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

Author:

Maree Francois12,de Klerk-Lorist Lin-Mari3,Gubbins Simon4,Zhang Fuquan4,Seago Julian4,Pérez-Martín Eva4,Reid Liz4,Scott Katherine1,van Schalkwyk Louis3,Bengis Roy3,Charleston Bryan4,Juleff Nicholas4

Affiliation:

1. Transboundary Animal Disease Programme, ARC-Onderstepoort Veterinary Institute, Onderstepoort, South Africa

2. South Africa Department of Microbiology and Plant Pathology, University of Pretoria, Pretoria, South Africa

3. Office of the State Veterinarian, Department of Agriculture, Forestry and Fisheries, Skukuza, South Africa

4. The Pirbright Institute, Woking, Surrey, United Kingdom

Abstract

ABSTRACT Foot-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 persistence in vivo was 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. IMPORTANCE Foot-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.

Funder

Wellcome Trust

Biotechnology and Biological Sciences Research Council

Publisher

American Society for Microbiology

Subject

Virology,Insect Science,Immunology,Microbiology

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