Predicting temperature-dependent transmission suitability of bluetongue virus in livestock

Fadoua El Moustaid,Zorian Thornton,Hani Slamani,Sadie J Ryan,Leah R Johnson

doi:10.1186/s13071-021-04826-y

Abstract

The transmission of vector-borne diseases is governed by complex factors including pathogen characteristics, vector–host interactions, and environmental conditions. Temperature is a major driver for many vector-borne diseases including Bluetongue viral (BTV) disease, a midge-borne febrile disease of ruminants, notably livestock, whose etiology ranges from mild or asymptomatic to rapidly fatal, thus threatening animal agriculture and the economy of affected countries. Using modeling tools, we seek to predict where the transmission can occur based on suitable temperatures for BTV. We fit thermal performance curves to temperature-sensitive midge life-history traits, using a Bayesian approach. We incorporate these curves into S(T), a transmission suitability metric derived from the disease’s basic reproductive number, R_0. This suitability metric encompasses all components that are known to be temperature-dependent. We use trait responses for two species of key midge vectors, Culicoides sonorensis and Culicoides variipennis present in North America. Our results show that outbreaks of BTV are more likely between 15^{circ } C and 34^{circ }hbox { C}, with predicted peak transmission risk at 26 ^circ C. The greatest uncertainty in S(T) is associated with the following: the uncertainty in mortality and fecundity of midges near optimal temperature for transmission; midges’ probability of becoming infectious post-infection at the lower edge of the thermal range; and the biting rate together with vector competence at the higher edge of the thermal range. We compare three model formulations and show that incorporating thermal curves into all three leads to similar BTV risk predictions. To demonstrate the utility of this modeling approach, we created global suitability maps indicating the areas at high and long-term risk of BTV transmission, to assess risk and to anticipate potential locations of disease establishment.

Highlights

With ongoing climate change, it is critical that we understand how temperature influences the dynamics of emerging diseases
We present the geography of suitability across the globe by mapping the number of months of suitable temperatures for transmission based on the monthly average temperatures from the WorldClim dataset [35]
Temperature‐dependence model components Here we summarize the model components that depend on temperature and explain their role in the model

Summary

Introduction

It is critical that we understand how temperature influences the dynamics of emerging diseases. BTV can infect most species of domestic and wild ruminants, including sheep, goats, and cattle [11]. In the majority of infections by strains of BTV’s 27 serotypes, animals rarely show any clinical signs [14]. Since clinical signs are rare, BTV infection often goes without detection. Undetected cases can still result in mortality, and while BTV vaccines exist, vaccine development is in its infancy [15]. An effective polyvalent vaccine to immunize against more than one strain of BTV has yet to be developed [16], and existing attenuated viral vaccines pose significant health risks to livestock, such as reduced milk production in lactating sheep, abortion, early embryonic death, and teratogenesis in pregnant females [17]

Methods

Results

Conclusion