The global distribution of Bacillus anthracis and associated anthrax risk to humans, livestock and wildlife

Abstract

Bacillus anthracis is a spore-forming, Gram-positive bacterium responsible for anthrax, an acute infection that most significantly affects grazing livestock and wild ungulates, but also poses a threat to human health. The geographic extent of B. anthracis is poorly understood, despite multi-decade research on anthrax epizootic and epidemic dynamics; many countries have limited or inadequate surveillance systems, even within known endemic regions. Here, we compile a global occurrence dataset of human, livestock and wildlife anthrax outbreaks. With these records, we use boosted regression trees to produce a map of the global distribution of B. anthracis as a proxy for anthrax risk. We estimate that 1.83 billion people (95% credible interval (CI): 0.59–4.16 billion) live within regions of anthrax risk, but most of that population faces little occupational exposure. More informatively, a global total of 63.8 million poor livestock keepers (95% CI: 17.5–168.6 million) and 1.1 billion livestock (95% CI: 0.4–2.3 billion) live within vulnerable regions. Human and livestock vulnerability are both concentrated in rural rainfed systems throughout arid and temperate land across Eurasia, Africa and North America. We conclude by mapping where anthrax risk could disrupt sensitive conservation efforts for wild ungulates that coincide with anthrax-prone landscapes.

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Fig. 1: Global distrubtion of outbreaks by country and geographic locations of anthrax events.
Fig. 2: Global distribution of B. anthracis suitability (probability of occurrence).
Fig. 3: Map of average anthrax vaccination rates per country for all livestock species.

Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request and approval from appropriate partner country ministries of health or agriculture.

References

  1. 1.

    Carlson, C. J. et al. Spores and soil from six sides: interdisciplinarity and the environmental biology of anthrax (Bacillus anthracis). Biol. Rev. 93, 1813–1831 (2018).

    Article  Google Scholar 

  2. 2.

    Swartz, M. N. Recognition and management of anthrax—an update. N. Engl. J. Med. 345, 1621–1626 (2001).

    CAS  Article  Google Scholar 

  3. 3.

    Anthrax in Humans and Animals (World Health Organization and International Office of Epizootics, 2008).

  4. 4.

    Alexander, K. A., Lewis, B. L., Marathe, M., Eubank, S. & Blackburn, J. K. Modeling of wildlife-associated zoonoses: applications and caveats. Vector-Borne Zoonotic Dis. 12, 1005–1018 (2012).

    Article  Google Scholar 

  5. 5.

    Hugh-Jones, M. & Blackburn, J. The ecology of Bacillus anthracis. Mol. Aspects Med. 30, 356–367 (2009).

    Article  Google Scholar 

  6. 6.

    Hugh-Jones, M. & De Vos, V. Anthrax and wildlife. Sci. Tech. Rev. Off. Int. Epizoot. 21, 359–384 (2002).

    CAS  Article  Google Scholar 

  7. 7.

    Turner, W. C. et al. Fatal attraction: vegetation responses to nutrient inputs attract herbivores to infectious anthrax carcass sites. Proc. R. Soc. Lond. B 281, 20141785 (2014).

    Article  Google Scholar 

  8. 8.

    Coleman, M. E., Thran, B., Morse, S. S., Hugh-Jones, M. & Massulik, S. Inhalation anthrax: dose response and risk analysis. Biosecurity Bioterrorism 6, 147–160 (2008).

    Article  Google Scholar 

  9. 9.

    Shadomy, S. et al. Anthrax Outbreaks: A Warning for Improved Prevention, Control and Heightened Awareness (EMPRES Watch Vol. 37, FAO, 2016).

  10. 10.

    Blackburn, J. K., Kracalik, I. T. & Fair, J. M. Applying science: opportunities to inform disease management policy with cooperative research within a one health framework. Front. Public Health 3, 276 (2016).

    Article  Google Scholar 

  11. 11.

    Mullins, J. C. et al. Ecological niche modeling of Bacillus anthracis on three continents: evidence for genetic–ecological divergence? PloS ONE 8, e72451 (2013).

    CAS  Article  Google Scholar 

  12. 12.

    Chen, W.-J. et al. Mapping the distribution of anthrax in mainland China, 2005–2013. PLoS Negl. Trop. Dis. 10, e0004637 (2016).

    Article  Google Scholar 

  13. 13.

    Mullins, J. et al. Ecological niche modelling of the Bacillus anthracis A1. A sub-lineage in Kazakhstan. BMC Ecol. 11, 32 (2011).

    Article  Google Scholar 

  14. 14.

    Blackburn, J. K., McNyset, K. M., Curtis, A. & Hugh-Jones, M. E. Modeling the geographic distribution of Bacillus anthracis, the causative agent of anthrax disease, for the contiguous United States using predictive ecologic niche modeling. Am. J. Trop. Med. Hyg. 77, 1103–1110 (2007).

    Article  Google Scholar 

  15. 15.

