1932

Abstract

The seasonal cycle of respiratory viral diseases has been widely recognized for thousands of years, as annual epidemics of the common cold and influenza disease hit the human population like clockwork in the winter season in temperate regions. Moreover, epidemics caused by viruses such as severe acute respiratory syndrome coronavirus (SARS-CoV) and the newly emerging SARS-CoV-2 occur during the winter months. The mechanisms underlying the seasonal nature of respiratory viral infections have been examined and debated for many years. The two major contributing factors are the changes in environmental parameters and human behavior. Studies have revealed the effect of temperature and humidity on respiratory virus stability and transmission rates. More recent research highlights the importance of the environmental factors, especially temperature and humidity, in modulating host intrinsic, innate, and adaptive immune responses to viral infections in the respiratory tract. Here we review evidence of how outdoor and indoor climates are linked to the seasonality of viral respiratory infections. We further discuss determinants of host response in the seasonality of respiratory viruses by highlighting recent studies in the field.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-virology-012420-022445
2020-09-29
2024-04-13
Loading full text...

Full text loading...

/deliver/fulltext/virology/7/1/annurev-virology-012420-022445.html?itemId=/content/journals/10.1146/annurev-virology-012420-022445&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Pappas G, Kiriaze IJ, Falagas ME 2008. Insights into infectious disease in the era of Hippocrates. Int. J. Infect. Dis. 12:347–50
    [Google Scholar]
  2. 2. 
    Fendrick AM, Monto AS, Nightengale B, Sarnes M 2003. The economic burden of non-influenza-related viral respiratory tract infection in the United States. Arch. Intern. Med. 163:487–94
    [Google Scholar]
  3. 3. 
    Molinari NA, Ortega-Sanchez IR, Messonnier ML, Thompson WW, Wortley PM et al. 2007. The annual impact of seasonal influenza in the US: measuring disease burden and costs. Vaccine 25:5086–96
    [Google Scholar]
  4. 4. 
    Li Q, Guan X, Wu P, Wang X, Zhou L et al. 2020. Early transmission dynamics in Wuhan, China, of novel coronavirus-infected pneumonia. N. Engl. J. Med 382:1199207
    [Google Scholar]
  5. 5. 
    Paules CI, Marston HD, Fauci AS 2020. Coronavirus infections—more than just the common cold. JAMA 323:7078
    [Google Scholar]
  6. 6. 
    Kuiken T, Fouchier RA, Schutten M, Rimmelzwaan GF, van Amerongen G et al. 2003. Newly discovered coronavirus as the primary cause of severe acute respiratory syndrome. Lancet 362:263–70
    [Google Scholar]
  7. 7. 
    Peiris JS, Lai ST, Poon LL, Guan Y, Yam LY et al. 2003. Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet 361:1319–25
    [Google Scholar]
  8. 8. 
    Fisman D. 2012. Seasonality of viral infections: mechanisms and unknowns. Clin. Microbiol. Infect. 18:946–54
    [Google Scholar]
  9. 9. 
    Dowell SF. 2001. Seasonal variation in host susceptibility and cycles of certain infectious diseases. Emerg. Infect. Dis. 7:369–74
    [Google Scholar]
  10. 10. 
    Cannell JJ, Vieth R, Umhau JC, Holick MF, Grant WB et al. 2006. Epidemic influenza and vitamin D. Epidemiol. Infect. 134:1129–40
    [Google Scholar]
  11. 11. 
    Sloan C, Moore ML, Hartert T 2011. Impact of pollution, climate, and sociodemographic factors on spatiotemporal dynamics of seasonal respiratory viruses. Clin. Transl. Sci. 4:48–54
    [Google Scholar]
  12. 12. 
    Shaman J, Kohn M. 2009. Absolute humidity modulates influenza survival, transmission, and seasonality. PNAS 106:3243–48
    [Google Scholar]
  13. 13. 
    Azziz Baumgartner E, Dao CN, Nasreen S, Bhuiyan MU, Mah EMS et al. 2012. Seasonality, timing, and climate drivers of influenza activity worldwide. J. Infect. Dis. 206:838–46
    [Google Scholar]
  14. 14. 
