Журнал микробиологии, эпидемиологии и иммунобиологии. 2022; 99: 7-19
Молекулярно-генетические особенности ротавирусов группы А, выявленных в Москве в 2015–2020 гг.
https://doi.org/10.36233/0372-9311-208Аннотация
Цель работы — анализ генетических характеристик штаммов ротавирусов группы А (РВА), циркулировавших в Москве в 2015–2020 гг., включая редкие штаммы, нетипируемые методом полимеразной цепной реакции (ПЦР).
Материалы и методы. Исследовали 289 фекальных образцов от детей в возрасте от 1 мес до 17 лет, госпитализированных с острым гастроэнтеритом. Выявление ротавирусов в образцах проводили методами иммунохроматографии и обратной транскрипции (ОТ) с ПЦР в реальном времени (ОТ-ПЦР-РВ). Секвенирование ротавирусного генома проводили по Сэнгеру и методом нанопорового секвенирования.
Результаты и обсуждение. В 131 клиническом образце была выявлена РНК РВА, в 125 случаях из них был установлен G/[P]-генотип. В общей структуре преобладали штаммы РВА с генотипом G9P[8]I1 (37%), за ними следовали варианты G3P[8]I2, G4P[8]I1, G2P[4]I2, G1P[8]I1 и G3P[8]I1 (18, 15, 11, 5 и 2% соответственно). Семь (5%) изолятов были идентифицированы как GxP[8]. В 2015–2020 гг. в регионе снизилась частота встречаемости генотипа G4P[8]I1 (с 39 до 9%) и выросла доля генотипа G9P[8]I1 (с 6 до 37%) по сравнению с 2009–2014 гг. В 2018–2020 гг. выявлена высокая доля не встречавшегося ранее DS-1-подобного реассортантного штамма G3P[8]I2, широко распространившегося в мире в последние годы, Методом нанопорового секвенирования проведён анализ генома штамма G3P[8]I2 и редкого штамма G4P[6]I1. Для штамма G4P[6]I1 установлена тесная филогенетическая связь с ротавирусами свиней.
Заключение. За последние годы в генетической структуре РВА, циркулирующих на территории московского региона, произошли существенные изменения. Полученные результаты свидетельствуют о необходимости постоянного мониторинга ротавирусной инфекции и выборочного секвенирования генов РВА для уточнения данных типоспецифической ОТ-ПЦР-РВ. Из-за постоянных изменений генетического состава циркулирующих штаммов РВА требуется периодическая оптимизация систем генотипирования РВА на основе ОТ-ПЦР-РВ.
Список литературы
1. Troeger C., Khalil I.A., Rao P.C., Cao S., Blacker B.F., Ahmed T., et al. Rotavirus vaccination and the global burden of rotavirus diarrhea among children younger than 5 years. JAMA Pediatr. 2018; 172(10): 958–65. https://doi.org/10.1001/jamapediatrics.2018.1960
2. Hoog M.L.A., Vesikari T., Giaquinto C., Huppertz H.I., Martinon-Torres F., Bruijning-Verhagen P. Report of the 5th European expert meeting on rotavirus vaccination (EEROVAC). Hum. Vaccin. Immunother. 2018; 14(4): 1027–34. https://doi.org/10.1080/21645515.2017.1412019
3. Matthijnssens J., Ciarlet M., Rahman M., Attoui H., Banyai K., Estes M.K., et al. Recommendations for the classification of group A rotaviruses using all 11 genomic RNA segments. Arch. Virol. 2008; 153(8): 1621–9. https://doi.org/10.1007/s00705-008-0155-1
4. WHO. Manual of rotavirus detection and characterization methods. Geneva; 2009. Available at: https://www.who.int/vaccines-documents
5. Doro R., Laszlo B., Martella V., Leshem E., Gentsch J., Parashar U., et al. Review of global rotavirus strain prevalence data from six years post vaccine licensure surveillance: is there evidence of strain selection from vaccine pressure? Infect. Genet. Evol. 2014; 28: 446–61. https://doi.org/10.1016/j.meegid.2014.08.017
6. Zhou X., Wang Y.H., Ghosh S., Tang W.F., Pang B.B., Liu M.Q., et al. Genomic characterization of G3P[6], G4P[6] and G4P[8] human rotaviruses from Wuhan, China: Evidence for interspecies transmission and reassortment events. Infect. Genet. Evol. 2015; 33: 55–71. https://doi.org/10.1016/j.meegid.2015.04.010
