Salient features of circulating respiratory viruses in the pre- and pandemic influenza and COVID-19 seasons

Cover Page


Cite item

Full Text

Abstract

A wide variety of zoonotic viruses that can cross the interspecies barrier promote the emergence of new, potentially pandemic viruses in the human population that is often accompanied by the disappearance of existing circulating strains. Among the various reasons underlying this phenomenon is the strengthening of herd immunity by expanding the immune layer of population and improving means and methods of medical care. However, natura abhorret vacuum, and new pathogens come to replace disappearing ones. Over the past ten years, humanity has faced two pandemics: swine flu A(H1N1)pdm09 in 2009 and COVID-19 in 2019, providing scientists with a unique opportunity to learn more about a relationship between respiratory viruses and their pathogenesis. Together with viruses of pandemic significance, a large number of seasonal respiratory viruses circulate, which contribute to the structure of human morbidity, and coinfections aggravate the condition of the illness. In the conditions of the spread of new viruses with unexplored characteristics, in the absence of means of prevention and therapy, it is especially important to prevent the aggravation of morbidity due to mixed infections. Here we review the mutual involvement of pandemic influenza A(H1N1)pdm09 and SARS-CoV-2 coronavirus and seasonal respiratory viruses in the epidemic process, discuss some issues related to their spread, potential causes affecting the spread and severity of the morbidity. The given facts testify to the existence of seasonality and temporal patterns of the beginning and end of respiratory viruses circulation. Interestingly, the beginning of circulation of the pandemic influenza A(H1N1)pdm09 virus led to a shift in the timing and intensity of circulation of some respiratory viruses, which is probably caused by existence of “replication conflicts” between them, and did not affect others. Coinfection with SARS-CoV-2-19 and other respiratory viruses, especially respiratory syncytial virus and rhinoviruses, was quite often observed. At the current stage, no aggravating effect of influenza on the course of COVID-19 in mixed infection has been established. Whether this is due to the mild course of influenza infection in the 2020 epidemic season, or the competitive impact of SARS-CoV-2 on influenza viruses is not yet clear. Experts are still at the stage of accumulating facts and working on creating means of effective prevention and treatment of the new coronavirus infection.

About the authors

I. V. Kiseleva

Institute of Experimental Medicine; St. Petersburg State University

Author for correspondence.
Email: irina.v.kiseleva@mail.ru
ORCID iD: 0000-0002-3892-9873

Irina V. Kiseleva - PhD, MD (Biology), Professor, Head of the Laboratory of General Virology, Institute of Experimental Medicine; Professor, Department of Fundamental Problems of Medicine and Medical technologies, St. Petersburg State University.

197376, St. Petersburg, Academician Pavlov str., 12.

Phone: +7 (812) 234-68-60. Fax: +7 (812) 234-68-68.

Russian Federation

N. V. Larionova

Institute of Experimental Medicine

Email: nvlarionova@mail.ru
ORCID iD: 0000-0003-1171-3383

PhD, MD (Biology), Leading Researcher, Laboratory of General Virology, Institute of Experimental Medicine.

St. Petersburg.

Russian Federation

E. P. Grigorieva

Institute of Experimental Medicine

Email: epgrigorieva@gmail.com
ORCID iD: 0000-0002-8439-6502

PhD (Мedicine), Senior Researcher, Laboratory of General Virology, Institute of Experimental Medicine.

St. Petersburg.

Russian Federation

A. D. Ksenafontov

Smorodintsev Research Institute of Influenza

Email: ksenandrey@yandex.ru
ORCID iD: 0000-0002-4532-6210

PhD Student, Smorodintsev Research Institute of Influenza.

St. Petersburg.

Russian Federation

M. Al Farroukh

Institute of Experimental Medicine

Email: mouhammad1farroukh@gmail.com
ORCID iD: 0000-0003-0017-4126

PhD Student, Institute of Experimental Medicine.

St. Petersburg.

Russian Federation

L. G. Rudenko

Institute of Experimental Medicine

Email: vaccine@mail.ru
ORCID iD: 0000-0002-0107-9959

PhD, MD (Мedicine), Professor, Head of the A.A. Smorodintsev Department of Virology, Institute of Experimental Medicine.

