Predictors of indoor absolute humidity and estimated effects on influenza virus survival in grade schools
© Koep et al.; licensee BioMed Central Ltd. 2013
Received: 13 November 2012
Accepted: 29 January 2013
Published: 5 February 2013
Low absolute humidity (AH) has been associated with increased influenza virus survival and transmissibility and the onset of seasonal influenza outbreaks. Humidification of indoor environments may mitigate viral transmission and may be an important control strategy, particularly in schools where viral transmission is common and contributes to the spread of influenza in communities. However, the variability and predictors of AH in the indoor school environment and the feasibility of classroom humidification to levels that could decrease viral survival have not been studied.
Automated sensors were used to measure temperature, humidity and CO2 levels in two Minnesota grade schools without central humidification during two successive winters. Outdoor AH measurements were derived from the North American Land Data Assimilation System. Variability in indoor AH within classrooms, between classrooms in the same school, and between schools was assessed using concordance correlation coefficients (CCC). Predictors of indoor AH were examined using time-series Auto-Regressive Conditional Heteroskedasticity models. Classroom humidifiers were used when school was not in session to assess the feasibility of increasing indoor AH to levels associated with decreased influenza virus survival, as projected from previously published animal experiments.
AH varied little within classrooms (CCC >0.90) but was more variable between classrooms in the same school (CCC 0.81 for School 1, 0.88 for School 2) and between schools (CCC 0.81). Indoor AH varied widely during the winter (range 2.60 to 10.34 millibars [mb]) and was strongly associated with changes in outdoor AH (p < 0.001). Changes in indoor AH on school weekdays were strongly associated with CO2 levels (p < 0.001). Over 4 hours, classroom humidifiers increased indoor AH by 4 mb, an increase sufficient to decrease projected 1-hour virus survival by an absolute value of 30% during winter months.
During winter, indoor AH in non-humidified grade schools varies substantially and often to levels that are very low. Indoor results are predicted by outdoor AH over a season and CO2 levels (which likely reflects human activity) during individual school days. Classroom humidification may be a feasible approach to increase indoor AH to levels that may decrease influenza virus survival and transmission.
KeywordsInfluenza Humidity Schools Climate
Previous influenza studies have examined the association between absolute and relative humidity and influenza activity [1–3]. Absolute humidity (AH) is the water content of air, measured in millibars (mb), independent of barometric pressure and temperature. Relative humidity (RH) is the ratio (expressed as a percent) of the measured water content of air relative to the maximum possible water content of that air, which is dependent on the barometric pressure and temperature. Given these relationships, at a specified AH, the RH of colder air will be higher than that of warmer air. Recent studies indicate that absolute humidity (AH) is associated with the transmission of influenza. Animal experiments show that viral survival and transmissibility are enhanced under conditions of low AH . In temperate climates, seasonal influenza epidemics and waves of the 2009 A/H1N1 influenza pandemic have been associated with decreases in outdoor AH [4, 5]. Despite these findings, the role of AH in viral transmission in indoor environments—where the bulk of influenza transmission in temperate regions likely occurs during winter—has not been examined.
Grade schools are an important setting to study the association between AH and influenza transmission because large numbers of school children are exposed to similar indoor air conditions for many hours during the day and because of the prominent role that viral transmission within schools plays in the spread of influenza in communities [6, 7].
In this study, we examined the variability of indoor AH within and between classrooms during winter in two grade schools in Minnesota, a state with a temperate climate including cold, dry winters. We also examined the association between hourly and daily fluctuations of indoor AH and outdoor AH and the association between indoor AH and indoor temperature, relative humidity (RH), and CO2 levels (as a surrogate for moisture contributions from human respiration). We then determined the effect of in-room humidification on indoor AH in classrooms. Based on these observations, we modeled the potential effects of indoor AH on influenza virus survival in classrooms.
