Research Article: Weather Regulates Location, Timing, and Intensity of Dengue Virus Transmission between Humans and Mosquitoes

Date Published: July 29, 2015

Publisher: Public Library of Science

Author(s): Karen M. Campbell, Kristin Haldeman, Chris Lehnig, Cesar V. Munayco, Eric S. Halsey, V. Alberto Laguna-Torres, Martín Yagui, Amy C. Morrison, Chii-Dean Lin, Thomas W. Scott, Edwin Michael. http://doi.org/10.1371/journal.pntd.0003957

Abstract: BackgroundDengue is one of the most aggressively expanding mosquito-transmitted viruses. The human burden approaches 400 million infections annually. Complex transmission dynamics pose challenges for predicting location, timing, and magnitude of risk; thus, models are needed to guide prevention strategies and policy development locally and globally. Weather regulates transmission-potential via its effects on vector dynamics. An important gap in understanding risk and roadblock in model development is an empirical perspective clarifying how weather impacts transmission in diverse ecological settings. We sought to determine if location, timing, and potential-intensity of transmission are systematically defined by weather.Methodology/Principal FindingsWe developed a high-resolution empirical profile of the local weather-disease connection across Peru, a country with considerable ecological diversity. Applying 2-dimensional weather-space that pairs temperature versus humidity, we mapped local transmission-potential in weather-space by week during 1994-2012. A binary classification-tree was developed to test whether weather data could classify 1828 Peruvian districts as positive/negative for transmission and into ranks of transmission-potential with respect to observed disease. We show that transmission-potential is regulated by temperature-humidity coupling, enabling epidemics in a limited area of weather-space. Duration within a specific temperature range defines transmission-potential that is amplified exponentially in higher humidity. Dengue-positive districts were identified by mean temperature >22°C for 7+ weeks and minimum temperature >14°C for 33+ weeks annually with 95% sensitivity and specificity. In elevated-risk locations, seasonal peak-incidence occurred when mean temperature was 26-29°C, coincident with humidity at its local maximum; highest incidence when humidity >80%. We profile transmission-potential in weather-space for temperature-humidity ranging 0-38°C and 5-100% at 1°C x 2% resolution.Conclusions/SignificanceLocal duration in limited areas of temperature-humidity weather-space identifies potential locations, timing, and magnitude of transmission. The weather-space profile of transmission-potential provides needed data that define a systematic and highly-sensitive weather-disease connection, demonstrating separate but coupled roles of temperature and humidity. New insights regarding natural regulation of human-mosquito transmission across diverse ecological settings advance our understanding of risk locally and globally for dengue and other mosquito-borne diseases and support advances in public health policy/operations, providing an evidence-base for modeling, predicting risk, and surveillance-prevention planning.

Partial Text: The escalating geographic scope and disease burden associated with dengue viruses (DENVs) over the past 50 years are serious global health concerns. Recent estimates of the global burden are nearly 400 million infections and 500,000 hospitalizations annually [1,2]. Weather is a fundamental and complex regulator of the local potential for DENV transmission [3,4], yet the significance of weather dynamics, especially in the contexts of strategic targeting of prevention resources and effects of global warming on risk, is hotly debated [4–9]. A clear understanding of the regulatory role of weather in DENV transmission has not yet evolved [3,4,7,10]. Weather-dengue dynamics are complex, multi-factorial, and non-linear and traditional statistical methods have produced diverse and conflicting perspectives regarding the weather-disease connection [3–5,7,8,11–18]. The seasonal nature of DENV dynamics in regions with hyper-endemic transmission has been linked to seasonal cycles in local weather and the mosquito Aedes aegypti [3,19,20]. Field and laboratory studies provided insights into relationships between local weather dynamics and specific aspects of mosquito ecology, development, life-cycle, survival, biting habits, extrinsic incubation period, and capacity to become infectious and transmit the virus [19–37]. Each of these individual biological processes related to the vector are sensitive to specific aspects of weather. A slight temperature change, for example, can impact life cycle dynamics, adult vector survival, or extrinsic incubation period in different ways [21–37]. Synthesis of many weather dependent dynamics into a measure of potential for virus transmission in ecological settings that continually change in space and time is a complex undertaking. Models have been used to explore the impact of weather on specific vector dynamics, however empirical data needed to support the computational link between weather, vector, and transmission dynamics across diverse ecological settings is lacking.

DENV transmission dynamics are complex. Weather plays a fundamental regulatory role in determining location, timing, and magnitude of virus transmission-potential. Key discriminators of potential and indicators of risk were defined by annual duration in specific areas of temperature-humidity weather-space. Temperature defined necessary vs optimal conditions for transmission; higher humidity levels concurrent with optimal temperature amplified potential; magnitude rose exponentially with increased humidity and annual duration in optimal weather-space. Dengue-positive districts were identified by mean temperature >22°C for 7+ weeks and minimum temperature >14°C for 33+ weeks per year, defining environmental conditions needed to sustain biological processes that enabled transmission. These results are consistent with observations from Thailand, 1983–2001, in which no cases were reported when mean temperature was <21°C or minimum temperature was <14.5°C [3]. Laboratory studies previously reported failure to obtain virus from salivary glands when Aedes aegypti were maintained at 20°C and failure for larvae to become adults below 14°C [24–26]. Temperature barriers observed in laboratory studies and now in long term observations of virus dynamics, likely represent a fundamental weather barrier for sustained DENV transmission. Source: http://doi.org/10.1371/journal.pntd.0003957

 

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