St. Petersburg.

Russian Federation

References

  1. Базан О.И. Патологоанатомическая служба в блокадном Ленинграде. Научный анализ, личные воспоминания. СПб.: ЭЛБИ-СПб., 2006. 134 с.
  2. Беляев А.Л., Феодоритова Е.Л., Слепушкин А.Н. Итоги эпидсезона 2007–2008 гг. по гриппу и другим ОРВИ и профилактика этих инфекций // Пест-Менеджмент. 2008. № 3. С. 26–31.
  3. Львов Д.К., Бурцева Е.И., Мукашева Е.А., Колобухина Л.В., Трушакова С.В., Бреслав Н.В., Феодоритова Е.Л., Меркулова Л.Н., Краснослободцев К.Г., Морозова Е.О., Федякина И.Т., Аристова В.А., Вартанян Р.В., Кистенева Л.Б., Прилипов А.Г., Альховский С.В., Росаткевич А.Г., Кружкова И.С., Беляев А.Л., Аксельрод Э.В., Базарова М.В., Сметанина С.В. Активность вирусов гриппа в сезон 2017–2018 гг. в России и странах Северного полушария: конфликт по В-вирусному компоненту вакцин // Эпидемиология и вакцинопрофилактика. 2018. Т. 19, № 3. С. 13–21. doi: 10.31631/2073-3046-2019-18-3-13-21
  4. Львов Д.К., Колобухина Л.В., Бурцева Е.И., Кружкова И.С., Малышев Н.А., Федякина И.Т., Кириллова Е.С., Трушакова С.В., Феодоритова Е.Л., Меркулова Л.Н., Краснослободцев К.Г., Мукашева Е.А., Гарина Е.О., Вартанян Р.В., Кистенева Л.Б., Прилипов А.Г., Базарова М.В., Девяткин А.В., Суточникова О.А. Эпидемический сезон 2015–2016 гг. в России и мире: особенности циркуляции вирусов гриппа, динамика заболеваемости, клинические аспекты и алгоритм лечения // Терапевтический архив. 2016. Т. 88, № 11. С. 112–120. doi: 10.17116/terarkh20168811112-120
  5. Морозенко М.А., Микуцкая Б.А., Сиротенко Е.А., Тимофеева Г.А., Смородинцев А.А. Удельный вес респираторно-синцитиальной инфекции в межэпидемические по гриппу периоды в Ленинграде. В кн.: Проблемы этиологии, диагностики, профилактики и клиники респираторных вирусных инфекций. Л., 1969. С. 417–424.
  6. Писарева М.М., Едер В.А., Бузицкая Ж.В., Мусаева Т.Д., Афанасьева В.С., Го А.А., Образцова Е.А., Суховецкая В.Ф., Комиссаров А.Б. Этиологическая структура гриппа и других ОРВИ в Санкт-Петербурге в эпидемические сезоны 2012–2016 гг. // Вопросы вирусологии. 2018. Т. 63, № 5. С. 233–239. doi: 10.18821/0507-4088-2018-63-5-233-239
  7. Akin L., Gözel M.G. Understanding dynamics of pandemics. Turk. J. Med. Sci., 2020, vol. 50, no. SI–1, pp. 515–519. doi: 10.3906/sag-2004-133
  8. Alcaide C., Rabadan M.P., Moreno-Perez M.G., Gomez P. Implications of mixed viral infections on plant disease ecology and evolution. Adv. Virus Res., 2020, vol. 106, pp. 145–169. doi: 10.1016/bs.aivir.2020.02.001
  9. Ånestad G. Interference between outbreaks of respiratory syncytial virus and influenza virus infection. Lancet, 1982, vol. 1, no. 8270, p. 502. doi: 10.1016/s0140-6736(82)91466-0
  10. Azekawa S., Namkoong H., Mitamura K., Kawaoka Y., Saito F. Co-infection with SARS-CoV-2 and influenza A virus. IDCases, 2020, vol. 20: e00775. doi: 10.1016/j.idcr.2020.e00775
  11. Babiuk L.A., Lawman M.J., Ohmann H.B. Viral-bacterial synergistic interaction in respiratory disease. Adv. Virus Res., 1988, vol. 35, pp. 219–249. doi: 10.1016/s0065-3527(08)60713-7