School descriptions and ventilation capacities
Size in square feet (year of construction)
Number of rooms
Main Building: 33,095 (1950)
Intra-Room Variability: 5 sensors in each of 3 rooms
Air Exchange: 15 cubic feet per minute (CFM) per person
Addition: 16,813 (1965)
7 student service rooms
Inter-Room Variability: 14 unique rooms
Heat: Steam and hot water
Inter-School Variability: 32 combined rooms between schools
Main Building: 145,279 (1962)
Intra-Room Variability: 5 sensors in 1 room
Air Exchange: 15 cubic feet per minute (CFM) per person
Addition: 20,704 (1989)
25 student service rooms
Inter-Room Variability: 18 unique rooms
Heat: Hot water
Inter-School Variability: 32 combined rooms between schools
Automated data loggers were used to measure temperature, relative humidity and CO2 continuously at 5-minute intervals (HOBO U12-012, Onset: Bourne, MA, temperature accuracy 0.35°C from 0° to 50°C, relative humidity accuracy ±2.5% from 10% to 90% RH; Telaire 7001, CO2 measurement accuracy ±50 ppm). All sensors are calibrated at time of manufacture. No additional validation was done prior to use. Individual home humidifiers (MoistAir MA1201, Essick Air: Little Rock, AR, whole house humidification up to 2,500 sq. ft, humidistat control) were used to raise school humidity levels on weekend days when no students or staff were present.
Temperature and RH data loggers were placed at a height of 5–7 feet in various locations in School 1 and 2 to assess variability in AH within and between classrooms (Table 1). Thirty loggers were used in School 1 and forty were used in School 2. Standardized locations of loggers for within-classroom measurements were: close to the main doorway from the hallway into the classroom; near exterior facing windows and walls; on interior walls. The standardized location of loggers for between-classroom measurements was close to the main doorway from the hallway into the classroom. CO2 data loggers were placed at three locations in School 1 and four locations in School 2 in both classrooms and common areas.
Moist-Air MA1201 Essick Humidifiers were placed in 3 individual classrooms on a single weekend day in February 2012, which was chosen for convenience. All manipulations were performed with classroom doors to the hallway closed and building air exchange systems off. Multiple data loggers were present in each room to determine the radius of humidification. Humidifiers were set to target levels of 60% RH and were turned off upon reaching this target. Data loggers continued recording approximately 12 hours after humidifiers were turned off. Data loggers were also present in other classrooms within the school to measure AH changes in non-humidified rooms.
Data management and statistics
Data loggers recorded indoor temperature, RH, and CO2 levels at 5-minute intervals from early January to late March 2011. Data were downloaded from the loggers once a month and exported into Excel using commercial software (HOBOware, Onset: Bourne, MA).
where q is specific humidity, p is surface pressure and ε = 0.622.
Concordance correlation coefficients were used to assess AH variability within classrooms (intra-room), between classrooms (inter-room), and between schools (inter-school).
Daily changes in indoor AH associated with changes in outdoor AH
0.51 [0.48, 0.54]
0.50 [0.48, 0.52]
-0.02 [-0.04, -0.002]
0.48 [0.39, 0.57]
-0.05 [-0.07, -0.02]
0.36 [0.27, 0.44]
Hourly changes in indoor AH associated with changes in CO 2
100 x CO2*
School vs non-school Hours
0. 15 [ 0.14, 0.16]
0. 15 [0.15, 0.16]
-0.08 [-0.01, -0.07]
0.09 [0.07, 0.11]
Intra- and inter-room and inter-school variability
We explored sensor agreement for indoor AH from January through March using concordance correlation coefficients (CCC) at 3-hour time intervals; details of sensor comparisons are listed in Table 1. There was little variability in indoor AH measurements at different locations within individual classrooms (intra-room concordance correlation coefficients [CCC] >0.90 in both School 1 and 2). Greater variability was observed between classrooms in both School 1 and School 2 (inter-room CCC, 0.81 [CI: 0.76, 0.87] and 0.88 [CI: 0.84, 0.92], respectively) and between School 1 and School 2 as a whole (inter-school CCC, 0.81 [CI: 0.75, 0.88]).
Daily and hourly variability
Adjusting for between school differences, daily periodicity in indoor AH, and auto-regressive lags within the model, outdoor AH was associated with indoor AH over the course of the winter school period (ARCH model regression coefficient 0.51; confidence intervals [CI] 0.48, 0.54; p < 0.001; Table 2: Model A). Further adjustments for outdoor temperature and indoor temperature did not substantially modify the association between outdoor and indoor AH (Models B, C). In the adjusted model (Model C), a one standard deviation (SD) increase in outdoor AH was associated with a 0.90 mb average increase in indoor AH, while a one SD increase in outdoor and indoor temperatures were associated with a −0.24 mb and 0.33 mb average difference in indoor AH, respectively. All three coefficients were highly statistically significant in the adjusted model (p < 0.001).
Indoor absolute humidity in grade schools varies substantially during winter—often to levels that are very low—and these fluctuations are associated primarily with changes in outdoor AH (Figure 1). In addition, during an individual school day, we noted that diurnal changes in indoor AH were associated closely with levels of CO2 (Figure 2). We speculate these diurnal changes in indoor AH are primarily due to the contribution of moisture from human respiration by students, teachers and other staff, although the use of toilets, sinks, and water fountains during weekday hours may account for a portion of these changes. Finally, we showed that classroom humidifiers can increase indoor AH substantially over several hours (Figure 3).
The implications of these findings are important with respect to the potential impact of ambient indoor AH and humidification on survival of influenza virus in the school environment. Modest, achievable changes in indoor AH are likely to have a substantial effect on 1-hour influenza virus survival, as projected from laboratory experiments (Figures 4A, 4B) . For example, mean calculated 1-hour virus survival is projected to decrease from approximately 75% during periods when indoor AH is very low (~3-4 mb) to 35% when indoor AH is raised to 10 mb, a target we demonstrate can be achieved over several hours by a classroom humidifier set to a target RH of 60% on a winter day. During late spring and early fall, indoor school AH often reached 10mb and 60% RH (data not shown). Our estimation of changes in virus survival are limited to models constructed from a single set of animal experiments; however, other experiments have demonstrated similar increases in survival at very low humidity [12, 13]. These data suggest that raising wintertime indoor AH to levels typically experienced indoors during fall and spring offers a strategy to reduce transmission of influenza in schools, and potentially the community, particularly when combined with vaccination and other non-pharmaceutical interventions [14–18]. As our measures reflect changes in 1 hour virus survival, humidification over a longer period (4 hours or longer) would afford a greater opportunity to reduce transmission more substantially. Indeed, this intervention may be particularly important when influenza outbreaks (or pandemics) due to novel influenza viruses occur and effective vaccines and antiviral medications are not available. However, the potential effects of wintertime humidification in older buildings need to be evaluated with respect to the potential for building rot or proliferations of mold.
Further research is needed to directly investigate the association of indoor AH with influenza virus survival in the school environment and to evaluate the effect of indoor AH on the incidence of influenza illness and school absence among school children. We also need a better understanding of school Heating Ventilation and Air Condition (HVAC) systems and their capacity for humidification, as well as additional tests of classroom humidification, to better estimate the potential benefit of humidification on decreasing influenza transmission in schools.
Our study is limited by the fact that we measured indoor AH in 2 schools using a single type of sensor in a region with very cold, dry winters. The schools were both older facilities and their HVAC systems had limited capacity for humidification. Measurement of indoor AH in newer facilities with humidification equipment may demonstrate different results. Our tests of classroom humidification were performed under controlled conditions (doors to the classroom closed and HVAC ventilation turned off), and additional study of the feasibility of classroom humidification under routine operating conditions is needed. Finally, our projections of virus survival are limited in that they are calculated using data from previously reported laboratory experiments of influenza virus survival, and we did not include direct measures of infectious virus or virus RNA [19–21]. As such, these projections serve only as an estimate of the potential impact of increasing AH in schools on influenza virus survival.
We report here environmental assessments exploring the association of absolute humidity on influenza epidemiology by expanding our understanding of AH in school classrooms. We note the potential for very low indoor AH, a condition that occurs frequently during wintertime months in some regions, to increase the survival and transmission of influenza in this environment. Further investigation is necessary to determine whether increasing humidity in school classrooms is a feasible and effective means of decreasing influenza transmission among school children and in the community.
Auto-Regressive Conditional Heteroskedasticity
Concordance Correlation Coefficient
Heating Ventilation and Air Conditioning.
The authors would like to thank Jen McCormick, Ph. D. and Carmen Tapia of the Mayo Clinic for considerations in study design and ethical concerns. We also thank staff and students and Rochester Public Schools for help in data collection.
Sources of financial support
This project is supported by NIH/NCRR CTSA Grant Number TL1 RR024152 and an intramural grant from the Mayo Clinic Department of Pediatric and Adolescent Medicine. Additional support provided by the NIH Models of Infectious Disease Agent Study program through cooperative agreement 1U54GM088558, as well as NIEHS Center grant ES009089. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health or the National Institute of General Medical Sciences.
- Lowen AC, Mubareka S, et al: Influenza virus transmission is dependent on relative humidity and temperature. PLoS Pathog. 2007, 3 (10): 1470-1476.View ArticlePubMed
- Yang W, Marr LC: Dynamics of airborne influenza A viruses indoors and dependence on humidity. PLoS One. 2011, 6 (6): e21481-10.1371/journal.pone.0021481.PubMed CentralView ArticlePubMed
- Shaman J, Kohn M: Absolute humidity modulates influenza survival, transmission, and seasonality. Proc Natl Acad Sci USA. 2009, 106 (9): 3243-3248. 10.1073/pnas.0806852106.PubMed CentralView ArticlePubMed
- Shaman J, Pitzer VE, et al: Absolute humidity and the seasonal onset of influenza in the continental United States. PLoS Biol. 2010, 8 (2): e1000316-10.1371/journal.pbio.1000316.PubMed CentralView ArticlePubMed
- Shaman J, Goldstein E, et al: Absolute humidity and pandemic versus epidemic influenza. Am J Epidemiol. 2011, 173 (2): 127-135. 10.1093/aje/kwq347.PubMed CentralView ArticlePubMed
- Chao DL, Halloran ME, et al: School opening dates predict pandemic influenza A(H1N1) outbreaks in the United States. J Infect Dis. 2010, 202 (6): 877-880. 10.1086/655810.PubMed CentralView ArticlePubMed
- Cauchemez S, Ferguson NM, et al: Closure of schools during an influenza pandemic. Lancet Infect Dis. 2009, 9 (8): 473-481. 10.1016/S1473-3099(09)70176-8.View ArticlePubMed
- Pierret C, Sonju J, Leicester J, et al: Significant improvement in student proficiency: rebuilding science education InSciEd Out. 2011, Washington, D.C: American Association for the Advancement of Science
- NOAA/NCEP/EMC: North American Land Data Assimilation System. 2011, http://www.emc.ncep.noaa.gov/mmb/nldas,
- Wallace JM, Hobbs PV: Atmospheric Science, An Introductory Survey. 2006, New York: Academic, 2
- Engle RF, Lilien DM, Robins RP: Estimating time varying risk premia in the term structure: The ARCH-M model. Econometrica. 1987, 55: 391-407. 10.2307/1913242.View Article
- Schaffer FL, Soergel ME, et al: Survival of airborne influenza virus: effects of propagating host, relative humidity, and composition of spray fluids. Arch Virol. 1976, 51 (4): 263-273. 10.1007/BF01317930.View ArticlePubMed
- Shechmeister IL: Studies on the experimental epidemiology of respiratory infections. J Infect Dis. 1950, 87 (2): 128-132. 10.1093/infdis/87.2.128.View ArticlePubMed
- Stebbins S, Cummings DA, et al: Reduction in the incidence of influenza A but not influenza B associated with use of hand sanitizer and cough hygiene in schools: a randomized controlled trial. Pediatr Infect Dis J. 2011, 30 (11): 921-926. 10.1097/INF.0b013e3182218656.PubMed CentralView ArticlePubMed
- Stebbins S, Downs JS, et al: Using nonpharmaceutical interventions to prevent influenza transmission in elementary school children: parent and teacher perspectives. J Public Health Manag Pract. 2009, 15 (2): 112-117.View ArticlePubMed
- Stebbins S, Downs JS, et al: The effect of grade on compliance using nonpharmaceutical interventions to reduce influenza in an urban elementary school setting. J Public Health Manag Pract. 2011, 17 (1): 65-71.View ArticlePubMed
- Vukotich CJ, Coulborn RM, et al: Findings, gaps, and future direction for research in nonpharmaceutical interventions for pandemic influenza. Emerg Infect Dis. 2010, 16 (4): e2-10.3201/eid1604.090719.View ArticlePubMed
- Lee BY, Brown ST, et al: Simulating school closure strategies to mitigate an influenza epidemic. J Public Health Manag Pract. 2010, 16 (3): 252-261.PubMed CentralView ArticlePubMed
- Blachere FM, Lindsley WG, et al: Measurement of airborne influenza virus in a hospital emergency department. Clin Infect Dis. 2009, 48 (4): 438-440. 10.1086/596478.View ArticlePubMed
- Simmerman JX, Suntarattiwong P, et al: Influenza virus contamination of common household surfaces during the 2009 influenza A (H1N1) pandemic in Bangkok, Thailand: implications for contact transmission. Clin Infect Dis. 2010, 51 (9): 1053-1061. 10.1086/656581.View ArticlePubMed
- Karim YG, Ijaz MK, et al: Effect of relative humidity on the airborne survival of rhinovirus-14. Can J Microbiol. 1985, 31 (11): 1058-1061. 10.1139/m85-199.View ArticlePubMed
- The pre-publication history for this paper can be accessed here:http://www.biomedcentral.com/1471-2334/13/71/prepub
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.