Spatio-temporal epidemiology of anthrax in Hippopotamus amphibious in Queen Elizabeth Protected Area, Uganda

Abstract

Background: Anthrax is a zoonotic disease primarily of herbivores, caused by Bacillus anthracis, a bacterium with diverse geographical and global distribution. Globally, livestock outbreaks have declined but in Africa significant outbreaks continue to occur with most countries still categorized as enzootic, hyper endemic or sporadic. Uganda experiences sporadic human and livestock cases. Severe large-scale outbreaks occur periodically in hippos (Hippopotamus amphibious) at Queen Elizabeth Protected Area, where in 2004/2005 and 2010 anthrax killed 437 hippos. Ecological drivers of these outbreaks and potential of hippos to maintain anthrax in the ecosystem remain unknown. This study aimed to describe spatio-temporal patterns of anthrax among hippos; examine significant trends associated with case distributions; and generate hypotheses for investigation of ecological drivers of anthrax.

Methods: Spatio-temporal patterns of 317 hippo cases in 2004/5 and 137 in 2010 were analyzed. QGIS was used to examine case distributions; Spearman's nonparametric tests to determine correlations between cases and at-risk hippo populations; permutation models of the spatial scan statistics to examine spatio-temporal clustering of cases; directional tests to determine directionality in epidemic movements; and standard epidemic curves to determine patterns of epidemic propagation.

Key findings: Results showed hippopotamus cases extensively distributed along water shorelines with strong positive correlations (p<0.01) between cases and at-risk populations. Significant (p<0.001) spatio-temporal clustering of cases occurred throughout the epidemics, pointing towards a defined source. Significant directional epidemic spread was detected along water flow gradient (206.6°) in 2004/5 and against flow gradient (20.4°) in 2010. Temporal distributions showed clustered pulsed epidemic waves.

Conclusion: These findings suggest mixed point-source propagated pattern of epidemic spread amongst hippos and points to likelihood of indirect spread of anthrax spores between hippos mediated by their social behaviour, forces of water flow, and persistent presence of infectious carcasses amidst schools. This information sheds light on the epidemiology of anthrax in highly social wildlife, can help drive insight into disease control, wildlife conservation, and tourism management, but highlights the need for analytical and longitudinal studies aimed at clarifying the hypotheses.

Fig 1. Spatial distribution of anthrax cases relative to hippo population size in 2004/5 outbreak.

Symbols represent case locations. Colour ramp from light to dark on gridded rectangle cells represent increasing number of at-risk hippos within a 6 km radius buffer zone. Hippopotamus amphibious live in water during day, congregating in social groups called schools. They walk out at night an average of 3–6 km to graze [4]. A buffer of 6 km radius was generated around each geo-referenced school to map high risk areas for hippo anthrax outbreaks. The study area was overlaid with 6 x 6 km grid cells and clipped to the buffers. Twenty-seven (n = 27) grid cells were used to map spatial overlap between cases and hippo populations. Cases were mostly recorded in areas with at-risk hippo populations exceeding 324.

Fig 2. patial distribution of anthrax cases relative to hippo population size in 2010.

Fig 3. Spatial and temporal distribution of Hippopotamus anthrax clusters in 2004/5.

Spatio-temporal data for clusters including centroid coordinates, radii, and time span were generated using the retrospective space-time permutation model of the spatial scan statistics and mapped using QGIS (Version 2.18.9). The first two clusters 1 & 2 had overlapping dates and were considered origins for this outbreak.

Fig 4. Spatial and temporal distribution of Hippopotamus anthrax clusters in 2010.

Clusters 2 & 4 occurred upstream, relative to cluster 1 and against direction of water flow.

Fig 5. Epidemic curve showing patterns of epidemic spread for weekly anthrax cases in Hippopotamus.

This outbreak occurred in clustered waves (epidemic generations), lasted 42 weeks from 25 July 2004 to May 2005 and died after 3 generations. Clusters that spanned over 20 days were considered protracted single outbreaks beyond anthrax incubation period or multiple outbreaks (Tables 2 and 3). Dashed line shows time in week 9 of outbreak when management intervention for carcass disposal was initiated. Number of cases did not drastically decline but epidemic peaks in the second and third epidemic generations dropped below the peak in the first wave instead of becoming successively larger.

Fig 6. Epidemic curve showing patterns of epidemic spread for weekly anthrax cases in Hippopotamus in2010.

Outbreak occurred in less distinct waves, lasted 27 weeks from 11 June to December and died after 3 generations. Dashed line shows time at onset of the outbreak in week 1 when management intervention for carcass disposal was initiated. Number of new cases drastically declined immediately following response.

Fig 7. Location specific patterns of epidemic spread for weekly Hippopotamus anthrax cases in 2004/5.

Epidemic curves were characterized by geographical locations at Lakes George and Edward (Panel A); Kazinga channel and R. Kyambura (Panel B) to examine possibilities of occurrence of a series of sporadic point source outbreaks. Epidemic waves detected were numbered 1–6 according to the sequence of occurrence of waves at the respective locations. Epidemic patterns remained clustered, progressing successively and waves lasted beyond one incubation period of anthrax (average 1–14 days) except at Kyambura River.