Influenza virus transmission is dependent on relative humidity and temperature - PubMed (original) (raw)
Influenza virus transmission is dependent on relative humidity and temperature
Anice C Lowen et al. PLoS Pathog. 2007.
Abstract
Using the guinea pig as a model host, we show that aerosol spread of influenza virus is dependent upon both ambient relative humidity and temperature. Twenty experiments performed at relative humidities from 20% to 80% and 5 degrees C, 20 degrees C, or 30 degrees C indicated that both cold and dry conditions favor transmission. The relationship between transmission via aerosols and relative humidity at 20 degrees C is similar to that previously reported for the stability of influenza viruses (except at high relative humidity, 80%), implying that the effects of humidity act largely at the level of the virus particle. For infected guinea pigs housed at 5 degrees C, the duration of peak shedding was approximately 40 h longer than that of animals housed at 20 degrees C; this increased shedding likely accounts for the enhanced transmission seen at 5 degrees C. To investigate the mechanism permitting prolonged viral growth, expression levels in the upper respiratory tract of several innate immune mediators were determined. Innate responses proved to be comparable between animals housed at 5 degrees C and 20 degrees C, suggesting that cold temperature (5 degrees C) does not impair the innate immune response in this system. Although the seasonal epidemiology of influenza is well characterized, the underlying reasons for predominant wintertime spread are not clear. We provide direct, experimental evidence to support the role of weather conditions in the dynamics of influenza and thereby address a long-standing question fundamental to the understanding of influenza epidemiology and evolution.
Conflict of interest statement
Competing interests. The authors have declared that no competing interests exist.
Figures
Figure 1. Arrangement of Infected and Exposed Guinea Pigs in Environmental Chamber
In each experiment, eight animals were housed in a Caron 6030 environmental chamber. Each guinea pig was placed in its own cage, and two cages were positioned on each shelf. Naïve animals were placed behind infected animals, such that the direction of airflow was toward the naïve animals. The cages used were open to airflow through the top and one side, both of which were covered by wire mesh. Although infected and exposed guinea pigs were placed in pairs, air flowed freely between shelves, allowing transmission to occur from any infected to any naïve animal.
Figure 2. Transmission of Influenza Virus from Guinea Pig to Guinea Pig Is Dependent on Relative Humidity
Titers of influenza virus in nasal wash samples are plotted as a function of day p.i. Overall transmission rate and the RH and temperature conditions of each experiment are stated underneath the graph. Titers from intranasally inoculated guinea pigs are represented as dashed lines; titers from exposed guinea pigs are shown with solid lines. Virus titrations were performed by plaque assay on Madin Darby canine kidney cells.
Figure 3. Transmission of Influenza Virus from Guinea Pig to Guinea Pig Is Highly Efficient at 5 °C and Blocked at 30 °C
Titers of influenza virus in nasal wash samples are plotted as a function of day p.i. Overall transmission rate and the RH and temperature conditions of each experiment are stated underneath the graph. Titers from intranasally inoculated guinea pigs are represented as dashed lines; titers from exposed guinea pigs are shown with solid lines.
Figure 4. Guinea Pigs Housed at 5 °C Shed Influenza Virus at Higher Titers on Days 4, 6, and 8 p.i. Than Guinea Pigs Housed at 20 °C
Average viral titers in nasal wash samples collected from animals housed at either 5 °C or 20 °C and all RH tested are plotted as function of time post-infection. Error bars indicate standard deviation; * indicates statistically significant difference between titers at 5 °C and 20 °C, with p ≤ 0.005.
Figure 5. Antiviral and Pro-Inflammatory Responses Are Similar between Guinea Pigs Housed at 5 °C and 20 °C
Levels of the indicated mRNA transcripts present in nasal turbinates of infected guinea pigs housed at 5 °C (black bars) or 20 °C (grey bars) were quantified by real-time PCR of reverse transcribed mRNA. RNA levels were normalized to β-actin and are expressed as fold-induction over mock-infected guinea pig. Error bars represent standard deviation. * indicates a statistically significant (p < 0.05) difference between 5 °C and 20 °C.
Figure 6. Variation of Transmission Efficiency with Relative Humidity: A Model
At 20 °C (dashed line), transmission efficiency is highest at low RH, when influenza virions in an aerosol are relatively stable, and desiccation of exhaled respiratory droplets produces droplet nuclei. Transmission is diminished at intermediate RH when virus particles are relatively unstable, but improves in parallel with influenza virus stability at higher humidities. At high RH, evaporation from exhaled particles is limited, respiratory droplets settle out of the air, and transmission is blocked. At 5 °C (solid line), transmission is more efficient than at 20 °C, but is reduced to a rate of 50% at higher humidities.
Similar articles
- Transmission of a 2009 pandemic influenza virus shows a sensitivity to temperature and humidity similar to that of an H3N2 seasonal strain.