  12. Belser J.A. Assessment of SARS-CoV-2 replication in the context of other respiratory viruses. Lancet Respir. Med., 2020, vol. 8, no. 7, pp. 651–652. doi: 10.1016/S2213-2600(20)30227-7
  13. Bengoechea J.A., Bamford C.G.G. SARS-CoV-2, bacterial co-infections, and AMR: the deadly trio in COVID-19? EMBO Mol. Med., 2020, vol. 12, no. 7: e12560. doi: 10.15252/emmm.202012560
  14. Benkovic S., Kim M., Sin E. Four cases: HIV and SARS-CoV-2 coinfection in patients from Long Island, New York. J. Med. Virol., 2020, vol. 92, no. 11, pp. 2338–2340. doi: 10.1002/jmv.26029
  15. Bogaert D., Dockrell D.H. 100 years of influenza research seen through the lens of COVID-19. Mucosal Immunol., 2020, vol. 13, no. 4, pp. 561–562. doi: 10.1038/s41385-020-0291-9
  16. Bosch A.A., Biesbroek G., Trzcinski K., Sanders E.A., Bogaert D. Viral and bacterial interactions in the upper respiratory tract. PLoS Pathog., 2013, vol. 9, no. 1: e1003057. doi: 10.1371/journal.ppat.1003057
  17. Calderaro A., De Conto F., Buttrini M., Piccolo G., Montecchin S., Maccari C., Martinelli M., Di Maio A., Ferraglia F., Pinardi F., Montagna P., Arcangeletti M.C., Chezzi C. Human respiratory viruses, including SARS-CoV-2, circulating in the winter season 2019–2020 in Parma, Northern Italy. Int. J. Infect. Dis., 2020, vol. 102, pp. 79–84. doi: 10.1016/j.ijid.2020.09.1473
  18. Casalegno J.S., Ottmann M., Duchamp M.B., Escuret V., Billaud G., Frobert E., Morfin F., Lina B. Rhinoviruses delayed the circulation of the pandemic influenza A (H1N1) 2009 virus in France. Clin. Microbiol. Infect., 2010, vol. 16, no. 4, pp. 326–329. doi: 10.1111/j.14690691.2010.03167.x
  19. Coughlin S.S. Anxiety and depression: linkages with viral diseases. Public Health Rev., 2012, vol. 34, no. 2, 17 p. doi: 10.1007/BF03391675
  20. Cuadrado-Payán E., Montagud-Marrahi E., Torres-Elorza M., Bodro M., Blasco M., Poch E., Soriano A., Piñeiro G.J. SARS-CoV-2 and influenza virus coinfection. Lancet, 2020, vol. 395, no. 10236: e84. doi: 10.1016/S0140-6736(20)31052-7
  21. D’Ardes D., Boccatonda A., Schiavone C., Santilli F., Guagnano M.T., Bucci M., Cipollone F. A case of coinfection with SARS-CoV-2 and cytomegalovirus in the era of COVID-19. Eur. J. Case Rep. Intern. Med., 2020, vol. 7, no. 5: 001652. doi: 10.12890/2020_001652
  22. Dawood F.S., Iuliano A.D., Reed C., Meltzer M.I., Shay D.K., Cheng P.Y., Bandaranayake D., Breiman R.F., Brooks W.A., Buchy P., Feikin D.R., Fowler K.B., Gordon A., Hien N.T., Horby P., Huang Q.S., Katz M.A., Krishnan A., Lal R., Montgomery J.M., Mølbak K., Pebody R., Presanis A.M., Razuri H., Steens A., Tinoco Y.O., Wallinga J., Yu H., Vong S., Bresee J., Widdowson M.A. Estimated global mortality associated with the first 12 months of 2009 pandemic influenza A H1N1 virus circulation: a modelling study. Lancet Infect. Dis., 2012, vol. 12, no. 9, pp. 687–695. doi: 10.1016/S1473-3099(12)70121-4
  23. Dhabhar F.S., Malarkey W.B., Neri E., McEwen B.S. Stress-induced redistribution of immune cells — from barracks to boulevards to battlefields: a tale of three hormones — Curt Richter Award winner. Psychoneuroendocrinology, 2012, vol. 37, no. 9, pp. 1345–1368. doi: 10.1016/j.psyneuen.2012.05.008
