CURRENT POSSIBILITIES AND POTENTIAL DEVELOPMENT OF MOLECULAR ENTEROVIRUS SURVEILLANCE. EXPERIENCE OF RUSSIAN FEDERATION
- Authors: Lukashev A.N.1, Golitsina L.N.2, Vakulenko Y.A.1, Akhmadishina L.V.1, Romanenkova N.I.3, Sapega E.Y.4, Morozova N.S.5, Novikova N.A.2, Trotsenko O.E.4, Ivanova O.E.6,7
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Affiliations:
- Martsinovsky Institute of Medical Parasitology, Tropical and Vector-Borne Diseases, Sechenov First Moscow State Medical University, Moscow
- Nizhny Novgorod Science Research institute of Epidemiology and Microbiology n.a. academician I.N. Blokhina, Nizhny Novgorod
- St. Petersburg Pasteur Institute, St. Petersburg
- Khabarovsk Research Institute of Epidemiology and Microbiology, Khabarovsk
- Federal Center of Hygiene and Epidemiology of the Inspectorate for Customers Protection of Rospotrebnadzor, Moscow
- Chumakov Federal Scientific Center for Research and Development of Immune-and-Biological Products of Russian Academy of Sciences, Moscow
- Institute of Translational Medicine and Biotechnology, Sechenov First Moscow State Medical University, Moscow
- Issue: Vol 8, No 4 (2018)
- Pages: 452-464
- Section: MOLECULAR BASES OF EPIDEMIOLOGY, DIAGNOSTICS, PREVENTION AND TREATMENT OF INFECTIOUS DISEASES
- Submitted: 14.12.2018
- Accepted: 14.12.2018
- Published: 30.12.2018
- URL: https://iimmun.ru/iimm/article/view/828
- DOI: https://doi.org/10.15789/2220-7619-2018-4-452-464
- ID: 828
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Abstract
Abstract. Enteroviruses are small RNA viruses, which are ubiquitous and commonly cause outbreaks with various clinical manifestations. In 2006, the Program on enterovirus surveillance was approved in the Russian Federation. Over the last years, molecular-biological and bioinformatics methods for enterovirus epidemiology studies have been developed both in Russia and worldwide. Currently, identification of enteroviruses is carried out by analyzing nucleotide sequence of the full-length VP1 genome region (ca. 900 nt). Routinely, it is sufficient to obtain a partial VP1 genome region sequence (ca. 300 bp) for enteroviruse verification in most cases; however, a more stringent type criterion of 80% sequence identity should be used compared to the 75% sequence identity cut-off for the complete VP1 genome region. Further sequence analysis may be performed by using Bayesian phylogenetic methods, which allow using molecular clock to trace outbreak emergence. Enteroviruses accumulate about 0.5–1% nucleotide substitutions per year. Therefore, a short genome fragment may be used to analyze virus phylodynamics at the level of international transfers and circulating virus variants. On a shorter timescale, a full-length VP1 genome region or a complete genome sequence are preferred for investigating molecular epidemiology, because a short sequence allows to reliably distinguish not more than 1–2 transmission events per year. Thus, determining enterovirus sequences for full-length VP1 genome region or full-genome sequence is preferred for examining viral outbreaks. It is increasingly apparent that analyzing available enterovirus nucleotide sequences reveals limitations related to uneven surveillance efficacy in various countries and short length of genome fragment measured in routine control. As a result, a proper global-scale analysis of enterovirus molecular epidemiology remains problematic. Over the last 20 years, the number of available enterovirus nucleotide sequences increased by hundred times, but understanding emergence of enterovirus infection outbreaks remains limited. Further development of enterovirus surveillance would require new methods for sewage monitoring, affordable high-throughput sequencing and harmonization of global surveillance systems.
Keywords
About the authors
A. N. Lukashev
Martsinovsky Institute of Medical Parasitology, Tropical and Vector-Borne Diseases, Sechenov First Moscow State Medical University, Moscow
Author for correspondence.
Email: alexander_lukashev@hotmail.com
PhD, MD (Medicine), Professor, Director
119435, Malaya Pirogovskaya str., 20/1,
Phone: +7 (499) 246-80-49
L. N. Golitsina
Nizhny Novgorod Science Research institute of Epidemiology and Microbiology n.a. academician I.N. Blokhina, Nizhny Novgorod
Email: fake@neicon.ru
PhD (Biology), Leading Researcher, Laboratory of Molecular Epidemiology of Viral Infections Россия
Y. A. Vakulenko
Martsinovsky Institute of Medical Parasitology, Tropical and Vector-Borne Diseases, Sechenov First Moscow State Medical University, Moscow
Email: fake@neicon.ru
Junior Researcher, Research Department Россия
L. V. Akhmadishina
Martsinovsky Institute of Medical Parasitology, Tropical and Vector-Borne Diseases, Sechenov First Moscow State Medical University, Moscow
Email: fake@neicon.ru
PhD (Medicine), Head of the Clinical Diagnostic Laboratory Россия
N. I. Romanenkova
St. Petersburg Pasteur Institute, St. Petersburg
Email: fake@neicon.ru
PhD (Medicine), Leading Researcher, Laboratory of Etiology and Control of Viral Infections Россия
E. Yu. Sapega
Khabarovsk Research Institute of Epidemiology and Microbiology, Khabarovsk
Email: fake@neicon.ru
PhD (Medicine), Head of Enterovirus Surveillance Center Россия
N. S. Morozova
Federal Center of Hygiene and Epidemiology of the Inspectorate for Customers Protection of Rospotrebnadzor, Moscow
Email: fake@neicon.ru
Head of Epidemiological Surveillance Department Россия
N. A. Novikova
Nizhny Novgorod Science Research institute of Epidemiology and Microbiology n.a. academician I.N. Blokhina, Nizhny Novgorod
Email: fake@neicon.ru
PhD (Biology), Professor Россия
O. E. Trotsenko
Khabarovsk Research Institute of Epidemiology and Microbiology, Khabarovsk
Email: fake@neicon.ru
PhD, MD (Medicine), Professor, Director Россия
O. E. Ivanova
Chumakov Federal Scientific Center for Research and Development of Immune-and-Biological Products of Russian Academy of Sciences, Moscow; Institute of Translational Medicine and Biotechnology, Sechenov First Moscow State Medical University, Moscow
Email: fake@neicon.ru
PhD, MD (Medicine), Professor, Head of Poliomyelitis and Other Enterovirus Infections Россия
References
- Голицына Л.Н., Зверев В.В., Парфенова О.В., Новикова Н.А. Эпидемические варианты неполиомиелитных энтеровирусов в России // Медицинский альманах. 2015. Т. 40, № 5. С. 136–140. [Golitsyna L.N., Zverev V.V., Parfenova O.V., Novikova N.A. Epidemic variants of non-poliomyelitic enteroviruses in Russia. Meditsinskii al’manakh = Medical Almanac, 2015, vol. 40, no. 5, pp. 136–140. (In Russ.)]
- Лашкевич В.А., Королева Г.А., Лукашев А.Н., Денисова Е.В., Катаргина Л.А., Хорошилова-Маслова И.П. Острый энтеровирусный увеит у детей младшего возраста // Вопросы вирусологии. 2005. T. 50, № 3. C. 36–45. [Lashkevich V.A., Koroleva G.A., Lukashev A.N., Denisova E.V., Katargina L.A., Khoroshilova-Maslova I.P. Acute enterovirus uveitis in young children. Voprosy virusologii = Problems of Virology, 2005, vol. 50, no. 3, pp. 36–45. (In Russ.)]
- Лукашев А.Н. Роль рекомбинации в эволюции энтеровирусов // Вопросы вирусологии. 2005. T. 50, № 3. C. 46–52. [Lukashev A.N. Role of recombination in evolution of enteroviruses. Voprosy virusologii = Problems of Virology, 2005, vol. 50, no. 3, pp. 46–52. (In Russ.)]
- Лукашев А.Н., Резник В.И., Иванова О.Е., Еремеева Т.П., Каравянская Т.Н., Перескокова М.А., Лебедева Л.А., Лашкевич В.А., Михайлов М.И. Молекулярная эпидемиология вируса ЕСНО 6 — возбудителя вспышки серозного менингита в Хабаровске в 2006 г. // Вопросы вирусологии. 2008. Т. 53, № 1. C. 16–21. [Lukashev A.N., Reznik V.I., Ivanova O.E., Eremeyeva T.P., Karavyanskaya T.N., Pereskokova M.A., Lebedeva L.A., Lashkevich V.A., Mikhallov M.I. Molecular epidemiolo gy of ECHO 6 virus, the causative agent of the 2006 outbreak of serous meningitis in Khabarovsk. Voprosy virusologii = Problems of Virology, 2008, vol. 53, no. 1, pp. 16–21. (In Russ.)]
- Устюжанин А.В., Резайкин А.В., Сергеев А.Г., Снитковская Т.Э. Значение молекулярно-генетического мониторинга в оценке степени вирулентности и эпидемической значимости штаммов неполиомиелитных энтеровирусов, циркулирующих среди населения // Вестник Уральской медицинской академической науки. 2015. Т. 52, № 1. С. 72–76. [Ustyuzhanin A.V., Rezaykin A.V., Sergeev A.G., Snitkovskaya T.E. Molecular genetic surveillance of circulating human nonpoliomyelitis viruses strains: implications for the estimates of epidemic significance and virulence. Vestnik Ural’skoi meditsinskoi akademicheskoi nauki = Journal of Ural Medical Academic Science, 2015, vol. 52, no. 1, pp. 72–76. (In Russ.)]
- Akhmadishina L.V., Govorukhina M.V., Kovalev E.V., Nenadskaya S.A., Ivanova O.E., Lukashev A.N. Enterovirus A71 meningoencephalitis outbreak, Rostov-on-Don, Russia, 2013. Emerg. Infect. Dis., 2015, vol. 21, no. 8, pp. 1440–1443. doi: 10.3201/eid2108.141084
- Bailly J.L., Mirand A., Henquell C., Archimbaud C., Chambon M., Charbonne F., Traore O., Peigue-Lafeuille H. Phylogeography of circulating populations of human echovirus 30 over 50 years: nucleotide polymorphism and signature of purifying selection in the VP1 capsid protein gene. Infect. Genet. Evol., 2009, vol. 9, no. 4, pp. 699–708. doi: 10.1016/j.meegid.2008.04.009
- Brown B.A., Maher K., Flemister M.R., Naraghi-Arani P., Uddin M., Oberste M.S., Pallansch M.A. Resolving ambiguities in genetic typing of human enterovirus species C clinical isolates and identification of enterovirus 96, 99 and 102. J. Gen. Virol., 2009, vol. 90, no. 7, pp. 1713–1723. doi: 10.1099/vir.0.008540-0
- Centers for Disease Control and Prevention. Certification of poliomyelitis eradication — European Region, June 2002. MMWR Morb. Mortal. Wkly Rep., 2002, vol. 51, no. 26, pp. 572–574.
- Chumakov K.M., Powers L.B., Noonan K.E., Roninson I.B., Levenbook I.S. Correlation between amount of virus with altered nucleotide sequence and the monkey test for acceptability of oral poliovirus vaccine. Proc. Natl. Acad. Sci. USA, 1991, vol. 88, no. 1, pp. 199–203.
- Drummond A.J., Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol., 2007, vol. 7, pp. 214. doi: 10.1186/1471-2148-7-214
- Gaunt E., Harvala H., Osterback R., Sreenu V.B., Thomson E., Waris M., Simmonds P. Genetic characterization of human coxsackievirus A6 variants associated with atypical hand, foot and mouth disease: a potential role of recombination in emergence and pathogenicity. J. Gen. Virol., 2015, vol. 96, no. 5, pp. 1067–1079. doi: 10.1099/vir.0.000062
- Hassel C., Mirand A., Lukashev A., Terletskaialadwig E., Farkas A., Schuffenecker I., Diedrich S., Huemer H.P., Archimbaud C., Peigue-Lafeuille H., Henquell C., Bailly J.L. Transmission patterns of human enterovirus 71 to, from and among European countries, 2003 to 2013. Euro Surveill., 2015, vol. 20, no. 34. doi: 10.2807/1560-7917.ES.2015.20.34.30005
- Ho M., Chen E.R., Hsu K.H., Twu S.J., Chen K.T., Tsai S.F., Wang J.R., Shih S.R. An epidemic of enterovirus 71 infection in Taiwan. Taiwan Enterovirus Epidemic Working Group. N. Engl. J. Med., 1999, vol. 341, no. 13, pp. 929–935. doi: 10.1056/NEJM199909233411301
- Khetsuriani N., Lamonte-Fowlkes A., Oberste S., Pallansch M.A. Enterovirus surveillance — United States, 1970–2005. MMWR Surveill. Summ., 2006, vol. 55, no. 8, pp. 1–20.
- Lancaster K.Z., Pfeiffer J.K. Mechanisms controlling virulence thresholds of mixed viral populations. J. Virol., 2011, vol. 85, no. 19, pp. 9778–9788. doi: 10.1128/JVI.00355-11
- Lemey P., Rambaut A., Welch J.J., Suchard M.A. Phylogeography takes a relaxed random walk in continuous space and time. Mol. Biol. Evol., 2010, vol. 27, no. 8, pp. 1877–1885. doi: 10.1093/molbev/msq067
- Liste M.B., Natera I., Suarez J.A., Pujol F.H., Liprandi F., Ludert J.E. Enteric virus infections and diarrhea in healthy and human immunodeficiency virus-infected children. J. Clin. Microbiol., 2000, vol. 38, no. 8, pp. 2873–2877.
- Liu W., Wu S., Xiong Y., Li T., Wen Z., Yan M., Qin K., Liu Y., Wu J. Co-circulation and genomic recombination of coxsackievirus A16 and enterovirus 71 during a large outbreak of hand, foot, and mouth disease in Central China. PLoS One, 2014, vol. 9, no. 4: e96051. doi: 10.1371/journal.pone.0096051
- Lukashev A.N., Lashkevich V.A., Ivanova O.E., Koroleva G.A., Hinkkanen A.E., Ilonen J. Recombination in circulating enteroviruses. J. Virol., 2003, vol. 77, no. 19, pp. 10423–10431. doi: 10.1128/JVI.77.19.10423-10431.2003
- Lukashev A.N., Lashkevich V.A., Ivanova O.E., Koroleva G.A., Hinkkanen A.E., Ilonen J. Recombination in circulating enterovirus B: independent evolution of structural and non-structural genome regions. J. Gen. Virol., 2005, vol. 86, no. 12, pp. 3281– 3290. doi: 10.1099/vir.0.81264-0
- Lukashev A.N., Vakulenko Y.A. Molecular evolution of types in non-polio enteroviruses. J. Gen. Virol., 2017, vol. 98, no. 12, pp. 2968–2981. doi: 10.1099/jgv.0.000966
- McMinn P.C. Recent advances in the molecular epidemiology and control of human enterovirus 71 infection. Curr. Opin. Virol., 2012, vol. 2, no. 2, pp. 199–205. doi: 10.1016/j.coviro.2012.02.009
- McWilliam Leitch E.C., Bendig J., Cabrerizo M., Cardosa J., Hyypia T., Ivanova O.E., Kelly A., Kroes A.C., Lukashev A., MacAdam A., McMinn P., Roivainen M., Trallero G., Evans D.J., Simmonds P. Transmission networks and population turnover of echovirus 30. J. Virol., 2009, vol. 83, no. 5, pp. 2109–2118. doi: 10.1128/JVI.02109-08
- McWilliam Leitch E.C., Cabrerizo M., Cardosa J., Harvala H., Ivanova O.E., Koike S., Kroes A.C., Lukashev A., Perera D., Roivainen M., Susi P., Trallero G., Evans D.J., Simmonds P. The association of recombination events in the founding and emergence of subgenogroup evolutionary lineages of human enterovirus 71. J. Virol., 2012, vol. 86, no. 5, pp. 2676–2685. doi: 10.1128/JVI.06065-11
- McWilliam Leitch E.C., Cabrerizo M., Cardosa J., Harvala H., Ivanova O.E., Kroes A.C., Lukashev A., Muir P., Odoom J., Roivainen M., Susi P., Trallero G., Evans D.J., Simmonds P. Evolutionary dynamics and temporal/geographical correlates of recombination in the human enterovirus echovirus types 9, 11, and 30. J. Virol., 2010, vol. 84, no. 18, pp. 9292–9300. doi: 10.1128/JVI.00783-10
- Nasri D., Bouslama L., Omar S., Saoudin H., Bourlet T., Aouni M., Pozzetto B., Pillet S. Typing of human enterovirus by partial sequencing of VP2. J. Clin. Microbiol., 2007, vol. 45, no. 8, pp. 2370–2379. doi: 10.1128/JCM.00093-07
- Nomoto A. Molecular aspects of poliovirus pathogenesis. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci., 2007, vol. 83, no. 8, pp. 266–275. doi: 10.2183/pjab/83.266
- Oberste M.S., Maher K., Kilpatrick D. R., Flemister M.R., Brown B.A., Pallansch M.A. Typing of human enteroviruses by partial sequencing of VP1. J. Clin. Microbiol., 1999, vol. 37, pp. 1288–1293.
- Oberste M.S., Maher K., Kilpatrick D.R., Pallansch M.A. Molecular evolution of the Human enteroviruses: correlation of serotype with VP1 sequence and application to picornavirus classification. J. Virol., 1999, vol. 73, pp. 1941–1948.
- Oberste M.S., Nix W.A., Kilpatrick D.R., Flemister M.R., Pallansch M.A. Molecular epidemiology and type-specific detection of echovirus 11 isolates from the Americas, Europe, Africa, Australia, southern Asia and the Middle East. Virus Res., 2003, vol. 91, pp. 241–248. doi: 10.1016/S0168-1702(02)00291-5
- Palacios G., Oberste M.S. Enteroviruses as agents of emerging infectious diseases. J. Neurovirol., 2005, vol. 11, no. 5, pp. 424–433. doi: 10.1080/13550280591002531
- Puenpa J., Vongpunsawad S., Osterback R., Waris M., Eriksson E., Albert J., Midgley S., Fischer T.K., Eis-Hubinger A.M., Cabrerizo M., Gaunt E., Simmonds P., Poovorawan Y. Molecular epidemiology and the evolution of human coxsackievirus A6. J. Gen. Virol., 2016, vol. 97, no. 12, pp. 3225–3231. doi: 10.1099/jgv.0.000619
- Savolainen-Kopra C., Paananen A., Blomqvist S., Klemola P., Simonen M.L., Lappalainen M., Vuorinen T., Kuusi M., Lemey P., Roivainen M. A large Finnish echovirus 30 outbreak was preceded by silent circulation of the same genotype. Virus Genes, 2011, vol. 42, no. 1, pp. 28–36. doi: 10.1007/s11262-010-0536-x
- Simonen-Tikka M.L., Hiekka A.K., Klemola P., Poussa T., Ludvigsson J., Korpela R., Vaarala O., Roivainen M. Early human enterovirus infections in healthy Swedish children participating in the PRODIA pilot study. J. Med. Virol., 2012, vol. 84, no. 6, pp. 923–930. doi: 10.1002/jmv.23284
- Solmone M., Vincenti D., Prosperi M.C., Bruselles A., Ippolito G., Capobianchi M.R. Use of massively parallel ultradeep pyrosequencing to characterize the genetic diversity of hepatitis B virus in drug-resistant and drug-naive patients and to detect minor variants in reverse transcriptase and hepatitis B S antigen. J. Virol., 2009, vol. 83, no. 4, pp. 1718–1726. doi: 10.1128/JVI.02011-08
- Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol. Biol. Evol., 2013, vol. 30, no. 12, pp. 2725–2729. doi: 10.1093/molbev/mst197
- Van der Sanden S.M., Koopmans M.P., van der Avoort H.G. Detection of human enteroviruses and parechoviruses as part of the national enterovirus surveillance in the Netherlands, 1996-2011. Eur. J. Clin. Microbiol. Infect. Dis., 2013, vol. 32, no. 12, pp. 1525– 1531. doi: 10.1007/s10096-013-1906-9
- Witso E., Palacios G., Cinek O., Stene L.C., Grinde B., Janowitz D., Lipkin W.I., Ronningen K.S. High prevalence of human enterovirus a infections in natural circulation of human enteroviruses. J. Clin. Microbiol., 2006, vol. 44, no. 11, pp. 4095–4100. doi: 10.1128/JCM.00653-06
- Wright P.W., Strauss G.H., Langford M.P. Acute hemorrhagic conjunctivitis. Am. Fam. Physician, 1992, vol. 45, no. 1, pp. 173–178.
- Yakovenko M.L., Gmyl A.P., Ivanova O.E., Eremeeva T.P., Ivanov A.P., Prostova M.A., Baykova O.Y., Isaeva O.V., Lipskaya G.Y., Shakaryan A.K., Kew O.M., Deshpande J.M., Agol V.I. The 2010 outbreak of poliomyelitis in Tajikistan: epidemiology and lessons learnt. Euro Surveill., 2014, vol. 19, no. 7, pp. 20706.
- Yarmolskaya M.S., Shumilina E.Y., Ivanova O.E., Drexler J.F., Lukashev A.N. Molecular epidemiology of echoviruses 11 and 30 in Russia: different properties of genotypes within an enterovirus serotype. Infect. Genet. Evol., 2015, vol. 30, pp. 244–248. doi: 10.1016/j.meegid.2014.12.033