    Tamerius J, Nelson MI, Zhou SZ, Viboud C, Miller MA, Alonso WJ 2011. Global influenza seasonality: reconciling patterns across temperate and tropical regions. Environ. Health Perspect. 119:439–45
    [Google Scholar]
  15. 15. 
    Shoji M, Katayama K, Sano K 2011. Absolute humidity as a deterministic factor affecting seasonal influenza epidemics in Japan. Tohoku J. Exp. Med. 224:251–56
    [Google Scholar]
  16. 16. 
    Peci A, Winter AL, Li Y, Gnaneshan S, Liu J et al. 2019. Effects of absolute humidity, relative humidity, temperature, and wind speed on influenza activity in Toronto, Ontario, Canada. Appl. Environ. Microbiol. 85:e02426-18
    [Google Scholar]
  17. 17. 
    Mourtzoukou EG, Falagas ME. 2007. Exposure to cold and respiratory tract infections. Int. J. Tuberc. Lung Dis. 11:938–43
    [Google Scholar]
  18. 18. 
    Shaman J, Pitzer VE, Viboud C, Grenfell BT, Lipsitch M 2010. Absolute humidity and the seasonal onset of influenza in the continental United States. PLOS Biol 8:e1000316
    [Google Scholar]
  19. 19. 
    Quinn A, Shaman J. 2017. Health symptoms in relation to temperature, humidity, and self-reported perceptions of climate in New York City residential environments. Int. J. Biometeorol. 61:1209–20
    [Google Scholar]
  20. 20. 
    Reynolds SJ, Black DW, Borin SS, Breuer G, Burmeister LF et al. 2001. Indoor environmental quality in six commercial office buildings in the midwest United States. Appl. Occup. Environ. Hyg. 16:1065–77
    [Google Scholar]
  21. 21. 
    Willem L, Van Kerckhove K, Chao DL, Hens N, Beutels P 2012. A nice day for an infection? Weather conditions and social contact patterns relevant to influenza transmission. PLOS ONE 7:e48695
    [Google Scholar]
  22. 22. 
    Schweizer C, Edwards RD, Bayer-Oglesby L, Gauderman WJ, Ilacqua V et al. 2007. Indoor time–microenvironment–activity patterns in seven regions of Europe. J. Expo. Sci. Environ. Epidemiol. 17:170–81
    [Google Scholar]
  23. 23. 
    Klepeis NE, Nelson WC, Ott WR, Robinson JP, Tsang AM et al. 2001. The National Human Activity Pattern Survey (NHAPS): a resource for assessing exposure to environmental pollutants. J. Expo. Anal. Environ. Epidemiol. 11:231–52
    [Google Scholar]
  24. 24. 
    Foxman EF, Iwasaki A. 2011. Genome-virome interactions: examining the role of common viral infections in complex disease. Nat. Rev. Microbiol. 9:254–64
    [Google Scholar]
  25. 25. 
    Nichols WG, Peck Campbell AJ, Boeckh M 2008. Respiratory viruses other than influenza virus: impact and therapeutic advances. Clin. Microbiol. Rev. 21:274–90
    [Google Scholar]
  26. 26. 
    Pavia AT. 2011. Viral infections of the lower respiratory tract: old viruses, new viruses, and the role of diagnosis. Clin. Infect. Dis. 52:Suppl. 4S284–284
    [Google Scholar]
  27. 27. 
    Midgley CM, Haynes AK, Baumgardner JL, Chommanard C, Demas SW et al. 2017. Determining the seasonality of respiratory syncytial virus in the United States: the impact of increased molecular testing. J. Infect. Dis. 216:345–55
    [Google Scholar]
  28. 28. 
    Killerby ME, Biggs HM, Haynes A, Dahl RM, Mustaquim D et al. 2018. Human coronavirus circulation in the United States 2014–2017. J. Clin. Virol. 101:52–56
    [Google Scholar]
  29. 29. 
