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Volume 28, Number 2—February 2022
Perspective

Viral Interference between Respiratory Viruses

Jocelyne Piret and Guy BoivinComments to Author 
Author affiliation: Centre de Recherche du Centre Hospitalier Universitaire de Québec‒Université Laval, Quebec City, Quebec, Canada

Main Article

Table 2

Potential viral interferences between respiratory viruses*

Interfering virus Second virus Observed effect in patients, animal models, and ex vivo systems Results and statistical significance Reference
pH1N1 H3N2 Prevents A(H3N2) shedding in ferret model No H3N2 virus shedding (17)

IBV
Prevents or delays IBV shedding in ferret model
Peak delayed by 1.8 d (p = 0.014)
(17)
IAV RSV Reduced likelihood of co-detection in patients OR 0.11 (95% CI 0.00–0.92) (18)
Reduced likelihood of co-detection in patients OR 0.37 (95% CI 0.24–0.57) (19)


Prevents or delays RSV shedding in ferret model
Peak delayed by 2 d (p = 0.009)
(3)
RSV HMPV Reduced likelihood of co-detection in patients OR 0.27 (95% CI 0.09–0.80) (19)


Reduces HMPV replication in HAEC model
By 1 or 2 log after 5 d (p<0.05)
(20)
HRV IAV Reduced likelihood of co-detection in patients OR 0.06 (95% CI 0.01–0.24) (18)
Reduced likelihood of co-detection in patients OR 0.08 (95% CI 0.02–0.30) (21)
Reduced likelihood of co-detection in patients OR 0.15 (95% CI 0.04–0.53) (22)
Reduced likelihood of co-detection in patients OR 0.16 (95% CI 0.09–0.28) (23)


Reduces IAV replication in HAEC model
>15-fold after 24 h (p = 0.0002)
(23)
RSV HRV Reduced infection rate with HRV in patients 8% vs. 14% (p<0.049) (24)
Reduced likelihood of co-infection in patients OR 0.17 (95% CI 0.09–0.33) (18)
TCRI study OR 0.30 (95% CI 0.22‒0.40) (25)
INSPIRE study OR 0.18 (95% CI 0.11–0.28) (25)


MAKI trial
OR  0.34 (95% CI 0.16–0.72)
(25)
HRV SARS-CoV-2 Reduces SARS-CoV-2 replication in HAEC model By 3 log after 48 h (p = 0.006) (26)
By 3.5 log after 72 h (p<0.0001) (27)

*HAEC, human airway epithelial cells; HMPV, human metapneumovirus; HRV, human rhinovirus; IAV, influenza A virus; IBV, influenza B virus; INSPIRE, Infant Susceptibility to Pulmonary Infections and Asthma Following RSV Exposure (in a region of the southeastern United States); MAKI, trial on the effects of RSV prophylaxis with palivuzimab in healthy preterm infants in the Netherlands; OR, odds ratio; RSV, respiratory syncytial virus; SARS-CoV-2, severe acute respiratory syndrome coronavirus 2; TCRI, Tennessee Children’s Respiratory Initiative.

