Serotype SAT 2 Species Transitions of Foot-and-Mouth Disease Virus Reconstructing Geographical Movements and Host 2013

Of the three foot-and-mouth-disease virus SAT serotypes mainly confined to sub-Saharan Africa, SAT 2 is the strain most often recorded in domestic animals and has caused outbreaks in North Africa and the Middle East six times in the last 25 years, with three apparently separate events occurring in 2012. This study updates the picture of SAT 2 phylogenetics by using all available sequences for the VP1 section of the genome available at the time of writing and uses phylogeographic methods to trace the origin of all outbreaks occurring north of the Sahara since 1990 and identify patterns of spread among countries of endemicity. Transitions between different host species are also enumerated. Outbreaks in North Africa appear to have origins in countries immediately south of the Sahara, whereas those in the Middle East are more often from East Africa. The results of the analysis of spread within sub-Saharan Africa are consistent with it being driven by relatively short-distance movements of animals across national borders, and the analysis of host species transitions supports the role of the African buffalo (Syncerus caffer) as an important natural reservoir. IMPORTANCE Foot-and-mouth disease virus is a livestock pathogen of major economic importance, with seven distinct serotypes occurring globally. The SAT 2 serotype, endemic in sub-Saharan Africa, has caused a number of outbreaks in North Africa and the Middle East during the last decades, including three separate incidents in 2012. A comprehensive analysis of all available RNA sequences for SAT 2 has not been published for some years. In this work, we performed this analysis using all previously published sequences and 49 newly determined examples. We also used phylogenetic methods to infer the source country for all outbreaks occurring outside sub-Saharan Africa since 1990 and to reconstruct the spread of viral lineages between countries where it is endemic and movements between different host species. Received 29 July 2013 Accepted 17 September 2013 Published 22 October 2013 Citation Hall MD, Knowles NJ, Wadsworth J, Rambaut A, Woolhouse MEJ. 2013. Reconstructing geographical movements and host species transitions of foot-and-mouth disease virus serotype SAT 2. mBio 4(5):e00591-13. doi:10.1128/mBio.00591-13. Editor Julian Parkhill, The Sanger Institute Copyright © 2013 Hall et al. This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited. Address correspondence to Matthew Hall, m.d.hall@sms.ed.ac.uk. Foot-and-mouth disease (FMD) is a highly contagious disease of cloven-hoofed mammals caused by FMD virus (FMDV), a single-stranded RNA virus of the family Picornaviridae. Seven serotypes exist, two of which (O and A) are found almost worldwide. Another, type C, is more geographically restricted and has not been detected anywhere in the world since 2004, while the Asia-1 serotype is normally confined to southern Asia (1, 2). The remaining three serotypes are the three Southern African Territories (SAT) viruses, designated SAT 1, SAT 2, and SAT 3, the first two of which are endemic in countries of Africa south of the Sahara; outbreaks due to SAT 3 in domesticated livestock have been confined to a few countries in southern Africa. SAT 2, the focus of this study, is the SAT serotype most often recorded in domestic animals (3) and is widely distributed across the continent, having been identified as far west as Senegal, east as Ethiopia, and south as South Africa. It is further subclassified into 14 topotypes, designated I to XIV, defined as having 80% nucleotide identity in the VP1 coding region (4, 5). SAT 2 has crossed the Sahara and caused outbreaks in North Africa and the Middle East on several occasions in recent years. Middle Eastern outbreaks occurred in North Yemen in 1990 (6) and in Saudi Arabia and Kuwait in 2000 (1). In North Africa, it appeared in Libya in 2003 after an apparent absence from the region for around 50 years (7). In 2012, outbreaks occurred in Egypt, the Palestinian Territories, Libya, and Bahrain (6). While it might be surmised that the occurrence of so many events in a single year might be the result of a single introduction that spread further once established north of the Sahara, Ahmed et al. (6) conducted a genetic study of the viruses involved and found that this did not appear to be the case. Although the bulk of the Egyptian and Palestinian isolates are closely related, those from Libya and Bahrain are of quite distinct lineages. The Bahraini virus is even of a different topotype. Furthermore, one of the samples obtained from Egypt proved to be yet another lineage, distinct from the others collected in the country during the epidemic. For the virus to escape from sub-Saharan Africa four times in 1 year is unprecedented, and it has been suggested that the political changes in the region from 2011 onwards (the “Arab Spring”) may have played a role (http://www.bbsrc.ac.uk/news/food-security /2012/120613-f-arab-spring-spread-of-animal-disease.aspx), as people and their animals were displaced by conflict or changing governments created new trading relationships and thus new RESEARCH ARTICLE September/October 2013 Volume 4 Issue 5 e00591-13 ® mbio.asm. org 1 m b.asm . rg on O cber 0, 2014 P ubished by m b.asm . rg D ow nladed fom