    Barro, A. S. et al. Redefining the Australian anthrax belt: modeling the ecological niche and predicting the geographic distribution of Bacillus anthracis. PLoS Negl. Trop. Dis. 10, e0004689 (2016).

    Article  Google Scholar 

  16. 16.

    Seboxa, T. & Goldhagen, J. Anthrax in Ethiopia. Trop. Geogr. Med. 41, 108–112 (1989).

    CAS  PubMed  Google Scholar 

  17. 17.

    Deribe, K. et al. The burden of neglected tropical diseases in Ethiopia, and opportunities for integrated control and elimination. Parasites Vectors 5, 240 (2012).

    Article  Google Scholar 

  18. 18.

    Pieracci, E. G. et al. Prioritizing zoonotic diseases in Ethiopia using a one health approach. One Health 2, 131–135 (2016).

    Article  Google Scholar 

  19. 19.

    Griffith, J. et al. Investigation of inhalation anthrax case, United States. Emerg. Infect. Dis. 20, 280 (2014).

    Article  Google Scholar 

  20. 20.

    Kracalik, I. et al. Changing patterns of human anthrax in Azerbaijan during the post-Soviet and preemptive livestock vaccination eras. PLoS Negl. Trop. Dis. 8, e2985 (2014).

    Article  Google Scholar 

  21. 21.

    Blackburn, J. K. et al. Bacillus anthracis diversity and geographic potential across Nigeria, Cameroon and Chad: further support of a novel West African lineage. PLoS Negl. Trop. Dis. 9, e0003931 (2015).

    Article  Google Scholar 

  22. 22.

    Kracalik, I., Malania, L., Imnadze, P. & Blackburn, J. K. Human anthrax transmission at the urban–rural interface, Georgia. Am. J. Trop. Med. Hyg. 93, 1156–1159 (2015).

    CAS  Article  Google Scholar 

  23. 23.

    Hampson, K. et al. Predictability of anthrax infection in the Serengeti, Tanzania. J. Appl. Ecol. 48, 1333–1344 (2011).

    Article  Google Scholar 

  24. 24.

    Clegg, S. Preparedness for anthrax epizootics in wildlife areas. Emerg. Infect. Dis. https://doi.org/10.3201/eid1207.060458 (2006).

    Article  Google Scholar 

  25. 25.

    Turnbull, P. et al. Vaccine-induced protection against anthrax in cheetah (Acinonyx jubatus) and black rhinoceros (Diceros bicornis). Vaccine 22, 3340–3347 (2004).

    CAS  Article  Google Scholar 

  26. 26.

    Bhatt, S. et al. The global distribution and burden of dengue. Nature 496, 504–507 (2013).

    CAS  Article  Google Scholar 

  27. 27.

    Limmathurotsakul, D. et al. Predicted global distribution of Burkholderia pseudomallei and burden of melioidosis. Nat. Microbiol. 1, 15008 (2016).

    CAS  Article  Google Scholar 

  28. 28.

    Kracalik, I. T. et al. Modeling the environmental suitability of anthrax in Ghana and estimating populations at risk: implications for vaccination and control. PLoS Negl. Trop. Dis. 11, e0005885 (2017).

    Article  Google Scholar 

  29. 29.

    Munang’andu, H. M. et al. The effect of seasonal variation on anthrax epidemiology in the upper Zambezi floodplain of western Zambia. J. Vet. Sci. 13, 293–298 (2012).

    Article  Google Scholar 

  30. 30.

    Lepheana, R. J., Oguttu, J. W. & Qekwana, D. N. Temporal patterns of anthrax outbreaks among livestock in Lesotho, 2005–2016. PloS One 13, e0204758 (2018).

    Article  Google Scholar 

  31. 31.

    Blackburn, J. K. et al. Modeling the ecological niche of Bacillus anthracis to map anthrax risk in Kyrgyzstan. Am. J. Trop. Med. Hyg. 96, 550–556 (2017).

    PubMed  PubMed Central  Google Scholar 

  32. 32.

    Cizauskas, C. A. et al. Gastrointestinal helminths may affect host susceptibility to anthrax through seasonal immune trade-offs. BMC Ecol. 14, 27 (2014).

    Article  Google Scholar 

  33. 33.

    Havarua, Z., Turner, W. C. & Mfune, J. K. Seasonal variation in foraging behaviour of plains zebra (Equus quagga) may alter contact with the anthrax bacterium (Bacillus anthracis). Can. J. Zool. 92, 331–337 (2014).

    Article  Google Scholar 

  34. 34.

    Zidon, R., Garti, S., Getz, W. M. & Saltz, D. Zebra migration strategies and anthrax in Etosha National Park, Namibia. Ecosphere 8, e01925 (2017).

    Article  Google Scholar 

  35. 35.

    Schmidt, J. P. et al. Spatiotemporal fluctuations and triggers of ebola virus spillover. Emerg. Infect. Dis. 23, 415–422 (2017).