Main Article

References
  1. Zhang  AJ, Lee  AC, Chan  JF, Liu  F, Li  C, Chen  Y, et al. Coinfection by severe acute respiratory syndrome coronavirus 2 and influenza A(H1N1)pdm09 virus enhances the severity of pneumonia in golden Syrian hamsters. Clin Infect Dis. 2021;72:e97892. DOIPubMedGoogle Scholar
  2. Laurie  KL, Horman  W, Carolan  LA, Chan  KF, Layton  D, Bean  A, et al. Evidence for viral interference and cross-reactive protective immunity between influenza B virus lineages. J Infect Dis. 2018;217:54859. DOIPubMedGoogle Scholar
  3. Chan  KF, Carolan  LA, Korenkov  D, Druce  J, McCaw  J, Reading  PC, et al. Investigating viral interference between influenza A virus and human respiratory syncytial virus in a ferret model of infection. J Infect Dis. 2018;218:40617. DOIPubMedGoogle Scholar
  4. Schneider  WM, Chevillotte  MD, Rice  CM. Interferon-stimulated genes: a complex web of host defenses. Annu Rev Immunol. 2014;32:51345. DOIPubMedGoogle Scholar
  5. Kikkert  M. Innate immune evasion by human respiratory RNA viruses. J Innate Immun. 2020;12:420. DOIPubMedGoogle Scholar
  6. Soto  JA, Gálvez  NMS, Benavente  FM, Pizarro-Ortega  MS, Lay  MK, Riedel  C, et al. Human metapneumovirus: mechanisms and molecular targets used by the virus to avoid the immune system. Front Immunol. 2018;9:2466. DOIPubMedGoogle Scholar
  7. Li  C, Wang  T, Zhang  Y, Wei  F. Evasion mechanisms of the type I interferons responses by influenza A virus. Crit Rev Microbiol. 2020;46:42032. DOIPubMedGoogle Scholar
  8. Sa Ribero  M, Jouvenet  N, Dreux  M, Nisole  S. Interplay between SARS-CoV-2 and the type I interferon response. PLoS Pathog. 2020;16:e1008737. DOIPubMedGoogle Scholar
  9. Huang  IC, Li  W, Sui  J, Marasco  W, Choe  H, Farzan  M. Influenza A virus neuraminidase limits viral superinfection. J Virol. 2008;82:483443. DOIPubMedGoogle Scholar
  10. Shinjoh  M, Omoe  K, Saito  N, Matsuo  N, Nerome  K. In vitro growth profiles of respiratory syncytial virus in the presence of influenza virus. Acta Virol. 2000;44:917.PubMedGoogle Scholar
  11. Goto  H, Ihira  H, Morishita  K, Tsuchiya  M, Ohta  K, Yumine  N, et al. Enhanced growth of influenza A virus by coinfection with human parainfluenza virus type 2. Med Microbiol Immunol (Berl). 2016;205:20918. DOIPubMedGoogle Scholar
  12. Nickbakhsh  S, Mair  C, Matthews  L, Reeve  R, Johnson  PCD, Thorburn  F, et al. Virus-virus interactions impact the population dynamics of influenza and the common cold. Proc Natl Acad Sci U S A. 2019;116:2714250. DOIPubMedGoogle Scholar
  13. Voroshilova  MK. Potential use of nonpathogenic enteroviruses for control of human disease. In: Melnick JL, editor. Progress in medical virology. Basel: Karger; 1989. p. 191–202.
  14. Chumakov  MP, Voroshilova  MK, Antsupova  AS, Boĭko  VM, Blinova  MI, Priĭmiagi  LS, et al. [Live enteroviral vaccines for the emergency nonspecific prevention of mass respiratory diseases during fall-winter epidemics of influenza and acute respiratory diseases] [in Russian]. Zh Mikrobiol Epidemiol Immunobiol. 1992;11‒12:3740.PubMedGoogle Scholar
  15. Rijsbergen  LC, van Dijk  LLA, Engel  MFM, de Vries  RD, de Swart  RL. In vitro modelling of respiratory virus infections in human airway epithelial cells: a systematic review. Front Immunol. 2021;12:683002. DOIPubMedGoogle Scholar
  16. Shou  S, Liu  M, Yang  Y, Kang  N, Song  Y, Tan  D, et al. Animal models for COVID-19: hamsters, mouse, ferret, mink, tree shrew, and non-human primates. Front Microbiol. 2021;12:626553. DOIPubMedGoogle Scholar
  17. Laurie  KL, Guarnaccia  TA, Carolan  LA, Yan  AW, Aban  M, Petrie  S, et al. Interval between infections and viral hierarchy are determinants of viral interference following influenza virus infection in a ferret model. J Infect Dis. 2015;212:170110. DOIPubMedGoogle Scholar
