Characterisation of a SAT-1 outbreak of foot-and-mouth disease in captive African buffalo (Syncerus caffer): Clinical symptoms, genetic characterisation and phylogenetic comparison of outbreak isolates

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Abstract

African buffalo (Syncerus caffer) play an important role in the maintenance of the SAT types of foot-and-mouth disease (FMD) in southern Africa. These long-term carriers mostly become sub-clinically infected, maintaining the disease and posing a threat to other susceptible wildlife and domestic species. During an unrelated bovine tuberculosis experiment using captive buffalo in the Kruger National Park (KNP), an outbreak of SAT-1 occurred and was further investigated. The clinical signs were recorded and all animals demonstrated significant weight loss and lymphopenia that lasted 100 days. In addition, the mean cell volume and mean cell haemoglobin values were significantly higher than before the outbreak started. Virus was isolated from several buffalo over a period of 167 days post infection and the molecular clock estimated to be 3 × 10−5 nucleotide substitutions per site per day. Seven amino acid changes occurred of which four occurred in hypervariable regions previously described for SAT-1. The genetic relationship of the outbreak virus was compared to buffalo viruses previously obtained from the KNP but the phylogeny was largely unresolved, therefore the relationship of this outbreak strain to others isolated from the KNP remains unclear.

Introduction

Foot-and-mouth disease (FMD) is one of the impediments on the continent of Africa that prevents access to lucrative export markets for animal products. Not only is the disease endemic to large parts of the continent, but serotype distribution and wildlife involvement differ in various parts (Vosloo et al., 2002). In eastern and southern Africa most African buffalo (Syncerus caffer) populations are carriers of the disease and although this status can last up to five years in a single animal, it is possibly not a lifelong infection (Thomson et al., 2003, Thomson and Bastos, 2004, Vosloo and Thomson, 2004). However, while acutely infected and in the carrier state these animals pose a constant threat to other susceptible cloven hoofed species with which they come into close contact and once the disease is present in domestic animals and no sufficient control measures taken, the disease could be maintained and spread by livestock. The presence of a wildlife maintenance host implies that FMD will not be eradicated from the sub continent unless large numbers of buffalo are eradicated, which is ethically not justifiable.

In southern Africa the three South African Territories (SAT) serotypes are prevalent (Vosloo and Thomson, 2004) and the only recent occurrence of serotype O was caused by an introduction from elsewhere and quickly eradicated (Brückner et al., 2002). The predominant part of South Africa has obtained zoned FMD free status without vaccination from the World Organisation for Animal Health (OIE). The only infected zone is the Kruger National Park (KNP) and adjoining game farms in the north-eastern part of the country where infected buffalo occur. Control of FMD in South Africa is reliant on separation of infected buffalo from susceptible livestock in the rest of the country by wildlife fences, vaccination of domestic animals in a narrow zone along the entire fence of the KNP and other movement control measures. However, experience has shown that outbreaks can still occur once control measures are compromised (Brückner et al., 2002). Buffalo are important for eco-tourism, but FMD carrier animals are not allowed outside the FMD control zone. For this reason several breeding projects are currently underway in southern Africa to breed buffalo calves free of several diseases including FMD (Vosloo and Thomson, 2004) to ensure that genetic diversity is maintained and that buffalo can be kept in disease free zones in several southern African countries.

Buffalo calves are born free of infection but become infected with FMD virus by their cohorts as soon as maternal antibody levels decrease. Serological data indicate that they become infected by the three SAT serotypes endemic to sub-Saharan Africa by the time they reach one year of age. This infection is mostly sub-clinical but during the two weeks that acute infection occurs, calves excrete virus in all their excretions and secretions at approximately the same level as cattle (Thomson and Bastos, 2004, Vosloo and Thomson, 2004). Thereafter virus disappears from all secretions and excretions except for the pharynx where low-level viral replication persists in less or equal than 60% of individuals and virus can only be isolated from probangs (oropharyngeal scrapings) (Thomson and Bastos, 2004). During persistence, the SAT viruses undergo high rates of mutations, giving rise to new genetic and antigenic variants (Vosloo et al., 1996).

It is not clear how virus is transmitted from carrier buffalo to susceptible animals, but for buffalo calves it is believed to spread like a childhood infection once individuals become infected (Thomson et al., 1992). Another possibility for which experimental confirmation is still required, is that virus can be transmitted via sexual transmission since virus was isolated from the semen of a bull of 3.5 years of age which can be accepted to be persistently infected based on its age (Bastos et al., 1999).

Other wildlife species can transmit FMD while in the acute stages of infection and in South Africa at least, the most important seem to be impala (Aepyceros melampus) (Vosloo et al., 2006). Buffalo have been shown unequivocally to infect impala in the KNP (Bastos et al., 2000) and these animals can in turn spread FMD to livestock in close proximity (Vosloo et al., 2006). In other parts of the sub-region, species such as kudu seems to play an important role in disseminating disease (C. Foggin, personal communication, 2003). None of these species become long-term carriers of the disease (Vosloo and Thomson, 2004) although kudu have been shown to carry the disease for up to 140 days post experimental infection (Hedger et al., 1972). Antelope are important since they have the ability to cross fences that normally prevent buffalo from crossing and in Zimbabwe at least one outbreak has been shown to have spread from buffalo to cattle via infected impala (Hargreaves et al., 2004).

Despite the fact that clinical disease in buffalo is a rare occurrence, this report describes an outbreak of FMD in a group of buffalo that were kept in captivity in the endemic zone of South Africa for an unrelated experiment concerning control of bovine tuberculosis (BTB).

Section snippets

Study group and description of the outbreak

Twenty-nine buffalo calves varying in age from ten to twenty months from five different BTB negative herds were captured in the north of the KNP, and transported to enclosures at Skukuza where they were kept for the duration of the BTB vaccine experiment. One group was vaccinated using a Bacille–Calmette–Guérin (BCG) vaccine, while the other served as nonvaccinated controls (see Table 1 for more detail and Fig. 1 for the locations of the herds). The animals were kept together and shared feeding

Viruses isolated during the outbreak

Serology results indicated that by October 2000 when the BTB experiment started, all the buffalo calves had high titres of mostly more than 2.4 log10 against all three SAT serotypes (results not shown). No clinical disease was observed during this time. During May 2001, five of the fourteen animals in the control group that was not vaccinated with BCG were clinically affected, compared to one of the fifteen animals that were vaccinated. The prevalence of FMD in the vaccinated and control groups

Discussion

Buffalo are important for their role in maintaining FMD infection and their ability of infecting other susceptible species in sub-Saharan Africa. They have been shown to be the source of infection for impala and domestic animals in proximity of the KNP and other game parks in southern Africa. Furthermore, it has been shown experimentally that buffalo can transmit virus to susceptible cattle (Thomson and Bastos, 2004, Vosloo and Thomson, 2004). For this reason extreme care is taken in South

Conclusion

The clinical manifestation of FMD in African buffalo has only been described once before. However, the weight loss and significant and long-lasting lymphopenia have not been observed previously. The rate of change of FMD virus within these buffalo has indicated again how important buffalo are for the generation of variants of viruses, emphasising their significant role in the epidemiology of FMD and its control in southern Africa.

Acknowledgements

Our sincere gratitude to Ms. Erika Kirkbride for compiling Fig. 1 and for Dr. Peter Roeder, FAO Animal Health Officer, for suggesting the use of the pharyngeal swabs. The assistance of the staff from Veterinary Wildlife Services and the Office of the State Veterinarian during this experiment is gratefully acknowledged.

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