    Monto AS. 2002. Epidemiology of viral respiratory infections. Am. J. Med. 112:Suppl. 6A4S–12S
    [Google Scholar]
  30. 30. 
    Landes MB, Neil RB, McCool SS, Mason BP, Woron AM et al. 2013. The frequency and seasonality of influenza and other respiratory viruses in Tennessee: two influenza seasons of surveillance data, 2010–2012. Influenza Other Respir. Viruses 7:1122–27
    [Google Scholar]
  31. 31. 
    Morikawa S, Kohdera U, Hosaka T, Ishii K, Akagawa S et al. 2015. Seasonal variations of respiratory viruses and etiology of human rhinovirus infection in children. J. Clin. Virol. 73:14–19
    [Google Scholar]
  32. 32. 
    Bastien N, Brandt K, Dust K, Ward D, Li Y 2006. Human Bocavirus infection, Canada. Emerg. Infect. Dis. 12:848–50
    [Google Scholar]
  33. 33. 
    Haynes AK, Fowlkes AL, Schneider E, Mutuc JD, Armstrong GL, Gerber SI 2016. Human metapneumovirus circulation in the United States, 2008 to 2014. Pediatrics 137:e20152927
    [Google Scholar]
  34. 34. 
    Abedi GR, Watson JT, Nix WA, Oberste MS, Gerber SI 2018. Enterovirus and parechovirus surveillance—United States, 2014–2016. MMWR Morb. Mortal. Wkly. Rep. 67:515–18
    [Google Scholar]
  35. 35. 
    Lee WM, Lemanske RF Jr, Evans MD, Vang F, Pappas T et al. 2012. Human rhinovirus species and season of infection determine illness severity. Am. J. Respir. Crit. Care Med. 186:886–91
    [Google Scholar]
  36. 36. 
    Monto AS. 2002. The seasonality of rhinovirus infections and its implications for clinical recognition. Clin. Ther. 24:1987–97
    [Google Scholar]
  37. 37. 
    Abedi GR, Prill MM, Langley GE, Wikswo ME, Weinberg GA et al. 2016. Estimates of parainfluenza virus-associated hospitalizations and cost among children aged less than 5 years in the United States, 1998–2010. J. Pediatr. Infect. Dis. Soc. 5:7–13
    [Google Scholar]
  38. 38. 
    Anestad G. 1982. Interference between outbreaks of respiratory syncytial virus and influenza virus infection. Lancet 1:502
    [Google Scholar]
  39. 39. 
    Linde A, Rotzen-Ostlund M, Zweygberg-Wirgart B, Rubinova S, Brytting M 2009. Does viral interference affect spread of influenza. ? Euro Surveill. 14:19354
    [Google Scholar]
  40. 40. 
    Casalegno JS, Ottmann M, Duchamp MB, Escuret V, Billaud G et al. 2010. Rhinoviruses delayed the circulation of the pandemic influenza A (H1N1) 2009 virus in France. Clin. Microbiol. Infect. 16:326–29
    [Google Scholar]
  41. 41. 
    Nickbakhsh S, Mair C, Matthews L, Reeve R, Johnson PCD et al. 2019. Virus–virus interactions impact the population dynamics of influenza and the common cold. PNAS 116:5227142–50
    [Google Scholar]
  42. 42. 
    Gonzalez AJ, Ijezie EC, Balemba OB, Miura TA 2018. Attenuation of influenza A virus disease severity by viral coinfection in a mouse model. J. Virol. 92:e00881-18
    [Google Scholar]
  43. 43. 
    Chan KF, Carolan LA, Korenkov D, Druce J, McCaw J et al. 2018. Investigating viral interference between influenza A virus and human respiratory syncytial virus in a ferret model of infection. J. Infect. Dis. 218:406–17
    [Google Scholar]
  44. 44. 
    Bhattacharyya S, Gesteland PH, Korgenski K, Bjornstad ON, Adler FR 2015. Cross-immunity between strains explains the dynamical pattern of paramyxoviruses. PNAS 112:13396–400
    [Google Scholar]
  45. 45. 
