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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/10.36233/0507-4088-2020-65-5-3

Аннотация

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

1. de Groot R.J., Baker S.C., Baric R., Enjuanes L., Gorbalenya A.E., Holmes K.V., et al. Family Coronaviridae. In: King A.M., Lefkowitz E., Adams M.J., Carstens E.B. Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses. London, San Diego: Elsevier Academic Press; 2011.

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

6. Николаева С.В., Зверева З.А., Каннер Е.В., Яцышина С.Б., Усенко Д.В., Горелов А.В. Клинико-лабораторная характеристика коронавирусной инфекции у детей. Инфекционные болезни. 2018; 16(1): 35-9. DOI: http://doi.org/10.20953/1729-9225-2018-1-35-39

7. Gaunt E.R., Hardie A., Claas E.C.J., Simmonds P., Templeton K.E. Epidemiology and clinical presentations of the four human coronaviruses 229E, HKU1, NL63, and OC43 detected over 3 years using a novel multiplex real-time PCR method. J. Clin. Microbiol. 2010; 48(8): 2940-7. DOI: http://doi.org/10.1128/JCM.00636-10

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

28. Яцышина С.Б., Спичак Т.В., Ким С.С., Воробьева Д.А., Агеева М.Р., Горелов А.В. и др. Выявление респираторных вирусов и атипичных бактерий у больных пневмонией и здоровых детей за десятилетний период наблюдения. Педиатрия. Журнал им. Г.Н. Сперанского. 2016; 95(2): 43-50.

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/10.36233/0507-4088-2020-65-5-3

Abstract

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

1. de Groot R.J., Baker S.C., Baric R., Enjuanes L., Gorbalenya A.E., Holmes K.V., et al. Family Coronaviridae. In: King A.M., Lefkowitz E., Adams M.J., Carstens E.B. Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses. London, San Diego: Elsevier Academic Press; 2011.

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

6. Nikolaeva S.V., Zvereva Z.A., Kanner E.V., Yatsyshina S.B., Usenko D.V., Gorelov A.V. Kliniko-laboratornaya kharakteristika koronavirusnoi infektsii u detei. Infektsionnye bolezni. 2018; 16(1): 35-9. DOI: http://doi.org/10.20953/1729-9225-2018-1-35-39

7. Gaunt E.R., Hardie A., Claas E.C.J., Simmonds P., Templeton K.E. Epidemiology and clinical presentations of the four human coronaviruses 229E, HKU1, NL63, and OC43 detected over 3 years using a novel multiplex real-time PCR method. J. Clin. Microbiol. 2010; 48(8): 2940-7. DOI: http://doi.org/10.1128/JCM.00636-10

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

28. Yatsyshina S.B., Spichak T.V., Kim S.S., Vorob'eva D.A., Ageeva M.R., Gorelov A.V. i dr. Vyyavlenie respiratornykh virusov i atipichnykh bakterii u bol'nykh pnevmoniei i zdorovykh detei za desyatiletnii period nablyudeniya. Pediatriya. Zhurnal im. G.N. Speranskogo. 2016; 95(2): 43-50.

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