  24. Diaz-Munoz S.L. Viral coinfection is shaped by host ecology and virus–virus interactions across diverse microbial taxa and environments. Virus Evol., 2017, vol. 3, no. 1: vex011. doi: 10.1093/ve/vex011
  25. Ding Q., Lu P., Fan Y., Xia Y., Liu M. The clinical characteristics of pneumonia patients coinfected with 2019 novel coronavirus and influenza virus in Wuhan, China. J. Med. Virol., 2020, vol. 92, no. 9, pp. 1549–1555. doi: 10.1002/jmv.25781
  26. Dunning J., Thwaites R.S., Openshaw P.J.M. Seasonal and pandemic influenza: 100 years of progress, still much to learn. Mucosal Immunol., 2020, vol. 13, no. 4, pp. 566–573. doi: 10.1038/s41385-020-0287-5
  27. Hashemi S.A., Safamanesh S., Ghafouri M., Taghavi M.R., Mohajer Zadeh Heydari M.S., Namdar Ahmadabad H., Ghasem Zadeh-Moghaddam H., Azimian A. Coinfection with COVID-19 and influenza A virus in two died patients with acute respiratory syndrome, Bojnurd, Iran. J. Med. Virol., 2020, vol. 92, no. 11, pp. 2319–2321. doi: 10.1002/jmv.26014
  28. Johnson N.P., Mueller J. Updating the accounts: global mortality of the 1918–1920 “Spanish” influenza pandemic. Bull. Hist. Med., 2002, vol. 76, no. 1, pp. 105–115. doi: 10.1353/bhm.2002.0022
  29. Jones N. How coronavirus lockdowns stopped flu in its tracks. Nature news. 21 May 2020. URL: https://www.nature.com/articles/d41586-020-01538-8
  30. Kakuya F., Okubo H., Fujiyasu H., Wakabayashi I., Syouji M., Kinebuchi T. The first pediatric patients with coronavirus disease 2019 (COVID-19) in Japan: risk of coinfection with other respiratory viruses. Jpn J. Infect. Dis., 2020, vol. 73, no. 5, pp. 377–380. doi: 10.7883/yoken.JJID.2020.181
  31. Khaitov M.R., Laza-Stanca V., Edwards M.R., Walton R.P., Rohde G., Contoli M., Papi A., Stanciu L.A., Kotenko S.V., Johnston S.L. Respiratory virus induction of alpha-, beta- and lambda-interferons in bronchial epithelial cells and peripheral blood mononuclear cells. Allergy, 2009, vol. 64, no. 3, pp. 375–386. doi: 10.1111/j.1398-9995.2008.01826.x
  32. Khodamoradi Z., Moghadami M., Lotfi M. Coinfection of coronavirus disease 2019 and influenza A: a report from Iran. Arch. Iran Med., 2020, vol. 23, no. 4, pp. 239–243. doi: 10.34172/aim.2020.04
  33. Kim D., Quinn J., Pinsky B., Shah N.H., Brown I. Rates of coinfection between SARS-CoV-2 and other respiratory pathogens. Jama, 2020, vol. 323, no. 20, pp. 2085–2086. doi: 10.1001/jama.2020.6266
  34. Kiseleva I. Will we ever be able to defeat human influenza? Open Microbiol. J., 2019, vol. 13, pp. 313–314. doi: 10.2174/1874285801913010313
  35. Kiseleva I., Grigorieva E., Larionova N., Al Farroukh M., Rudenko L. COVID-19 in light of seasonal respiratory infections. Biology (Basel), 2020, vol. 9, no. 9, p. 240. doi: 10.3390/biology9090240
  36. Klempa B. Reassortment events in the evolution of hantaviruses. Virus Genes, 2018, vol. 54, no. 5, pp. 638–646. doi: 10.1007/s11262-018-1590-z
