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International Journal of Biometeorology

, Volume 61, Issue 4, pp 613–622 | Cite as

Influenza transmission during extreme indoor conditions in a low-resource tropical setting

  • James TameriusEmail author
  • Sergio Ojeda
  • Christopher K. Uejio
  • Jeffrey Shaman
  • Brenda Lopez
  • Nery Sanchez
  • Aubree Gordon
Original Paper

Abstract

Influenza transmission occurs throughout the planet across wide-ranging environmental conditions. However, our understanding of the environmental factors mediating transmission is evaluated using outdoor environmental measurements, which may not be representative of the indoor conditions where influenza is transmitted. In this study, we examined the relationship between indoor environment and influenza transmission in a low-resource tropical population. We used a case-based ascertainment design to enroll 34 households with a suspected influenza case and then monitored households for influenza, while recording indoor temperature and humidity data in each household. We show that the indoor environment is not commensurate with outdoor conditions and that the relationship between indoor and outdoor conditions varies significantly across homes. We also show evidence of influenza transmission in extreme indoor environments. Specifically, our data suggests that indoor environments averaged 29 °C, 18 g/kg specific humidity, and 68 % relative humidity across 15 transmission events observed. These indoor settings also exhibited significant temporal variability with temperatures as high as 39 °C and specific and relative humidity increasing to 22 g/kg and 85 %, respectively, during some transmission events. However, we were unable to detect differences in the transmission efficiency by indoor temperature or humidity conditions. Overall, these results indicate that laboratory studies investigating influenza transmission and virus survival should increase the range of environmental conditions that they assess and that observational studies investigating the relationship between environment and influenza activity should use caution using outdoor environmental measurements since they can be imprecise estimates of the conditions that mediate transmission indoors.

Keywords

Influenza Indoor Environment Specific Humidity Transmission Efficiency Outdoor Temperature 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

This publication was developed under Assistance Agreement No. (RD No. 83574901) awarded by the US Environmental Protection Agency to Christopher K. Uejio. It has not been formally reviewed by the EPA. The views expressed in this document are solely those of the authors and do not necessarily reflect those of the Agency. EPA does not endorse any products or commercial services mentioned in this publication. This work was also supported by an Old Gold Fellowship form the College of Liberal Arts and Sciences at the University of Iowa (JT); the US Environmental Protection Agency RD No. 83574901 (JT, CU); and the National Institute of Allergy and Infectious Diseases, National Institutes of Health, under grant number U01AI088654 (AG), and was funded through a career development award from the John E. Fogarty International Center, National Institutes of Health (K02 TW009483; AG).

Compliance with ethical standards

Written informed consent or parental proxy was obtained for all participants. In addition, verbal assent was obtained from children aged 6 years and older. This study was approved by the Institutional Review Boards at the Ministry of Health, Nicaragua, the University of Michigan, and the University of California, Berkeley.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

484_2016_1238_MOESM1_ESM.docx (728 kb)
ESM 1 (DOCX 727 kb)

