Вопросы вирусологии. 2020; 65: 267-276
Анализ циркуляции коронавирусов человека
Яцышина С. Б., Мамошина М. В., Шипулина О. Ю., Подколзин А. Т., Акимкин В. Г.
https://doi.org/10.36233/0507-4088-2020-65-5-3Аннотация
Введение. Появление в конце 2019 г. нового коронавируса SARS-CoV-2, ставшего причиной пандемии, породило массу вопросов относительно эпидемиологии нового заболевания COVID-19 и известных ранее инфекций, вызываемых коронавирусами, которым по причине более лёгкого течения заболеваний уделяли мало внимания.
Цель данной работы – многолетнее ретроспективное исследование распространённости и особенностей циркуляции эпидемических коронавирусов человека в Москве при проведении рутинного скрининга.
Материал и методы. Методом полимеразной цепной реакции с детекцией в режиме реального времени исследовали на РНК эпидемических коронавирусов человека (HCoVs) мазки из носо- и ротоглотки 16 511 больных острой респираторной инфекцией (ОРИ) в возрасте от 1 мес до 95 лет (58,3% составили дети), собранные с января 2016 г. по март 2020 г., и мазки 505 условно-здоровых детей, собранные в 2008, 2010 и 2011 гг.
Результаты. HCoVs обнаруживали у 2,6–6,1% обследованных больных в год, статистически значимо чаще у взрослых по сравнению с детьми, без различий по полу. На пике заболеваемости в декабре 2019 г. HCoVs обнаружены у 13,7% обследованных, что в 2 раза выше среднемноголетнего уровня данного месяца. У больных ОРИ детей до 6 лет HCoVs выявляли статистически значимо чаще, чем у здоровых (3,7 vs 0,7%, p = 0,008).
Заключение. HCoVs циркулируют ежегодно, демонстрируя в Московском регионе зимне- весеннюю сезонность с пиком в декабре. За годы наблюдения эпидемическая активность HCoVs росла до максимальных значений в декабре 2019 г. – феврале 2020 г., снизившись в марте до среднемноголетнего уровня. На фоне растущего количества случаев завоза SARS-CoV-2 в Москву в марте 2020 г. частота выявления HCoVs резко понизилась, что, по-видимому, отражает наличие конкуренции между разными коронавирусами и подтверждает специфичность выявления HCoVs использованным в данной работе диагностическим набором.
Список литературы
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11. Poland A.M., Vennema H., Foley J.E., Pedersen N.C. Two related strains of feline infectious peritonitis virus isolated from immunocompromised cats infected with a feline enteric coronavirus. J. Clin. Microbiol. 1996; 34(12): 3180-4.
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13. Lu S., Wang Y., Chen Y., Wu B., Qin K., Zhao J., et al. Discovery of a novel canine respiratory coronavirus support genetic recombination among betacoronavirus1. Virus Res. 2017; 237: 7-13. DOI: http://doi.org/10.1016/j.virusres.2017.05.006
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15. Luk H.K.H., Li X., Fung J., Lau S.K.P., Woo P.C.Y. Molecular epidemiology, evolution and phylogeny of SARS coronavirus. Infect. Genet. Evol. 2019; 71: 21-30. DOI: http://doi.org/10.1016/j.meegid.2019.03.001
16. Abdel-Moneim A.S. Middle East respiratory syndrome coronavirus (MERS-CoV): evidence and speculations. Arch. Virol. 2014; 159(7): 1575-84. DOI: http://doi.org/10.1007/s00705-014-1995-5
17. Andersen K.G., Rambaut A., Lipkin W.I., Holmes E.C., Garry R.F. The proximal origin of SARS-CoV-2. Nat. Med. 2020; 26(4): 450-2. DOI: http://doi.org/10.1038/s41591-020-0820-9
18. Corman V.M., Muth D., Niemeyer D., Drosten C. Hosts and sources of endemic human coronaviruses. Adv. Virus Res. 2018; 100: 163-88. DOI: http://doi.org/10.1016/bs.aivir.2018.01.001
19. Ye Z.W., Yuan S., Yuen K.S., Fung S.Y., Chan C.P., Jin D.Y. Zoonotic origins of human coronaviruses. Int. J. Biol. Sci. 2020; 16(10): 1686-97. DOI: http://doi.org/10.7150/ijbs.45472
20. Wertheim J.O., Chu D.K., Peiris J.S., Kosakovsky Pond S.L., Poon L.L. A case for the ancient origin of coronaviruses. J. Virol. 2013; 87(12): 7039-45. DOI: http://doi.org/10.1128/JVI.03273-12
21. Jevšnik M., Uršič T., Zigon N., Lusa L., Krivec U., Petrovec M. Coronavirus infections in hospitalized pediatric patients with acute respiratory tract disease. BMC Infect. Dis. 2012; 12: 365. DOI: http://doi.org/10.1186/1471-2334-12-365