    Article  Google Scholar 

  36. 36.

    Kaul, R. B., Evans, M. V., Murdock, C. C. & Drake, J. M. Spatio-temporal spillover risk of yellow fever in Brazil. Parasites Vectors 11, 488 (2018).

    Article  Google Scholar 

  37. 37.

    Getz, W. M. et al. Making ecological models adequate. Ecol. Lett. 21, 153–166 (2018).

    Article  Google Scholar 

  38. 38.

    Blackburn, J. K. in Emerging and Endemic Pathogens (eds O'Connell, K., Skowronski, E., Sulakvelidze A. & Bakanidze, L.) 59–88 (Springer, 2010).

  39. 39.

    Walsh, M. G., de Smalen, A. W. & Mor, S. Climatic influence on the anthrax niche in warming northern latitudes. Sci. Rep. 8, 9269 (2018).

    Article  Google Scholar 

  40. 40.

    Hoffmann, C. et al. Persistent anthrax as a major driver of wildlife mortality in a tropical rainforest. Nature 548, 82–86 (2017).

    CAS  Article  Google Scholar 

  41. 41.

    Boria, R. A., Olson, L. E., Goodman, S. M. & Anderson, R. P. Spatial filtering to reduce sampling bias can improve the performance of ecological niche models. Ecol. Model. 275, 73–77 (2014).

    Article  Google Scholar 

  42. 42.

    Nsoesie, E. O. et al. Global distribution and environmental suitability for chikungunya virus, 1952 to 2015. Euro Surveill. 21, 30234 (2016).

    Article  Google Scholar 

  43. 43.

    Barbet-Massin, M., Jiguet, F., Albert, C. H. & Thuiller, W. Selecting pseudo-absences for species distribution models: how, where and how many? Methods Ecol. Evol. 3, 327–338 (2012).

    Article  Google Scholar 

  44. 44.

    Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. & Jarvis, A. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965–1978 (2005).

    Article  Google Scholar 

  45. 45.

    Hengl, T. et al. SoilGrids250m: global gridded soil information based on machine learning. PloS ONE 12, e0169748 (2017).

    Article  Google Scholar 

  46. 46.

    Hay, S., Tatem, A., Graham, A., Goetz, S. & Rogers, D. Global environmental data for mapping infectious disease distribution. Adv. Parasitol. 62, 37–77 (2006).

    CAS  Article  Google Scholar 

  47. 47.

    Messina, J. P. et al. The global distribution of Crimean-Congo hemorrhagic fever. Trans. R. Soc. Trop. Med. Hyg. 109, trv050 (2015).

    Article  Google Scholar 

  48. 48.

    Global Livestock Production Systems (Food and Agriculture Organization of the United Nations, 2011).

  49. 49.

    Robinson, T. P. et al. Mapping the global distribution of livestock. PLoS ONE 9, e96084 (2014).

    Article  Google Scholar 

  50. 50.

    Thornton, P. Mapping Poverty and Livestock in the Developing World (ILRI, 2002).

  51. 51.

    Ramesh, V., Gopalakrishna, T., Barve, S. & Melnick, D. J. IUCN greatly underestimates threat levels of endemic birds in the Western Ghats. Biol. Conserv. 210, 205–221 (2017).

    Article  Google Scholar 

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Acknowledgements

The authors thank D. Pigott for helpful tips on BRT modelling; A. Barner for help obtaining World Animal Health Information System vaccination data; S. J. Ryan for general feedback and technical support; G. Simpson for visualization advice; P. Thornton for access to the global dataset of rural poor livestock keepers; T. A. Joyner for data support; and countless livestock and wildlife managers, clinicians and field technicians for contributing data points. Partial funding for this study was provided by NIH 1R01GM117617-01 to J.K.B. and W.M.G. C.J.C. was supported by the National Socio-Environmental Synthesis Center (SESYNC) under funding received from the National Science Foundation DBI-1639145. K.A. was supported in part under the National Science Foundation (NSF EEID grant 1518663). We also thank the Botswana Government Department of Wildlife and National Parks for their assistance and active collaboration on research directed at understanding Botswana anthrax dynamics.

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C.J.C., I.T.K. and J.K.B. conceived of the study. J.K.B., M.E.H.-J., I.T.K. and C.J.C. collected and georeferenced data. C.J.C., I.T.K. and J.K.B. designed the models, and C.J.C. ran models and analyses. N.R. contributed R code. All authors contributed to the writing and editing of the draft and approved the study before submission.

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Correspondence to Jason K. Blackburn.

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Supplementary Text and Discussion, Supplementary Figures 1–21, Supplementary Tables 1–33 and Supplementary References.

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Carlson, C.J., Kracalik, I.T., Ross, N. et al. The global distribution of Bacillus anthracis and associated anthrax risk to humans, livestock and wildlife. Nat Microbiol 4, 1337–1343 (2019). https://doi.org/10.1038/s41564-019-0435-4

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