References

  1. Alonso WJ, Guillebaud J, Viboud C, et al. (2015) Influenza seasonality in Madagascar: the mysterious African free-runner. Influenza Other Respir Viruses 9:101–109. doi: 10.1111/irv.12308 CrossRefGoogle Scholar
  2. Carrat F, Vergu E, Ferguson NM, et al. (2008) Time lines of infection and disease in human influenza: a review of volunteer challenge studies. Am J Epidemiol 167:775–785. doi: 10.1093/aje/kwm375 CrossRefGoogle Scholar
  3. Cauchemez S, Carrat F, Viboud C, et al. (2004) A Bayesian MCMC approach to study transmission of influenza: application to household longitudinal data. Stat Med 23:3469–3487. doi: 10.1002/sim.1912 CrossRefGoogle Scholar
  4. Chow GC (1960) Tests of equality between sets of coefficients in two linear regressions. Econometrica 28:591. doi: 10.2307/1910133 CrossRefGoogle Scholar
  5. Chowell G, Towers S, Viboud C, et al. (2012) The influence of climatic conditions on the transmission dynamics of the 2009 A/H1N1 influenza pandemic in Chile. BMC Infect Dis 12:298. doi: 10.1186/1471-2334-12-298 CrossRefGoogle Scholar
  6. Davis RE, McGregor GR, Enfield KB (2016) Humidity: a review and primer on atmospheric moisture and human health. Environ Res 144:106–116. doi: 10.1016/j.envres.2015.10.014 CrossRefGoogle Scholar
  7. Ferguson NM, Cummings DAT, Cauchemez S, et al. (2005) Strategies for containing an emerging influenza pandemic in Southeast. Asia 437:209–214. doi: 10.1038/nature04017 Google Scholar
  8. Hanley BP, Borup B (2010) Research aerosol influenza transmission risk contours: a study of humid tropics versus winter temperate zoneGoogle Scholar
  9. Lofgren E, Fefferman NH, Naumov YN, et al. (2007) Influenza seasonality: underlying causes and modeling theories. J Virol 81:5429–5436. doi: 10.1128/JVI.01680-06 CrossRefGoogle Scholar
  10. Lowen AC, Mubareka S, Steel J, Palese P (2007) Influenza virus transmission is dependent on relative humidity and temperature. PLoS Pathog 3:e151–1476. doi: 10.1371/journal.ppat.0030151 CrossRefGoogle Scholar
  11. Lowen AC, Steel J, Mubareka S, Palese P (2008) High temperature (30° C) blocks aerosol but not contact transmission of influenza virus. J Virol 82:5650–5652. doi: 10.1128/JVI.00325-08 CrossRefGoogle Scholar
  12. Manly BFJ (2006) Randomization, bootstrap and Monte Carlo methods in biology, Third edn. CRC Press, USAGoogle Scholar
  13. McDevitt J, Rudnick S, First M, Spengler J (2010) Role of absolute humidity in the inactivation of influenza viruses on stainless steel surfaces at elevated temperatures. Appl Environ Microbiol 76:3943–3947. doi: 10.1128/AEM.02674-09 CrossRefGoogle Scholar
  14. Moser MR, Bender TR, Margolis HS, et al. (1979) An outbreak of influenza aboard a commercial airliner. Am J Epidemiol 110:1–6CrossRefGoogle Scholar
  15. Nguyen JL, Schwartz J, Dockery DW (2014) The relationship between indoor and outdoor temperature, apparent temperature, relative humidity, and absolute humidity. Indoor Air 24:103–112. doi: 10.1111/ina.12052 CrossRefGoogle Scholar
  16. Shaman J, Kohn M (2009) Absolute humidity modulates influenza survival, transmission, and seasonality. Proc Natl Acad Sci U S A 106:3243–3248. doi: 10.1073/pnas.0806852106 CrossRefGoogle Scholar
  17. Shaman J, Pitzer VE, Viboud C, et al. (2010) Absolute humidity and the seasonal onset of influenza in the continental United States. PLoS Biol 8:e1000316. doi: 10.1371/journal.pbio.1000316 CrossRefGoogle Scholar
  18. Smirnov NV (1933) Estimate of deviation between empirical distribution functions in two independent samples. Bulletin Moscow University 2:3–16Google Scholar
  19. Soebiyanto RP, Clara W, Jara J, et al. (2014) The role of temperature and humidity on seasonal influenza in tropical areas: Guatemala, El Salvador and Panama, 2008–2013. PLoS One 9:e100659. doi: 10.1371/journal.pone.0100659 CrossRefGoogle Scholar
  20. Soebiyanto RP, Clara WA, Jara J (2015) Associations between seasonal influenza and meteorological parameters in Costa Rica, Honduras and Nicaragua. Geospatial. doi: 10.4081/gh.2015.372 Google Scholar
  21. Tamerius J, Nelson MI, Zhou SZ, et al. (2011) Global influenza seasonality: reconciling patterns across temperate and tropical regions. Environ Health Perspect 119:439–445. doi: 10.1289/ehp.1002383 CrossRefGoogle Scholar
  22. Tamerius JD, Shaman J, Alonso WJ, et al. (2013a) Environmental predictors of seasonal influenza epidemics across temperate and tropical climates. PLoS Pathog 9:e1003194. doi: 10.1371/journal.ppat.1003194 CrossRefGoogle Scholar
  23. Tamerius JD, Perzanowski MS, Acosta LM, et al. (2013b) Socioeconomic and outdoor meteorological determinants of indoor temperature and humidity in New York City dwellings*. Wea Climate Soc 5:168–179. doi: 10.1175/WCAS-D-12-00030.s1 CrossRefGoogle Scholar
  24. Tamerius J, Viboud C, Shaman J, Chowell G (2015) Impact of school cycles and environmental forcing on the timing of pandemic influenza activity in Mexican states, May-December 2009. PLoS Comput Biol 11:e1004337. doi: 10.1371/journal.pcbi.1004337 CrossRefGoogle Scholar
  25. Te Beest DE, van Boven M, Hooiveld M, et al. (2013) Driving factors of influenza transmission in the Netherlands. Am J Epidemiol 178:1469–1477. doi: 10.1093/aje/kwt132 CrossRefGoogle Scholar
  26. Thai PQ, Choisy M, Duong TN, et al. (2015) Seasonality of absolute humidity explains seasonality of influenza-like illness in Vietnam. Epidemics. doi: 10.1016/j.epidem.2015.06.002 Google Scholar
  27. Uejio CK, Tamerius JD, Vredenburg J, et al. (2015) Summer indoor heat exposure and respiratory and cardiovascular distress calls in New York City, NY, U.S. Indoor Air n/a–n/a. doi: 10.1111/ina.12227 Google Scholar
  28. White-Newsome JL, Sánchez BN, Jolliet O, et al. (2012) Climate change and health: indoor heat exposure in vulnerable populations. Environ Res 112:20–27. doi: 10.1016/j.envres.2011.10.008 CrossRefGoogle Scholar
  29. 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. doi: 10.1371/journal.pone.0046789 CrossRefGoogle Scholar
  30. Yu H, Alonso WJ, Feng L, et al. (2013) Characterization of regional influenza seasonality patterns in China and implications for vaccination strategies: Spatio-temporal modeling of surveillance data. PLoS Med 10:e1001552. doi: 10.1371/journal.pmed.1001552 CrossRefGoogle Scholar

Copyright information

© ISB 2016

Authors and Affiliations

  • James Tamerius
    • 1
    Email author
  • Sergio Ojeda
    • 2
  • Christopher K. Uejio
    • 3
    • 4
  • Jeffrey Shaman
    • 5
  • Brenda Lopez
    • 2
  • Nery Sanchez
    • 2
  • Aubree Gordon
    • 3
    • 4
  1. 1.Department of Geographical and Sustainability SciencesUniversity of IowaIowa CityUSA
  2. 2.Sustainable Sciences InstituteManaguaNicaragua
  3. 3.Department of Geography and Program in Public HealthFlorida State UniversityTallahasseeUSA
  4. 4.Department of Epidemiology, School of Public HealthUniversity of MichiganAnn ArborUSA
  5. 5.Environmental Health Sciences, Mailman School of Public HealthColumbia UniversityNew YorkUSA

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