Steel J, Palese P, Lowen AC. Steel J, et al. J Virol. 2011 Feb;85(3):1400-2. doi: 10.1128/JVI.02186-10. Epub 2010 Nov 17. J Virol. 2011. PMID: 21084485 Free PMC article. - Environmental Conditions Affect Exhalation of H3N2 Seasonal and Variant Influenza Viruses and Respiratory Droplet Transmission in Ferrets.
Gustin KM, Belser JA, Veguilla V, Zeng H, Katz JM, Tumpey TM, Maines TR. Gustin KM, et al. PLoS One. 2015 May 13;10(5):e0125874. doi: 10.1371/journal.pone.0125874. eCollection 2015. PLoS One. 2015. PMID: 25969995 Free PMC article. - Environmental Persistence of Influenza Viruses Is Dependent upon Virus Type and Host Origin.
Kormuth KA, Lin K, Qian Z, Myerburg MM, Marr LC, Lakdawala SS. Kormuth KA, et al. mSphere. 2019 Aug 21;4(4):e00552-19. doi: 10.1128/mSphere.00552-19. mSphere. 2019. PMID: 31434749 Free PMC article. - Humidity and respiratory virus transmission in tropical and temperate settings.
Paynter S. Paynter S. Epidemiol Infect. 2015 Apr;143(6):1110-8. doi: 10.1017/S0950268814002702. Epub 2014 Oct 13. Epidemiol Infect. 2015. PMID: 25307020 Free PMC article. Review. - Aerosol transmission of influenza A virus: a review of new studies.
Tellier R. Tellier R. J R Soc Interface. 2009 Dec 6;6 Suppl 6(Suppl 6):S783-90. doi: 10.1098/rsif.2009.0302.focus. Epub 2009 Sep 22. J R Soc Interface. 2009. PMID: 19773292 Free PMC article. Review.
Cited by
- Role of vitamin D in COVID-19 and other viral infections.
Engin MMN, Özdemir Ö. Engin MMN, et al. World J Virol. 2024 Sep 25;13(3):95349. doi: 10.5501/wjv.v13.i3.95349. World J Virol. 2024. PMID: 39323448 Free PMC article. Review. - Forecasting influenza epidemics in China using transmission dynamic model with absolute humidity.
Chen X, Tao F, Chen Y, Cheng J, Zhou Y, Wang X. Chen X, et al. Infect Dis Model. 2024 Aug 10;10(1):50-59. doi: 10.1016/j.idm.2024.08.003. eCollection 2025 Mar. Infect Dis Model. 2024. PMID: 39319283 Free PMC article. - Breathing Clean Air: Navigating Indoor Air Purification Techniques and Finding the Ideal Solution.
Alhussain H, Ghani S, Eltai NO. Alhussain H, et al. Int J Environ Res Public Health. 2024 Aug 21;21(8):1107. doi: 10.3390/ijerph21081107. Int J Environ Res Public Health. 2024. PMID: 39200716 Free PMC article. Review. - Impact of organic compounds on the stability of influenza A virus in deposited 1-μL droplets.
Schaub A, David SC, Glas I, Klein LK, Violaki K, Terrettaz C, Motos G, Bluvshtein N, Luo B, Pohl M, Hugentobler W, Nenes A, Krieger UK, Peter T, Stertz S, Kohn T. Schaub A, et al. mSphere. 2024 Sep 25;9(9):e0041424. doi: 10.1128/msphere.00414-24. Epub 2024 Aug 22. mSphere. 2024. PMID: 39171937 Free PMC article. - Increased Risk of Influenza Infection During Cold Spells in China: National Time Series Study.
Wang H, Geng M, Schikowski T, Areal AT, Hu K, Li W, Coelho MSZS, Saldiva PHN, Sun W, Zhou C, Lu L, Zhao Q, Ma W. Wang H, et al. JMIR Public Health Surveill. 2024 Aug 13;10:e55822. doi: 10.2196/55822. JMIR Public Health Surveill. 2024. PMID: 39140274 Free PMC article.
References
- Thompson WW, Shay DK, Weintraub E, Brammer L, Bridges CB, et al. Influenza-associated hospitalizations in the United States. JAMA. 2004;292:1333–1340. - PubMed
- Shek LP, Lee BW. Epidemiology and seasonality of respiratory tract virus infections in the tropics. Paediatr Respir Rev. 2003;4:105–111. - PubMed
Publication types
MeSH terms
Grants and funding
- U01 CI000354/CI/NCPDCID CDC HHS/United States
- U19 AI062623/AI/NIAID NIH HHS/United States
- UC19 AI062623-023/AI/NIAID NIH HHS/United States
- U01CI000354-01/CI/NCPDCID CDC HHS/United States
LinkOut - more resources
Full Text Sources
Other Literature Sources
Medical