Reservoir dynamics of rabies in south-east Tanzania and the roles of cross-species transmission and domestic dog vaccination

Abstract

Understanding the role of different species in the transmission of multi-host pathogens, such as rabies virus, is vital for effective control strategies. Across most of sub-Saharan Africa domestic dogs Canis familiaris are considered the reservoir for rabies, but the role of wildlife has been long debated. Here we explore the multi-host transmission dynamics of rabies across south-east Tanzania.Between January 2011 and July 2019, data on probable rabies cases were collected in the regions of Lindi and Mtwara. Hospital records of animal-bite patients presenting to healthcare facilities were used as sentinels for animal contact tracing. The timing, location and species of probable rabid animals were used to reconstruct transmission trees to infer who infected whom and the relative frequencies of within- and between-species transmission.During the study, 688 probable human rabies exposures were identified, resulting in 47 deaths. Of these exposures, 389 were from domestic dogs (56.5%) and 262 from jackals (38.1%). Over the same period, 549 probable animal rabies cases were traced: 303 in domestic dogs (55.2%) and 221 in jackals (40.3%), with the remainder in domestic cats and other wildlife species.Although dog-to-dog transmission was most commonly inferred (40.5% of transmission events), a third of inferred events involved wildlife-to-wildlife transmission (32.6%), and evidence suggested some sustained transmission chains within jackal populations.A steady decline in probable rabies cases in both humans and animals coincided with the implementation of widespread domestic dog vaccination during the first 6 years of the study. Following the lapse of this program, dog rabies cases began to increase in one of the northernmost districts. Synthesis and applications. In south-east Tanzania, despite a relatively high incidence of rabies in wildlife and evidence of wildlife-to-wildlife transmission, domestic dogs remain essential to the reservoir of infection. Continued dog vaccination alongside improved surveillance would allow a fuller understanding of the role of wildlife in maintaining transmission in this area. Nonetheless, dog vaccination clearly suppressed rabies in both domestic dog and wildlife populations, reducing both public health and conservation risks and, if sustained, has potential to eliminate rabies from this region.

Keywords: One Health; dog-mediated rabies; lyssavirus; spillover; surveillance; vaccination; zero by thirty; zoonoses.

Figure 1

Potential rabies reservoir systems in south-east Tanzania. Here humans are indicated as the target population, but the target may include livestock or endangered wildlife, for example African Wild Dogs (Lycaon pictus). We investigate whether the reservoir consists of both maintenance and non-maintenance populations (a and b) transmitting infection to the non-maintenance target (humans); or either two maintenance (c) or non-maintenance (d) populations which are capable of transmitting infection to the target

Figure 2. Study districts and locations of probable rabies cases.

(a) The study area (dark grey) and protected areas where no human settlements are allowed (light grey): Selous Game Reserve in south-east Tanzania and Serengeti National Park in northern Tanzania. (b) Districts in Lindi and Mtwara regions (labelled) with estimated dog density on a 4-km² raster (grey shading). Urban districts within Masasi, Lindi and Mtwara are not labelled to improve readability. (c) Probable rabies cases in dogs (red) and wildlife (blue) each year in Lindi and Mtwara regions

Figure 3. Probable animal rabies cases, human rabies exposures and deaths by species from January 2011 to July 2019.

(a) Exposures (lines) and deaths (dots scaled by the number) from domestic dogs (red) and wildlife, mainly jackals (blue). (b) Cases in domestic dogs (red), jackals (blue), domestic cats (pink) and other wildlife (pale blue). Dashed lines indicate vaccination campaigns from 2011 to 2016. (c) The proportion of human exposures by species (dogs in red, wildlife in blue)

Figure 4. Inferred transmission chains and corresponding clusters according to species involved. Inferred transmission events within the 99th percentile of the serial interval and convolution of two distance kernel distributions (156 days and 9,803 m), using the single most likely progenitor for each case.

(a) Inferred transmission chains showing domestic dogs (red), wildlife (blue) and cats (yellow); (b) Frequency and composition of clusters by size; and (c) inferred transmission chains by date of cases and district (coloured as for (a))

Figure 5

Trend in mean cluster size per 6-month period from January 2011 until July 2019. Mean cluster sizes for each 6-month period (orange) with the fitted linear spline regression (green) and associated 95% CI. A statistically significant downward trend in mean cluster size was observed over the initial 6-and-a-half years of the study (p = 0.001, reduction in mean cluster size of 0.12 (95% CI: 0.06–0.17) per 6-month period), followed by a statistically significant increase from July to December 2017 (p = 0.028, increase in mean cluster size of 0.52 (95% CI: 0.10–0.93) per 6-month period)

Figure 6

Relationship between the proportion of jackals in the susceptible animal population and the proportion of probable rabies cases in jackals. The susceptible population consists of jackals and unvaccinated dogs assuming the median level of vaccination coverage. Probable rabies cases refer to those in jackals and domestic dogs only. Dots represent the 16 districts in this analysis, scaled by the log10 cases in the district. Grey bars represent 95% confidence intervals (CIs). The CIs around the proportion of probable cases in jackals are exact binomial 95% CIs and were calculated keeping jackal estimates and levels of vaccination coverage constant but incorporating the lower and upper limits of the 95% CIs of the dog number estimates. The fitted logistic regression line is shown in black with the associated 95% CI in pink