    Brankston G, Gitterman L, Hirji Z, Lemieux C, Gardam M 2007. Transmission of influenza A in human beings. Lancet Infect. Dis. 7:257–65
    [Google Scholar]
  46. 46. 
    Weber TP, Stilianakis NI. 2008. Inactivation of influenza A viruses in the environment and modes of transmission: a critical review. J. Infect. 57:361–73
    [Google Scholar]
  47. 47. 
    Lowen A, Palese P. 2009. Transmission of influenza virus in temperate zones is predominantly by aerosol, in the tropics by contact: a hypothesis. PLOS Curr 1:RRN1002
    [Google Scholar]
  48. 48. 
    Yang W, Marr LC. 2011. Dynamics of airborne influenza A viruses indoors and dependence on humidity. PLOS ONE 6:e21481
    [Google Scholar]
  49. 49. 
    Yang W, Elankumaran S, Marr LC 2012. Relationship between humidity and influenza A viability in droplets and implications for influenza's seasonality. PLOS ONE 7:e46789
    [Google Scholar]
  50. 50. 
    Yang W, Marr LC. 2012. Mechanisms by which ambient humidity may affect viruses in aerosols. Appl. Environ. Microbiol. 78:6781–88
    [Google Scholar]
  51. 51. 
    Irwin CK, Yoon KJ, Wang C, Hoff SJ, Zimmerman JJ et al. 2011. Using the systematic review methodology to evaluate factors that influence the persistence of influenza virus in environmental matrices. Appl. Environ. Microbiol. 77:1049–60
    [Google Scholar]
  52. 52. 
    Lowen AC, Mubareka S, Steel J, Palese P 2007. Influenza virus transmission is dependent on relative humidity and temperature. PLOS Pathog 3:1470–76
    [Google Scholar]
  53. 53. 
    Lowen AC, Steel J, Mubareka S, Palese P 2008. High temperature (30 degrees C) blocks aerosol but not contact transmission of influenza virus. J. Virol. 82:5650–52
    [Google Scholar]
  54. 54. 
    Gustin KM, Belser JA, Veguilla V, Zeng H, Katz JM et al. 2015. Environmental conditions affect exhalation of H3N2 seasonal and variant influenza viruses and respiratory droplet transmission in ferrets. PLOS ONE 10:e0125874
    [Google Scholar]
  55. 55. 
    Marr LC, Tang JW, Van Mullekom J, Lakdawala SS 2019. Mechanistic insights into the effect of humidity on airborne influenza virus survival, transmission and incidence. J. R. Soc. Interface 16:20180298
    [Google Scholar]
  56. 56. 
    Noti JD, Blachere FM, McMillen CM, Lindsley WG, Kashon ML et al. 2013. High humidity leads to loss of infectious influenza virus from simulated coughs. PLOS ONE 8:e57485
    [Google Scholar]
  57. 57. 
    Harper GJ. 1961. Airborne micro-organisms: survival tests with four viruses. Epidemiol. Infect. 59:479–86
    [Google Scholar]
  58. 58. 
    Miller WS, Artenstein MS. 1967. Aerosol stability of three acute respiratory disease viruses. Proc. Soc. Exp. Biol. Med. 125:222–27
    [Google Scholar]
  59. 59. 
    Ijaz MK, Brunner AH, Sattar SA, Nair RC, Johnson-Lussenburg CM 1985. Survival characteristics of airborne human coronavirus 229E. J. Gen. Virol. 66:122743–48
    [Google Scholar]
  60. 60. 
    Rechsteiner J. 1969. Inactivation of respiratory syncytial virus in air. Antonie Van Leeuwenhoek 35:238
    [Google Scholar]
  61. 61. 
    Karim YG, Ijaz MK, Sattar SA, Johnson-Lussenburg CM 1985. Effect of relative humidity on the airborne survival of rhinovirus-14. Can. J. Microbiol. 31:1058–61
    [Google Scholar]
  62. 62. 
