Bluetongue

Bluetongue

Bluetongue

Previous authors: D W VERWOERD AND B J ERASMUS

Current authors:
N J MACLACHLAN - Distinguished Professor Emeritus, BVSc, PhD, Dip ACVP, Department of Pathology, Microbiology and Immunology, VetMed 3A, School of Veterinary Medicine, University of California, One Shlelds Ave, Davis, California, 95616, USA / Department of Veterinary Tropical Diseases, Faculty of Veterinary Science, University of Pretoria, South Africa
G SAVINI - Head of the Animal Health Department and of the National and OIE Reference Laboratory for BT, DVM, PhD, Istituto Zooprofilatico Sperimentale dell'Abruzzo e Molise "G. Caporale" Via Campo Boario, Teramo, 64100, Italy

Introduction

Bluetongue (BT) is an arthropod-borne viral disease of domestic and wild ruminants, particularly sheep amongst domestic livestock. Clinical disease is characterized by haemorrhage, excoriations and erosion, and cyanosis of the mucous membranes of the oronasal cavity, coronitis and laminitis, oedema of the head and neck, and torticollis. The name of the disease derives from distinctive cyanosis of the tongue, which may occasionally be severe.

Bluetongue was first described in South Africa,142 where the infection (but not disease) has probably been endemic in wild ruminants from antiquity. The disease has been recognized since Merino sheep were introduced into the Cape Colony in the late eighteenth century. From the outset, BT was known to be most prevalent during the summer months, especially in wet seasons. The first detailed study of BT was made by Spreull,293, 294 but Theiler312 was the first to demonstrate the filterability of the aetiological agent, thus indicating its viral nature. He also introduced the first vaccination, making use of a virus strain (subsequently shown to be serotype 4) ‘attenuated’ by passage in sheep.313 This crude vaccine, which consisted of sheep blood, produced mild BT in recipient animals and, although it contained a single serotype, nevertheless induced remarkable protection.  Despite its obvious shortcomings it afforded sheep farmers a reasonably effective method of control, and was used for almost 40 years.

Bluetongue was initially thought to be confined to the African continent. In 1943 the first confirmed outbreak outside Africa was reported in Cyprus,101 but the disease may have occurred there as early as 1924.284 Outbreaks of BT or presence of the causative agent, Bluetongue virus (BTV), were subsequently reported in Israel,162 the USA,118, 207 Portugal197 Spain,167 Pakistan278 and India,277 and later in  the Middle East, China, Southeast Asia  and Australia.84, 185, 239, 287, 289, 345 With the notable exception of transient incursions of single virus serotypes into the Iberian Peninsula and Greece, Europe was historically free of BT  until 1998241 when multiple serotypes of BTV spread throughout  extensive portions of the continent.86, 214, 256, 273 This recent epidemic initially involved only regions of Europe adjacent to the Mediterranean Sea but later, with the incursion of a novel strain of BTV serotype 8, spread to affect virtually the entire continent as well as portions of the United Kingdom and Scandinavia. In recent years live-attenuated vaccine-derived strains of BTV have also spread through much of Europe.67, 93, 233

Early reports incriminating blood-sucking insects as vectors were based on circumstantial evidence. The first experimental proof that BTV is transmitted in South Africa by Culicoides imicola (= C. pallidipennis) was obtained by Du Toit in 1944.77 Subsequently many other Culicoides spp. (Figure 1) were proved to be vectors of BTV in the Americas, Asia,  Australia, and Europe, indeed it is now clear that different vector species are responsible for dissemination of different constellations of BTV serotypes  in distinct global “episystems”.17, 31, 104, 108, 191, 252, 297, 309, 311, 339

Figure 1 Culicoides zuluensis female

The existence of a plurality of BTV serotypes, which had long been surmised, was confirmed by Neitz in 1948 by means of cross-protection studies in sheep.226 It provided an explanation for the vaccination failures that had been experienced with the monovalent Theiler vaccine and also formed the basis for later studies on the in vitro serotyping of viral isolates.127, 128

Further advances in the understanding of BT and BTV followed rapidly on the development of techniques for the study of viruses. Some of the important milestones were the isolation and propagation of BTV in embryonated chicken eggs (ECE) by yolk sac6, 201 and intravascular109 inoculation, and its adaptation to the brains of suckling mice for antigen production.162, 318 This was followed in 1956 by the successful propagation of BTV in cell cultures by Haig et al.117

The availability of cell culture systems for the propagation of BTV led to its successful purification, to the demonstration that it is composed of a segmented, double-stranded RNA genome enclosed in a double-layered capsid,326 and to its classification in the genus Orbivirus in the family Reoviridae.37, 224, 327 Most recently, rapid sequencing procedures have facilitated the genetic characterization of strains and serotypes of BTV from different global ecosystems.17, 43, 169, 231

The continued natural evolution of BTV and other orbiviruses poses a substantial challenge to research and regulatory...

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