The isolation of foot-and-mouth disease virus from African buffalo (Syncerus caffer)

ABSTRACTAfrican buffaloes (Syncerus caffer) are the principal “carrier” hosts of foot-and-mouth disease virus (FMDV). Currently, the epithelia and lymphoid germinal centers of the oropharynx have been identified as sites for FMDV persistence. We carried out studies in FMDV SAT1 persistently infected buffaloes to characterize the diversity of viruses in oropharyngeal epithelia, germinal centers, probang samples (oropharyngeal scrapings), and tonsil swabs to determine if sufficient virus variation is generated during persistence for immune escape. Most sequencing reads of the VP1 coding region of the SAT1 virus inoculum clustered around 2 subpopulations differing by 22 single-nucleotide variants of intermediate frequency. Similarly, most sequences from oropharynx tissue clustered into two subpopulations, albeit with different proportions, depending on the day postinfection (dpi). There was a significant difference between the populations of viruses in the inoculum and in lymphoid tissue taken at 35 dpi. Thereafter, until 400 dpi, no significant variation was detected in the viral populations in samples from individual animals, germinal centers, and epithelial tissues. Deep sequencing of virus from probang or tonsil swab samples harvested prior to postmortem showed less within-sample variability of VP1 than that of tissue sample sequences analyzed at the same time. Importantly, there was no significant difference in the ability of sera collected between 14 and 400 dpi to neutralize the inoculum or viruses isolated at later time points in the study from the same animal. Therefore, based on this study, there is no evidence of escape from antibody neutralization contributing to FMDV persistent infection in African buffalo.IMPORTANCEFoot-and-mouth disease virus (FMDV) is a highly contagious virus of cloven-hoofed animals and is recognized as the most important constraint to international trade in animals and animal products. African buffaloes (Syncerus caffer) are efficient carriers of FMDV, and it has been proposed that new virus variants are produced in buffalo during the prolonged carriage after acute infection, which may spread to cause disease in livestock populations. Here, we show that despite an accumulation of low-frequency sequence variants over time, there is no evidence of significant antigenic variation leading to immune escape. Therefore, carrier buffalo are unlikely to be a major source of new virus variants.

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Differential Persistence of Foot-and-Mouth Disease Virus in African Buffalo Is Related to Virus Virulence

Journal of Virology ◽

10.1128/jvi.00166-16 ◽

2016 ◽

Vol 90 (10) ◽

pp. 5132-5140 ◽

Cited By ~ 29

Author(s):

Francois Maree ◽

Lin-Mari de Klerk-Lorist ◽

Simon Gubbins ◽

Fuquan Zhang ◽

Julian Seago ◽

...

Keyword(s):

Disease Virus ◽

Foot And Mouth Disease ◽

Germinal Centers ◽

Cell Killing ◽

Mouth Disease ◽

Lymphoid Tissues ◽

African Buffalo ◽

Mouth Disease Virus ◽

Foot And Mouth

ABSTRACTFoot-and-mouth disease (FMD) virus (FMDV) circulates as multiple serotypes and strains in many regions of endemicity. In particular, the three Southern African Territories (SAT) serotypes are maintained effectively in their wildlife reservoir, the African buffalo, and individuals may harbor multiple SAT serotypes for extended periods in the pharyngeal region. However, the exact site and mechanism for persistence remain unclear. FMD in buffaloes offers a unique opportunity to study FMDV persistence, as transmission from carrier ruminants has convincingly been demonstrated for only this species. Following coinfection of naive African buffaloes with isolates of three SAT serotypes from field buffaloes, palatine tonsil swabs were the sample of choice for recovering infectious FMDV up to 400 days postinfection (dpi). Postmortem examination identified infectious virus for up to 185 dpi and viral genomes for up to 400 dpi in lymphoid tissues of the head and neck, focused mainly in germinal centers. Interestingly, viral persistencein vivowas not homogenous, and the SAT-1 isolate persisted longer than the SAT-2 and SAT-3 isolates. Coinfection and passage of these SAT isolates in goat and buffalo cell lines demonstrated a direct correlation between persistence and cell-killing capacity. These data suggest that FMDV persistence occurs in the germinal centers of lymphoid tissue but that the duration of persistence is related to virus replication and cell-killing capacity.IMPORTANCEFoot-and-mouth disease virus (FMDV) causes a highly contagious acute vesicular disease in domestic livestock and wildlife species. African buffaloes (Syncerus caffer) are the primary carrier hosts of FMDV in African savannah ecosystems, where the disease is endemic. We have shown that the virus persists for up to 400 days in buffaloes and that there is competition between viruses during mixed infections. There was similar competition in cell culture: viruses that killed cells quickly persisted more efficiently in passaged cell cultures. These results may provide a mechanism for the dominance of particular viruses in an ecosystem.