  37. Konala V.M., Adap S., Gaya V., Naramal S., Daggubat S.R., Kammar C.B., Chenn A. Coinfection with influenza A and COVID-19. Eur. J. Case Rep. Intern. Med., 2020, vol. 7, no. 5: 001656. doi: 10.12890/2020_001656
  38. Lansbury L., Lim B., Baskaran V., Lim W.S. Co-infections in people with COVID-19: a systematic review and meta-analysis. J. Infect., 2020, vol. 81, no. 2, pp. 266–275. doi: 10.1016/j.jinf.2020.05.046
  39. Li Y., Wang J., Wang C., Yang Q., Xu Y., Xu J., Li Y., Yu X., Zhu H., Liu J. Characteristics of respiratory virus infection during the outbreak of 2019 novel coronavirus in Beijing. Int. J. Infect. Dis., 2020, vol. 96, pp. 266–269. doi: 10.1016/j.ijid.2020.05.008
  40. Li Z.T., Chen Z.M., Chen L.D., Zhan Y.Q., Li S.Q., Cheng J., Zhu A.R., Chen L.Y., Zhong N.S., Li S.Y., Lu W.J., Ye F. Coinfection with SARS-CoV-2 and other respiratory pathogens in COVID-19 patients in Guangzhou, China. J. Med. Virol., 2020, vol. 92, no. 11, pp. 2381–2383. doi: 10.1002/jmv.26073
  41. Linde A., Rotzén-Ostlund M., Zweygberg-Wirgart B., Rubinova S., Brytting M. Does viral interference affect spread of influenza? Euro Surveill., 2009, vol. 14, no. 40: 19354. doi: 10.2807/ese.14.40.19354-en
  42. Lloyd-Smith J.O. Vacated niches, competitive release and the community ecology of pathogen eradication. Philos Trans. R. Soc. Lond. B. Biol. Sci., 2013, vol. 368, no. 1623: 20120150. doi: 10.1098/rstb.2012.0150
  43. Lowen A.C., Mubareka S., Tumpey T.M., Garcia-Sastre A., Palese P. The guinea pig as a transmission model for human influenza viruses. Proc. Natl. Acad. Sci. USA, 2006, vol. 103, no. 26, pp. 9988–9992. doi: 10.1073/pnas.0604157103
  44. Mak G.C., Wong A.H., Ho W.Y., Lim W. The impact of pandemic influenza A (H1N1) 2009 on the circulation of respiratory viruses 2009–2011. Influenza Other Respir. Viruses, 2012, vol. 6, no. 3: e6–10. doi: 10.1111/j.1750-2659.2011.00323.x
  45. Matsuzaki Y., Sugawara K., Takashita E., Muraki Y., Hongo S., Katsushima N., Mizuta K., Nishimura H. Genetic diversity of influenza B virus: the frequent reassortment and cocirculation of the genetically distinct reassortant viruses in a community. J. Med. Virol., 2004, vol. 74, no. 1, pp. 132–140. doi: 10.1002/jmv.20156
  46. Maurice J.B., Patel A., Scott A.J., Patel K., Thursz M., Lemoine M. Prevalence and risk factors of nonalcoholic fatty liver disease in HIV-monoinfection. AIDS, 2017, vol. 31, no. 11, pp. 1621–1632. doi: 10.1097/QAD.0000000000001504
  47. Meningher T., Hindiyeh M., Regev L., Sherbany H., Mendelson E., Mandelboim M. Relationships between A(H1N1)pdm09 influenza infection and infections with other respiratory viruses. Influenza Other Respir. Viruses, 2014, vol. 8, no. 4, pp. 422–430. doi: 10.1111/irv.12249
  48. Moriyama M., Hugentobler W.J., Iwasaki A. Seasonality of respiratory viral infections. Annu. Rev. Virol., 2020, vol. 7, no. 1, pp. 83–101. doi: 10.1146/annurev-virology-012420-022445
  49. Navarro-Marí J.M., Pérez-Ruiz M., Galán Montemayor J.C., Marcos Maeso M., Reina J., de Oña Navarro M., Cilla Eguiluz C.G. Circulation of other respiratory viruses and viral coinfection during the 2009 pandemic influenza. Enferm. Infect. Microbiol. Clin., 2012, vol. 30, no. 4, pp. 25–31. doi: 10.1016/S0213-005X(12)70101-5