7. Salamunova S., Jackova A., Csank T., Mandelik R., Novotny J., Beckova Z., et al. Genetic variability of pig and human rotavirus group A isolates from Slovakia. Arch. Virol. 2020; 165(2): 463–70. https://doi.org/10.1007/s00705-019-04504-6
8. Doro R., Farkas S.L., Martella V., Banyai K. Zoonotic transmission of rotavirus: surveillance and control. Expert. Rev. Anti. Infect. Ther. 2015; 13(11): 1337–50. https://doi.org/10.1586/14787210.2015.1089171
9. Velasquez D.E., Jiang B. Evolution of P[8], P[4], and P[6] VP8* genes of human rotaviruses globally reported during 1974 and 2017: possible implications for rotavirus vaccines in development. Hum. Vaccin. Immunother. 2019; 15(12): 3003–8. https://doi.org/10.1080/21645515.2019.1619400
10. Hungerford D., Vivancos R., Read J.M., Iturriza-Gomicronmara M., French N., Cunliffe N.A. Rotavirus vaccine impact and socioeconomic deprivation: an interrupted time-series analysis of gastrointestinal disease outcomes across primary and secondary care in the UK. BMC Med. 2018; 16(1): 10. https://doi.org/10.1186/s12916-017-0989-z
11. Freeman M.M., Kerin T., Hull J., McCaustland K., Gentsch J. Enhancement of detection and quantification of rotavirus in stool using a modified real-time RT-PCR assay. J. Med. Virol. 2008; 80(8): 1489–96. https://doi.org/10.1002/jmv.21228
12. Kiseleva V., Faizuloev E., Meskina E., Marova A., Oksanich A., Samartseva T., et al. Molecular-genetic characterization of human rotavirus a strains circulating in Moscow, Russia (2009- 2014). Virol. Sin. 2018; 33(4): 304–13. https://doi.org/10.1007/s12250-018-0043-0
13. Iturriza-Gomara M., Isherwood B., Desselberger U., Gray J. Reassortment in vivo: driving force for diversity of human rotavirus strains isolated in the United Kingdom between 1995 and 1999. J. Virol. 2001; 75(8): 3696–705. https://doi.org/10.1128/JVI.75.8.3696-3705.2001
14. Simmonds M.K., Armah G., Asmah R., Banerjee I., Damanka S., Esona M., et al. New oligonucleotide primers for P-typing of rotavirus strains: Strategies for typing previously untypeable strains. J. Clin. Virol. 2008; 42(4): 368–73. https://doi.org/10.1016/j.jcv.2008.02.011
15. Froussard P. rPCR: a powerful tool for random amplification of whole RNA sequences. PCR Methods Appl. 1993; 2(3): 185–90. https://doi.org/10.1101/gr.2.3.185
16. Li H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics. 2018; 34(18): 3094–100. https://doi.org/10.1093/bioinformatics/bty191
17. Maes P., Matthijnssens J., Rahman M., Van Ranst M. RotaC: a web-based tool for the complete genome classification of group A rotaviruses. BMC Microbiol. 2009; 9: 238. https://doi.org/10.1186/1471-2180-9-238
18. Faizuloev E., Mintaev R., Petrusha O., Marova A., Smirnova D., Ammour Y., et al. New approach to genetic characterization of group A rotaviruses by the nanopore sequencing method. J. Virol. Methods. 2021; 292: 114114. https://doi.org/10.1016/j.jviromet.2021.114114
19. Kumar S., Stecher G., Li M., Knyaz C., Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Mol. Biol. Evol. 2018; 35(6): 1547–9. https://doi.org/10.1093/molbev/msy096
20. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 1980; 16(2): 111–20. https://doi.org/10.1007/BF01731581
21. Cowley D., Donato C.M., Roczo-Farkas S., Kirkwood C.D. Emergence of a novel equine-like G3P[8] inter-genogroup reassortant rotavirus strain associated with gastroenteritis in Australian children. J. Gen. Virol. 2016; 97(2): 403–10. https://doi.org/10.1099/jgv.0.000352
22. Arana A., Montes M., Jere K.C., Alkorta M., Iturriza-Gomara M., Cilla G. Emergence and spread of G3P[8] rotaviruses possessing an equine-like VP7 and a DS-1-like genetic backbone in the Basque Country (North of Spain), 2015. Infect. Genet. Evol. 2016; 44: 137–44. https://doi.org/10.1016/j.meegid.2016.06.048
