Our knowledge of how epidemics of respiratory syncytial virus (RSV) are initiated and sustained is incomplete. In geographic regions with temperate climates, epidemics of RSV have been reported to peak during winter in both the Northern and Southern hemispheres.1,2 This suggests that cold weather may increase RSV activity. In contrast, RSV activity has been described as being continuous throughout the year in warm equatorial areas,3,4 suggesting that temperature cannot be the only factor influencing activity of the virus.
We undertook this study to gain a better understanding of the duration of RSV activity in geographic areas that differ widely in climate, and to determine which meteorological conditions might affect the activity of RSV in local communities.
Collection of Data on Numbers of RSV Cases.
Data on local RSV activity were obtained with the valued cooperation of scientists at each site listed in Table 1. Data were obtained from routine year-round viral surveillance programs at most sites, as a result of the interest of individual investigators in Delhi, India and, in some seasons, from Bethel, AK. Commercial antigen detection methods were used at all sites to identify RSV cases. Individuals at the 9 sites identified cases of RSV infection using 4 different kits, each with a sensitivity and specificity of more than 90%. More importantly, cases of RSV infection initially identified by antigen detection assays were confirmed by culture throughout all years of the study in Miami, FL; Houston, TX; and Winnipeg, Manitoba, Canada, and in some study years in Buffalo, NY; Bethel; and Delhi.
Meteorological Data for Study Sites.
Data concerning mean temperatures, dew point, relative humidity, precipitation, and barometric pressure were obtained from the 9 cities listed in Table 1. These sites were chosen to reflect a variety of climatic conditions: warm and wet (Miami; Mexico City, Mexico; Delhi; and Houston), warm and dry (Tucson, AZ), cold and wet (Buffalo), or cold and dry (Winnipeg and Bethel). Santiago, Chile was chosen as a site from the Southern hemisphere with intermediate weather conditions. Meteorological data were obtained by primary investigators at each site from local weather services or from the National Climatic Data Center (www.ncdc.noaa.gov) or WeatherNetwork.com (www.theweathernetwork.com). Data on ultraviolet B (UVB) radiation were obtained from the Colorado State University Web site (uvb.nrel.colostate.edu); however, data on UVB radiance were only available from 4 of our study sites during the time that this study was performed. Weather data for Delhi were obtained from the following Web sites: WorldClimate (www.worldclimate.com), Weatherbase (www.weatherbase.com), and the National Oceanic and Atmospheric Administration Central Region Headquarters (www.crh.noaa.gov). Further details are available in a previous publication.5
Meteorological Features of Selected Cities.
A summary of meteorological features of the cities from which data were available is presented in Table 1. Weekly averages of the various factors are displayed, except as noted. The meteorological data suggest a reasonable range of temperature, humidity, and precipitation among these cities.
RSV Activity Analyzed by Latitude.
Weekly totals of RSV activity for the 6 North American sites are illustrated in Figure 1. Over the 4-year period of observation, in Miami (25.8°N), the average peak of RSV activity occurred from weeks 38 to 42 (late September into October; Fig. 1, lower panel). A smaller secondary peak occurred during January and February. RSV activity was continuous throughout all years studied. At least 5 cases of RSV were identified (and confirmed by culture) during each week of the survey.
In Houston (29.6°N), the peak of RSV activity occurred from mid-October into early January (Fig. 1). RSV was detected (and confirmed by culture) at a rate of 1–4 cases per week during May through August of the first year studied, but was not detected from May through August in the second and third years of surveillance. Thus, the autumn peak observed in Miami was diminished or delayed into the winter peak, and RSV activity was decreased during the summer months.
In Tucson (32.1°N), the peak of RSV activity occurred from January to March (Fig. 1). For each year studied, no cases were identified from late April into late November of most years. Thus, there was a further reduction in autumn activity of RSV and no summer activity, and epidemics were focused in the winter months.
In Buffalo (42.6°N), the peak of RSV activity occurred from late December through late April (Fig. 1). In May, early June, and late November, 0–5 cases per week were noted. RSV was absent from the community from late June through early November. Thus, in this cooler climate, winter RSV peaks were of broader duration than in warmer climates, but RSV also was absent during summer and early autumn.
Surprisingly, in Winnipeg (49.5°N) and in Bethel (60.5°N), the pattern of RSV activity was continuous (Fig. 1). In Winnipeg, peaks of RSV activity were very broad, extending from December through May. In addition, in 1 of the 2 summers studied, 1–6 cases of RSV (confirmed by culture) were identified during each week. In Bethel, considerable RSV activity was present from October to May, and cases (confirmed by culture in 3 of the surveillance years) were frequently identified in summer months.
To attempt to substantiate the relationship of RSV activity to latitude, information also was obtained from Mexico City (19.2°N), Delhi, (28.4°N, or approximately the same distance from the equator as Houston), and Santiago, (33.2°S, or approximately the same distance from the equator as Tucson). In Mexico City, cases of RSV infection were detected in each month of the year (Fig. 2, lower panel), with the greatest number of cases identified in September and October. This pattern of activity is somewhat similar to that observed in Miami. RSV activity in Delhi (Fig. 2, middle panel) was present throughout 10 months of the year and was absent only in the summer months of July and August, with the greatest number of cases in late autumn and winter. Thus, the pattern could be interpreted as being similar to that of Houston.
RSV activity in Santiago, Chile, is illustrated in Figure 2 (upper panel). A distinct peak of activity was observed in the winter months of July and August. In 3 of the 4 years studied, RSV activity was undetectable from the community during the summer months of December through April. Three or fewer cases of RSV were identified throughout the entire months of April and December in the fourth year studied. This pattern might be considered similar to that occurring in Tucson, given the reversal of seasons in these 2 cities.
Meteorological Features and RSV Activity
Data for All Sites Providing Weekly Results.
The association of RSV activity with mean temperature is illustrated in Figure 3 (upper panel). Only those data obtained on a weekly basis were included. A bimodal relationship of RSV activity with temperature was observed. The number of RSV cases increased when the mean temperature was above 24–30°C, and again when the temperature was in the range of 2–6°C. Perhaps because of this bimodal relationship, the relationship of temperature to RSV totals at these sites was not strong (linear R = 0.135, P = 0.036; curvilinear R = 0.218, P = 0.021).
The association of RSV activity and relative humidity is illustrated in Figure 3 (lower panel). RSV activity was increased when the mean relative humidity was between 45% and 65%. The linear correlation was weak (R = 0.24, P = 0.011). UVB radiance was inversely related to the number of RSV cases (R = −0.382, P < 0.001). No other meteorological factor bore a significant relationship to RSV totals when the sites were analyzed together.
Data for Individual Study Sites.
The association of various meteorological features with RSV activity in different locations (based on weekly or monthly data) is summarized in Table 2. The strongest association observed was that of mean temperature and RSV activity, most of which have an absolute degree of correlation of ≥0.39 (P < 0.001). This suggests that RSV activity is dependent on temperature. However, the relationship between temperature and RSV activity is direct in Miami (and, to an extent, in Mexico City) and inverse at all other sites.
Dew point (reflecting absolute humidity) also was associated with RSV activity, and most correlations were highly statistically significant (P < 0.001, Table 2). This suggests an effect of absolute humidity on RSV activity in the community. As for temperature, the relationship of dew point to RSV activity was direct in Miami and Mexico City, and inverse at all other sites.
For Buffalo, Winnipeg, and Miami, a statistically significant negative correlation (each P ≤ 0.001) was verified between RSV cases and UVB radiance, indicating that the frequency of RSV cases rose as UVB levels fell. Conversely, the UVB and RSV data for Alaska showed no statistically significant relationship.
Relative Humidity, Precipitation, and Barometric Pressure.
The correlation of relative humidity with RSV activity attained statistical significance in Miami, Mexico City, and Santiago, where positive correlations were observed (Table 3). At other sites, statistically insignificant correlations were observed. Barometric pressure was not significantly associated with RSV activity at any site; however, a significant correlation was observed only in Miami between precipitation and RSV activity.
Stepwise Regression Analysis.
Results of stepwise regression analysis of meteorological factors with RSV totals for individual sites are presented in Table 3. In this analysis, the major factor correlated with RSV activity was determined at each site, and the proportion of RSV activity attributable to that factor was calculated. For example, in Miami, mean temperature was the meteorological factor most closely associated with the number of RSV cases identified (R = 0.458; all probability values for correlations shown in Table 3 are <0.001). In the third column, it can be seen that 21% of RSV activity could be related to temperature changes. When UVB radiance is considered with RSV cases (temperature held constant), 13% of RSV activity could be related to UVB radiance. Table 3 illustrates a similar analysis for all study sites.
In this analysis, temperature was the meteorological condition most strongly associated with RSV activity at 4 sites overall, including 3 of the 5 sites from which weekly RSV data were available. Again, the relationship of temperature to RSV cases was positive at the Miami site but inverse at other sites. Temperature alone accounted for between 15% and 35% of RSV activity at different sites, with additional increases of up to 4% when other factors were added. The effects of UVB radiance were statistically significant at 3 sites. UVB effects were somewhat less strong than those of temperature or dew point, and accounted for 0–13% of RSV activity. Either relative or absolute humidity was the principal correlate of RSV cases at 4 sites (all inverse correlations), accounting for 125–41% of RSV activity. Barometric pressure was the principal correlate of RSV totals at the Delhi site and a secondary correlate at 2 others, being related to as much as 22% of total RSV activity.
Because temperature and UVB radiance were interrelated, we repeated the analysis of the contribution of UVB radiance to RSV cases with temperature not held constant (data not shown). According to this type of analysis, UVB radiance accounted for 17% of RSV activity in Miami, 8.6% in Buffalo, 8.4% in Winnipeg, and 0.9% in Bethel.
Data generated from the present study reveal a complex interaction of latitude, temperature, humidity, and UVB radiance with RSV activity. In the present study, when data from all sites providing weekly results were included for analysis, a bimodal relationship of temperature and RSV activity was observed, with increased activity at mean daily temperatures above 24°C and below 6°C. RSV activity also was greatest when relative humidity was near 40%. The relationship of RSV activity to absolute humidity (dew point) was positive in Mexico City and Miami but negative at other sites. At 3 of 4 sites where data were available, RSV activity was inversely related to UVB radiance. RSV activity was related positively to relative humidity at some sites. Barometric pressure may contribute somewhat to RSV activity in certain locations, whereas sunlight and weekly precipitation are not as important.
RSV is believed to be transmitted by large particle aerosols and by direct contact with RSV in solutions of human secretions.6 Rechsteiner and Winkler7 tested the stability of aerosols (average droplet size = 4.9 μm) of RSV in a cylinder. Within 1 minute of being aerosolized, maximal stability of RSV was obtained at 80–90% humidity. Maximal inactivation of RSV (approximately 1 log10) in the first minute occurred at low (20–30%) humidity. When aerosols were maintained for periods of 1–61 minutes, RSV became most stable at 40% humidity.
Hambling8 evaluated the stability of RSV in solutions at varying temperatures. At a temperature of 37°C, 99% inactivation of RSV occurred over 3 days. At a temperature of 4°C, the same degree of inactivation required more than 6 days. It would be expected that a slight decrease in environmental temperatures below room temperature would markedly prolong the stability of RSV in secretions on fomites if reasonable humidity were maintained.
Although numerous factors other than meteorological conditions surely contribute to the spread of RSV in the community, we suggest that, in tropical and subtropical areas, high humidity and stable high temperatures enable RSV to be sustained well enough in large-particle aerosols to permit year-round transmission of the virus. Because maximal rainfall and temperature occur in summer months in theses areas, the association of RSV with temperature and humidity would be positive (Table 2). However, the appearance of drier weather might be expected to inactivate RSV more rapidly and interfere with aerosol transmission of the virus.
In more temperate climates with more variable temperatures and rainfall, summertime RSV would only be sustainable in areas with very high rainfall and warm temperatures (for example, Mexico City, and possibly, Houston). In more arid regions of the temperate zones (Tucson and Santiago), aerosol transmission of RSV would be terminated by the lower humidity. The appearance of winter epidemics of RSV in these areas might be influenced by the lower winter temperatures that enhance stability of RSV in solutions of human secretions in the environment. Because rainfall in most of these areas is maximal in summer, RSV activity would correlate negatively with absolute humidity (Table 2). The relationship to relative humidity would be less predictable, but a certain degree of relative humidity would be necessary to prevent drying.
For colder climates (Buffalo, Winnipeg, and Bethel), we speculate that the prolonged cold temperatures are again more important than the effects of humidity. If temperatures remain below a threshold that enhances RSV stability for most of the year, RSV activity would be more persistent (and an association with temperature might be less apparent). Thus, RSV activity in colder regions would be expected to be greater in the months of both autumn and into spring, when ambient temperatures are similar to those in January at lower latitudes. Gradually warmer temperatures should slowly reduce the degree of spread of RSV during the summer. If the degree of precipitation also were greater during the summer, an inverse correlation of RSV activity with humidity would be expected (Table 2).
Finally, RSV activity was inversely related to UVB radiance. The effect of UVB on RSV cases was greater when total UVB radiance was highest (Miami). The relationship of UVB radiance to RSV cases was less strong where UVB radiance is lower (Buffalo and Winnipeg), but still statistically significant. No effect of UVB radiance on RSV cases was observed in Bethel, where total UVB radiance is remarkably low. Therefore, our results suggest that substantial UVB exposure may limit RSV activity during summer, but the lesser degrees of UVB radiance in winter or in overcast areas may permit greater spread of RSV. UVB radiance could interfere with the spread of RSV by inactivating the virus in nature. UVB also could indirectly affect RSV activity by stimulating vitamin D metabolism in the host. It has been reported that children with vitamin-D deficient rickets have greater numbers of viral respiratory infections.9 At least one study has suggested that vitamin D supplementation of these children reduces their frequency of respiratory illnesses.10
It has been stated that extreme cold or very high rainfall might drive populations indoors, where RSV would spread more readily.11 Indoor spread would be independent of external temperature and humidity and would, therefore, reduce the observed statistical association with these climatic factors. In addition, human susceptibility to viral infection might be altered by weather conditions.6 These factors undoubtedly account for a great deal of RSV activity, probably more than climate, because only 15–40% of RSV totals could be attributed statistically to meteorological factors. For instance, reopening of schools may contribute to late summer and autumn increases in RSV activity in hot, wet climates where RSV is active during summer. Conversely, the data in the present study were derived from cities in temperate climates. The mild weather extremes occurring in these cities do not cause substantial changes in human behavior, yet the effects of temperature and humidity were still statistically significant. Thus, the effects of climate appear to add to the effects of alterations in human behavior. Alternatively, it is possible that changes in climate might not influence transmission of RSV in nature, but rather activate RSV replication from a latent state in humans.
In summary, community activity of RSV is substantial in tropical areas when both ambient temperatures and humidity are very high (perhaps as a result of prolonged stability of RSV in aerosols), and in cooler climates if reasonable humidity is maintained (possibly as a result of better stability in secretions in the environment). Reduced UVB radiation can be expected to enhance the survival of RSV in nature.
The authors gratefully acknowledge the assistance of Shabana Yusuf, MD; Giovanni Piedimonte, MD; Alexander Auais, MD; Gail Demmler, MD; Subramaniam Krishnan, PhD; Paul Van Caeseele, MD FRCPC; Rosalyn Singleton, MD; Shobha Broor, MD; Shama Parveen, MSc; Luis Avendano, MD; Jorge Parra, MD; Susana Chavez-Bueno, MD; Teresa Murguía de Sierra, MD; Eric A.F. Simoes, MD, MBBS; Wayne Sullender, MD; Barbara Law, MD; Jewel Greer; Anna Gongora; Marianne B. Fife, MT, who reported RSV cases. Steven Shaha, PhD DBA, performed statistical analyses.