  18. Greer  RM, McErlean  P, Arden  KE, Faux  CE, Nitsche  A, Lambert  SB, et al. Do rhinoviruses reduce the probability of viral co-detection during acute respiratory tract infections? J Clin Virol. 2009;45:105. DOIPubMedGoogle Scholar
  19. Price  OH, Sullivan  SG, Sutterby  C, Druce  J, Carville  KS. Using routine testing data to understand circulation patterns of influenza A, respiratory syncytial virus and other respiratory viruses in Victoria, Australia. Epidemiol Infect. 2019;147:e221. DOIPubMedGoogle Scholar
  20. Geiser  J, Boivin  G, Huang  S, Constant  S, Kaiser  L, Tapparel  C, et al. RSV and HMPV infections in 3D tissue cultures: mechanisms involved in virus-host and virus-virus interactions. Viruses. 2021;13:139. DOIPubMedGoogle Scholar
  21. Arden  KE, Greer  RM, Wang  CYT, Mackay  IM. Genotypic diversity, circulation patterns and co-detections among rhinoviruses in Queensland, 2001. Access Microbiol. 2019;2:acmi000075.PubMedGoogle Scholar
  22. Mackay  IM, Lambert  SB, Faux  CE, Arden  KE, Nissen  MD, Sloots  TP, et al. Community-wide, contemporaneous circulation of a broad spectrum of human rhinoviruses in healthy Australian preschool-aged children during a 12-month period. J Infect Dis. 2013;207:143341. DOIPubMedGoogle Scholar
  23. Wu  A, Mihaylova  VT, Landry  ML, Foxman  EF. Interference between rhinovirus and influenza A virus: a clinical data analysis and experimental infection study. Lancet Microbe. 2020;1:e25462. DOIPubMedGoogle Scholar
  24. Karppinen  S, Toivonen  L, Schuez-Havupalo  L, Waris  M, Peltola  V. Interference between respiratory syncytial virus and rhinovirus in respiratory tract infections in children. Clin Microbiol Infect. 2016;22:208.e16. DOIPubMedGoogle Scholar
  25. Achten  NB, Wu  P, Bont  L, Blanken  MO, Gebretsadik  T, Chappell  JD, et al. Interference between respiratory syncytial virus and human rhinovirus infection in infancy. J Infect Dis. 2017;215:11026. DOIPubMedGoogle Scholar
  26. Dee  K, Goldfarb  DM, Haney  J, Amat  JA, Herder  V, Stewart  M, et al. Human rhinovirus infection blocks SARS-CoV-2 replication within the respiratory epithelium: implications for COVID-19 epidemiology. J Infect Dis. 2021;224:318. DOIPubMedGoogle Scholar
  27. Cheemarla  NR, Watkins  TA, Mihaylova  VT, Wang  B, Zhao  D, Wang  G, et al. Dynamic innate immune response determines susceptibility to SARS-CoV-2 infection and early replication kinetics. J Exp Med. 2021;218:e20210583. DOIPubMedGoogle Scholar
  28. Sonoguchi  T, Naito  H, Hara  M, Takeuchi  Y, Fukumi  H. Cross-subtype protection in humans during sequential, overlapping, and/or concurrent epidemics caused by H3N2 and H1N1 influenza viruses. J Infect Dis. 1985;151:818. DOIPubMedGoogle Scholar
  29. Van Kerkhove  MD, Mounts  AW. 2009 versus 2010 comparison of influenza activity in southern hemisphere temperate countries. Influenza Other Respir Viruses. 2011;5:3759. DOIPubMedGoogle Scholar
  30. Yang  Y, Wang  Z, Ren  L, Wang  W, Vernet  G, Paranhos-Baccalà  G, et al. Influenza A/H1N1 2009 pandemic and respiratory virus infections, Beijing, 2009-2010. PLoS One. 2012;7:e45807. DOIPubMedGoogle Scholar
  31. Anestad  G, Vainio  K, Hungnes  O. Interference between outbreaks of epidemic viruses. Scand J Infect Dis. 2007;39:6534. DOIPubMedGoogle Scholar
  32. Nishimura  N, Nishio  H, Lee  MJ, Uemura  K. The clinical features of respiratory syncytial virus: lower respiratory tract infection after upper respiratory tract infection due to influenza virus. Pediatr Int. 2005;47:4126. DOIPubMedGoogle Scholar
  33. van Asten  L, Bijkerk  P, Fanoy  E, van Ginkel  A, Suijkerbuijk  A, van der Hoek  W, et al. Early occurrence of influenza A epidemics coincided with changes in occurrence of other respiratory virus infections. Influenza Other Respir Viruses. 2016;10:1426. DOIPubMedGoogle Scholar