23. Doro R., Marton S., Bartokne A.H., Lengyel G., Agocs Z., Jakab F., et al. Equine-like G3 rotavirus in Hungary, 2015 — Is it a novel intergenogroup reassortant pandemic strain? Acta. Microbiol. Immunol. Hung. 2016; 63(2): 243–55. https://doi.org/10.1556/030.63.2016.2.8
24. Guerra S.F.S., Soares L.S., Lobo P.S., Penha Junior E.T., Sousa Junior E.C., Bezerra D.A.M., et al. Detection of a novel equinelike G3 rotavirus associated with acute gastroenteritis in Brazil. J. Gen. Virol. 2016; 97(12): 3131–8. https://doi.org/10.1099/jgv.0.000626
25. Komoto S., Tacharoenmuang R., Guntapong R., Ide T., Haga K., Katayama K., et al. Emergence and characterization of unusual DS-1-Like G1P[8] rotavirus strains in children with diarrhea in Thailand. PLoS One. 2015; 10(11): e0141739. https://doi.org/10.1371/journal.pone.0141739
26. Kaira A.N., Fayzuloyev E.B., Lavrov V.F., Svitich O.A., Solomay T.V., Nikonova A.A., et al. Epidemiological trends of morbidity and issues of rotavirus vaccination at the present stage. Sanitary Doctor. 2020; 6: 16–25. https://doi.org/0.33920/med-08-2006-02
27. Ivashechkin A.A., Yuzhakov A.G., Grebennikova T.V., Yuzhakova K.A., Kulikova N.Y., Kisteneva L.B., et al. Genetic diversity of group A rotaviruses in Moscow in 2018-2019. Arch. Virol. 2020; 165(3): 691–702. https://doi.org/10.1007/s00705-020-04534-5
28. Yuzhakov G., Yuzhakova K., Kulikova N., Kisteneva L., Cherepushkin S., Smetanina S., et al. Prevalence and genetic diversity of group a rotavirus genotypes in Moscow (2019–2020). Pathogens. 2021; 10: 674. https://doi.org/10.3390/pathogens10060674
29. Sashina T.A., Morozova O.V., Epifanova N.V., Novikova N.A. Predominance of new G9P[8] rotaviruses closely related to Turkish strains in Nizhny Novgorod (Russia). Arch. Virol. 2017; 162(8): 2387–92. https://doi.org/10.1007/s00705-017-3364-7
30. Новикова Н.А., Сашина Т.A., Солнцев Л.А., Епифанова Н.В., Кашников A.Ю., Погодина Л.В. и др. Проявление эпидемического процесса ротавирусного процесса в Нижнем Новгороде в предвакцинальный период. Журнал микробиологии, эпидемиологии и иммунобиологии. 2017; 94(5): 46–52. https://doi.org/10.36233/0372-9311-2017-5-46-52
31. Денисюк Н.Б. Генетическая характеристика ротавирусов группы А, циркулирующих в Оренбургском регионе в сезон 2016–2017 гг. Детские инфекции. 2017; 16(4): 42–5. https://doi.org/10.22627/2072-8107-2017-16-4-42-45
32. Мескина Е.Р., Ушакова А.Ю., Файзулоев Е.Б., Бахтояров Г.Н., Киселева В.В. Сравнительная характеристика гастроэнтерита, вызванного ротавирусами генотипов G4P[8] и G9P[8], у детей, госпитализированных в стационар г. Москвы (эпидсезон 2012–2013 гг.). Инфекционные болезни. 2017; 15(1): 23–8. https://doi.org/10.20953/1729-9225-2017-1-23-28
33. Katz E.M., Esona M.D., Betrapally N.S., De La Cruz De Leon L.A., Neira Y.R., Rey G.J., et al. Whole-gene analysis of inter-genogroup reassortant rotaviruses from the Dominican Republic: Emergence of equine-like G3 strains and evidence of their reassortment with locally-circulating strains. Virology. 2019; 534: 114–31. https://doi.org/10.1016/j.virol.2019.06.007
34. Fujii Y., Oda M., Somura Y., Shinkai T. Molecular characteristics of novel mono-reassortant G9P[8] rotavirus a strains possessing the NSP4 gene of the E2 genotype detected in Tokyo, Japan. Jpn J. Infect. Dis. 2020; 73(1): 26–35. https://doi.org/10.7883/yoken.JJID.2019.211
35. McDonald S.M., Matthijnssens J., McAllen J.K., Hine E., Overton L., Wang S., et al. Evolutionary dynamics of human rotaviruses: balancing reassortment with preferred genome constellations. PLoS Pathog. 2009; 5(10): e1000634. https://doi.org/10.1371/journal.ppat.1000634