    Hemmes JH, Winkler KC, Kool SM 1960. Virus survival as a seasonal factor in influenza and polimyelitis. Nature 188:430–31
    [Google Scholar]
  63. 63. 
    Polozov IV, Bezrukov L, Gawrisch K, Zimmerberg J 2008. Progressive ordering with decreasing temperature of the phospholipids of influenza virus. Nat. Chem. Biol. 4:248–55
    [Google Scholar]
  64. 64. 
    Schulman JL, Kilbourne ED. 1963. Experimental transmission of influenza virus infection in mice. I. The period of transmissibility. J. Exp. Med. 118:257–66
    [Google Scholar]
  65. 65. 
    Schulman JL, Kilbourne ED. 1963. Experimental transmission of influenza virus infection in mice. II. Some factors affecting the incidence of transmitted infection. J. Exp. Med. 118:267–75
    [Google Scholar]
  66. 66. 
    Herlocher ML, Elias S, Truscon R, Harrison S, Mindell D et al. 2001. Ferrets as a transmission model for influenza: sequence changes in HA1 of type A (H3N2) virus. J. Infect. Dis. 184:542–46
    [Google Scholar]
  67. 67. 
    Lowen AC, Mubareka S, Tumpey TM, Garcia-Sastre A, Palese P 2006. The guinea pig as a transmission model for human influenza viruses. PNAS 103:9988–92
    [Google Scholar]
  68. 68. 
    Belser JA, Katz JM, Tumpey TM 2011. The ferret as a model organism to study influenza A virus infection. Dis. Model. Mech. 4:575–79
    [Google Scholar]
  69. 69. 
    Schulman JL, Kilbourne ED. 1962. Airborne transmission of influenza virus infection in mice. Nature 195:1129–30
    [Google Scholar]
  70. 70. 
    Lester W Jr 1948. The influence of relative humidity on the infectivity of air-borne influenza A virus, PR8 strain. J. Exp. Med. 88:361–68
    [Google Scholar]
  71. 71. 
    Van Hoeven N, Belser JA, Szretter KJ, Zeng H, Staeheli P et al. 2009. Pathogenesis of 1918 pandemic and H5N1 influenza virus infections in a guinea pig model: antiviral potential of exogenous alpha interferon to reduce virus shedding. J. Virol. 83:2851–61
    [Google Scholar]
  72. 72. 
    Steel J, Palese P, Lowen AC 2011. Transmission of a 2009 pandemic influenza virus shows a sensitivity to temperature and humidity similar to that of an H3N2 seasonal strain. J. Virol. 85:1400–2
    [Google Scholar]
  73. 73. 
    Iwasaki A, Foxman EF, Molony RD 2017. Early local immune defences in the respiratory tract. Nat. Rev. Immunol. 17:7–20
    [Google Scholar]
  74. 74. 
    Fokkens WJ, Scheeren RA. 2000. Upper airway defence mechanisms. Paediatr. Respir. Rev. 1:336–41
    [Google Scholar]
  75. 75. 
    Bustamante-Marin XM, Ostrowski LE. 2017. Cilia and mucociliary clearance. Cold Spring Harb. Perspect. Biol. 9:a028241
    [Google Scholar]
  76. 76. 
    Hamed R, Fiegel J. 2014. Synthetic tracheal mucus with native rheological and surface tension properties. J. Biomed. Mater. Res. A 102:1788–98
    [Google Scholar]
  77. 77. 
    Thornton DJ, Gray T, Nettesheim P, Howard M, Koo JS, Sheehan JK 2000. Characterization of mucins from cultured normal human tracheobronchial epithelial cells. Am. J. Physiol. Lung Cell Mol. Physiol. 278:L1118–1118
    [Google Scholar]
  78. 78. 
    Tian PW, Wen FQ. 2015. Clinical significance of airway mucus hypersecretion in chronic obstructive pulmonary disease. J. Transl. Int. Med. 3:89–92
    [Google Scholar]
  79. 79. 