  34. Gröndahl  B, Ankermann  T, von Bismarck  P, Rockahr  S, Kowalzik  F, Gehring  S, et al. The 2009 pandemic influenza A(H1N1) coincides with changes in the epidemiology of other viral pathogens causing acute respiratory tract infections in children. Infection. 2014;42:3038. DOIPubMedGoogle Scholar
  35. Mak  GC, Wong  AH, Ho  WY, Lim  W. The impact of pandemic influenza A (H1N1) 2009 on the circulation of respiratory viruses 2009-2011. Influenza Other Respir Viruses. 2012;6:e610. DOIPubMedGoogle Scholar
  36. Green  HK, Ellis  J, Galiano  M, Watson  JM, Pebody  RG. Critical care surveillance: insights into the impact of the 2010/11 influenza season relative to the 2009/10 pandemic season in England. Euro Surveill. 2013;18:20499. DOIPubMedGoogle Scholar
  37. Casalegno  JS, Ottmann  M, Bouscambert-Duchamp  M, Valette  M, Morfin  F, Lina  B. Impact of the 2009 influenza A(H1N1) pandemic wave on the pattern of hibernal respiratory virus epidemics, France, 2009. Euro Surveill. 2010;15:19485. DOIPubMedGoogle Scholar
  38. 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;8:42230. DOIPubMedGoogle Scholar
  39. Ånestad  G, Nordbø  SA. Virus interference. Did rhinoviruses activity hamper the progress of the 2009 influenza A (H1N1) pandemic in Norway? Med Hypotheses. 2011;77:11324. DOIPubMedGoogle Scholar
  40. Linde  A, Rotzén-Ostlund  M, Zweygberg-Wirgart  B, Rubinova  S, Brytting  M. Does viral interference affect spread of influenza? Euro Surveill. 2009;14:19354. DOIPubMedGoogle Scholar
  41. Casalegno  JS, Ottmann  M, Duchamp  MB, Escuret  V, Billaud  G, Frobert  E, et al. Rhinoviruses delayed the circulation of the pandemic influenza A (H1N1) 2009 virus in France. Clin Microbiol Infect. 2010;16:3269. DOIPubMedGoogle Scholar
  42. Zheng  X, Song  Z, Li  Y, Zhang  J, Wang  XL. Possible interference between seasonal epidemics of influenza and other respiratory viruses in Hong Kong, 2014-2017. BMC Infect Dis. 2017;17:772. DOIPubMedGoogle Scholar
  43. Gonzalez  AJ, Ijezie  EC, Balemba  OB, Miura  TA. Attenuation of influenza A virus disease severity by viral coinfection in a mouse model. J Virol. 2018;92:e0088118. DOIPubMedGoogle Scholar
  44. Park  S, Michelow  IC, Choe  YJ. Shifting patterns of respiratory virus activity following social distancing measures for COVID-19 in South Korea. J Infect Dis. 2021;jiab231.
  45. Leung  NHL, Chu  DKW, Shiu  EYC, Chan  KH, McDevitt  JJ, Hau  BJP, et al. Respiratory virus shedding in exhaled breath and efficacy of face masks. Nat Med. 2020;26:67680. DOIPubMedGoogle Scholar
  46. Alfi  O, Yakirevitch  A, Wald  O, Wandel  O, Izhar  U, Oiknine-Djian  E, et al. Human nasal and lung tissues infected ex vivo with SARS-CoV-2 provide insights into differential tissue-specific and virus-specific innate immune responses in the upper and lower respiratory tract. J Virol. 2021;95:e0013021. DOIPubMedGoogle Scholar
  47. Vignuzzi  M, López  CB. Defective viral genomes are key drivers of the virus-host interaction. Nat Microbiol. 2019;4:107587. DOIPubMedGoogle Scholar
  48. Scott  PD, Meng  B, Marriott  AC, Easton  AJ, Dimmock  NJ. Defective interfering influenza A virus protects in vivo against disease caused by a heterologous influenza B virus. J Gen Virol. 2011;92:212232. DOIPubMedGoogle Scholar
  49. Easton  AJ, Scott  PD, Edworthy  NL, Meng  B, Marriott  AC, Dimmock  NJ. A novel broad-spectrum treatment for respiratory virus infections: influenza-based defective interfering virus provides protection against pneumovirus infection in vivo. Vaccine. 2011;29:277784. DOIPubMedGoogle Scholar
  50. Musuuza  JS, Watson  L, Parmasad  V, Putman-Buehler  N, Christensen  L, Safdar  N. Prevalence and outcomes of co-infection and superinfection with SARS-CoV-2 and other pathogens: A systematic review and meta-analysis. PLoS One. 2021;16:e0251170. DOIPubMedGoogle Scholar

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