36. Papp H., Borzak R., Farkas S., Kisfali P., Lengyel G., Molnar P., et al. Zoonotic transmission of reassortant porcine G4P[6] rotaviruses in Hungarian pediatric patients identified sporadically over a 15 year period. Infect. Genet. Evol. 2013; 19: 71–80. https://doi.org/10.1016/j.meegid.2013.06.013
37. Esona M.D., Geyer A., Banyai K., Page N., Aminu M., Armah G.E., et al. Novel human rotavirus genotype G5P[7] from child with diarrhea, Cameroon. Emerg. Infect. Dis. 2009; 15(1): 83–6. https://doi.org/10.3201/eid1501.080899
38. Wang Y.H., Kobayashi N., Nagashima S., Zhou X., Ghosh S., Peng J.S., et al. Full genomic analysis of a porcine-bovine reassortant G4P[6] rotavirus strain R479 isolated from an infant in China. J. Med. Virol. 2010; 82(6): 1094–102. https://doi.org/10.1002/jmv.21760
39. Zeller M., Patton J.T., Heylen E., De Coster S., Ciarlet M., Van Ranst M., et al. Genetic analyses reveal differences in the VP7 and VP4 antigenic epitopes between human rotaviruses circulating in Belgium and rotaviruses in Rotarix and RotaTeq. J. Clin. Microbiol. 2012; 50(3): 966–76. https://doi.org/10.1128/JCM.05590-11
40. Imagawa T., Saito M., Yamamoto D., Saito-Obata M., Masago Y., Ablola A.C., et al. Genetic diversity of species A rotaviruses detected in clinical and environmental samples, including porcine-like rotaviruses from hospitalized children in the Philippines. Infect. Genet. Evol. 2020; 85: 104465. https://doi.org/10.1016/j.meegid.2020.104465
Journal of microbiology, epidemiology and immunobiology. 2022; 99: 7-19
Molecular and genetic characteristics of group A rotaviruses detected in Moscow in 2015–2020
https://doi.org/10.36233/0372-9311-208Abstract
The aim of the study was to analyze genetic characteristics of strains belonging to group A rotaviruses (RVA) circulating in Moscow in 2015–2020, including rare strains non-typeable by polymerase chain reaction (PCR).
Materials and methods. A total of 289 stool samples were tested; the samples were collected from children aged 1 month to 17 years, hospitalized with acute gastroenteritis. Immunochromatography and real-time reverse transcription-polymerase chain reaction (real-time RT-PCR) assays were used for detection of rotaviruses in the samples. The rotavirus genome sequencing was performed using the Sanger technique and nanopore sequencing.
Results and discussion. RVA RNA was detected in 131 clinical samples, and the G/[P] genotype was identified in 125 samples. The general profile showed prevalence of RVA strains with the G9P[8]I1 genotype (37%) followed by G3P[8]I2, G4P[8]I1, G2P[4]I2, G1P[8]I1, and G3P[8]I1 variants (18, 15, 11, 5, and 2%, respectively). Seven (5%) isolates were identified as GxP[8]. In 2015–2020, the region reported a decline in G4P[8]I1 genotype prevalence (from 39% to 9%) and an increase in the proportion of the G9P[8]I1 genotype (from 6% to 37%) as compared to 2009–2014. In 2018–2020, a large number of cases with the previously unknown DS-1-like reassortant strain with the G3P[8]I2 genotype were reported; the above strain has become widely common worldwide in the recent years. Nanopore sequencing was performed to analyze the genome of the G3P[8]I2 strain and the rare G4P[6]I1 strain. It was found that the G4P[6]I1 strain was phylogenetically related to porcine rotaviruses.
Conclusion. In the recent years, the genetic diversity of RVA circulating in the Moscow Region has changed significantly. The obtained results prove the importance of continuous monitoring of rotavirus infection and selective sequencing of RVA genes to fine-tune data of the type-specific real-time RT-PCR. The ever-changing genetic composition of the circulating RVA strains calls for regular optimization of RVA genotyping systems based on real-time RT-PCR.
