Modeling environmentally mediated rotavirus transmission: The role of temperature and hydrologic factors

Abstract

Rotavirus is considered a directly transmitted disease due to its high infectivity. Environmental pathways have, therefore, largely been ignored. Rotavirus, however, persists in water sources, and both its surface water concentrations and infection incidence vary with temperature. Here, we examine the potential for waterborne rotavirus transmission. We use a mechanistic model that incorporates both direct and waterborne transmission pathways, coupled with a hydrological model, and we simulate rotavirus transmission between two communities with interconnected water sources. To parameterize temperature dependency, we estimated temperature-dependent decay rates in water through a meta-analysis. Our meta-analysis suggests that rotavirus decay rates are positively associated with temperature ( = 39, [Formula: see text] 0.001). This association is stronger at higher temperatures (over 20 °C), consistent with tropical climate conditions. Our model analysis demonstrates that water could disseminate rotavirus between the two communities for all modeled temperatures. While direct transmission was important for disease amplification within communities, waterborne transmission could also amplify transmission. In standing-water systems, the modeled increase in decay led to decreased disease, with every 1 °C increase in temperature leading to up to a 2.4% decrease in incidence. These effect sizes are consistent with prior meta-analyses, suggesting that environmental transmission through water sources may partially explain the observed associations between temperature and rotavirus incidence. Waterborne rotavirus transmission is likely most important in cooler seasons and in communities that use slow-moving or stagnant water sources. Even when indirect transmission through water cannot sustain outbreaks, it can seed outbreaks that are maintained by high direct transmission rates.

Tubewell use protects against rotavirus infection during the monsoons in an urban setting

“…While rotavirus transmission is typically considered to occur via direct person-to-person contact, this result highlights the importance of environmental transmission via water in Dhaka. This is consistent with recent studies showing that rotavirus transmission is sensitive to interannual variation in flooding [8], and that waterborne transmission alone is sufficient to spread the virus between hydrologically connected locations [7]. The use of tubewells has also been shown to provide a protective effect against other diarrheal diseases in Bangladesh, such as cholera [11,12] and shigellosis [12], especially in areas that are not protected from flooding [13].…”

“…Bangladesh is an example of a country with high incidence all year round, particularly in Dhaka the capital city, where high temperatures, low humidity, and flooding events have been associated with an increased risk for rotavirus [6]. Current dogma suggests that person-to-person contact is the dominant mode of transmission of the virus, although it has been shown to persist in water [7] and to respond to climatic changes [8]. Dhaka has more than 18 million inhabitants and a population growth of about 4% annually, making it one of the densest and fastest growing megacities in the world.…”

Ecological drivers of African swine fever virus persistence in wild boar populations: Insight for control

“…Understanding mechanisms by which pathogens transmit between hosts is key for defining disease risk and for planning effective control strategies. In addition to direct host‐to‐host or vector‐borne transmission, pathogens can spread through environmental sources, such as through contact with fomites (Allerson, Cardpna, & Torremorell, ), ingestion of contaminated drinking water (Breban, ; Kraay et al, ), contact with contaminated soil (Turner et al, ), contact with contaminated carcasses (Chenais, Ståhl, Guberti, & Depner, ), or carcass scavenging (Brown & Bevins, ; Wille et al, ). Environmental sources of infection can promote pathogen persistence by increasing their likelihood of contact with susceptible hosts because many pathogens can remain viable in the environment longer than they can keep a host infectious.…”

“…The persistence of infectious agents in environmental reservoirs can enable high pathogen reproductive numbers when epidemic growth rates are low by extending the infectious period beyond the life expectancy of the host (Almberg, Cross, Johnson, Heisey, & Richards, ). In some systems, environmental transmission mechanisms can explain recurrent epidemics (Towers et al, ), even at intervals that are longer than demographic cycling (Breban, ), as well as amplifying rates of interpopulation transmission by increasing infectious contact opportunity between groups (Kraay et al, ). Theoretical metapopulation modeling has shown that accounting for mechanisms of environmental transmission in addition to routes of direct transmission can lead to qualitatively different disease dynamics and predict different animal movement thresholds for metapopulation decline (Park, ).…”

“…The persistence of infectious agents in environmental reservoirs can enable high pathogen reproductive numbers when epidemic growth rates are low by extending the infectious period beyond the life expectancy of the host (Almberg, Cross, Johnson, Heisey, & Richards, 2011). In some systems, environmental transmission mechanisms can explain recurrent epidemics (Towers et al, 2018), even at intervals that are longer than demographic cycling (Breban, 2013), as well as amplifying rates of interpopulation transmission by increasing infectious contact opportunity between groups (Kraay et al, 2018).…”