    Donaldson GC, Seemungal T, Jeffries DJ, Wedzicha JA 1999. Effect of temperature on lung function and symptoms in chronic obstructive pulmonary disease. Eur. Respir. J. 13:844–49
    [Google Scholar]
  80. 80. 
    McKemy DD, Neuhausser WM, Julius D 2002. Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416:52–58
    [Google Scholar]
  81. 81. 
    Peier AM, Moqrich A, Hergarden AC, Reeve AJ, Andersson DA et al. 2002. A TRP channel that senses cold stimuli and menthol. Cell 108:705–15
    [Google Scholar]
  82. 82. 
    Li M, Li Q, Yang G, Kolosov VP, Perelman JM, Zhou XD 2011. Cold temperature induces mucin hypersecretion from normal human bronchial epithelial cells in vitro through a transient receptor potential melastatin 8 (TRPM8)-mediated mechanism. J. Allergy Clin. Immunol. 128:626–34
    [Google Scholar]
  83. 83. 
    Baetjer AM. 1967. Effect of ambient temperature and vapor pressure on cilia-mucus clearance rate. J. Appl. Physiol. 23:498–504
    [Google Scholar]
  84. 84. 
    Even-Tzur N, Zaretsky U, Grinberg O, Davidovich T, Kloog Y et al. 2010. Climate chamber for environmentally controlled laboratory airflow experiments. Technol. Health Care 18:157–63
    [Google Scholar]
  85. 85. 
    Iwasaki A. 2007. Mucosal dendritic cells. Annu. Rev. Immunol. 25:381–418
    [Google Scholar]
  86. 86. 
    Erjefalt JS, Erjefalt I, Sundler F, Persson CG 1995. In vivo restitution of airway epithelium. Cell Tissue Res 281:305–16
    [Google Scholar]
  87. 87. 
    Barbet JP, Chauveau M, Labbe S, Lockhart A 1988. Breathing dry air causes acute epithelial damage and inflammation of the guinea pig trachea. J. Appl. Physiol. 64:1851–57
    [Google Scholar]
  88. 88. 
    Kudo E, Song E, Yockey LJ, Rakib T, Wong PW et al. 2019. Low ambient humidity impairs barrier function and innate resistance against influenza infection. PNAS 116:10905–10
    [Google Scholar]
  89. 89. 
    Clary-Meinesz CF, Cosson J, Huitorel P, Blaive B 1992. Temperature effect on the ciliary beat frequency of human nasal and tracheal ciliated cells. Biol. Cell 76:335–38
    [Google Scholar]
  90. 90. 
    Williams R, Rankin N, Smith T, Galler D, Seakins P 1996. Relationship between the humidity and temperature of inspired gas and the function of the airway mucosa. Crit. Care Med. 24:1920–29
    [Google Scholar]
  91. 91. 
    Rogers TD, Ostrowski LE, Livraghi-Butrico A, Button B, Grubb BR 2018. Mucociliary clearance in mice measured by tracking trans-tracheal fluorescence of nasally aerosolized beads. Sci. Rep. 8:14744
    [Google Scholar]
  92. 92. 
    Andersen I, Lundqvist GR, Jensen PL, Proctor DF 1974. Human response to 78-hour exposure to dry air. Arch. Environ. Health 29:319–24
    [Google Scholar]
  93. 93. 
    Ewert G. 1965. On the mucus flow rate in the human nose. Acta Otolaryngol. Suppl. 200:SUPPL-200
    [Google Scholar]
  94. 94. 
    Soane RJ, Carney AS, Jones NS, Frier M, Perkins AC et al. 2001. The effect of the nasal cycle on mucociliary clearance. Clin. Otolaryngol. Allied Sci. 26:9–15
    [Google Scholar]
  95. 95. 
    Seo H, Kim SH, Choi JH, Hong JY, Hwang JH 2014. Effect of heated humidified ventilation on bronchial mucus transport velocity in general anaesthesia: a randomized trial. J. Int. Med. Res. 42:1222–31
    [Google Scholar]
  96. 96. 