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Experimental infection of eland (Taurotrages oryx), sable antelope (Ozanna grandicomis) and buffalo (Syncerus caffer) with foot-and-mouth disease virus

Journal of Comparative Pathology ◽

10.1016/0021-9975(89)90040-6 ◽

1989 ◽

Vol 101 (3) ◽

pp. 307-316 ◽

Cited By ~ 9

Author(s):

N.P. Ferris ◽

J.B. Condy ◽

I.T.R. Barnett ◽

R.M. Armstrong

Keyword(s):

Disease Virus ◽

Experimental Infection ◽

Foot And Mouth Disease ◽

Mouth Disease ◽

Syncerus Caffer ◽

Mouth Disease Virus ◽

Foot And Mouth

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Evidence for Positive Selection in Foot-and-Mouth Disease Virus Capsid Genes From Field Isolates

Genetics ◽

10.1093/genetics/157.1.7 ◽

2001 ◽

Vol 157 (1) ◽

pp. 7-15 ◽

Cited By ~ 1

Author(s):

Daniel T Haydon ◽

Armanda D Bastos ◽

Nick J Knowles ◽

Alan R Samuel

Keyword(s):

Amino Acid ◽

Positive Selection ◽

Disease Virus ◽

Foot And Mouth Disease ◽

Selective Advantage ◽

Mouth Disease ◽

Data Sets ◽

African Buffalo ◽

Mouth Disease Virus ◽

Foot And Mouth

AbstractThe nature of selection on capsid genes of foot-and-mouth disease virus (FMDV) was characterized by examining the ratio of nonsynonymous to synonymous substitutions in 11 data sets of sequences obtained from six different serotypes of FMDV. Using a method of analysis that assigns each codon position to one of a number of estimated values of nonsynonymous to synonymous ratio, significant evidence of positive selection was identified in 5 data sets, operating at 1-7% of codon positions. Evidence of positive selection was identified in complete capsid sequences of serotypes A and C and in VP1 sequences of serotypes SAT 1 and 2. Sequences of serotype SAT-2 recovered from a persistently infected African buffalo also revealed evidence for positive selection. Locations of codons under positive selection coincide closely with those of antigenic sites previously identified with the use of monoclonal antibody escape mutants. The vast majority of codons are under mild to strong purifying selection. However, these results suggest that arising antigenic variants benefit from a selective advantage in their interaction with the immune system, either during the course of an infection or in transmission to individuals with previous exposure to antigen. Analysis of amino acid usage at sites under positive selection indicates that this selective advantage can be conferred by amino acid substitutions that share physicochemically similar properties.

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Tracing foot-and-mouth disease virus phylogeographical patterns and transmission dynamics.

10.21203/rs.2.20387/v1 ◽

2020 ◽

Author(s):

Manuel Jara ◽

Alba Frias-De-Diego ◽

Simon Dellicour ◽

Guy Baele ◽

Gustavo Machado

Keyword(s):

Disease Virus ◽

Host Species ◽

Bayes Factor ◽

Foot And Mouth Disease ◽

Mouth Disease ◽

African Buffalo ◽

Fmdv Serotypes ◽

Mouth Disease Virus ◽

Foot And Mouth

Abstract Background Foot-and-mouth disease virus (FMDV) has proven its potential to propagate across local and international borders on numerous occasions, but yet details about the directionality of the spread along with the role of the different host in transmission remain unexplored. To elucidate FMDV global spread characteristics, we studied the spatiotemporal phylodynamics of serotypes O, A, Asia1, SAT1, SAT2, and SAT3, based on more than 50 years of phylogenetic and epidemiological information. Results Our results revealed phylogeographic patterns, dispersal rates, and the role of host species in the dispersal and maintenance of virus circulation. Contrary to previous studies, our results showed that three serotypes were monophyletic (O, A, and Asia1), while all SATs serotypes did not evidence a defined common ancestor. Root state posterior probability (RSPP) analysis suggested Belgium as the country of origin for serotype O (RSPP= 0.27). India was the ancestral country for serotypes A (RSPP= 0.28), and Asia-1 (RSPP= 0.34), while Uganda appeared as the most likely origin country of all SAT serotypes (RSPP> 0.45). Furthermore, we identified the key centers of dispersal of the virus, being China, India and Uganda the most important ones. Bayes factor analysis revealed cattle as the major source of the virus for most of the serotypes (RSPP> 0.63), where the most important host-species transition route for serotypes O, A, and Asia1 was from cattle Bos taurus to swine Sus scrofa domesticus (BF>500), while, for SAT serotypes was from B. taurus to African buffalo Syncerus caffer. Conclusions This study provides significant insights into the spatiotemporal dynamics of the global circulation of FMDV serotypes, by characterizing the viral routes of spread at serotype level, especially uncovering the importance of host species for each serotype in the evolution and spread of FMDV which further improve future decisions for more efficient control and eradication.

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