Understanding Spatio-Temporal Variability in the Reproduction Ratio of the Bluetongue (BTV-1) Epidemic in Southern Spain (Andalusia) in 2007 Using Epidemic Trees

Abstract

Andalusia (Southern Spain) is considered one of the main routes of introduction of bluetongue virus (BTV) into Europe, evidenced by a devastating epidemic caused by BTV-1 in 2007. Understanding the pattern and the drivers of BTV-1 spread in Andalusia is critical for effective detection and control of future epidemics. A long-standing metric for quantifying the behaviour of infectious diseases is the case-reproduction ratio (Rt), defined as the average number of secondary cases arising from a single infected case at time t (for t>0). Here we apply a method using epidemic trees to estimate the between-herd case reproduction ratio directly from epidemic data allowing the spatial and temporal variability in transmission to be described. We then relate this variability to predictors describing the hosts, vectors and the environment to better understand why the epidemic spread more quickly in some regions or periods. The Rt value for the BTV-1 epidemic in Andalusia peaked in July at 4.6, at the start of the epidemic, then decreased to 2.2 by August, dropped below 1 by September (0.8), and by October it had decreased to 0.02. BTV spread was the consequence of both local transmission within established disease foci and BTV expansion to distant new areas (i.e. new foci), which resulted in a high variability in BTV transmission, not only among different areas, but particularly through time, which suggests that general control measures applied at broad spatial scales are unlikely to be effective. This high variability through time was probably due to the impact of temperature on BTV transmission, as evidenced by a reduction in the value of Rt by 0.0041 for every unit increase (day) in the extrinsic incubation period (EIP), which is itself directly dependent on temperature. Moreover, within the range of values at which BTV-1 transmission occurred in Andalusia (20.6°C to 29.5°C) there was a positive correlation between temperature and Rt values, although the relationship was not linear, probably as a result of the complex relationship between temperature and the different parameters affecting BTV transmission. Rt values for BTV-1 in Andalusia fell below the threshold of 1 when temperatures dropped below 21°C, a much higher threshold than that reported in other BTV outbreaks, such as the BTV-8 epidemic in Northern Europe. This divergence may be explained by differences in the adaptation to temperature of the main vectors of the BTV-1 epidemic in Andalusia (Culicoides imicola) compared those of the BTV-8 epidemic in Northern Europe (Culicoides obsoletus). Importantly, we found that BTV transmission (Rt value) increased significantly in areas with higher densities of sheep. Our analysis also established that control of BTV-1 in Andalusia was complicated by the simultaneous establishment of several distant foci at the start of the epidemic, which may have been caused by several independent introductions of infected vectors from the North of Africa. We discuss the implications of these findings for BTV surveillance and control in ...

Bluetongue virus spread in Europe is a consequence of climatic, landscape and vertebrate host factors as revealed by phylogeographic inference

“…Consistent with this hypothesis, the re-emergence of the virus in France in 2015 occurred in a cattle production region and only involved a few cases in sheep [ 14 ]. Results revealing a considerable role played by sheep are, however, also congruent with a recent work that showed that BTV-1 transmission increased significantly in areas with higher densities of sheep during the epidemic of 2007 in southern Spain [ 55 ]. Our results also supported a positive association of BTV spread with the density of goats, which rarely display clinical signs and are generally not considered to play an important role in BTV transmission [ 56 ].…”

“…BTV transmission is optimal at a mean temperature of 20°C–25°C and decreases at both warmer and cooler temperatures [ 21 , 60 ]. During a 2007 outbreak of BTV-1 in Andalusia for example, there was an overall positive correlation between temperature and basic reproductive number (R0); however, it has been shown that this relationship was not linear [ 55 ]. Given these complexities, it might be more appropriate to consider temperature in a nonlinear fashion by examining critical thresholds and classifying resistance values accordingly [ 61 ].…”

Assessment of listing and categorisation of animal diseases within the framework of the Animal Health Law (Regulation (EU) No 2016/429): bluetongue

“…Napp et al. () estimated the case‐reproduction ratio (R t ) for the BTV‐1 spread in Andalusia in 2007, resulting in values ranging from 4.6 in July, to 2.2 in August, and below 1 in September (0.8) and October (0.02).…”

“…Obviously, the speed of transmission is strongly influenced by the vector abundance and, therefore, by the local climatic conditions. Napp et al (2016) estimated the case-reproduction ratio (R t ) for the BTV-1 spread in Andalusia in 2007, resulting in values ranging from 4.6 in July, to 2.2 in August, and below 1 in September (0.8) and October (0.02).…”

Identifying Spanish Areas at More Risk of Monthly BTV Transmission with a Basic Reproduction Number Approach

“…To externally assess the performance and usefulness of the monthly transmission risk maps we used historical data from 2007–2018 of BTV-1 (11,482) and BTV-4 (506) outbreaks from the European Animal Disease Notification System (ADNS) database [ 97 ], excluding BTV outbreaks in wildlife. We used an estimation of 14 day-lapse between the day of infection and the date of suspicion [ 98 ]. The suspicion date was calculated when missing from the mean lapse time between the suspicion and confirmation dates from observations with data (approximately 20 days).…”