    Chalon J, Loew DA, Malebranche J 1972. Effects of dry anesthetic gases on tracheobronchial ciliated epithelium. Anesthesiology 37:338–43
    [Google Scholar]
  97. 97. 
    Iwasaki A, Medzhitov R. 2010. Regulation of adaptive immunity by the innate immune system. Science 327:291–95
    [Google Scholar]
  98. 98. 
    Ivashkiv LB, Donlin LT. 2014. Regulation of type I interferon responses. Nat. Rev. Immunol. 14:36–49
    [Google Scholar]
  99. 99. 
    Foxman EF, Storer JA, Fitzgerald ME, Wasik BR, Hou L et al. 2015. Temperature-dependent innate defense against the common cold virus limits viral replication at warm temperature in mouse airway cells. PNAS 112:827–32
    [Google Scholar]
  100. 100. 
    Foxman EF, Storer JA, Vanaja K, Levchenko A, Iwasaki A 2016. Two interferon-independent double-stranded RNA-induced host defense strategies suppress the common cold virus at warm temperature. PNAS 113:8496–501
    [Google Scholar]
  101. 101. 
    Moriyama M, Ichinohe T. 2019. High ambient temperature dampens adaptive immune responses to influenza A virus infection. PNAS 116:3118–25
    [Google Scholar]
  102. 102. 
    Pillai PS, Molony RD, Martinod K, Dong H, Pang IK et al. 2016. Mx1 reveals innate pathways to antiviral resistance and lethal influenza disease. Science 352:463–66
    [Google Scholar]
  103. 103. 
    Yellon SM, Fagoaga OR, Nehlsen-Cannarella SL 1999. Influence of photoperiod on immune cell functions in the male Siberian hamster. Am. J. Physiol. 276:R97–97
    [Google Scholar]
  104. 104. 
    Abu-Amer Y, Bar-Shavit Z. 1993. Impaired bone marrow-derived macrophage differentiation in vitamin D deficiency. Cell Immunol 151:356–68
    [Google Scholar]
  105. 105. 
    Braciale TJ, Sun J, Kim TS 2012. Regulating the adaptive immune response to respiratory virus infection. Nat. Rev. Immunol. 12:295–305
    [Google Scholar]
  106. 106. 
    Vinuesa CG, Linterman MA, Yu D, MacLennan IC 2016. Follicular helper T cells. Annu. Rev. Immunol. 34:335–68
    [Google Scholar]
  107. 107. 
    Kokolus KM, Capitano ML, Lee CT, Eng JW, Waight JD et al. 2013. Baseline tumor growth and immune control in laboratory mice are significantly influenced by subthermoneutral housing temperature. PNAS 110:20176–81
    [Google Scholar]
  108. 108. 
    Eng JW, Reed CB, Kokolus KM, Pitoniak R, Utley A et al. 2015. Housing temperature-induced stress drives therapeutic resistance in murine tumour models through β2-adrenergic receptor activation. Nat. Commun. 6:6426
    [Google Scholar]
  109. 109. 
    Leigh ND, Kokolus KM, O'Neill RE, Du W, Eng JW et al. 2015. Housing temperature-induced stress is suppressing murine graft-versus-host disease through β2-adrenergic receptor signaling. J. Immunol. 195:5045–54
    [Google Scholar]
  110. 110. 
    Fox SJ, Miller JC, Meyers LA 2017. Seasonality in risk of pandemic influenza emergence. PLOS Comput. Biol. 13:e1005749
    [Google Scholar]
  111. 111. 
    Medzhitov R, Schneider DS, Soares MP 2012. Disease tolerance as a defense strategy. Science 335:936–41
    [Google Scholar]
  112. 112. 
    Molony RD, Nguyen JT, Kong Y, Montgomery RR, Shaw AC, Iwasaki A 2017. Aging impairs both primary and secondary RIG-I signaling for interferon induction in human monocytes. Sci. Signal. 10:eaan2392
    [Google Scholar]
  113. 113. 