  50. Nickbakhsh S., Ho A., Marques D.F.P., McMenamin J., Gunson R.N., Murcia P.R. Epidemiology of seasonal coronaviruses: Establishing the context for COVID-19 emergence. J. Infect. Dis., 2020, vol. 222, no. 1, pp. 17–25. doi: 10.1093/infdis/jiaa185
  51. Nickbakhsh S., Mair C., Matthews L., Reeve R., Johnson P.C.D., Thorburn F., von Wissmann B., Reynolds A., McMenamin J., Gunson R.N., Murcia P.R. Virus–virus interactions impact the population dynamics of influenza and the common cold. Proc. Natl. Acad. Sci. USA, 2019, vol. 116, no. 52, pp. 27142–27150. doi: 10.1073/pnas.1911083116
  52. Nowak M.D., Sordillo E.M., Gitman M.R., Paniz Mondolfi A.E. Coinfection in SARS-CoV-2 infected patients: where are influenza virus and rhinovirus/enterovirus? J. Med. Virol., 2020, vol. 92, no. 10, pp. 1699–1700. doi: 10.1002/jmv.25953
  53. Osterhaus A.D.M.E. Influenza and RSV in a COVID-19 world. The first ESWI webinar 11 June 2020. URL: https://eswi.org/eswi-tv/influenza-and-rsv-in-a-covid-19-world-full-webinar
  54. Ou X., Zhou L., Huang H., Lin Y., Pan X., Chen D. A severe case with coinfection of SARS-CoV-2 and common respiratory pathogens. Trav. Med. Infect. Dis., 2020, vol. 36: 101672. doi: 10.1016/j.tmaid.2020.101672
  55. Ozaras R., Cirpin R., Duran A., Duman H., Arslan O., Bakcan Y., Kaya M., Mutlu H., Isayeva L., Kebanli F., Deger B.A., Bekeshev E., Kaya F., Bilir S. Influenza and COVID-19 coinfection: report of 6 cases and review of the literature. J. Med. Virol., 2020, vol. 92, no. 11, pp. 2657–2665. doi: 10.1002/jmv.26125
  56. Ozawa M., Kawaoka Y. Cross talk between animal and human influenza viruses. Annu. Rev. Anim. Biosci., 2013, vol. 1, pp. 21–42. doi: 10.1146/annurev-animal-031412-103733
  57. Palese P., Wang T.T. Why do influenza virus subtypes die out? A hypothesis. mBio, 2011, vol. 2, no. 5: e00150-11. doi: 10.1128/mBio.00150-11
  58. Pascalis H., Temmam S., Turpin M., Rollot O., Flahault A., Carrat F., de Lamballerie X., Gérardin P., Dellagi K. Intense co-circulation of non-influenza respiratory viruses during the first wave of pandemic influenza pH1N1/2009: a cohort study in Reunion Island. PLoS One, 2012, vol. 7, no. 9: e44755. doi: 10.1371/journal.pone.0044755
  59. Pennington H. The impact of infectious disease in war time: a look back at WW1. Fut. Micr., 2019, vol. 14, pp. 165–168. doi: 10.2217/fmb-2018-0323
  60. Petersen E., Koopmans M., Go U., Hamer D.H., Petrosillo N., Castelli F., Storgaard M., Al Khalili S., Simonsen L. Comparing SARS-CoV-2 with SARS-CoV and influenza pandemics. Lancet Infect. Dis., 2020, vol. 20, no. 9, pp. e238–e244. doi: 10.1016/ S1473-3099(20)30484-9
  61. Rawson T.M., Moore L.S.P., Zhu N., Ranganathan N., Skolimowska K., Gilchrist M., Satta G., Cooke G., Holmes A. Bacterial and fungal coinfection in individuals with coronavirus: a rapid review to support COVID-19 antimicrobial prescribing. Clin. Infect. Dis., 2020, vol. 71, no. 9, pp. 2459–2468. doi: 10.1093/cid/ciaa530