References
1. Troeger C., Khalil I.A., Rao P.C., Cao S., Blacker B.F., Ahmed T., et al. Rotavirus vaccination and the global burden of rotavirus diarrhea among children younger than 5 years. JAMA Pediatr. 2018; 172(10): 958–65. https://doi.org/10.1001/jamapediatrics.2018.1960
2. Hoog M.L.A., Vesikari T., Giaquinto C., Huppertz H.I., Martinon-Torres F., Bruijning-Verhagen P. Report of the 5th European expert meeting on rotavirus vaccination (EEROVAC). Hum. Vaccin. Immunother. 2018; 14(4): 1027–34. https://doi.org/10.1080/21645515.2017.1412019
3. Matthijnssens J., Ciarlet M., Rahman M., Attoui H., Banyai K., Estes M.K., et al. Recommendations for the classification of group A rotaviruses using all 11 genomic RNA segments. Arch. Virol. 2008; 153(8): 1621–9. https://doi.org/10.1007/s00705-008-0155-1
4. WHO. Manual of rotavirus detection and characterization methods. Geneva; 2009. Available at: https://www.who.int/vaccines-documents
5. Doro R., Laszlo B., Martella V., Leshem E., Gentsch J., Parashar U., et al. Review of global rotavirus strain prevalence data from six years post vaccine licensure surveillance: is there evidence of strain selection from vaccine pressure? Infect. Genet. Evol. 2014; 28: 446–61. https://doi.org/10.1016/j.meegid.2014.08.017
6. Zhou X., Wang Y.H., Ghosh S., Tang W.F., Pang B.B., Liu M.Q., et al. Genomic characterization of G3P[6], G4P[6] and G4P[8] human rotaviruses from Wuhan, China: Evidence for interspecies transmission and reassortment events. Infect. Genet. Evol. 2015; 33: 55–71. https://doi.org/10.1016/j.meegid.2015.04.010
7. Salamunova S., Jackova A., Csank T., Mandelik R., Novotny J., Beckova Z., et al. Genetic variability of pig and human rotavirus group A isolates from Slovakia. Arch. Virol. 2020; 165(2): 463–70. https://doi.org/10.1007/s00705-019-04504-6
8. Doro R., Farkas S.L., Martella V., Banyai K. Zoonotic transmission of rotavirus: surveillance and control. Expert. Rev. Anti. Infect. Ther. 2015; 13(11): 1337–50. https://doi.org/10.1586/14787210.2015.1089171
9. Velasquez D.E., Jiang B. Evolution of P[8], P[4], and P[6] VP8* genes of human rotaviruses globally reported during 1974 and 2017: possible implications for rotavirus vaccines in development. Hum. Vaccin. Immunother. 2019; 15(12): 3003–8. https://doi.org/10.1080/21645515.2019.1619400
10. Hungerford D., Vivancos R., Read J.M., Iturriza-Gomicronmara M., French N., Cunliffe N.A. Rotavirus vaccine impact and socioeconomic deprivation: an interrupted time-series analysis of gastrointestinal disease outcomes across primary and secondary care in the UK. BMC Med. 2018; 16(1): 10. https://doi.org/10.1186/s12916-017-0989-z
11. Freeman M.M., Kerin T., Hull J., McCaustland K., Gentsch J. Enhancement of detection and quantification of rotavirus in stool using a modified real-time RT-PCR assay. J. Med. Virol. 2008; 80(8): 1489–96. https://doi.org/10.1002/jmv.21228
12. Kiseleva V., Faizuloev E., Meskina E., Marova A., Oksanich A., Samartseva T., et al. Molecular-genetic characterization of human rotavirus a strains circulating in Moscow, Russia (2009- 2014). Virol. Sin. 2018; 33(4): 304–13. https://doi.org/10.1007/s12250-018-0043-0
13. Iturriza-Gomara M., Isherwood B., Desselberger U., Gray J. Reassortment in vivo: driving force for diversity of human rotavirus strains isolated in the United Kingdom between 1995 and 1999. J. Virol. 2001; 75(8): 3696–705. https://doi.org/10.1128/JVI.75.8.3696-3705.2001