22. Varghese L., Zachariah P., Vargas C., LaRussa P., Demmer R.T., Furuya Y.E., et al. Epidemiology and clinical features of human coronaviruses in the pediatric population. J. Pediatric. Infect. Dis. Soc. 2018; 7(2): 151-8. DOI: http://doi.org/10.1093/jpids/pix027
23. Monto A.S., Cowling B.J., Peiris J.S.M. Coronaviruses. In: Kaslow R.A., Stanberry L.R., Le Duc J.W., eds. Viral Infections of Humans: Epidemiology and Control. Boston, MA: Springer US; 2014: 199-223. DOI: http://doi.org/10.1007/978-1-4899-7448-8_10
24. Dominguez S.R., Robinson C.C., Holmes K.V. Detection of four human coronaviruses in respiratory infections in children: a oneyear study in Colorado. J. Med. Virol. 2009; 81(9): 1597-604. DOI: http://doi.org/10.1002/jmv.21541
25. Jevšnik M., Steyer A., Pokorn M., Mrvič T., Grosek Š., Strle F., et al. The role of human coronaviruses in children hospitalized for acute bronchiolitis, acute gastroenteritis, and febrile seizures: a 2-year prospective study. PLoS One. 2016; 11(5): e0155555. DOI: http://doi.org/10.1371/journal.pone.0155555
26. Vabret A., Dina J., Gouarin S., Petitjean J., Tripey V., Brouard J., et al. Human (non-severe acute respiratory syndrome) coronavirus infections in hospitalised children in France. J. Paediatr. Child Health. 2008; 44(4): 176-81. DOI: http://doi.org/10.1111/j.1440-1754.2007.01246.x.
27. Friedman N., Alter H., Hindiyeh M., Mendelson E., Shemer Avni Y., Mandelboim M. Human coronavirus infections in Israel: epidemiology, clinical symptoms and summer seasonality of HCoV-HKU1. Viruses. 2018; 10(10): 515. DOI: http://doi.org/10.3390/v10100515
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29. Sauro J., Lewis J. Estimating completion rates from small samples using binomial confidence intervals: comparisons and recommendations. Proc. Hum. Factors Ergon. Soc. Annu. Meet. 2005; 49(24): 2100-3. DOI: http://doi.org/10.1177/154193120504902407
30. Heimdal I., Moe N., Krokstad S., Christensen A., Skanke L.H., Nordbø S.A., et al. Human coronavirus in hospitalized children with respiratory tract infections: a 9-year population-based study from Norway. J. Infect. Dis. 2019; 219(8): 1198-206. DOI: http://doi.org/10.1093/infdis/jiy646
31. Chiu S.S., Chan K.H., Chu K.W., Kwan S.W., Guan Y., Poon L.L.M., et al. Human coronavirus NL63 infection and other coronavirus infections in children hospitalized with acute respiratory disease in Hong Kong, China. Clin. Infect. Dis. 2005; 40(12): 1721-9. DOI: http://doi.org/10.1086/430301
32. Li Y., Reeves R.M., Wang X., Bassat Q., Brooks W.A., Cohen C., et al. Global patterns in monthly activity of influenza virus, respiratory syncytial virus, parainfluenza virus, and metapneumovirus: a systematic analysis. Lancet Glob. Health. 2019; 7(8): e1031-45. DOI: http://doi.org/10.1016/S2214-109X(19)30264-5
33. Biggs H.M., Killerby M.E., Haynes A.K., Dahl R.M., Gerber S.I., Watson J.T. Human coronavirus circulation in the USA, 2014 ‒ 2017. Open. Forum Infect. Dis. 2017; 4(Suppl. 1): S311-2. DOI: http://doi.org/10.1093/ofid/ofx163.727
34. Gorse G.J., Patel G.B., Vitale J.N., O’Connor T.Z. Prevalence of antibodies to four human coronaviruses is lower in nasal secretions than in serum. Clin. Vaccine Immunol. 2010; 17(12): 1875-80. DOI: http://doi.org/10.1128/CVI.00278-10
35. Chan C.M., Tse H., Wong S.S.Y., Woo P.C.Y., Lau S.K.P., Chen L., et al. Examination of seroprevalence of coronavirus HKU1 infection with S protein-based ELISA and neutralization assay against viral spike pseudotyped virus. J. Clin. Virol. 2009; 45(1): 54-60. DOI: http://doi.org/10.1016/j.jcv.2009.02.011
36. McIntosh K., Dees J.H., Becker W.B., Kapikian A.Z., Chanock R.M. Recovery in tracheal organ cultures of novel viruses from patients with respiratory disease. Proc. Natl. Acad. Sci. USA. 1967; 57(4): 933-40. DOI: http://doi.org/10.1073/pnas.57.4.933
Problems of Virology. 2020; 65: 267-276
Analysis of human coronaviruses circulation
Yatsyshina S. B., Mamoshina M. V., Shipulina O. Yu., Podkolzin A. T., Akimkin V. G.
https://doi.org/10.36233/0507-4088-2020-65-5-3Abstract
Introduction. The novel SARS-CoV-2 coronavirus, which emerged at the end of 2019 and caused a worldwide pandemic, triggered numerous questions about the epidemiology of the novel COVID-19 disease and about wellknown coronavirus infections, which used to be given little attention due to their mild symptoms.
The purpose: The routine screening-based multiyear retrospective observational study of prevalence and circulation patterns of epidemic-prone human coronaviruses in Moscow.
Material and methods. The real-time polymerase chain reaction was used to detect RNA of human coronaviruses (HCoVs) in nasal and throat swabs from 16,511 patients with an acute respiratory infection (ARI), aged 1 month to 95 years (children accounted for 58.3%) from January 2016 to March 2020, and swabs from 505 relatively healthy children in 2008, 2010 and 2011.
Results. HCoVs were yearly found in 2.6–6.1% of the examined patients; the detection frequency was statistically higher in adults than in children, regardless of sex. At the height of the disease incidence in December 2019, HCoVs were detected in 13.7% of the examined, demonstrating a two-fold increase as compared to the multi-year average for that month. The statistical frequency of HCoV detection in ARI pediatric patients under 6 years was significantly higher than in their healthy peers (3.7 vs 0.7%, p = 0.008).
Conclusion. HCoVs circulate annually, demonstrating a winter-spring seasonal activity pattern in the Moscow Region and reaching peak levels in December. Over the years of observation, the HCoV epidemic activity reached maximum levels in December 2019–February 2020 and decreased in March to the multi-year average. Amid a growing number of SARS-CoV-2 cases imported to Moscow in March 2020, the HCoV detection frequency dropped sharply, which can be explained by the competition between different coronaviruses and by the specificity of HCoV detection with the diagnostic test kit used in this study.
References
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2. Cabeça T.K., Granato C., Bellei N. Epidemiological and clinical features of human coronavirus infections among different subsets of patients. Influenza Other Respir. Viruses. 2013; 7(6): 1040-7. DOI: http://doi.org/10.1111/irv.12101
3. Bradburne A.F., Bynoe M.L., Tyrrell D.A. Effects of a «new» human respiratory virus in volunteers. Br. Med. J. 1967; 3(5568): 767-9. DOI: http://doi.org/10.1136/bmj.3.5568.767
4. Esposito S., Bosis S., Niesters H.G.M., Tremolati E., Begliatti E., Rognoni A., et al. Impact of human coronavirus infections in otherwise healthy children who attended an emergency department. J. Med. Virol. 2006; 78(12): 1609-15. DOI: http://doi.org/10.1002/jmv.20745
5. Dare R.K., Fry A.M., Chittaganpitch M., Sawanpanyalert P., Olsen S.J., Erdman D.D. Human coronavirus infections in rural Thailand: a comprehensive study using real-time reverse-transcription polymerase chain reaction assays. J. Infect. Dis. 2007; 196(9): 1321-8. DOI: http://doi.org/10.1086/521308
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8. Woo P.C.Y., Lau S.K.P., Chu C., Chan K., Tsoi H., Huang Y., et al. Characterization and complete genome sequence of a novel coronavirus, coronavirus HKU1, from patients with pneumonia. J Virol. 2005; 79(2): 884-95. DOI: http://doi.org/10.1128/JVI.79.2.884-895.2005
9. Dent S., Neuman B.W. Purification of coronavirus virions for CryoEM and proteomic analysis. Methods Mol. Biol. 2015; 1282: 99-108. DOI: https://doi.org/ 10.1007/978-1-4939-2438-7_10
10. Gralinski L.E., Baric R.S. Molecular pathology of emerging coronavirus infections. J. Pathol. 2015; 235(2): 185-95. DOI: http://doi.org/10.1002/path.4454
11. Poland A.M., Vennema H., Foley J.E., Pedersen N.C. Two related strains of feline infectious peritonitis virus isolated from immunocompromised cats infected with a feline enteric coronavirus. J. Clin. Microbiol. 1996; 34(12): 3180-4.
12. Woo P.C., Lau S.K., Huang Y., Yuen K.Y. Coronavirus diversity, phylogeny and interspecies jumping. Exp. Biol. Med. (Maywood). 2009; 234(10): 1117-27. DOI: http://doi.org/10.3181/0903-MR-94/
13. Lu S., Wang Y., Chen Y., Wu B., Qin K., Zhao J., et al. Discovery of a novel canine respiratory coronavirus support genetic recombination among betacoronavirus1. Virus Res. 2017; 237: 7-13. DOI: http://doi.org/10.1016/j.virusres.2017.05.006
14. Poon L.L.M., Chu D.K.W., Chan K.H., Wong O.K., Ellis T.M., Leung Y.H.C., et al. Identification of a novel coronavirus in bats. J. Virol. 2005; 79(4): 2001-9. DOI: http://doi.org/10.1128/JVI.79.4.2001-2009.2005
15. Luk H.K.H., Li X., Fung J., Lau S.K.P., Woo P.C.Y. Molecular epidemiology, evolution and phylogeny of SARS coronavirus. Infect. Genet. Evol. 2019; 71: 21-30. DOI: http://doi.org/10.1016/j.meegid.2019.03.001
16. Abdel-Moneim A.S. Middle East respiratory syndrome coronavirus (MERS-CoV): evidence and speculations. Arch. Virol. 2014; 159(7): 1575-84. DOI: http://doi.org/10.1007/s00705-014-1995-5
17. Andersen K.G., Rambaut A., Lipkin W.I., Holmes E.C., Garry R.F. The proximal origin of SARS-CoV-2. Nat. Med. 2020; 26(4): 450-2. DOI: http://doi.org/10.1038/s41591-020-0820-9
18. Corman V.M., Muth D., Niemeyer D., Drosten C. Hosts and sources of endemic human coronaviruses. Adv. Virus Res. 2018; 100: 163-88. DOI: http://doi.org/10.1016/bs.aivir.2018.01.001
19. Ye Z.W., Yuan S., Yuen K.S., Fung S.Y., Chan C.P., Jin D.Y. Zoonotic origins of human coronaviruses. Int. J. Biol. Sci. 2020; 16(10): 1686-97. DOI: http://doi.org/10.7150/ijbs.45472
20. Wertheim J.O., Chu D.K., Peiris J.S., Kosakovsky Pond S.L., Poon L.L. A case for the ancient origin of coronaviruses. J. Virol. 2013; 87(12): 7039-45. DOI: http://doi.org/10.1128/JVI.03273-12
21. Jevšnik M., Uršič T., Zigon N., Lusa L., Krivec U., Petrovec M. Coronavirus infections in hospitalized pediatric patients with acute respiratory tract disease. BMC Infect. Dis. 2012; 12: 365. DOI: http://doi.org/10.1186/1471-2334-12-365
22. Varghese L., Zachariah P., Vargas C., LaRussa P., Demmer R.T., Furuya Y.E., et al. Epidemiology and clinical features of human coronaviruses in the pediatric population. J. Pediatric. Infect. Dis. Soc. 2018; 7(2): 151-8. DOI: http://doi.org/10.1093/jpids/pix027
23. Monto A.S., Cowling B.J., Peiris J.S.M. Coronaviruses. In: Kaslow R.A., Stanberry L.R., Le Duc J.W., eds. Viral Infections of Humans: Epidemiology and Control. Boston, MA: Springer US; 2014: 199-223. DOI: http://doi.org/10.1007/978-1-4899-7448-8_10
24. Dominguez S.R., Robinson C.C., Holmes K.V. Detection of four human coronaviruses in respiratory infections in children: a oneyear study in Colorado. J. Med. Virol. 2009; 81(9): 1597-604. DOI: http://doi.org/10.1002/jmv.21541
25. Jevšnik M., Steyer A., Pokorn M., Mrvič T., Grosek Š., Strle F., et al. The role of human coronaviruses in children hospitalized for acute bronchiolitis, acute gastroenteritis, and febrile seizures: a 2-year prospective study. PLoS One. 2016; 11(5): e0155555. DOI: http://doi.org/10.1371/journal.pone.0155555
26. Vabret A., Dina J., Gouarin S., Petitjean J., Tripey V., Brouard J., et al. Human (non-severe acute respiratory syndrome) coronavirus infections in hospitalised children in France. J. Paediatr. Child Health. 2008; 44(4): 176-81. DOI: http://doi.org/10.1111/j.1440-1754.2007.01246.x.
27. Friedman N., Alter H., Hindiyeh M., Mendelson E., Shemer Avni Y., Mandelboim M. Human coronavirus infections in Israel: epidemiology, clinical symptoms and summer seasonality of HCoV-HKU1. Viruses. 2018; 10(10): 515. DOI: http://doi.org/10.3390/v10100515
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29. Sauro J., Lewis J. Estimating completion rates from small samples using binomial confidence intervals: comparisons and recommendations. Proc. Hum. Factors Ergon. Soc. Annu. Meet. 2005; 49(24): 2100-3. DOI: http://doi.org/10.1177/154193120504902407
30. Heimdal I., Moe N., Krokstad S., Christensen A., Skanke L.H., Nordbø S.A., et al. Human coronavirus in hospitalized children with respiratory tract infections: a 9-year population-based study from Norway. J. Infect. Dis. 2019; 219(8): 1198-206. DOI: http://doi.org/10.1093/infdis/jiy646
31. Chiu S.S., Chan K.H., Chu K.W., Kwan S.W., Guan Y., Poon L.L.M., et al. Human coronavirus NL63 infection and other coronavirus infections in children hospitalized with acute respiratory disease in Hong Kong, China. Clin. Infect. Dis. 2005; 40(12): 1721-9. DOI: http://doi.org/10.1086/430301
32. Li Y., Reeves R.M., Wang X., Bassat Q., Brooks W.A., Cohen C., et al. Global patterns in monthly activity of influenza virus, respiratory syncytial virus, parainfluenza virus, and metapneumovirus: a systematic analysis. Lancet Glob. Health. 2019; 7(8): e1031-45. DOI: http://doi.org/10.1016/S2214-109X(19)30264-5
33. Biggs H.M., Killerby M.E., Haynes A.K., Dahl R.M., Gerber S.I., Watson J.T. Human coronavirus circulation in the USA, 2014 ‒ 2017. Open. Forum Infect. Dis. 2017; 4(Suppl. 1): S311-2. DOI: http://doi.org/10.1093/ofid/ofx163.727
34. Gorse G.J., Patel G.B., Vitale J.N., O’Connor T.Z. Prevalence of antibodies to four human coronaviruses is lower in nasal secretions than in serum. Clin. Vaccine Immunol. 2010; 17(12): 1875-80. DOI: http://doi.org/10.1128/CVI.00278-10
35. Chan C.M., Tse H., Wong S.S.Y., Woo P.C.Y., Lau S.K.P., Chen L., et al. Examination of seroprevalence of coronavirus HKU1 infection with S protein-based ELISA and neutralization assay against viral spike pseudotyped virus. J. Clin. Virol. 2009; 45(1): 54-60. DOI: http://doi.org/10.1016/j.jcv.2009.02.011
36. McIntosh K., Dees J.H., Becker W.B., Kapikian A.Z., Chanock R.M. Recovery in tracheal organ cultures of novel viruses from patients with respiratory disease. Proc. Natl. Acad. Sci. USA. 1967; 57(4): 933-40. DOI: http://doi.org/10.1073/pnas.57.4.933
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