  62. Rodriguez J.A., Rubio-Gomez H., Roa A.A., Miller N., Eckardt P.A. Coinfection with SARS-CoV-2 and parainfluenza in a young adult patient with pneumonia: case report. IDCases, 2020, vol. 20: e00762. doi: 10.1016/j.idcr.2020.e00762
  63. Sánchez-Duque J.A., Orozco-Hernández J.P., Marín-Medina D.S., Cvetkovic-Vega A., Aveiro-Róbalo T.R., Mondragon-Cardona A., Failoc-Rojas V.E., Gutiérrez-Ocampo E., Villamizar-Peña R., Henao-Martínez J.F., Arteaga-Livias K., Rodríguez-Morales A.J. Are we now observing an increasing number of coinfections between SARS-CoV-2 and other respiratory pathogens? J. Med. Virol., 2020, vol. 92, no. 11, pp. 2398–2400. doi: 10.1002/jmv.26089
  64. Shrestha S., Foxman B., Weinberger D.M., Steiner C., Viboud C., Rohani P. Identifying the interaction between influenza and pneumococcal pneumonia using incidence data. Sci. Transl. Med., 2013, vol. 5, no. 191: 191ra184. doi: 10.1126/scitranslmed.3005982
  65. Steel J., Lowen A.C. Influenza A virus reassortment. Curr. Top. Microbiol. Immunol., 2014, vol. 385, pp. 377–401. doi: 10.1007/82_2014_395
  66. Touzard-Romo F., Tapé C., Lonks J.R. Co-infection with SARS-CoV-2 and human metapneumovirus. R. I. Med. J. (2013), 2020, vol. 103, no. 2, pp. 75–76.
  67. Viboud C., Simonsen L., Fuentes R., Flores J., Miller M.A., Chowell G. Global mortality impact of the 1957–1959 influenza pandemic. J. Infect. Dis., 2016, vol. 213, no. 5, pp. 738–745. doi: 10.1093/infdis/jiv534
  68. Wehl G., Laible M., Rauchenzauner M. Co-infection of SARS-CoV-2 and influenza A in a pediatric patient in Germany. Klin. Pediatr., 2020, vol. 232, no. 4, pp. 217–218. doi: 10.1055/a-1163-7385
  69. WHO. Coronavirus disease (COVID-19) dashboard. 2020. URL: https://covid19.who.int
  70. WHO. Coronavirus disease (COVID-19) pandemic. Press Conference of 15 June 2020. URL: https://www.who.int/emergencies/diseases/novel-coronavirus-2019
  71. WHO. Overview of influenza activity globally. Influenza Update No. 383 of 21 December 2020. URL: https://www.who.int/influenza/surveillance_monitoring/updates/latest_update_GIP_surveillance/en
  72. Wu D., Lu J., Ma X., Liu Q., Wang D., Gu Y., Li Y., He W. Coinfection of influenza virus and severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Pediatr. Infect. Dis. J., 2020, vol. 39, no. 6: e79. doi: 10.1097/INF.0000000000002688
  73. Wu Q., Xing Y., Shi L., Li W., Gao Y., Pan S., Wang Y., Wang W., Xing Q. Coinfection and other clinical characteristics of COVID-19 in children. Pediatrics, 2020, vol. 146, no. 1: e20200961. doi: 10.1542/peds.2020-0961
  74. Wu X., Cai Y., Huang X., Yu X., Zhao L., Wang F., Li Q., Gu S., Xu T., Li Y., Lu B., Zhan Q. Co-infection with SARS-CoV-2 and influenza A virus in patient with pneumonia, China. Emerg. Infect. Dis., 2020, vol. 26, no. 6, pp. 1324–1326. doi: 10.3201/eid2606.200299

Supplementary files

Supplementary Files
Action
1. JATS XML

Copyright (c) 2021 Kiseleva I.V., Larionova N.V., Grigorieva E.P., Ksenafontov A.D., Al Farroukh M., Rudenko L.G.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 64788 от 02.02.2016.


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies