REVIEW ARTICLE Humidity and respiratory virus transmission in tropical and temperate settings
←
→
Page content transcription
If your browser does not render page correctly, please read the page content below
Epidemiol. Infect. (2015), 143, 1110–1118. © Cambridge University Press 2014 doi:10.1017/S0950268814002702 REVIEW ARTICLE Humidity and respiratory virus transmission in tropical and temperate settings S. PAYNTER* School of Population Health, University of Queensland, Brisbane, Australia Received 3 August 2014; Final revision 12 August 2014; Accepted 18 August 2014; first published online 13 October 2014 SUMMARY Influenza and respiratory syncytial virus (RSV) are similarly structured viruses with similar environmental survival, but different routes of transmission. While RSV is transmitted predominantly by direct and indirect contact, influenza is also transmitted by aerosol. The cold, dry conditions of temperate winters appear to encourage the transmission of both viruses, by increasing influenza virus survival in aerosols, and increasing influenza and RSV survival on surfaces. In contrast, the hot, wet conditions of tropical rainy seasons appear to discourage aerosol transmission of influenza, by reducing the amount of influenza virus that is aerosolized, and probably also by reducing influenza survival in aerosol. The wet conditions of tropical rainy seasons may, however, encourage contact transmission of both viruses, by increasing the amount of virus that is deposited on surfaces, and by increasing virus survival in droplets on surfaces. This evidence suggests that the increased incidence of influenza and RSV in tropical rainy seasons may be due to increased contact transmission. This hypothesis is consistent with the observation that tropical rainy seasons appear to encourage the transmission of RSV more than influenza. More research is required to examine the environmental survival of respiratory viruses in the high humidity and temperature of the tropics. Key words: Influenza, respiratory syncytial virus. I N T RO D U C T I O N levels (including low vitamin D levels) [3–5]. In tropical A number of environmental factors have the potential settings seasonal influenza and RSV epidemics often to drive the transmission of influenza and respiratory occur during the rainy season; however, the mechanisms syncytial virus (RSV). Low absolute humidity appears driving this seasonal pattern are not clear [4, 6, 7]. to be the dominant driver of seasonal influenza and RSV and influenza are structurally similar viruses: RSV epidemics in temperate climates [1–3]. This effect both are lipid enveloped, single-stranded RNA viruses. For this reason, the survival of these viruses of low humidity in temperate winters is probably aug- mented by one or more of the following factors: low in the environment is likely to be similar. However, temperature, increased crowding, and low micronutrient the route of transmission appears to differ between RSV and influenza. Respiratory infections can be transmitted by three main routes [8]. Large respiratory droplets can travel short distances and may deposit di- * Address for correspondence: Dr S. Paynter, School of Population rectly on mucous membranes of the respiratory tract Health, Level 2, Public Health Building, University of Queensland, Herston Road, Herston, 4006, Australia. (direct contact). These same droplets will also deposit (Email: s.paynter@uq.edu.au) on surfaces where the virus may persist for long Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 18 Dec 2021 at 09:52:27, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0950268814002702
Humidity and respiratory virus transmission 1111 1 Virus recovery (relative to 20% RH) Harper Schaffer et al. Noti et al. 0.1 0.01 0 10 20 30 40 50 60 70 80 90 100 Relative humidity (%) Fig. 1. Influenza persistence in artificially produced aerosols. All studies measured influenza persistence after 1 h. All studies were performed at temperatures between 20 °C and 24 °C. Data from Harper [15], Schaffer et al. [18], and Noti et al. [23]. enough to be transferred to mucous membranes AND (persistence OR survival OR viability) AND (indirect contact). Small respiratory droplets can humidity. form droplet nuclei, which are small enough to be Search results were restricted to papers published inhaled, and can remain suspended in the air for in English. The Medline search was complemented hours (aerosol transmission). The relative importance by citation searches of the retrieved articles. Articles of each of these three routes varies between different citing the retrieved articles were also searched using infections, and for a particular infection the relative Google Scholar. importance of each route is also likely to vary accord- ing to the setting and ambient conditions. RSV appears to be predominantly spread by direct and R E S ULTS indirect contact through large respiratory droplets Humidity and aerosol transmission of influenza [9–11], thus virus survival on surfaces is likely to be Humidity can influence aerosol transmission via two the more important factor. Influenza appears to mechanisms: the proportion of respiratory droplets spread by all three routes [8, 12], thus viral survival becoming aerosolised and remaining in aerosol, and both in aerosol and on surfaces is important. the survival of the virus within these aerosols. This paper reviews the effect of humidity upon Respiratory droplets are generated in the high hu- influenza and RSV transmission – in particular, the midity of the respiratory tract. On entering an en- different effects of humidity on aerosol and contact vironment with low humidity, respiratory droplets transmission. This paper also reviews the different sea- reduce in size within seconds due to evaporation. sonal patterns of influenza and RSV in temperate, The resulting small droplets and aerosol nuclei settle subtropical and tropical climates. The results from slowly. At higher environmental humidity, respiratory these reviews are then combined to assess whether droplets evaporate more slowly, and hence are larger the differing effects of humidity on aerosol and con- and settle faster, and less aerosol nuclei are produced tact transmission may be a plausible explanation for [13, 14]. differences on influenza and RSV seasonality. The persistence of infectious influenza in artificially produced aerosols exposed to different levels of rela- tive humidity (RH) was examined in several studies between 1940 and 1980. Virus persistence was assessed METHODS by culture of air sampled from experimental settling A Medline search was performed using the following chambers. Some of these studies found a monotonic terms: (influenza OR ‘respiratory syncytial virus’) relationship, with decreasing influenza virus Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 18 Dec 2021 at 09:52:27, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0950268814002702
1112 S. Paynter 5 °C 20 °C 100 100 80 80 Percent infected 60 60 40 40 20 20 0 0 20% 35% 50% 65% 80% 20% 35% 50% 65% 80% Relative humidity Fig. 2. Percentage of guinea pigs infected via aerosol transmission (with 95% confidence intervals) at different levels of relative humidity and temperature. Data from Lowen et al. [24]. persistence in aerosol with increasing RH (tested up to artificially produced solutions. At both 5 °C and 20 ° 80%) [15–17]. Figure 1 shows the results from one of C, aerosol transmission of influenza between guinea these studies [15] which is representative of the results pigs was reduced with increasing RH, with the lowest from all three studies. Other studies found a U-shaped transmission occurring at 80% RH (Fig. 2) [24]. function of viral persistence with increasing humidity, Influenza transmission between mice showed a similar with maximum virus persistence at low RH, minimum relationship with humidity in an earlier study: in- persistence at 40–60% RH, and moderate persistence fluenza transmission reduced as RH increased from at higher RH (tested up to 80%) [18–20]. Figure 1 47% to 70% [25]. shows the results from one of these studies [18] Both influenza persistence in aerosol and trans- which is representative of the results from all of mission via aerosol are reduced by increasing tempera- these three studies. The reason for the differing pat- ture. The effects of temperature and humidity appear terns between 40% and 70% RH is not clear. It has to be additive, as shown in Figures 2 and 3. Aerosol been suggested that the low virus survival at transmission of influenza between guinea pigs was 50–60% RH in the U-shaped pattern may be due to completely blocked at 30 °C despite viral shedding the low protein content of the solutions used in these from infectious individuals [26]. studies, adversely impacting on virus survival at these levels of RH [21]. In all of these older studies, influenza persistence in air may have been affected Humidity and indirect transmission of influenza and by aerosol settling as well as virus survival [22]. RSV A more recent study measured both the total amount Virus deposition on surfaces of virus remaining suspended in aerosol (using quan- Humidity can influence indirect transmission via two titative PCR) as well as the amount that remained in- mechanisms: the mass of respiratory droplets accumu- fectious (using viral culture) enabling a more direct lating on surfaces, and the survival of the virus on sur- measure of viral survival [23]. Figure 1 shows the faces. While increased humidity reduces the number of results from this study [23]. All three patterns in droplet nuclei formed, the same mechanisms (reduced Figure 1 indicate the steepest change in virus survival droplet evaporation and faster droplet settling) mean in aerosol occurs between 30% and 50% RH (at a greater mass of respiratory droplets is deposited on approximately room temperature). surfaces [13, 14]. Animal transmission studies may provide the most pragmatic evidence examining the effect of humidity on influenza transmission, because animal trans- Influenza survival on surfaces mission studies examine the net effect of respiratory A study examining influenza survival over 2½ h in 0·1 droplet settling and virus survival, and droplet compo- μl droplets placed on glass slides at room temperature sition is more physiologically relevant than for found survival was lower at 84% RH compared to Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 18 Dec 2021 at 09:52:27, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0950268814002702
Humidity and respiratory virus transmission 1113 100 7 – 8 °C 20 – 24 °C 32 °C 80 Virus recovery (%) 60 40 20 0 0 10 20 30 40 50 60 70 80 90 100 Relative humidity, (%) Fig. 3. Influenza persistence in artificially produced aerosols after 1 h, showing the effects of humidity and temperature. Data from Harper [15]. 1 Virus recovery (relative to 100% RH) 0.1 0.01 0.001 0 10 20 30 40 50 60 70 80 90 100 Relative humidity, (%) Fig. 4. Influenza survival in 1 μl drops of mucus on a non-porous surface, after 2 h at room temperature. Data from Yang et al. [21]. 24% RH, but survival was greatest at 100% RH [27]. At in survival at 99% RH (Fig. 4) [21]. The authors 100% humidity, the influenza virus suspension placed hypothesize that at high RH the low evaporation on the slides was still wet after 2½ h, suggesting this from droplets leaves solute concentrations within drop- was why the virus remained viable. At 24% and 84% lets relatively unchanged, protecting the virus. humidity, the slides were dry, suggesting that when Increased temperature probably reduces influenza dry, influenza virus viability appears greater at lower survival on surfaces. The studies examining this directly humidity. A similar experiment assessed the survival found reduced influenza survival with increasing tem- of influenza in droplets of human mucus placed on cul- perature; however, these studies did not hold humidity ture plates, and found similar results. The experiments constant, so it is difficult to separate out the effects of were performed over 3 h at room temperature, and temperature and humidity [28, 29]. It is worth noting the droplet size used was 1 μl. The results show pro- that influenza survival in water is reduced at higher gressively reduced influenza survival with increasing temperatures, which suggests that increasing tempera- RH over the range from 27% to 84%, with an increase ture will reduce influenza survival in droplets Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 18 Dec 2021 at 09:52:27, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0950268814002702
1114 S. Paynter Table 1. Survival of respiratory syncytial virus (RSV) increasing humidity. Consistent with this explanation, on surfaces at room temperature according to relative only 1% of RSV was lost over the 72 h when stored in humidity (RH). Data from Kingston et al. [31] liquid culture medium, and in addition, the authors noted that RSV survival was increased with increased RSV survival over the period* droplet size. Similarly, in another study the survival of RH 0–5 h 5–24 h 24–72 h RSV on countertops was reduced if the virus was in droplets that were dried quickly [32]. These results 32% 1 1 1 are consistent with the studies examining influenza 52% 10 0·1 0·4 survival on surfaces, suggesting that while the virus re- 77% 18 0·3 0·2 mains ‘wet’ in droplets, high humidity prolongs its * Relative to survival at 32% RH. survival, by reducing evaporation. independently of humidity [28]. No studies have exam- Humidity and the seasonality of influenza and RSV ined the effect of high temperature combined with high The reviewed studies suggest that aerosol transmission humidity on influenza survival on surfaces. of influenza decreases with increasing RH, due to a progressive reduction in the amount of aerosol nuclei Animal transmission studies produced, and a reduction in virus survival in aerosol. Contact transmission of influenza between guinea pigs Aerosol transmission of influenza also appears to be appeared unaffected by increasing humidity and tem- greatly reduced at temperatures above 30 °C. These perature. Four out of four susceptible guinea pigs were results indicate that aerosol transmission would be infected at 20% RH and 20 °C, while three out of four low during the high temperature, high humidity con- were infected at 80% RH and 30 °C [26]. Because in- ditions of tropical rainy seasons. High humidity fectious and susceptible animals were kept in the appears to promote increased survival of influenza same cages in these experiments, it is not possible to and RSV while they are in droplets on surfaces, by tell whether transmission was direct or indirect. slowing the evaporation of the droplets (however, Much of the transmission in this study may have once the droplets are dry, higher humidity appears been due to direct contact rather than indirect contact. to reduce survival). In addition, the deposition of res- A later study examining indirect contact transmission piratory droplets is increased at higher humidity. (by removing infectious animals from cages before Transfer of virus from surfaces to hands also appears replacing them with susceptible animals) found increased at higher humidity (although this has only lower transmission rates: only three out of 16 exposed been tested up to 65% RH) [33]. These results suggest guinea pigs were infected [30]. These latter experi- that the high humidity found in tropical rainy seasons ments were performed at constant humidity. could favour indirect transmission, however the net effect of high humidity and high temperature in on indirect transmission in these settings needs to be RSV survival on surfaces resolved. One study examined the effect of humidity on RSV One notable observation of RSV and influenza epi- survival in 1 μl droplets of tissue culture medium on demiology is the differing seasonal patterns in tropical polythene at room temperature [31]. Over the first 5 and temperate climates, which have been reviewed in h, RSV survival was highest at the highest humidity, detail previously [4, 7, 34, 35]. The general trend of while over the next 67 h, RSV survival was highest the change in seasonality with latitude is illustrated at the lowest humidity (Table 1). The explanation of in Table 2. In the temperate settings (Vancouver, these findings may lie in the droplet drying time in Melbourne, Santiago) both RSV and influenza inci- this study. Droplets exposed to 77% RH were still dence consistently peak in winter. In the middle lati- wet at 18 h (no data were given for drying times at tudes of the subtropical climates (Brisbane, Florida, 32% or 52% RH). The relatively high survival at São Paulo) the different seasonality of RSV and higher humidity over the first 5 h was probably due influenza is evident: while influenza still occurs in win- to the fact that the droplets remained wet in these con- ter, RSV occurs during the rainy season, several ditions. The survival over the final 48 h (when all dro- months before the winter influenza peak. In the trop- plets were dry) was progressively reduced with ical settings, RSV incidence is usually maximal during Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 18 Dec 2021 at 09:52:27, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0950268814002702
Humidity and respiratory virus transmission 1115 Table 2. Seasonal patterns of respiratory syncytial virus (RSV) and influenza in temperate, subtropical and tropical settings Setting Latitude RSV seasonality Influenza seasonality Vancouver, Canada [34] 49° N Winter (Feb.) Winter (Feb.) Melbourne, Australia [45, 46] 38° S Winter (July) Winter (July) Santiago, Chile [34] 33° S Winter (July) Winter (June) Brisbane, Australia [47, 48] 27° S Late rainy season (Apr.) Winter (Aug.) Florida, USA [49, 50] 26° N Late rainy season (Oct.) Winter (Jan.) São Paulo, Brazil [34, 51] 24° S Late rainy season (Apr.) Winter (June) Bangladesh [7, 43, 52, 53] 23° N Rainy season main peak (Sep.) Rainy season main peak (July-Sep.) ±Winter peak (Feb.) ± Spring peak (Apr.) Hong Kong, China [7, 54–56] 22° N Rainy season (July) Winter main peak (Feb.) ± Rainy season peak (July) Pune, India [57, 58] 19° N Rainy season (Aug.) Rainy season main peak (Aug.) ± Late winter peak (Mar.) Thailand [52, 59, 60] 14° N Rainy season (Sep.) Rainy season main peak (Aug.) ± Winter peak (Feb.) Darwin, Australia [46, 61] 12° S Rainy season (Feb.) Winter main peak (Aug.) ± Rainy season peak (Mar.) Java/Lombok, Indonesia [41, 62, 63] 7° S Rainy season (Mar.) Rainy season (Jan.) Fortaleza, Brazil [34, 51, 64, 65] 4° S Rainy season (May) Rainy season (Apr.) the rainy season, while the influenza peak is some- influencing RSV and influenza transmission as well times associated with the rainy season, and sometimes as (or more than) humidity. These factors may ex- during winter (and sometimes both). plain a number of exceptions to the overall trend de- The overall trend of these seasonal patterns could be scribed in Table 2. For example, malnutrition is a explained by variations in humidity. In the low hu- known risk factor for respiratory infection [36–38]. midity and low temperature conditions of temperate In settings with substantial seasonal malnutrition, it winters, both RSV and influenza will survive better is plausible that malnutrition may be a stronger dri- in the environment, whether in aerosols or on surfaces. ver of seasonality than climate [39]. This may explain In the subtropical settings, the high humidity during the seasonality of RSV in settings such as Kenya and the rainy season may improve the transmission of Nigeria, where RSV epidemics occur outside the RSV, because RSV is spread predominantly by direct rainy season [40, 41]. Singapore has high rainfall all and indirect contact. Influenza, on the other hand, is year round, with little variation in humidity (the av- also spread by aerosol, and this may explain why erage monthly RH varies between 77% and 82%) influenza does not have a clear advantage during the [42]. The timing of influenza epidemics is irregular subtropical rainy season, maintaining its peak inci- in Singapore: in some years influenza circulates for dence during the cool winters. In the tropics, the most of the year, while in others one or two distinct more humid rainy season (combined with warmer win- epidemics occur, at different times from year to year ters) may tip the balance, making the rainy season [43]. This irregular pattern could be due to the lack of more favourable than the winter for influenza trans- a dominant environmental driver, consistent with the mission as well as RSV transmission. small variation in humidity. This hypothesis offers a parsimonious explanation Although there is enough existing data to hypothe- for the overall trend of the seasonal patterns of size that high humidity may be driving influenza and RSV and influenza, consistent with the observation RSV transmission in tropical settings via indirect con- that the rainy season appears to encourage RSV tact transmission, more research is required to fill transmission more than influenza transmission. in the gaps in our knowledge of how climate affects However, a number of other environmental factors the transmission of these viruses. No studies have are known to increase the risk of respiratory infec- examined influenza transmission above 80% RH. tion, and seasonal variations in these may be Few studies have examined transmission at high Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 18 Dec 2021 at 09:52:27, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0950268814002702
1116 S. Paynter temperatures, and very few studies have provided data 2. Shaman J, et al. Absolute humidity and the seasonal to assess indirect contact transmission. In particular, onset of influenza in the continental United States. PLoS Biology 2010; 8: e1000316. the interaction between high temperature and high hu- 3. Yusuf S, et al. The relationship of meteorological condi- midity on indirect contact transmission needs further tions to the epidemic activity of respiratory syncytial exploration. More can be learned by contrasting the virus. Epidemiology and Infection 2007; 135: 1077–1090. differing epidemiology of influenza and RSV, and 4. Tamerius J, et al. Global influenza seasonality: reconcil- transmission models of these viruses incorporating en- ing patterns across temperate and tropical regions. vironmental effects will be required to explain the dif- Environmental Health Perspectives 2011; 119: 439. 5. Lofgren E, et al. Influenza seasonality: underlying ferent seasonal patterns of these two viruses. causes and modeling theories. Journal of Virology 2007; 81: 5429–5436. 6. Tamerius JD, et al. Environmental predictors of seas- CO N CLU S IO N S onal influenza epidemics across temperate and tropical For infections with such a high burden of disease, very climates. PLoS Pathogens 2013; 9: e1003194. little is known about how tropical climates affect the 7. Weber MW, Mulholland EK, Greenwood BM. Respiratory syncytial virus infection in tropical and developing coun- transmission of influenza and RSV. Predicting the tries. Tropical Medicine & International Health 1998; 3: timing of peaks in RSV and influenza activity can im- 268–280. prove disease control. Considerable effort is put into 8. Killingley B, Nguyen Van Tam J. Routes of influenza predicting and detecting increases in influenza and transmission. Influenza and Other Respiratory Viruses RSV activity in temperate climates, where the onset 2013; 7: 42–51. of seasonal epidemics generally varies by a few 9. Hall CB, Douglas RG. Jr. Modes of transmission of res- piratory syncytial virus. Journal of pediatrics 1981; 99: weeks from year to year. In contrast, in tropical cli- 100–103. mates influenza epidemics can occur in completely dif- 10. Gala CL, et al. The use of eye-nose goggles to control ferent seasons from year to year, and methods to nosocomial respiratory syncytial virus infection. predict oncoming epidemics will be particularly valu- Journal of the American Medical Association 1986; able. Improved knowledge of the drivers of transmission 256: 2706–2708. 11. Leclair JM, et al. Prevention of nosocomial respiratory in tropical settings will also enable improved prediction syncytial virus infections through compliance with glove of the consequences of environmental change. Recent and gown isolation precautions. New England Journal of projections from the Intergovernmental Panel on Medicine 1987; 317: 329–334. Climate Change indicate monsoon systems will inten- 12. Tellier R. Review of aerosol transmission of influenza sify, last longer and cover a larger geographical area A virus. Emerging Infectious Diseases 2006; 12: 1657– than currently [44]. If high humidity is driving contact 1662. 13. Xie X, et al. How far droplets can move in indoor envir- transmission of influenza and RSV, this will clearly onments–revisiting the Wells evaporation–falling curve. have implications for future disease burdens. Finally, Indoor Air 2007; 17: 211–225. improved knowledge of the effects of humidity and tem- 14. Yang W, Marr LC. Dynamics of airborne influenza A perature on influenza and RSV transmission can be viruses indoors and dependence on humidity. PLoS used to modify indoor environments to improve infec- ONE 2011; 6: e21481. 15. Harper G. Airborne micro-organisms: survival tests tion control. Our current state of ignorance concerning with four viruses. Journal of Hygiene 1961; 59: 479– the environmental drivers of influenza and RSV trans- 486. mission in tropical settings, and the role of humidity 16. Hemmes J, Winkler K, Kool S. Virus survival as a sea- in particular, needs addressing. sonal factor in influenza and poliomyelitis. Nature 1960; 188: 430–431. 