage G., Mizokami M., Richardson R., Sablon E., Yusim K., Pawlotsky J.M., Simmonds P. A comprehensive system for consistent numbering of HCV sequences, proteins and epitopes. Hepatology, 2006, vol. 44, no. 5, pp. 1355–1361.
- Kuiken C., Simmonds P. Nomenclature and numbering of the hepatitis C virus. Methods. Mol. Biol., 2009, vol. 510, pp. 33–53. doi: 10.1007/978-1-59745-394-3_4
- Kurbanov F., Tanaka Y., Sugauchi F., Kato H., Ruzibakiev R., Zalyalieva M., Yunusova Z., Mizokami M. Hepatitis C virus molecular epidemiology in Uzbekistan. J. Med. Virol., 2003, vol. 69. no. 3, pp. 367–375.
- Lavanchy D. The global burden of hepatitis C. Liver. Int., 2009, vol. 29, suppl. 1, pp. 74–81. doi: 10.1111/j.14783231.2008.01934.x
- Li C., Lu L., Wu X., Wang C., Bennett P., Lu T., Murphy D. Complete genomic sequences for hepatitis C virus subtypes 4b, 4c, 4d, 4g, 4k, 4l, 4m, 4n, 4o, 4p, 4q, 4r and 4t. J. Gen. Virol., 2009, vol. 90, pt. 8, pp. 1820–1826. doi: 10.1099/vir.0.010330-0
- 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, vol. 93, pt. 6, pp. 1173–1184. doi: 10.1099/vir.0.038315-0
- Linqi Z., Zhiwei C., Yunzhen C., Jian Y., Guanghan L., Wenjie Y., Ning Y., Shan M., Li L., Balfe P., Tian H., Lei B., Fengwen Z., His-Hsun L., Man-Fung Y., Ching-Lung L., David D.H. Molecular characterization of human immunodeficiency virus type 1 and hepatitis C virus in paid blood donors and injection drug users in China. J. Virol., 2004, vol. 78, no. 24, pp. 13591–13599. doi: 10.1128/JVI.78.24.1359113599.2004
- Lu L., Li C., Fu Y., Thaikruea L., Thongswat S., Maneekarn N., Apichartpiyakul C., Hotta H., Okamoto H., Netski D., Pybus O.G., Murphy D., Hagedorn C.H., Nelson K.E. Complete genomes for hepatitis C virus subtypes 6f, 6i, 6j and 6m: viral genetic diversity among Thai blood donors and infected spouses. J. Gen. Virol., 2007, vol. 88, pt. 5, pp. 1505–1518.
- Maksyutov R.A., Gavrilova E.V., Maksyutov A.Z., Kanev A.N. Genotyping of hepatitis B and C virus Russian isolates for reference serum panel construction. J. Med. Virol., 2015, vol. 87, no. 7, pp. 1192–1198. doi: 10.1002/jmv.24170
- Murphy D.G., Sablon E., Chamberland J., Fournier E., Dandavino R., Tremblay C.L. Hepatitis C virus genotype 7, a new genotype originating from central Africa. J. Clin. Microbiol., 2015, vol. 53, no. 3, pp. 967–972. doi: 10.1128/JCM.02831-14
- Myers R.P., Krajden M., Bilodeau M., Kaita K., Marotta P., Peltekian K., Ramji A., Estes C., Razavi H., Sherman M. Burden of disease and cost of chronic hepatitis C infection in Canada. Can. J. Gastroent. Hepatol., 2014, vol. 28, no. 5, pp. 243–250.
- 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, vol. 208, no. 1, pp. 17–31. doi: 10.1093/infdis/jis679
- Nishiya A.S., de Almeida-Neto C., Ferreira S.C., Alencar C.S., Di-Lorenzo-Oliveira C., Levi J.E., Salles N.A., Mendrone A. Jr, Sabino E.C. HCV genotypes, characterization of mutations conferring drug resistance to protease inhibitors, and risk factors among blood donors in São Paulo, Brazil. PLoS One, 2014, vol. 9, no. 1, e86413. doi: 10.1371/journal.pone.0086413
- Ohno T., Lau J.Y. The “gold-standard”, accuracy, and the current concepts: hepatitis C virus genotype and viremia. Hepatology, 1996, vol. 24, no. 5, pp. 1312–1315.
- Olinger C.M., Lazouskaya N.V., Eremin V.F., Muller C.P. Multiple genotypes and subtypes of hepatitis B and C viruses in Belarus: similarities with Russia and western European influences. Clin. Microbiol. Infect., 2008, vol. 14, no. 6, pp. 575–581. doi: 10.1111/j.14690691.2008.01988.x
- Paintsil E., Verevochkin S.V., Dukhovlinova E., Niccolai L., Barbour R., White E., Toussova O.V., Alexander L., Kozlov A.P., Heimer R. Hepatitis C virus infection among drug injectors in St. Petersburg, Russia: social and molecular epidemiology of an endemic infection. Addiction, 2009, vol. 104, no. 11, pp. 1881–1890. doi: 10.1111/j.13600443.2009.02687.x
- Panigrahi A.K., Roca J., Acharya S.K., Jameel S., Panda S.K. Genotype determination of hepatitis C virus from northern India: identification of a new subtype. J. Med. Virol., 1996, vol. 48, no. 2, pp. 191–198.
- Semjonov S.I., Savvin R.G., Nikitina S.G., Maximova S.S., Sleptsova S.S. Parenteral viral hepatitis (В, С, D) in the Sakha Republic (Yakutia). Life Sci. J., 2014, vol. 11, no. 8, pp. 454–458.
- Sharma S., Carballo M., Feld J.J., Janssen H.L. Immigration and viral hepatitis. J. Hepatol., 2015, vol. 63, no. 2, pp. 515–522. doi: 10.1016/j.jhep.2015.04.026
- Sharvadze L., Nelson K.E., Imnadze P., Karchava M., Tsertsvadze T. Prevalence of HCV and genotypes distribution in general population of Georgia. Georgian Med. News, 2008, vol. 165, pp. 71–77.
- Shustov A.V., Kochneva G.V., Sivolobova G.F., Grazhdantseva A.A., Gavrilova I.V., Akinfeeva L.A., Rakova I.G., Aleshina M.V., Bukin V.N., Orlovsky V.G., Bespalov V.S., Robertson B.H., Netesov S.V. Molecular epidemiology of the hepatitis C virus in Western Siberia. J. Med. Virol., 2005, vol. 77, no. 3, pp. 382–389.
- Simmonds P., Bukh J., Combet C., Deleage G., Enomoto N., Feinstone S., Halfon P., Inchauspe G., Kuiken C., Maertens G., Mizokami M., Murphy D.G., Okamoto H., Pawlotsky J.M., Penin F., Sablon E., ShinI 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, vol. 42, no. 4, pp. 962–973. doi: 10.1002/hep.20819
- Simmonds P., Mellor J., Sakuldamrongpanich T., Nuchaprayoon C., Tanprasert S., Holmes E.C., Smith D.B. Evolutionary analysis of variants of hepatitis C virus found in South-East Asia: comparison with classifications based upon sequence similarity. J. Gen. Virol., 1996, vol. 77, pt. 12, pp. 3013–3024.
- Singh P., Bhatia V., Pandey M., Shashank M., Tidke P., Jha N., Dutt S. HCV genotypes distribution pattern & its association with viral load in India. Int. J. Recent Sci. Res., 2013, vol. 4, no. 11, pp. 1682–1684.
- 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, vol. 59, no. 1, pp. 318–327. doi: 10.1002/hep.26744
- Sominskaya I., Mihailova M., Jansons J., Emelyanova V., Folkmane I., Smagris E., Dumpis U., Rozentals R., Pumpens P. Hepatitis B and C virus variants in longterm immunosuppressed renal transplant patients in Latvia. Intervirology, 2005, vol. 48, no. 2–3, pp. 192–200.
- Tallo T., Norder H., Tefanova V., Krispin T., Schmidt J., Ilmoja M., Orgulas K., Pruunsild K., Priimagi L., Magnius L.O. Genetic characterization of hepatitis C virus strains in Estonia: fluctuations in the predominating subtype with time. J. Med. Virol., 2007, vol. 79, no. 4, pp. 374–382.
- Tamura K., Peterson D., Peterson N., Stecher G. Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol., 2011, vol. 28, no. 10, pp. 2731–2739. doi: 10.1093/molbev/msr121
- Van de Laar T.J., Koppelman M.H., van der Bij A.K., Zaaijer H.L., Cuijpers H.T., van der Poel C.L., Coutinho R.A., Bruisten S.M. Diversity and origin of hepatitis C virus infection among unpaid blood donors in the Netherlands. Transfusion, 2006, vol. 46, no. 10, pp. 1719–1728.
- Viazov S., Kuzin S., Paladi N., Tchernovetsky M., Isaeva E., Mazhul L., Vasychova F., Widell A., Roggendorf M. Hepatitis C virus genotypes in different regions of the former Soviet Union (Russia, Belarus, Moldova and Uzbekistan). J. Med. Virol., 1997, vol. 53, no. 1, pp. 36–40.
- Yu M.L., Chuang W.L. Treatment of chronic hepatitis C in Asia: when East meets West. J. Gastroenterol. Hepatol., 2009, vol. 24, no. 3, pp. 336–345. doi: 10.1111/j.1440-1746.2009.05789.x
- Zein N.N. Clinical significance of hepatitis C virus genotypes. Clin. Microbiol. Rev., 2000, vol. 13, no. 2, pp. 223–235.