14. Simmonds M.K., Armah G., Asmah R., Banerjee I., Damanka S., Esona M., et al. New oligonucleotide primers for P-typing of rotavirus strains: Strategies for typing previously untypeable strains. J. Clin. Virol. 2008; 42(4): 368–73. https://doi.org/10.1016/j.jcv.2008.02.011
15. Froussard P. rPCR: a powerful tool for random amplification of whole RNA sequences. PCR Methods Appl. 1993; 2(3): 185–90. https://doi.org/10.1101/gr.2.3.185
16. Li H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics. 2018; 34(18): 3094–100. https://doi.org/10.1093/bioinformatics/bty191
17. Maes P., Matthijnssens J., Rahman M., Van Ranst M. RotaC: a web-based tool for the complete genome classification of group A rotaviruses. BMC Microbiol. 2009; 9: 238. https://doi.org/10.1186/1471-2180-9-238
18. Faizuloev E., Mintaev R., Petrusha O., Marova A., Smirnova D., Ammour Y., et al. New approach to genetic characterization of group A rotaviruses by the nanopore sequencing method. J. Virol. Methods. 2021; 292: 114114. https://doi.org/10.1016/j.jviromet.2021.114114
19. Kumar S., Stecher G., Li M., Knyaz C., Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Mol. Biol. Evol. 2018; 35(6): 1547–9. https://doi.org/10.1093/molbev/msy096
20. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 1980; 16(2): 111–20. https://doi.org/10.1007/BF01731581
21. Cowley D., Donato C.M., Roczo-Farkas S., Kirkwood C.D. Emergence of a novel equine-like G3P[8] inter-genogroup reassortant rotavirus strain associated with gastroenteritis in Australian children. J. Gen. Virol. 2016; 97(2): 403–10. https://doi.org/10.1099/jgv.0.000352
22. Arana A., Montes M., Jere K.C., Alkorta M., Iturriza-Gomara M., Cilla G. Emergence and spread of G3P[8] rotaviruses possessing an equine-like VP7 and a DS-1-like genetic backbone in the Basque Country (North of Spain), 2015. Infect. Genet. Evol. 2016; 44: 137–44. https://doi.org/10.1016/j.meegid.2016.06.048
23. Doro R., Marton S., Bartokne A.H., Lengyel G., Agocs Z., Jakab F., et al. Equine-like G3 rotavirus in Hungary, 2015 — Is it a novel intergenogroup reassortant pandemic strain? Acta. Microbiol. Immunol. Hung. 2016; 63(2): 243–55. https://doi.org/10.1556/030.63.2016.2.8
24. Guerra S.F.S., Soares L.S., Lobo P.S., Penha Junior E.T., Sousa Junior E.C., Bezerra D.A.M., et al. Detection of a novel equinelike G3 rotavirus associated with acute gastroenteritis in Brazil. J. Gen. Virol. 2016; 97(12): 3131–8. https://doi.org/10.1099/jgv.0.000626
25. Komoto S., Tacharoenmuang R., Guntapong R., Ide T., Haga K., Katayama K., et al. Emergence and characterization of unusual DS-1-Like G1P[8] rotavirus strains in children with diarrhea in Thailand. PLoS One. 2015; 10(11): e0141739. https://doi.org/10.1371/journal.pone.0141739
26. Kaira A.N., Fayzuloyev E.B., Lavrov V.F., Svitich O.A., Solomay T.V., Nikonova A.A., et al. Epidemiological trends of morbidity and issues of rotavirus vaccination at the present stage. Sanitary Doctor. 2020; 6: 16–25. https://doi.org/0.33920/med-08-2006-02
27. Ivashechkin A.A., Yuzhakov A.G., Grebennikova T.V., Yuzhakova K.A., Kulikova N.Y., Kisteneva L.B., et al. Genetic diversity of group A rotaviruses in Moscow in 2018-2019. Arch. Virol. 2020; 165(3): 691–702. https://doi.org/10.1007/s00705-020-04534-5
28. Yuzhakov G., Yuzhakova K., Kulikova N., Kisteneva L., Cherepushkin S., Smetanina S., et al. Prevalence and genetic diversity of group a rotavirus genotypes in Moscow (2019–2020). Pathogens. 2021; 10: 674. https://doi.org/10.3390/pathogens10060674
29. Sashina T.A., Morozova O.V., Epifanova N.V., Novikova N.A. Predominance of new G9P[8] rotaviruses closely related to Turkish strains in Nizhny Novgorod (Russia). Arch. Virol. 2017; 162(8): 2387–92. https://doi.org/10.1007/s00705-017-3364-7
30. Novikova N.A., Sashina T.A., Solntsev L.A., Epifanova N.V., Kashnikov A.Yu., Pogodina L.V. i dr. Proyavlenie epidemicheskogo protsessa rotavirusnogo protsessa v Nizhnem Novgorode v predvaktsinal'nyi period. Zhurnal mikrobiologii, epidemiologii i immunobiologii. 2017; 94(5): 46–52. https://doi.org/10.36233/0372-9311-2017-5-46-52
31. Denisyuk N.B. Geneticheskaya kharakteristika rotavirusov gruppy A, tsirkuliruyushchikh v Orenburgskom regione v sezon 2016–2017 gg. Detskie infektsii. 2017; 16(4): 42–5. https://doi.org/10.22627/2072-8107-2017-16-4-42-45
32. Meskina E.R., Ushakova A.Yu., Faizuloev E.B., Bakhtoyarov G.N., Kiseleva V.V. Sravnitel'naya kharakteristika gastroenterita, vyzvannogo rotavirusami genotipov G4P[8] i G9P[8], u detei, gospitalizirovannykh v statsionar g. Moskvy (epidsezon 2012–2013 gg.). Infektsionnye bolezni. 2017; 15(1): 23–8. https://doi.org/10.20953/1729-9225-2017-1-23-28
33. Katz E.M., Esona M.D., Betrapally N.S., De La Cruz De Leon L.A., Neira Y.R., Rey G.J., et al. Whole-gene analysis of inter-genogroup reassortant rotaviruses from the Dominican Republic: Emergence of equine-like G3 strains and evidence of their reassortment with locally-circulating strains. Virology. 2019; 534: 114–31. https://doi.org/10.1016/j.virol.2019.06.007
34. Fujii Y., Oda M., Somura Y., Shinkai T. Molecular characteristics of novel mono-reassortant G9P[8] rotavirus a strains possessing the NSP4 gene of the E2 genotype detected in Tokyo, Japan. Jpn J. Infect. Dis. 2020; 73(1): 26–35. https://doi.org/10.7883/yoken.JJID.2019.211
35. McDonald S.M., Matthijnssens J., McAllen J.K., Hine E., Overton L., Wang S., et al. Evolutionary dynamics of human rotaviruses: balancing reassortment with preferred genome constellations. PLoS Pathog. 2009; 5(10): e1000634. https://doi.org/10.1371/journal.ppat.1000634
36. Papp H., Borzak R., Farkas S., Kisfali P., Lengyel G., Molnar P., et al. Zoonotic transmission of reassortant porcine G4P[6] rotaviruses in Hungarian pediatric patients identified sporadically over a 15 year period. Infect. Genet. Evol. 2013; 19: 71–80. https://doi.org/10.1016/j.meegid.2013.06.013
37. Esona M.D., Geyer A., Banyai K., Page N., Aminu M., Armah G.E., et al. Novel human rotavirus genotype G5P[7] from child with diarrhea, Cameroon. Emerg. Infect. Dis. 2009; 15(1): 83–6. https://doi.org/10.3201/eid1501.080899
38. Wang Y.H., Kobayashi N., Nagashima S., Zhou X., Ghosh S., Peng J.S., et al. Full genomic analysis of a porcine-bovine reassortant G4P[6] rotavirus strain R479 isolated from an infant in China. J. Med. Virol. 2010; 82(6): 1094–102. https://doi.org/10.1002/jmv.21760
39. Zeller M., Patton J.T., Heylen E., De Coster S., Ciarlet M., Van Ranst M., et al. Genetic analyses reveal differences in the VP7 and VP4 antigenic epitopes between human rotaviruses circulating in Belgium and rotaviruses in Rotarix and RotaTeq. J. Clin. Microbiol. 2012; 50(3): 966–76. https://doi.org/10.1128/JCM.05590-11
40. Imagawa T., Saito M., Yamamoto D., Saito-Obata M., Masago Y., Ablola A.C., et al. Genetic diversity of species A rotaviruses detected in clinical and environmental samples, including porcine-like rotaviruses from hospitalized children in the Philippines. Infect. Genet. Evol. 2020; 85: 104465. https://doi.org/10.1016/j.meegid.2020.104465