17. Loosli C, et al. Experimental air-borne influenza D E C L A R ATI O N O F I N T E R E S T infection. I. Influence of humidity on survival of virus in air. Proceedings of the Society for Experimental None. Biology and Medicine (New York, NY). Royal Society of Medicine, 1943, pp. 205–206. 18. Schaffer F, Soergel M, Straube D. Survival of airborne R E F E RE NC E S influenza virus: effects of propagating host, relative hu- 1. Shaman J, Kohn M. Absolute humidity modulates midity, and composition of spray fluids. Archives of influenza survival, transmission, and seasonality. Virology 1976; 51: 263–273. Proceedings of the National Academy of Sciences USA 19. Shechmeister I. Studies on the experimental epidemi- 2009; 106: 3243–3248. ology of respiratory infections III. Certain aspects Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 18 Dec 2021 at 09:52:27, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0950268814002702
Humidity and respiratory virus transmission 1117 of the behavior of type A influenza virus as an air- 37. Okiro EA, et al. Factors associated with increased risk of borne cloud. Journal of Infectious Diseases 1950; 87: progression to respiratory syncytial virus-associated pneu- 128–132. monia in young Kenyan children. Tropical Medicine & 20. Lester W. The influence of relative humidity on the International Health 2008; 13: 914–926. infectivity of air-borne influenza A virus (PR8 38. Paynter S, et al. Malnutrition: a risk factor for severe Strain). Journal of Experimental Medicine 1948; 88: respiratory syncytial virus infection and hospitaliza- 361–368. tion. Pediatric Infectious Disease Journal 2014; 33: 21. Yang W, Elankumaran S, Marr LC. Relationship be- 267–271. tween humidity and influenza A viability in droplets 39. Paynter S, et al. The importance of the local environ- and implications for influenza’s seasonality. PLoS ment in the transmission of respiratory syncytial virus. ONE 2012; 7: e46789. Science of the Total Environment 2014; 493: 521–525. 22. Hinds WC. Aerosol Technology: Properties, Behavior, 40. Nokes DJ, et al. Respiratory syncytial virus infection and Measurement of Airborne Particles, 2nd edn. John and disease in infants and young children observed Wiley & Sons, 1999. from birth in Kilifi District, Kenya. Clinical Infectious 23. Noti JD, et al. High humidity leads to loss of infectious Diseases 2008; 46: 50–57. influenza virus from simulated coughs. PLoS ONE 41. Robertson SE, et al. Respiratory syncytial virus infection: 2013; 8: e57485. denominator-based studies in Indonesia, Mozambique, 24. Lowen AC, et al. Influenza virus transmission is depen- Nigeria and South Africa. Bulletin of the World Health dent on relative humidity and temperature. PLoS Organization 2004; 82: 914–922. Pathogens 2007; 3: e151. 42. BBC. BBC Weather. 2014. 25. Schulman JL, Kilbourne ED. Airborne transmission of 43. World Health Organisation. FluNet. 2014. influenza virus infection in mice. Nature 1962; 195: 44. Intergovernmental Panel on Climate Change. Climate 1129–1130. change 2013: the physical science basis. Summary for 26. Lowen AC, et al. High temperature (30 °C) blocks aero- policymakers, 2013. sol but not contact transmission of influenza virus. 45. Lazzaro T, Hogg G, Barnett P. Respiratory syncytial Journal of Virology 2008; 82: 5650–5652. virus infection and recurrent wheeze/asthma in children 27. Buckland F, Tyrrell D. Loss of infectivity on drying vari- under five years: an epidemiological survey. Journal of ous viruses. Nature 1962; 195: 1063. Paediatrics and Child Health 2007; 43: 29–33. 28. Dublineau A, et al. Persistence of the 2009 pandemic 46. Department of Health. Australian Influenza Surveillance influenza A (H1N1) virus in water and on non-porous Report. Australian Government, 2013. surface. PLoS ONE 2011; 6: e28043. 47. Chappell K, et al. Respiratory syncytial virus infection is 29. Edward D. Resistance of influenza virus to drying associated with increased bacterial load in the upper res- and its demonstration on dust. Lancet 1941; 238: piratory tract in young children. Journal of Medical 664–666. Microbiology & Diagnosis 2013; 1: 2161–0703. 30. Mubareka S, et al. Transmission of influenza virus via 48. Queensland Health. Statewide weekly influenza surveil- aerosols and fomites in the guinea pig model. Journal lance report. Queensland Health, 2013. of Infectious Diseases 2009; 199: 858–865. 49. Florida Department of Health. Respiratory syncytial 31. Kingston D. Towards the isolation of respiratory syncy- virus. Florida Department of Health, 2013. tial virus from the environment. Journal of Applied 50. Florida Department of Health. Florida flu review. Microbiology 1968; 31: 498–510. Florida Department of Health, 2014. 32. Hall CB, Douglas RG, Geiman JM. Possible trans- 51. de Mello Freitas FT. Sentinel surveillance of influenza mission by fomites of respiratory syncytial virus. and other respiratory viruses, Brazil, 2000–2010. Journal of Infectious Diseases 1980; 141: 98–102. Brazilian Journal of Infectious Diseases 2013; 17: 62–68. 33. Lopez GU, et al. Transfer efficiency of bacteria and 52. Haynes AK, et al. Respiratory syncytial virus circulation viruses from porous and nonporous fomites to fingers in seven countries with global disease detection regional under different relative humidity conditions. Applied centers. Journal of Infectious Diseases 2013; 208 (Suppl. and Environmental Microbiology 2013; 79: 5728–5734. 3): S246–S254. 34. Bloom-Feshbach K, et al. Latitudinal variations in seaso- 53. Brooks WA, et al. Influenza is a major contributor to nal activity of influenza and respiratory syncytial virus childhood pneumonia in a tropical developing country. (RSV): a global comparative review. PLoS ONE 2013; Pediatric Infectious Disease Journal 2010; 29: 216–221. 8: e54445. 54. Chan P, et al. Epidemiology of respiratory syncytial 35. Stensballe L, Devasundaram J, Simoes E. Respiratory virus infection among paediatric patients in Hong syncytial virus epidemics: the ups and downs of a seaso- Kong: seasonality and disease impact. Epidemiology nal virus. Pediatric Infectious Disease Journal 2003; 22: and Infection 1999; 123: 257–262. S21–S32. 55. Yang L, et al. Synchrony of clinical and laboratory sur- 36. Caulfield LE, et al. Undernutrition as an underlying veillance for influenza in Hong Kong. PLoS ONE 2008; cause of child deaths associated with diarrhea, pneu- 3: e1399. monia, malaria, and measles. American Journal of 56. Centre for Health Protection. Flu express. Hong Kong Clinical Nutrition 2004; 80: 193–198. Department of Health, 2013. Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 18 Dec 2021 at 09:52:27, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0950268814002702
1118 S. Paynter 57. Yeolekar LR, et al. Respiratory viruses in acute respira- 62. Omer SB, et al. Climatic, temporal, and geographic tory tract infections in Western India. Indian Journal of characteristics of respiratory syncytial virus disease in Pediatrics 2008; 75: 341–345. a tropical island population. Epidemiology and Infection 58. Rao B, et al. Influenza surveillance in Pune, India, 2003. 2008; 136: 1319–1327. Southeast Asian Journal of Tropical Medicine and Public 63. Kosasih H, et al. Surveillance of influenza in Indonesia, Health 2005; 36: 906–909. 2003–2007. Influenza and Other Respiratory Viruses 59. Simmerman JM, et al. Incidence, seasonality and mor- 2013; 7: 312–320. tality associated with influenza pneumonia in Thailand: 64. Moura FE, et al. Respiratory syncytial virus infections 2005–2008. PLoS ONE 2009; 4: e7776. in northeastern Brazil: seasonal trends and general 60. Simmerman JM, et al. Influenza in Thailand: a case study aspects. American Journal of Tropical Medicine and for middle income countries. Vaccine 2004; 23: 182–187. Hygiene 2006; 74: 165–167. 61. O’Grady K-AF, Torzillo PJ, Chang AB. Hospitalisation 65. Moura FE, Perdigão AC, Siqueira MM. Seasonality of of Indigenous children in the Northern Territory for influenza in the tropics: a distinct pattern in northeast- lower respiratory illness in the first year of life. ern Brazil. American Journal of Tropical Medicine and Medical Journal of Australia 2010; 192: 586. Hygiene 2009; 81: 180. Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 18 Dec 2021 at 09:52:27, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0950268814002702
You can also read