Waves of endemic foot-and-mouth disease in eastern Africa suggest feasibility of proactive vaccination approaches

Abstract

Livestock production in Africa is key to national economies, food security and rural livelihoods, and > 85% of livestock keepers live in extreme poverty. With poverty elimination central to the Sustainable Development Goals, livestock keepers are therefore critically important. Foot-and-mouth disease is a highly contagious livestock disease widespread in Africa that contributes to this poverty. Despite its US$2.3 billion impact, control of the disease is not prioritized: standard vaccination regimens are too costly, its impact on the poorest is underestimated, and its epidemiology is too weakly understood. Our integrated analysis in Tanzania shows that the disease is of high concern, reduces household budgets for human health, and has major impacts on milk production and draft power for crop production. Critically, foot-and-mouth disease outbreaks in cattle are driven by livestock-related factors with a pattern of changing serotype dominance over time. Contrary to findings in southern Africa, we find no evidence of frequent infection from wildlife, with outbreaks in cattle sweeping slowly across the region through a sequence of dominant serotypes. This regularity suggests that timely identification of the epidemic serotype could allow proactive vaccination ahead of the wave of infection, mitigating impacts, and our preliminary matching work has identified potential vaccine candidates. This strategy is more realistic than wildlife–livestock separation or conventional foot-and-mouth disease vaccination approaches. Overall, we provide strong evidence for the feasibility of coordinated foot-and-mouth disease control as part of livestock development policies in eastern Africa, and our integrated socioeconomic, epidemiological, laboratory and modelling approach provides a framework for the study of other disease systems.

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Fig. 1: Study area.
Fig. 2: Household-level impacts of FMD.
Fig. 3: FMDV serotype frequency over time in eastern African cattle.
Fig. 4: Serum virus neutralization testing results in buffalo (Syncerus caffer) and cattle.

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Acknowledgements

We are grateful to the Tanzania Commission for Science and Technology, Tanzania Ministry of Livestock and Fisheries, Tanzania Wildlife Research Institute, Tanzania National Parks and the Ngorongoro Conservation Area Authority for permissions and productive collaborations; the District Veterinary Officers, Livestock Field Officers and Community Animal Health Workers in Mara and Arusha regions for assistance with data and sample collection, and stakeholder engagement activities; the Frankfurt Zoological Society and Tanzania Conservation Resource Centre for logistical and administrative support in Tanzania; and colleagues in the WRLFMD for their contribution to laboratory analyses. We are indebted to R. Mahemba Shabani for his dedication and hard work throughout the study, and E. Kamani for coordinating field activities in the initial stages of the project. We are grateful to J. Yoder for valuable contributions to the socioeconomic surveys and comments on an earlier version of the manuscript. We thank G. Hopcraft and M. Shand for assistance with production of maps for this manuscript. This work was supported by the Biotechnology and Biological Sciences Research Council (BBSRC), the Department for International Development and the Scottish Government through the Combating Infectious Diseases of Livestock for International Development initiative (projects BB/H009302/1 and BB/H009175/1). The work of the WRLFMD was supported by the Department for Environment, Food and Rural Affairs (Project SE2943: Defra, UK) and funding provided to the EuFMD from the European Union. Doctoral training for M.C.-B. was funded by a BBSRC Doctoral Training Grant. T.L. and R.R. received support from the Scottish Universities Life Sciences Alliance (SULSA). R.R. was supported by BBSRC grant BB/L004828/1. R.F. and G.N. were supported by the Wellcome Trust–funded Afrique One consortium. Community- and policy-related knowledge exchange initiatives were funded through the Afrique One consortium, contributions by Merck Animal Health to the University of Glasgow and the Boyd Orr Centre for Population and Ecosystem Health. The African Development Bank funded the Southern African Development Community Transboundary Animal Diseases (SADC TADs) Project at the SADC Secretariat. Opinions, findings, conclusions and recommendations are those of the authors and do not necessarily reflect the views of the funding bodies.

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Contributions

The study was designed by M.C.-B., R.R., H.A., D.J.P., S.P., D.T.H., T.L.M., S.C. and T.L. Field work was carried out by H.A., R.F., R.K., T.K., F.L., A.L., D.M., G.N. and T.L. Laboratory work was performed by M.C.-B., N.J.K., K.B.-B., V.L.F., D.P.K., A.B.L., F.F.M., K.P., J.W., S.P., S.C. and T.L. Modelling and data analysis was conducted by M.C.-B., R.R., U.B., N.J.K. and T.L.M. The paper was written and revised by all authors.

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Correspondence to Tiziana Lembo.

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Competing interests

A.K. works for Merck Animal Health (known as MSD Animal Health outside USA and Canada), which manufactures FMD vaccines. The workshops described in Supplementary Notes 1 and 2 were funded jointly by the Wellcome Trust through the Afrique One Consortium, the University of Glasgow and its Boyd Orr Centre for Population and Ecosystem Health, and MSD Animal Health. MSD had no control over the design, implementation or analysis of the results of the workshops, and the MSD funding has not influenced the work presented in this manuscript in any way. A.K. had no influence on the study design or the analysis described in the manuscript as a whole, but was consulted in discussions about the feasibility of the proposed solutions and during the manuscript preparation process.

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Supplementary Figures 1–4, Supplementary Tables 1–20, Supplementary Methods, Supplementary References, Supplementary Notes 1–2

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Casey-Bryars, M., Reeve, R., Bastola, U. et al. Waves of endemic foot-and-mouth disease in eastern Africa suggest feasibility of proactive vaccination approaches. Nat Ecol Evol 2, 1449–1457 (2018). https://doi.org/10.1038/s41559-018-0636-x

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