    Arundel AV, Sterling EM, Biggin JH, Sterling TD 1986. Indirect health effects of relative humidity in indoor environments. Environ. Health Perspect. 65:351–61
    [Google Scholar]
  114. 114. 
    Zhou P, Yang X-L, Wang X-G, Hu B, Zhang L et al. 2020. Discovery of a novel coronavirus associated with the recent pneumonia outbreak in humans and its potential bat origin. bioRxiv 2020.01.22.914952. https://doi.org/10.1101/2020.01.22.914952
    [Crossref]
  115. 115. 
    Letko M, Munster V. 2020. Functional assessment of cell entry and receptor usage for lineage B β-coronaviruses, including 2019-nCoV. bioRxiv 2020.01.22.915660. https://doi.org/10.1101/2020.01.22.915660
    [Crossref]
  116. 116. 
    Zhao Y, Zhao Z, Wang Y, Zhou Y, Ma Y, Zuo W 2020. Single-cell RNA expression profiling of ACE2, the putative receptor of Wuhan 2019-nCov. bioRxiv 2020.01.26.919985. https://doi.org/10.1101/2020.01.26.919985
    [Crossref]
  117. 117. 
    Luo W, Majumder MS, Liu D, Poirier C, Mandl KD et al. 2020. The role of absolute humidity on transmission rates of the COVID-19 outbreak. medRxiv 2020.02.12.20022467. https://doi.org/10.1101/2020.02.12.20022467
    [Crossref]
  118. 118. 
    Rondanelli M, Miccono A, Lamburghini S, Avanzato I, Riva A et al. 2018. Self-care for common colds: the pivotal role of vitamin D, vitamin C, zinc, and echinacea in three main immune interactive clusters (physical barriers, innate and adaptive immunity) involved during an episode of common colds—practical advice on dosages and on the time to take these nutrients/botanicals in order to prevent or treat common colds. Evid. Based Complement. Alternat. Med. 2018:5813095
    [Google Scholar]
  119. 119. 
    Besedovsky L, Lange T, Haack M 2019. The sleep-immune crosstalk in health and disease. Physiol. Rev. 99:1325–80
    [Google Scholar]
  120. 120. 
    Lee BY, Shah M. 2012. Prevention of influenza in healthy children. Expert Rev. Anti Infect. Ther. 10:1139–52
    [Google Scholar]
  121. 121. 
    Warren-Gash C, Fragaszy E, Hayward AC 2013. Hand hygiene to reduce community transmission of influenza and acute respiratory tract infection: a systematic review. Influenza Other Respir. Viruses 7:738–49
    [Google Scholar]
  122. 122. 
    Ritzel G. 1966. Sozialmedizinische Erhebungen zur Pathogenese und Prophylaxe von Erkältungskrankheiten. Int. J. Public Health 11:9–16
    [Google Scholar]
  123. 123. 
    Sale CS. 1972. Humidification to reduce respiratory illnesses in nursery school children. South. Med. J. 65:882–85
    [Google Scholar]
  124. 124. 
    Green GH. 1974. The effect of indoor relative humidity on absenteeism and colds in schools. ASHRAE Trans 80:131–41
    [Google Scholar]
  125. 125. 
    Green GH. 1985. Indoor relative humidities in winter and the related absenteeism. ASHRAE Trans 91:643–56
    [Google Scholar]
  126. 126. 
    Green GH. 1982. The positive and negative effects of building humidification. ASHRAE Trans 88:1049–61
    [Google Scholar]
  127. 127. 
    Gelperin A. 1973. Humidification and upper respiratory infection incidence. Heating, Piping, Air Conditioning 45:77–78
    [Google Scholar]
  128. 128. 
    Reiman JM, Das B, Sindberg GM, Urban MD, Hammerlund MEM et al. 2018. Humidity as a non-pharmaceutical intervention for influenza A. PLOS ONE 13:e0204337
    [Google Scholar]
/content/journals/10.1146/annurev-virology-012420-022445
Loading
/content/journals/10.1146/annurev-virology-012420-022445
Loading

Data & Media loading...

Supplemental Material

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error